Skip to main content

Lipid Domains and Membrane (Re)Shaping: From Biophysics to Biology

  • Chapter
  • First Online:
The Biophysics of Cell Membranes

Part of the book series: Springer Series in Biophysics ((BIOPHYSICS,volume 19))

Abstract

The surface of living cells provides an interface that not only separates the outer and inner environments but also contributes to several functions, including regulation of solute influx and efflux, signal transduction, lipid metabolism and trafficking. To fulfill these roles, the cell surface must be tough and plastic at the same time. This could explain why cell membranes exhibit such a large number of different lipid species and why some lipids form membrane domains. Besides the transient nanometric lipid rafts, morphogical evidence for stable submicrometric domains, well-accepted for artificial and highly specialized biological membranes, has been recently reported for a variety of living cells. Such complexity in lipid distribution could play a role in cell physiology, including in cell shaping and reshaping upon deformation and vesiculation. However, this remains to be clearly demonstrated. In this chapter, we highlight the main actors involved in cell (re)shaping, including the cytoskeleton, membrane-bending proteins and membrane biophysical properties. Based on integration of theoretical work and data obtained on model membranes, highly specialized cells and living cells (from prokaryotes to yeast and mammalian cells), we then discuss recent evidences supporting the existence of submicrometric lipid domains and documented mechanisms involved in their control. We also provide key recent advances supporting the role of lipid domains in cell (re)shaping. We believe that the surface of living cells is made of a variety of lipid domains that are differentially controlled and remodelled upon cell (re)shaping.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AFM:

atomic force microscopy

BODIPY:

4,4-difluoro-5,7-dimethyl-4-bora-3a,4a-diaza-s-indacene

Ca2+ :

calcium ion

Chol:

cholesterol

CTxB:

cholera toxin B subunit

ER:

endoplasmic reticulum

ERM:

ezrin, radixin, moesin

FCS:

fluorescence correlation spectroscopy

FRAP:

fluorescence recovery after photobleaching

FRET:

fluorescence resonance energy transfer

GPI:

glycosylphosphatidylinositol

GPMV:

giant plasma membrane vesicle

GSL:

glycosphingolipid

GUV:

giant unilamellar vesicle

Ld:

liquid-disordered

Lo:

liquid-ordered

mβCD:

methyl-β-cyclodextrin

MV:

microvesicle

PC:

phosphatidylcholine

PE:

phosphatidylethanolamine

PI:

phosphatidylinositol

PIP2 :

PI(4,5)P2, phosphatidylinositol-4,5-bisphosphate

PIPs:

phosphoinositides

PM:

plasma membrane

PS:

phosphatidylserine

RBC:

red blood cell

SDS:

sodium dodecyl sulfate

SIM:

structured illumination microscopy

SIMS:

secondary ion mass spectrometry

SM:

sphingomyelin

SMase:

sphingomyelinase

STED:

stimulated emission depletion microscopy

TCR:

T cell receptor

Tm :

melting temperature

References

  1. Thomas JA, Rana FR (2007) The influence of environmental conditions, lipid composition, and phase behavior on the origin of cell membranes. Orig Life Evol Biosph 37(3):267–285

    Article  CAS  PubMed  Google Scholar 

  2. Bigay J, Antonny B (2012) Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev Cell 23(5):886–895

    Article  CAS  PubMed  Google Scholar 

  3. Sodt AJ et al (2016) Nonadditive compositional curvature energetics of lipid bilayers. Phys Rev Lett 117(13):138104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Janmey PA, Kinnunen PK (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16(10):538–546

    Article  CAS  PubMed  Google Scholar 

  5. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(4023):720–731

    Article  CAS  PubMed  Google Scholar 

  6. Nicolson GL (2014) The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim Biophys Acta 1838(6):1451–1466

    Article  CAS  PubMed  Google Scholar 

  7. Goni FM (2014) The basic structure and dynamics of cell membranes: an update of the singer-Nicolson model. Biochim Biophys Acta 1838(6):1467–1476

    Article  CAS  PubMed  Google Scholar 

  8. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387(6633):569–572

    Article  CAS  PubMed  Google Scholar 

  9. Pike LJ (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J Lipid Res 47(7):1597–1598

    Article  CAS  PubMed  Google Scholar 

  10. Bagatolli LA et al (2010) An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog Lipid Res 49(4):378–389

    Article  CAS  PubMed  Google Scholar 

  11. Bagatolli LA, Mouritsen OG (2013) Is the fluid mosaic (and the accompanying raft hypothesis) a suitable model to describe fundamental features of biological membranes? What may be missing? Front Plant Sci 4:457

    Article  PubMed  PubMed Central  Google Scholar 

  12. Vicidomini G et al (2015) STED-FLCS: an advanced tool to reveal spatiotemporal heterogeneity of molecular membrane dynamics. Nano Lett 15(9):5912–5918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Stone MB, Shelby SA, Veatch SL (2017) Super-resolution microscopy: shedding light on the cellular plasma membrane. Chem Rev 117:7457

    Article  CAS  PubMed  Google Scholar 

  14. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46–50

    Article  CAS  PubMed  Google Scholar 

  15. Parton RG, del Pozo MA (2013) Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol 14(2):98–112

    Article  CAS  PubMed  Google Scholar 

  16. Yanez-Mo M et al (2009) Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19(9):434–446

    Article  CAS  PubMed  Google Scholar 

  17. Baumgart T et al (2007) Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci USA 104(9):3165–3170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. de la Serna JB et al (2004) Cholesterol rules: direct observation of the coexistence of two fluid phases in native pulmonary surfactant membranes at physiological temperatures. J Biol Chem 279(39):40715–40722

    Article  CAS  Google Scholar 

  19. Kahya N et al (2003) Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J Biol Chem 278(30):28109–28115

    Article  CAS  PubMed  Google Scholar 

  20. Plasencia I, Norlen L, Bagatolli LA (2007) Direct visualization of lipid domains in human skin stratum corneum's lipid membranes: effect of pH and temperature. Biophys J 93(9):3142–3155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Carquin M et al (2014) Endogenous sphingomyelin segregates into submicrometric domains in the living erythrocyte membrane. J Lipid Res 55(7):1331–1342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. D’Auria L et al (2013) Micrometric segregation of fluorescent membrane lipids: relevance for endogenous lipids and biogenesis in erythrocytes. J Lipid Res 54(4):1066–1076

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Sanchez SA, Tricerri MA, Gratton E (2012) Laurdan generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo. Proc Natl Acad Sci USA 109(19):7314–7319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Carquin M et al (2015) Cholesterol segregates into submicrometric domains at the living erythrocyte membrane: evidence and regulation. Cell Mol Life Sci 72(23):4633–4651

    Article  CAS  PubMed  Google Scholar 

  25. Tyteca D et al (2010) Three unrelated sphingomyelin analogs spontaneously cluster into plasma membrane micrometric domains. Biochim Biophys Acta 1798(5):909–927

    Article  CAS  PubMed  Google Scholar 

  26. Bach JN, Bramkamp M (2013) Flotillins functionally organize the bacterial membrane. Mol Microbiol 88(6):1205–1217

    Article  CAS  PubMed  Google Scholar 

  27. Grossmann G et al (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J 26(1):1–8

    Article  CAS  PubMed  Google Scholar 

  28. Lux SE (2016) Anatomy of the red cell membrane skeleton: unanswered questions. Blood 127(2):187–199

    Article  CAS  PubMed  Google Scholar 

  29. Waugh RE (1996) Elastic energy of curvature-driven bump formation on red blood cell membrane. Biophys J 70(2):1027–1035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438(7068):590–596

    Article  CAS  PubMed  Google Scholar 

  31. Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7(1):9–19

    Article  CAS  PubMed  Google Scholar 

  32. Hansen GH et al (2007) Intestinal alkaline phosphatase: selective endocytosis from the enterocyte brush border during fat absorption. Am J Physiol Gastrointest Liver Physiol 293(6):G1325–G1332

