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Lateral Membrane Heterogeneity Probed by FRET Spectroscopy and Microscopy

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Fluorescent Methods to Study Biological Membranes

Part of the book series: Springer Series on Fluorescence ((SS FLUOR,volume 13))

Abstract

Förster resonance energy transfer (FRET) is a photophysical process highly dependent on interchromophore distance. Due to this feature, it is very sensitive to membrane lateral heterogeneity, as the donor and acceptor fluorophores involved in FRET tend to have different preference for distinct types of lipid bilayer domains. In this chapter, the basic formalisms of FRET in situations of increasing complexity (from a single donor-acceptor pair at a fixed distance to non-random probe distribution) are presented and illustrated with selected examples from the literature. The importance of time-resolved fluorescence data is emphasized. It is shown that FRET can be used to study the occurrence of domain formation, allowing their detection as well as size estimation. Lateral lipid distribution heterogeneity may also result from peptide- or protein-lipid interaction. Formalisms that apply to these situations are also presented, as well as selected examples of their use. Applications of FRET under the microscope have recently come to the fore, and representative studies are mentioned.

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References

  1. Abrams FS, London E (1993) Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 32:10826–10831

    CAS  Google Scholar 

  2. Acasandrei MA, Dale RE, VandeVen M, Ameloot M (2006) Two-dimensional Förster resonance energy transfer (2-D FRET) and the membrane raft hypothesis. Chem Phys Lett 419:469–473

    CAS  Google Scholar 

  3. Almeida PFF, Vaz WLC, Thompson TE (1992) Lateral diffusion in the liquid-phases of dimyristoylphosphatidylcholine cholesterol lipid bilayers - a free-volume analysis. Biochemistry 31:6739–6747

    CAS  Google Scholar 

  4. Almeida PF, Pokorny A, Hinderliter A (2005) Thermodynamics of membrane domains. Biochim Biophys Acta 1720:1–13

    CAS  Google Scholar 

  5. Anikovsky M, Dale L, Ferguson S, Petersen N (2008) Resonance energy transfer in cells: a new look at fixation effect and receptor aggregation on cell membrane. Biophys J 95:1349–1359

    CAS  Google Scholar 

  6. Berning S, Willig KI, Steffens H, Dibaj P, Hell SW (2012) Nanoscopy in a living mouse brain. Science 335:551

    CAS  Google Scholar 

  7. Bloom M, Mouritsen OG (1995) The evolution of membranes. In: Lipowsky R, Sackmann E (eds) Handbook of biological physics, vol 1A, Structure and dynamics of membranes - from cells to vesicles. Elsevier, Amsterdam, pp 65–95

    Google Scholar 

  8. Bogdanov M, Dowhan W (1995) Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J Biol Chem 270:732–739

    CAS  Google Scholar 

  9. Bogdanov M, Dowhan W (1998) Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J 17:5255–5264

    CAS  Google Scholar 

  10. Bogdanov M, Heacock PN, Dowhan W (2002) A polytopic membrane protein displays a reversible topology dependent on membrane lipid composition. EMBO J 21:2107–2116

    CAS  Google Scholar 

  11. Bogdanov M, Xie J, Heacock P, Dowhan W (2008) To flip or not to flip: lipid-protein charge interactions are a determinant of final membrane protein topology. J Cell Biol 182:925–935

    CAS  Google Scholar 

  12. Bogdanov M, Xie J, Dowhan W (2009) Lipid-protein interactions drive membrane protein topogenesis in accordance with the positive inside rule. J Biol Chem 284:9637–9641

    CAS  Google Scholar 

  13. Bogdanov M, Heacock P, Guan Z, Dowhan W (2010) Plasticity of lipid-protein interactions in the function and topogenesis of the membrane protein lactose permease from Escherichia coli. Proc Natl Acad Sci USA 107:15057–15062

    CAS  Google Scholar 

  14. Breitenstein D, Batenburg JJ, Hagenhoff B, Galla HJ (2006) Lipid specificity of surfactant protein B studied by time-of-flight secondary ion mass spectrometry. Biophys J 91:1347–1356

    CAS  Google Scholar 

  15. Brown AC, Towles KB, Wrenn SP (2007) Measuring raft size as a function of membrane composition in PC-based systems: Part I - binary systems. Langmuir 23:11180–11187

    CAS  Google Scholar 

  16. Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221–17224

    CAS  Google Scholar 

  17. Buboltz JT (2007) Steady-state probe-partitioning FRET: A simple and robust tool for the study of membrane phase behavior. Phys Rev E 76:021903

