Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion

Nature Communications

Volumn 7, Issue , 2016, Pages

  Yang, Sung Tae ^a   Kiessling, Volker ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL; GLYCOPROTEIN GP 41; LIPID; STEROL; VIRUS FUSION PROTEIN; 1,2-OLEOYLPHOSPHATIDYLCHOLINE; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOSERINE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLETHANOLAMINE; CHOLESTEROL; LIPID BILAYER; PEPTIDE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLSERINE;

BIOENERGY; CHEMICAL BINDING; INHIBITOR; LIPID; PROTEIN; VITAMIN;

ARTICLE; ARTIFICIAL MEMBRANE; CONTROLLED STUDY; FLUORESCENCE; HUMAN IMMUNODEFICIENCY VIRUS; HYDROPHOBICITY; LINE TENSION; LIPID BILAYER; LIPID MEMBRANE; LIPID RAFT; MEMBRANE BIOLOGY; MEMBRANE FUSION; NONHUMAN; PHASE SEPARATION; PROTEIN DOMAIN; X RAY DIFFRACTION; CHEMISTRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE MICRODOMAIN; THERMODYNAMICS; VIRUS ENTRY;

CHOLESTEROL; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; LIPID BILAYERS; MEMBRANE FUSION; MEMBRANE MICRODOMAINS; PEPTIDES; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; PHOSPHATIDYLGLYCEROLS; PHOSPHATIDYLSERINES; THERMODYNAMICS; VIRUS INTERNALIZATION; VITAMIN E;

EID: 84964607696     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11401     Document Type: Article

References (55)

1. Doms, R. W., Moore, J. P. HIV-1 membrane fusion: targets of opportunity. J. Cell Biol. 151, F9-F14 (2000).
2. Wilen, C. B., Tilton, J. C., Doms, R. W. HIV: cell binding and entry. Cold Spring Harb. Perspect. Med. 2, a006866 (2012).
3. Harrison, S. C. Viral membrane fusion. Virology 479-480, 498-507 (2015).
4. Tamm, L. K., Han, X. Viral fusion peptides: a tool set to disrupt and connect biological membranes. Biosci. Rep. 20, 501-518 (2000).
5. Tamm, L. K., Lee, J., Liang, B. Capturing glimpses of an elusive HIV gp41 prehairpin fusion intermediate. Structure 22, 1225-1226 (2014).
6. Ono, A., Freed, E. O. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl Acad. Sci. USA 98, 13925-13930 (2001).
7. Brugger, B. et al. The HIV lipidome: a raft with an unusual composition. Proc. Natl Acad. Sci. USA 103, 2641-2646 (2006).
8. Waheed, A. A., Freed, E. O. Lipids and membrane microdomains in HIV-1 replication. Virus Res. 143, 162-176 (2009).
9. Simons, K., Ikonen, E. Functional rafts in cell membranes. Nature 387, 569-572 (1997).
10. van Meer, G., Voelker, D. R., Feigenson, G. W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124 (2008).
11. Lingwood, D., Kaiser, H. J., Levental, I., Simons, K. Lipid rafts as functional heterogeneity in cell membranes. Biochem. Soc. Trans. 37, 955-960 (2009).
12. Brown, D. A., London, E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14, 111-136 (1998).
13. Gaus, K., Chklovskaia, E., Fazekas de St Groth, B., Jessup, W., Harder, T. Condensation of the plasma membrane at the site of T lymphocyte activation. J. Cell Biol. 171, 121-131 (2005).
14. Biancotto, A. et al. HIV-1 induced activation of CD4\+ T cells creates new targets for HIV-1 infection in human lymphoid tissue ex vivo. Blood 111, 699-704 (2008).
15. Campbell, S. M., Crowe, S. M., Mak, J. Lipid rafts and HIV-1: from viral entry to assembly of progeny virions. J. Clin. Virol. 22, 217-227 (2001).
16. Popik, W., Alce, T. M., Au, W. C. Human immunodeficiency virus type 1 uses lipid raft-colocalized CD4 and chemokine receptors for productive entry into CD4(\+) T cells. J. Virol. 76, 4709-4722 (2002).
17. 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, 8237-8248 (2003).
18. 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. USA 98, 5619-5624 (2001).
19. Mukai, A. et al. Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells. Exp. Cell Res. 315, 3052-3063 (2009).
20. Sleight, S. B. et al. Isolation and proteomic analysis of mouse sperm detergentresistant membrane fractions: evidence for dissociation of lipid rafts during capacitation. Biol. Reprod. 73, 721-729 (2005).
21. Chernomordik, L. V., Kozlov, M. M. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15, 675-683 (2008).
22. 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, 424-431 (2015).
23. London, E. Membrane fusion: a new role for lipid domains? Nat. Chem. Biol. 11, 383-384 (2015).
24. Beach, R. S. et al. Specific nutrient abnormalities in asymptomatic HIV-1 infection. AIDS 6, 701-708 (1992).
25. Heredia, A. et al. In vitro suppression of latent HIV-1 activation by vitamin E: potential clinical implications. AIDS 19, 836-837 (2005).
26. Baumgart, T., Hess, S. T., Webb, W. W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821-824 (2003).
27. Feigenson, G. W. Phase behavior of lipid mixtures. Nat. Chem. Biol. 2, 560-563 (2006).
28. Eggeling, C. Super-resolution optical microscopy of lipid plasma membrane dynamics. Essays Biochem. 57, 69-80 (2015).
29. Jacobson, K., Mouritsen, O. G., Anderson, R. G. W. Lipid rafts: at a crossroad between cell biology and physics. Nat. Cell Biol. 9, 7-14 (2007).
30. Dietrich, C. et al. Lipid rafts reconstituted in model membranes. Biophys. J. 80, 1417-1428 (2001).
31. Heberle, F. A., Feigenson, G. W. Phase separation in lipid membranes. Cold Spring Harb. Perspect. Biol. 3, a004630 (2011).
32. Veatch, S. L., Keller, S. L. Seeing spots: complex phase behavior in simple membranes. Biochim. Biophys. Acta 1746, 172-185 (2005).
33. Moissoglu, K. et al. Regulation of Rac1 translocation and activation by membrane domains and their boundaries. J. Cell Sci. 127, 2565-2576 (2014).
34. Xu, X., London, E. The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39, 843-849 (2000).
35. Beattie, M. E., Veatch, S. L., Stottrup, B. L., Keller, S. L. Sterol structure determines miscibility versus melting transitions in lipid vesicles. Biophys. J. 89, 1760-1768 (2005).
36. Scherfeld, D., Kahya, N., Schwille, P. Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol. Biophys. J. 85, 3758-3768 (2003).
37. Nagle, J. F., Tristram-Nagle, S. Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159-195 (2000).
38. Pan, J., Mills, T. T., Tristram-Nagle, S., Nagle, J. F. Cholesterol perturbs lipid bilayers nonuniversally. Phys. Rev. Lett. 100, 198103 (2008).
39. Brewster, R., Safran, S. A. Line active hybrid lipids determine domain size in phase separation of saturated and unsaturated lipids. Biophys. J. 98, L21-L23 (2010).
40. Muddana, H. S., Chiang, H. H., Butler, P. J. Tuning membrane phase separation using nonlipid amphiphiles. Biophys. J. 102, 489-497 (2012).
41. Lipowsky, R. Domain-induced budding of fluid membranes. Biophys. J. 64, 1133-1138 (1993).
42. Garcia-Saez, A. J., Chiantia, S., Schwille, P. Effect of line tension on the lateral organization of lipid membranes. J. Biol. Chem. 282, 33537-33544 (2007).
43. Chernomordik, L. V., Kozlov, M. M. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72, 175-207 (2003).
44. Kuzmin, P. I., Akimov, S. A., Chizmadzhev, Y. A., Zimmerberg, J., Cohen, F. S. Line tension and interaction energies of membrane rafts calculated from lipid splay and tilt. Biophys. J. 88, 1120-1133 (2005).
45. Honerkamp-Smith, A. R. et al. Line tensions, correlation lengths, and critical exponents in lipid membranes near critical points. Biophys. J. 95, 236-246 (2008).
46. Markin, V. S., Kozlov, M. M., Borovjagin, V. L. On the theory of membrane fusion. The stalk mechanism. Gen. Physiol. Biophys. 3, 361-377 (1984).
47. Zimmerberg, J., Vogel, S. S., Chernomordik, L. V. Mechanisms of membrane fusion. Annu. Rev. Biophys. Biomol. Struct. 22, 433-466 (1993).
48. Melikyan, G. B. Common principles and intermediates of viral proteinmediated fusion: the HIV-1 paradigm. Retrovirology 5, 111 (2008).
49. Li, Y., Han, X., Tamm, L. K. Thermodynamics of fusion peptide-membrane interactions. Biochemistry 42, 7245-7251 (2003).
50. Tayebi, L. et al. Long-range interlayer alignment of intralayer domains in stacked lipid bilayers. Nat. Mater. 11, 1074-1080 (2012).
51. Wagner, M. L., Tamm, L. K. Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silanepolyethyleneglycol-lipid as a cushion and covalent linker. Biophys. J. 79, 1400-1414 (2000).
52. Struck, D. K., Hoekstra, D., Pagano, R. E. Use of resonance energy-transfer to monitor membrane-fusion. Biochemistry 20, 4093-4099 (1981).
53. Ellens, H., Bentz, J., Szoka, F. C. H\+-and Ca2\+-induced fusion and destabilization of liposomes. Biochemistry 24, 3099-3106 (1985).
54. 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, 3313-3326 (2006).
55. Domanska, M. K., Kiessling, V., Stein, A., Fasshauer, D., Tamm, L. K. Single vesicle millisecond fusion kinetics reveals number of SNARE complexes optimal for fast SNARE-mediated membrane fusion. J. Biol. Chem. 284, 32158-32166 (2009).