Regulation of paramyxovirus fusion activation, the hemagglutinin-neuraminidase protein stabilizes the fusion protein in a pretriggered state

Journal of Virology

Volumn 86, Issue 23, 2012, Pages 12838-12848

  Porotto, Matteo ^a   Salah, Zuhair W ^a,b   Gui, Long ^c   DeVito, Ilaria ^a   Jurgens, Eric M ^a   Lu, Hong ^a   Yokoyama, Christine C ^a   Palermo, Laura M ^a   Lee, Kelly K ^c   Moscona, Anne ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Department of Obstetrics Gynecology   (Qatar)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; SIALIDASE;

ARTICLE; CONTROLLED STUDY; HEAT TREATMENT; HUMAN; HUMAN CELL; NONHUMAN; PARAMYXOVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; STRUCTURE ANALYSIS; VIRION; VIRUS ACTIVATION;

BETA-GALACTOSIDASE; CELL LINE; FLOW CYTOMETRY; HN PROTEIN; HUMANS; MICROSCOPY, FLUORESCENCE; PARAINFLUENZA VIRUS 1, HUMAN; PROTEIN STABILITY; RECEPTORS, CELL SURFACE; TEMPERATURE; VIRAL FUSION PROTEINS; VIRUS INTERNALIZATION;

ORTHOMYXOVIRIDAE; PARAMYXOVIRIDAE;

EID: 84869204459     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01965-12     Document Type: Article

References (72)

