The role of cholesterol in membrane fusion

Chemistry and Physics of Lipids

Volumn 199, Issue , 2016, Pages 136-143

  Yang, Sung Tae ^a   Kreutzberger, Alex J B ^a   Lee, Jinwoo ^a   Kiessling, Volker ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cholesterol; Exocytosis; Fusion peptide; Fusion protein; Membrane fusion; SNARE; Viral envelope protein; Virus entry

Indexed keywords

CHOLESTEROL; GLYCOPROTEIN; MEMBRANE FUSION PROTEIN; LIPID BILAYER; SNARE PROTEIN;

ARTICLE; HUMAN; INTRACELLULAR SPACE; LIPID BILAYER; MEMBRANE FUSION; MOLECULAR MECHANICS; PHASE SEPARATION; PRIORITY JOURNAL; VIRUS ENTRY; VIRUS ENVELOPE; ANIMAL; METABOLISM;

ANIMALS; CHOLESTEROL; HUMANS; LIPID BILAYERS; MEMBRANE FUSION; SNARE PROTEINS; VIRUS INTERNALIZATION;

EID: 84971631289     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2016.05.003     Document Type: Article

References (115)

1. Aeffner, S., Reusch, T., Weinhausen, B., Salditt, T., Energetics of stalk intermediates in membrane fusion are controlled by lipid composition. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), E1609–1618.
2. Bacia, K., Schuette, C.G., Kahya, N., Jahn, R., Schwille, P., SNAREs prefer liquid-disordered over raft (liquid-ordered) domains when reconstituted into giant unilamellar vesicles. J. Biol. Chem. 279 (2004), 37951–37955.
3. Baier, C.J., Fantini, J., Barrantes, F.J., Disclosure of cholesterol recognition motifs in transmembrane domains of the human nicotinic acetylcholine receptor. Sci. Rep., 1, 2011, 69.
4. Barrett, P.J., Song, Y., Van Horn, W.D., Hustedt, E.J., Schafer, J.M., Hadziselimovic, A., Beel, A.J., Sanders, C.R., The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336 (2012), 1168–1171.
5. Baumgart, T., Hess, S.T., Webb, W.W., Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425 (2003), 821–824.
6. Bennett, M.P., Mitchell, D.C., Regulation of membrane proteins by dietary lipids: effects of cholesterol and docosahexaenoic acid acyl chain-containing phospholipids on rhodopsin stability and function. Biophys. J. 95 (2008), 1206–1216.
7. Biswas, S., Yin, S.R., Blank, P.S., Zimmerberg, J., Cholesterol promotes hemifusion and pore widening in membrane fusion induced by influenza hemagglutinin. J. Gen. Physiol. 131 (2008), 503–513.
8. Blumenthal, R., Clague, M.J., Durell, S.R., Epand, R.M., Membrane fusion. Chem. Rev. 103 (2003), 53–69.
9. Brown, D.A., London, E., Functions of lipid rafts in biological membranes. Annu. Rev. Cell. Dev. Biol. 14 (1998), 111–136.
10. Chamberlain, L.H., Burgoyne, R.D., Gould, G.W., SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 5619–5624.
11. Chen, Z., Rand, R.P., The influence of cholesterol on phospholipid membrane curvature and bending elasticity. Biophys. J. 73 (1997), 267–276.
12. Chen, S.S., Yang, P., Ke, P.Y., Li, H.F., Chan, W.E., Chang, D.K., Chuang, C.K., Tsai, Y., Huang, S.C., Identification of the LWYIK motif located in the human immunodeficiency virus type 1 transmembrane gp41 protein as a distinct determinant for viral infection. J. Virol. 83 (2009), 870–883.
13. Chernomordik, L.V., Kozlov, M.M., Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72 (2003), 175–207.
14. Chernomordik, L.V., Kozlov, M.M., Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15 (2008), 675–683.
15. Chiantia, S., Schwille, P., Klymchenko, A.S., London, E., Asymmetric GUVs prepared by MbetaCD-mediated lipid exchange: an FCS study. Biophys. J. 100 (2011), L1–3.
