1887

Abstract

In order to analyse the pattern of sequence variation in maedi–visna virus (MVV) in persistently infected sheep and to answer the question of whether antigenic variants are selected in a long-term MVV infection, an 87 bp variable region in the gene of ten antigenic variants and 24 non-variants was sequenced. Nine of the ten antigenic variants had mutations in this region, comprising 24 point mutations and a deletion of 3 bp. Twenty-three of the point mutations (96%) were non-synonymous. There was only a single mutation in this region in the 24 non-variants. A type-specific neutralizing antibody response appeared in all the sheep 2–5 months post-infection, and in most sheep more broadly reacting neutralizing antibodies appeared up to 4 years later. All the antigenic variants were neutralized by the broadly reacting sera. It is noteworthy that the antigenic variants were isolated at a time when only the type-specific antibodies were acting, before the broadly reacting antibodies appeared. The same picture emerged when molecularly cloned virus was used for infection. Three sheep were infected with a molecularly cloned virus, and of six virus isolates, one was an antigenic variant. This variant arose in the absence of broadly reacting antibodies. The results indicate that there is selection for mutants that escape neutralization.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-10-2543
2002-10-01
2020-01-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/10/0832543a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-10-2543&mimeType=html&fmt=ahah

References

  1. Agnarsdóttir, G., Thorsteinsdóttir, H., Óskarsson, T., Matthı́asdóttir, S., Haflidadóttir, B. S., Andrésson, Ó. S. & Andrésdóttir, V. ( 2000; ). The long terminal repeat is a determinant of cell tropism of maedi–visna virus. Journal of General Virology 81, 1901-1905.
    [Google Scholar]
  2. Andrésdóttir, V., Tang, X., Agnarsdóttir, G., Andrésson, Ó. S., Georgsson, G., Skraban, R., Torsteinsdóttir, S., Rafnar, B., Benediktsdóttir, E., Matthı́asdóttir, S., Árnadóttir, S., Högnadóttir, S., Pálsson, P. A. & Pétursson, G. ( 1998; ). Biological and genetic differences between lung- and brain-derived isolates of maedi–visna virus. Virus Genes 16, 281-293.[CrossRef]
    [Google Scholar]
  3. Andrésson, Ó. S., Elser, J. E., Tobin, G. J., Greenwood, J. D., Gonda, M. A., Georgsson, G., Andrésdóttir, V., Benediktsdóttir, E., Carlsdóttir, H. M., Mantyla, E. O., Rafnar, B., Pálsson, P. A., Casey, J. W. & Pétursson, G. ( 1993; ). Nucleotide sequence and biological properties of pathogenic proviral molecular clone of neurovirulent visna virus. Virology 193, 89-105.[CrossRef]
    [Google Scholar]
  4. Back, N. K. T., Smit, L., de Jong, J.-J., Keulen, W., Schutten, M., Goudsmit, J. & Tersmette, M. ( 1994; ). An N-glycan within the human immunodeficiency virus type 1 gp120 V3 loop affects virus neutralization. Virology 199, 431-438.[CrossRef]
    [Google Scholar]
  5. Braun, M. J., Clements, J. E. & Gonda, M. A. ( 1987; ). The visna virus genome: evidence for a hypervariable site in the env gene and sequence homology among lentivirus envelope proteins. Journal of Virology 61, 4046-4054.
    [Google Scholar]
  6. Burns, D. P. W., Collignon, C. & Desrosiers, R. C. ( 1993; ). Simian immunodeficiency virus mutants resistant to serum neutralization arise during persistent infection of rhesus monkeys. Journal of Virology 67, 4104-4113.