    Google Scholar 

  18. Buboltz JT, Bwalya C, Reyes S, Kamburov D (2007) Stern-Volmer modeling of steady-state Forster energy transfer between dilute, freely diffusing membrane-bound fluorophores. J Chem Phys 127:215101

    Google Scholar 

  19. Buboltz JT, Bwalya C, Williams K, Schutzer M (2007) High resolution mapping of phase behavior in a ternary lipid mixture: do lipid-raft phase boundaries depend on sample-prep procedure? Langmuir 23:11968–11971

    CAS  Google Scholar 

  20. Cabré EJ, Loura LMS, Fedorov A, Pérez-Gil J, Prieto M (2012) Topology and lipid selectivity of pulmonary surfactant protein SP-B in membranes: answers from fluorescence. Biochim Biophys Acta. doi:10.1016/j.bbamem.2012.03.008

  21. Castro BM, de Almeida RF, Goormaghtigh E, Fedorov A, Prieto M (2011) Organization and dynamics of Fas transmembrane domain in raft membranes and modulation by ceramide. Biophys J 101:1632–1641

    CAS  Google Scholar 

  22. Chachaty C, Rainteau D, Tessier C, Quinn PJ, Wolf C (2005) Building up of the liquid-ordered phase formed by sphingomyelin and cholesterol. Biophys J 88:4032–4044

    CAS  Google Scholar 

  23. Chattopadhyay A (1990) Chemistry and biology of N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)-labeled lipids: fluorescent probes of biological and model membranes. Chem Phys Lipids 53:1–15

    CAS  Google Scholar 

  24. Chen CC, Wilson TH (1984) The phospholipid requirement for activity of the lactose carrier of Escherichia coli. J Biol Chem 259:10150–10158

    CAS  Google Scholar 

  25. Chiantia S, Kahya N, Schwille P (2007) Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 23:7659–7665

    CAS  Google Scholar 

  26. Clements JA (1977) Functions of the alveolar lining. Am Rev Respir Dis 115:67–71

    CAS  Google Scholar 

  27. Coutinho A, Loura LMS, Fedorov A, Prieto M (2008) Pinched multilamellar structure of aggregates of lysozyme and phosphatidylserine-containing membranes revealed by FRET. Biophys J 95:4726–4736

    CAS  Google Scholar 

  28. Cruz A, Casals C, Plasencia I, Marsh D, Pérez-Gil J (1998) Depth profiles of pulmonary surfactant protein B in phosphatidylcholine bilayers, studied by fluorescence and electron spin resonance spectroscopy. Biochemistry 37:9488–9496

    CAS  Google Scholar 

  29. Cruz A, Marsh D, Pérez-Gil J (1998) Rotational dynamics of spin-labelled surfactant-associated proteins SP-B and SP-C in dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers. Biochim Biophys Acta 1415:125–134

    CAS  Google Scholar 

  30. Czech MP (2000) PIP2 and PIP3: complex roles at the cell surface. Cell 100:603–606

    CAS  Google Scholar 

  31. Davenport L (1997) Fluorescence probes for studying membrane heterogeneity. Meth Enzymol 278:487–512

    CAS  Google Scholar 

  32. de Almeida RFM, Loura LMS, Fedorov A, Prieto M (2002) Nonequilibrium phenomena in the phase separation of a two-component lipid bilayer. Biophys J 82:823–834

    Google Scholar 

  33. de Almeida RFM, Fedorov A, Prieto M (2003) Sphingomyelin/Phosphatidylcholine/Cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys J 85:2406–2416

    Google Scholar 

  34. de Almeida RFM, Loura LMS, Prieto M, Watts A, Fedorov A, Barrantes FJ (2004) Cholesterol modulates the organization of the γM4 transmembrane domain of the muscle nicotinic acetylcholine receptor. Biophys J 86:2261–2272

    Google Scholar 

  35. de Almeida RFM, Loura LMS, Fedorov A, Prieto M (2005) Lipid rafts have different sizes depending on membrane composition: a time-resolved fluorescence resonance energy transfer study. J Mol Biol 346:1109–1120

    Google Scholar 

  36. de Almeida RFM, Borst J, Fedorov A, Prieto M, Visser AJWG (2007) Complexity of lipid domains and rafts in giant unilamellar vesicles revealed by combining imaging and microscopic and macroscopic time-resolved fluorescence. Biophys J 93:539–553

    Google Scholar 

  37. de Almeida RF, Loura LMS, Prieto M (2009) Membrane lipid domains and rafts: current applications of fluorescence lifetime spectroscopy and imaging. Chem Phys Lipids 157:61–77