1. Ader N, et al. 2012. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger f protein refolding for membrane fusion. J. Biol. Chem. 287, 16324-16334.
2. Aguilar HC, et al. 2007. Polybasic KKR motif in the cytoplasmic tail of Nipah virus fusion protein modulates membrane fusion by inside-out signaling. J. Virol. 81, 4520-4532.
3. Aguilar HC, et al. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J. Virol. 80, 4878-4889.
4. Bagai S, Lamb R. 1995. Quantitative measurement of paramyxovirus fusion, differences in requirements of glycoproteins between simian virus 5 and human parainfluenza virus 3 or Newcastle disease virus. J. Virol. 69, 6712-6719.
5. Bishop KA, et al. 2008. Residues in the stalk domain of the Hendra virus g glycoprotein modulate conformational changes associated with receptor binding. J. Virol. 82, 11398-11409.
6. Bose S, et al. 2011. Structure and mutagenesis of the parainfluenza virus 5 hemagglutinin-neuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 85, 12855-12866.
7. Chaiwatpongsakorn S, Epand RF, Collins PL, Epand RM, Peeples ME. 2011. Soluble respiratory syncytial virus fusion protein in the fully cleaved, pretriggered state is triggered by exposure to low-molarity buffer. J. Virol. 85, 3968-3977.
8. Chang A, Dutch RE. 2012. Paramyxovirus fusion and entry, multiple paths to a common end. Viruses 4, 613-636.
9. Connolly SA, Leser GP, Jardetzky TS, Lamb RA. 2009. Bimolecular complementation of paramyxovirus fusion and hemagglutininneuraminidase proteins enhances fusion, implications for the mechanism of fusion triggering. J. Virol. 83, 10857-10868.
10. Corey EA, Iorio RM. 2007. Mutations in the stalk of the measles virus hemagglutinin protein decrease fusion but do not interfere with virusspecific interaction with the homologous fusion protein. J. Virol. 81, 9900-9910.
11. Crennell S, Takimoto T, Portner A, Taylor G. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 7, 1068-1074.
12. Deng R, Wang Z, Mirza A, Iorio R. 1995. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 209, 457-469.
13. Dutch RE. 2010. Entry and fusion of emerging paramyxoviruses. PLoS Pathog. 6, e1000881. doi, 10.1371/journal.ppat.1000881.
14. Eckert DM, Kim PS. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70, 777-810.15.
15. Farzan SF, et al. 2011. Premature activation of the paramyxovirus fusion protein before target cell attachment with corruption of the viral fusion machinery. J. Biol. Chem. 286, 37945-37954.
16. Greengard O, Poltoratskaia N, Leikina E, Zimmerberg J, Moscona A. 2000. The anti-influenza virus agent 4-GU-DANA (Zanamivir) inhibits cell fusion mediated by human parainfluenza virus and influenza virus HA. J. Virol. 74, 11108-11114.
17. Horvath CM, Paterson RG, Shaughnessy MA, Wood R, Lamb RA. 1992. Biological activity of paramyxovirus fusion proteins, factors influencing formation of syncytia. J. Virol. 66, 4564-4569.
18. Hu CD, Chinenov Y, Kerppola TK. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798.
19. Hu CD, Kerppola TK. 2003. Simultaneous visualization of multiple protein interactions in living cells using multicolor fluorescence complementation analysis. Nat. Biotechnol. 21, 539-545.
20. Hu X, Ray R, Compans RW. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66, 1528-1534.
21. Ingallinella P, et al. 2009. Addition of a cholesterol group to an HIV-1 peptide fusion inhibitor dramatically increases its antiviral potency. Proc. Natl. Acad. Sci. U. S. A. 106, 5801-5806.
22. Iorio RM, Mahon PJ. 2008. Paramyxoviruses, different receptors- different mechanisms of fusion. Trends Microbiol. 16, 135-137.
23. Iorio RM, Melanson VR, Mahon PJ. 2009. Glycoprotein interactions in paramyxovirus fusion. Future Virol. 4, 335-351.
24. Kerppola TK. 2006. Visualization of molecular interactions by fluorescence complementation. Nat. Rev. Mol. Cell Biol. 7, 449-456.
25. Kremer J, Mastronarde D, McIntosh J. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76.
26. Lamb R. 1993. Paramyxovirus fusion, a hypothesis for changes. Virology 197, 1-11.
27. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion, lessons from the F andHNatomic structures. Virology 344, 30-37.
28. Lawrence MC, et al. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335, 1343-1357.
29. Lee B, Ataman ZA. 2011. Modes of paramyxovirus fusion, a Henipavirus perspective. Trends Microbiol. 19, 389-399.
30. Lee JK, et al. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J. Biol. Chem. 283, 16561-16572.
31. Lin HP, Vincenz C, Eliceiri KW, Kerppola TK, Ogle BM. 2010. Bimolecular fluorescence complementation analysis of eukaryotic fusion products. Biol. Cell 102, 525-537.
32. Ludwig K, et al. 2008. Electron cryomicroscopy reveals different F1+F2 protein states in intact parainfluenza virions. J. Virol. 82, 3775-3781.
33. Melanson VR, Iorio RM. 2006. Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion. J. Virol. 80, 623-633.
34. Moosmann P, Rusconi S. 1996. Alpha complementation of LacZ in mammalian cells. Nucleic Acids Res. 24, 1171-1172.
35. Moscona A. 2005. Entry of parainfluenza virus into cells as a target for interrupting childhood respiratory disease. J. Clin. Invest. 115, 1688-1698.
36. Moscona A, Peluso R. 1991. Properties of the human parainfluenza virus type 3 RNA polymerase/replicase in vitro, consensus with other negativestranded RNA viruses. J. Virol. 65, 4470-4474.
37. Moscona A, Peluso RW. 1993. Relative affinity of the human parainfluenza virus 3 hemagglutinin-neuraminidase for sialic acid correlates with virus-induced fusion activity. J. Virol. 67, 6463-6468.
38. Murrell M, Porotto M, Weber T, Greengard O, Moscona A. 2003. Mutations in human parainfluenza virus type 3 HN causing increased receptor binding activity and resistance to the transition state sialic acid analog 4-GU-DANA (zanamivir). J. Virol. 77, 309-317.
