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Advanced Concepts and Perspectives of Membrane Physics

  • Erich SackmannEmail author
Chapter

Abstract

Highly effective pathways of transmembrane signal transmission are realized by functional membrane domain formation through logistically controlled recruitment of functional proteins to specific sites on cytoplasmic membrane leaflets. Sites of assembly are selected by priming membranes through master switches generating local swarms of super affinity lipid anchors, such as PI(3,4,5)P3 and diacylglycerol (DAG).

Formation and activation of functional domains are regulated by agonistically or antagonistically cooperating molecular switches. We consider here the agonistic Rab4/Rab 5 tandem, serving the rapid receptor recycling, and the antagonistic pair of GTPases Rac-1 and Rho A, controlling the state of the actin cortex. To avoid over-excitations of cells (implying the danger of tumorigenesis), the omnipresent phosphoinositide anchors are protected by layers of the polybasic protein MACKS recruited by electrostatic-hydrophobic forces.

The universality of cell control systems is exemplified by the observation that extrinsic forces and hormones can trigger the generation of very similar types of transmembrane signal transmission centers assembled around receptor tyrosine kinases (RTK). These signal amplifying domains can regulate cellular membrane processes simultaneously through fast biochemical signals, eliciting the rapid structural change of the composite cell envelope, and slow, genetically controlled processes for adapting the mechanical impedances of cells and tissues.

Membrane-based reactions can be controlled via the access of reaction spaces by constituents or enzymes. They can be regulated over large distances by contacting distant membranes through synaptic contacts (such as endoplasmic and of immunological synapses).

Hopefully, insights in the analogy of technical and biological control mechanism may teach us how to generate new self-healing composite materials in logistic ways.

Keywords

Functional membrane domain formation Membrane-associated protein recruitment by electrostatic hydrophobic forces Transmembrane signal amplifying domains MARCKS protein-controlled membrane processes Reticulons controlled tubular membrane networks Immunological and endoplasmic synapses 

Abbreviations

DAG

Diacylglycerol

GAP

Guanine hydrolyzing protein accelerating the deactivation of GTPase

GEF

Guanine exchange factor accelerating the activation of GTPases by replacement of GDP by GTP

GIP

Guanine exchange inhibitor that maintains GTPases in the resting state

P(4,5)P2, P(3,4,5)P3

Phosphoinositol (4,5)-diphosphate, Phosphatidylinositol (3,4,5)-trisphosphate

PCK

Protein kinase C, a regulator of filopoida formation

PI-3K

Protein kinase 3 that catalyzes the phosphorylation of the 3-OH position on the inositol ring

PSL-γ

Phospholipase gamma, the generator of DAG lipids

Notes

Acknowledgements

Financial support by the Excellence Program of the Technical University of Munich and by the Lehrstuhl für Angewandte Physik of the Ludwig Maximilian University is gratefully acknowledged.

