Home LiteratureArticle Details
PMID: 10982335 Published · ppublish English Journal Article

Bovine parainfluenza virus type 3 (BPIV3) fusion and hemagglutinin-neuraminidase glycoproteins make an important contribution to the restricted replication of BPIV3 in primates.

Journal of virology ·Vol. 74 ·No. 19 ·2000-10-00 ·Pages 8922-9

Schmidt AC, McAuliffe JM, Huang A, Surman SR, Bailly JE, Elkins WR, Collins PL, Murphy BR, Skiadopoulos MH

Abstract

This study examines the contribution of the fusion (F) and hemagglutinin-neuraminidase (HN) glycoprotein genes of bovine parainfluenza virus type 3 (BPIV3) to its restricted replication in the respiratory tract of nonhuman primates. A chimeric recombinant human parainfluenza type 3 virus (HPIV3) containing BPIV3 F and HN glycoprotein genes in place of its own and the reciprocal recombinant consisting of BPIV3 bearing the HPIV3 F and HN genes (rBPIV3-F(H)HN(H)) were generated to assess the effect of glycoprotein substitution on replication of HPIV3 and BPIV3 in the upper and lower respiratory tract of rhesus monkeys. The chimeric viruses were readily recovered and replicated in simian LLC-MK2 cells to a level comparable to that of their parental viruses, suggesting that the heterologous glycoproteins were compatible with the PIV3 internal proteins. HPIV3 bearing the BPIV3 F and HN genes was restricted in replication in rhesus monkeys to a level similar to that of its BPIV3 parent virus, indicating that the glycoprotein genes of BPIV3 are major determinants of its host range restriction of replication in rhesus monkeys. rBPIV3-F(H)HN(H) replicated in rhesus monkeys to a level intermediate between that of HPIV3 and BPIV3. This observation indicates that the F and HN genes make a significant contribution to the overall attenuation of BPIV3 for rhesus monkeys. Furthermore, it shows that BPIV3 sequences outside the F and HN region also contribute to the attenuation phenotype in primates, a finding consistent with the previous demonstration that the nucleoprotein coding sequence of BPIV3 is a determinant of its attenuation for primates. Despite its restricted replication in the respiratory tract of rhesus monkeys, rBPIV3-F(H)HN(H) conferred a level of protection against challenge with HPIV3 that was indistinguishable from that induced by previous infection with wild-type HPIV3. The usefulness of rBPIV3-F(H)HN(H) as a vaccine candidate against HPIV3 and as a vector for other viral antigens is discussed.

MeSH Terms
Animals Cattle Cell Line HN Protein/physiology Humans Primates Respirovirus/physiology Viral Fusion Proteins/physiology Virus Replication
Chemicals
HN Protein Viral Fusion Proteins
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Schmidt A C
Laboratory of Infectious Disease, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892, USA. aschmidt@niaid.nih.gov
McAuliffe J M
Huang A
Surman S R
Bailly J E
Elkins W R
Collins P L
Murphy B R
Skiadopoulos M H
References (42)
42 references, click to expand
  1. Dose response of influenza A/Washington/897/80 (H3N2) avian-human reassortant virus in adult volunteers.
    J Infect Dis. 1985 Jul;152(1):225-9 PMID: 4008988
  2. Inhibition of the neuraminidase of paramyxoviruses by halide ions: a possible means of modulating the two activities of the HN protein.
    Virology. 1981 Jul 15;112(1):296-305 PMID: 6264686
  3. Evaluation of live avian-human reassortant influenza A H3N2 and H1N1 virus vaccines in seronegative adult volunteers.
    J Clin Microbiol. 1986 May;23(5):852-7 PMID: 3711273
  4. Conserved epitopes on the hemagglutinin-neuraminidase proteins of human and bovine parainfluenza type 3 viruses: nucleotide sequence analysis of variants selected with monoclonal antibodies.
    J Virol. 1986 Oct;60(1):90-6 PMID: 2427750
  5. Single gene substitution rotavirus reassortants containing the major neutralization protein (VP7) of human rotavirus serotype 4.
    J Clin Microbiol. 1986 Nov;24(5):822-6 PMID: 3021814
  6. Quantitative basic residue requirements in the cleavage-activation site of the fusion glycoprotein as a determinant of virulence for Newcastle disease virus.
    J Virol. 1988 Jan;62(1):354-6 PMID: 3275436
  7. Attenuation of bovine parainfluenza virus type 3 in nonhuman primates and its ability to confer immunity to human parainfluenza virus type 3 challenge.
    J Infect Dis. 1988 Apr;157(4):655-62 PMID: 2831282
  8. Comparison of the virologic and immunologic responses of volunteers to live avian-human influenza A H3N2 reassortant virus vaccines derived from two different avian influenza virus donors.
    J Clin Microbiol. 1989 Jan;27(1):219-22 PMID: 2913033
  9. Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3273-89 PMID: 2557352
  10. Antigenic variation of human and bovine parainfluenza virus type 3 strains.
    J Gen Virol. 1990 Jul;71 ( Pt 7):1577-80 PMID: 1695673
  11. Evaluation of bovine, cold-adapted human, and wild-type human parainfluenza type 3 viruses in adult volunteers and in chimpanzees.
    J Clin Microbiol. 1991 Jun;29(6):1175-82 PMID: 1650789
  12. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses.
    J Virol. 1992 Mar;66(3):1528-34 PMID: 1310764
  13. Use of single-gene reassortant viruses to study the role of avian influenza A virus genes in attenuation of wild-type human influenza A virus for squirrel monkeys and adult human volunteers.
    J Clin Microbiol. 1992 Mar;30(3):655-62 PMID: 1551982
  14. Cold-passaged human parainfluenza type 3 viruses contain ts and non-ts mutations leading to attenuation in rhesus monkeys.
    Virus Res. 1992 Mar;22(3):173-84 PMID: 1320790
  15. A mutant CHO-K1 strain with resistance to Pseudomonas exotoxin A is unable to process the precursor fusion glycoprotein of Newcastle disease virus.
    J Virol. 1993 Jan;67(1):593-5 PMID: 8416387
  16. An update on the "Jennerian" and modified "Jennerian" approach to vaccination of infants and young children against rotavirus diarrhea.
    Adv Exp Med Biol. 1992;327:59-69 PMID: 1295353
  17. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates.
    Virology. 1994 Nov 15;205(1):17-23 PMID: 7975212
  18. Pneumotropism of Sendai virus in relation to protease-mediated activation in mouse lungs.
    Infect Immun. 1983 Feb;39(2):879-88 PMID: 6299951
  19. Recovery of infectious human parainfluenza virus type 3 from cDNA.
    Virology. 1997 Sep 1;235(2):323-32 PMID: 9281512
  20. Molecular basis for the generation in pigs of influenza A viruses with pandemic potential.
    J Virol. 1998 Sep;72(9):7367-73 PMID: 9696833
  21. Influence of host species on the evolution of the nonstructural (NS) gene of influenza A viruses.
    Virus Res. 1998 Jun;55(2):143-56 PMID: 9725667
  22. A live attenuated chimeric recombinant parainfluenza virus (PIV) encoding the internal proteins of PIV type 3 and the surface glycoproteins of PIV type 1 induces complete resistance to PIV1 challenge and partial resistance to PIV3 challenge.
    Vaccine. 1999 Mar 5;17(9-10):1100-8 PMID: 10195620
  23. Comparison of the immunogenicity and efficacy of a replication-defective vaccinia virus expressing antigens of human parainfluenza virus type 3 (HPIV3) with those of a live attenuated HPIV3 vaccine candidate in rhesus monkeys passively immunized with PIV3 antibodies.
    J Infect Dis. 1999 Jun;179(6):1345-51 PMID: 10228053
  24. Safety and immunogenicity of live attenuated human-bovine (UK) reassortant rotavirus vaccines with VP7-specificity for serotypes 1, 2, 3 or 4 in adults, children and infants.
    Vaccine. 1999 Jun 4;17(20-21):2715-25 PMID: 10418923
  25. Mutations in the C, D, and V open reading frames of human parainfluenza virus type 3 attenuate replication in rodents and primates.
    Virology. 1999 Sep 1;261(2):319-30 PMID: 10497117
  26. A live attenuated bovine parainfluenza virus type 3 vaccine is safe, infectious, immunogenic, and phenotypically stable in infants and children.
    J Infect Dis. 1995 May;171(5):1107-14 PMID: 7751684
  27. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike.
    Virology. 1995 Jun 1;209(2):457-69 PMID: 7778280
  28. Interaction of Sendai viral F, HN, and M proteins with host cytoskeletal and lipid components in Sendai virus-infected BHK cells.
    Virology. 1995 Jun 1;209(2):701-7 PMID: 7778306
  29. Replication-deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells.
    Virology. 1995 Jun 20;210(1):202-5 PMID: 7793072
  30. Current approaches to the development of vaccines against disease caused by respiratory syncytial virus (RSV) and parainfluenza virus (PIV). A meeting report of the WHO Programme for Vaccine Development.
    Vaccine. 1995 Mar;13(4):415-21 PMID: 7793140
  31. Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses.
    Virus Res. 1995 Apr;36(1):107-18 PMID: 7625123
  32. A live human parainfluenza type 3 virus vaccine is attenuated and immunogenic in healthy infants and children.
    J Infect Dis. 1995 Dec;172(6):1445-50 PMID: 7594701
  33. A simian strain of hepatitis A virus, AGM-27, functions as an attenuated vaccine for chimpanzees.
    J Infect Dis. 1996 Mar;173(3):592-7 PMID: 8627022
  34. Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion.
    J Virol. 1996 Sep;70(9):6112-8 PMID: 8709235
  35. Molecular evolution of influenza viruses.
    Virus Genes. 1995;11(2-3):209-15 PMID: 8828147
  36. Evaluation of a live attenuated bovine parainfluenza type 3 vaccine in two- to six-month-old infants.
    Pediatr Infect Dis J. 1996 Aug;15(8):650-4 PMID: 8858666
  37. Intranasal Sendai virus vaccine protects African green monkeys from infection with human parainfluenza virus-type one.
    Vaccine. 1997 Apr;15(5):533-40 PMID: 9160521
  38. Chimeric bovine respiratory syncytial virus with glycoprotein gene substitutions from human respiratory syncytial virus (HRSV): effects on host range and evaluation as a live-attenuated HRSV vaccine.
    J Virol. 2000 Feb;74(3):1187-99 PMID: 10627529
  39. A recombinant human parainfluenza virus type 3 (PIV3) in which the nucleocapsid N protein has been replaced by that of bovine PIV3 is attenuated in primates.
    J Virol. 2000 Apr;74(7):3188-95 PMID: 10708435
  40. Sequence determination and molecular analysis of two strains of bovine parainfluenza virus type 3 that are attenuated for primates.
    Virus Genes. 2000;20(2):173-82 PMID: 10872880
  41. Human parainfluenza virus type 3 (PIV3) expressing the hemagglutinin protein of measles virus provides a potential method for immunization against measles virus and PIV3 in early infancy.
    J Virol. 2000 Aug;74(15):6821-31 PMID: 10888621
  42. The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses.
    Virology. 1985 Dec;147(2):287-94 PMID: 2416114
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2000-10-00
Pages
8922-9
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC102087
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com