Selection of a rare neutralization-resistant variant following passive transfer of convalescent immune plasma in equine infectious anemia virus-challenged SCID horses

Journal of Virology

Volumn 84, Issue 13, 2010, Pages 6536-6548

  Taylor, Sandra D ^a   Leib, Steven R ^a   Carpenter, Susan ^a,b   Mealey, Robert H ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A 2150; ANTISERUM; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EQUINE INFECTION ANEMIA; EQUINE INFECTIOUS ANEMIA; EQUINE INFECTIOUS ANEMIA VIRUS; FEVER; GENE AMPLIFICATION; GENE SEQUENCE; HORSE; INOCULATION; LENTIVIRUS INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEVERE COMBINED IMMUNODEFICIENCY; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; EQUINE INFECTIOUS ANEMIA; HORSES; IMMUNE SERA; INFECTIOUS ANEMIA VIRUS, EQUINE; SEVERE COMBINED IMMUNODEFICIENCY; T-LYMPHOCYTES, CYTOTOXIC;

EQUIDAE; EQUINE INFECTIOUS ANEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS;

EID: 77953318297     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00218-10     Document Type: Article

References (63)

1. Ball, J. M., K. E. Rushlow, C. J. Issel, and R. C. Montelaro. 1992. Detailed mapping of the antigenicity of the surface unit glycoprotein of equine infectious anemia virus by using synthetic peptide strategies. J. Virol. 66:732-742.
2. Carpenter, S., L. H. Evans, M. Sevoian, and B. Chesebro. 1987. Role of the host immune response in selection of equine infectious anemia virus variants. J. Virol. 61:3783-3789. (Pubitemid 18011476)
3. Carpenter, S., L. H. Evans, M. Sevoian, and B. Chesebro. 1990. In vivo and in vitro selection of equine infectious anemia virus variants, p. 99-115. In E. Kurstak, R. G. Marusyk, F. A. Murphy, and M. H. V. Van Regenmortel (ed.), Applied virology research. Plenum Publishing Corp., New York, NY.
4. Chen, L., Y. D. Kwon, T. Zhou, X. Wu, S. O'Dell, L. Cavacini, A. J. Hessell, M. Pancera, M. Tang, L. Xu, Z. Y. Yang, M. Y. Zhang, J. Arthos, D. R. Burton, D. S. Dimitrov, G. J. Nabsel, M. R. Posner, J. Sodroski, R. Wyatt, J. R. Mascola, and P. D. Kwong. 2009. Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326:1123-1127.
5. Chung, C., R. H. Mealey, and T. C. McGuire. 2004. CTL from EIAV carrier horses with diverse MHC class I alleles recognize epitope clusters in Gag matrix and capsid proteins. Virology 327:144-154.
6. Chung, C., R. H. Mealey, and T. C. McGuire. 2005. Evaluation of high functional avidity CTL to Gag epitope clusters in EIAV carrier horses. Virology 342:228-239.
7. Coggins, L., N. L. Norcross, and S. R. Nusbaum. 1972. Diagnosis of equine infectious anemia by immunodiffusion test. Am. J. Vet. Res. 33:11-18.
8. Craigo, J. K., C. Leroux, L. Howe, J. D. Steckbeck, S. J. Cook, C. J. Issel, and R. C. Montelaro. 2002. Transient immune suppression of inapparent carriers infected with a principal neutralizing domain-deficient equine infectious anaemia virus induces neutralizing antibodies and lowers steady-state virus replication. J. Gen. Virol. 83:1353-1359.
9. Craigo, J. K., B. Zhang, S. Barnes, T. L. Tagmyer, S. J. Cook, C. J. Issel, and R. C. Montelaro. 2007. Envelope variation as a primary determinant of lentiviral vaccine efficacy. Proc. Natl. Acad. Sci. U. S. A. 104:15105-15110.
10. Crawford, T. B., K. J. Wardrop, S. J. Tornquist, E. Reilich, K. M. Meyers, and T. C. McGuire. 1996. A primary production deficit in the thrombocytopenia of equine infectious anemia. J. Virol. 70:7842-7850.
11. Dickover, R., E. Garratty, K. Yusim, C. Miller, B. Korber, and Y. Bryson. 2006. Role of maternal autologous neutralizing antibody in selective perinatal transmission of human immunodeficiency virus type 1 escape variants. J. Virol. 80:6525-6533.
12. Ferrantelli, F., K. A. Buckley, R. A. Rasmussen, A. Chalmers, T. Wang, P. L. Li, A. L. Williams, R. Hofmann-Lehmann, D. C. Montefiori, L. A. Cavacini, H. Katinger, G. Stiegler, D. C. Anderson, H. M. McClure, and R. M. Ruprecht. 2007. Time dependence of protective post-exposure prophylaxis with human monoclonal antibodies against pathogenic SHIV challenge in newborn macaques. Virology 358:69-78.
13. Ferrantelli, F., R. Hofmann-Lehmann, R. A. Rasmussen, T. Wang, W. Xu, P. L. Li, D. C. Montefiori, L. A. Cavacini, H. Katinger, G. Stiegler, D. C. Anderson, H. M. McClure, and R. M. Ruprecht. 2003. Post-exposure prophylaxis with human monoclonal antibodies prevented SHIV89.6P infection or disease in neonatal macaques. AIDS 17:301-309.
14. Ferrantelli, F., R. A. Rasmussen, K. A. Buckley, P. L. Li, T. Wang, D. C. Montefiori, H. Katinger, G. Stiegler, D. C. Anderson, H. M. McClure, and R. M. Ruprecht. 2004. Complete protection of neonatal rhesus macaques against oral exposure to pathogenic simian-human immunodeficiency virus by human anti-HIV monoclonal antibodies. J. Infect. Dis. 189:2167-2173.
15. Floyd, R. A., J. E. Schneider, Jr., and D. P. Dittmer. 2004. Methylene blue photoinactivation of RNA viruses. Antiviral Res. 61:141-151.
16. Frost, S. D., T. Wrin, D. M. Smith, S. L. Kosakovsky Pond, Y. Liu, E. Paxinos, C. Chappey, J. Galovich, J. Beauchaine, C. J. Petropoulos, S. J. Little, and D. D. Richman. 2005. Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc. Natl. Acad. Sci. U. S. A. 102:18514-18519.
17. Hotzel, I. 2003. Conservation of the human immunodeficiency virus type 1 gp120 V1/V2 stem/loop structure in the equine infectious anemia virus (EIAV) gp90. AIDS Res. Hum. Retroviruses 19:923-924.
18. Howe, L., J. K. Craigo, C. J. Issel, and R. C. Montelaro. 2005. Specificity of serum neutralizing antibodies induced by transient immune suppression of inapparent carrier ponies infected with a neutralization- resistant equine infectious anemia virus envelope strain. J. Gen. Virol. 86:139-149.
19. Howe, L., C. Leroux, C. J. Issel, and R. C. Montelaro. 2002. Equine infectious anemia virus envelope evolution in vivo during persistent infection progressively increases resistance to in vitro serum antibody neutralization as a dominant phenotype. J. Virol. 76:10588-10597.
20. Hussain, K. A., C. J. Issel, K. L. Schnorr, P. M. Rwambo, and R. C. Montelaro. 1987. Antigenic analysis of equine infectious anemia virus (EIAV) variants by using monoclonal antibodies: epitopes of glycoprotein gp90 of EIAV stimulate neutralizing antibodies. J. Virol. 61:2956-2961.
21. Karlsson Hedestam, G. B., R. A. Fouchier, S. Phogat, D. R. Burton, J. Sodroski, and R. T. Wyatt. 2008. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6:143-155.
22. Kono, Y. 1988. Antigenic variation of equine infectious anemia virus as detected by virus neutralization. Brief report. Arch. Virol. 98:91-97.
23. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
24. Leroux, C., J. K. Craigo, C. J. Issel, and R. C. Montelaro. 2001. Equine infectious anemia virus genomic evolution in progressor and nonprogressor ponies. J. Virol. 75:4570-4583.
25. Leroux, C., C. J. Issel, and R. C. Montelaro. 1997. Novel and dynamic evolution of equine infectious anemia virus genomic quasispecies associated with sequential disease cycles in an experimentally infected pony. J. Virol. 71:9627-9639. (Pubitemid 27492410)
26. Li, H., X. Zhang, X. Fan, T. Shen, X. Tong, R. Shen, and Y. Shao. 2005. A conservative domain shared by HIV gp120 and EIAV gp90: implications for HIV vaccine design. AIDS Res. Hum. Retroviruses 21:1057-1059.
27. Mahalanabis, M., P. Jayaraman, T. Miura, F. Pereyra, E. M. Chester, B. Richardson, B. Walker, and N. L. Haigwood. 2009. Continuous viral escape and selection by autologous neutralizing antibodies in drug-naive human immunodeficiency virus controllers. J. Virol. 83:662-672.
28. Mascola, J. R. 2007. HIV/AIDS: allied responses. Nature 449:29-30.
29. Mascola, J. R., M. G. Lewis, G. Stiegler, D. Harris, T. C. VanCott, D. Hayes, M. K. Louder, C. R. Brown, C. V. Sapan, S. S. Frankel, Y. Lu, M. L. Robb, H. Katinger, and D. L. Birx. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73:4009-4018.
30. McGuire, T. C., S. R. Leib, S. M. Lonning, W. Zhang, K. M. Byrne, and R. H. Mealey. 2000. Equine infectious anaemia virus proteins with epitopes most frequently recognized by cytotoxic T lymphocytes from infected horses. J. Gen. Virol. 81:2735-2739.
31. McGuire, T. C., K. I. O'Rourke, and L. E. Perryman. 1990. Immunopathogenesis of equine infectious anemia lentivirus disease. Dev. Biol. Stand. 72:31-37.
32. McGuire, T. C., M. J. Poppie, and K. L. Banks. 1974. Combined (B- and T-lymphocyte) immunodeficiency: a fatal genetic disease in Arabian foals. J. Am. Vet. Med. Assoc. 164:70-76.
33. Mealey, R. H., D. G. Fraser, J. L. Oaks, G. H. Cantor, and T. C. McGuire. 2001. Immune reconstitution prevents continuous equine infectious anemia virus replication in an Arabian foal with severe combined immunodeficiency: lessons for control of lentiviruses. Clin. Immunol. 101:237-247.
34. Mealey, R. H., S. R. Leib, M. H. Littke, B. Wagner, D. W. Horohov, and T. C. McGuire. 2009. Viral load and clinical disease enhancement associated with a lentivirus cytotoxic T lymphocyte vaccine regimen. Vaccine 27:2453-2468.
35. Mealey, R. H., S. R. Leib, S. L. Pownder, and T. C. McGuire. 2004. Adaptive immunity is the primary force driving selection of equine infectious anemia virus envelope SU variants during acute infection. J. Virol. 78:9295-9305.
36. Mealey, R. H., M. H. Littke, S. R. Leib, W. C. Davis, and T. C. McGuire. 2008. Failure of low-dose recombinant human IL-2 to support the survival of virus-specific CTL clones infused into severe combined immunodeficient foals: lack of correlation between in vitro activity and in vivo efficacy. Vet. Immunol. Immunopathol. 121:8-22.
37. Mealey, R. H., A. Sharif, S. A. Ellis, M. H. Littke, S. R. Leib, and T. C. McGuire. 2005. Early detection of dominant Env-specific and subdominant Gag-specific CD8 lymphocytes in equine infectious anemia virus-infected horses using major histocompatibility complex class I/peptide tetrameric complexes. Virology 339:110-126.
38. Mealey, R. H., B. Zhang, S. R. Leib, M. H. Littke, and T. C. McGuire. 2003. Epitope specificity is critical for high and moderate avidity cytotoxic T lymphocytes associated with control of viral load and clinical disease in horses with equine infectious anemia virus. Virology 313:537-552.
39. Miura, T., M. A. Brockman, A. Schneidewind, M. Lobritz, F. Pereyra, A. Rathod, B. L. Block, Z. L. Brumme, C. J. Brumme, B. Baker, A. C. Rothchild, B. Li, A. Trocha, E. Cutrell, N. Frahm, C. Brander, I. Toth, E. J. Arts, T. M. Allen, and B. D. Walker. 2009. HLA-B57/B*5801 human immunodeficiency virus type 1 elite controllers select for rare Gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte [corrected] recognition. J. Virol. 83:2743-2755.
40. Mohr, H., J. Knuver-Hopf, U. Gravemann, A. Redecker-Klein, and T. H. Muller. 2004. West Nile virus in plasma is highly sensitive to methylene blue-light treatment. Transfusion 44:886-890.
41. Motulsky, H. 1995. Intuitive biostatistics. Oxford University Press, New York, NY.
42. O'Rourke, K., L. E. Perryman, and T. C. McGuire. 1988. Antiviral, antiglycoprotein and neutralizing antibodies in foals with equine infectious anaemia virus. J. Gen. Virol. 69:667-674.
43. O'Rourke, K. I., L. E. Perryman, and T. C. McGuire. 1989. Cross-neutralizing and subclass characteristics of antibody from horses with equine infectious anemia virus. Vet. Immunol. Immunopathol. 23:41-49.
44. Palmer, S., M. Kearney, F. Maldarelli, E. K. Halvas, C. J. Bixby, H. Bazmi, D. Rock, J. Falloon, R. T. Davey, Jr., R. L. Dewar, J. A. Metcalf, S. Hammer, J. W. Mellors, and J. M. Coffin. 2005. Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol. 43: 406-413.
45. Perryman, L. E., T. C. McGuire, and T. B. Crawford. 1978. Maintenance of foals with combined immunodeficiency: causes and control of secondary infections. Am. J. Vet. Res. 39:1043-1047.
46. Perryman, L. E., K. I. O'Rourke, and T. C. McGuire. 1988. Immune responses are required to terminate viremia in equine infectious anemia lentivirus infection. J. Virol. 62:3073-3076.
47. Perryman, L. E., and R. L. Torbeck. 1980. Combined immunodeficiency of Arabian horses: confirmation of autosomal recessive mode of inheritance. J. Am. Vet. Med. Assoc. 176:1250-1251.
48. Quakkelaar, E. D., E. M. Bunnik, F. P. van Alphen, B. D. Boeser-Nunnink, A. C. van Nuenen, and H. Schuitemaker. 2007. Escape of human immunodeficiency virus type 1 from broadly neutralizing antibodies is not associated with a reduction of viral replicative capacity in vitro. Virology 363:447-453.
49. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U. S. A. 100:4144-4149.
50. Rybarczyk, B. J., D. Montefiori, P. R. Johnson, A. West, R. E. Johnston, and R. Swanstrom. 2004. Correlation between env V1/V2 region diversification and neutralizing antibodies during primary infection by simian immunodeficiency virus sm in rhesus macaques. J. Virol. 78:3561-3571.
51. Salazar-Gonzalez, J. F., E. Bailes, K. T. Pham, M. G. Salazar, M. B. Guffey, B. F. Keele, C. A. Derdeyn, P. Farmer, E. Hunter, S. Allen, O. Manigart, J. Mulenga, J. A. Anderson, R. Swanstrom, B. F. Haynes, G. S. Athreya, B. T. Korber, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 2008. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 82: 3952-3970.
52. Salinovich, O., S. L. Payne, R. C. Montelaro, K. A. Hussain, C. J. Issel, and K. L. Schnorr. 1986. Rapid emergence of novel antigenic and genetic variants of equine infectious anemia virus during persistent infection. J. Virol. 57:71-80. (Pubitemid 16147919)
53. Scheid, J. F., H. Mouquet, N. Feldhahn, M. S. Seaman, K. Velinzon, J. Pietzsch, R. G. Ott, R. M. Anthony, H. Zebroski, A. Hurley, A. Phogat, B. Chakrabarti, Y. Li, M. Connors, F. Pereyra, B. D. Walker, H. Wardemann, D. Ho, R. T. Wyatt, J. R. Mascola, J. V. Ravetch, and M. C. Nussenzweig. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458:636-640.
54. Shibata, R., T. Igarashi, N. Haigwood, A. Buckler-White, R. Ogert, W. Ross, R. Willey, M. W. Cho, and M. A. Martin. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5:204-210.
55. Shin, E. K., L. E. Perryman, and K. Meek. 1997. A kinase-negative mutation of DNA-PK(CS) in equine SCID results in defective coding and signal joint formation. J. Immunol. 158:3565-3569.
56. Siliciano, R. F., A. D. Keegan, R. Z. Dintzis, H. M. Dintzis, and H. S. Shin. 1985. The interaction of nominal antigen with T cell antigen receptors. I. Specific binding of multivalent nominal antigen to cytolytic T cell clones. J. Immunol. 135:906-914.
57. Sponseller, B. A., W. O. Sparks, Y. Wannemuehler, Y. Li, A. K. Antons, J. L. Oaks, and S. Carpenter. 2007. Immune selection of equine infectious anemia virus env variants during the long-term inapparent stage of disease. Virology 363:156-165.
58. Sun, C., B. Zhang, J. Jin, and R. C. Montelaro. 2008. Binding of equine infectious anemia virus to the equine lentivirus receptor-1 is mediated by complex discontinuous sequences in the viral envelope gp90 protein. J. Gen. Virol. 89:2011-2019.
59. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
60. Wiler, R., R. Leber, B. B. Moore, L. F. VanDyk, L. E. Perryman, and K. Meek. 1995. Equine severe combined immunodeficiency: a defect in V(D)J. recombination and DNA-dependent protein kinase activity. Proc. Natl. Acad. Sci. U. S. A. 92:11485-11489.
61. Zhang, B., S. Jin, J. Jin, F. Li, and R. C. Montelaro. 2005. A tumor necrosis factor receptor family protein serves as a cellular receptor for the macrophage-tropic equine lentivirus. Proc. Natl. Acad. Sci. U. S. A. 102:9918-9923.
62. Zhang, W., D. B. Auyong, J. L. Oaks, and T. C. McGuire. 1999. Natural variation of equine infectious anemia virus Gag protein cytotoxic T lymphocyte epitopes. Virology 261:242-252.
63. Zolla-Pazner, S. 2004. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol. 4:199-210.