    Article  CAS  PubMed  Google Scholar 

  33. Andreae LC, Burrone J (2015) Spontaneous neurotransmitter release shapes dendritic arbors via long-range activation of NMDA receptors. Cell Rep 10:873

    Article  CAS  PubMed Central  Google Scholar 

  34. Deplaine G et al (2011) The sensing of poorly deformable red blood cells by the human spleen can be mimicked in vitro. Blood 117(8):e88–e95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Danilchik MV, Brown EE, Riegert K (2006) Intrinsic chiral properties of the Xenopus egg cortex: an early indicator of left-right asymmetry? Development 133(22):4517–4526

    Article  CAS  PubMed  Google Scholar 

  36. Osumi M (1998) The ultrastructure of yeast: cell wall structure and formation. Micron 29(2–3):207–233

    Article  CAS  PubMed  Google Scholar 

  37. Singleton K et al (2006) A large T cell invagination with CD2 enrichment resets receptor engagement in the immunological synapse. J Immunol 177(7):4402–4413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Turturici G et al (2014) Extracellular membrane vesicles as a mechanism of cell-to-cell communication: advantages and disadvantages. Am J Physiol Cell Physiol 306(7):C621–C633

    Article  CAS  PubMed  Google Scholar 

  39. Yuana Y, Sturk A, Nieuwland R (2013) Extracellular vesicles in physiological and pathological conditions. Blood Rev 27(1):31–39

    Article  CAS  PubMed  Google Scholar 

  40. Gupta A, Pulliam L (2014) Exosomes as mediators of neuroinflammation. J Neuroinflammation 11:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Muralidharan-Chari V et al (2010) Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 123(Pt 10):1603–1611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Shen B et al (2011) Biogenesis of the posterior pole is mediated by the exosome/microvesicle protein-sorting pathway. J Biol Chem 286(51):44162–44176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tian A, Baumgart T (2009) Sorting of lipids and proteins in membrane curvature gradients. Biophys J 96(7):2676–2688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sorre B et al (2009) Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc Natl Acad Sci 106(14):5622–5626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Garcia-Saez AJ, Chiantia S, Schwille P (2007) Effect of line tension on the lateral Organization of Lipid Membranes. J Biol Chem 282(46):33537–33544

    Article  CAS  PubMed  Google Scholar 

  46. Robinson T et al (2012) Investigating the effects of membrane tension and shear stress on lipid domains in model membranes. 16th international conference on miniaturized systems for chemistry and life sciences

    Google Scholar 

  47. Henon S et al (1999) A new determination of the shear modulus of the human erythrocyte membrane using optical tweezers. Biophys J 76(2):1145–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Reid HL et al (1976) A simple method for measuring erythrocyte deformability. J Clin Pathol 29(9):855–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rand RP, Burton AC (1964) Mechanical properties of the red cell membrane. I membrane stiffness and intracellular pressure. Biophys J 4:115–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hochmuth RM (2000) Micropipette aspiration of living cells. J Biomech 33(1):15–22

    Article  CAS  PubMed  Google Scholar 

  51. Hosseini SM, Feng JJ (2012) How malaria parasites reduce the deformability of infected red blood cells. Biophys J 103(1):1–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lee LM, Liu AP (2015) A microfluidic pipette array for mechanophenotyping of cancer cells and mechanical gating of mechanosensitive channels. Lab Chip 15(1):264–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chivukula VK et al (2015) Alterations in cancer cell mechanical properties after fluid shear stress exposure: a micropipette aspiration study. Cell Health Cytoskelet 7:25–35

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Müller DJ et al (2009) Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5(6):383–390

    Article  PubMed  CAS  Google Scholar 

  55. Gerber C, Lang HP (2006) How the doors to the nanoworld were opened. Nat Nanotechnol 1(1):3–5

    Article  CAS  PubMed  Google Scholar 

  56. Butt H-J, Cappella B, Kappl M (2005) Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep 59(1–6):1–152

    Article  CAS  Google Scholar 

  57. Dufrêne YF et al (2013) Multiparametric imaging of biological systems by force-distance curve-based AFM. Nat Methods 10(9):847–854

    Article  PubMed  CAS  Google Scholar 

  58. Sullan RMA, Li JK, Zou S (2009) Direct correlation of structures and Nanomechanical properties of multicomponent lipid bilayers. Langmuir 25(13):7471–7477

    Article  CAS  PubMed  Google Scholar 

  59. Bremmell KE, Evans A, Prestidge CA (2006) Deformation and nano-rheology of red blood cells: an AFM investigation. Colloids Surf B: Biointerfaces 50(1):43–48

    Article  CAS  PubMed  Google Scholar 

  60. Heu C et al (2012) Glyphosate-induced stiffening of HaCaT keratinocytes, a peak force tapping study on living cells. J Struct Biol 178(1):1–7

    Article  CAS  PubMed  Google Scholar 

  61. Alsteens D et al (2013) Multiparametric atomic force microscopy imaging of single bacteriophages extruding from living bacteria. Nat Commun 4:2926

    Article  PubMed  CAS  Google Scholar 

  62. Grandbois M et al (2000) Affinity imaging of red blood cells using an atomic force microscope. J Histochem Cytochem 48(5):719–724

    Article  CAS  PubMed  Google Scholar 

  63. Baumgartner W et al (2000) Cadherin interaction probed by atomic force microscopy. Proc Natl Acad Sci USA 97(8):4005–4010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Thie M et al (1998) Interactions between trophoblast and uterine epithelium: monitoring of adhesive forces. Hum Reprod 13(11):3211–3219

    Article  CAS  PubMed  Google Scholar 

  65. Kim H et al (2006) Quantification of the number of EP3 receptors on a living CHO cell surface by the AFM. Ultramicroscopy 106(8–9):652–662

    Article  CAS  PubMed  Google Scholar 

  66. Roduit C et al (2008) Elastic membrane heterogeneity of living cells revealed by stiff nanoscale membrane domains. Biophys J 94(4):1521–1532

    Article  CAS  PubMed  Google Scholar 

  67. Zheng Y et al (2013) Recent advances in microfluidic techniques for single-cell biophysical characterization. Lab Chip 13(13):2464–2483

    Article  CAS  PubMed  Google Scholar 

  68. Lee WG et al (2007) On-chip erythrocyte deformability test under optical pressure. Lab Chip 7(4):516–519

    Article  CAS  PubMed  Google Scholar 

  69. Rosenbluth MJ, Lam WA, Fletcher DA (2008) Analyzing cell mechanics in hematologic diseases with microfluidic biophysical flow cytometry. Lab Chip 8(7):1062–1070

    Article  CAS  PubMed  Google Scholar 

  70. Guck J et al (2005) Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J 88(5):3689–3698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Remmerbach TW et al (2009) Oral cancer diagnosis by mechanical phenotyping. Cancer Res 69(5):1728–1732

    Article  CAS  PubMed  Google Scholar 

  72. Hou HW et al (2009) Deformability study of breast cancer cells using microfluidics. Biomed Microdevices 11(3):557–564

    Article  CAS  PubMed  Google Scholar 

  73. Gossett DR et al (2012) Hydrodynamic stretching of single cells for large population mechanical phenotyping. Proc Natl Acad Sci USA 109(20):7630–7635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Bao N et al (2011) Single-cell electrical lysis of erythrocytes detects deficiencies in the cytoskeletal protein network. Lab Chip 11(18):3053–3056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Robinson T, Kuhn P, Dittrich PS (2013) Reorganization of lipid domains in model membranes under deformation. 17th international conference on miniaturized systems for chemistry and life sciences 2013

    Google Scholar 

  76. Radosinska J, Vrbjar N (2016) The role of red blood cell deformability and Na,K-ATPase function in selected risk factors of cardiovascular diseases in humans: focus on hypertension, diabetes mellitus and hypercholesterolemia. Physiol Res 65(Suppl 1):S43–S54

    PubMed  Google Scholar 

  77. Maher AD, Kuchel PW (2003) The Gardos channel: a review of the Ca2+−activated K+ channel in human erythrocytes. Int J Biochem Cell Biol 35(8):1182–1197

