Interaction between the hemagglutinin-neuraminidase and fusion glycoproteins of human parainfluenza virus type III regulates viral growth in vivo

mBio

Volumn 4, Issue 5, 2013, Pages

  Xu, Rui ^a   Palmer, Samantha G ^b   Porotto, Matteo ^b   Palermo, Laura M ^b   Niewiesk, Stefan ^c   Wilson, Ian A ^a   Moscona, Anne ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HN PROTEIN; HYBRID PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHIOLITIS; CELL IMMORTALIZATION; CELL MEMBRANE; CONTROLLED STUDY; CORRELATION ANALYSIS; CROUP; CRYSTALLOGRAPHY; DIMERIZATION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG INFECTION; NONHUMAN; PARAINFLUENZA VIRUS 3; PNEUMONIA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; RESPIRATORY EPITHELIUM; VIROGENESIS; VIRUS ENVELOPE; VIRUS STRAIN; VIRUS SURVIVAL;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; FEMALE; HN PROTEIN; HUMANS; PARAINFLUENZA VIRUS 3, HUMAN; PROTEIN BINDING; RATS; RESPIROVIRUS INFECTIONS; SIGMODONTINAE; VIRAL FUSION PROTEINS; VIRAL PROTEINS;

EID: 84887135418     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00803-13     Document Type: Article

References (60)

