The transmembrane domain peptide of vesicular stomatitis virus promotes both intermediate and pore formation during peg-mediated vesicle fusion

Biophysical Journal

Volumn 107, Issue 6, 2014, Pages 1318-1326

  Sengupta, Tanusree ^a,b,d   Chakraborty, Hirak ^a,b,c   Lentz, Barry R ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^d INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALKANE; LIPID BILAYER; MACROGOL DERIVATIVE; N-HEXADECANE; PEPTIDE; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; BOVINE; CELL MEMBRANE; CHEMISTRY; DRUG EFFECTS; LIPID BILAYER; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; POROSITY; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS; VESICULOVIRUS; VIROLOGY; VIRUS ENTRY;

ALKANES; AMINO ACID SEQUENCE; ANIMALS; CATTLE; CELL MEMBRANE; LIPID BILAYERS; MOLECULAR SEQUENCE DATA; PEPTIDES; POLYETHYLENE GLYCOLS; POROSITY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; VESICULOVIRUS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84909607967     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.03.053     Document Type: Article

References (36)

1. Bullough, P. A., F. M. Hughson, ..., D. C. Wiley. 1994. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature. 371:37-43.
2. Yin, H. S., R. G. Paterson, ..., T. S. Jardetzky. 2005. Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc. Natl. Acad. Sci. USA. 102:9288-9293.
3. Harrison, S. C. 2008. Viral membrane fusion. Nat. Struct. Mol. Biol. 15:690-698.
4. White, J. M., S. E. Delos, ..., K. Schornberg. 2008. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 43:189-219.
5. Burgess, S. W., T. J. McIntosh, and B. R. Lentz. 1992. Modulation of poly(ethylene glycol)-induced fusion by membrane hydration: importance of interbilayer separation. Biochemistry. 31:2653-2661.
6. Kemble, G. W., T. Danieli, and J. M. White. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell. 76:383-391.
7. Nüssler, F., M. J. Clague, and A. Herrmann. 1997. Meta-stability of the hemifusion intermediate induced by glycosylphosphatidylinositol-anchored influenza hemagglutinin. Biophys. J. 73:2280-2291.
8. Odell, D., E. Wanas, ..., H. P. Ghosh. 1997. Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G. J. Virol. 71:7996-8000.
9. Miyauchi, K., R. Curran, ..., Z. Matsuda. 2006. Mutations of conserved glycine residues within the membrane-spanning domain of human immunodeficiency virus type 1 gp41 can inhibit membrane fusion and incorporation of Env onto virions. Jpn. J. Infect. Dis. 59:77-84.
10. Owens, R. J., C. Burke, and J. K. Rose. 1994. Mutations in the membrane-spanning domain of the human immunodeficiency virus envelope glycoprotein that affect fusion activity. J. Virol. 68:570-574.
11. Shang, L., L. Yue, and E. Hunter. 2008. Role of the membrane-spanning domain of human immunodeficiency virus type 1 envelope glycoprotein in cell-cell fusion and virus infection. J. Virol. 82:5417-5428.
12. Cleverley, D. Z., and J. Lenard. 1998. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA. 95:3425-3430.
13. Dennison, S. M., N. Greenfield, ..., B. R. Lentz. 2002. VSV transmembrane domain (TMD) peptide promotes PEG-mediated fusion of liposomes in a conformationally sensitive fashion. Biochemistry. 41:14925-14934.
14. Melikyan, G. B., R. M. Markosyan, ..., F. S. Cohen. 2000. A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol. Biol. Cell. 11:3765-3775.
15. Cohen, F. S., and G. B. Melikyan. 2004. The energetics of membrane fusion from binding, through hemifusion, pore formation, and pore enlargement. J. Membr. Biol. 199:1-14.