    Article  CAS  PubMed  Google Scholar 

  78. Thomas SL et al (2011) Ion channels in human red blood cell membrane: actors or relics? Blood Cells Mol Dis 46(4):261–265

    Article  CAS  PubMed  Google Scholar 

  79. Cahalan SM et al (2015) Piezo1 links mechanical forces to red blood cell volume. Elife 4:e07370

    Article  PubMed Central  CAS  Google Scholar 

  80. Evans E, Mohandas N, Leung A (1984) Static and dynamic rigidities of normal and sickle erythrocytes. Major influence of cell hemoglobin concentration. J Clin Invest 73(2):477–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Picas L et al (2013) Structural and mechanical heterogeneity of the erythrocyte membrane reveals hallmarks of membrane stability. ACS Nano 7(2):1054–1063

    Article  CAS  PubMed  Google Scholar 

  82. Betz T et al (2009) ATP-dependent mechanics of red blood cells. Proc Natl Acad Sci USA 106(36):15320–15325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Park Y et al (2010) Metabolic remodeling of the human red blood cell membrane. Proc Natl Acad Sci USA 107(4):1289–1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Yoon YZ et al (2008) The nonlinear mechanical response of the red blood cell. Phys Biol 5(3):036007

    Article  PubMed  Google Scholar 

  85. Wan J, Ristenpart WD, Stone HA (2008) Dynamics of shear-induced ATP release from red blood cells. Proc Natl Acad Sci USA 105(43):16432–16437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Chu H et al (2016) Reversible binding of hemoglobin to band 3 constitutes the molecular switch that mediates O2 regulation of erythrocyte properties. Blood 128(23):2708–2716

    Article  CAS  PubMed  Google Scholar 

  87. Manno S, Takakuwa Y, Mohandas N (2005) Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem 280(9):7581–7587

    Article  CAS  PubMed  Google Scholar 

  88. Manno S et al (1995) Modulation of erythrocyte membrane mechanical function by beta-spectrin phosphorylation and dephosphorylation. J Biol Chem 270(10):5659–5665

    Article  CAS  PubMed  Google Scholar 

  89. An X et al (2006) Phosphatidylinositol-4,5-biphosphate (PIP2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins. Biochemistry 45(18):5725–5732

    Article  CAS  PubMed  Google Scholar 

  90. Saleh HS et al (2009) Properties of an Ezrin mutant defective in F-actin binding. J Mol Biol 385(4):1015–1031

    Article  CAS  PubMed  Google Scholar 

  91. Bretscher A et al (2000) ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu Rev Cell Dev Biol 16(1):113–143

    Article  CAS  PubMed  Google Scholar 

  92. Gimona M et al (2002) Functional plasticity of CH domains. FEBS Lett 513(1):98–106

    Article  CAS  PubMed  Google Scholar 

  93. Paunola E, Mattila PK, Lappalainen P (2002) WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett 513(1):92–97

    Article  CAS  PubMed  Google Scholar 

  94. Fukami K et al (1992) Requirement of phosphatidylinositol 4,5-bisphosphate for [alpha]-actinin function. Nature 359(6391):150–152

    Article  CAS  PubMed  Google Scholar 

  95. Fukami K et al (1996) Identification of a phosphatidylinositol 4,5-bisphosphate-binding site in chicken skeletal muscle α-Actinin. J Biol Chem 271(5):2646–2650

    Article  CAS  PubMed  Google Scholar 

  96. McKenna JMD, Ostap EM (2009) Kinetics of the interaction of myo1c with Phosphoinositides. J Biol Chem 284(42):28650–28659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Liu X et al (2016) Mammalian nonmuscle myosin II binds to anionic phospholipids with concomitant dissociation of the regulatory light chain. J Biol Chem 291(48):24828–24837

    Article  CAS  PubMed  Google Scholar 

  98. Feeser EA, Ostap EM (2010) Myo1e binds anionic phospholipids with high affinity. Biophys J 98(3):561a

    Article  Google Scholar 

  99. Yu H et al (2012) PtdIns (3,4,5) P3 recruitment of Myo10 is essential for axon development. PLoS One 7(5):e36988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Köster DV, Mayor S (2016) Cortical actin and the plasma membrane: inextricably intertwined. Curr Opin Cell Biol 38:81–89

    Article  PubMed  CAS  Google Scholar 

  101. Raghupathy R et al (2015) Transbilayer lipid interactions mediate Nanoclustering of lipid-anchored proteins. Cell 161(3):581–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Stachowiak JC et al (2012) Membrane bending by protein–protein crowding. Nat Cell Biol 14(9):944–949

    Article  CAS  PubMed  Google Scholar 

  103. MacKinnon R (2003) Potassium channels. FEBS Lett 555(1):62–65

    Article  CAS  PubMed  Google Scholar 

  104. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J Mol Biol 346(4):967–989

    Article  CAS  PubMed  Google Scholar 

  105. Ehrlich M et al (2004) Endocytosis by Random Initiation and Stabilization of Clathrin-Coated Pits. Cell 118(5):591–605

    Article  CAS  PubMed  Google Scholar 

  106. Drin G, Antonny B (2010) Amphipathic helices and membrane curvature. FEBS Lett 584(9):1840–1847

    Article  CAS  PubMed  Google Scholar 

  107. Hurley JH, Hanson PI (2010) Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol 11(8):556–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Raiborg C, Stenmark H (2009) The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 458(7237):445–452

    Article  CAS  PubMed  Google Scholar 

  109. Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37(12):526–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Rao Y, Haucke V (2011) Membrane shaping by the bin/amphiphysin/Rvs (BAR) domain protein superfamily. Cell Mol Life Sci 68(24):3983–3993

    Article  CAS  PubMed  Google Scholar 

  111. Hinshaw JE, Schmid SL (1995) Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding. Nature 374(6518):190–192

    Article  CAS  PubMed  Google Scholar 

  112. Peter BJ et al (2004) BAR domains as sensors of membrane curvature: the Amphiphysin BAR structure. Science 303(5657):495–499

    Article  CAS  PubMed  Google Scholar 

  113. Frost A, Unger VM, De Camilli P (2009) The BAR domain superfamily: membrane-molding macromolecules. Cell 137(2):191–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Sit ST, Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124(5):679–683

    Article  CAS  PubMed  Google Scholar 

  115. Aspenstrom P (2014) BAR domain proteins regulate Rho GTPase signaling. Small GTPases 5(2):7

    Article  PubMed  Google Scholar 

  116. McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12(8):517–533

    Article  CAS  PubMed  Google Scholar 

  117. Zanetti G et al (2012) COPII and the regulation of protein sorting in mammals. Nat Cell Biol 14(1):20–28

    Article  CAS  Google Scholar 

  118. Shibata Y et al (2009) Mechanisms shaping the membranes of cellular organelles. Annu Rev Cell Dev Biol 25(1):329–354

    Article  CAS  PubMed  Google Scholar 

  119. Bretscher MS (1972) Phosphatidyl-ethanolamine: differential labelling in intact cells and cell ghosts of human erythrocytes by a membrane-impermeable reagent. J Mol Biol 71(3):523–528

    Article  CAS  PubMed  Google Scholar 

  120. Daleke DL (2008) Regulation of phospholipid asymmetry in the erythrocyte membrane. Curr Opin Hematol 15(3):191–195

    Article  CAS  PubMed  Google Scholar 

  121. Lhermusier T, Chap H, Payrastre B (2011) Platelet membrane phospholipid asymmetry: from the characterization of a scramblase activity to the identification of an essential protein mutated in Scott syndrome. J Thromb Haemost 9(10):1883–1891

    Article  CAS  PubMed  Google Scholar 

  122. Murate M et al (2015) Transbilayer distribution of lipids at nano scale. J Cell Sci 128(8):1627–1638

    Article  CAS  PubMed  Google Scholar 

  123. Murate M, Kobayashi T (2015) Revisiting transbilayer distribution of lipids in the plasma membrane. Chem Phys Lipids 194:58