    [Google Scholar]
  7. Cheevers, W. P., Cordery-Cotter, R., McGuire, T. C. & DeMartini, J. C. ( 1999; ). Neutralizing antibody responses and evolution of antigenic variants in monozygotic twin lambs infected with phenotypically distinct ovine lentiviruses. Virology 258, 382-388.[CrossRef]
    [Google Scholar]
  8. Choi, W. S., Collignon, C., Thiriart, C., Burns, D. P. W., Stott, E. J., Kent, K. A. & Desrosiers, R. C. ( 1994; ). Effects of natural sequence variation on recognition by monoclonal antibodies that neutralize simian immunodeficiency virus infectivity. Journal of Virology 68, 5395-5402.
    [Google Scholar]
  9. Clements, J. E., Montelaro, R. C., Zink, M. C., Amedee, A. M., Miller, S., Trichel, A. M., Jagerski, B., Hauer, D., Martin, L. N., Bohm, R. P. & Murphey-Corb, M. ( 1995; ). Cross-protective immune responses induced in rhesus macaques by immunization with attenuated macrophage-tropic simian immunodeficiency virus. Journal of Virology 69, 2737-2744.
    [Google Scholar]
  10. Domingo, E., Dı́ez, J., Martı́nez, M. A., Hernández, J., Holguı́n, A., Borrego, B. & Mateu, M. G. ( 1993; ). New observations on antigenic diversification of RNA viruses. Antigenic variation is not dependent on immune selection. Journal of General Virology 74, 2039-2045.[CrossRef]
    [Google Scholar]
  11. Dubois-Dalq, M., Narayan, O. & Griffin, D. E. ( 1979; ). Cell surface changes associated with mutation of visna virus in antibody-treated cell cultures. Virology 92, 353-366.[CrossRef]
    [Google Scholar]
  12. Ellis, T. M., Wilcox, G. E. & Robinson, W. F. ( 1987; ). Antigenic variation of caprine arthritis encephalitis virus during persistent infection of goats. Journal of General Virology 68, 3145-3152.[CrossRef]
    [Google Scholar]
  13. Gendelman, H. E., Narayan, O., Kennedy-Stoskopf, S., Kennedy, P. G. E., Ghotbi, Z., Clements, J. E., Stanley, J. & Pezeshkpour, G. ( 1986; ). Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages. Journal of Virology 58, 67-74.
    [Google Scholar]
  14. Georgsson, G., Torsteinsdóttir, S., Pétursson, G., Pálsson, P. A. & Andrésson, Ó. S. ( 1993; ). Role of the immune response in visna, a lentiviral central nervous system disease of sheep. In Animal models of HIV and other retroviral infections , pp. 183-195. Edited by P. Racz, N. L. Levtin & J. C. Gluckman. Basel:Karger.
  15. Griffin, D. E., Narayan, O. & Adams, R. J. ( 1978; ). Early immune responses in visna, a slow disease of sheep. Journal of Infectious Diseases 138, 340-350.[CrossRef]
    [Google Scholar]
  16. Gudnadóttir, M. ( 1974; ). Visna-maedi in sheep. Progress in Medical Virology 18, 336-349.
    [Google Scholar]
  17. Javaherian, K., Langlois, A. J., Montefiori, D. C., Kent, K. A., Ryan, K. A., Wyman, P. D., Stott, J., Bolognesi, D. P., Murphey-Corb, M. & Larosa, G. J. ( 1994; ). Studies of the conformation-dependent neutralizing epitopes of simian immunodeficiency virus envelope protein. Journal of Virology 68, 2624-2631.
    [Google Scholar]
  18. Kono, Y., Kobayashi, K. & Fukunaga, Y. ( 1973; ). Antigenic drift of equine infectious anemia virus in chronically infected horses. Archiv für die gesamte Virusforschung 41, 1-10.[CrossRef]
    [Google Scholar]
  19. Larsen, H. J., Hyllseth, B. & Krogsrud, J. ( 1982; ). Experimental maedi virus infection in sheep: early cellular and humoral immune response during three years following parenteral inoculation. American Journal of Veterinary Research 43, 379-383.
