Characterization of a persistent respiratory syncytial virus showing a low-fusogenic activity associated to an impaired F protein

Virus Research

Volumn 139, Issue 1, 2009, Pages 39-47

  Sarmiento, R E ^a   Arias, C F ^b   Mendez E ^b   Gomez B ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Fusogenic activity; Persistence; Respiratory syncytial virus

Indexed keywords

FURIN; PROTEINASE; TRYPSIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FUSION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; STRAIN DIFFERENCE; VERO CELL; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL FUSION; CELL LINE; CELL LINE, TUMOR; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; GIANT CELLS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RESPIRATORY SYNCYTIAL VIRUSES; SEQUENCE ALIGNMENT; TRYPSIN; VERO CELLS; VIRAL FUSION PROTEINS; VIRUS ACTIVATION;

MURINAE; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 57749086721     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2008.10.007     Document Type: Article

References (57)

1. Bangham C.R., and McMichael A.J. Specific human cytotoxic T cells recognize B-cell lines persistently infected with respiratory syncytial virus. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 9183-9187
2. Baker K.A., Dutch R.E., Lamb R.A., and Jardetzky T.S. Structural basis for paramyxovirus-mediated membrane fusion. Mol. Cell. 3 (1999) 309-319
3. Boggs W.M., Hahn C.S., Strauss E.G., Strauss J.H., and Griffin D.E. Low pH-dependent Sindbis virus-induced fusion of BHK cells: differences between strains correlate with amino acid changes in the E1 glycoprotein. Virology 169 (1989) 485-488
4. Bolt G., Pedersen L.O., and Birkeslund H.H. Cleavage of the respiratory syncytial virus fusion protein is required for its surface expression: role of furin. Virus. Res. 68 (2000) 25-33
5. Bramley A.M., Vitalis T.Z., Wiggs B.R., and Hegele R.G. Effects of respiratory syncytial virus persistence on airway responsiveness and inflammation in guinea-pigs. Eur. Respir. J. 14 (1999) 1061-1067
6. Chen L., Gorman J.J., McKimm-Breschkin J., Lawrence L.J., Tulloch P.A., Smith B.J., Colman P.M., and Lawrence M.C. The structure of the fusion glycoprotein of Newcastle disease virus suggests a novel paradigm for the molecular mechanism of membrane fusion. Structure 9 (2001) 255-266
7. Collins P.L., and Mottet G. Post-translational processing and oligomerization of the fusion glycoprotein of human respiratory syncytial virus. J. Gen. Virol. 72 (1991) 3095-3101
8. Collins P.L., and Crowe J.E. Respiratory syncytial virus and Metaneumovirus. In: Knipe D.M., and Howley P.M. (Eds). Fields Virology. 5th edition (2007), Lippincott Williams and Wilkins, Philadelphia 1601-1646
9. Connolly S.A., Leser G.P., Yin H.S., Jardetzky T.S., and Lamb R.A. Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 17903-17908
10. Cubie H.A., Duncan L.A., Marshall L.A., and Smith N.M. Detection of respiratory syncytial virus nucleic acid in archival postmortem tissue from infants. Pediatr. Pathol. Lab. Med. 17 (1997) 927-938
11. Day N.D., Branigan P.J., Liu C., Gutshall L.L., Luo J., Melero J.A., Sarisky R.T., and Del Vecchio A.M. Contribution of cysteine residues in the extracellular domain of the F protein of human respiratory syncytial virus to its function. Virol. J. 3 (2006) 34
12. Dutch R.E., Hagglund R.N., Nagel M.A., Paterson R.G., and Lamb R.A. Paramyxovirus fusion (F) protein: a conformational change on cleavage activation. Virology 281 (2001) 138-150
13. Ebbert J.O., and Limper A.H. Respiratory syncytial virus pneumonitis in immunocompromised adults: clinical features and outcome. Respiration 72 (2005) 263-269
14. Falsey A.R., Hennerssey P.A., Formica M.A., Cox C., and Walsh E.E. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352 (2005) 1749-1759
15. Fernie B.F., Ford E.C., and Gerin J.L. The development of Balb/c cells persistently infected with respiratory syncytial virus: presence of ribonucleoprotein on the cell surface. Proc. Soc. Exp. Biol. Med. 167 (1981) 83-86