1. Moscona A, Peluso RW. 1991. Fusion properties of cells persistently infected with human parainfluenza virus type 3: participation of hemagglutinin-neuraminidase in membrane fusion. J. Virol. 65: 2773-2777.
2. Moscona A, Peluso RW. 1993. Relative affinity of the human parainflu-enza virus type 3 hemagglutinin-neuraminidase for sialic acid correlates with virus-induced fusion activity. J. Virol. 67:6463-6468.
3. Bagai S, Lamb RA. 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.
4. 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.
5. Hu XL, Ray R, Compans RW. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainflu-enza viruses. J. Virol. 66:1528-1534.
6. Lamb RA. 1993. Paramyxovirus fusion: a hypothesis for changes. Virol-ogy 197:1-11.
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. San-Juan-Vergara H, Sampayo-Escobar V, Reyes N, Cha B, Pacheco-Lugo L, Wong T, Peeples ME, Collins PL, Castaño ME, Mohapatra SS. 2012. Cholesterol-rich microdomains as docking platforms for respira-tory syncytial virus in normal human bronchial epithelial cells. J. Virol. 86:1832-1843.
9. Chang A, Masante C, Buchholz UJ, Dutch RE. 2012. Human metap-neumovirus (HMPV) binding and infection are mediated by interactions between the HMPV fusion protein and heparan sulfate. J. Virol. 86: 3230-3243.
10. Schildgen V, van den Hoogen B, Fouchier R, Tripp RA, Alvarez R, Manoha C, Williams J, Schildgen O. 2011. Human metapneumovirus: lessons learned over the first decade. Clin. Microbiol. Rev. 24:734-754.
11. 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.
12. Porotto M, Salah ZW, Gui L, Devito I, Jurgens EM, Lu H, Yokoyama CC, Palermo LM, Lee KK, Moscona A. 2012. Regulation of paramyxovirus fusion activation: the hemagglutinin-neuraminidase protein stabi-lizes the fusion protein in a pre-triggered state. J. Virol. 86:12838-12848.
13. Chang A, Dutch RE. 2012. Paramyxovirus fusion and entry: multiple paths to a common end. Viruses 4:613-636.
14. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F and HN atomic structures. Virology 344:30-37.
15. Lee B, Ataman ZA. 2011. Modes of paramyxovirus fusion: a henipavirus perspective. Trends Microbiol. 19:389-399.
16. Moscona A. 2005. Entry of parainfluenza virus into cells as a target for interrupting childhood respiratory disease. J. Clin. Invest. 115: 1688-1698.
17. 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.
18. 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.
19. Bose S, Welch BD, Kors CA, Yuan P, Jardetzky TS, Lamb RA. 2011. Structure and mutagenesis of the parainfluenza virus 5 hemagglutininneuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 85:12855-12866.
20. Deng R, Wang Z, Mirza AM, Iorio RM. 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.
21. 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.
22. 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.
23. 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 activa-tion and fusion. J. Virol. 77:3647-3654.
24. 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 mu-tation. Virology 193:717-726.
25. 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.
26. Tanabayashi K, Compans RW. 1996. Functional interactions of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70:6112-6118.
27. Yuan P, Swanson KA, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 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.
28. Yuasa T, Kawano M, Tabata N, Nishio M, Kusagawa S, Komada H, Matsumura H, Ito Y, Tsurudome M. 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.
29. Porotto M, Devito I, Palmer SG, Jurgens EM, Yee JL, Yokoyama CC, Pessi A, Moscona A. 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.
30. Porotto M, Salah Z, Devito I, Talekar A, Palmer SG, Xu R, Wilson IA, Moscona A. 2012. The second receptor binding site of the globular head of the Newcastle disease virus (NDV) hemagglutinin-neuraminidase acti-vates the stalk of multiple paramyxovirus receptor binding proteins to trigger fusion. J. Virol. 86:5730-5741.
31. Palermo LM, Porotto M, Yokoyama CC, Palmer SG, Mungall BA, Greengard O, Niewiesk S, Moscona A. 2009. Human parainfluenza virus infection of the airway epithelium: viral hemagglutinin-neuraminidase regulates fusion protein activation and modulates infectivity. J. Virol. 83: 6900-6908.
32. 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.
33. Palmer SG, Porotto M, Palermo LM, Cunha LF, Greengard O, Moscona A. 2012. Adaptation of human parainfluenza virus to airway epithelium reveals fusion properties required for growth in host tissue. mBio 3:e00137-12. doi:10.1128/mBio.00137-12.
34. Farzan SF, Palermo LM, Yokoyama CC, Orefice G, Fornabaio M, Sarkar A, Kellogg GE, Greengard O, Porotto M, Moscona A. 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.
35. Moscona A, Porotto M, Palmer S, Tai C, Aschenbrenner L, Triana-Baltzer G, Li QX, Wurtman D, Niewiesk S, Fang F. 2010. A recombinant sialidase fusion protein effectively inhibits human parainfluenza viral in-fection in vitro and in vivo. J. Infect. Dis. 202:234-241.
36. Hernandez FP, Sandri-Goldin RM. 2010. Head-to-tail intramolecular interaction of herpes simplex virus type 1 regulatory protein ICP27 is important for its interaction with cellular mRNA export receptor TAP /NXF1. mBio 1:e00268-10. doi:10.1128/mBio.00268-10.
37. Hernandez FP, Sandri-Goldin RM. 2010. Herpes simplex virus 1 regu-latory protein ICP27 undergoes a head-to-tail intramolecular interaction. J. Virol. 84:4124-4135.
38. Hu CD, Chinenov Y, Kerppola TK. 2002. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular flu-orescence complementation. Mol. Cell 9:789-798.
39. Hu CD, Kerppola TK. 2003. Simultaneous visualization of multiple pro-tein interactions in living cells using multicolor fluorescence complemen-tation analysis. Nat. Biotechnol. 21:539-545.
40. Kerppola TK. 2006. Visualization of molecular interactions by fluorescence complementation. Nat. Rev. Mol. Cell Biol. 7:449-456.
41. Lin HP, Vincenz C, Eliceiri KW, Kerppola TK, Ogle BM. 2010. Bimolecular fluorescence complementation analysis of eukaryotic fusion products. Biol. Cell 102:525-537.
42. Porotto M, Murrell M, Greengard O, Lawrence MC, McKimm-Breschkin JL, Moscona A. 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.
43. Brindley MA, Plemper RK. 2010. Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organiza-tion of the physiological measles virus attachment protein H. J. Virol. 84:12174-12184.
44. Robach JG, Lamb RA. 2010. Analysis of parainfluenza virus-5 hemagglutinin-neuraminidase protein mutants that are blocked in internalization and degradation. Virology 406:189-201.
45. Mahon PJ, Mirza AM, Musich TA, Iorio RM. 2008. Engineered intermonomeric disulfide bonds in the globular domain of Newcastle disease virus hemagglutinin-neuraminidase protein: implications for the mecha-nism of fusion promotion. J. Virol. 82:10386-10396.
46. Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, McKimm-Breschkin JL, Colman PM. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357.
47. Batschelet E, Domingo E, Weissmann C. 1976. The proportion of rever-tant and mutant phage in a growing population, as a function of mutation and growth rate. Gene 1:27-32.
48. Chao L. 1990. Fitness of RNA virus decreased by Muller's ratchet. Nature 348:454-455.
49. Holland JJ, de la Torre JC, Clarke DK, Duarte E. 1991. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J. Virol. 65:2960-2967.
50. Martínez MA, Carrillo C, González-Candelas F, Moya A, Domingo E, Sobrino F. 1991. Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies. J. Virol. 65: 3954-3957.
51. Zhang L, Bukreyev A, Thompson CI, Watson B, Peeples ME, Collins PL, Pickles RJ. 2005. Infection of ciliated cells by human parainfluenza virus type 3 in an in vitro model of human airway epithelium. J. Virol. 79:1113-1124.
52. Steffen DL, Xu K, Nikolov DB, Broder CC. 2012. Henipavirus mediated membrane fusion, virus entry and targeted therapeutics. Viruses 4:280-309.
53. Russell CJ, Jardetzky TS, Lamb RA. 2001. Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J. 20: 4024-4034.
54. Bose S, Zokarkar A, Welch BD, Leser GP, Jardetzky TS, Lamb RA. 2012. Fusion activation by a headless parainfluenza virus 5 hemagglutininneuraminidase stalk suggests a modular mechanism for triggering. Proc. Natl. Acad. Sci. U. S. A. 109:E2625-E2634.
55. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
56. Klock HE, Lesley SA. 2009. The polymerase incomplete primer extension (PIPE) method applied to high-throughput cloning and site-directed mu-tagenesis. Methods Mol. Biol. 498:91-103.
57. Otwinowski Z, Minor W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
58. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ. 2005. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. D61:458-464.
59. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. D60:2126-2132.
60. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, Read RJ, Sacchettini JC, Sauter NK, Terwilliger TC. 2002. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58:1948-1954.