    [Google Scholar]
  20. Leonard, C. K., Spellman, M. W., Riddle, L., Harris, R. J., Thomas, J. N. & Gregory, T. J. ( 1990; ). Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant HIV envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. Journal of Biological Chemistry 265, 10373-10382.
    [Google Scholar]
  21. Li, W.-H., Wu, C.-I. & Luo, C.-C. ( 1985; ). A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Molecular Biology and Evolution 2, 150-174.
    [Google Scholar]
  22. Li, Y., Luo, L., Rasool, N. & Kang, C. Y. ( 1993; ). Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding. Journal of Virology 67, 584-588.
    [Google Scholar]
  23. Lutley, R., Pétursson, G., Pálsson, P. A., Georgsson, G., Klein, J. & Nathanson, N. ( 1983; ). Antigenic drift in visna: virus variation during long-term infection of Icelandic sheep. Journal of General Virology 64, 1433-1440.[CrossRef]
    [Google Scholar]
  24. McGuire, T. C., Norton, L. K., O’Rourke, K. I. & Cheevers, W. P. ( 1988; ). Antigenic variation of neutralization-sensitive epitopes of caprine arthritis–encephalitis lentivirus during persistent arthritis. Journal of Virology 62, 3488-3492.
    [Google Scholar]
  25. McKeating, J. A., Gow, J., Goudsmit, J., Pearl, L. H., Mulder, C. & Weiss, R. A. ( 1989; ). Characterization of HIV-1 neutralization escape mutants. AIDS 3, 777-784.[CrossRef]
    [Google Scholar]
  26. McKnight, A., Weiss, R. A., Shotton, C., Takeuchi, Y., Hoshino, H. & Clapham, P. R. ( 1995; ). Change in tropism upon immune escape by human immunodeficiency virus. Journal of Virology 69, 3167-3170.
    [Google Scholar]
  27. Montelaro, R. C., Perekh, B., Orrego, A. & Issel, C. J. ( 1984; ). Antigenic variation during persistent infection by equine infectious anemia virus, a retrovirus. Journal of Biological Chemistry 259, 10539-10544.
    [Google Scholar]
  28. Narayan, O., Griffin, D. E. & Chase, J. ( 1977; ). Antigenic shift of visna virus in persistently infected sheep. Science 197, 376-378.[CrossRef]
    [Google Scholar]
  29. Pétursson, G., Nathanson, N., Georgsson, G., Panitch, H. & Pálsson, P. A. ( 1976; ). Pathogenesis of visna. I. Sequential virologic, serologic, and pathologic studies. Laboratory Investigation 35, 402-412.
    [Google Scholar]
  30. Reitter, J. N., Means, R. E. & Desrosiers, R. C. ( 1998; ). A role for carbohydrates in immune evasion in AIDS. Nature Medicine 4, 679-684.[CrossRef]
    [Google Scholar]
  31. Sargan, D. R., Bennet, I. D., Cousens, C., Roy, D. J., Blacklaws, B. A., Dalziel, R. G., Watt, N. J. & McConnell, I. ( 1991; ). Nucleotide sequence of EV1, a British isolate of maedi–visna virus. Journal of General Virology 72, 1893-1903.[CrossRef]
    [Google Scholar]
  32. Schønning, K., Jansson, B., Olofsson, S., Nielsen, J. O. & Hansen, J.-E. S. ( 1996; ). Resistance to V3-directed neutralization caused by an N-linked oligosaccharide depends on the quaternary structure of the HIV-1 envelope oligomer. Virology 218, 134-140.[CrossRef]
    [Google Scholar]
  33. Siebelink, K. H. J., Rimmelzwaan, G. F., Bosch, M. L., Meloen, R. H. & Osterhaus, A. D. M. E. ( 1993; ). A single amino acid substitution in hypervariable region 5 of the envelope protein of feline immunodeficiency virus allows escape from virus neutralization. Journal of Virology 67, 2202-2208.
    [Google Scholar]