    Article  PubMed  CAS  Google Scholar 

  124. Elani Y et al (2015) Measurements of the effect of membrane asymmetry on the mechanical properties of lipid bilayers. Chem Commun (Camb) 51(32):6976–6979

    Article  CAS  Google Scholar 

  125. Liu SL et al (2016) Orthogonal lipid sensors identify transbilayer asymmetry of plasma membrane cholesterol. Nat Chem Biol 13:268

    Article  PubMed  CAS  Google Scholar 

  126. Arashiki N et al (2016) An unrecognized function of cholesterol: regulating the mechanism controlling membrane phospholipid asymmetry. Biochemistry 55(25):3504–3513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Pomorski TG, Menon AK (2016) Lipid somersaults: uncovering the mechanisms of protein-mediated lipid flipping. Prog Lipid Res 64:69–84

    Article  CAS  PubMed  Google Scholar 

  128. Chiantia S, London E (2012) Acyl chain length and saturation modulate interleaflet coupling in asymmetric bilayers: effects on dynamics and structural order. Biophys J 103(11):2311–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Lin Q, London E (2015) Ordered raft domains induced by outer leaflet sphingomyelin in cholesterol-rich asymmetric vesicles. Biophys J 108(9):2212–2222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Koynova R, Caffrey M (1998) Phases and phase transitions of the phosphatidylcholines. Biochim Biophys Acta 1376(1):91–145

    Article  CAS  PubMed  Google Scholar 

  131. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9(2):112–124

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. Slotte JP (2013) Biological functions of sphingomyelins. Prog Lipid Res 52(4):424–437

    Article  CAS  PubMed  Google Scholar 

  133. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136

    Article  CAS  PubMed  Google Scholar 

  134. McConnell HM, Vrljic M (2003) Liquid-liquid immiscibility in membranes. Annu Rev Biophys Biomol Struct 32:469–492

    Article  CAS  PubMed  Google Scholar 

  135. Holthuis JC, Menon AK (2014) Lipid landscapes and pipelines in membrane homeostasis. Nature 510(7503):48–57

    Article  CAS  PubMed  Google Scholar 

  136. Puth K et al (2015) Homeostatic control of biological membranes by dedicated lipid and membrane packing sensors. Biol Chem 396(9–10):1043–1058

    CAS  PubMed  Google Scholar 

  137. Ernst R, Ejsing CS, Antonny B (2016) Homeoviscous adaptation and the regulation of membrane lipids. J Mol Biol 428(24):4776–4791

    Article  CAS  PubMed  Google Scholar 

  138. Gawrisch K et al (1992) Membrane dipole potentials, hydration forces, and the ordering of water at membrane surfaces. Biophys J 61(5):1213–1223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Schamberger J, Clarke RJ (2002) Hydrophobic ion hydration and the magnitude of the dipole potential. Biophys J 82(6):3081–3088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Zheng C, Vanderkooi G (1992) Molecular origin of the internal dipole potential in lipid bilayers: calculation of the electrostatic potential. Biophys J 63(4):935–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Clarke RJ (1997) Effect of lipid structure on the dipole potential of phosphatidylcholine bilayers. Biochim Biophys Acta Biomembr 1327(2):269–278

    Article  CAS  Google Scholar 

  142. Starke-Peterkovic T, Clarke RJ (2009) Effect of headgroup on the dipole potential of phospholipid vesicles. Eur Biophys J 39(1):103–110

    Article  CAS  PubMed  Google Scholar 

  143. Szabo G (1974) Dual mechanism for the action of cholesterol on membrane permeability. Nature 252(5478):47–49

    Article  CAS  PubMed  Google Scholar 

  144. McIntosh TJ, Magid AD, Simon SA (1989) Repulsive interactions between uncharged bilayers. Hydration and fluctuation pressures for monoglycerides. Biophys J 55(5):897–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Starke-Peterkovic T et al (2006) Cholesterol effect on the dipole potential of lipid membranes. Biophys J 90(11):4060–4070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Haldar S et al (2012) Differential effect of cholesterol and its biosynthetic precursors on membrane dipole potential. Biophys J 102(7):1561–1569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Cullis PR, De Kruijff B (1979) Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta Rev Biomembr 559(4):399–420

    Article  CAS  Google Scholar 

  148. Sheetz MP, Singer SJ (1974) Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci USA 71(11):4457–4461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15(7):675–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Ailte I et al (2016) Addition of lysophospholipids with large head groups to cells inhibits Shiga toxin binding. Sci Rep 6:30336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. McMahon HT, Boucrot E (2015) Membrane curvature at a glance. J Cell Sci 128(6):1065–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Holdbrook DA et al (2016) Dynamics of crowded vesicles: local and global responses to membrane composition. PLoS One 11(6):e0156963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Frisz JF et al (2013) Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol. J Biol Chem 288(23):16855–16861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Frisz JF et al (2013) Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts. Proc Natl Acad Sci USA 110(8):E613–E622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Sevcsik E et al (2015) GPI-anchored proteins do not reside in ordered domains in the live cell plasma membrane. Nat Commun 6:6969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Carquin M et al (2016) Recent progress on lipid lateral heterogeneity in plasma membranes: from rafts to submicrometric domains. Prog Lipid Res 62:1–24

    Article  CAS  PubMed  Google Scholar 

  157. Takatori S, Mesman R, Fujimoto T (2014) Microscopic methods to observe the distribution of lipids in the cellular membrane. Biochemistry 53(4):639–653

    Article  CAS  PubMed  Google Scholar 

  158. Maekawa M, Fairn GD (2014) Molecular probes to visualize the location, organization and dynamics of lipids. J Cell Sci 127(22):4801–4812

    Article  PubMed  CAS  Google Scholar 

  159. Skocaj M et al (2013) The sensing of membrane microdomains based on pore-forming toxins. Curr Med Chem 20(4):491–501

    CAS  PubMed  Google Scholar 

  160. Maekawa M, Yang Y, Fairn GD, Perfringolysin O (2016) Theta toxin as a tool to monitor the distribution and inhomogeneity of cholesterol in cellular membranes. Toxins (Basel) 8(3):67

    Article  CAS  Google Scholar 

  161. Montes LR et al (2008) Ceramide-enriched membrane domains in red blood cells and the mechanism of sphingomyelinase-induced hot-cold hemolysis. Biochemistry 47(43):11222–11230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Cai M et al (2012) Direct evidence of lipid rafts by in situ atomic force microscopy. Small 8(8):1243–1250

    Article  CAS  PubMed  Google Scholar 

  163. Hao M, Mukherjee S, Maxfield FR (2001) Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc Natl Acad Sci USA 98(23):13072–13077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Grassme H et al (2003) Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat Med 9(3):322–330

    Article  CAS  PubMed  Google Scholar 

  165. Stancevic B, Kolesnick R (2010) Ceramide-rich platforms in transmembrane signaling. FEBS Lett 584(9):1728–1740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Kaiser HJ et al (2009) Order of lipid phases in model and plasma membranes. Proc Natl Acad Sci USA 106(39):16645–16650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Pataraia S et al (2014) Effect of cytochrome c on the phase behavior of charged multicomponent lipid membranes. Biochim Biophys Acta 1838(8):2036–2045

    Article  CAS  PubMed  Google Scholar 

  168. de la Serna JB et al (2009) Segregated phases in pulmonary surfactant membranes do not show coexistence of lipid populations with differentiated dynamic properties. Biophys J 97(5):1381–1389

    Article  PubMed Central  CAS  Google Scholar 

  169. Hammond AT et al (2005) Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc Natl Acad Sci 102(18):6320–6325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Fidorra M et al (2006) Absence of fluid-ordered/fluid-disordered phase coexistence in ceramide/POPC mixtures containing cholesterol. Biophys J 90(12):4437–4451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Bagatolli LA (2006) To see or not to see: lateral organization of biological membranes and fluorescence microscopy. Biochim Biophys Acta Biomembr 1758(10):1541–1556