16. Churchward, M.A., Rogasevskaia, T., Hofgen, J., Bau, J., Coorssen, J.R., Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion. J. Cell Sci. 118 (2005), 4833–4848.
17. Churchward, M.A., Rogasevskaia, T., Brandman, D.M., Khosravani, H., Nava, P., Atkinson, J.K., Coorssen, J.R., Specific lipids supply critical negative spontaneous curvature–an essential component of native Ca2+-triggered membrane fusion. Biophys. J. 94 (2008), 3976–3986.
18. Collins, M.D., Keller, S.L., Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 124–128.
19. Crane, J.M., Tamm, L.K., Role of cholesterol in the formation and nature of lipid rafts in planar and spherical model membranes. Biophys. J. 86 (2004), 2965–2979.
20. Crane, J.M., Tamm, L.K., Fluorescence microscopy to study domains in supported lipid bilayers. Methods Mol. Biol. 400 (2007), 481–488.
21. Crane, J.M., Kiessling, V., Tamm, L.K., Measuring lipid asymmetry in planar supported bilayers by fluorescence interference contrast microscopy. Langmuir 21 (2005), 1377–1388.
22. Destainville, N., Schmidt, T.H., Lang, T., Where biology meets physics—a converging view on membrane microdomain dynamics. Curr. Top. Membr. 77 (2016), 27–65.
23. de Vries, M., Herrmann, A., Veit, M., A cholesterol consensus motif is required for efficient intracellular transport and raft association of a group 2HA from influenza virus. Biochem. J. 465 (2015), 305–314.
24. Domanska, M.K., Wrona, D., Kasson, P.M., Multiphasic effects of cholesterol on influenza fusion kinetics reflect multiple mechanistic roles. Biophys. J. 105 (2013), 1383–1387.
25. Domanska, M.K., Dunning, R.A., Dryden, K.A., Zawada, K.E., Yeager, M., Kasson, P.M., Hemagglutinin spatial distribution shifts in response to cholesterol in the influenza viral envelope. Biophys. J. 109 (2015), 1917–1924.
26. Ekanayake, E.V., Fu, R., Cross, T.A., Structural influences: cholesterol, drug, and proton binding to full-length influenza a M2 protein. Biophys. J. 110 (2016), 1391–1399.
27. Enrich, C., Rentero, C., Hierro, A., Grewal, T., Role of cholesterol in SNARE-mediated trafficking on intracellular membranes. J. Cell Sci. 128 (2015), 1071–1081.
28. Epand, R.M., Fusion peptides and the mechanism of viral fusion. Biochim. Biophys. Acta 1614 (2003), 116–121.
29. Epand, R.M., Proteins and cholesterol-rich domains. Biochim. Biophys. Acta 1778 (2008), 1576–1582.
30. Evans, E., Rawicz, W., Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64 (1990), 2094–2097.
31. Falck, E., Patra, M., Karttunen, M., Hyvonen, M.T., Vattulainen, I., Impact of cholesterol on voids in phospholipid membranes. J. Chem. Phys. 121 (2004), 12676–12689.
32. Fantini, J., Barrantes, F.J., How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front. Physiol., 4, 2013, 31.
33. Fantini, J., Yahi, N., Molecular basis for the glycosphingolipid-binding specificity of alpha-synuclein: key role of tyrosine 39 in membrane insertion. J. Mol. Biol. 408 (2011), 654–669.
34. Feigenson, G.W., Phase behavior of lipid mixtures. Nat. Chem. Biol. 2 (2006), 560–563.
35. Finkenstaedt-Quinn, S.A., Gruba, S.M., Haynes, C.L., Variations in fusion pore formation in cholesterol-treated platelets. Biophys. J. 110 (2016), 922–929.
36. Freed, E.O., HIV-1 assembly, release and maturation. Nat. Rev. Microbiol. 13 (2015), 484–496.
37. Garcia-Saez, A.J., Chiantia, S., Schwille, P., Effect of line tension on the lateral organization of lipid membranes. J. Biol. Chem. 282 (2007), 33537–33544.
38. Garg, S., Ruhe, J., Ludtke, K., Jordan, R., Naumann, C.A., Domain registration in raft-mimicking lipid mixtures studied using polymer-tethered lipid bilayers. Biophys. J. 92 (2007), 1263–1270.