References

  1. 1.
    Mouritsen OG (2011) Model answers to lipid membrane questions. Cold Spring Harb Perspect Biol 3:a004622CrossRefGoogle Scholar
  2. 2.
    Sackmann E (2006) Thermo-elasticity and adhesion as regulators of cell membrane architecture and function. J Phys Condens Matter 18(45):R785–R825CrossRefGoogle Scholar
  3. 3.
    Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch 28c:693–703CrossRefGoogle Scholar
  4. 4.
    Helfrich W (1978) Steric interaction of fluid membranes in multilayer systems. Z Naturforsch 33a:305–315Google Scholar
  5. 5.
    Evans EA (1974) Bending resistance and chemically induced moments in membrane bilayers. Biophys J 14:923–931CrossRefGoogle Scholar
  6. 6.
    Seifert U, Lipowsky R (1995) Morphology of vesicles. In: Lipowsky R, Sackmann E (eds) Handbook of biological physics, vol 1A. Elsevier, AmsterdamGoogle Scholar
  7. 7.
    Seifert U (1997) Configurations of fluid membranes and vesicles. Adv Phys 46:13–137CrossRefGoogle Scholar
  8. 8.
    Nelson P, Powers T, Seifert U (1995) Dynamical theory of the pearling instability in cylindrical vesicles. Phys Rev Lett 74:3384–3387CrossRefGoogle Scholar
  9. 9.
    Kozlov M (1999) Dynamin: possible mechanism of “Pinchase” action. Biophys J 59:604–616CrossRefGoogle Scholar
  10. 10.
    Brochard F, Lennon JF (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys France 36:1035–1047CrossRefGoogle Scholar
  11. 11.
    Millner ST, Safran S (1987) Dynamical fluctuations of droplet microemulsions and vesicles. Phys Rev A 36:4371–4382CrossRefGoogle Scholar
  12. 12.
    Mukhopadhyay R, Lim H, Wortis M (2002) Echinocyte shapes: bending, stretching, and shear determine spicule shape and spacing. Biophys J 82:1756–1772CrossRefGoogle Scholar
  13. 13.
    Auth T, Safran S, Gov N (2007) Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E 76:051910CrossRefGoogle Scholar
  14. 14.
    Zilker A, Ziegler M, Sackmann E (1992) Spectral analysis of erythrocyte flickering in the 0.3-4.0 μm regime by microinterferometry combined with fast image processing. Phys Rev A 46:7998–8001CrossRefGoogle Scholar
  15. 15.
    Döbereiner HG, Kas J, Noppl D, Sprenger I, Sackmann E (1993) Budding and fission of vesicles. Biophys J 65:1386–1403CrossRefGoogle Scholar
  16. 16.
    Bretcher M, Munro S (1993) Cholesterol and the Golgi apparatus. Science 26:1280–1281CrossRefGoogle Scholar
  17. 17.
    Ben-Shaul A (1995) Molecular theory of chain packing elasticity and lipid protein interaction in lipid bilayers. In: Lipowsky R, Sackmann E (eds) Handbook of biological physics, vol 1A. Elsevier, AmsterdamGoogle Scholar
  18. 18.
    Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425:821–824CrossRefGoogle Scholar
  19. 19.
    Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2008) Rab GTPases at a glance. J Cell Sci 120:3905–3910CrossRefGoogle Scholar
  20. 20.
    Wegener KL, Partridge AW, Han J, Pickford AR, Liddington RC, Ginsberg MH, Campbell ID (2007) Structural basis of integrin activation by talin. Cell 128:171–182CrossRefGoogle Scholar
  21. 21.
    Rädler J, Feder TJ, Strey HH, Sackmann E (1995) Fluctuation analysis of tension controlled undulation forces between giant vesicles and solid substrates. Phys Rev E 51:4526–4536CrossRefGoogle Scholar
  22. 22.
    Legate K, Fässler R (2009) Mechanisms that regulate adaptor binding to β-integrin cytoplasmic tails. J Cell Sci 122:187–198CrossRefGoogle Scholar
  23. 23.
    Scott A, Antal C, Newton A (2013) Electrostatic and hydrophobic interactions differentially tune membrane binding kinetics of the C2 domain of protein kinase C. J Biol Chem 288:16905–16915CrossRefGoogle Scholar
  24. 24.
    Galla HJ, Sackmann E (1975) Chemically induced lipid phase separation in model membranes containing containing charged lipids: a spin label study. Biochim Biophys Acta 401:509–529CrossRefGoogle Scholar
  25. 25.
    Traeuble H, Eibl H (1974) Electrostatic effects on lipid phase transitions: membrane structure and ionic environment. Proc Natl Acad Sci USA 71:214–219CrossRefGoogle Scholar
  26. 26.
    Cevc G (1990) Membrane electrostatics. Biochim Biophys Acta 1031:311–382CrossRefGoogle Scholar
  27. 27.
    Andelman D (1995) Chapter12—Electrostatic properties of membranes: the Poisson-Boltzmann theory. In: Lipowsky R, Sackmann E (eds) Handbook of biological physics, vol 1. North-Holland, Amsterdam, pp 603–642Google Scholar
  28. 28.
    Netz RR (1999) Debye-Hückel theory for interfacial geometries. Phys Rev E 60:3174–3182CrossRefGoogle Scholar
  29. 29.
    Stahelin RV, Karathanassis D, Bruzik KS, Waterfield MD, Bravo J, Williams RL, Cho W (2006) Structural and membrane binding analysis of the Phox homology domain of phosphoinositide 3-kinase-C2α. J Biol Chem 281:9845–9856CrossRefGoogle Scholar
  30. 30.
    McLaughlin S (2002) PIP2 and proteins: interactions, organization and information flow. Annu Rev Biophys Biomol Struct 31:151–175CrossRefGoogle Scholar
  31. 31.
    Tzlil S, Murray D, Ben Shaul A (2008) The electrostatic switch mechanism: Monte Carlo study of MARCKS-Membrane interaction. Biophys J 95:1745–1757CrossRefGoogle Scholar
  32. 32.
