Trypsin-and low pH-mediated fusogenicity of avian metapneumovirus fusion proteins is determined by residues at positions 100, 101 and 294

Scientific Reports

Volumn 5, Issue 1, 2015, Pages

  Yun, Bingling ^a   Guan, Xiaolu ^a   Liu, Yongzhen ^a   Gao, Yanni ^a   Wang, Yongqiang ^a   Qi, Xiaole ^a   Cui, Hongyu ^a   Liu, Changjun ^a   Zhang, Yanping ^a   Gao, Li ^a   Li, Kai ^a   Gao, Honglei ^a   Gao, Yulong ^a   Wang, Xiaomei ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

TRYPSIN; VIRUS FUSION PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; GENETICS; HAMSTER; MEMBRANE FUSION; METABOLISM; METAPNEUMOVIRUS; MUTAGENESIS; MUTATION; PH; VERO CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; CRICETINAE; HYDROGEN-ION CONCENTRATION; MEMBRANE FUSION; METAPNEUMOVIRUS; MUTAGENESIS; MUTATION; TRYPSIN; VERO CELLS; VIRAL FUSION PROTEINS;

EID: 84966703954     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/SREP15584     Document Type: Article

References (58)

1. Cook, J. Avian pneumovirus infections of turkeys and chickens. Vet. J. 160, 118–125 (2000).
2. Htut Aung, Y., Liman, M., Neumann, U. & Rautenschlein, S. Reproducibility of swollen sinuses in broilers by experimental infection with avian metapneumovirus subtypes A and B of turkey origin and their comparative pathogenesis. Avian Pathol. 37, 65–74 (2008).
3. Guionie, O. et al. Laboratory evaluation of a quantitative real-time reverse transcription PCR assay for the detection and identification of the four subgroups of avian metapneumovirus. J. Virol. Methods 139, 150–158 (2007).
4. Bäyon-Auboyer, M. H., Arnauld, C., Toquin, D. & Eterradossi, N. Nucleotide sequences of the F, L and G protein genes of two non-A/non-B avian pneumoviruses (APV) reveal a novel APV subgroup. J. Gen. Virol. 81, 2723–2733 (2000).
5. Brown, P. A. et al. Molecular Comparisons of Full Length Metapneumovirus (MPV) Genomes, Including Newly Determined French AMPV-C and–D Isolates, Further Supports Possible Subclassification within the MPV Genus. PloS one 9, e102740 (2014).
6. Earp, L., Delos, S., Park, H. & White, J. In Membrane trafficking in viral replication. 25–66 (Springer, 2005).
7. Moore, J., Jameson, B. A., Weiss, R. A. & Sattentau, Q. The HIV-cell fusion reaction. Viral fusion mechanisms. CRC Press, Boca Raton, Fla 233–289 (1993).
8. Nussbaum, O., Broder, C. C. & Berger, E. A. Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68, 5411–5422 (1994).
9. Bagai, S. & Lamb, R. A. 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 (1995).
10. Dutch, R. E., Joshi, S. B. & Lamb, R. A. Membrane fusion promoted by increasing surface densities of the paramyxovirus F and HN proteins: comparison of fusion reactions mediated by simian virus 5 F, human parainfluenza virus type 3 F, and influenza virus HA. J. Virol. 72, 7745–7753 (1998).
11. Stone-Hulslander, J. & Morrison, T. G. Detection of an interaction between the HN and F proteins in Newcastle disease virus-infected cells. J. Virol. 71, 6287–6295 (1997).
12. Talekar, A. et al. Identification of a region in the stalk domain of the Nipah virus receptor binding protein that is critical for fusion activation. J. Virol. 87, 10980–10996 (2013).
13. Biacchesi, S. et al. Recombinant human metapneumovirus lacking the small hydrophobic SH and/or attachment G glycoprotein: deletion of G yields a promising vaccine candidate. J. Virol. 78, 12877–12887 (2004).
14. Naylor, C. J. et al. Development of a reverse-genetics system for avian pneumovirus demonstrates that the small hydrophobic (SH) and attachment (G) genes are not essential for virus viability. J. Gen. Virol. 85, 3219 (2004).
15. Biacchesi, S. et al. Infection of nonhuman primates with recombinant human metapneumovirus lacking the SH, G, or M2-2 protein categorizes each as a nonessential accessory protein and identifies vaccine candidates. J. Virol. 79, 12608–12613 (2005).
16. Ling, R. et al. Deletion of the SH gene from avian metapneumovirus has a greater impact on virus production and immunogenicity in turkeys than deletion of the G gene or M2-2 open reading frame. J. Gen. Virol. 89, 525–533 (2008).
17. Karron, R. A. et al. Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proc. Natl. Acad. Sci. USA 94, 13961–13966 (1997).
18. Wei, Y. et al. Localization of a region in the fusion protein of avian metapneumovirus that modulates cell-cell fusion. J. Virol. 86, 11800–11814 (2012).
19. Schickli, J. H., Kaur, J., Ulbrandt, N., Spaete, R. R. & Tang, R. S. An S101P substitution in the putative cleavage motif of the human metapneumovirus fusion protein is a major determinant for trypsin-independent growth in Vero cells and does not alter tissue tropism in hamsters. J. Virol. 79, 10678–10689 (2005).
20. Schowalter, R. M., Smith, S. E. & Dutch, R. E. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J. Virol. 80, 10931–10941 (2006).
21. Zimmer, G., Budz, L. & Herrler, G. Proteolytic activation of respiratory syncytial virus fusion protein cleavage at two furin consensus sequences. J. Biol. Chem. 276, 31642–31650 (2001).
22. González-Reyes, L. et al. Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc. Natl. Acad. Sci. USA 98, 9859–9864 (2001).
23. Weissenhorn, W., Hinz, A. & Gaudin, Y. Virus membrane fusion. FEBS letters 581, 2150–2155 (2007).
24. Knappe, S., Wu, F., Masikat, M. R., Morser, J. & Wu, Q. Functional analysis of the transmembrane domain and activation cleavage of human corin design and characterization of a soluble corin. J. Biol. Chem. 278, 52363–52370 (2003).
25. Bosch, B. J., van der Zee, R., de Haan, C. A. & Rottier, P. J. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77, 8801–8811 (2003).
26. Zaitseva, E., Mittal, A., Griffin, D. E. & Chernomordik, L. V. Class II fusion protein of alphaviruses drives membrane fusion through the same pathway as class I proteins. J. Cell Biol. 169, 167–177 (2005)
27. Homma, M. & Ohuchi, M. Trypsin action on the growth of Sendai virus in tissue culture cells III. Structural difference of Sendai viruses grown in eggs and tissue culture cells. J. Virol. 12, 1457–1465 (1973).
28. Scheid, A. & Choppin, P. W. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity by proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology 57, 475–490 (1974).
29. Glickman, R. L., Syddall, R. J., Iorio, R. M., Sheehan, J. P. & Bratt, M. A. Quantitative basic residue requirements in the cleavage-activation site of the fusion glycoprotein as a determinant of virulence for Newcastle disease virus. J. Virol. 62, 354–356 (1988).
30. Nagai, Y., Klenk, H.-D. & Rott, R. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72, 494–508 (1976).
31. Morrison, T. G. Structure and function of a paramyxovirus fusion protein. Biochimica et Biophysica Acta (BBA)-Biomembranes 1614, 73–84 (2003).
32. Cseke, G. et al. Integrin αvβ1 promotes infection by human metapneumovirus. Proc. Natl. Acad. Sci. USA 106, 1566–1571 (2009).
33. Biacchesi, S. et al. Recovery of human metapneumovirus from cDNA: optimization of growth in vitro and expression of additional genes. Virology 321, 247–259 (2004).
34. Van den Hoogen, B. G. et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat. Med. 7, 719–724 (2001).
35. Peret, T. C. et al. Characterization of human metapneumoviruses isolated from patients in North America. J. Infect. Dis. 185, 1660–1663 (2002).
36. Deffrasnes, C., Côté, S. & Boivin, G. Analysis of replication kinetics of the human metapneumovirus in different cell lines by real-time PCR. J. Clin. Microbiol. 43, 488–490 (2005).
37. Hamelin, M.-È., Abed, Y. & Boivin, G. Human metapneumovirus: a new player among respiratory viruses. Clin. Infect. Dis. 38, 983–990 (2004).
38. Schowalter, R. M., Chang, A., Robach, J. G., Buchholz, U. J. & Dutch, R. E. Low-pH triggering of human metapneumovirus fusion: essential residues and importance in entry. J. Virol. 83, 1511–1522 (2009).
39. Herfst, S. et al. Low-pH-induced membrane fusion mediated by human metapneumovirus F protein is a rare, strain-dependent phenomenon. J. Virol. 82, 8891–8895 (2008).
40. Dimitrov, D. S. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2, 109–122 (2004).
41. Marsh, M. & Helenius, A. Virus entry: open sesame. Cell 124, 729–740 (2006).
42. Russell, C. J. & Luque, L. E. The structural basis of paramyxovirus invasion. Trends Microbiol. 14, 243–246 (2006).
43. Lamb, R. A. & Jardetzky, T. S. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17, 427–436 (2007).
44. Avitabile, E., Lombardi, G., Gianni, T., Capri, M. & Campadelli-Fiume, G. Coexpression of UL20p and gK inhibits cell-cell fusion mediated by herpes simplex virus glycoproteins gD, gH-gL, and wild-type gB or an endocytosis-defective gB mutant and downmodulates their cell surface expression. J. Virol. 78, 8015–8025 (2004).
45. Kinzler, E. R. & Compton, T. Characterization of human cytomegalovirus glycoprotein-induced cell-cell fusion. J. Virol. 79, 7827–7837 (2005).
46. Mirza, A. M. et al. Triggering of the Newcastle Disease Virus Fusion Protein by a Chimeric Attachment Protein That Binds to Nipah Virus Receptors. J. Biol. Chem. 286, 17851–17860 (2011).
47. Bissonnette, M. L. Z., Donald, J. E., DeGrado, W. F., Jardetzky, T. S. & Lamb, R. A. Functional Analysis of the Transmembrane Domain in Paramyxovirus F Protein-Mediated Membrane Fusion. J. Mol. Biol. 386, 14–36 (2009).
48. Lamb, R. A. Paramyxovirus fusion: a hypothesis for changes. Virology 197, 1–11 (1993).
49. Sergel, T., McGinnes, L. W., Peeples, M. E. & Morrison, T. G. The attachment function of the Newcastle disease virus hemagglutinin-neuraminidase protein can be separated from fusion promotion by mutation. Virology 193, 717–726 (1993).
50. Seth, S., Vincent, A. & Compans, R. Activation of fusion by the SER virus F protein: a low-pH-dependent paramyxovirus entry process. J. Virol. 77, 6520–6527 (2003).
51. Carneiro, F. A. et al. Membrane fusion induced by vesicular stomatitis virus depends on histidine protonation. J. Biol. Chem. 278, 13789–13794 (2003).
52. Wen, X. et al. Structure of the human metapneumovirus fusion protein with neutralizing antibody identifies a pneumovirus antigenic site. Nat. Struct. Mol. Biol. 19, 461–463 (2012).
53. de Graaf, M. et al. Fusion protein is the main determinant of metapneumovirus host tropism. J. Gen. Virol. 90, 1408–1416 (2009).
54. Kido, H., Niwa, Y., Beppu, Y. & Towatari, T. Cellular proteases involved in the pathogenicity of enveloped animal viruses, human immunodeficiency virus, influenza virus A and Sendai virus. Adv. Virus Res. 36, 325–347 (1996).
55. Toquin, D., de Boisseson, C., Beven, V., Senne, D. A. & Eterradossi, N. Subgroup C avian metapneumovirus (MPV) and the recently isolated human MPV exhibit a common organization but have extensive sequence divergence in their putative SH and G genes. J. Gen. Virol. 84, 2169–2178 (2003).
56. Wei, L. et al. Viral Replication and Lung Lesions in BALB/c Mice Experimentally Inoculated with Avian Metapneumovirus Subgroup C Isolated from Chickens. Plos One 9, e92136 (2014).
57. van den Hoogen, B. G., Bestebroer, T. M., Osterhaus, A. & Fouchier, R. A. M. Analysis of the genomic sequence of a human metapneumovirus. Virology 295, 119–132 (2002).
58. Yunus, A. S., Govindarajan, D., Huang, Z. H. & Samal, S. K. Deduced amino acid sequence of the small hydrophobic protein of US avian pneumovirus has greater identity with that of human metapneumovirus than those of non-US avian pneumoviruses. Virus Res. 93, 91–97 (2003).