    Google Scholar 

  38. Dickenson NE, Armendariz KP, Huckabay HA, Livanec PW, Dunn RC (2010) Near-field scanning optical microscopy: a tool for nanometric exploration of biological membranes. Anal Bioanal Chem 396:31–43

    CAS  Google Scholar 

  39. Dico AS, Hancock J, Morrow MR, Stewart J, Harris S, Keough KM (1997) Pulmonary surfactant protein SP-B interacts similarly with dipalmitoylphosphatidylglycerol and dipalmitoylphosphatidylcholine in phosphatidylcholine/phosphatidylglycerol mixtures. Biochemistry 36:4172–4177

    CAS  Google Scholar 

  40. Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232

    CAS  Google Scholar 

  41. Fernandes F, Loura LMS, Prieto M, Koehorst R, Spruijt R, Hemminga MA (2003) Dependence of M13 major coat protein oligomerization and lateral segregation on bilayer composition. Biophys J 85:2430–2441

    CAS  Google Scholar 

  42. Fernandes F, Loura LM, Koehorst R, Spruijt RB, Hemminga MA, Fedorov A, Prieto M (2004) Quantification of protein-lipid selectivity using FRET: application to the M13 major coat protein. Biophys J 87:344–352

    CAS  Google Scholar 

  43. Fernandes F, Loura LMS, Fedorov A, Prieto M (2006) Absence of clustering of phosphatidylinositol-(4,5)-bisphosphate in fluid phosphatidylcholine. J Lipid Res 47:1521–1525

    CAS  Google Scholar 

  44. Förster T (1949)) Experimentelle und theoretische Untersuchung des Zwischenmolekularen übergangs von Elektrinenanregungsenergie. Z Naturforsch 4a:321–327

    Google Scholar 

  45. Frazier ML, Wright JR, Pokorny A, Almeida PF (2007) Investigation of domain formation in sphingomyelin/cholesterol/POPC mixtures by fluorescence resonance energy transfer and Monte Carlo simulations. Biophys J 92:2422–2433

    CAS  Google Scholar 

  46. Fung BK, Stryer L (1978) Surface density determination in membranes by fluorescence energy transfer. Biochemistry 17:5241–5248

    CAS  Google Scholar 

  47. Goswami D, Gowrishankar K, Bilgrami S, Ghosh S, Raghupathy R, Chadda R, Vishwakarma R, Rao M, Mayor S (2008) Nanoclusters of GPI-anchored proteins are formed by cortical actin-driven activity. Cell 135:1085–1097

    CAS  Google Scholar 

  48. Heberle FA, Wu J, Goh SL, Petruzielo RS, Feigenson GW (2010) Comparison of three ternary lipid bilayer mixtures: FRET and ESR reveal nanodomains. Biophys J 99:3309–3318

    CAS  Google Scholar 

  49. Hemminga MA, Sanders JC, Spruijt RB (1992) Spectroscopy of lipid-protein interactions: structural aspects of two different forms of the coat protein of bacteriophage M13 incorporated in model membranes. Prog Lipid Res 31:301–333

    CAS  Google Scholar 

  50. Hofman EG, Ruonala MO, Bader AN, van den Heuvel D, Voortman J, Roovers RC, Verkleij AJ, Gerritsen HC, van Bergen en Henegouwen PMP (2008) EGF induces coalescence of different lipid rafts. J Cell Sci 121:2519–2528

    CAS  Google Scholar 

  51. Holt A, de Almeida RFM, Nyholm TK, Loura LMS, Daily AE, Staffhorst RW, Rijkers DT, Koeppe RE 2nd, Prieto M, Killian JA (2008) Is there a preferential interaction between cholesterol and tryptophan residues in membrane proteins? Biochemistry 47:2638–2649

    CAS  Google Scholar 

  52. Goñi FM, Alonso A, Bagatolli LA, Brown RE, Marsh D, Prieto M, Thewalt JL (2008) Phase diagrams of lipid mixtures relevant to the study of membrane rafts. Biochim Biophys Acta 1781:665–684

    Google Scholar 

  53. Grecco HE, Roda-Navarro P, Verveer PJ (2009) Global analysis of time correlated single photon counting FRET-FLIM data. Opt Express 17:6493–6508

    CAS  Google Scholar 

  54. Guan L, Smirnova IN, Verner G, Nagamori S, Kaback HR (2006) Manipulating phospholipids for crystallization of a membrane transport protein. Proc Natl Acad Sci USA 103:1723–1726

