Efficient replication of a paramyxovirus independent of full zippering of the fusion protein six-helix bundle domain

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 36, 2014, Pages E3795-E3804

  Brindley, Melinda A ^a   Plattet, Philippe ^b   Plemper, Richard Karl ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Measles virus; Membrane fusion

Indexed keywords

CYSTEINE; DISULFIDE; MUTANT PROTEIN; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHICKEN; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETIC RECOMBINATION; GENETICS; HUMAN; KINETICS; MEASLES VIRUS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN REFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CHICKENS; COS CELLS; CYSTEINE; DISULFIDES; HUMANS; KINETICS; MEASLES VIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PROTEIN ENGINEERING; PROTEIN MULTIMERIZATION; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINATION, GENETIC; VIRAL FUSION PROTEINS; VIRUS REPLICATION;

EID: 84906993334     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1403609111     Document Type: Article

References (68)

1. Kozlov MM, McMahon HT, Chernomordik LV (2010) Protein-driven membrane stresses in fusion and fission. Trends Biochem Sci 35(12):699-706.
2. Chen YA, Scheller RH (2001) SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol 2(2):98-106.
3. Plemper RK (2011) Cell entry of enveloped viruses. Curr Opin Virol 1(2):92-100.
4. Bartesaghi A, Merk A, Borgnia MJ, Milne JL, Subramaniam S (2013) Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat Struct Mol Biol 20(12):1352-1357.
5. Bizebard T, et al. (1995) Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376(6535):92-94.
6. Welch BD, et al. (2012) Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc Natl Acad Sci USA 109(41):16672-16677.
7. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289(5796):366-373.
8. Yin HS, Wen X, Paterson RG, Lamb RA, Jardetzky TS (2006) Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439(7072):38-44.
9. Buzon V, et al. (2010) Crystal structure of HIV-1 gp41 including both fusion peptide and membrane proximal external regions. PLoS Pathog 6(5):e1000880.
10. Zokarkar A, Connolly SA, Jardetzky TS, Lamb RA (2012) Reversible inhibition of fusion activity of a paramyxovirus fusion protein by an engineered disulfide bond in the membrane-proximal external region. J Virol 86(22):12397-12401.
11. Chernomordik LV, Kozlov MM (2008) Mechanics of membrane fusion. Nat Struct Mol Biol 15(7):675-683.
12. Harrison SC (2008) Viral membrane fusion. Nat Struct Mol Biol 15(7):690-698.
13. Donald JE, et al. (2011) Transmembrane orientation and possible role of the fusogenic peptide from parainfluenza virus 5 (PIV5) in promoting fusion. Proc Natl Acad Sci USA 108(10):3958-3963.
14. Eckert DM, Kim PS (2001) Mechanisms of viral membrane fusion and its inhibition. Annu Rev Biochem 70:777-810.
15. Markosyan RM, Cohen FS, Melikyan GB (2003) HIV-1 envelope proteins complete their folding into six-helix bundles immediately after fusion pore formation. Mol Biol Cell 14(3):926-938.
16. Melikyan GB, et al. (2000) Evidence that the transition of HIV-1 gp41 into a six-helix bundle, not the bundle configuration, induces membrane fusion. J Cell Biol 151(2):413-423.
17. Markosyan RM, Leung MY, Cohen FS (2009) The six-helix bundle of human immunodeficiency virus Env controls pore formation and enlargement and is initiated at residues proximal to the hairpin turn. J Virol 83(19):10048-10057.
18. McLellan JS, et al. (2013) Structure of RSV fusion glycoprotein trimer bound to a prefusion-specific neutralizing antibody. Science 340(6136):1113-1117.
19. Yin HS, Paterson RG, Wen X, Lamb RA, Jardetzky TS (2005) Structure of the uncleaved ectodomain of the paramyxovirus (hPIV3) fusion protein. Proc Natl Acad Sci USA 102(26):9288-9293.
