Abstract
Borna disease is a neurologic syndrome caused by infection with a nonsegmented, negative-strand RNA virus, Borna disease virus. Infected animals have antibodies to two soluble viral proteins, p40 and p23, and a membrane-associated viral glycoprotein, gp18. We examined the time course for the development of neutralization activity and the expression of antibodies to individual viral proteins in sera of infected rats. The appearance of neutralizing activity correlated with the development of immunoreactivity to gp18, but not p40 or p23. Monospecific and monoclonal antibodies to native gp18 and recombinant nonglycosylated gp18 were also found to have neutralizing activity and to immunoprecipitate viral particles or subparticles. These findings suggest that gp18 is likely to be present on the surface of the viral particles and is likely to contain epitopes important for virus neutralization.
Full Text
The Full Text of this article is available as a PDF (260.2 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baldridge J. R., Buchmeier M. J. Mechanisms of antibody-mediated protection against lymphocytic choriomeningitis virus infection: mother-to-baby transfer of humoral protection. J Virol. 1992 Jul;66(7):4252–4257. doi: 10.1128/jvi.66.7.4252-4257.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Battegay M., Moskophidis D., Waldner H., Bründler M. A., Fung-Leung W. P., Mak T. W., Hengartner H., Zinkernagel R. M. Impairment and delay of neutralizing antiviral antibody responses by virus-specific cytotoxic T cells. J Immunol. 1993 Nov 15;151(10):5408–5415. [PubMed] [Google Scholar]
- Bause-Niedrig I., Jackson M., Schein E., Ludwig H., Pauli G. Borna disease virus-specific antigens. II. The soluble antigen is a protein complex. Vet Immunol Immunopathol. 1992 Mar;31(3-4):361–369. doi: 10.1016/0165-2427(92)90022-i. [DOI] [PubMed] [Google Scholar]
- Briese T., Schneemann A., Lewis A. J., Park Y. S., Kim S., Ludwig H., Lipkin W. I. Genomic organization of Borna disease virus. Proc Natl Acad Sci U S A. 1994 May 10;91(10):4362–4366. doi: 10.1073/pnas.91.10.4362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Briese T., de la Torre J. C., Lewis A., Ludwig H., Lipkin W. I. Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11486–11489. doi: 10.1073/pnas.89.23.11486. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carbone K. M., Duchala C. S., Griffin J. W., Kincaid A. L., Narayan O. Pathogenesis of Borna disease in rats: evidence that intra-axonal spread is the major route for virus dissemination and the determinant for disease incubation. J Virol. 1987 Nov;61(11):3431–3440. doi: 10.1128/jvi.61.11.3431-3440.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Crabb B. S., Nagesha H. S., Studdert M. J. Identification of equine herpesvirus 4 glycoprotein G: a type-specific, secreted glycoprotein. Virology. 1992 Sep;190(1):143–154. doi: 10.1016/0042-6822(92)91200-e. [DOI] [PubMed] [Google Scholar]
- Cubitt B., Oldstone C., de la Torre J. C. Sequence and genome organization of Borna disease virus. J Virol. 1994 Mar;68(3):1382–1396. doi: 10.1128/jvi.68.3.1382-1396.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Danner K., Lüthgen K., Herlyn M., Mayr A. Vergleichende Untersuchungen über Nachweis und Bildung von Serumantiköpern gegen das Borna-Virus. Zentralbl Veterinarmed B. 1978 Jun;25(5):345–355. [PubMed] [Google Scholar]
- Dietzschold B., Kao M., Zheng Y. M., Chen Z. Y., Maul G., Fu Z. F., Rupprecht C. E., Koprowski H. Delineation of putative mechanisms involved in antibody-mediated clearance of rabies virus from the central nervous system. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7252–7256. doi: 10.1073/pnas.89.15.7252. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dimmock N. J. Neutralization of animal viruses. Curr Top Microbiol Immunol. 1993;183:1–149. doi: 10.1007/978-3-642-77849-0. [DOI] [PubMed] [Google Scholar]
- Fujinami R. S., Rosenthal A., Lampert P. W., Zurbriggen A., Yamada M. Survival of athymic (nu/nu) mice after Theiler's murine encephalomyelitis virus infection by passive administration of neutralizing monoclonal antibody. J Virol. 1989 May;63(5):2081–2087. doi: 10.1128/jvi.63.5.2081-2087.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haas B., Becht H., Rott R. Purification and properties of an intranuclear virus-specific antigen from tissue infected with Borna disease virus. J Gen Virol. 1986 Feb;67(Pt 2):235–241. doi: 10.1099/0022-1317-67-2-235. [DOI] [PubMed] [Google Scholar]