39. Obrig TG, Culp WJ, McKeehan WL, Hardesty B. 1971. The mechanism by which cycloheximide and related glutarimide antibiotics inhibit peptide synthesis on reticulocyte ribosomes. J. Biol. Chem. 246, 174-181.
40. Palermo L, et al. 2009. Human parainfluenza virus infection of the airway epithelium, the viral hemagglutinin-neuraminidase regulates fusion protein activation and modulates infectivity. J. Virol. 83, 6900-6908.
41. Palermo LM, Porotto M, Greengard O, Moscona A. 2007. Fusion promotion by a paramyxovirus hemagglutinin-neuraminidase protein, pH modulation of receptor avidity of binding sites I and II. J. Virol. 81, 9152-9161.
42. Palmer SG, et al. 2012. Adaptation of human parainfluenza virus to airway epithelium reveals fusion properties required for growth in host tissue. mBio 3(3), e00137-12. doi, 10.1128/mBio.00137-12.
43. Plemper RK, Brindley MA, Iorio RM. 2011. Structural and mechanistic studies of measles virus illuminate paramyxovirus entry. PLoS Pathog. 7, e1002058. doi, 10.1371/journal.ppat.1002058.
44. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76, 5051-5061.
45. Porotto M, et al. 2011. Spring-loaded model revisited, Paramyxovirus fusion requires engagement of a receptor binding protein beyond initial triggering of the fusion protein. J. Virol. 85, 12867-12880.
46. Porotto M, et al. 2006. Inhibition of Hendra virus membrane fusion. J. Virol. 80, 9837-9849.
47. Porotto M, et al. 2006. Paramyxovirus receptor-binding molecules, engagement of one site on the hemagglutinin-neuraminidase protein modulates activity at the second site. J. Virol. 80, 1204-1213.
48. Porotto M, Fornabaio M, Kellogg GE, Moscona A. 2007. A second receptor binding site on human parainfluenza virus type 3 hemagglutininneuraminidase contributes to activation of the fusion mechanism. J. Virol. 81, 3216-3228.
49. Porotto M, Greengard O, Poltoratskaia N, Horga M-A, Moscona A. 2001. Human parainfluenza virus type 3 HN-receptor interaction, the effect of 4-GU-DANA on a neuraminidase-deficient variant. J. Virol. 75, 7481-7488.
50. Porotto M, Murrell M, Greengard O, Doctor L, Moscona A. 2005. Influence of the human parainfluenza virus 3 attachment protein's neuraminidase activity on its capacity to activate the fusion protein. J. Virol. 79, 2383-2392.
51. Porotto M, et al. 2004. Inhibition of parainfluenza type 3 and Newcastle disease virus hemagglutinin-neuraminidase receptor binding, effect of receptor avidity and steric hindrance at the inhibitor binding sites. J. Virol. 78, 13911-13919.
52. Porotto M, Murrell M, Greengard O, Moscona A. 2003. Triggering of human parainfluenza virus 3 fusion protein (F) by the hemagglutininneuraminidase (HN), an HN mutation diminishing the rate of F activation and fusion. J. Virol. 77, 3647-3654.
53. Porotto M, Palmer SG, Palermo LM, Moscona A. 2012. Mechanism of fusion triggering by human parainfluenza virus type III, communication between viral glycoproteins during entry. J. Biol. Chem. 287, 778-793.
54. 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, e1001168. doi, 10.1371/journal.ppat.1001168.
55. Porotto M, et al. 2012. The second receptor binding site of the globular head of the Newcastle disease virus hemagglutinin-neuraminidase activates the stalk of multiple paramyxovirus receptor binding proteins to trigger fusion. J. Virol. 86, 5730-5741.
56. Porotto M, Yi F, Moscona A, LaVan DA. 2011. Synthetic protocells interact with viral nanomachinery and inactivate pathogenic human virus. PLoS One 6, e16874. doi, 10.1371/journal.pone.0016874.
57. Porotto M, et al. 2010. Viral entry inhibitors targeted to the membrane site of action. J. Virol. 84, 6760-6768.
58. Russell CJ, Kantor KL, Jardetzky TS, Lamb RA. 2003. A dual-functional paramyxovirus F protein regulatory switch segment, activation and membrane fusion. J. Cell Biol. 163, 363-374.
59. San-Juan-Vergara H, et al. 2012. Cholesterol-rich microdomains as docking platforms for respiratory syncytial virus in normal human bronchial epithelial cells. J. Virol. 86, 1832-1843.
60. Schildgen V, et al. 2011. Human metapneumovirus, lessons learned over the first decade. Clin. Microbiol. Rev. 24, 734-754.
61. Schowalter RM, Chang A, Robach JG, Buchholz UJ, Dutch RE. 2009. Low-pH triggering of human metapneumovirus fusion, essential residues and importance in entry. J. Virol. 83, 1511-1522.
62. Sergel T, McGinnes LW, Peeples ME, Morrison TG. 1993. The attachment function of the Newcastle disease virus hemagglutininneuraminidase protein can be separated from fusion promotion by mutation. Virology 193, 717-726.
63. Smith EC, Popa A, Chang A, Masante C, Dutch RE. 2009. Viral entry mechanisms, the increasing diversity of paramyxovirus entry. FEBS J. 276, 7217-7227.
64. Stone-Hulslander J, Morrison TG. 1999. Mutational analysis of heptad repeats in the membrane-proximal region of Newcastle disease virus HN protein. J. Virol. 73, 3630-3637.65.
65. Tanabayashi K, Compans R. 1996. Functional interactions of paramyxovirus glycoproteins, identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70, 6112-6118.
66. Wharton SA, Skehel JJ, Wiley DC. 2000. Temperature dependence of fusion by Sendai virus. Virology 271, 71-78.
67. 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. U. S. A. 102, 9288-9293.
68. 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, 38-44.
69. Yuan P, et al. 2011. Structure of the Newcastle disease virus hemagglutinin-neuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc. Natl. Acad. Sci. U. S. A. 108, 14920-14925.
70. Yuan P, et al. 2005. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13, 803-815.
71. Yuasa T, et al. 1995. A cell fusion-inhibiting monoclonal antibody binds to the presumed stalk domain of the human parainfluenza type 2 virus hemagglutinin-neuraminidase protein. Virology 206, 1117-1125.
72. Zaitsev V, et al. 2004. Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase, implications for fusion. J. Virol. 78, 3733-3741.