    CAS  Google Scholar 

  55. Gutberlet T, Dietrich U, Bradaczek H, Pohlentz G, Leopold K, Fischer W (2000) Cardiolipin, alpha-D-glucopyranosyl, and L-lysylcardiolipin from gram-positive bacteria: FAB MS, monofilm and X-ray powder diffraction studies. Biochim Biophys Acta 1463:307–322

    CAS  Google Scholar 

  56. Herreros J, Ng T, Schiavo G (2001) Lipid rafts act as specialized domains for tetanus toxin binding and internalization into neurons. Mol Biol Cell 12:2947–2960

    CAS  Google Scholar 

  57. Hughes WE, Larijani B, Parker PJ (2002) Detecting protein-phospholipid interactions. J Biol Chem 277:22974–22979

    CAS  Google Scholar 

  58. Ipsen JH, Karlström G, Mouritsen OG, Wennerström H, Zuckermann MJ (1987) Phase equilibria in the phosphatidylcholine-cholesterol system. Biochim Biophys Acta 905:162–172

    CAS  Google Scholar 

  59. Jacobson K, Mouritsen OG, Anderson RG (2007) Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol 9:7–14

    CAS  Google Scholar 

  60. Jares-Erijman EA, Jovin TM (2006) Imaging molecular interactions in living cells by FRET microscopy. Curr Opin Chem Biol 10:409–416

    CAS  Google Scholar 

  61. Johansson J, Curstedt T (1997) Molecular structures and interactions of pulmonary surfactant components. Eur J Biochem 244:675–693

    CAS  Google Scholar 

  62. Johansson J, Curstedt T, Jornvall H (1991) Surfactant protein B: disulfide bridges, structural properties, and Kringle similarities. Biochemistry 30:6917–6921

    CAS  Google Scholar 

  63. Jørgensen K, Klinger A, Biltonen RL (2000) Nonequilibrium lipid domain growth in the gel-fluid two phase region of a DC16PC-DC22PC lipid mixture investigated by Monte-Carlo computer simulation, FT-IR and fluorescence spectroscopy. J Phys Chem 104:11763–11773

    Google Scholar 

  64. Karmakar S, Raghunathan VA, Mayor S (2005) Phase behaviour of dipalmitoylphospatidylcholine (DPPC)-cholesterol membranes. J Phys Condens Matter 17:S1177–S1182

    CAS  Google Scholar 

  65. Kenworthy AK, Edidin M (1998) Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 Å using imaging fluorescence resonance energy transfer. J Cell Biol 142:69–84

    CAS  Google Scholar 

  66. Kiskowski MA, Kenworthy AK (2007) In silico characterization of resonance energy transfer for disk-shaped membrane domains. Biophys J 92:3040–3051

    CAS  Google Scholar 

  67. Koehorst RB, Spruijt RB, Vergeldt FJ, Hemminga MA (2004) Lipid bilayer topology of the transmembrane alpha-helix of M13 Major coat protein and bilayer polarity profile by site-directed fluorescence spectroscopy. Biophys J 87:1445–1455

    CAS  Google Scholar 

  68. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (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

    CAS  Google Scholar 

  69. Lantzsch G, Binder H, Heerklotz H (1994) Surface area per molecule in lipid/C12En membranes as seen by fluorescence resonance energy transfer. J Fluoresc 4:339–343

    CAS  Google Scholar 

  70. Lakowicz JR (2006) Principles of fluorescence spectroscopy. Kluwer Academic/Plenum, New York

    Google Scholar 

  71. Lee AG (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612:1–40

    CAS  Google Scholar 

  72. Lentz BR, Barrow DA, Hoechli M (1980) Cholesterol-phosphatidylcholine interactions in multilamellar vesicles. Biochemistry 19:1943–1954

    CAS  Google Scholar 

  73. Li M, Reddy LG, Bennett R, Silva ND Jr, Jones LR, Thomas DD (1999) A fluorescence energy transfer method for analyzing protein oligomeric structure: application to phospholamban. Biophys J 76:2587–2599

    CAS  Google Scholar 

  74. Loura LMS, Prieto M (2000) Resonance energy transfer in heterogeneous planar and bilayer systems: theory and simulation. J Phys Chem B 104:6911–6919

    CAS  Google Scholar 

  75. Loura LM, Ramalho JP (2007) Location and dynamics of acyl chain NBD-labeled phosphati-dylcholine (NBD-PC) in DPPC bilayers. A molecular dynamics and time-resolved fluorescence anisotropy study. Biochim Biophys Acta 1768:467–478

    CAS  Google Scholar 

  76. Loura LMS, Fedorov A, Prieto M (1996) Resonance energy transfer in a model system of membranes: application to gel and liquid crystalline phases. Biophys J 71:1823–1836