    Article  CAS  Google Scholar 

  172. Levental I, Grzybek M, Simons K (2011) Raft domains of variable properties and compositions in plasma membrane vesicles. Proc Natl Acad Sci 108(28):11411–11416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Girard P et al (2004) A new method for the reconstitution of membrane proteins into Giant Unilamellar vesicles. Biophys J 87(1):419–429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Veatch SL et al (2008) Critical fluctuations in plasma membrane vesicles. ACS Chem Biol 3(5):287–293

    Article  CAS  PubMed  Google Scholar 

  175. Bouwstra JA et al (2003) Structure of the skin barrier and its modulation by vesicular formulations. Prog Lipid Res 42(1):1–36

    Article  CAS  PubMed  Google Scholar 

  176. Downing DT (1992) Lipid and protein structures in the permeability barrier of mammalian epidermis. J Lipid Res 33(3):301–313

    CAS  PubMed  Google Scholar 

  177. Mileykovskaya E, Dowhan W (2000) Visualization of phospholipid domains in Escherichia coli by using the Cardiolipin-specific fluorescent dye 10-N-Nonyl Acridine Orange. J Bacteriol 182(4):1172–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Kawai F et al (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186(5):1475–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Lopez D (2015) Molecular composition of functional microdomains in bacterial membranes. Chem Phys Lipids 192:3–11

    Article  CAS  PubMed  Google Scholar 

  180. Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79(1):81–100

    Article  PubMed  PubMed Central  Google Scholar 

  181. Huijbregts RP, de Kroon AI, de Kruijff B (2000) Topology and transport of membrane lipids in bacteria. Biochim Biophys Acta 1469(1):43–61

    Article  CAS  PubMed  Google Scholar 

  182. Lopez-Lara IM, Geiger O (2016) Bacterial lipid diversity. Biochim Biophys Acta

    Google Scholar 

  183. Parsons JB, Rock CO (2013) Bacterial lipids: metabolism and membrane homeostasis. Prog Lipid Res 52(3):249–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Huang Z, London E (2016) Cholesterol lipids and cholesterol-containing lipid rafts in bacteria. Chem Phys Lipids 199:11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Lin M, Rikihisa Y (2003) Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid a biosynthesis and incorporate cholesterol for their survival. Infect Immun 71(9):5324–5331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Saenz JP et al (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci USA 109(35):14236–14240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Doughty DM et al (2014) Probing the subcellular localization of Hopanoid lipids in bacteria using NanoSIMS. PLoS One 9(1):e84455

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  188. Donovan C, Bramkamp M (2009) Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 155(6):1786–1799

    Article  CAS  PubMed  Google Scholar 

  189. López D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24(17):1893–1902

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  190. Malinska K et al (2003) Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol Biol Cell 14(11):4427–4436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Klose C et al (2010) Yeast lipids can phase-separate into micrometer-scale membrane domains. J Biol Chem 285(39):30224–30232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Spira F et al (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat Cell Biol 14(8):890–890

    Article  CAS  Google Scholar 

  193. Kabeche R et al (2015) Eisosomes regulate phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) cortical clusters and mitogen-activated protein (MAP) kinase signaling upon osmotic stress. J Biol Chem 290(43):25960–25973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Guiney EL et al (2015) Calcineurin regulates the yeast synaptojanin Inp53/Sjl3 during membrane stress. Mol Biol Cell 26(4):769–785

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  195. Toulmay A, Prinz WA (2013) Direct imaging reveals stable, micrometer-scale lipid domains that segregate proteins in live cells. J Cell Biol 202(1):35–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Zachowski A (1993) Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J 294(1):1–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Goodman SR et al (2013) The proteomics and interactomics of human erythrocytes. Exp Biol Med (Maywood) 238(5):509–518

    Article  CAS  Google Scholar 

  198. D'Auria L et al (2011) Segregation of fluorescent membrane lipids into distinct micrometric domains: evidence for phase compartmentation of natural lipids? PLoS One 6(2):e17021

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  199. Ekyalongo RC et al (2015) Organization and functions of glycolipid-enriched microdomains in phagocytes. Biochim Biophys Acta 1851(1):90–97

    Article  CAS  PubMed  Google Scholar 

  200. Makino A et al (2015) Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis. FASEB J 29(2):477–493

    Article  CAS  PubMed  Google Scholar 

  201. Abe M et al (2012) A role for sphingomyelin-rich lipid domains in the accumulation of phosphatidylinositol-4,5-bisphosphate to the cleavage furrow during cytokinesis. Mol Cell Biol 32(8):1396–1407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Mizuno H et al (2011) Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem Sci 2:1548–1553

    Article  CAS  Google Scholar 

  203. Kiyokawa E et al (2005) Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J Biol Chem 280(25):24072–24084

    Article  CAS  PubMed  Google Scholar 

  204. Leonard et al (2017) Science reports 2017. Sci Rep 7(1):4264. doi:10.1038/s41598-017-04388-z

  205. Agbani EO et al (2015) Coordinated membrane ballooning and Procoagulant spreading in human platelets. Circulation 132(15):1414–1424

    Article  CAS  PubMed  Google Scholar 

  206. Heemskerk JW et al (1997) Collagen but not fibrinogen surfaces induce bleb formation, exposure of phosphatidylserine, and procoagulant activity of adherent platelets: evidence for regulation by protein tyrosine kinase-dependent Ca2+ responses. Blood 90(7):2615–2625

    CAS  PubMed  Google Scholar 

  207. Gousset K et al (2002) Evidence for a physiological role for membrane rafts in human platelets. J Cell Physiol 190(1):117–128

    Article  CAS  PubMed  Google Scholar 

  208. Bali R et al (2009) Macroscopic domain formation during cooling in the platelet plasma membrane: an issue of low cholesterol content. Biochim Biophys Acta 1788(6):1229–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Pierini LM et al (2003) Membrane lipid organization is critical for human neutrophil polarization. J Biol Chem 278(12):10831–10841

    Article  CAS  PubMed  Google Scholar 

  210. Sonnino S et al (2009) Role of very long fatty acid-containing glycosphingolipids in membrane organization and cell signaling: the model of lactosylceramide in neutrophils. Glycoconj J 26(6):615–621

    Article  CAS  PubMed  Google Scholar 

  211. Jackman N, Ishii A, Bansal R (2009) Oligodendrocyte development and myelin biogenesis: parsing out the roles of glycosphingolipids. Physiology (Bethesda) 24:290–297

    Article  CAS  Google Scholar 

  212. Aggarwal S, Yurlova L, Simons M (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21(10):585–593

    Article  CAS  PubMed  Google Scholar 

  213. Boggs JM, Wang H (2004) Co-clustering of galactosylceramide and membrane proteins in oligodendrocyte membranes on interaction with polyvalent carbohydrate and prevention by an intact cytoskeleton. J Neurosci Res 76(3):342–355

    Article  CAS  PubMed  Google Scholar 

  214. Boggs JM et al (2010) Participation of galactosylceramide and sulfatide in glycosynapses between oligodendrocyte or myelin membranes. FEBS Lett 584(9):1771–1778

    Article  CAS  PubMed  Google Scholar 

  215. Ozgen H et al (2014) The lateral membrane organization and dynamics of myelin proteins PLP and MBP are dictated by distinct galactolipids and the extracellular matrix. PLoS One 9(7):e101834

    Article  PubMed  PubMed Central  Google Scholar 

  216. Decker L, French-Constant C (2004) Lipid rafts and integrin activation regulate oligodendrocyte survival. J Neurosci 24(15):3816–3825

    Article  CAS  PubMed  Google Scholar 

  217. Meder D et al (2006) Phase coexistence and connectivity in the apical membrane of polarized epithelial cells. Proc Natl Acad Sci USA 103(2):329–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Ikenouchi J et al (2012) Lipid polarity is maintained in absence of tight junctions. J Biol Chem 287(12):9525–9533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  219. Umeda K et al (2006) ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126(4):741–754

    Article  CAS  PubMed  Google Scholar 

  220. Fanning AS, Van Itallie CM, Anderson JM (2012) Zonula occludens-1 and -2 regulate apical cell structure and the zonula adherens cytoskeleton in polarized epithelia. Mol Biol Cell 23(4):577–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Orsini F et al (2012) Atomic force microscopy imaging of lipid rafts of human breast cancer cells. Biochim Biophys Acta 1818(12):2943–2949

