Specific passage of simian immunodeficiency virus from end-stage disease results in accelerated progression to AIDS in rhesus macaques

Journal of General Virology

Volumn 80, Issue 12, 1999, Pages 3089-3097

  Holterman, Lennart ^a   Niphuis, Henk ^a   Ten Haaft, Peter J F ^a   Goudsmit, Jaap ^b   Baskin, Gary ^c   Heeney, Jonathan L ^a  

^a BIOMEDICAL PRIMATE RESEARCH CENTRE   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c TULANE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS ANTIGEN; VIRUS RNA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DISEASE COURSE; MACACA; MALE; MEMORY CELL; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALIA; MACACA; MACACA MULATTA; RNA VIRUSES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0032723572     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/0022-1317-80-12-3089     Document Type: Article

References (57)

1. Allan, J. S., Short, M., Taylor, M. E., Su, S., Hirsch, V. M., Johnson, P. R., Shaw, G. M. & Hahn, B. H. (1991). Species-specific diversity among simian immunodeficiency viruses from African green monkeys. Journal of Virology 65, 2816-2828.
2. Anzala, A. O., Ball, T. B., Rostron, T., O'Brien, S. J., Plummer, F. A. & Rowland-Jones, S. L. (1998). CCR2-64I allele and genotype association with delayed AIDS progression in African women. University of Nairobi Collaboration for HIV Research. Lancet 351, 1632-1633.
3. Baskin, G. B. & Soike, K. F. (1989). Adenovirus enteritis in SIV-infected rhesus monkeys. Journal of Infectious Diseases 160, 905-907.
4. Baskin, G. B., Martin, L. N., Rangan, S. R., Gormus, B. J., Murphey-Corb, M., Wolf, R. H. & Soike, K. F. (1986). Transmissible lymphoma and simian acquired immunodeficiency syndrome in rhesus monkeys. Journal of the National Cancer Institute 77, 127-139.
5. Daniel, M. D., Letvin, N. L., King, N. W., Sehgal, P. K., Hunt, R. D., Kanki, P. J., Essex, M. & Desrosiers, R. C. (1985). Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228, 1201-1204.
6. Daniel, M. D., Letvin, N. L., Sehgal, P. K., Hunsmann, G., Schmidt, D. K., King, N. W. & Desrosiers, R. C. (1987). Long-term persistent infection of macaque monkeys with the simian immunodeficiency virus. Journal of General Virology 68, 3183-3189.
7. Dean, M., Carrington, M., Winkler, C., Huttley, G. A., Smith, M. W., Allikmets, R., Goedert, J. J., Buchbinder, S. P., Vittinghoff, E., Gomperts, E., Donfield, S., Vlahov, D., Kaslow, R., Saah, A., Rinaldo, C., Detels, R. & O'Brien, S. J. (1996). Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 273, 1856-1862.
8. Desrosiers, R. C. & Ringler, D. J. (1989). Use of simian immunodeficiency viruses for AIDS research. Intervirology 30, 301-312.
9. Dewhurst, S., Embretson, J. E., Anderson, D. C., Mullins, J. I. & Fultz, P. N. (1990). Sequence analysis and acute pathogenicity of molecularly cloned SIVSMM-PBj14. Nature 345, 636-640.
10. Donahue, R. E., Bunnell, B. A., Zink, M. C., Metzger, M. E., Westro, R. P., Kirby, M. R., Unangst, T., Clements, J. E. & Morgan, R. A. (1998). Reduction in SIV replication in rhesus macaques infused with autologous lymphocytes engineered with antiviral genes. Nature Medicine 4, 181-186.
11. Edmonson, P., Murphey-Corb, M., Martin, L. N., Delahunty, C., Heeney, J., Kornfeld, H., Donahue, P. R., Learn, G. H., Hood, L. & Mullins, J. I. (1998). Evolution of a simian immunodeficiency virus pathogen. Journal of Virology 72, 405-414.
12. Fultz, P. N. & Zack, P. M. (1994). Unique lentivirus-host interactions: SIVsmmPBj14 infection of macaques. Virus Research 32, 205-225.
13. Fultz, P. N., McClure, H. M., Anderson, D. C. & Switzer, W. M. (1989). Identification and biologic characterization of an acutely lethal variant of simian immunodeficiency virus from sooty mangabeys (SIV/SMM). AIDS Research and Human Retroviruses 5, 397-409.
