Abstract
Two strains of bovine rotavirus (BRV), designated strain Nebraska Scottsbluff-1 (NS-1) and NS-2, were isolated from 2 neighboring cow-calf beef cattle ranches where dams had been vaccinated with a commercial vaccine containing group A BRV strain Neonatal Calf Diarrhea Virus (NCDV)-Lincoln (P1:G6). Nothern blot by hybridizations using whole genomic RNA probes indicated that strains NS-1 and NS-2 had identical group A RNA electrophoretic patterns and were homologous at all gene segments. Strain NS-1 was compared with reference group A BRV strains using serological and genotypic methods. In vitro virus neutralization assays indicated that strain NS-1 was neutralized by a G6-specific neutralizing monoclonal antibody (mAb) and guinea pig hyperimmune serum (GPHS) raised against BRV strain B641 (P5:G6), but not by G10-specific neutralizing mAb or GPHS raised against BRV strain BRV strain B223 (P11:G10). Nucleic acid hybridization experiments using whole-genomic RNA probes revealed that gene segment 4 of strain NS-1 differed from BRV strains NCDV-Lincoln and B223, but hybridized with strain B641. Conversely, gene segment 5 of strain NS-1 hybridized with BRV strain B223, but not with BRV strains NCDV-Lincoln and B641. A G-specific cDNA probe produced by reverse transcription polymerase chain reaction (RT-PCR) amplification of strain NS-1 hybridized specifically only with G6 strains NCDV-Lincoln and B641, but not with G10 strain B223. Co-electrophoresis experiments using strains NS-1, B641, and B223 further confirmed these results, suggesting that strain NS-1 was a naturally-occurring reassortant BRV between strains B641 and B223. Taken together these results indicated that a naturally-occurring group A BRV reassortant with a P gene different from the vaccine virus was responsible for the diarrheal syndrome observed on both ranches. Results from this study also indicate the existence of at least 2 different gene segments 5 among group A BRV infecting cattle.
Keywords: Rotavirus; Cattle, rotavirus; Diagnosis, rotavirus; Diarrhoea; Vaccination
Footnotes
This paper represents a portion of the thesis submitted by W. Lu to the University of Nebraska in partial fulfilment of the requirements for the PhD degree
References
- Coulson B.S., Fowler K.J., Bishop R.F., Cotton R.G.H. Neutralizing monoclonal antibodies to human rotavirus and indications of antigenic drift among strains from neonates. J. Virol. 1985;54:14–20. doi: 10.1128/jvi.54.1.14-20.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Estes M.K., Cohen J. Rotavirus gene structure and function. Microbiol. Rev. 1989;53:410–449. doi: 10.1128/mr.53.4.410-449.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flores J., Greenberg H.B., Myslinski J., Kalica A.R., Wyatt R.G., Kapikian A.Z., Chanock R.M. Use of transcription probes for genotyping rotavirus reassortants. Virology. 1982;121:288–295. doi: 10.1016/0042-6822(82)90168-4. [DOI] [PubMed] [Google Scholar]
- Flores J., Sears J., Schael I.P., White L., Garcia D., Lanata C., Kapikian A.Z. Identification of human rotavirus serotype by hybridization to polymerase chain reaction- generated probes derived from a hyperdivergent region of the gene encoding outer capsid protein VP7. J. Virol. 1991;64:4021–4024. doi: 10.1128/jvi.64.8.4021-4024.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Galfre G., Howe S.C., Milstein C., Butcher G.W., Howard J.C. Antibodies to major histocompatibility antigens produced by hybrid cells lines. Nature. 1977;266:550–552. doi: 10.1038/266550a0. [DOI] [PubMed] [Google Scholar]