    Article  CAS  PubMed  Google Scholar 

  222. Dinic J et al (2015) The T cell receptor resides in ordered plasma membrane nanodomains that aggregate upon patching of the receptor. Sci Rep 5:10082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Gomez-Mouton C et al (2001) Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization. Proc Natl Acad Sci USA 98(17):9642–9647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Paparelli L et al (2016) Inhomogeneity based characterization of distribution patterns on the plasma membrane. PLoS Comput Biol 12(9):e1005095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  225. Golebiewska U et al (2008) Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol Biol Cell 19(4):1663–1669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Perkins RG, Scott RE (1978) Plasma membrane phospholipid, cholesterol and fatty acyl composition of differentiated and undifferentiated L6 myoblasts. Lipids 13(5):334–337

    Article  CAS  PubMed  Google Scholar 

  227. Aresta-Branco F et al (2011) Gel domains in the plasma membrane of Saccharomyces cerevisiae: highly ordered, ergosterol-free, and sphingolipid-enriched lipid rafts. J Biol Chem 286(7):5043–5054

    Article  CAS  PubMed  Google Scholar 

  228. Fujita A, Cheng J, Fujimoto T (2009) Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim Biophys Acta 1791(5):388–396

    Article  CAS  PubMed  Google Scholar 

  229. Das A et al (2013) Use of mutant 125I-perfringolysin O to probe transport and organization of cholesterol in membranes of animal cells. Proc Natl Acad Sci USA 110(26):10580–10585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  230. Jin H, McCaffery JM, Grote E (2008) Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J Cell Biol 180(4):813–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  231. Chierico L et al (2014) Live cell imaging of membrane/cytoskeleton interactions and membrane topology. Sci Rep 4:6056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Veatch SL, Keller SL (2003) Separation of liquid phases in giant vesicles of ternary mixtures of phospholipids and cholesterol. Biophys J 85(5):3074–3083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Machta BB, Veatch SL, Sethna JP (2012) Critical Casimir forces in cellular membranes. Phys Rev Lett 109(13):138101–138101

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  234. Lee I-H et al (2015) Live cell plasma membranes do not exhibit a miscibility phase transition over a wide range of temperatures. J Phys Chem B 119(12):4450–4459

    Article  CAS  PubMed  Google Scholar 

  235. Adami C (1995) Self-organized criticality in living systems. Phys Lett A 2013:29–32

    Article  Google Scholar 

  236. Jensen H (1998) Self-organized criticality: emergent complex behavior in physical and biological systems (Cambridge lecture notes in Physics), Cambridge University Press,Cambridge

    Google Scholar 

  237. Heberle FA et al (2013) Bilayer thickness mismatch controls domain size in model membranes. J Am Chem Soc 135(18):6853–6859

    Article  CAS  PubMed  Google Scholar 

  238. Samsonov AV, Mihalyov I, Cohen FS (2001) Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys J 81(3):1486–1500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. D'Auria L et al (2013) Surfactins modulate the lateral organization of fluorescent membrane polar lipids: a new tool to study drug:membrane interaction and assessment of the role of cholesterol and drug acyl chain length. Biochim Biophys Acta 1828(9):2064–2073

    Article  PubMed  CAS  Google Scholar 

  240. Kuzmin PI et al (2005) Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys J 88(2):1120–1133

    Article  CAS  PubMed  Google Scholar 

  241. Frolov VAJ et al (2006) “Entropic Traps” in the Kinetics of Phase Separation in Multicomponent Membranes Stabilize Nanodomains. Biophys J 91(1):189–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. García-Sáez AJ, Schwille P (2010) Stability of lipid domains. FEBS Lett 584(9):1653–1658

    Article  PubMed  CAS  Google Scholar 

  243. Simons K, Vaz WLC (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33(1):269–295

    Article  CAS  PubMed  Google Scholar 

  244. Castro BM, Prieto M, Silva LC (2014) Ceramide: a simple sphingolipid with unique biophysical properties. Prog Lipid Res 54:53–67

    Article  CAS  PubMed  Google Scholar 

  245. Sot J et al (2006) Detergent-resistant, ceramide-enriched domains in sphingomyelin/ceramide bilayers. Biophys J 90(3):903–914

    Article  CAS  PubMed  Google Scholar 

  246. Koldso H et al (2014) Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLoS Comput Biol 10(10):e1003911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  247. Patel DS et al (2016) Influence of ganglioside GM1 concentration on lipid clustering and membrane properties and curvature. Biophys J 111(9):1987–1999

    Article  CAS  PubMed  Google Scholar 

  248. Mukherjee S, Soe TT, Maxfield FR (1999) Endocytic sorting of lipid analogues differing solely in the chemistry of their hydrophobic tails. J Cell Biol 144(6):1271–1284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Mukherjee S, Maxfield FR (2000) Role of membrane organization and membrane domains in endocytic lipid trafficking. Traffic (Copenhagen, Denmark) 1(3):203–211

    Article  CAS  Google Scholar 

  250. Roux A et al (2005) Role of curvature and phase transition in lipid sorting and fission of membrane tubules. EMBO J 24(8):1537–1545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Parthasarathy R, Yu C-h, Groves JT (2006) Curvature-modulated phase separation in lipid bilayer membranes. LANGMUIR 22(11):5095–5099

    Article  CAS  PubMed  Google Scholar 

  252. Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425(6960):821–824

    Article  CAS  PubMed  Google Scholar 

  253. Ursell TS, Klug WS, Phillips R (2009) Morphology and interaction between lipid domains. Proc Natl Acad Sci USA 106(32):13301–13306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  254. Veatch SL, Keller SL (2005) Seeing spots: complex phase behavior in simple membranes. Biochimica et Biophysica Acta (BBA) Mol Cell Res 1746(3):172–185

    Article  CAS  Google Scholar 

  255. Kiessling V, Crane JM, Tamm LK (2006) Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys J 91(9):3313–3326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Fujiwara T et al (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157(6):1071–1082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Nawaz S et al (2009) Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in Oligodendroglial cells and its rapid perturbation by elevated calcium. J Neurosci 29(15):4794

    Article  CAS  PubMed  Google Scholar 

  258. May S et al (2009) Trans-monolayer coupling of fluid domains in lipid bilayers. Soft Matter 5(17):3148–3148

    Article  CAS  Google Scholar 

  259. Leibler S, Andelman D (1987) Ordered and curved meso-structures in membranes and amphiphilic films. J Phys 48(11):2013–2018

    Article  CAS  Google Scholar 

  260. Merkel R, Sackmann E, Evans E (1989) Molecular friction and epitactic coupling between monolayers in supported bilayers. J Phys 50(12):1535–1555

    Article  CAS  Google Scholar 

  261. Collins MD, Keller SL (2008) Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc Natl Acad Sci 105(1):124–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Brewer J et al (2017) Enzymatic studies on planar supported membranes using a widefield fluorescence LAURDAN generalized polarization imaging approach. Biochim Biophys Acta 1859(5):888–895

    Article  CAS  PubMed  Google Scholar 

  263. Kusumi A, Koyama-Honda I, Suzuki K (2004) Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5(4):213–230

    Article  CAS  PubMed  Google Scholar 

  264. Gri G et al (2004) The inner side of T cell lipid rafts. Immunol Lett 94(3):247–252

    Article  CAS  PubMed  Google Scholar 

  265. Pyenta PS, Holowka D, Baird B (2001) Cross-correlation analysis of inner-leaflet-anchored green fluorescent protein co-redistributed with IgE receptors and outer leaflet lipid raft components. Biophys J 80(5):2120–2132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  266. Lee KYC, McConnell HM (1993) Quantized symmetry of liquid monolayer domains. J Phys Chem 97(37):9532–9539

    Article  CAS  Google Scholar 

  267. Travesset A (2006) Effect of dipolar moments in domain sizes of lipid bilayers and monolayers. J Chem Phys 125(8):084905–084905