14. Fultz, P. N., Anderson, D. C., McClure, H. M., Dewhurst, S. & Mullins, J. I. (1990). SIVsmm infection of macaque and mangabey monkeys: correlation between in vivo and in vitro properties of different isolates. Developments in Biological Standardization 72, 253-258.
15. Goodenow, M., Huet, T., Saurin, W., Kwok, S., Sninsky, J. & Wain-Hobson, S. (1989). HIV-1 isolates are rapidly evolving quasispecies: evidence for viral mixtures and preferred nucleotide substitutions. Journal of Acquired Immune Deficiency Syndromes 2, 344-352.
16. Heeney, J. L. (1996). Primate models for AIDS vaccine development. AIDS 10 (Suppl. A), S115-S122.
17. Heeney, J., Bogers, W., Buijs, L., Dubbes, R., ten Haaft, P., Koornstra, W., Niphuis, H., Nara, P. & Teeuwsen, V. (1996). Immune strategies utilized by lentivirus infected chimpanzees to resist progression to AIDS. Immunology Letters 51, 45-52.
18. Hirsch, V. M. (1999). Evolution of the fittest ends in tragedy [comment]. Nature Medicine 5, 488-489.
19. Hirsch, V. M. & Johnson, P. R. (1994). Pathogenic diversity of simian immunodeficiency viruses. Virus Research 32, 183-203.
20. Hirsch, V. M., Edmondson, P., Murphey-Corb, M., Arbeille, B., Johnson, P. R. & Mullins, J. I. (1989). SIV adaptation to human cells. Nature 341, 573-574.
21. Johnson, P. R., Fomsgaard, A., Allan, J., Gravell, M., London, W. T., Olmsted, R. A. & Hirsch, V. M. (1990). Simian immunodeficiency viruses from African green monkeys display unusual genetic diversity. Journal of Virology 64, 1086-1092.
22. Kaslow, R. A., Carrington, M., Apple, R., Park, L., Munoz, A., Saah, A. J., Goedert, J. J., Winkler, C., O'Brien, S. J., Rinaldo, C., Detels, R., Blattner, W., Phair, J., Erlich, H. & Mann, D. L. (1996). Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nature Medicine 2, 405-411.
23. Kestler, H. W., III, Ringler, D. J., Mori, K., Panicali, D. L., Sehgal, P. K., Daniel, M. D. & Desrosiers, R. C. (1991). Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65, 651-662.
24. Kimata, J. T., Kuller, L., Anderson, D. B., Dailey, P. & Overbaugh, J. (1999). Emerging cytopathic and antigenic simian immunodeficiency virus variants influence AIDS progression [see comments]. Nature Medicine 5, 535-541.
25. Kirchhoff, F., Greenough, T. C., Brettler, D. B., Sullivan, J. L. & Desrosiers, R. C. (1995). Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. New England Journal of Medicine 332, 228-232.
26. Kodama, T., Burns, D. P., Kestler, H. W., III, Daniel, M. D. & Desrosiers, R. C. (1990). Molecular changes associated with replication of simian immunodeficiency virus in human cells. Journal of Medical Primatology 19, 431-437.
27. Koot, M., Keet, I. P., Vos, A. H., de Goede, R. E., Roos, M. T., Coutinho, R. A., Miedema, F., Schellekens, P. T. & Tersmette, M. (1993). Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS [see comments]. Annals of Internal Medicine 118, 681-688.
28. Koot, M., van Leeuwen, R., de Goede, R. E., Keet, I. P., Danner, S., Eeftinck Schattenkerk, J. K., Reiss, P., Tersmette, M., Lange, J. M. & Schuitemaker, H. (1999). Conversion rate towards a syncytium-inducing (SI) phenotype during different stages of human immunodeficiency virus type 1 infection and prognostic value of SI phenotype for survival after AIDS diagnosis. Journal of Infectious Diseases 179, 254-258.
29. Kornfeld, H., Riedel, N., Viglianti, G. A., Hirsch, V. & Mullins, J. L. (1987). Cloning of HTLV-4 and its relation to simian and human immunodeficiency viruses. Nature 326, 610-613.
30. Kostrikis, L. G., Huang, Y., Moore, J. P., Wolinsky, S. M., Zhang, L., Guo, Y., Deutsch, L., Phair, J., Neumann, A. U. & Ho, D. D. (1998). A chemokine receptor CCR2 allele delays HIV-1 disease progression and is associated with a CCR5 promoter mutation [see comments]. Nature Medicine 4, 350-353.