16. Fujinami R.S., and Oldstone M.B. Failure to cleave measles virus fusion protein in lymphoid cells. J. Exp. Med. 154 (1981) 1489-1499
17. Gardner A.E., Martin K.L., and Dutch R.E. A conserved region between the heptad repeats of paramyxovirus fusion proteins is critical for proper F protein folding. Biochemistry 46 (2007) 5094-5105
18. Glomb-Reinmund S., and Kielian M. fus-1, a pH shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 72 (1998) 4281-4287
19. Gonzalez-Reyes L., Ruiz-Arguello M.B., Garcia-Barreno B., Calder L., Lopez J.A., Albar J.P., Skehel J.J., Wiley D.C., and Melero J.A. Cleavage of the human respiratory syncytial virus fusion protein at two distinct sites is required for activation of membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 9859-9864
20. Hall C.B., Hall W.J., Gala C.L., MaGill F.B., and Leddy J.P. Long term prospective study in children after respiratory syncytial virus infection. J. Pediatr. 105 (1984) 358-364
21. Hegele R.G., Hayashi S., Bramley A.M., and Hogg J.C. Persistence of respiratory syncytial virus genome and protein after acute bronchiolitis in guinea pigs. Chest 105 (1994) 1848-1854
22. Hilleman M.R. Strategies and mechanisms for host and pathogen survival in acute and persistent viral infections. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 14560-15566
23. Isaia G., Teodosiu O., Popescu G., Athanasiu P., Sternberg I., and Dumitriu Z. Persistence of viruses in the nasopharynx of apparently healthy children aged 0-5 years. Results of investigations performed in 1982-1983. Virologie 36 (1985) 175-179
24. Klenk H.D., and Garten W. Host cell proteases controlling virus pathogenicity. Trends Microbiol. 2 (1994) 39-43
25. Lawless-Delmedico M.K., Sista P., Sen R., Moore N.C., Antczak J.B., White J.M., Greene R.J., Leanza K.C., Matthews T.J., and Lambert D.M. Heptad-repeat regions of respiratory syncytial virus F1 protein form a six-membered coiled-coil complex. Biochemistry 39 (2000) 11684-11695
26. Lopez J.A., Bustos R., Orvell C., Berois M., Arbiza J., Garcia-Barreno B., and Melero J.A. Antigenic structure of human respiratory syncytial virus fusion glycoprotein. J. Virol. 72 (1998) 6922-6928
27. Matthews J.M., Young T.F., Tucker S.P., and Mackay J.P. The core of the respiratory syncytial virus fusion protein is a trimeric coiled coil. J. Virol. 74 (2000) 5911-5920
28. Martin D., Calder L.J., Garcia-Barreno B., Skehel J.J., and Melero J.A. Sequence elements of the fusion peptide of human respiratory syncytial virus fusion protein required for activity. J. Gen. Virol. 87 (2006) 1649-1658
29. Meertens N., Stoffel M.H., Cherpillod P., Wittek R., Vandevelde M., and Zurbriggen A. Mechanism of reduction of virus release and cell-cell fusion in persistent canine distemper virus infection. Acta Neuropathol. 106 (2003) 303-310
30. Mejias A., Chavez-Bueno S., Jafri H.S., and Ramilo O. Respiratory syncytial virus infections: old challenges and new opportunities. Pediatr. Infect. Dis. J. 24 (2005) 189-196
31. Mohapatra S.S., and Boyapalle S. Epidemiologic, experimental, and clinical links between respiratory syncytial virus infection and asthma. Clin. Microbiol. Rev. 21 3 (2008) 495-504
32. Nagai Y., Klenk H.D., and Rott R. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72 (1976) 494-508
33. Oldstone M.B. Viral persistence: parameters, mechanisms and future predictions. Virology 344 (2006) 111-118
34. Openshaw P.J., Yamaguchi Y., and Tregoning J.S. Childhood infections, the developing immune system, and the origins of asthma. J. Allergy. Clin. Immunol. 114 (2004) 1275-1277
35. Pastey M.K., Crow J.E., and Graham B.S. RhoA interacts with the fusion glycoprotein of respiratory syncytial virus and facilitates virus-induced syncytium formation. J. Virol. 73 (1999) 7262-7270
36. Plattet P., Rivals J.P., Zuber B., Brunner J.M., Zurbriggen A., and Wittek R. The fusion protein of wild-type canine distemper virus is a major determinant of persistent infection. Virology 337 (2005) 312-326
