Home LiteratureArticle Details
PMID: 8411379 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Mutations in the cytoplasmic tail of influenza A virus neuraminidase affect incorporation into virions.

Journal of virology ·Vol. 67 ·No. 11 ·1993-11-00 ·Pages 6762-7

Bilsel P, Castrucci MR, Kawaoka Y

Abstract

The significance of the conserved cytoplasmic tail sequence of influenza A virus neuraminidase (NA) was analyzed by the recently developed reverse genetics technique (W. Luytjes, M. Krystal, M. Enami, J. D. Parvin, and P. Palese, Cell 59:1107-1113, 1989). A chimeric influenza virus A/WSN/33 NA containing the influenza B virus cytoplasmic tail rescued influenza A virus infectivity. The transfectant virus had less NA incorporated into virions than A/WSN/33, indicating that the cytoplasmic tail of influenza virus NA plays a role in incorporation of NA into virions. However, these results also suggest that the influenza A virus and influenza B virus cytoplasmic tail sequences share common features that lead to the production of infectious virus. Transfectant virus was obtained with all cytoplasmic tail mutants generated by site-directed mutagenesis of the influenza A virus tail, except for the mutant resulting from substitution of the conserved proline residue, presumably because of its contribution to the secondary structure of the tail. No virus was rescued when the cytoplasmic tail was deleted, indicating that the cytoplasmic tail is essential for production of the virus. The virulence of the transfectant viruses in mice was directly proportional to the amount of NA incorporated. The importance of the NA cytoplasmic tail in virus assembly and virulence has implications for use in developing antiviral strategies.