    Article  CAS  PubMed  Google Scholar 

  268. Inoue I, Kobatake Y, Tasaki I (1973) Excitability, instability and phase transitions in squid axon membrane under internal perfusion with dilute salt solutions. Biochim Biophys Acta Biomembr 307(3):471–477

    Article  CAS  Google Scholar 

  269. Melamed-Harel H, Reinhold L (1979) Hysteresis in the responses of membrane potential, membrane resistance, and growth rate to cyclic temperature change. Plant Physiol 63(6):1089–1094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  270. Herman P et al (2015) Depolarization affects the lateral microdomain structure of yeast plasma membrane. FEBS J 282(3):419–434

    Article  CAS  PubMed  Google Scholar 

  271. Malinsky J, Tanner W, Opekarova M (2016) Transmembrane voltage: Potential to induce lateral microdomains. Biochimica et Biophysica Acta (BBA) – Mol Cell Biol Lipids 1861(8):806–811

    Article  CAS  Google Scholar 

  272. Rossy J, Ma Y, Gaus K (2014) The organisation of the cell membrane: do proteins rule lipids? Curr Opin Chem Biol 20:54–59

    Article  CAS  PubMed  Google Scholar 

  273. Mayor S, Rao M (2004) Rafts: scale-dependent, active lipid Organization at the Cell Surface. Traffic 5(4):231–240

    Article  CAS  PubMed  Google Scholar 

  274. Sharma P et al (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116(4):577–589

    Article  CAS  PubMed  Google Scholar 

  275. Nicolini C et al (2006) Visualizing association of N-Ras in lipid microdomains: influence of domain structure and interfacial adsorption. J Am Chem Soc 128(1):192–201

    Article  CAS  PubMed  Google Scholar 

  276. García-Sáez AJ et al (2007) Pore formation by a Bax-derived peptide: effect on the line tension of the membrane probed by AFM. Biophys J 93(1):103–112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  277. Jensen MØ, Mouritsen OG (2004) Lipids do influence protein function—the hydrophobic matching hypothesis revisited. Biochim Biophys Acta Biomembr 1666(1–2):205–226

    Article  CAS  Google Scholar 

  278. Mitra K et al (2004) Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proc Natl Acad Sci USA 101(12):4083–4088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Larson DR et al (2005) Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. J Cell Biol 171(3):527–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  280. Gaus K et al (2005) Condensation of the plasma membrane at the site of T lymphocyte activation. J Cell Biol 171(1):121–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Kusumi A et al (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351–378

    Article  CAS  PubMed  Google Scholar 

  282. Kay JG et al (2012) Phosphatidylserine dynamics in cellular membranes. Mol Biol Cell 23(11):2198–2212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  283. Liu AP, Fletcher DA (2006) Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys J 91(11):4064–4070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Honigmann A et al (2014) A lipid bound actin meshwork organizes liquid phase separation in model membranes. Elife 3:e01671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  285. Arumugam S, Petrov EP, Schwille P (2015) Cytoskeletal pinning controls phase separation in multicomponent lipid membranes. Biophys J 108(5):1104–1113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  286. Honigmann A, Pralle A (2016) Compartmentalization of the cell membrane. J Mol Biol 428(24):4739–4748

    Article  CAS  PubMed  Google Scholar 

  287. Kusumi A et al (2012) Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of singer and Nicolson's fluid-mosaic model. Annu Rev Cell Dev Biol 28:215–250

    Article  CAS  PubMed  Google Scholar 

  288. Kusumi A et al (2012) Membrane mechanisms for signal transduction: the coupling of the meso-scale raft domains to membrane-skeleton-induced compartments and dynamic protein complexes. Semin Cell Dev Biol 23(2):126–144

    Article  CAS  PubMed  Google Scholar 

  289. Kusumi A et al (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36(11):604–615

    Article  CAS  PubMed  Google Scholar 

  290. Janmey PA, Lindberg U (2004) Cytoskeletal regulation: rich in lipids. Nat Rev Mol Cell Biol 5(8):658–666

    Article  CAS  PubMed  Google Scholar 

  291. Rao M, Mayor S (2014) Active organization of membrane constituents in living cells. Curr Opin Cell Biol 29:126–132

    Article  CAS  PubMed  Google Scholar 

  292. Sheetz MP, Sable JE, Dobereiner HG (2006) Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu Rev Biophys Biomol Struct 35:417–434

    Article  CAS  PubMed  Google Scholar 

  293. de la Serna JB et al (2016) There is no simple model of the plasma membrane organization. Front Cell Dev Biol 4:106

    Google Scholar 

  294. Johnson SA et al (2010) Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim Biophys Acta Biomembr 1798(7):1427–1435

    Article  CAS  Google Scholar 

  295. Lingwood D et al (2008) Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc Natl Acad Sci USA 105(29):10005–10010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  296. Windschiegl B et al (2009) Lipid reorganization induced by Shiga toxin clustering on planar membranes. PLoS One 4(7):e6238–e6238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  297. Zhao H et al (2013) Membrane-sculpting BAR domains generate stable lipid microdomains. Cell Rep 4(6):1213–1223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  298. Picas L et al (2014) BIN1/M-Amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin. Nat Commun 5:5647

    Article  CAS  PubMed  Google Scholar 

  299. Levental I et al (2009) Calcium-dependent lateral organization in phosphatidylinositol 4,5-bisphosphate (PIP2)- and cholesterol-containing monolayers. Biochemistry 48(34):8241–8248

    Article  CAS  PubMed  Google Scholar 

  300. Sarmento MJ et al (2014) Ca(2+) induces PI(4,5)P2 clusters on lipid bilayers at physiological PI(4,5)P2 and Ca(2+) concentrations. Biochim Biophys Acta 1838(3):822–830

    Article  CAS  PubMed  Google Scholar 

  301. Carvalho K et al (2008) Giant unilamellar vesicles containing phosphatidylinositol(4,5)bisphosphate: characterization and functionality. Biophys J 95(9):4348–4360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  302. Laux T et al (2000) GAP43, MARCKS, and CAP23 modulate PI(4,5)P(2) at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149(7):1455–1472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  303. McLaughlin S, Murray D (2005) Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438(7068):605–611

    Article  CAS  PubMed  Google Scholar 

  304. Milovanovic D et al (2016) Calcium promotes the formation of Syntaxin 1 mesoscale domains through phosphatidylinositol 4,5-bisphosphate. J Biol Chem 291(15):7868–7876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  305. Shi X et al (2013) Ca2+ regulates T-cell receptor activation by modulating the charge property of lipids. Nature 493(7430):111–115

    Article  PubMed  CAS  Google Scholar 

  306. Li L et al (2014) Ionic protein-lipid interaction at the plasma membrane: what can the charge do? Trends Biochem Sci 39(3):130–140

    Article  CAS  PubMed  Google Scholar 

  307. Visser D et al (2013) TRPM7 triggers Ca2+ sparks and invadosome formation in neuroblastoma cells. Cell Calcium 54(6):404–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  308. Wei C et al (2009) Calcium flickers steer cell migration. Nature 457(7231):901–905

    Article  CAS  PubMed  Google Scholar 

  309. Wu M, Wu X, De Camilli P (2013) Calcium oscillations-coupled conversion of actin travelling waves to standing oscillations. Proc Natl Acad Sci USA 110(4):1339–1344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  310. Foret L et al (2005) A simple mechanism of raft formation in two-component fluid membranes. Europhy Lett (EPL) 71(3):508–514

    Article  CAS  Google Scholar 

  311. Turner MS, Sens P, Socci ND (2005) Nonequilibrium raftlike membrane domains under continuous recycling. Phys Rev Lett 95(16):168301

    Article  PubMed  CAS  Google Scholar 

  312. Schmid F (2016) Physical mechanisms of micro- and nanodomain formation in multicomponent lipid membranes. Biochim Biophys Acta 1859:509

    Article  PubMed  CAS  Google Scholar 

  313. Fan J, Sammalkorpi M, Haataja M (2010) Formation and regulation of lipid microdomains in cell membranes: theory, modeling, and speculation. FEBS Lett 584(9):1678–1684

    Article  CAS  PubMed  Google Scholar 

  314. Bernal P et al (2007) A pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ Microbiol 9(5):1135–1145

    Article  CAS  PubMed  Google Scholar 

  315. Tocheva EI, Li Z, Jensen GJ (2010) Electron cryotomography. Cold Spring Harb Perspect Biol 2(6):a003442–a003442

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  316. Huang KC, Ramamurthi KS (2010) Macromolecules that prefer their membranes curvy. Mol Microbiol 76(4):822–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  317. Hirschberg CB, Kennedy EP (1972) Mechanism of the enzymatic synthesis of cardiolipin in Escherichia coli. Proc Natl Acad Sci USA 69(3):648–651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  318. Huang KC et al (2006) A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2(11):e151–e151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  319. Mukhopadhyay R, Huang KC, Wingreen NS (2008) Lipid localization in bacterial cells through curvature-mediated microphase separation. Biophys J 95(3):1034–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  320. Lin T-Y et al (2015) A Cardiolipin-deficient mutant of Rhodobacter sphaeroides has an altered cell shape and is impaired in biofilm formation. J Bacteriol 197(21):3446–3455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  321. Ursell TS et al (2014) Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci USA 111(11):E1025–E1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  322. Derganc J (2007) Curvature-driven lateral segregation of membrane constituents in Golgi cisternae. Phys Biol 4(4):317–324

    Article  CAS  PubMed  Google Scholar 

  323. Akimov SA et al (2007) Lateral tension increases the line tension between two domains in a lipid bilayer membrane. Phys Rev E Stat Nonlinear Soft Matter Phys 75(1):011919

    Article  CAS  Google Scholar 

  324. Mohandas N, Gallagher PG (2008) Red cell membrane: past, present, and future. Blood 112(10):3939–3948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  325. Lutz HU, Bogdanova A (2013) Mechanisms tagging senescent red blood cells for clearance in healthy humans. Front Physiol 4:387

    Article  PubMed  PubMed Central  Google Scholar 

  326. Antonelou MH, Kriebardis AG, Papassideri IS (2010) Aging and death signalling in mature red cells: from basic science to transfusion practice. Blood Transfus 8(Suppl 3):s39–s47

    PubMed  PubMed Central  Google Scholar 

  327. Fricke K, Sackmann E (1984) Variation of frequency spectrum of the erythrocyte flickering caused by aging, osmolarity, temperature and pathological changes. Biochim Biophys Acta 803(3):145–152

    Article  CAS  PubMed  Google Scholar 

  328. Gov NS, Safran SA (2005) Red blood cell membrane fluctuations and shape controlled by ATP-induced cytoskeletal defects. Biophys J 88(3):1859–1874

    Article  CAS  PubMed  Google Scholar 

  329. Edwards CL et al (2005) A brief review of the pathophysiology, associated pain, and psychosocial issues in sickle cell disease. Int J Behav Med 12(3):171–179

    Article  PubMed  Google Scholar 

  330. Willekens FL et al (2008) Erythrocyte vesiculation: a self-protective mechanism? Br J Haematol 141(4):549–556

    Article  CAS  PubMed  Google Scholar 

  331. Stewart A et al (2005) The application of a new quantitative assay for the monitoring of integrin-associated protein CD47 on red blood cells during storage and comparison with the expression of CD47 and phosphatidylserine with flow cytometry. Transfusion 45(9):1496–1503

    Article  CAS  PubMed  Google Scholar 

  332. Bogdanova A et al (2013) Calcium in red blood cells-a perilous balance. Int J Mol Sci 14(5):9848–9872

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  333. Salzer U et al (2002) Ca(++)-dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood 99(7):2569–2577

    Article  CAS  PubMed  Google Scholar 

  334. Li H, Lykotrafitis G (2015) Vesiculation of healthy and defective red blood cells. Phys Rev E Stat Nonlinear Soft Matter Phys 92(1):012715

    Article  CAS  Google Scholar 

  335. Vind-Kezunovic D et al (2008) Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells. Biochim Biophys Acta 1778(11):2480–2486

    Article  CAS  PubMed  Google Scholar 

  336. Del Conde I et al (2005) Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106(5):1604–1611

    Article  PubMed  CAS  Google Scholar 

  337. Scheiffele P et al (1999) Influenza viruses select ordered lipid domains during budding from the plasma membrane. J Biol Chem 274(4):2038–2044

    Article  CAS  PubMed  Google Scholar 

  338. Maddock JR, Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science (New York, NY) 259(5102):1717–1723

    Article  CAS  Google Scholar 

  339. Lutkenhaus J (2002) Dynamic proteins in bacteria. Curr Opin Microbiol 5(6):548–552

    Article  CAS  PubMed  Google Scholar 

  340. Mileykovskaya E et al (1998) Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. J Bacteriol 180(16):4252–4257

    CAS  PubMed  PubMed Central  Google Scholar 

  341. Renner LD, Weibel DB (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci USA 108(15):6264–6269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  342. Martin SW, Konopka JB (2004) Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 3(3):675–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  343. Takeshita N et al (2008) Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19(1):339–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  344. Wachtler V, Rajagopalan S, Balasubramanian MK (2003) Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. J Cell Sci 116(5):867–874

    Article  CAS  PubMed  Google Scholar 

  345. Bagnat M, Simons K (2002) Cell surface polarization during yeast mating. Proc Natl Acad Sci USA 99(22):14183–14188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  346. Sun Y et al (2000) Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipid-mediated signaling pathway of yeast. Mol Cell Biol 20(12):4411–4419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  347. Proszynski TJ et al (2006) Plasma membrane polarization during mating in yeast cells. J Cell Biol 173(6):861–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  348. Garrenton LS et al (2010) Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling. Proc Natl Acad Sci USA 107(26):11805–11810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  349. Vernay A et al (2012) A steep phosphoinositide bis-phosphate gradient forms during fungal filamentous growth. J Cell Biol 198(4):711–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  350. Iwamoto K et al (2004) Local exposure of phosphatidylethanolamine on the yeast plasma membrane is implicated in cell polarity. Genes Cells 9(10):891–903

    Article  CAS  PubMed  Google Scholar 

  351. Ng MM, Chang F, Burgess DR (2005) Movement of membrane domains and requirement of membrane signaling molecules for cytokinesis. Dev Cell 9(6):781–790

    Article  CAS  PubMed  Google Scholar 

  352. Emoto K et al (2005) Local change in phospholipid composition at the cleavage furrow is essential for completion of cytokinesis. J Biol Chem 280(45):37901–37907

    Article  CAS  PubMed  Google Scholar 

  353. Field SJ et al (2005) PtdIns(4,5)P2 functions at the cleavage furrow during cytokinesis. Curr Biol 15(15):1407–1412

    Article  CAS  PubMed  Google Scholar 

  354. Emoto K, Umeda M (2000) An essential role for a membrane lipid in cytokinesis. Regulation of contractile ring disassembly by redistribution of phosphatidylethanolamine. J Cell Biol 149(6):1215–1224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  355. Kraft ML (2013) Plasma membrane organization and function: moving past lipid rafts. Mol Biol Cell 24(18):2765–2768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  356. Sevcsik E, Schutz GJ (2016) With or without rafts? Alternative views on cell membranes. BioEssays 38(2):129–139

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge funding by UCL (FSR, ARC), the F.R.S-FNRS and the Salus Sanguinis foundation. We apologize to all colleagues whose work was not cited due to space constriction.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Donatienne Tyteca .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Léonard, C., Alsteens, D., Dumitru, A.C., Mingeot-Leclercq, MP., Tyteca, D. (2017). Lipid Domains and Membrane (Re)Shaping: From Biophysics to Biology. In: Epand, R., Ruysschaert, JM. (eds) The Biophysics of Cell Membranes. Springer Series in Biophysics, vol 19. Springer, Singapore. https://doi.org/10.1007/978-981-10-6244-5_5

Download citation

Publish with us

Policies and ethics