Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1991 Jul;65(7):3738–3745. doi: 10.1128/jvi.65.7.3738-3745.1991

Rotavirus YM gene 4: analysis of its deduced amino acid sequence and prediction of the secondary structure of the VP4 protein.

S López 1, I López 1, P Romero 1, E Méndez 1, X Soberón 1, C F Arias 1
PMCID: PMC241399  PMID: 1645789

Abstract

We have determined the complete nucleotide sequence of the VP4 gene of porcine rotavirus YM. It is 2,362 nucleotides long, with a single open reading frame coding for a protein of 776 amino acids. A phylogenetic tree was derived from the deduced YM VP4 amino acid sequence and 18 other available VP4 sequences of rotavirus strains belonging to different serotypes and isolated from different animal species. In this tree, VP4 proteins were grouped by the hosts that the corresponding viruses infect rather than by the serotypes they belong to, suggesting that this protein is involved in the host specificity of the viruses. In an attempt to predict the secondary structure of the VP4 protein, we selected the more divergent VP4 sequences and made a secondary structure analysis of each protein. In spite of variations within the individual structures predicted, there was a general structural pattern which suggested the existence of at least two different domains. One, comprising the amino-terminal 63% of the protein, is predicted to be a possible globular domain rich in beta-strands alternated with turns and coils. The second domain, represented by the remaining, carboxy-terminal part of VP4, is rich in long stretches of alpha-helix, one of which, 63 amino acids long, has heptad repeats resembling those found in proteins known to form alpha-helical coiled-coils. The predicted secondary structure correlates well with the available data on the protein accessibility delineated by immunological and biochemical findings and with the spike structure of the protein, which has been determined by cryoelectron microscopy.