31. Lang, S. M., Iafrate, A. J., Stahl-Hennig, C., Kuhn, E. M., Nisslein, T., Kaup, F. J., Haupt, M., Hunsmann, G., Skowonski, J. & Kirchhoff, F. (1997). Association of simian immunodeficiency virus Nef with cellular serine/threonine kinases is dispensable for the development of AIDS in rhesus macaques. Nature Medicine 3, 860-865.
32. Letvin, N. L., Daniel, M. D., Sehgal, P. K., Desrosiers, R. C., Hunt, R. D., Waldron, L. M., MacKey, J. J., Schmidt, D. K., Chalifoux, L. V. & King, N. W. (1985). Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230, 71-73.
33. Li, Y., Naidu, Y., Fultz, P., Daniel, M. D. & Desrosiers, R. C. (1989). Genetic diversity of simian immunodeficiency virus. Journal of Medical Primatology 18, 261-269.
34. Marthas, M. L., Ramos, R. A., Lohman, B. L., Van Rompay, K. K., Unger, R. E., Miller, C. J., Banapour, B., Pedersen, N. C. & Luciw, P. A. (1993). Viral determinants of simian immunodeficiency virus (SIV) virulence in rhesus macaques assessed by using attenuated and pathogenic molecular clones of SIVmac. Journal of Virology 67, 6047-6055.
35. Mellors, J. W., Rinaldo, C. R., Jr, Gupta, P., White, R. M., Todd, J. A. & Kingsley, L. A. (1996). Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272, 1167-1170.
36. Meyerhans, A., Cheynier, R., Albert, J., Seth, M., Kwok, S., Sninsky, J., Morfeldt-Manson, L., Asjo, B. & Wain-Hobson, S. (1989). Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell 58, 901-910.
37. Miller, C. J. (1998). Does viral tropism play a role in heterosexual transmission of HIV? Findings in the SIV-rhesus macaque model. AIDS Research and Human Retroviruses 14 (Suppl. 1), S79-S82.
38. Miller, C. J., Marthas, M., Greenier, J., Lu, D., Dailey, P. J. & Lu, Y. (1998). In vivo replication capacity rather than in vitro macrophage tropism predicts efficiency of vaginal transmission of simian immunodeficiency virus or simian/human immunodeficiency virus in rhesus macaques. Journal of Virology 72, 3248-3258.
39. Munoz, A., Wang, M. C., Bass, S., Taylor, J. M., Kingsley, L. A., Chmiel, J. S. & Polk, B. F. (1989). Acquired immunodeficiency syndrome (AIDS)-free time after human immunodeficiency virus type 1 (HIV-1) seroconversion in homosexual men. Multicenter AIDS Cohort Study Group. American Journal of Epidemiology 130, 530-539.
40. Munoz, A., Kirby, A. J., He, Y. D., Margolick, J. B., Visscher, B. R., Rinaldo, C. R., Kaslow, R. A. & Phair, J. P. (1995). Long-term survivors with HIV-1 infection: incubation period and longitudinal patterns of CD4+ lymphocytes. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 8, 496-505.
41. Murphey-Corb, M., Martin, L. N., Rangan, S. R., Baskin, G. B., Gormus, B. J., Wolf, R. H., Andes, W. A., West, M. & Montelaro, R. C. (1986). Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature 321, 435-437.
42. Peeters, M., Fransen, K., Delaporte, E., Van der Haesevelde, M., Gershy-Damet, G. M., Kostens, L., van der Groen, G. & Piot, P. (1992). Isolation and characterization of a new chimpanzee lentivirus (simian immunodeficiency virus isolate cpz-ant) from a wild-captured chimpanzee. AIDS 6, 447-451.
43. Rosenberg, Y. J., White, B. D., Papermaster, S. F., Zack, P., Jarling, P. B., Eddy, G. A., Burke, D. S. & Lewis, M. G. (1991). Variation in T-lymphocyte activation and susceptibility to SIVPBj-14-induced acute death in macaques. Journal of Medical Primatology 20, 206-210.
44. Salvi, R., Garbuglia, A. R., Di Caro, A., Pulciani, S., Montella, F. & Benedetto, A. (1998). Grossly defective nef gene sequences in a human immunodeficiency virus type 1-seropositive long-term nonprogressor. Journal of Virology 72, 3646-3657.
45. Sawai, E. T., Khan, I. H., Montbriand, P. M., Peterlin, B. M., Cheng-Mayer, C. & Lueiw, P. A. (1996). Activation of PAK by HIV and SIV Nef: importance for AIDS in rhesus macaques. Current Biology 6, 1519-1527.
46. Simon, M. A., Brodie, S. J., Sasseville, V. G., Chalifoux, L. V., Desrosiers, R. C. & Ringler, D. J. (1994). Immunopathogenesis of SIVmac. Virus Research 32, 227-251.
47. Smith, M. W., Dean, M., Carrington, M., Huttley, G. A. & O'Brien, S. J. (1997). CCR5-delta 32 gene deletion in HIV-1 infected patients. Lancet 350, 741; discussion 742.
48. ten Haaft, P., Verstrepen, B., Uberla, K., Rosenwirth, B. & Heeney, J. (1998). A pathogenic threshold of virus load defined in simian immunodeficiency virus-or simian-human immunodeficiency virus-infected macaques. Journal of Virology 72, 10281-10285.
49. Tersmette, M., de Goede, R. E., Al, B. J., Winkel, I. N., Gruters, R. A., Cuypers, H. T., Huisman, H. G. & Miedema, F. (1988). Differential syncytium-inducing capacity of human immunodeficiency virus isolates: frequent detection of syncytium-inducing isolates in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. Journal of Virology 62, 2026-2032.
50. Tersmette, M., Gruters, R. A., de Wolf, F., de Goede, R. E., Lange, J. M., Schellekens, P. T., Goudsmit, J., Huisman, H. G. & Miedema, F. (1989a). Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. Journal of Virology 63, 2116-2125.
51. Tersmette, M., Lange, J. M., de Goede, R. E., de Wolf, F., Eeftinck-Schattenkerk, J. K., Schellekens, P. T., Coutinho, R. A., Huisman, J. G., Goudsmit, J. & Miedema, F. (1989b). Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet i, 983-985.
52. Trichel, A. M., Roberts, E. D., Wilson, L. A., Martin, L. N., Ruprecht, R. M. & Murphey-Corb, M. (1997). SIV/DeltaB670 transmission across oral, colonic, and vaginal mucosae in the macaque. Journal of Medical Primatology 26, 3-10.
53. Tsujimoto, H., Hasegawa, A., Maki, N., Fukasawa, M., Miura, T., Speidel, S., Cooper, R. W., Moriyama, E. N., Gojobori, T. & Hayami, M. (1989). Sequence of a novel simian immunodeficiency virus from a wild-caught African mandrill. Nature 341, 539-541.
54. Valli, P. J., Lukashov, V. V., Heeney, J. L. & Goudsmit, J. (1998). Shortening of the symptom-free period in rhesus macaques is associated with decreasing nonsynonymous variation in the env variable regions of simian immunodeficiency virus SlVsm during passage. Journal of Virology 72, 7494-7500.
55. Van Rompay, K. K., Berardi, C. J., Aguirre, N. L., Bischofberger, N., Lietman, P. S., Pedersen, N. C. & Marthas, M. L. (1998). Two doses of PMPA protect newborn macaques against oral simian immunodeficiency virus infection. AIDS 12, F79-F83.
56. Winkler, C., Modi, W., Smith, M. W., Nelson, G. W., Wu, X., Carrington, M., Dean, M., Honjo, T., Tashiro, K., Yabe, D., Buchbinder, S., Vittinghoff, E., Goedert, J. J., O'Brien, T. R., Jacobson, L. P., Detels, R., Donfield, S., Willoughby, A., Gomperts, E., Vlahov, D., Phair, J. & O'Brien, S. J. (1998). Genetic restriction of AIDS pathogenesis by an SDF-1 chemokine gene variant. ALIVE Study, Hemophilia Growth and Development Study (HGDS), Multicenter AIDS Cohort Study (MACS), Multicenter Hemophilia Cohort Study (MHCS), San Francisco City Cohort. Science 279, 389-393.
57. Zacharias, D. A., Garamszegi, N. & Strehler, E. E. (1994). Characterization of persistent artifacts resulting from RT-PCR of alternatively spliced mRNAs. Biotechniques 17, 652-655.