Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1987 Apr 10;15(7):2927–2944. doi: 10.1093/nar/15.7.2927

Nucleotide sequence of the bovine parainfluenza 3 virus genome: its 3' end and the genes of NP, P, C and M proteins.

Y Sakai, S Suzu, T Shioda, H Shibuta
PMCID: PMC340707  PMID: 3031614

Abstract

We present the nucleotide sequence of bovine parainfluenza 3 virus (BPIV3) genome from its 3' end to the opening region of the F gene, through the NP, P plus C, and M genes. Comparison of the sequence with those reported for other paramyxoviruses indicated that BPIV3 was most similar to human parainfluenza 3 virus (HPIV3), and also very similar to Sendai virus in the structural make-up of its genome and the amino acid sequences of its gene products, suggesting that these three viruses constitute a paramyxovirus subgroup from which Newcastle disease and measles viruses are separable. In BPIV3 and Sendai virus, the NP and M proteins, the main structural elements, were more highly conserved than the functionally important P and C proteins. This tendency was also observed even in BPIV3 and HPIV3. Virus-specific amino acid sequences of the NP and M proteins were found at the carboxyl and amino terminal regions, respectively. BPIV3 M mRNA was found to have aberrations in its poly A attachment site.

Full text

PDF
2927

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ABINANTI F. R., CHANOCK R. M., COOK M. K., WONG D., WARFIELD M. Relationship of human and bovine strains of myxovirus para-influenza 3. Proc Soc Exp Biol Med. 1961 Mar;106:466–469. doi: 10.3181/00379727-106-26371. [DOI] [PubMed] [Google Scholar]
  2. Bellini W. J., Englund G., Richardson C. D., Rozenblatt S., Lazzarini R. A. Matrix genes of measles virus and canine distemper virus: cloning, nucleotide sequences, and deduced amino acid sequences. J Virol. 1986 May;58(2):408–416. doi: 10.1128/jvi.58.2.408-416.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bellini W. J., Englund G., Rozenblatt S., Arnheiter H., Richardson C. D. Measles virus P gene codes for two proteins. J Virol. 1985 Mar;53(3):908–919. doi: 10.1128/jvi.53.3.908-919.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Billeter M. A., Baczko K., Schmid A., Ter Meulen V. Cloning of DNA corresponding to four different measles virus genomic regions. Virology. 1984 Jan 15;132(1):147–159. doi: 10.1016/0042-6822(84)90099-0. [DOI] [PubMed] [Google Scholar]
  5. Blumberg B. M., Giorgi C., Rose K., Kolakofsky D. Preparation and analysis of the nucleocapsid proteins of vesicular stomatitis virus and sendai virus, and analysis of the sendai virus leader-NP gene region. J Gen Virol. 1984 Apr;65(Pt 4):769–779. doi: 10.1099/0022-1317-65-4-769. [DOI] [PubMed] [Google Scholar]
  6. Blumberg B. M., Giorgi C., Rose K., Kolakofsky D. Sequence determination of the Sendai virus fusion protein gene. J Gen Virol. 1985 Feb;66(Pt 2):317–331. doi: 10.1099/0022-1317-66-2-317. [DOI] [PubMed] [Google Scholar]
  7. Blumberg B. M., Rose K., Simona M. G., Roux L., Giorgi C., Kolakofsky D. Analysis of the Sendai virus M gene and protein. J Virol. 1984 Nov;52(2):656–663. doi: 10.1128/jvi.52.2.656-663.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blumberg B., Giorgi C., Roux L., Raju R., Dowling P., Chollet A., Kolakofsky D. Sequence determination of the Sendai virus HN gene and its comparison to the influenza virus glycoproteins. Cell. 1985 May;41(1):269–278. doi: 10.1016/0092-8674(85)90080-7. [DOI] [PubMed] [Google Scholar]
  9. Bolivar F., Backman K. Plasmids of Escherichia coli as cloning vectors. Methods Enzymol. 1979;68:245–267. doi: 10.1016/0076-6879(79)68018-7. [DOI] [PubMed] [Google Scholar]