Full text

PDF
3738

Images in this article

Selected References

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

  1. Arias C. F., López S., Bell J. R., Strauss J. H. Primary structure of the neutralization antigen of simian rotavirus SA11 as deduced from cDNA sequence. J Virol. 1984 May;50(2):657–661. doi: 10.1128/jvi.50.2.657-661.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arias C. F., Ruiz A. M., López S. Further antigenic characterization of porcine rotavirus YM. J Clin Microbiol. 1989 Dec;27(12):2871–2873. doi: 10.1128/jcm.27.12.2871-2873.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chou P. Y., Fasman G. D. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. doi: 10.1021/bi00699a002. [DOI] [PubMed] [Google Scholar]
  4. Clark S. M., Roth J. R., Clark M. L., Barnett B. B., Spendlove R. S. Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J Virol. 1981 Sep;39(3):816–822. doi: 10.1128/jvi.39.3.816-822.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cohen C., Parry D. A. Alpha-helical coiled coils and bundles: how to design an alpha-helical protein. Proteins. 1990;7(1):1–15. doi: 10.1002/prot.340070102. [DOI] [PubMed] [Google Scholar]
  6. Crawford I. P., Niermann T., Kirschner K. Prediction of secondary structure by evolutionary comparison: application to the alpha subunit of tryptophan synthase. Proteins. 1987;2(2):118–129. doi: 10.1002/prot.340020206. [DOI] [PubMed] [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ericson B. L., Graham D. Y., Mason B. B., Hanssen H. H., Estes M. K. Two types of glycoprotein precursors are produced by the simian rotavirus SA11. Virology. 1983 Jun;127(2):320–332. doi: 10.1016/0042-6822(83)90147-2. [DOI] [PubMed] [Google Scholar]
  9. Espejo R. T., López S., Arias C. Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. J Virol. 1981 Jan;37(1):156–160. doi: 10.1128/jvi.37.1.156-160.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Estes M. K., Cohen J. Rotavirus gene structure and function. Microbiol Rev. 1989 Dec;53(4):410–449. doi: 10.1128/mr.53.4.410-449.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Estes M. K., Graham D. Y., Mason B. B. Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. J Virol. 1981 Sep;39(3):879–888. doi: 10.1128/jvi.39.3.879-888.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fitch W. M., Margoliash E. Construction of phylogenetic trees. Science. 1967 Jan 20;155(3760):279–284. doi: 10.1126/science.155.3760.279. [DOI] [PubMed] [Google Scholar]
  13. Fukuhara N., Yoshie O., Kitaoka S., Konno T. Role of VP3 in human rotavirus internalization after target cell attachment via VP7. J Virol. 1988 Jul;62(7):2209–2218. doi: 10.1128/jvi.62.7.2209-2218.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  15. Gorziglia M., Green K., Nishikawa K., Taniguchi K., Jones R., Kapikian A. Z., Chanock R. M. Sequence of the fourth gene of human rotaviruses recovered from asymptomatic or symptomatic infections. J Virol. 1988 Aug;62(8):2978–2984. doi: 10.1128/jvi.62.8.2978-2984.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gorziglia M., Larralde G., Kapikian A. Z., Chanock R. M. Antigenic relationships among human rotaviruses as determined by outer capsid protein VP4. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7155–7159. doi: 10.1073/pnas.87.18.7155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gorziglia M., Larralde G., Ward R. L. Neutralization epitopes on rotavirus SA11 4fM outer capsid proteins. J Virol. 1990 Sep;64(9):4534–4539. doi: 10.1128/jvi.64.9.4534-4539.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gorziglia M., Nishikawa K., Hoshino Y., Taniguchi K. Similarity of the outer capsid protein VP4 of the Gottfried strain of porcine rotavirus to that of asymptomatic human rotavirus strains. J Virol. 1990 Jan;64(1):414–418. doi: 10.1128/jvi.64.1.414-418.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Greenberg H. B., Flores J., Kalica A. R., Wyatt R. G., Jones R. Gene coding assignments for growth restriction, neutralization and subgroup specificities of the W and DS-1 strains of human rotavirus. J Gen Virol. 1983 Feb;64(Pt 2):313–320. doi: 10.1099/0022-1317-64-2-313. [DOI] [PubMed] [Google Scholar]
  20. Greenberg H. B., Wyatt R. G., Kapikian A. Z., Kalica A. R., Flores J., Jones R. Rescue and serotypic characterization of noncultivable human rotavirus by gene reassortment. Infect Immun. 1982 Jul;37(1):104–109. doi: 10.1128/iai.37.1.104-109.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kalica A. R., Flores J., Greenberg H. B. Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology. 1983 Feb;125(1):194–205. doi: 10.1016/0042-6822(83)90073-9. [DOI] [PubMed] [Google Scholar]
  22. Kalica A. R., Greenberg H. B., Wyatt R. G., Flores J., Sereno M. M., Kapikian A. Z., Chanock R. M. Genes of human (strain Wa) and bovine (strain UK) rotaviruses that code for neutralization and subgroup antigens. Virology. 1981 Jul 30;112(2):385–390. doi: 10.1016/0042-6822(81)90285-3. [DOI] [PubMed] [Google Scholar]
  23. Kaljot K. T., Shaw R. D., Rubin D. H., Greenberg H. B. Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. J Virol. 1988 Apr;62(4):1136–1144. doi: 10.1128/jvi.62.4.1136-1144.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kantharidis P., Dyall-Smith M. L., Holmes I. H. Marked sequence variation between segment 4 genes of human RV-5 and simian SA 11 rotaviruses. Arch Virol. 1987;93(1-2):111–121. doi: 10.1007/BF01313897. [DOI] [PubMed] [Google Scholar]
  25. Kantharidis P., Dyall-Smith M. L., Tregear G. W., Holmes I. H. Nucleotide sequence of UK bovine rotavirus segment 4: possible host restriction of VP3 genes. Virology. 1988 Oct;166(2):308–315. doi: 10.1016/0042-6822(88)90501-6. [DOI] [PubMed] [Google Scholar]
  26. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  27. Liprandi F., Rodriguez I., Piña C., Larralde G., Gorziglia M. VP4 monotype specificities among porcine rotavirus strains of the same VP4 serotype. J Virol. 1991 Mar;65(3):1658–1661. doi: 10.1128/jvi.65.3.1658-1661.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lizano M., López S., Arias C. F. The amino-terminal half of rotavirus SA114fM VP4 protein contains a hemagglutination domain and primes for neutralizing antibodies to the virus. J Virol. 1991 Mar;65(3):1383–1391. doi: 10.1128/jvi.65.3.1383-1391.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. López S., Arias C. F., Bell J. R., Strauss J. H., Espejo R. T. Primary structure of the cleavage site associated with trypsin enhancement of rotavirus SA11 infectivity. Virology. 1985 Jul 15;144(1):11–19. doi: 10.1016/0042-6822(85)90300-9. [DOI] [PubMed] [Google Scholar]