37. Romero V.M., and Gomez B. Establishment of respiratory syncytial virus persistence in cell lines: association with defective interfering particles. Intervirology 46 (2003) 190-198
38. Sarmiento R.E., Tirado R., and Gomez B. Characteristics of a respiratory syncytial virus persistently infected macrophage-like culture. Virus Res. 84 (2002) 45-58
39. Schowalter R.M., Smith S.E., and Dutch R.E. Characterization of human metapneumovirus F protein-promoted membrane fusion: critical roles for proteolytic processing and low pH. J. Virol. 80 (2006) 10931-10941
40. Schwarze J., O'Donnell D.R., Rohwedder A., and Openshaw P.J. Latency and persistence of respiratory syncytial virus despite T cell immunity. Am. J. Respir. Crit. Care Med. 169 (2004) 801-805
41. Scott P.D., Ochola R., Ngama M., Okiro E.A., James Nokes D., Medley G.F., and Cane P.A. Molecular analysis of respiratory syncytial virus reinfections in infants from coastal Kenya. J. Infect. Dis. 193 (2006) 59-67
42. Sergel T., and Morrison T.G. Mutations in the cytoplasmic domain of the fusion glycoprotein of Newcastle disease virus depress syncytia formation. Virology 210 (1995) 264-272
43. Seth S., Vincent A., and Compans R.W. Activation of fusion by the SER virus F protein: a low-pH-dependent paramyxovirus entry process. J. Virol. 77 11 (2003) 6520-6527
44. Sigurs N., Bjarnason R., Sigurbergsson F., and Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am. J. Respir. Crit. Care Med. 161 (2000) 150-157
45. Skehel J.J., and Wiley D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69 (2000) 531-569
46. Smith B.J., Lawrence M.C., and Colman P.M. Modelling the structure of the fusion protein from human respiratory syncytial virus. Protein Eng. 15 (2002) 365-371
47. Sugrue R.J., Brown C., Brown G., Aitken J., and McL Rixon H.W. Furin cleavage of the respiratory syncytial virus fusion protein is not a requirement for its transport to the surface of virus-infected cells. J. Gen. Virol. 82 (2001) 1375-1386
48. Sutton T.C., Tayyari F., Khan M.A., Manson H.E., and Hegele R.G. T helper 1 background protects against airway hyperresponsiveness and inflammation in guinea pigs with persistent respiratory syncytial virus infection. Pediatr. Res. 61 (2007) 525-529
49. Tirado R., Ortega A., Sarmiento R.E., and Gómez B. Interleukin-8 mRNA synthesis and protein secretion are continuously up-regulated by respiratory syncytial virus persistently infected cells. Cell. Immunol. 233 (2005) 61-71
50. Tripp R.A. The brume surrounding respiratory syncytial virus persistence. Am. J. Respir. Crit. Care Med. 169 (2004) 778-779
51. Valarcher J.F., Bourhy H., Lavenu A., Bourges-Abella N., Roth M., Andreoletti O., Ave P., and Schelcher F. Persistent infection of B lymphocytes by bovine respiratory syncytial virus. Virology 291 (2001) 55-67
52. Wang S.Z., Rosenberger C.L., Bao Y.X., Stark J.M., and Harrod K.S. Clara cell secretory protein modulates lung inflammatory and immune responses to respiratory syncytial virus infection. J. Immunol. 171 (2003) 1051-1060
53. Wiener D., Plattet P., Cherpillod P., Zipperle L., Doherr M.G., Vandevelde M., and Zurbriggen A. Synergistic inhibition in cell-cell fusion mediated by the matrix and nucleocapsid protein of canine distemper virus. Virus Res. 129 (2007) 145-154
54. Wilkinson T.M., Donaldson G.C., Johnston S.L., Openshaw P.J., and Wedzicha J.A. Respiratory syncytial virus, airway inflammation and FEV1 decline in patients with COPD. Am. J. Respir. Crit. Care Med. 173 (2006) 871-876
55. Yang D., Hwang D., Qiu Z., and Gillam S. Effects of mutations in the rubella virus E1 glycoprotein on E1-E2 interaction and membrane fusion activity. J. Virol. 72 (1998) 8747-8755
56. Zimmer G., Budz L., and Herrler G. Proteolytic activation of respiratory syncytial virus fusion protein: cleavage at two furin consensus sequences. J. Biol. Chem. 276 (2001) 31642-31650
57. Zimmer G., Trotz I., and Herrler G. N-glycans of F protein differentially affect fusion activity of human respiratory syncytial virus. J. Virol. 75 (2001) 4744-4751