39. Ge, S., White, J.G., Haynes, C.L., Critical role of membrane cholesterol in exocytosis revealed by single platelet study. ACS Chem. Biol. 5 (2010), 819–828.
40. Gil, C., Soler-Jover, A., Blasi, J., Aguilera, J., Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes. Biochem. Biophys. Res. Commun. 329 (2005), 117–124.
41. Gimpl, G., Fahrenholz, F., Cholesterol as stabilizer of the oxytocin receptor. Biochim. Biophys. Acta 1564 (2002), 384–392.
42. Gimpl, G., Burger, K., Fahrenholz, F., Cholesterol as modulator of receptor function. Biochemistry 36 (1997), 10959–10974.
43. Graham, D.R., Chertova, E., Hilburn, J.M., Arthur, L.O., Hildreth, J.E., Cholesterol depletion of human immunodeficiency virus type 1 and simian immunodeficiency virus with beta-cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J. Virol. 77 (2003), 8237–8248.
44. Gruba, S.M., Koseoglu, S., Meyer, A.F., Meyer, B.M., Maurer-Jones, M.A., Haynes, C.L., Platelet membrane variations and their effects on delta-granule secretion kinetics and aggregation spreading among different species. Biochim. Biophys. Acta 1848 (2015), 1609–1618.
45. Hanson, M.A., Cherezov, V., Griffith, M.T., Roth, C.B., Jaakola, V.P., Chien, E.Y., Velasquez, J., Kuhn, P., Stevens, R.C., A specific cholesterol binding site is established by the 2.8 A structure of the human beta2-adrenergic receptor. Structure 16 (2008), 897–905.
46. Hao, M., Bogan, J.S., Cholesterol regulates glucose-stimulated insulin secretion through phosphatidylinositol 4,5-bisphosphate. J. Biol. Chem. 284 (2009), 29489–29498.
47. Harrison, S.C., Viral membrane fusion. Nat. Struct. Mol. Biol. 15 (2008), 690–698.
48. Heftberger, P., Kollmitzer, B., Rieder, A.A., Amenitsch, H., Pabst, G., In situ determination of structure and fluctuations of coexisting fluid membrane domains. Biophys. J. 108 (2015), 854–862.
49. Ipsen, J.H., Mouritsen, O.G., Zuckermann, M.J., Theory of thermal anomalies in the specific-heat of lipid bilayers containing cholesterol. Biophys. J. 56 (1989), 661–667.
50. Jacobson, K., Mouritsen, O.G., Anderson, R.G.W., Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9 (2007), 7–14.
51. Jafurulla, M., Tiwari, S., Chattopadhyay, A., Identification of cholesterol recognition amino acid consensus (CRAC) motif in G-protein coupled receptors. Biochem. Biophys. Res. Commun. 404 (2011), 569–573.
52. Jamin, N., Neumann, J.M., Ostuni, M.A., Vu, T.K., Yao, Z.X., Murail, S., Robert, J.C., Giatzakis, C., Papadopoulos, V., Lacapere, J.J., Characterization of the cholesterol recognition amino acid consensus sequence of the peripheral-type benzodiazepine receptor. Mol. Endocrinol. 19 (2005), 588–594.
53. Julicher, F., Lipowsky, R., Domain-induced budding of vesicles. Phys. Rev. Lett. 70 (1993), 2964–2967.
54. Kahya, N., Scherfeld, D., Bacia, K., Poolman, B., Schwille, P., Probing lipid mobility of raft-exhibiting model membranes by fluorescence correlation spectroscopy. J. Biol. Chem. 278 (2003), 28109–28115.
55. Kiessling, V., Crane, J.M., Tamm, L.K., Transbilayer effects of raft-like lipid domains in asymmetric planar bilayers measured by single molecule tracking. Biophys. J. 91 (2006), 3313–3326.
56. Kiessling, V., Wan, C., Tamm, L.K., Domain coupling in asymmetric lipid bilayers. Biochim. Biophys. Acta 1788 (2009), 64–71.