  30. López S., Arias C. F., Méndez E., Espejo R. T. Conservation in rotaviruses of the protein region containing the two sites associated with trypsin enhancement of infectivity. Virology. 1986 Oct 15;154(1):224–227. doi: 10.1016/0042-6822(86)90445-9. [DOI] [PubMed] [Google Scholar]
  31. Mackow E. R., Barnett J. W., Chan H., Greenberg H. B. The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a baculovirus recombinant. J Virol. 1989 Apr;63(4):1661–1668. doi: 10.1128/jvi.63.4.1661-1668.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Mackow E. R., Shaw R. D., Matsui S. M., Vo P. T., Dang M. N., Greenberg H. B. The rhesus rotavirus gene encoding protein VP3: location of amino acids involved in homologous and heterologous rotavirus neutralization and identification of a putative fusion region. Proc Natl Acad Sci U S A. 1988 Feb;85(3):645–649. doi: 10.1073/pnas.85.3.645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mason B. B., Graham D. Y., Estes M. K. Biochemical mapping of the simian rotavirus SA11 genome. J Virol. 1983 May;46(2):413–423. doi: 10.1128/jvi.46.2.413-423.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Matsuno S., Inouye S. Purification of an outer capsid glycoprotein of neonatal calf diarrhea virus and preparation of its antisera. Infect Immun. 1983 Jan;39(1):155–158. doi: 10.1128/iai.39.1.155-158.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Myers E. W., Miller W. Optimal alignments in linear space. Comput Appl Biosci. 1988 Mar;4(1):11–17. doi: 10.1093/bioinformatics/4.1.11. [DOI] [PubMed] [Google Scholar]
  37. Nibert M. L., Dermody T. S., Fields B. N. Structure of the reovirus cell-attachment protein: a model for the domain organization of sigma 1. J Virol. 1990 Jun;64(6):2976–2989. doi: 10.1128/jvi.64.6.2976-2989.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Nishikawa K., Gorziglia M. The nucleotide sequence of the VP3 gene of porcine rotavirus OSU. Nucleic Acids Res. 1988 Dec 23;16(24):11847–11847. doi: 10.1093/nar/16.24.11847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Nishikawa K., Taniguchi K., Torres A., Hoshino Y., Green K., Kapikian A. Z., Chanock R. M., Gorziglia M. Comparative analysis of the VP3 gene of divergent strains of the rotaviruses simian SA11 and bovine Nebraska calf diarrhea virus. J Virol. 1988 Nov;62(11):4022–4026. doi: 10.1128/jvi.62.11.4022-4026.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Offit P. A., Blavat G., Greenberg H. B., Clark H. F. Molecular basis of rotavirus virulence: role of gene segment 4. J Virol. 1986 Jan;57(1):46–49. doi: 10.1128/jvi.57.1.46-49.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Offit P. A., Clark H. F., Blavat G., Greenberg H. B. Reassortant rotaviruses containing structural proteins vp3 and vp7 from different parents induce antibodies protective against each parental serotype. J Virol. 1986 Nov;60(2):491–496. doi: 10.1128/jvi.60.2.491-496.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Offit P. A., Shaw R. D., Greenberg H. B. Passive protection against rotavirus-induced diarrhea by monoclonal antibodies to surface proteins vp3 and vp7. J Virol. 1986 May;58(2):700–703. doi: 10.1128/jvi.58.2.700-703.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Potter A. A., Cox G., Parker M., Babiuk L. A. The complete nucleotide sequence of bovine rotavirus C486 gene 4 cDNA. Nucleic Acids Res. 1987 May 26;15(10):4361–4361. doi: 10.1093/nar/15.10.4361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Prasad B. V., Burns J. W., Marietta E., Estes M. K., Chiu W. Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy. Nature. 1990 Feb 1;343(6257):476–479. doi: 10.1038/343476a0. [DOI] [PubMed] [Google Scholar]
  45. Prasad B. V., Wang G. J., Clerx J. P., Chiu W. Three-dimensional structure of rotavirus. J Mol Biol. 1988 Jan 20;199(2):269–275. doi: 10.1016/0022-2836(88)90313-0. [DOI] [PubMed] [Google Scholar]
  46. Ruiz A. M., López I. V., López S., Espejo R. T., Arias C. F. Molecular and antigenic characterization of porcine rotavirus YM, a possible new rotavirus serotype. J Virol. 1988 Nov;62(11):4331–4336. doi: 10.1128/jvi.62.11.4331-4336.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sabara M., Barrington A., Babiuk L. A. Immunogenicity of a bovine rotavirus glycoprotein fragment. J Virol. 1985 Dec;56(3):1037–1040. doi: 10.1128/jvi.56.3.1037-1040.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Schulz G. E. A critical evaluation of methods for prediction of protein secondary structures. Annu Rev Biophys Biophys Chem. 1988;17:1–21. doi: 10.1146/annurev.bb.17.060188.000245. [DOI] [PubMed] [Google Scholar]
  49. Taniguchi K., Maloy W. L., Nishikawa K., Green K. Y., Hoshino Y., Urasawa S., Kapikian A. Z., Chanock R. M., Gorziglia M. Identification of cross-reactive and serotype 2-specific neutralization epitopes on VP3 of human rotavirus. J Virol. 1988 Jul;62(7):2421–2426. doi: 10.1128/jvi.62.7.2421-2426.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Taniguchi K., Urasawa T., Morita Y., Greenberg H. B., Urasawa S. Direct serotyping of human rotavirus in stools by an enzyme-linked immunosorbent assay using serotype 1-, 2-, 3-, and 4-specific monoclonal antibodies to VP7. J Infect Dis. 1987 Jun;155(6):1159–1166. doi: 10.1093/infdis/155.6.1159. [DOI] [PubMed] [Google Scholar]
  51. Wilson I. A., Skehel J. J., Wiley D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature. 1981 Jan 29;289(5796):366–373. doi: 10.1038/289366a0. [DOI] [PubMed] [Google Scholar]
  52. Yeager M., Dryden K. A., Olson N. H., Greenberg H. B., Baker T. S. Three-dimensional structure of rhesus rotavirus by cryoelectron microscopy and image reconstruction. J Cell Biol. 1990 Jun;110(6):2133–2144. doi: 10.1083/jcb.110.6.2133. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES