A novel membrane fusion protein family in Flaviviridae?

Trends in Microbiology

Volumn 22, Issue 4, 2014, Pages 176-182

  Li, Yue ^a   Modis, Yorgo ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Bovine viral diarrhea virus; Envelope glycoprotein; Hepacivirus; Horizontal gene transfer; Host virus coevolution; Paleovirology

Indexed keywords

GLYCOPROTEIN E2; MEMBRANE FUSION PROTEIN; VIRUS FUSION PROTEIN;

BOVINE VIRAL DIARRHEA VIRUS 2; CATALYSIS; CONFORMATIONAL TRANSITION; FLAVIVIRUS; HEPATITIS C VIRUS; MEMBRANE FUSION; NONHUMAN; PESTIVIRUS; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VIRUS ENTRY;

BOVINE VIRAL DIARRHEA VIRUS 1; FLAVIVIRIDAE; HEPACIVIRUS; HEPATITIS C VIRUS; PESTIVIRUS;

BOVINE VIRAL DIARRHEA VIRUS; ENVELOPE GLYCOPROTEIN; HEPACIVIRUS; HORIZONTAL GENE TRANSFER; HOST-VIRUS COEVOLUTION; PALEOVIROLOGY;

HEPACIVIRUS; MEMBRANE FUSION; MODELS, MOLECULAR; PESTIVIRUS; PROTEIN CONFORMATION; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

EID: 84897378275     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.01.008     Document Type: Review

References (53)

