Abstract
Feline infectious peritonitis virus (FIPV) causes a mostly fatal, immunologically mediated disease in cats. Previously, we demonstrated that immunization with a recombinant vaccinia virus expressing the FIPV spike protein (S) induced early death after challenge with FIPV (Vennema et al., 1990, J. Virol. 64, 1407–1409). In this paper we describe similar immunizations with the FIPV membrane (M) and nucleocapsid (N) proteins. The genes encoding these proteins were cloned and sequenced. Comparison of the amino acid sequences with the corresponding sequences of porcine transmissible gastroenteritis virus revealed 84.7 and 77% identity for M and N, respectively. Vaccinia virus recombinants expressing the cloned genes induced antibodies in immunized kittens. Immunization with neither recombinant induced early death after challenge with FIPV, strongly suggesting that antibody-dependent enhancement is mediated by antibodies against S only. Immunization with the N protein recombinant had no apparent effect on the outcome of challenge. However, three of eight kittens immunized with the M protein recombinant survived the challenge, as compared to one of eight kittens of the control group.
References
- Boyle J.F., Pedersen N.C., Everman J.F., McKeirnan A.J., Ott R.L., Black J.W. Plaque assay, polypeptide composition and immunochemistry of feline infectious peritonitis virus and feline enteric coronavirus. Adv. Exp. Med. Biol. 1984;173:133–147. doi: 10.1007/978-1-4615-9373-7_12. [DOI] [PubMed] [Google Scholar]
- Britton P., Carmenes R.S., Page K.W., Garwes D.J. The integral membrane protein from a virulent isolate of transmissible gastroenteritis virus: Molecular characterization, sequence and expression in Escherichia coli. Mol. Microbiol. 1988;2:497–505. doi: 10.1111/j.1365-2958.1988.tb00056.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavanagh D., Brian D.A., Enjuanes L., Holmes K.V., Lai M.M.C., Laude H., Siddell S.G., Spaan W., Taguchi F., Talbot P.J. Recommendations of the Coronavirus Study Group for the nomenclature of the structural proteins mRNAs, and genes of coronaviruses. Virology. 1990;176:306–307. doi: 10.1016/0042-6822(90)90259-T. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chakrabarti S., Brechling K., Moss B. Vaccinia virus expression vector: Coexpression of β-galactosidase provides visual screening of recombinant virus plaques. Mol. Cell. Biol. 1985;5:3403–3409. doi: 10.1128/mcb.5.12.3403. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984;12:387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Earl P.L., Huegin A.W., Moss B. Removal of cryptic poxvirus transcription termination signals from the human immunodeficiency virus type 1 envelope gene enhances expression and immunogenicity of a recombinant vaccinia virus. J. Virol. 1990;64:2448–2451. doi: 10.1128/jvi.64.5.2448-2451.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fiscus S.A., Teramoto Y.A. Antigenic comparison of feline coronavirus isolates: Evidence for markedly different peplomer glycoproteins. J. Virol. 1987;61:2607–2613. doi: 10.1128/jvi.61.8.2607-2613.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fleming J.O., Shubin R.A., Sussman M.A., Casteel N., Stohlman S.A. Monoclonal antibodies to the matrix (E1) glycoprotein of mouse hepatitis virus protect mice from encephalitis. Virology. 1989;168:162–167. doi: 10.1016/0042-6822(89)90415-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuerst T.R., Niles E.G., Studier F.W., Moss B. Vol. 83. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase; pp. 8122–8126. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Groot R.J., Andeweg A.C., Horzinek M.C., Spaan W.J.M. Sequence analysis of the Tend of the feline coronavirus FIPV 79–1146 genome: Comparison with the genome of porcine coronavirus TGEV reveals large insertions. Virology. 1988;167:370–376. doi: 10.1016/0042-6822(88)90097-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Groot R.J., ter Haar R.J., Horzinek M.C., van der Zeijst B.A.M. Intracellular RNAs of the feline infectious peritonitis coronavirus strain 79–1146. J. Gen. Virol. 1987;68:995–1002. doi: 10.1099/0022-1317-68-4-995. [DOI] [PubMed] [Google Scholar]
- de Groot R.J., van Leen R.W., Dalderup M.J.M., Vennema H., Horzinek M.C., Spaan W.J.M. Stably expressed FIPV peplomer protein induces cell fusion and elicits neutralizing antibodies in mice. Virology. 1989;171:493–502. doi: 10.1016/0042-6822(89)90619-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Groot R.J., Maduro J., Lenstra J.A., Horzinek M.C., van der Zeijst B.A.M., Spaan W.J.M. cDNA cloning and sequence analysis of the gene encoding the peplomer protein of feline infectious peritonitis virus. J. Gen. Virol. 1987;68:2639–2646. doi: 10.1099/0022-1317-68-10-2639. [DOI] [PubMed] [Google Scholar]
- Horzinek M.C., Ederveen J., Egberink H., Jacobse-Geels H.E.L., Niewold T., Prins J. Virion polypeptide specificity of immune complexes in cats inoculated with feline infectious peritonitis virus. Amer. J. Vet. Res. 1986;47:754–761. [PubMed] [Google Scholar]
- Jacobs L., de Groot R.J., Horzinek M.C., van der Zeijst B.A.M., Spaan W.J.M. The nucleotide sequence of the peplomer gene of porcine transmissible gastroenteritis virus (TGEV): Comparison with the sequence of the peplomer protein of feline infectious peritonitis virus (FIPV) Virus Res. 1987;8:363–371. doi: 10.1016/0168-1702(87)90008-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kapke P.A., Tung F.Y.T., Hogue B.G., Brian D.A., Woods R.D., Wesley R. The amino-terminal signal peptide on the porcine transmissible gastroenteritis coronavirus matrixprotein is not an absolute requirement for membrane translocation and glycosylation. Virology. 1988;165:367–376. doi: 10.1016/0042-6822(88)90581-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laude H., Rasschaert D., Huet J-C. Sequence and N-terminal processing of the transmembrane protein E1 of the coronavirus transmissible gastroenteritis virus. J. Gen. Virol. 1987;68:1687–1693. doi: 10.1099/0022-1317-68-6-1687. [DOI] [PubMed] [Google Scholar]
- Lecomte J., Cainelli-Gebara V., Mercier G., Mansour S., Talbot P.J., Lussier G., Oth D. Protection from mouse hepatitis virus type 3-induced acute disease by an anti-nucleoprotein monoclonal antibody. Arch. Virol. 1987;97:123–130. doi: 10.1007/BF01310740. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maniatis T., Fritsch E.F., Sambrook J. Cold Spring Harbor Laboratory; Cold Spring Harbor, NY: 1982. (Molecular Cloning: A Laboratory Manual). [Google Scholar]
- McKeirnan A.J., Everman J.F., Hargis A., Miller L.M., Ott R.L. Isolation of feline coronavirus from two cats with diverse disease manifestations. Feline Pract. 1981;11:16–20. [Google Scholar]
- Nakanaga K., Yamanouchi K., Fujiwara K. Protective effect of monoclonal antibodies on lethal mouse hepatitis virus infection in mice. J. Virol. 1986;59:168–171. doi: 10.1128/jvi.59.1.168-171.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pedersen N.C. Virologic and immunologic aspects of feline infectious peritonitis virus infection. Adv. Exp. Med. Biol. 1987;218:529–550. doi: 10.1007/978-1-4684-1280-2_69. [DOI] [PubMed] [Google Scholar]
- Pedersen N.C. Animal infections that defy vaccination: Equine infectious anemia, caprine encephalitis, maedi-visna, and feline infectious peritonitis virus. Adv. Vet. Sci. Comp. Med. 1989;33:413–428. doi: 10.1016/B978-0-12-039233-9.50017-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pedersen N.C., Boyle J.F. Immunologic phenomena in the effusive form of feline infectious peritonitis. Amer. J. Vet. Res. 1980;41:868–876. [PubMed] [Google Scholar]
- Porterfield J.S. Antibody-dependent enhancement of viral infectivity. Adv. Virus Res. 1986;31:335–355. doi: 10.1016/s0065-3527(08)60268-7. [DOI] [PubMed] [Google Scholar]
- Rasschaert D., Gelfi J., Laude H. Enteric coronavirus TGEV: Partial sequence of the genomic RNA, its organization and expression. Biochimie. 1987;69:591–600. doi: 10.1016/0300-9084(87)90178-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rohrmann G., Yuen L., Moss B. Transcription of vaccinia virus early genes by enzymes isolated from vaccinia virions terminates downstream of a regulatory sequence. Cell. 1986;46:1029–1035. doi: 10.1016/0092-8674(86)90702-6. [DOI] [PubMed] [Google Scholar]
- Rottier P.J.M., Welling G.W., Welling-Wester S., Niesters H.G.M., Lenstra J.A., van der Zeijst B.A.M. Predicted membrane topology of the coronavirus protein E1. Biochemistry. 1986;25:1335–1339. doi: 10.1021/bi00354a022. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A.R. Vol. 74. 1977. DNA sequencing with chain termination inhibitors; pp. 5463–5467. (Proc. Natl. Acad. Sci. USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spaan W., Cavanagh D., Horzinek M.C. Coronaviruses: Structure and genome expression. J. Gen. Virol. 1988;69:2939–2952. doi: 10.1099/0022-1317-69-12-2939. [DOI] [PubMed] [Google Scholar]
- Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982;10:4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sturman L.S., Holmes K.V., Behnke J. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid. J. Virol. 1980;33:449–462. doi: 10.1128/jvi.33.1.449-462.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vennema H., de Groot R.J., Harbour D.A., Dalderup M., Gruffydd-Jones T., Horzinek M.C., Spaan W.J.M. Early death after feline infectious peritonitis virus challenge due to recombinant vaccinia virus immunization. J. Virol. 1990;64:1407–1409. doi: 10.1128/jvi.64.3.1407-1409.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vennema H., Heijnen L., Zijderveld A., Horzinek M.C., Spaan W.J.M. Intracellular transport of recombinant coronavirus spike proteins: Implications for virus assembly. J. Virol. 1990;64:339–346. doi: 10.1128/jvi.64.1.339-346.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wachsman M., Luo J.H., Aurelian L., Perkus M.E., Paoletti E. Antigen-presenting capacity of epidermal cells infected with vaccinia virus recombinants containing the herpes simplex virus glycoprotein D, and protective immunity. J. Gen. Virol. 1989;70:2531. doi: 10.1099/0022-1317-70-9-2513. [DOI] [PubMed] [Google Scholar]
- Weiss R.C., Scott F.W. Antibody-mediated enhancement of disease in feline infectious peritonitis: Comparison with Dengue hemorrhagic fever. Comp. Immunol. Microbiol. Infect. Dis. 1981;4:175–189. doi: 10.1016/0147-9571(81)90003-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woods R.D., Wesley R.D., Kapke P.A. Neutralization of porcine transmissible gastroenteritis virus by complement-dependent monoclonal antibodies. Amer. J. Vet. Res. 1988;49:300–304. [PubMed] [Google Scholar]