- Gombold J.L., Ramig R.M. Analysis of reassortment of genomic segments in mice mixedly infected with rotaviruses SA11 and PRV. J. Virol. 1986;57:110–116. doi: 10.1128/jvi.57.1.110-116.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grotelueschen D.M., Duhamel G.E., Lu W., Hesse R.A., Berry J.G. Possible vaccination failure in beef cow herds caused by infection with rotavirus distinct from the vaccine virus: Clinical observations. 17th World Buiatrics Congr. and 25th Am. Assoc. Bov. Pract. Conf. 1992;1:190–196. August 31 – September 4, St. Paul, MN, USA. [Google Scholar]
- Hardy M.E., Woode G.N., Xu Z., Gorziglia M. Comparative amino acid sequence analysis of VP4 for VP7 serotype 6 bovine rotavirus strains NCDV, B641 and UK. J. Virol. 1991;65:5535–5538. doi: 10.1128/jvi.65.10.5535-5538.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hardy M.E., Gorziglia M., Wood G.N. Amino acid sequence analysis of bovine rotavirus B223 reveals a unique outer capsid protein VP4 and confirms a third bovine VP4 type. Virol. 1992;191:291–300. doi: 10.1016/0042-6822(92)90191-q. [DOI] [PubMed] [Google Scholar]
- Harlow E., Lane D. Cold Spring Harbor Laboratory; Cold Spring Harbor, N.Y: 1988. Antibodies — A laboratory manual; pp. 421–450. [Google Scholar]
- Hesse R.A., Couture L.P., Ellsworth S.R., Duhamel G.E., Lu W., Dickinson E.O., Benfield D.A. Production and characterization of VP4/VP7 reassortant swine rotaviruses derived from Gottfried and OSU parental strains. Am. J. Vet. Res. 1993;54:1623–1629. [PubMed] [Google Scholar]
- Hoshino Y., Wyatt R.G., Greenberg H.B., Flores J., Kapikian A.Z. Serotypic similarity and diversity of rotaviruses of mammalian and avian origin as studied by plaque-reduction neutralization. J. Infect. Dis. 1984;149:694–702. doi: 10.1093/infdis/149.5.694. [DOI] [PubMed] [Google Scholar]
- Hoshino Y., Sereno M.M., Midthun K., Flores J., Kapikian A.Z., Channock R.M. Vol. 82. 1985. Independent segregation of two antigen specificities (VP3 and VP7) involved in neutralization of rotavirus infectivity; pp. 8701–8704. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hussein H.A., Parwani A.V., Rosen B.I., Luchelli A., Saif L.J. Detection of rotavirus G1, G2, G3, and G11 in feces of diarrheic calves by using polymerase chain reaction-derived cDNA probes. J. Clin. Microbiol. 1993;31:2491–2496. doi: 10.1128/jcm.31.9.2491-2496.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isegawa Y., Nakagomi O., Nakagomi T., Ueda S. A VP4 sequence highly conserved in human strain AU-1 and feline rotavirus strain FRV-1. J. Gen. Virol. 1992;73:1939–1946. doi: 10.1099/0022-1317-73-8-1939. [DOI] [PubMed] [Google Scholar]
- Knowlton D.R., Spector D.M., Ward R.L. Development of an improved method for measuring neutralizing antibody to rotavirus. J. Virol. Methods. 1991;33:127–134. doi: 10.1016/0166-0934(91)90013-p. [DOI] [PubMed] [Google Scholar]
- Matsuda Y., Nakagomi O., Offit P.O. Presence of three types (VP4 serotypes) and two G (VP7 serotypes) among bovine rotavirus strains. Arch. Virol. 1990;115:199–207. doi: 10.1007/BF01310530. [DOI] [PubMed] [Google Scholar]
- Matsuda Y., Mukoyama A., Hasegawa A., Taniguchi K., Inouye A. Characterization of a human rotavirus strain which is possibly a naturally-occuring reassortant virus. Viral Res. 1988;10:167–175. doi: 10.1016/0168-1702(88)90013-5. [DOI] [PubMed] [Google Scholar]
- Mebus C.A., Konno M., Underdahl N.R., Twienhaus M.J. Cell culture propagation of neonatal calf diarrhea (scours) virus. Can. Vet. J. 1971;12:69–72. [PMC free article] [PubMed] [Google Scholar]
- Nakagomi O., Nakagomi T. Molecular evidence for naturally occuring single VP7 gene substitution reassortment between human rotaviruses belonging to two different genogroups. Arch. Virol. 1991;119:67–81. doi: 10.1007/BF01314324. [DOI] [PubMed] [Google Scholar]
- Offit P.A., Blavat G., Clark H.F., Shaw R., Greenberg H.B. Role of gene segments 4 and 9 in determining rotavirus virulence and protection against rotavirus challenge. In: Brown F., Chanock R.M., Lerner R.A., editors. Vaccines 86, New approaches to immunization. Cold Spring Harbor Laboratory; Cold Spring Harbor, N.Y: 1986. pp. 267–273. [Google Scholar]
- Parwani A.V., Hussein H.A., Rosen B.I., Luchelli A., Navarro L., Saif L.J. Characterization of field strains of group A bovine rotaviruses by using polymerase chain reaction-generated G and P type-specific cDNA probes. J. Clin. Microbiol. 1993;31:2010–2015. doi: 10.1128/jcm.31.8.2010-2015.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Richardson S.C., Grimwood K., Bishop R.F. Analysis of homotypic and heterotypic serum immune responses to rotavirus proteins following primary rotavirus infection by using the radioimmunoprecipitation technique. J. Clin. Microbiol. 1993;31:377–385. doi: 10.1128/jcm.31.2.377-385.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saif L.J., Jackwood A.J. Enteric virus vaccines: Theoretical considerations, current status, and future approaches. In: Saif L.J., Theil K.W., editors. Viral Diarrhea of Man and Animals. CRC press, Inc; Boca Raton, FL: 1989. pp. 73–95. [Google Scholar]
- Sharpee R.L., Nelson L.D., Beckenhauer W.H. Immunogenicity of a vaccine containing inactivated bovine rotavirus and coronavirus combined with an Escherichia coli bacterin. Proc. Symp. Bov. Neonatal Diarrhea, Western Vet. Conf.; Las Vegas, NV; 1988. pp. 27–32. [Google Scholar]
- Shaw R.D., Mackow E.R., Dyall-Smith M.L., Lazdins I., Holmes I.H., Greenberg H.B. Serotypic analysis of VP3 and VP7 neutralization escape mutants of rhesus rotavirus. J. Virol. 1988;62:3509–3512. doi: 10.1128/jvi.62.9.3509-3512.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snodgrass D.R., Ojeh C.K., Campbell I., Herring A.J. Bovine rotavirus serotypes and their significance for immunization. J. Clin. Microbiol. 1984;20:342–346. doi: 10.1128/jcm.20.3.342-346.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snodgrass D.R., Fitzgerald T., Campbell I., Scott P.M.M., Browning G.F., Miller D.I., Herring A.J., Greenberg H.B. Rotavirus serotype 6 and 10 predominate in cattle. J. Clin. Microbiol. 1990;28:504–507. doi: 10.1128/jcm.28.3.504-507.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Theil K.W. Nongroup A rotaviruses. In: Saif L.J., Theil K.W., editors. Viral Diarrhea of Man and Animals. CRC press, Inc; Boca Raton, FL: 1989. pp. 73–95. [Google Scholar]
- Urasawa S., Urasawa T., Taniguchi K. Genetic reassortment between two human rotaviruses having different serotype and subgroup specificities. J. Gen. Virol. 1986;67:1551–1559. doi: 10.1099/0022-1317-67-8-1551. [DOI] [PubMed] [Google Scholar]
- Ward R.L., McNeal M.M., Sander D.S., Greenberg H.B., Bernstein D.I. Immunodominance of the VP4 neutralization protein of rotavirus in protective natural infections of young children. J. Virol. 1993;67:464–468. doi: 10.1128/jvi.67.1.464-468.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woode G.N., Kelso N.E., Simpson T.F., Gaul S.K., Evans L.E., Babiuk L. Antigenic relationships among rotavirus: serum neutralization and cross-protection in gnotobiotic calves. J. Clin. Microbiol. 1983;18:358–364. doi: 10.1128/jcm.18.2.358-364.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zheng S., Woode G.N., Melendy D.R., Ramig R.F. Comparative studies of the antigenic polypeptide species VP4, VP6, and VP7 of three strains of bovine rotavirus. J. Clin. Microbiol. 1989;27:1939–1945. doi: 10.1128/jcm.27.9.1939-1945.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]