57. Kiessling, V., Yang, S.T., Tamm, L.K., Supported lipid bilayers as models for studying membrane domains. Curr. Top. Membr. 75 (2015), 1–23.
58. Knowles, M.K., Barg, S., Wan, L., Midorikawa, M., Chen, X., Almers, W., Single secretory granules of live cells recruit syntaxin-1 and synaptosomal associated protein 25 (SNAP-25) in large copy numbers. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 20810–20815.
59. Koseoglu, S., Love, S.A., Haynes, C.L., Cholesterol effects on vesicle pools in chromaffin cells revealed by carbon-fiber microelectrode amperometry. Anal. Bioanal. Chem. 400 (2011), 2963–2971.
60. Kreutzberger, A.J., Kiessling, V., Tamm, L.K., High cholesterol obviates a prolonged hemifusion intermediate in fast SNARE-mediated membrane fusion. Biophys. J. 109 (2015), 319–329.
61. Kruit, J.K., Wijesekara, N., Fox, J.E., Dai, X.Q., Brunham, L.R., Searle, G.J., Morgan, G.P., Costin, A.J., Tang, R., Bhattacharjee, A., Johnson, J.D., Light, P.E., Marsh, B.J., Macdonald, P.E., Verchere, C.B., Hayden, M.R., Islet cholesterol accumulation due to loss of ABCA1 leads to impaired exocytosis of insulin granules. Diabetes 60 (2011), 3186–3196.
62. Lai, A.L., Li, Y.L., Tamm, L.K., Interplay of proteins and lipids in virus entry by membrane fusion. Tamm, L.K., (eds.) Protein-Lipid Interactions, 2005, Wiley-VCH, 279–303.
63. Lai, A.L., Moorthy, A.E., Li, Y., Tamm, L.K., Fusion activity of HIV gp41 fusion domain is related to its secondary structure and depth of membrane insertion in a cholesterol-dependent fashion. J. Mol. Biol. 418 (2012), 3–15.
64. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., Jahn, R., SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20 (2001), 2202–2213.
65. Lang, T., SNARE proteins and ‘membrane rafts’. J. Physiol. 585 (2007), 693–698.
66. Lee, D.E., Lew, M.G., Woodbury, D.J., Vesicle fusion to planar membranes is enhanced by cholesterol and low temperature. Chem. Phys. Lipids 166 (2013), 45–54.
67. Li, H., Yao, Z., Degenhardt, B., Teper, G., Papadopoulos, V., Cholesterol binding at the cholesterol recognition/interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 1267–1272.
68. Liang, B., Dawidowski, D., Ellena, J.F., Tamm, L.K., Cafiso, D.S., The SNARE motif of synaptobrevin exhibits an aqueous-interfacial partitioning that is modulated by membrane curvature. Biochemistry 53 (2014), 1485–1494.
69. Liao, Z., Cimakasky, L.M., Hampton, R., Nguyen, D.H., Hildreth, J.E., Lipid rafts and HIV pathogenesis: host membrane cholesterol is required for infection by HIV type 1. AIDS Res. Hum. Retroviruses 17 (2001), 1009–1019.
70. Lin, Q., London, E., Preparation of artificial plasma membrane mimicking vesicles with lipid asymmetry. PLoS One, 9, 2014, e87903.
71. Linetti, A., Fratangeli, A., Taverna, E., Valnegri, P., Francolini, M., Cappello, V., Matteoli, M., Passafaro, M., Rosa, P., Cholesterol reduction impairs exocytosis of synaptic vesicles. J. Cell Sci. 123 (2010), 595–605.
72. Lingwood, D., Simons, K., Lipid rafts as a membrane-organizing principle. Science 327 (2010), 46–50.
73. Manes, S., del Real, G., Martinez, A.C., Pathogens: raft hijackers. Nat. Rev. Immunol. 3 (2003), 557–568.
74. Milovanovic, D., Honigmann, A., Koike, S., Gottfert, F., Pahler, G., Junius, M., Mullar, S., Diederichsen, U., Janshoff, A., Grubmuller, H., Risselada, H.J., Eggeling, C., Hell, S.W., van den Bogaart, G., Jahn, R., Hydrophobic mismatch sorts SNARE proteins into distinct membrane domains. Nat. Commun., 6, 2015, 5984.
75. Murray, D.H., Tamm, L.K., Clustering of syntaxin-1A in model membranes is modulated by phosphatidylinositol 4,5-bisphosphate and cholesterol. Biochemistry 48 (2009), 4617–4625.
76. Murray, D.H., Tamm, L.K., Molecular mechanism of cholesterol- and polyphosphoinositide-mediated syntaxin clustering. Biochemistry 50 (2011), 9014–9022.
77. Niu, S.L., Mitchell, D.C., Litman, B.J., Manipulation of cholesterol levels in rod disk membranes by methyl-beta-cyclodextrin: effects on receptor activation. J. Biol. Chem. 277 (2002), 20139–20145.
78. Oddi, S., Dainese, E., Fezza, F., Lanuti, M., Barcaroli, D., De Laurenzi, V., Centonze, D., Maccarrone, M., Functional characterization of putative cholesterol binding sequence (CRAC) in human type-1 cannabinoid receptor. J. Neurochem. 116 (2011), 858–865.
79. Paila, Y.D., Chattopadhyay, A., Membrane cholesterol in the function and organization of G-protein coupled receptors. Sub Cell. Biochem. 51 (2010), 439–466.
80. Pan, J., Mills, T.T., Tristram-Nagle, S., Nagle, J.F., Cholesterol perturbs lipid bilayers nonuniversally. Phys. Rev. Lett., 100, 2008, 198103.
81. Pan, J., Tristram-Nagle, S., Nagle, J.F., Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation. Phys. Rev. E Stat. Nonlin Soft Matter Phys., 80, 2009, 021931.
82. Rossman, J.S., Jing, X., Leser, G.P., Lamb, R.A., Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142 (2010), 902–913.
83. Rothman, J.E., The principle of membrane fusion in the cell (Nobel lecture). Angew. Chem. Int. Ed. Engl. 53 (2014), 12676–12694.
84. Rubenstein, J.L., Smith, B.A., McConnell, H.M., Lateral diffusion in binary mixtures of cholesterol and phosphatidylcholines. Proc. Natl. Acad. Sci. U. S. A. 76 (1979), 15–18.
85. Sankaram, M.B., Thompson, T.E., Modulation of phospholipid acyl chain order by cholesterol. A solid-state 2H nuclear magnetic resonance study. Biochemistry 29 (1990), 10676–10684.
86. Saxena, R., Chattopadhyay, A., Membrane cholesterol stabilizes the human serotonin(1A) receptor. Biochim. Biophys. Acta 1818 (2012), 2936–2942.
87. Scheiffele, P., Roth, M.G., Simons, K., Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16 (1997), 5501–5508.
88. Scheiffele, P., Rietveld, A., Wilk, T., Simons, K., Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274 (1999), 2038–2044.
89. Sezgin, E., Levental, I., Grzybek, M., Schwarzmann, G., Mueller, V., Honigmann, A., Belov, V.N., Eggeling, C., Coskun, U., Simons, K., Schwille, P., Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim. Biophys. Acta 1818 (2012), 1777–1784.
90. Shaikh, S.R., Edidin, M.A., Membranes are not just rafts. Chem. Phys. Lipids 144 (2006), 1–3.
91. Sieber, J.J., Willig, K.I., Kutzner, C., Gerding-Reimers, C., Harke, B., Donnert, G., Rammner, B., Eggeling, C., Hell, S.W., Grubmuller, H., Lang, T., Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317 (2007), 1072–1076.
92. Simons, K., Ikonen, E., Functional rafts in cell membranes. Nature 387 (1997), 569–572.
93. Smondyrev, A.M., Berkowitz, M.L., Structure of dipalmitoylphosphatidylcholine/cholesterol bilayer at low and high cholesterol concentrations: molecular dynamics simulation. Biophys. J. 77 (1999), 2075–2089.
94. Soubias, O., Gawrisch, K., The role of the lipid matrix for structure and function of the GPCR rhodopsin. Biochim. Biophys. Acta 1818 (2012), 234–240.
95. Stratton, B.S., Warner, J.M., Wu, Z., Nikolaus, J., Wei, G., Wagnon, E., Baddeley, D., Karatekin, E., O'Shaughnessy, B., Cholesterol increases the openness of SNARE-mediated flickering fusion pores. Biophys. J. 110 (2016), 1538–1550.
96. Sturek, J.M., Castle, J.D., Trace, A.P., Page, L.C., Castle, A.M., Evans-Molina, C., Parks, J.S., Mirmira, R.G., Hedrick, C.C., An intracellular role for ABCG1-mediated cholesterol transport in the regulated secretory pathway of mouse pancreatic beta cells. J. Clin. Invest. 120 (2010), 2575–2589.
97. Sun, X., Whittaker, G.R., Role for influenza virus envelope cholesterol in virus entry and infection. J. Virol. 77 (2003), 12543–12551.
98. Tamm, L.K., Han, X., Li, Y., Lai, A.L., Structure and function of membrane fusion peptides. Biopolymers 66 (2002), 249–260.
99. Tamm, L.K., Crane, J., Kiessling, V., Membrane fusion: a structural perspective on the interplay of lipids and proteins. Curr. Opin. Struct. Biol. 13 (2003), 453–466.
100. Tamm, L.K., Lee, J., Liang, B., Capturing glimpses of an elusive HIV gp41 prehairpin fusion intermediate. Structure 22 (2014), 1225–1226.
101. Tong, J., Borbat, P.P., Freed, J.H., Shin, Y.K., A scissors mechanism for stimulation of SNARE-mediated lipid mixing by cholesterol. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 5141–5146.
102. van den Bogaart, G., Jahn, R., Counting the SNAREs needed for membrane fusion. J. Mol. Cell. Biol. 3 (2011), 204–205.
103. van Meer, G., Voelker, D.R., Feigenson, G.W., Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9 (2008), 112–124.
104. Veatch, S.L., Keller, S.L., Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta 1746 (2005), 172–185.
105. Vishwanathan, S.A., Thomas, A., Brasseur, R., Epand, R.F., Hunter, E., Epand, R.M., Hydrophobic substitutions in the first residue of the CRAC segment of the gp41 protein of HIV. Biochemistry 47 (2008), 124–130.
106. Waheed, A.A., Freed, E.O., Lipids and membrane microdomains in HIV-1 replication. Virus Res. 143 (2009), 162–176.
107. Wan, C., Kiessling, V., Tamm, L.K., Coupling of cholesterol-rich lipid phases in asymmetric bilayers. Biochemistry 47 (2008), 2190–2198.
108. Wan, C., Kiessling, V., Cafiso, D.S., Tamm, L.K., Partitioning of synaptotagmin I C2 domains between liquid-ordered and liquid-disordered inner leaflet lipid phases. Biochemistry 50 (2011), 2478–2485.
109. Wang, N., Kwan, C., Gong, X., de Chaves, E.P., Tse, A., Tse, F.W., Influence of cholesterol on catecholamine release from the fusion pore of large dense core chromaffin granules. J. Neurosci. 30 (2010), 3904–3911.
110. Wasser, C.R., Ertunc, M., Liu, X., Kavalali, E.T., Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J. Physiol. 579 (2007), 413–429.
111. Yang, L., Huang, H.W., Observation of a membrane fusion intermediate structure. Science 297 (2002), 1877–1879.
112. Yang, S.-T., Kiessling, V., Simmons, J.A., White, J.M., Tamm, L.K., HIV gp41-mediated membrane fusion occurs at edges of cholesterol-rich lipid domains. Nat. Chem. Biol. 11 (2015), 424–431.
113. Yang, S.-T., Kiessling, V., Tamm, L.K., Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion. Nat. Commun., 7, 2016, 11401.
114. Zhang, J., Xue, R., Ong, W.Y., Chen, P., Roles of cholesterol in vesicle fusion and motion. Biophys. J. 97 (2009), 1371–1380.
115. Zimmerberg, J., Vogel, S.S., Chernomordik, L.V., Mechanisms of membrane fusion. Annu. Rev. Biophys. Biomol. Struct. 22 (1993), 433–466.