1887

Journal of General Virology header logo

Volume 67, Issue 9

Nucleotide Sequence Analysis of the Haemagglutinin-Neuraminidase Gene of Newcastle Disease Virus Free

Abstract

Summary

The nucleotide sequence of the haemagglutinin-neuraminidase (HN) gene of Newcastle disease virus (NDV) has been determined. The HN gene is 2031 nucleotides long, approximately 13.5% of the viral genome. The nucleotide sequence contains a single long open reading frame which would encode a protein of 577 amino acids, with a mol. wt. of 63149. This is in good agreement with estimates of the molecular weight of the unglycosylated HN protein. Analysis of the amino acid sequence reveals six potential glycosylation sites and shows the major hydrophobic region to be close to the N terminus. This provides evidence for the N-terminal attachment of HN to the viral membrane. The hydrophilic nature of the extreme N-terminal amino acids suggests the absence of a cleaved signal sequence. Analysis of the long non-coding region at the 3′ end of the mRNA encoded by the HN gene of NDV suggests a possible explanation for the origin of HN in extremely avirulent strains of NDV. There are regions of high homology between the deduced amino acid sequence of the NDV HN glycoprotein and the HN glycoproteins of two other paramyxoviruses, Sendai virus and simian virus 5 (SV5). An alignment of the HN amino acid sequences of these viruses shows 32% of amino acid residues are conserved between NDV and SV5, and 23% between NDV and Sendai virus. In contrast, only very limited homology is found between NDV HN and the influenza virus glycoproteins.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): haemagglutinin-neuraminidase , NDV , nucleotide sequence and paramyxovirus
© The Journal of General Virology 1986
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-67-9-1917
1986-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/67/9/JV0670091917.html?itemId=/content/journal/jgv/10.1099/0022-1317-67-9-1917&mimeType=html&fmt=ahah