    CAS  Google Scholar 

  77. Loura LMS, Fedorov A, Prieto M (2000) Membrane probe distribution heterogeneity: a resonance energy transfer study. J Phys Chem B 104:6920–6931

    CAS  Google Scholar 

  78. Loura LMS, Fedorov A, Prieto M (2000) Partition of membrane probes in a gel/fluid two-component lipid system: a fluorescence resonance energy transfer study. Biochim Biophys Acta 1467:101–112

    CAS  Google Scholar 

  79. Loura LMS, Fedorov A, Prieto M (2001) Fluid-fluid membrane microheterogeneity: a fluorescence resonance energy transfer study. Biophys J 80:776–788

    CAS  Google Scholar 

  80. Loura LMS, Coutinho A, Silva A, Fedorov A, Prieto M (2006) Structural effects of a basic peptide on the organization of dipalmitoylphosphatidylcholine/dipalmitoylphosphatidylserine membranes: a fluorescent resonance energy transfer study. J Phys Chem B 110:8130–8141

    CAS  Google Scholar 

  81. Loura LMS, Fernandes F, Prieto M (2010) Membrane microheterogeneity: Förster resonance energy transfer characterization of lateral membrane domains. Eur Biophys J 39:589–607

    CAS  Google Scholar 

  82. Loura LMS, Prieto M, Fernandes F (2010) Quantification of protein-lipid selectivity using FRET. Eur Biophys J 39:565–578

    CAS  Google Scholar 

  83. Loura LMS, Palace Carvalho AJ, Prates Ramalho JP (2010) Direct calculation of Förster orientation factor of membrane probes by molecular simulation. J Mol Struct THEOCHEM 946:107–112

    CAS  Google Scholar 

  84. Loura LMS, Prates Ramalho JP (2011) Recent developments in molecular dynamics simulations of fluorescent membrane probes. Molecules 16:5437–5452

    CAS  Google Scholar 

  85. Mabrey S, Sturtevant JM (1976) Investigation of phase transitions of lipids and lipid mixtures by sensitivity differential scanning calorimetry. Proc Natl Acad Sci U S A 73:3862–3866

    CAS  Google Scholar 

  86. Marsh D (1990) Handbook of Lipid Bilayers. CRC Press, Boca Raton

    Google Scholar 

  87. Marsh D (2010) Liquid-ordered phases induced by cholesterol: a compendium of binary phase diagrams. Biochim Biophys Acta 1798:688–699

    CAS  Google Scholar 

  88. Marsh D, Horváth LI (1998) Structure, dynamics and composition of the lipid-protein interface. Perspectives from spin-labelling. Biochim Biophys Acta 1376:267–296

    CAS  Google Scholar 

  89. Mateo CR, Acuna AU, Brochon J-C (1995) Liquid-crystalline phases of cholesterol lipid bilayers as revealed by the fluorescence of trans-parinaric acid. Biophys J 68:978–987

    CAS  Google Scholar 

  90. Mayor S, Rao M (2004) Rafts: scale-dependent, active lipid organization at the cell surface. Traffic 5:231–240

    CAS  Google Scholar 

  91. Mazères S, Schram V, Tocanne JF, Lopez A (1996) 7-nitrobenz-2-oxa-1,3-diazole-4-yl-labeled phospholipids in lipid membranes: differences in fluorescence behavior. Biophys J 71:327–335

    Google Scholar 

  92. McMullen TP, McElhaney RN (1995) New aspects of the interaction of cholesterol with dipalmitoylphosphatidylcholine bilayers as revealed by high-sensitivity differential scanning calorimetry. Biochim Biophys Acta 1234:90–98

    Google Scholar 

  93. Meyer BH, Segura J-M, Martinez KL, Hovius R, George N, Johnsson K, Vogel H (2006) FRET imaging reveals that functional neurokinin-1 receptors are monomeric and reside in membrane microdomains of live cells. Proc Natl Acad Sci USA 103:2138–2143

    CAS  Google Scholar 

  94. Morrow MR, Pérez-Gil J, Simatos G, Boland C, Stewart J, Absolom D, Sarin V, Keough KM (1993 Apr 27) Pulmonary surfactant-associated protein SP-B has little effect on acyl chains in dipalmitoylphosphatidylcholine dispersions. Biochemistry 32(16):4397–402

    CAS  Google Scholar 

  95. Mouritsen OG, Bloom M (1984) Mattress model of lipid-protein interactions in membranes. Biophys J 46:141–153

    CAS  Google Scholar 

  96. Needham D, Nunn RS (1990) Elastic deformation and failure of lipid bilayer membranes containing cholesterol. Biophys J 58:997–1009