16. Chernomordik, L. V., and M. M. Kozlov. 2003. Protein-lipid interplay in fusion and fission of biological membranes. Annu. Rev. Biochem. 72:175-207.
17. Malinin, V. S., and B. R. Lentz. 2004. Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. Biophys. J. 86:2951-2964.
18. Chakraborty, H., T. Sengupta, and B. R. Lentz. 2014. pH alters PEG-mediated fusion of phosphatidylethanolamine-containing vesicles. Biophys. J.: In review.
19. Chakraborty, H., P. K. Tarafdar, ..., B. R. Lentz. 2012. Activation thermodynamics of poly(ethylene glycol)-mediated model membrane fusion support mechanistic models of stalk and pore formation. Biophys. J. 102:2751-2760.
20. Le Blanc, I., P. P. Luyet, ..., J. Gruenberg. 2005. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7:653-664.
21. Roche, S., F. A. Rey, ..., S. Bressanelli. 2007. Structure of the prefusion form of the vesicular stomatitis virus glycoprotein G. Science. 315:843-848.
22. Weinreb, G., and B. R. Lentz. 2007. Analysis of membrane fusion as a two-state sequential process: evaluation of the stalk model. Biophys. J. 92:4012-4029.
23. Lee, J., and B. R. Lentz. 1997. Evolution of lipidic structures during model membrane fusion and the relation of this process to cell membrane fusion. Biochemistry. 36:6251-6259.
24. Chen, P. S., T. Y. Toribara, and H. Warner. 1956. Microdetermination of phosphate. Anal. Chem. 28:1756-1758.
25. Schwenk, E., and N. T. Werthessen. 1952. Studies on the biosynthesis of cholesterol. III. Purification of C14-cholesterol from perfusions of livers and other organs. Arch. Biochem. Biophys. 40:334-341.
26. Lentz, B. R., G. F. McIntyre, ..., D. Massenburg. 1992. Bilayer curvature and certain amphipaths promote poly(ethylene glycol)-induced fusion of dipalmitoylphosphatidylcholine unilamellar vesicles. Biochemistry. 31:2643-2653.
27. Chakraborty, H., P. K. Tarafdar, ..., B. R. Lentz. 2013. Wild-type and mutant hemagglutinin fusion peptides alter bilayer structure as well as kinetics and activation thermodynamics of stalk and pore formation differently: mechanistic implications. Biophys. J. 105:2495-2506.
28. Kyoung, M., A. Srivastava, ..., A. T. Brunger. 2011. In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc. Natl. Acad. Sci. USA. 108:E304-E313.
29. Lee, J., and B. R. Lentz. 1997. Outer leaflet-packing defects promote poly(ethylene glycol)-mediated fusion of large unilamellar vesicles. Biochemistry. 36:421-431.
30. Ho, C., S. J. Slater, and C. D. Stubbs. 1995. Hydration and order in lipid bilayers. Biochemistry. 34:6188-6195.
31. Tarafdar, P. K., H. Chakraborty, ..., B. R. Lentz. 2012. Phosphatidylserine inhibits and calcium promotes model membrane fusion. Biophys. J. 103:1880-1889.
32. Haque, M. E., H. Chakraborty, ..., B. R. Lentz. 2011. Hemagglutinin fusion peptide mutants in model membranes: structural properties, membrane physical properties, and PEG-mediated fusion. Biophys. J. 101:1095-1104.
33. Siegel, D. P. 1999. The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion. Biophys. J. 76:291-313.
34. Smirnova, Y. G., S. J. Marrink, ..., V. Knecht. 2010. Solvent-exposed tails as prestalk transition states for membrane fusion at low hydration. J. Am. Chem. Soc. 132:6710-6718.
35. Kasson, P. M., E. Lindahl, and V. S. Pande. 2010. Atomic-resolution simulations predict a transition state for vesicle fusion defined by contact of a few lipid tails. PLOS Comput. Biol. 6:e1000829.
36. Kozlov, M. M., S. Leikin, and R. P. Rand. 1994. Bending, hydration and interstitial energies quantitatively account for the hexagonal-lamellar-hexagonal reentrant phase transition in dioleoylphosphatidylethanolamine. Biophys. J. 67:1603-1611.