20. Swanson K, et al. (2010) Structure of the Newcastle disease virus F protein in the postfusion conformation. Virology 402(2):372-379.
21. Swanson KA, et al. (2011) Structural basis for immunization with postfusion respiratory syncytial virus fusion F glycoprotein (RSV F) to elicit high neutralizing antibody titers. Proc Natl Acad Sci USA 108(23):9619-9624.
22. Russell CJ, Jardetzky TS, Lamb RA (2001) Membrane fusion machines of paramyxoviruses: Capture of intermediates of fusion. EMBO J 20(15):4024-4034.
23. Ellgaard L, Molinari M, Helenius A (1999) Setting the standards: Quality control in the secretory pathway. Science 286(5446):1882-1888.
24. Lee JK, Prussia A, Snyder JP, Plemper RK (2007) Reversible inhibition of the fusion activity of measles virus F protein by an engineered intersubunit disulfide bridge. J Virol 81(16):8821-8826.
25. Bose S, et al. (2013) Mutations in the parainfluenza virus 5 fusion protein reveal domains important for fusion triggering and metastability. J Virol 87(24):13520-13531.
26. Diaz-Aguilar B, Dewispelaere K, Yi HA, Jacobs A (2013) Significant differences in cell-cell fusion and viral entry between strains revealed by scanning mutagenesis of the C-heptad repeat of HIV gp41. Biochemistry 52(20):3552-3563.
27. Hernandez LD, Hoffman LR, Wolfsberg TG, White JM (1996) Virus-cell and cell-cell fusion. Annu Rev Cell Dev Biol 12:627-661.
28. Lawrence DM, et al. (2000) Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J Virol 74(4):1908-1918.
29. Kondo N, Miyauchi K, Matsuda Z (2011) Monitoring viral-mediated membrane fusion using fluorescent reporter methods. Curr Protoc Cell Biol Chapter 26:Units 26-29.
30. Ader N, et al. (2013) Mechanism for active membrane fusion triggering by morbillivirus attachment protein. J Virol 87(1):314-326.
31. Brindley MA, Takeda M, Plattet P, Plemper RK (2012) Triggering the measles virus membrane fusion machinery. Proc Natl Acad Sci USA 109(44):E3018-E3027.
32. Prado GN, Romero JR, Rivera A (2013) Endothelin-1 receptor antagonists regulate cell surface-associated protein disulfide isomerase in sickle cell disease. FASEB J 27(11):4619-4629.
33. Turano C, Coppari S, Altieri F, Ferraro A (2002) Proteins of the PDI family: Unpredicted non-ER locations and functions. J Cell Physiol 193(2):154-163.
34. Stantchev TS, et al. (2012) Cell-type specific requirements for thiol/disulfide exchange during HIV-1 entry and infection. Retrovirology 9:97-111.
35. Mandel R, Ryser HJ, Ghani F, Wu M, Peak D (1993) Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc Natl Acad Sci USA 90(9):4112-4116.
36. Plemper RK, et al. (2005) Design of a small-molecule entry inhibitor with activity against primary measles virus strains. Antimicrob Agents Chemother 49(9):3755-3761.
37. Doyle J, et al. (2006) Two domains that control prefusion stability and transport competence of the measles virus fusion protein. J Virol 80(3):1524-1536.
38. Maisner A, et al. (2000) Recombinant measles virus requiring an exogenous protease for activation of infectivity. J Gen Virol 81(Pt 2):441-449.
39. Brindley MA, et al. (2013) A stabilized headless measles virus attachment protein stalk efficiently triggers membrane fusion. J Virol 87(21):11693-11703.
40. Yan D, et al. (2013) Dual myxovirus screen identifies a small-molecule agonist of the host antiviral response. J Virol 87(20):11076-11087.
41. Kielian M, Rey FA (2006) Virus membrane-fusion proteins: More than one way to make a hairpin. Nat Rev Microbiol 4(1):67-76.
42. Weissenhorn W, Hinz A, Gaudin Y (2007) Virus membrane fusion. FEBS Lett 581(11):2150-2155.
43. Bissonnette ML, Donald JE, DeGrado WF, Jardetzky TS, Lamb RA (2009) Functional analysis of the transmembrane domain in paramyxovirus F protein-mediated membrane fusion. J Mol Biol 386(1):14-36.
44. Smith EC, et al. (2013) Trimeric transmembrane domain interactions in paramyxovirus fusion proteins: Roles in protein folding, stability, and function. J Biol Chem 288(50):35726-35735.