1. Skehel J.J., Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 2000, 69:531-569.
2. Lamb R.A., Jardetzky T.S. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 2007, 17:427-436.
3. Chan D.C., et al. Core structure of gp41 from the HIV envelope glycoprotein. Cell 1997, 89:263-273.
4. Weissenhorn W., et al. Atomic structure of the ectodomain from HIV-1 gp41. Nature 1997, 387:426-430.
5. Weissenhorn W., et al. Crystal structure of the Ebola virus membrane fusion subunit, GP2, from the envelope glycoprotein ectodomain. Mol. Cell 1998, 2:605-616.
6. Xu Y., et al. Crystal structure of severe acute respiratory syndrome coronavirus spike protein fusion core. J. Biol. Chem. 2004, 279:49414-49419.
7. Xu Y., et al. Structural basis for coronavirus-mediated membrane fusion. Crystal structure of mouse hepatitis virus spike protein fusion core. J. Biol. Chem. 2004, 279:30514-30522.
8. Schibli D.J., Weissenhorn W. Class I and class II viral fusion protein structures reveal similar principles in membrane fusion. Mol. Membr. Biol. 2004, 21:361-371.
9. Rey F.A., et al. The envelope glycoprotein from tick-borne encephalitis virus at 2A resolution. Nature 1995, 375:291-298.
10. Lescar J., et al. The fusion glycoprotein shell of Semliki Forest virus: an icosahedral assembly primed for fusogenic activation at endosomal pH. Cell 2001, 105:137-148.
11. DuBois R.M., et al. Functional and evolutionary insight from the crystal structure of rubella virus protein E1. Nature 2013, 493:552-556.
12. Dessau M., Modis Y. Crystal structure of glycoprotein C from Rift Valley fever virus. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1696-1701.
13. Modis Y. Relating structure to evolution in class II viral membrane fusion proteins. Curr. Opin. Virol. 2014, 5:34-41.
14. Heldwein E.E., et al. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 2006, 313:217-220.
15. Roche S., et al. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 2006, 313:187-191.
16. Kadlec J., et al. The postfusion structure of baculovirus gp64 supports a unified view of viral fusion machines. Nat. Struct. Mol. Biol. 2008, 15:1024-1030.
17. Boutilier J., Duncan R. The reovirus fusion-associated small transmembrane (FAST) proteins: virus-encoded cellular fusogens. Curr. Top. Membr. 2011, 68:107-140.
18. Krey T., et al. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 2010, 6:e1000762.
19. Garry R.F., Dash S. Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 2003, 307:255-265.
20. Li Y., et al. Crystal structure of glycoprotein E2 from bovine viral diarrhea virus. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:6805-6810.
21. El Omari K., et al. Structure of a pestivirus envelope glycoprotein E2 clarifies its role in cell entry. Cell Rep. 2013, 3:30-35.
22. Kong L., et al. Hepatitis C virus E2 envelope glycoprotein core structure. Science 2013, 342:1090-1094.
23. Kielian M., Rey F.A. Virus membrane-fusion proteins: more than one way to make a hairpin. Nat. Rev. Microbiol. 2006, 4:67-76.
24. Baquero E., et al. Intermediate conformations during viral fusion glycoprotein structural transition. Curr. Opin. Virol. 2013, 3:143-150.
25. Li L., et al. Structural changes of envelope proteins during alphavirus fusion. Nature 2010, 468:705-708.
26. Sanchez-San Martin C., et al. A stable prefusion intermediate of the alphavirus fusion protein reveals critical features of class II membrane fusion. Cell Host Microbe 2008, 4:600-608.
27. Xu R., Wilson I.A. Structural characterization of an early fusion intermediate of influenza virus hemagglutinin. J. Virol. 2011, 85:5172-5182.
28. Kim Y.H., et al. Capture and imaging of a prehairpin fusion intermediate of the paramyxovirus PIV5. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:20992-20997.
29. Cardone G., et al. Visualization of the two-step fusion process of the retrovirus avian sarcoma/leukosis virus by cryo-electron tomography. J. Virol. 2012, 86:12129-12137.
30. Albertini A.A., et al. Characterization of monomeric intermediates during VSV glycoprotein structural transition. PLoS Pathog. 2012, 8:e1002556.
31. Cao S., Zhang W. Characterization of an early-stage fusion intermediate of Sindbis virus using cryoelectron microscopy. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:13362-13367.
32. Modis Y., et al. Structure of the dengue virus envelope protein after membrane fusion. Nature 2004, 427:313-319.
33. Chernomordik L.V., Kozlov M.M. Membrane hemifusion: crossing a chasm in two leaps. Cell 2005, 123:375-382.
34. Gibbons D.L., et al. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell 2003, 114:573-583.
35. Stiasny K., et al. Characterization of a membrane-associated trimeric low-pH-induced form of the class II viral fusion protein E from tick-borne encephalitis virus and its crystallization. J. Virol. 2004, 78:3178-3183.
36. Libersou S., et al. Distinct structural rearrangements of the VSV glycoprotein drive membrane fusion. J. Cell Biol. 2010, 191:199-210.
37. Maurer U.E., et al. The structure of herpesvirus fusion glycoprotein B-bilayer complex reveals the protein-membrane and lateral protein-protein interaction. Structure 2013, 21:1396-1405.
38. Ivanovic T., et al. Influenza-virus membrane fusion by cooperative fold-back of stochastically induced hemagglutinin intermediates. eLIFE 2013, 2:e00333.
39. Leikina E., et al. Influenza hemagglutinins outside of the contact zone are necessary for fusion pore expansion. J. Biol. Chem. 2004, 279:26526-26532.
40. Shepard C.W., et al. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005, 5:558-567.
41. Drummer H.E., et al. Mutagenesis of a conserved fusion peptide-like motif and membrane-proximal heptad-repeat region of hepatitis C virus glycoprotein E1. J. Gen. Virol. 2007, 88:1144-1148.
42. Ronecker S., et al. Formation of bovine viral diarrhea virus E1-E2 heterodimers is essential for virus entry and depends on charged residues in the transmembrane domains. J. Gen. Virol. 2008, 89:2114-2121.
43. Patel J., et al. The transmembrane domain of the hepatitis C virus E2 glycoprotein is required for correct folding of the E1 glycoprotein and native complex formation. Virology 2001, 279:58-68.
44. Durantel D., et al. Study of the mechanism of antiviral action of iminosugar derivatives against bovine viral diarrhea virus. J. Virol. 2001, 75:8987-8998.
45. Weiland E., et al. Pestivirus glycoprotein which induces neutralizing antibodies forms part of a disulfide-linked heterodimer. J. Virol. 1990, 64:3563-3569.
46. Branza-Nichita N., et al. Antiviral effect of N-butyldeoxynojirimycin against bovine viral diarrhea virus correlates with misfolding of E2 envelope proteins and impairment of their association into E1-E2 heterodimers. J. Virol. 2001, 75:3527-3536.
47. Vieyres G., et al. Characterization of the envelope glycoproteins associated with infectious hepatitis C virus. J. Virol. 2010, 84:10159-10168.
48. Modis Y., et al. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:6986-6991.
49. Skehel J.J., Wiley D.C. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell 1998, 95:871-874.
50. Donald J.E., et al. Transmembrane orientation and possible role of the fusogenic peptide from parainfluenza virus 5 (PIV5) in promoting fusion. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3958-3963.
51. Stein A., et al. Helical extension of the neuronal SNARE complex into the membrane. Nature 2009, 460:525-528.
52. Dupressoir A., et al. From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation. Placenta 2012, 33:663-671.
53. Gardner A., Welch J.J. A formal theory of the selfish gene. J. Evol. Biol. 2011, 24:1801-1813.