References

  1. Alexander D. J. 1985; Advances in the diagnosis of Newcastle disease. In Veterinary Viral Diseases: Their Significance in South-east Asia and the Western Pacific pp. 317–325 Edited by Della-Porta A. J. Sydney: Academic Press;
     [Google Scholar]
  2. Biggin M. D., Gibson T. J., Hong G. F. 1983; Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proceedings of the National Academy of Sciences, U.S.A. 80:3963–3965
     [Google Scholar]
  3. Blok J., Air G. M., Laver W. G., Ward C. W., Lilley G. G., Woods E. F., Roxburgh C. M., Inglis A. S. 1982; Studies on the size, chemical composition, and partial sequence of neuraminidase (NA) from type A influenza viruses show that the N-terminal region of NA is not processed and serves to anchor the NA in the viral membrane. Virology 119:109–121
     [Google Scholar]
  4. Blumberg B. M., Giorgi C., Rose K., Kolakofsky D. 1985a; Sequence determination of the Sendai virus fusion protein gene. Journal of General Virology 66:317–331
     [Google Scholar]
  5. Blumberg B., Giorgi C., Roux L., Rajin R., Dowling P., Chollet A., Kolakofsky D. 1985b; Sequence determination of the Sendai virus HN gene and its comparison to the influenza virus glycoproteins. Cell 41:269–278
     [Google Scholar]
  6. Box P. G. 1967; Poultry and the practitioner. Veterinary Record 81 Clinical supplement No. 13, 30 December
    [Google Scholar]
  7. Chambers P., Samson A. C. R. 1982; Non-structural proteins in Newcastle disease virus-infected cells. Journal of General Virology 58:1–12
     [Google Scholar]
  8. Chambers P., Millar N. S., Bingham R. W., Emmerson P. T. 1986; 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. Journal of General Virology 67:475–486
     [Google Scholar]
  9. Clinkscales C. W., Bratt M. A., Morrison T. G. 1977; Synthesis of Newcastle disease virus polypeptides in a wheat germ cell-free system. Journal of Virology 22:97–101
     [Google Scholar]
  10. Collins P. L., Wertz G. W., Ball L. A., Hightower L. E. 1982; Coding assignments of the five smaller mRNAs of Newcastle disease virus. Journal of Virology 43:1024–1031
     [Google Scholar]
  11. Fields S., Winter G., Brownlee G. G. 1981; Structure of the neuraminidase gene in human influenza virus A/PR/8/34. Nature, London 290:213–217
     [Google Scholar]
  12. Garnier J., Osguthorpe D. J., Robson B. 1978; Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. Journal of Molecular Biology 120:97–120
     [Google Scholar]
  13. Garten W., Berk W., Nagai Y., Rott R., Klenk H. -D. 1980a; Mutational changes of the protease susceptibility of glycoprotein F of Newcastle disease virus: effects on pathogenicity. Journal of General Virology 50:135–147
     [Google Scholar]
  14. Garten W., Kohama T., Klenk H. -D. 1980b; Proteolytic activation of the haemagglutinin–neuraminidase of Newcastle disease virus involves loss of a glycopeptide. Journal of General Virology 51:207–211
     [Google Scholar]
  15. Gupta C., Kingsbury D. W. 1984; Complete sequences of the intergenic and mRNA start signals in the Sendai virus genome: homologies with the genome of vesicular stomatitis virus. Nucleic Acids Research 12:3829–3841
     [Google Scholar]
  16. Hamaguchi M., Yoshida T., Nishikawa K., Naruse H., Nagai Y. 1983; Transcriptive complex of Newcastle disease virus. I. Both L and P proteins are required to constitute an active complex. Virology 128:105–107
     [Google Scholar]
  17. Hart G. W., Brew K., Grant G. A., Bradshaw R. A., Lennarz W. J. 1979; Primary structural requirements for the enzymatic formation of the N-glycosidic bond in glycoproteins. Journal of Biological Chemistry 254:9747–9753
     [Google Scholar]
  18. Haseloff J., Goelet P., Zimmern D., Ahlquist P., Dasgupta R., Kaesberg P. 1984; Striking similarities in amino acid sequence among nonstructural proteins encoded by RNA viruses that have dissimilar genomic organisation. Proceedings of the National Academy of Sciences, U.S.A 81:4358–4362
     [Google Scholar]
  19. Hiebert S. W., Paterson R. G., Lamb R. A. 1985a; Hemagglutinin-neuraminidase protein of the paramyxovirus simian virus 5: nucleotide sequence of the mRNA predicts an N-terminal membrane anchor. Journal of Virology 54:1–6
     [Google Scholar]
  20. Hiebert S. W., Paterson R. G., Lamb R. A. 1985b; Identification and predicted sequence of a previously unrecognized small hydrophobic protein, SH, of the paramyxovirus simian virus 5. Journal of Virology 55:744–751
     [Google Scholar]
  21. Homma M., Ohuchi M. 1973; 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. Journal of Virology 12:1457–1465
     [Google Scholar]
  22. Horisberger M. A., De Staritzky C., Content J. 1980; Intracellular glycosylation of influenza hemagglutinin: the effect of glucosamine. Archives of Virology 64:9–16
     [Google Scholar]
  23. Iorio R. M., Bratt M. A. 1984; Monoclonal antibodies as functional probes of the HN glycoprotein of Newcastle disease virus: antigenic separation of the hemagglutinating and neuraminidase sites. Journal of Immunology 133:2215–2219
     [Google Scholar]
  24. Keil W., Klenk H. -D., Schwarz R. T. 1979; Carbohydrates of influenza virus. III. Nature of oligosaccharide-protein linkage in viral glycoproteins. Journal of Virology 31:253–256
     [Google Scholar]
  25. Kozak M. 1981; Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes. Nucleic Acids Research 9:5233–5252
     [Google Scholar]
  26. Kozak M. 1986; Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44:283–292
     [Google Scholar]
  27. Kurilla M. G., Stone H. O., Keene J. D. 1985; RNA sequence and transcriptional properties of the 3′ end of the Newcastle disease virus genome. Virology 145:203–212
     [Google Scholar]
  28. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157:105–132
     [Google Scholar]
  29. Messing J., Vieira I. 1982; A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene 19:269–276
     [Google Scholar]
  30. Miura N., Nakatani Y., Ishiura M., Uchida T., Okada Y. 1985; Molecular cloning of a full length cDNA encoding the hemagglutinin-neuraminidase glycoprotein of Sendai virus. FEBS Letters 188:112–116
     [Google Scholar]
  31. Morrison T. G., Simpson D. 1980; Synthesis, stability, and cleavage of Newcastle disease virus glycoproteins in the absence of glycosylation. Journal of Virology 36:171–180
     [Google Scholar]
  32. Naeve C. W., Hinshaw V. S., Webster R. G. 1984; Mutations in the hemagglutinin receptor-binding site can change the biological properties of an influenza virus. Journal of Virology 51:567–569
     [Google Scholar]
  33. Nagai Y., Klenk H. -D. 1977; Activation of precursors to both glycoproteins of NDV by proteolytic cleavage. Virology 77:125–134
     [Google Scholar]
  34. Nagai Y., Klenk H. -D., Rott R. 1976; Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology 72:494–508
     [Google Scholar]
  35. Paterson R. G., Harris T. J. R., Lamb R. A. 1984; Fusion protein of the paramyxovirus simian virus 5: nucleotide sequence of mRNA predicts a highly hydrophobic glycoprotein. Proceedings of the National Academy of Sciences, U.S.A. 81:6706–6710
     [Google Scholar]
  36. Queen C., Korn L. J. 1984; A comprehensive sequence analysis program for the IBM personal computer. Nucleic Acids Research 12:581–599
     [Google Scholar]
  37. Rogers G. N., Paulson J. C., Daniels R. S., Skehel J. J., Wilson I. A., Wiley D. C. 1983; Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature, London 304:76–78
     [Google Scholar]
  38. Ronin C., Bouchilloux S., Garnier C., Van Rietschoten J. 1978; Enzymatic N-glycosylation of synthetic Asn-X-Thr containing peptides. FEBS Letters 96:179–182
     [Google Scholar]
  39. Rose L. K. 1980; Complete intergenic and flanking gene sequences from the genome of vesicular stomatitis virus. Cell 19:415–421
     [Google Scholar]
  40. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, U.S.A 74:5463–5467
     [Google Scholar]
  41. Satake M., Coligan J. E., Elango N., Norrby E., Venkatesan S. 1985; Respiratory syncytial virus envelope glycoprotein (G) has a novel structure. Nucleic Acids Research 13:7795–7812
     [Google Scholar]
  42. Scheid A., Choppin P. W. 1973; Isolation and purification of the envelope proteins of Newcastle disease virus. Journal of Virology 11:263–271
     [Google Scholar]
  43. Scheid A., Choppin P. W. 1977; Two disulfide-linked polypeptide chains constitute the active F protein of paramyxoviruses. Virology 80:54–66
     [Google Scholar]
  44. Scheid A., Graves M. C., Silver S. M., Choppin P. W. 1978; Studies on the structure and functions of paramyxovirus glycoproteins. In Negative Strand Viruses and the Host Cell pp. 181–193 Edited by Mahy B. W. J., Barry R. D. London: Academic Press;
     [Google Scholar]
  45. Schuy W., Garten W., Linder D., Klenk H. -D. 1984; The carboxyterminus of the haemagglutinin-neuraminidase of Newcastle disease virus is exposed at the surface of the viral envelope. Virus Research 1:415–426
     [Google Scholar]
  46. Shioda T., Iwaski K., Shibuta H. 1986; 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 Research 14:1545–1563
     [Google Scholar]
  47. St Aden R. 1982a; An interactive graphics program for comparing and aligning nucleic acid and amino acid sequences. Nucleic Acids Research 10:2951–2961
     [Google Scholar]
  48. Staden R. 1982b; Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Research 10:4731–4751
     [Google Scholar]
  49. Staden R. 1984; Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Research 12:521–538
     [Google Scholar]
  50. Staden R. 1986; The current status and portability of our sequence handling software. Nucleic Acids Research 14:217–231
     [Google Scholar]
  51. Umino Y., Kohama T., Kohase M., Sugaira A., Klenk H. -D., Rott R. 1984; Biological functions of monospecific antibodies to envelope glycoproteins of Newcastle disease virus. Archives of Virology 81:53–65
     [Google Scholar]
  52. Varghese J. N., Laver W. G., Colman P. M. 1983; Structure of the influenza virus glycoprotein antigen neuraminidase at 2–9 A resolution. Nature, London 303:35–40
     [Google Scholar]
  53. Von Heijne G. 1983; Patterns of amino acids near signal sequence cleavage sites. European Journal of Biochemistry 133:17–21
     [Google Scholar]
  54. Wertz G. W., Collins P. L., Huang Y., Gruber C., Levine S., Ball L. A. 1985; Nucleotide sequence of the G protein gene of human respiratory syncytial virus reveals an unusual type of viral membrane protein. Proceedings of the National Academy of Sciences, U.S.A 82:4075–4079
     [Google Scholar]
  55. Wiley D. C. 1985; Viral membranes. In Virology pp. 45–67 Edited by Fields B. N. New York: Raven Press;
     [Google Scholar]
  56. Wilson I. A., Skehel J. J., Wiley D. C. 1981; Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature, London 289:366–378
     [Google Scholar]
  57. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequence of the M13 mpl8 and pUC19 vectors. Gene 33103–119
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-67-9-1917
Loading
Nucleotide Sequence Analysis of the Haemagglutinin-Neuraminidase Gene of Newcastle Disease Virus
J. Gen. Virol. 67, 1917 (1986); https://doi.org/10.1099/0022-1317-67-9-1917
/content/journal/jgv/10.1099/0022-1317-67-9-1917
/content/journal/jgv/10.1099/0022-1317-67-9-1917
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error