45. Chang DK, Cheng SF, Kantchev EA, Lin CH, Liu YT (2008) Membrane interaction and structure of the transmembrane domain of influenza hemagglutinin and its fusion peptide complex. BMC Biol 6:2-13.
46. Tatulian SA, Tamm LK (2000) Secondary structure, orientation, oligomerization, and lipid interactions of the transmembrane domain of influenza hemagglutinin. Biochemistry 39(3):496-507.
47. Reuven EM, et al. (2012) HIV-1 gp41 transmembrane domain interacts with the fusion peptide: Implication in lipid mixing and inhibition of virus-cell fusion. Biochemistry 51(13):2867-2878.
48. Charloteaux B, Lorin A, Brasseur R, Lins L (2009) The "Tilted Peptide Theory" links membrane insertion properties and fusogenicity of viral fusion peptides. Protein Pept Lett 16(7):718-725.
49. Epand RM (2003) Fusion peptides and the mechanism of viral fusion. Biochim Biophys Acta 1614(1):116-121.
50. Stein A, Weber G, Wahl MC, Jahn R (2009) Helical extension of the neuronal SNARE complex into the membrane. Nature 460(7254):525-528.
51. Ryser HJ, Levy EM, Mandel R, DiSciullo GJ (1994) Inhibition of human immunodeficiency virus infection by agents that interfere with thiol-disulfide interchange upon virus-receptor interaction. Proc Natl Acad Sci USA 91(10):4559-4563.
52. Connolly SA, Leser GP, Yin HS, Jardetzky TS, Lamb RA (2006) Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc Natl Acad Sci USA 103(47):17903-17908.
53. Porotto M, et al. (2010) Inhibition of Nipah virus infection in vivo: Targeting an early stage of paramyxovirus fusion activation during viral entry. PLoS Pathog 6(10):e1001168.
54. Welsch JC, et al. (2013) Fatal measles virus infection prevented by brain-penetrant fusion inhibitors. J Virol 87(24):13785-13794.
55. Roymans D, et al. (2010) Binding of a potent small-molecule inhibitor of six-helix bundle formation requires interactions with both heptad-repeats of the RSV fusion protein. Proc Natl Acad Sci USA 107(1):308-313.
56. Ganellin CR, Jefferis R, Roberts SM, eds (2013) Introduction to Biological and Small Molecule Drug Research and Development: Theory and Case Studies (Academic, Oxford, UK), p 1.
57. Aydin H, Cook JD, Lee JE (2014) Crystal structures of beta- and gammaretrovirus fusion proteins reveal a role for electrostatic stapling in viral entry. J Virol 88(1):143-153.
58. Ono N, et al. (2001) Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75(9):4399-4401.
59. Cathomen T, Naim HY, Cattaneo R (1998) Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J Virol 72(2):1224-1234.
60. Paal T, et al. (2009) Probing the spatial organization of measles virus fusion complexes. J Virol 83(20):10480-10493.
61. Buchholz UJ, Finke S, Conzelmann KK (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73(1):251-259.
62. Singh M, Billeter MA (1999) A recombinant measles virus expressing biologically active human interleukin-12. J Gen Virol 80(Pt 1):101-106.
63. Plemper RK, Compans RW (2003) Mutations in the putative HR-C region of the measles virus F2 glycoprotein modulate syncytium formation. J Virol 77(7):4181-4190.
64. Takeda M, et al. (2000) Recovery of pathogenic measles virus from cloned cDNA. J Virol 74(14):6643-6647.
65. Tahara M, et al. (2013) Functional and structural characterization of neutralizing epitopes of measles virus hemagglutinin protein. J Virol 87(1):666-675.
66. Plemper RK, Hammond AL, Cattaneo R (2000) Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J Virol 74(14):6485-6493.
67. Avila M, et al. (2014) Molecular determinants defining the triggering range of prefusion F complexes of canine distemper virus. J Virol 88(5):2951-2966.
68. Lambert DM, et al. (1996) Peptides from conserved regions of paramyxovirus fusion (F) proteins are potent inhibitors of viral fusion. Proc Natl Acad Sci USA 93(5):2186-2191.