MeSH Terms
Amino Acid Sequence Animals Cell Membrane/metabolism Cytoplasm DNA Mutational Analysis Influenza A virus/chemistry,genetics,ultrastructure Influenza B virus/chemistry,genetics,ultrastructure Mice Molecular Sequence Data Neuraminidase/chemistry,genetics,ultrastructure Recombinant Fusion Proteins Structure-Activity Relationship Transfection Virion/metabolism
Chemicals
Recombinant Fusion Proteins Neuraminidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bilsel P
Department of Virology and Molecular Biology, St. Jude Children's Research Hospital, Memphis, Tennessee 38101-0318.
Castrucci M R
Kawaoka Y
References (42)
42 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. A viral protease-mediated cleavage of the transmembrane glycoprotein of Mason-Pfizer monkey virus can be suppressed by mutations within the matrix protein.
    Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3443-7 PMID: 1565636
  3. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase.
    Virology. 1974 Oct;61(2):397-410 PMID: 4472498
  4. Neurovirulence of influenza virus in mice. I. Neurovirulence of recombinants between virulent and avirulent virus strains.
    Virology. 1980 Mar;101(2):440-9 PMID: 7361453
  5. Complete nucleotide sequence of the neuraminidase gene of influenza B virus.
    Proc Natl Acad Sci U S A. 1982 Nov;79(22):6817-21 PMID: 6294654
  6. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution.
    Nature. 1983 May 5-11;303(5912):35-40 PMID: 6843658
  7. Rous sarcoma virus p19 and gp35 can be chemically crosslinked to high molecular weight complexes. An insight into virus assembly.
    J Mol Biol. 1984 Apr 5;174(2):297-317 PMID: 6325711
  8. NH2-terminal hydrophobic region of influenza virus neuraminidase provides the signal function in translocation.
    Proc Natl Acad Sci U S A. 1984 Apr;81(8):2327-31 PMID: 6326121
  9. The complete nucleotide sequence of the influenza virus neuraminidase gene of A/NJ/8/76 strain and its evolution by segmental duplication and deletion.
    Mol Biol Med. 1983 Nov;1(4):401-13 PMID: 6094954
  10. Structure and diversity of influenza virus neuraminidase.
    Curr Top Microbiol Immunol. 1985;114:177-255 PMID: 2581739
  11. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122-6 PMID: 3095828
  12. Formation of influenza virus particles lacking hemagglutinin on the viral envelope.
    J Virol. 1986 Dec;60(3):994-1001 PMID: 3783822
  13. Mutational analysis of the signal-anchor domain of influenza virus neuraminidase.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):1-5 PMID: 3025850
  14. Three-dimensional structure of a complex of antibody with influenza virus neuraminidase.
    Nature. 1987 Mar 26-Apr 1;326(6111):358-63 PMID: 2436051
  15. Mutants of the Rous sarcoma virus envelope glycoprotein that lack the transmembrane anchor and cytoplasmic domains: analysis of intracellular transport and assembly into virions.
    J Virol. 1987 Oct;61(10):2981-8 PMID: 3041017
  16. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Methods Enzymol. 1987;154:367-82 PMID: 3323813
  17. Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant.
    J Virol. 1989 Sep;63(9):3569-78 PMID: 2547986
  18. Promoter analysis of influenza virus RNA polymerase.
    J Virol. 1989 Dec;63(12):5142-52 PMID: 2585601
  19. Amplification, expression, and packaging of foreign gene by influenza virus.
    Cell. 1989 Dec 22;59(6):1107-13 PMID: 2598262
  20. The neuraminidase of influenza virus.
    Proteins. 1989;6(4):341-56 PMID: 2482974
  21. Conversion of a class II integral membrane protein into a soluble and efficiently secreted protein: multiple intracellular and extracellular oligomeric and conformational forms.
    J Cell Biol. 1990 Apr;110(4):999-1011 PMID: 2324203
  22. Replication and amplification of defective interfering particle RNAs of vesicular stomatitis virus in cells expressing viral proteins from vectors containing cloned cDNAs.
    J Virol. 1990 Jun;64(6):2948-57 PMID: 2159555
  23. Introduction of site-specific mutations into the genome of influenza virus.
    Proc Natl Acad Sci U S A. 1990 May;87(10):3802-5 PMID: 2339122
  24. Oligomers of the cytoplasmic domain of the p62/E2 membrane protein of Semliki Forest virus bind to the nucleocapsid in vitro.
    J Virol. 1990 Oct;64(10):4678-83 PMID: 2398527
  25. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins.
    J Virol. 1992 Jun;66(6):3306-15 PMID: 1583717
  26. Attenuation of influenza A virus by insertion of a foreign epitope into the neuraminidase.
    J Virol. 1992 Aug;66(8):4647-53 PMID: 1378505
  27. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity.
    J Virol. 1992 Nov;66(11):6616-25 PMID: 1357190
  28. Selection and characterization of a neuraminidase-minus mutant of influenza virus and its rescue by cloned neuraminidase genes.
    Virology. 1993 May;194(1):403-7 PMID: 8480427
  29. Basis for selective incorporation of glycoproteins into the influenza virus envelope.
    J Virol. 1993 Aug;67(8):4831-41 PMID: 8392617
  30. High-efficiency formation of influenza virus transfectants.
    J Virol. 1991 May;65(5):2711-3 PMID: 2016777
  31. Cell surface transport, oligomerization, and endocytosis of chimeric type II glycoproteins: role of cytoplasmic and anchor domains.
    Mol Cell Biol. 1991 May;11(5):2675-85 PMID: 1826760
  32. An influenza A virus containing influenza B virus 5' and 3' noncoding regions on the neuraminidase gene is attenuated in mice.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5177-81 PMID: 2052599
  33. Site-directed mutations in Sindbis virus E2 glycoprotein's cytoplasmic domain and the 6K protein lead to similar defects in virus assembly and budding.
    Virology. 1991 Jul;183(1):206-14 PMID: 1647069
  34. Rescue of a foreign gene by Sendai virus.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5537-41 PMID: 1648220
  35. Transfer of the hemagglutinin activity of influenza virus neuraminidase subtype N9 into an N2 neuraminidase background.
    Virology. 1991 Aug;183(2):496-504 PMID: 1853557
  36. Inhibition of influenza virus formation by a peptide that corresponds to sequences in the cytoplasmic domain of the hemagglutinin.
    Virology. 1991 Aug;183(2):769-72 PMID: 1853575
  37. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import.
    Cell. 1991 Oct 4;67(1):117-30 PMID: 1913813
  38. An influenza virus containing nine different RNA segments.
    Virology. 1991 Nov;185(1):291-8 PMID: 1833874
  39. Rescue of synthetic analogs of respiratory syncytial virus genomic RNA and effect of truncations and mutations on the expression of a foreign reporter gene.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9663-7 PMID: 1946383
  40. Subunit interactions of vesicular stomatitis virus envelope glycoprotein stabilized by binding to viral matrix protein.
    J Virol. 1992 Jan;66(1):349-58 PMID: 1309251
  41. Alterations to influenza virus hemagglutinin cytoplasmic tail modulate virus infectivity.
    J Virol. 1992 Feb;66(2):790-803 PMID: 1309913
  42. Influenzavirus neuraminidase and neuraminidase-inhibition test procedures.
    Bull World Health Organ. 1973;48(2):199-202 PMID: 4541685
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1993-11-00
Pages
6762-7
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC238117
Subset
IM
Grants
NCI NIH HHS · 5-T32-CA09346 · United States
NIAID NIH HHS · AI-29599 · United States
NCI NIH HHS · CA-21765 · United States
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