    CAS  Google Scholar 

  97. Notter RH, Finkelstein JN (1984) Pulmonary surfactant: an interdisciplinary approach. J Appl Physiol 57:1613–1624

    CAS  Google Scholar 

  98. O’Keefe AH, East JM, Lee AG (2000) Selectivity in lipid binding to the bacterial outer membrane protein OmpF. Biophys J 79:2066–2074

    Google Scholar 

  99. Oosterlaken-Dijksterhuis MA, Haagsman HP, van Golde LM, Demel RA (1991) Characterization of lipid insertion into monomolecular layers mediated by lung surfactant proteins SP-B and SP-C. Biochemistry 30:10965–10971

    CAS  Google Scholar 

  100. Oosterlaken-Dijksterhuis MA, van Eijk M, van Golde LM, Haagsman HP (1992) Lipid mixing is mediated by the hydrophobic surfactant protein SP-B but not by SP-C. Biochim Biophys Acta 1110:45–50

    CAS  Google Scholar 

  101. Owen DM, Neil MAA, French PMW, Magee AI (2007) Optical techniques for imaging membrane lipid microdomains in living cells. Sem Cell Develop Biol 18:591–598

    CAS  Google Scholar 

  102. Owen DM, Gaus K, Magee AI, Cebecauer M (2010) Dynamic organization of lymphocyte plasma membrane: lessons from advanced imaging methods. Immunology 131:1–8

    CAS  Google Scholar 

  103. Padilla-Parra S, Auduge N, Coppey-Moisan M, Tramier M (2008) Quantitative FRET analysis by fast acquisition time domain FLIM at high spatial resolution in living cells. Biophys J 95:2976–2988

    CAS  Google Scholar 

  104. Peelen SJ, Sanders JC, Hemminga MA, Marsh D (1992) Stoichiometry, selectivity, and ex-change dynamics of lipid-protein interaction with bacteriophage M13 coat protein studied by spin label electron spin resonance. Effects of protein secondary structure. Biochemistry 31:2670–2677

    CAS  Google Scholar 

  105. Pérez-Gil J (2001) Lipid-protein interactions of hydrophobic proteins SP-B and SP-C in lung surfactant assembly and dynamics. Pediatr Pathol Mol Med 20:445–469

    Google Scholar 

  106. Pérez-Gil J, Keough KM (1998) Interfacial properties of surfactant proteins. Biochim Biophys Acta 1408:203–217

    Google Scholar 

  107. Pérez-Gil J, Casals C, Marsh D (1995) Interactions of hydrophobic lung surfactant proteins SP-B and SP-C with dipalmitoylphosphatidylcholine and dipalmitoylphosphatidylglycerol bilayers studied by electron spin resonance spectroscopy. Biochemistry 34:3964–3971

    Google Scholar 

  108. Picas L, Suárez-Germà C, Montero MT, Vázquez-Ibar JL, Hernández-Borrell J, Prieto M, Loura LM (2010) Lactose permease lipid selectivity using Förster resonance energy transfer. Bio-chim Biophys Acta 1798:1707–1713

    CAS  Google Scholar 

  109. Pluschke G, Hirota Y, Overath P (1978) Function of phospholipids in Escherichia coli. Charac-terization of a mutant deficient in cardiolipin synthesis. J Biol Chem 253:5048–5055

    CAS  Google Scholar 

  110. Poulain FR, Allen L, Williams MC, Hamilton RL, Hawgood S (1992) Effects of surfactant apolipoproteins on liposome structure: implications for tubular myelin formation. Am J Physiol 262:L730–L739

    CAS  Google Scholar 

  111. Powl AM, East JM, Lee AG (2003) Lipid-protein interactions studied by introduction of a tryp-tophan residue: the mechanosensitive channel MscL. Biochemistry 42:14306–14317

    CAS  Google Scholar 

  112. Rand RP, Parsegian VA (1989) Hydration forces between phospholipid-bilayers. Biochim Biophys Acta 988:351–376

    CAS  Google Scholar 

  113. Rao M, Mayor S (2005) Use of Förster’s resonance energy transfer microscopy to study lipid rafts. Biochim Biophys Acta 1746:221–233

    CAS  Google Scholar 

  114. Ryan MA, Qi X, Serrano AG, Ikegami M, Perez-Gil J, Johansson J, Weaver TE (2005) Mapping and analysis of the lytic and fusogenic domains of surfactant protein B. Biochemistry 44:861–872

    CAS  Google Scholar 

  115. Šachl R, Humpolíčková J, Stefl M, Johansson LB, Hof M (2011) Limitations of electronic energy transfer in the determination of lipid nanodomain sizes. Biophys J 101:L60–L62

    Google Scholar 

  116. Seifert M, Breitenstein D, Klenz U, Meyer MC, Galla HJ (2007) Solubility versus electrostatics: what determines lipid/protein interaction in lung surfactant. Biophys J 93:1192–1203

    CAS  Google Scholar 

  117. Sharma P, Varma R, Sarasij RC, Gousset K, Ira RC, Krishnamoorthy G, Rao M, Mayor S (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116:577–589

    CAS  Google Scholar 

  118. Shiffer K, Hawgood S, Haagsman HP, Benson B, Clements JA, Goerke J (1993) Lung surfactant proteins, SP-B and SP-C, alter the thermodynamic properties of phospholipid membranes: a differential calorimetry study. Biochemistry 32:590–597

    CAS  Google Scholar 

  119. Silva L, de Almeida RF, Fedorov A, Matos AP, Prieto M (2006) Ceramide-platform formation and -induced biophysical changes in a fluid phospholipid membrane. Mol Membr Biol 23:137–148

    CAS  Google Scholar 

  120. Silva LC, de Almeida RF, Castro BM, Fedorov A, Prieto M (2007) Ceramide-domain formation and collapse in lipid rafts: membrane reorganization by an apoptotic lipid. Biophys J 92:502–516

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  123. Soubias O, Teague WE Jr, Hines KG, Mitchell DC, Gawrisch K (2010) Contribution of membrane elastic energy to rhodopsin function. Biophys J 99:817–824

    CAS  Google Scholar 

  124. Spruijt RB, Wolfs CJ, Verver JW, Hemminga MA (1996) Accessibility and environment probing using cysteine residues introduced along the putative transmembrane domain of the major coat protein of bacteriophage M13. Biochemistry 35:10383–10391

    CAS  Google Scholar 

  125. Stöckl MT, Herrmann A (2010) Detection of lipid domains in model and cell membranes by fluorescence lifetime imaging microscopy. Biochim Biophys Acta 1798:1444–1456

    Google Scholar 

  126. Stopar D, Jansen KA, Páli T, Marsh D, Hemminga MA (1997) Membrane location of spin-labeled M13 major coat protein mutants determined by paramagnetic relaxation agents. Biochemistry 36:8261–8268

    CAS  Google Scholar 

  127. Stopar D, Spruijt RB, Wolfs CJ, Hemminga MA (2003) Protein-lipid interactions of bacterio-phage M13 major coat protein. Biochim Biophys Acta 1611:5–15

    CAS  Google Scholar 

  128. Stryer L (1978) Fluorescence energy transfer as a spectroscopic ruler. Annu Rev Biochem 47:819–846

    CAS  Google Scholar 

  129. Suárez-Germà C, Loura LMS, Prieto M, Domènech O, Montero MT, Rodríguez-Banqueri A, Vázquez-Ibar JL, Hernández-Borrell J (2012) Membrane protein-lipid selectivity: enhancing sensitivity for modeling FRET data. J Phys Chem B 116:2438–2445

    Google Scholar 

  130. Tahara Y, Murata M, Ohnishi S, Fujiyoshi Y, Kikuchi M, Yamamoto Y (1992) Functional signal peptide reduces bilayer thickness of phosphatidylcholine liposomes. Biochemistry 31:8747–8754

    CAS  Google Scholar 

  131. Towles KB, Dan N (2007) Determination of membrane domain size by fluorescence resonance energy transfer: effects of domain polydispersity and packing. Langmuir 23:4737–4739

    CAS  Google Scholar 

  132. Towles KB, Brown AC, Wrenn SP, Dan N (2007) Effect of membrane microheterogeneity and domain size on fluorescence resonance energy transfer. Biophys J 93:655–667

    CAS  Google Scholar 

  133. Vandenbussche G, Clercx A, Clercx M, Curstedt T, Johansson J, Jörnvall H, Ruysschaert JM (1992) Secondary structure and orientation of the surfactant protein SP-B in a lipid environment. A Fourier transform infrared spectroscopy study. Biochemistry 31:9169–9176

    CAS  Google Scholar 

  134. Van Der Meer B, Coker G 3rd, Chen S-YS (1994) Resonance energy transfer: theory and data. VCH Publishers, New York

    Google Scholar 

  135. Varma R, Mayor S (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798–801

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  137. Veatch SL, Keller SL (2005) Miscibility phase diagrams of giant vesicles containing sphingomyelin. Phys Rev Lett 94:148101–148104

    Google Scholar 

  138. Veatch SL, Keller SL, Gawrisch K (2007) Critical fluctuations in domain-forming lipid mixtures. Proc Natl Acad Sci USA 104:17650–17655

    CAS  Google Scholar 

  139. Veatch SL, Polozov IV, Gawrisch K, Keller SL (2004) Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys J 86:2910–2922

    CAS  Google Scholar 

  140. Vist MR, Davis JH (1990) Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2 H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 29:451–464

    CAS  Google Scholar 

  141. Von Arnim CAF, Kinoshita A, Peltan ID, Tangredi MM, Herl L, Lee BM, Spoelgen R, Hshieh TT, Ranganathan S, Battey FD, Liu CX, Bacskai BJ, Sever S, Irizarry MC, Strickland DK, Hyman BT (2005) The low density lipoprotein receptor-related protein (LRP) is a novel beta-secretase (BACE1) substrate. J Biol Chem 280:17777–17785

    Google Scholar 

  142. Wang X, Bogdanov M, Dowhan W (2002) Topology of polytopic membrane protein subdomains is dictated by membrane phospholipid composition. EMBO J 21:5673–5681

    CAS  Google Scholar 

  143. Wikström M, Kelly AA, Georgiev A, Eriksson HM, Klement MR, Bogdanov M, Dowhan W, Wieslander A (2009) Lipid-engineered Escherichia coli membranes reveal critical lipid headgroup size for protein function. J Biol Chem 284:954–965

    Google Scholar 

  144. Williamson IM, Alvis SJ, East JM, Lee AG (2002) Interactions of phospholipids with the potassium channel KcsA. Biophys J 83:2026–2038

    CAS  Google Scholar 

  145. Wolber PK, Hudson BS (1979) An analytical solution to the Förster energy transfer problem in two dimensions. Biophys J 28:197–210

    CAS  Google Scholar 

  146. Wu SH, McConnell HM (1975) Phase separations in phospholipid membranes. Biochemistry 14:847–854

    CAS  Google Scholar 

  147. Zaltash S, Palmblad M, Curstedt T, Johansson J, Persson B (2000) Pulmonary surfactant protein B: a structural model and a functional analogue. Biochim Biophys Acta 1466:179–186

    CAS  Google Scholar 

  148. Edidin M (2003) Lipids on the frontier: a century of cell-membrane bilayers. Nat Rev Mol Cell Biol 4:414–418

    CAS  Google Scholar 

  149. London E, Brown DA (2000) Insolubility of lipids in triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim Biophys Acta 1508:182–195

    CAS  Google Scholar 

  150. Sanders JC, Ottaviani MF, van Hoek A, Visser AJ, Hemminga MA (1992) A small protein in model membranes: a time-resolved fluorescence and ESR study on the interaction of M13 coat protein with lipid bilayers. Eur Biophys J 21:305–311

    CAS  Google Scholar 

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Acknowledgments

The authors acknowledge funding by FEDER (COMPETE program) and by FCT (Fundação para a Ciência e Tecnologia); projects references: PTDC/QUI-BIQ/119494/2010, PTDC/QUI-BIQ/112067/2009, PTDC/QUI-BIQ/099947/2008, and FCOMP-01-0124-FEDER-010787 (FCT PTDC/QUI-QUI/098198/2008).

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  1. Faculdade de Farmácia, Universidade de Coimbra, Pólo das Ciências da Saúde, Azinhaga de Santa Comba, 3000-548, Coimbra, Portugal

    Luís M. S. Loura

  2. Centro de Química de Coimbra, Universidade de Coimbra, Rua Larga, 3004-535, Coimbra, Portugal

    Luís M. S. Loura

  3. Centro de Química-Física Molecular and Institute of Nanosciences and Nanotechnology, Complexo I, IST, UTL, Av. Rovisco Pais, 1049-001, Lisboa, Portugal

    Manuel Prieto

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Correspondence to Luís M. S. Loura .

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  1. Faculté de Pharmacie, Laboratoire de Biophotonique, Université de Strasbourg, route du Rhin 74, Illkirch, 67401, France

    Yves Mély

  2. Faculté de Pharmacie, Laboratoire de Biophotonique et, Université de Strasbourg, route du Rhin 74, Illkirch, 67401, France

    Guy Duportail

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Loura, L.M.S., Prieto, M. (2012). Lateral Membrane Heterogeneity Probed by FRET Spectroscopy and Microscopy. In: Mély, Y., Duportail, G. (eds) Fluorescent Methods to Study Biological Membranes. Springer Series on Fluorescence, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/4243_2012_59

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