    Côté JF, Vuori K (2007) GEF what? Dock180 and related proteins help Rac to polarize cells. Trends Cell Biol 17:383–393CrossRefGoogle Scholar
  33. 33.
    Sackmann E (2015) How actin-myosin cross talks guides the adhesion, locomotion and polarization of cells. Biochim Biophys Acta 1853:3132–3142CrossRefGoogle Scholar
  34. 34.
    Das S, Dixon J, Cho W (2003) Membrane-binding and activation mechanism of PTEN. Proc Natl Acad Sci USA 100:7491–7496CrossRefGoogle Scholar
  35. 35.
    Landgraf KE, Pilling C, Falke JJ (2008) Molecular mechanism of an oncogenic mutation that alters membrane targeting: Glu17Lys modifies the PIP lipid specificity of the AKT1 PH domain. Biochemistry 47:12260–12269CrossRefGoogle Scholar
  36. 36.
    Bruinsma R, Behrisch A, Sackmann E (2000) Adhesive switching of membranes: Experiment and theory. Phys Rev E 61:4253–4267CrossRefGoogle Scholar
  37. 37.
    Sackmann E, Smith A (2014) Physics of cell adhesion: some lessons learned from cell mimetic systems. Soft Matter 10:1644–1659CrossRefGoogle Scholar
  38. 38.
    Sackmann E (2011) Quantal concept of T-cell activation: adhesion domains as immunological synapses. New J Phys 13:065013CrossRefGoogle Scholar
  39. 39.
    Dustin M, Allen PM, Shaw AS (2001) Environmental control of immunological synapse formation and duration. Trends Immunol 22:192–204CrossRefGoogle Scholar
  40. 40.
    Watanabe TM, Tokuo H, Gonda K, Higuchi H, Ikebe M (2010) Myosin-X induces filopodia by multiple elongations. J Biol Chem 285:19605–19614CrossRefGoogle Scholar
  41. 41.
    Breitsprecher D, Kiesewetter AK, Linkner J, Vinzenz M, Stradal TE, Small JV, Curth U, Dickinson RB, Faix J (2011) Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J 30:456–467CrossRefGoogle Scholar
  42. 42.
    Smith KA (2006) The quantal theory of immunity. Cell Res 16:11–19CrossRefGoogle Scholar
  43. 43.
    Sackmann E (2014) Endoplasmatic reticulum shaping by generic mechanisms and protein-induced spontaneous curvature. Adv Colloid Interf Sci 208:153–160CrossRefGoogle Scholar
  44. 44.
    Griner EM, Kazanietz MG (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 7:281–294CrossRefGoogle Scholar
  45. 45.
    Haimin L, Gang C, Bing Z, Shumin D (2008) Actin filament assembly by myristoylated, alanine-rich C Kinase substrate-phosphatidylinositol-4,5-diphosphate signaling is critical for dendrite branching. Mol Biol Cell 19:4804–4813CrossRefGoogle Scholar
  46. 46.
    Calabrese B, Wilson M, Halpain S (2006) Development and regulation of dendritic spine synapses. Physiology 21:38–47CrossRefGoogle Scholar
  47. 47.
    Bornschlögl T, Romero S, Vestergaard C, Joanny JF, Tran Van Nhieu G, Bassereau P (2013) Filopodial retraction force is generated by cortical actin dynamics and controlled by reversible tethering at the tip. Proc Natl Acad Sci USA 110:18928–18933CrossRefGoogle Scholar
  48. 48.
    Zidovska A, Sackmann E (2011) On the mechanical stabilization of filopodia. Biophys J 100:1428–1437CrossRefGoogle Scholar
  49. 49.
    Khelashvili K, Weinstein H, Harries D (2008) Protein diffusion on charged membranes: a dynamic mean-field model describes time evolution and lipid reorganization. Biophys J 94:2580–2597CrossRefGoogle Scholar
  50. 50.
    Diamant H, Andelman D (1997) Adsorption kinetic of surfactants at fluid-fluid interfaces. Progr Colloid Polym Sci 103:51–59CrossRefGoogle Scholar
  51. 51.
    Góźdź W, Gompper G (1998) Composition-driven shape transformations of membranes of complex topology. Phys Rev Lett 80:4213–4217CrossRefGoogle Scholar
  52. 52.
    Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124:573–586CrossRefGoogle Scholar
  53. 53.
    Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J, Bassereau P, Roux A (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci USA 109:173–179CrossRefGoogle Scholar
  54. 54.
    Tlusty T, Safran S, Strey R (2000) Topology, phase instabilities, and wetting of microemulsion networks. Phys Rev Lett 84:1244CrossRefGoogle Scholar
  55. 55.
    Park SH (2010) Hereditary spastic paraplegia proteinREEP1, spastin, and atlastin-1 coordinate microtubule interactions with the tubular ER network. J Clin Invest 120:1097–1109CrossRefGoogle Scholar
  56. 56.
    Monteleone MC, González Wusener AE, Burdisso JE, Conde C, Cáceres A, Arregui CO (2012) ER-bound protein tyrosine phosphatase PTP1B interacts with Src at the plasma membrane/substrate interface. PLoS One 7:e38948CrossRefGoogle Scholar
  57. 57.
    Bian X, Klemm RW, Liu TY, Zhang M, Sun S, Sui X, Liu X, Rapoport TA, Hu J (2001) Structures of the atlastin GTPase provide insight into homotypic fusion of endoplasmic reticulum membranes. Proc Natl Acad Sci USA 108:3976CrossRefGoogle Scholar
  58. 58.
    Simunovic M, Voth GA, Callan-Jones A, Bassereau P (2015) When physics takes over: BAR proteins and membrane curvature. Trends Cell Biol 25:780–792CrossRefGoogle Scholar
  59. 59.
    Keber F, Loiseau E, Sanchez T, DeCamp S, Giomi L, Bowick M, Marchetti M, Dogic Z, Bausch A (2014) Topology and dynamics of active nematic vesicles. Science 345:1135–1139CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Technical University MunichMunichGermany
  2. 2.Physics Department E22/E27GarchingGermany

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