  34. Sigurdsson, B. & Pálsson, P. A. ( 1958; ). Visna of sheep. A slow demyelinating infection. British Journal of Experimental Pathology 39, 519-528.
    [Google Scholar]
  35. Sigurdsson, B., Thormar, H. & Pálsson, P. A. ( 1960; ). Cultivation of visna virus in tissue culture. Archiv für die gesamte Virusforschung 10, 368-380.[CrossRef]
    [Google Scholar]
  36. Sihvonen, L. ( 1981; ). Early immune responses in experimental maedi. Research in Veterinary Science 30, 217-222.
    [Google Scholar]
  37. Skraban, R., Matthı́asdóttir, S., Torsteinsdóttir, S., Agnarsdóttir, G., Gudmundsson, B., Georgsson, G., Meloen, R. H., Andrésson, Ó. S., Staskus, K. A., Thormar, H. & Andrésdóttir, V. ( 1999; ). Naturally occurring mutations within 39 amino acids in the envelope glycoprotein of maedi–visna virus alter the neutralization phenotype. Journal of Virology 73, 8064-8072.
    [Google Scholar]
  38. Sonigo, P., Alizon, M., Staskus, K., Klatzmann, D., Cole, S., Danos, O., Retzel, E. & Wain-Hobson, S. ( 1985; ). Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell 42, 369-382.[CrossRef]
    [Google Scholar]
  39. Thormar, H. & Helgadóttir, H. ( 1965; ). A comparison of visna and maedi viruses. II. Serological relationship. Research in Veterinary Science 6, 456-465.
    [Google Scholar]
  40. Thormar, H., Barshatzky, M. R., Arnesen, K. & Kozlowski, P. B. ( 1983; ). The emergence of antigenic variants is a rare event in long-term visna virus infection in vivo. Journal of General Virology 64, 1427-1432.[CrossRef]
    [Google Scholar]
  41. Torsteinsdóttir, S., Georgsson, G., Gı́sladóttir, E., Rafnar, B., Pálsson, P. A. & Pétursson, G. ( 1992; ). Pathogenesis of central nervous system lesions in visna: cell-mediated immunity and lymphocyte subsets in blood, brain and cerebrospinal fluid. Journal of Neuroimmunology 41, 149-158.[CrossRef]
    [Google Scholar]
  42. Valas, S., Benoit, C., Baudry, C., Perrin, G. & Mamoun, R. Z. ( 2000; ). Variability and immunogenicity of caprine arthritis–encephalitis virus surface glycoprotein. Journal of Virology 74, 6178-6185.[CrossRef]
    [Google Scholar]
  43. Wolfs, T. F. W., Zwart, G., Bakker, M., Valk, M., Kuiken, C. L. & Goudsmit, J. ( 1991; ). Naturally occurring mutations within HIV-1 V3 genomic RNA lead to antigenic variation dependent on a single amino acid substitution. Virology 185, 195-205.[CrossRef]
    [Google Scholar]
  44. Wolinsky, S. M., Korber, B. T. M., Neumann, A. U., Daniels, M., Kunstman, K. J., Whetsell, A. J., Furtado, M. R., Cao, Y., Ho, D. D., Safrit, J. T. & Koup, R. A. ( 1996; ). Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272, 537-541.[CrossRef]
    [Google Scholar]
  45. Yoshida, K., Nakamura, M. & Ohno, T. ( 1997; ). Mutations of the HIV type 1 V3 loop under selection pressure with neutralizing monoclonal antibody NM-01. AIDS Research and Human Retroviruses 13, 1283-1290.[CrossRef]
    [Google Scholar]
  46. Zhang, P. F., Chen, X., Fu, D. W., Margolick, J. B. & Quinnan, G. V.Jr ( 1999; ). Primary virus envelope cross-reactivity of the broadening neutralizing antibody response during early chronic human immunodeficiency virus type 1 infection. Journal of Virology 73, 5225-5230.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-10-2543
Loading
/content/journal/jgv/10.1099/0022-1317-83-10-2543
Loading

Data & Media loading...

Most cited articles

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