- Herzog S., Rott R. Replication of Borna disease virus in cell cultures. Med Microbiol Immunol. 1980;168(3):153–158. doi: 10.1007/BF02122849. [DOI] [PubMed] [Google Scholar]
- Herzog S., Wonigeit K., Frese K., Hedrich H. J., Rott R. Effect of Borna disease virus infection on athymic rats. J Gen Virol. 1985 Mar;66(Pt 3):503–508. doi: 10.1099/0022-1317-66-3-503. [DOI] [PubMed] [Google Scholar]
- Hirano N., Kao M., Ludwig H. Persistent, tolerant or subacute infection in Borna disease virus-infected rats. J Gen Virol. 1983 Jul;64(Pt 7):1521–1530. doi: 10.1099/0022-1317-64-7-1521. [DOI] [PubMed] [Google Scholar]
- Kearney J. F., Radbruch A., Liesegang B., Rajewsky K. A new mouse myeloma cell line that has lost immunoglobulin expression but permits the construction of antibody-secreting hybrid cell lines. J Immunol. 1979 Oct;123(4):1548–1550. [PubMed] [Google Scholar]
- Laemmli U. K., Favre M. Maturation of the head of bacteriophage T4. I. DNA packaging events. J Mol Biol. 1973 Nov 15;80(4):575–599. doi: 10.1016/0022-2836(73)90198-8. [DOI] [PubMed] [Google Scholar]
- Levine B., Hardwick J. M., Trapp B. D., Crawford T. O., Bollinger R. C., Griffin D. E. Antibody-mediated clearance of alphavirus infection from neurons. Science. 1991 Nov 8;254(5033):856–860. doi: 10.1126/science.1658936. [DOI] [PubMed] [Google Scholar]
- Liebert U. G., Schneider-Schaulies S., Baczko K., ter Meulen V. Antibody-induced restriction of viral gene expression in measles encephalitis in rats. J Virol. 1990 Feb;64(2):706–713. doi: 10.1128/jvi.64.2.706-713.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lipkin W. I., Travis G. H., Carbone K. M., Wilson M. C. Isolation and characterization of Borna disease agent cDNA clones. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4184–4188. doi: 10.1073/pnas.87.11.4184. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ludwig H., Bode L., Gosztonyi G. Borna disease: a persistent virus infection of the central nervous system. Prog Med Virol. 1988;35:107–151. [PubMed] [Google Scholar]
- Ludwig H., Furuya K., Bode L., Klein N., Dürrwald R., Lee D. S. Biology and neurobiology of Borna disease viruses (BDV), defined by antibodies, neutralizability and their pathogenic potential. Arch Virol Suppl. 1993;7:111–133. doi: 10.1007/978-3-7091-9300-6_10. [DOI] [PubMed] [Google Scholar]
- Ludwig H., Koester V., Pauli G., Rott R. The cerebrospinal fluid of rabbits infected with Borna disease virus. Arch Virol. 1977;55(3):209–223. doi: 10.1007/BF01319907. [DOI] [PubMed] [Google Scholar]
- Ludwig H., Kraft W., Kao M., Gosztonyi G., Dahme E., Krey H. Borna-Virus-Infektion (Borna-Krankheit) bei natürlich und experimentell infizierten Tieren: ihre Bedeutung für Forschung und Praxis. Tierarztl Prax. 1985;13(4):421–453. [PubMed] [Google Scholar]
- Ludwig H., Thein P. Demonstration of specific antibodies in the central nervous system of horses naturally infected with Borna disease virus. Med Microbiol Immunol. 1977 Dec 27;163(4):215–226. doi: 10.1007/BF02125505. [DOI] [PubMed] [Google Scholar]
- Lundgren A. L., Czech G., Bode L., Ludwig H. Natural Borna disease in domestic animals others than horses and sheep. Zentralbl Veterinarmed B. 1993 Jun;40(4):298–303. doi: 10.1111/j.1439-0450.1993.tb00142.x. [DOI] [PubMed] [Google Scholar]
- Malkinson M., Weisman Y., Ashash E., Bode L., Ludwig H. Borna disease in ostriches. Vet Rec. 1993 Sep 18;133(12):304–304. doi: 10.1136/vr.133.12.304-b. [DOI] [PubMed] [Google Scholar]
- McClure M. A., Thibault K. J., Hatalski C. G., Lipkin W. I. Sequence similarity between Borna disease virus p40 and a duplicated domain within the paramyxovirus and rhabdovirus polymerase proteins. J Virol. 1992 Nov;66(11):6572–6577. doi: 10.1128/jvi.66.11.6572-6577.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Narayan O., Herzog S., Frese K., Scheefers H., Rott R. Behavioral disease in rats caused by immunopathological responses to persistent borna virus in the brain. Science. 1983 Jun 24;220(4604):1401–1403. doi: 10.1126/science.6602380. [DOI] [PubMed] [Google Scholar]
- Narayan O., Herzog S., Frese K., Scheefers H., Rott R. Pathogenesis of Borna disease in rats: immune-mediated viral ophthalmoencephalopathy causing blindness and behavioral abnormalities. J Infect Dis. 1983 Aug;148(2):305–315. doi: 10.1093/infdis/148.2.305. [DOI] [PubMed] [Google Scholar]
- Outlaw M. C., Dimmock N. J. Mechanisms of neutralization of influenza virus on mouse tracheal epithelial cells by mouse monoclonal polymeric IgA and polyclonal IgM directed against the viral haemagglutinin. J Gen Virol. 1990 Jan;71(Pt 1):69–76. doi: 10.1099/0022-1317-71-1-69. [DOI] [PubMed] [Google Scholar]
- Pauli G., Grunmach J., Ludwig H. Focus-immunoassay for Borna disease virus-specific antigens. Zentralbl Veterinarmed B. 1984 Aug;31(7):552–557. doi: 10.1111/j.1439-0450.1984.tb01336.x. [DOI] [PubMed] [Google Scholar]
- Persson H., Hennighausen L., Taub R., DeGrado W., Leder P. Antibodies to human c-myc oncogene product: evidence of an evolutionarily conserved protein induced during cell proliferation. Science. 1984 Aug 17;225(4663):687–693. doi: 10.1126/science.6431612. [DOI] [PubMed] [Google Scholar]
- Pyper J. M., Richt J. A., Brown L., Rott R., Narayan O., Clements J. E. Genomic organization of the structural proteins of borna disease virus revealed by a cDNA clone encoding the 38-kDa protein. Virology. 1993 Jul;195(1):229–238. doi: 10.1006/viro.1993.1364. [DOI] [PubMed] [Google Scholar]
- Richt J. A., Vande Woude S., Zink M. C., Narayan O., Clements J. E. Analysis of Borna disease virus-specific RNAs in infected cells and tissues. J Gen Virol. 1991 Sep;72(Pt 9):2251–2255. doi: 10.1099/0022-1317-72-9-2251. [DOI] [PubMed] [Google Scholar]
- Rubin S. A., Waltrip R. W., 2nd, Bautista J. R., Carbone K. M. Borna disease virus in mice: host-specific differences in disease expression. J Virol. 1993 Jan;67(1):548–552. doi: 10.1128/jvi.67.1.548-552.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schneider P. A., Briese T., Zimmermann W., Ludwig H., Lipkin W. I. Sequence conservation in field and experimental isolates of Borna disease virus. J Virol. 1994 Jan;68(1):63–68. doi: 10.1128/jvi.68.1.63-68.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schädler R., Diringer H., Ludwig H. Isolation and characterization of a 14500 molecular weight protein from brains and tissue cultures persistently infected with borna disease virus. J Gen Virol. 1985 Nov;66(Pt 11):2479–2484. doi: 10.1099/0022-1317-66-11-2479. [DOI] [PubMed] [Google Scholar]
- Simmons A., Nash A. A. Role of antibody in primary and recurrent herpes simplex virus infection. J Virol. 1985 Mar;53(3):944–948. doi: 10.1128/jvi.53.3.944-948.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stitz L., Sobbe M., Bilzer T. Preventive effects of early anti-CD4 or anti-CD8 treatment on Borna disease in rats. J Virol. 1992 Jun;66(6):3316–3323. doi: 10.1128/jvi.66.6.3316-3323.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stoyloff R., Briese T., Borchers K., Zimmermann W., Ludwig H. N-glycosylated protein(s) are important for the infectivity of Borna disease virus (BDV). Arch Virol. 1994;137(3-4):405–409. doi: 10.1007/BF01309486. [DOI] [PubMed] [Google Scholar]
- Thiedemann N., Presek P., Rott R., Stitz L. Antigenic relationship and further characterization of two major Borna disease virus-specific proteins. J Gen Virol. 1992 May;73(Pt 5):1057–1064. doi: 10.1099/0022-1317-73-5-1057. [DOI] [PubMed] [Google Scholar]
- Thierer J., Riehle H., Grebenstein O., Binz T., Herzog S., Thiedemann N., Stitz L., Rott R., Lottspeich F., Niemann H. The 24K protein of Borna disease virus. J Gen Virol. 1992 Feb;73(Pt 2):413–416. doi: 10.1099/0022-1317-73-2-413. [DOI] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tyler K. L., Virgin H. W., 4th, Bassel-Duby R., Fields B. N. Antibody inhibits defined stages in the pathogenesis of reovirus serotype 3 infection of the central nervous system. J Exp Med. 1989 Sep 1;170(3):887–900. doi: 10.1084/jem.170.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
- VandeWoude S., Richt J. A., Zink M. C., Rott R., Narayan O., Clements J. E. A borna virus cDNA encoding a protein recognized by antibodies in humans with behavioral diseases. Science. 1990 Nov 30;250(4985):1278–1281. doi: 10.1126/science.2244211. [DOI] [PubMed] [Google Scholar]
- Virgin H. W., 4th, Bassel-Duby R., Fields B. N., Tyler K. L. Antibody protects against lethal infection with the neurally spreading reovirus type 3 (Dearing). J Virol. 1988 Dec;62(12):4594–4604. doi: 10.1128/jvi.62.12.4594-4604.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de la Torre J. C., Carbone K. M., Lipkin W. I. Molecular characterization of the Borna disease agent. Virology. 1990 Dec;179(2):853–856. doi: 10.1016/0042-6822(90)90154-j. [DOI] [PubMed] [Google Scholar]