  10. Chambers P., Millar N. S., Bingham R. W., Emmerson P. T. Molecular cloning of complementary DNA to Newcastle disease virus, and nucleotide sequence analysis of the junction between the genes encoding the haemagglutinin-neuraminidase and the large protein. J Gen Virol. 1986 Mar;67(Pt 3):475–486. doi: 10.1099/0022-1317-67-3-475. [DOI] [PubMed] [Google Scholar]
  11. Chambers P., Millar N. S., Platt S. G., Emmerson P. T. Nucleotide sequence of the gene encoding the matrix protein of Newcastle disease virus. Nucleic Acids Res. 1986 Nov 25;14(22):9051–9061. doi: 10.1093/nar/14.22.9051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  13. Curran J. A., Richardson C., Kolakofsky D. Ribosomal initiation at alternate AUGs on the Sendai virus P/C mRNA. J Virol. 1986 Feb;57(2):684–687. doi: 10.1128/jvi.57.2.684-687.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dimock K., Rud E. W., Kang C. Y. 3'-Terminal sequence of human parainfluenza virus 3 genomic RNA. Nucleic Acids Res. 1986 Jun 11;14(11):4694–4694. doi: 10.1093/nar/14.11.4694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dowling P. C., Giorgi C., Roux L., Dethlefsen L. A., Galantowicz M. E., Blumberg B. M., Kolakofsky D. Molecular cloning of the 3'-proximal third of Sendai virus genome. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5213–5216. doi: 10.1073/pnas.80.17.5213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Elango N., Coligan J. E., Jambou R. C., Venkatesan S. Human parainfluenza type 3 virus hemagglutinin-neuraminidase glycoprotein: nucleotide sequence of mRNA and limited amino acid sequence of the purified protein. J Virol. 1986 Feb;57(2):481–489. doi: 10.1128/jvi.57.2.481-489.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fischman H. R., Bang F. B. Antigenic relationship of the human and bovine parainfluenza 3 viruses using the Ouchterlony technique. Proc Soc Exp Biol Med. 1966 Mar;121(3):966–970. doi: 10.3181/00379727-121-30938. [DOI] [PubMed] [Google Scholar]
  18. Galinski M. S., Mink M. A., Lambert D. M., Wechsler S. L., Pons M. W. Molecular cloning and sequence analysis of the human parainfluenza 3 virus RNA encoding the nucleocapsid protein. Virology. 1986 Mar;149(2):139–151. doi: 10.1016/0042-6822(86)90116-9. [DOI] [PubMed] [Google Scholar]
  19. Gill D. S., Chattopadhyay D., Banerjee A. K. Identification of a domain within the phosphoprotein of vesicular stomatitis virus that is essential for transcription in vitro. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8873–8877. doi: 10.1073/pnas.83.23.8873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Giorgi C., Blumberg B. M., Kolakofsky D. Sendai virus contains overlapping genes expressed from a single mRNA. Cell. 1983 Dec;35(3 Pt 2):829–836. doi: 10.1016/0092-8674(83)90115-0. [DOI] [PubMed] [Google Scholar]
  21. Gupta K. C., Kingsbury D. W. Complete sequences of the intergenic and mRNA start signals in the Sendai virus genome: homologies with the genome of vesicular stomatitis virus. Nucleic Acids Res. 1984 May 11;12(9):3829–3841. doi: 10.1093/nar/12.9.3829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hidaka Y., Kanda T., Iwasaki K., Nomoto A., Shioda T., Shibuta H. Nucleotide sequence of a Sendai virus genome region covering the entire M gene and the 3' proximal 1013 nucleotides of the F gene. Nucleic Acids Res. 1984 Nov 12;12(21):7965–7973. doi: 10.1093/nar/12.21.7965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hsu M., Choppin P. W. Analysis of Sendai virus mRNAs with cDNA clones of viral genes and sequences of biologically important regions of the fusion protein. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7732–7736. doi: 10.1073/pnas.81.24.7732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ishida N., Taira H., Omata T., Mizumoto K., Hattori S., Iwasaki K., Kawakita M. Sequence of 2,617 nucleotides from the 3' end of Newcastle disease virus genome RNA and the predicted amino acid sequence of viral NP protein. Nucleic Acids Res. 1986 Aug 26;14(16):6551–6564. doi: 10.1093/nar/14.16.6551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kurilla M. G., Stone H. O., Keene J. D. RNA sequence and transcriptional properties of the 3' end of the Newcastle disease virus genome. Virology. 1985 Sep;145(2):203–212. doi: 10.1016/0042-6822(85)90154-0. [DOI] [PubMed] [Google Scholar]
  26. Leppert M., Rittenhouse L., Perrault J., Summers D. F., Kolakofsky D. Plus and minus strand leader RNAs in negative strand virus-infected cells. Cell. 1979 Nov;18(3):735–747. doi: 10.1016/0092-8674(79)90127-2. [DOI] [PubMed] [Google Scholar]
  27. Luk D., Sánchez A., Banerjee A. K. Messenger RNA encoding the phosphoprotein (P) gene of human parainfluenza virus 3 is bicistronic. Virology. 1986 Sep;153(2):318–325. doi: 10.1016/0042-6822(86)90036-x. [DOI] [PubMed] [Google Scholar]
  28. Maizel J. V., Jr, White D. O., Scharff M. D. The polypeptides of adenovirus. I. Evidence for multiple protein components in the virion and a comparison of types 2, 7A, and 12. Virology. 1968 Sep;36(1):115–125. doi: 10.1016/0042-6822(68)90121-9. [DOI] [PubMed] [Google Scholar]
  29. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  30. McGinnes L. W., Morrison T. G. Nucleotide sequence of the gene encoding the Newcastle disease virus fusion protein and comparisons of paramyxovirus fusion protein sequences. Virus Res. 1986 Sep;5(4):343–356. doi: 10.1016/0168-1702(86)90028-6. [DOI] [PubMed] [Google Scholar]
  31. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  32. Millar N. S., Chambers P., Emmerson P. T. Nucleotide sequence analysis of the haemagglutinin-neuraminidase gene of Newcastle disease virus. J Gen Virol. 1986 Sep;67(Pt 9):1917–1927. doi: 10.1099/0022-1317-67-9-1917. [DOI] [PubMed] [Google Scholar]
  33. Miura N., Nakatani Y., Ishiura M., Uchida T., Okada Y. Molecular cloning of a full-length cDNA encoding the hemagglutinin-neuraminidase glycoprotein of Sendai virus. FEBS Lett. 1985 Aug 19;188(1):112–116. doi: 10.1016/0014-5793(85)80885-1. [DOI] [PubMed] [Google Scholar]
  34. Morgan E. M., Rakestraw K. M. Sequence of the Sendai virus L gene: open reading frames upstream of the main coding region suggest that the gene may be polycistronic. Virology. 1986 Oct 15;154(1):31–40. doi: 10.1016/0042-6822(86)90427-7. [DOI] [PubMed] [Google Scholar]
  35. Morgan E. M., Re G. G., Kingsbury D. W. Complete sequence of the Sendai virus NP gene from a cloned insert. Virology. 1984 May;135(1):279–287. doi: 10.1016/0042-6822(84)90137-5. [DOI] [PubMed] [Google Scholar]
  36. Okayama H., Berg P. A cDNA cloning vector that permits expression of cDNA inserts in mammalian cells. Mol Cell Biol. 1983 Feb;3(2):280–289. doi: 10.1128/mcb.3.2.280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Okayama H., Berg P. High-efficiency cloning of full-length cDNA. Mol Cell Biol. 1982 Feb;2(2):161–170. doi: 10.1128/mcb.2.2.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Paterson B. M., Roberts B. E., Kuff E. L. Structural gene identification and mapping by DNA-mRNA hybrid-arrested cell-free translation. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4370–4374. doi: 10.1073/pnas.74.10.4370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Paterson R. G., Harris T. J., Lamb R. A. Analysis and gene assignment of mRNAs of a paramyxovirus, simian virus 5. Virology. 1984 Oct 30;138(2):310–323. doi: 10.1016/0042-6822(84)90354-4. [DOI] [PubMed] [Google Scholar]
  40. Pelham H. R., Jackson R. J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem. 1976 Aug 1;67(1):247–256. doi: 10.1111/j.1432-1033.1976.tb10656.x. [DOI] [PubMed] [Google Scholar]
  41. Rozenblatt S., Eizenberg O., Ben-Levy R., Lavie V., Bellini W. J. Sequence homology within the morbilliviruses. J Virol. 1985 Feb;53(2):684–690. doi: 10.1128/jvi.53.2.684-690.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Shibuta H., Adachi A., Kanda T., Matumoto M. Experimental parainfluenzavirus infection in mice: fatal illness with atrophy of thymus and spleen in mice caused by a variant of parainfluenza 3 virus. Infect Immun. 1982 Feb;35(2):437–441. doi: 10.1128/iai.35.2.437-441.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Shibuta H., Kanda T., Adachi A., Yogo Y. Characterization of bovine parainfluenza virus type 3. Microbiol Immunol. 1979;23(7):617–628. doi: 10.1111/j.1348-0421.1979.tb00502.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Shibuta H., Kanda T., Hazama A., Adachi A., Matumoto M. Parainfluenza 3 virus: plaque-type variants lacking neuraminidase activity. Infect Immun. 1981 Oct;34(1):262–267. doi: 10.1128/iai.34.1.262-267.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Shibuta H., Kanda T., Nozawa A., Sato S., Kumanishi T. Experimental parainfluenza virus infection in mice: growth and spread of a highly pathogenic variant of parainfluenza 3 virus in the mouse brain. Arch Virol. 1985;83(1-2):43–52. doi: 10.1007/BF01310963. [DOI] [PubMed] [Google Scholar]
  47. Shibuta H., Nozawa A., Shioda T., Kanda T. Neuraminidase activity and syncytial formation in variants of parainfluenza 3 virus. Infect Immun. 1983 Aug;41(2):780–788. doi: 10.1128/iai.41.2.780-788.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Shibuta H., Suzu S., Shioda T. Differences in bovine parainfluenza 3 virus variants studied by monoclonal antibodies against viral glycoproteins. Virology. 1986 Dec;155(2):688–696. doi: 10.1016/0042-6822(86)90228-x. [DOI] [PubMed] [Google Scholar]
  49. Shioda T., Hidaka Y., Kanda T., Shibuta H., Nomoto A., Iwasaki K. Sequence of 3,687 nucleotides from the 3' end of Sendai virus genome RNA and the predicted amino acid sequences of viral NP, P and C proteins. Nucleic Acids Res. 1983 Nov 11;11(21):7317–7330. doi: 10.1093/nar/11.21.7317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Shioda T., Iwasaki K., Shibuta H. Determination of the complete nucleotide sequence of the Sendai virus genome RNA and the predicted amino acid sequences of the F, HN and L proteins. Nucleic Acids Res. 1986 Feb 25;14(4):1545–1563. doi: 10.1093/nar/14.4.1545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Spriggs M. K., Collins P. L. Human parainfluenza virus type 3: messenger RNAs, polypeptide coding assignments, intergenic sequences, and genetic map. J Virol. 1986 Sep;59(3):646–654. doi: 10.1128/jvi.59.3.646-654.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Spriggs M. K., Olmsted R. A., Venkatesan S., Coligan J. E., Collins P. L. Fusion glycoprotein of human parainfluenza virus type 3: nucleotide sequence of the gene, direct identification of the cleavage-activation site, and comparison with other paramyxoviruses. Virology. 1986 Jul 15;152(1):241–251. doi: 10.1016/0042-6822(86)90388-0. [DOI] [PubMed] [Google Scholar]
  53. Sánchez A., Banerjee A. K., Furuichi Y., Richardson M. A. Conserved structures among the nucleocapsid proteins of the paramyxoviridae: complete nucleotide sequence of human parainfluenza virus type 3 NP mRNA. Virology. 1986 Jul 15;152(1):171–180. doi: 10.1016/0042-6822(86)90382-x. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES