Apoptosis correlates with immune activation in intestinal lymphoid tissue from macaques acutely infected by a highly enteropathic simian immunodeficiency virus, SIV(smmPBj14)

Virology

Volumn 225, Issue 1, 1996, Pages 21-32

  Gummuluru, Suryaram ^a   Novembre, Francis J ^b   Lewis, Mark ^c   Gelbard, Harris A ^a   Dewhurst, Stephen ^a,d  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b EMORY UNIVERSITY   (United States)

^c HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^d UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ETIOLOGY; INTESTINE LYMPHATIC TISSUE; LYMPHOCYTE ACTIVATION; MACACA; NONHUMAN; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; VIRUS INFECTION;

ANIMALIA; MACACA; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 0344036754     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1996.0571     Document Type: Article

References (61)

1. Andrieu, J.-M., Lu, W., and Levy, R. (1995). Sustained increases in CD4 cell counts in asymptomatic human immunodeficiency virus type 1-seropositive patients treated with prednisolone for 1 year. J. Infect. Dis. 171, 523-530.
2. Baba, T. W., Jeong, Y. S., Penninck, D., Bronson, R., Greene, M. F., and Ruprecht, R. M. (1995). Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science 267, 820-825.
3. Badley, A. D., McElhinny, J. A., Leibson, P. J., Lynch, D. H., Alderson, M. R., and Paya, C. V. (1996). Upregulation of Fas ligand expression by human immunodeficiency virus in human macrophages mediates apoptosis of uninfected T lymphocytes. J. Virol. 70, 199-206.
4. Baeuerle, P. A., and Henkel, T. (1994). Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12, 141-179.
5. Banda, N. K., Bernier, J., Kurahara, D. K., Kurrle, R., Haigwood, N., Sekaly, R.-P., and Finkel, T. H. (1992). Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J. Exp. Med. 176, 1099-1108.
6. smmPBj14 in pigtailed macaques. AIDS Res. Hum. Retroviruses 9, 1123-1129.
7. + patients. Am. J. Pathol. 146, 1542-1555.
8. Bukrinsky, M. I., Stanwick, T. L., Dempsey, M. P., and Stevenson, M. (1991). Quiescent T lymphocytes as an inducible virus reservoir in HIV-1 infection. Science 254, 423-427.
9. Chen, Y., Inobe, J.-I., Marks, R., Gonnella, P., Kuchroo, V. K., and Weiner, H. L. (1995). Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature 376, 177-180.
10. Clark, S. J., Saag, M. S., Decker, W. D., Campbell-Hill, S., Roberson, H. L., Veldkamp, P. J., Kappes, J. C., Hahn, B. H., and Shaw, G. M. (1991). High titers of cytopathic virus in plasma of patients with symptomatic primary HIV-1 infection. N. Engl. J. Med. 324, 954-960.
11. Cooper, D. A., Maclean, P., Finlayson, R., Michelmore, H. M., Gold, J., Donovan, B., Barnes, T. G., Brooke, P., and Penny, R. (1985). Acute AIDS Retrovirus infection. Definition of a clinical illness associated with seroconversion. Lancet i, 537-545.
12. Corey, L. (1995). Editorial: Reducing T cell activation as a therapy for human immunodeficiency virus infection. J. Infect. Dis. 171, 521-522.
13. Cossarizza, A., Ortolani, C., Mussini, C., Borghi, V., Guaraldi, G., Mongiardo, N., Bellesia, E., Franceschini, M. G., De Rienzo, B., and Franceschi, C. (1995). Massive activation of immune cells with an intact T cell repertoire in acute human immunodeficiency virus syndrome. J. Virol. 172, 105-112.
14. Critchfield, J. M., Racke, M. K., Zuniga-Pflucker, J. C., Cannella, B., Raine, C. S., Goverman, J., and Lenardo, M. J. (1994). T cell deletion in high antigen dose therapy of autoimmune encephalitis. Science 263, 1139-1143.
15. Daar, E. S., Moudgil, T., Meyer, R. D., and Ho, D. D. (1991). Transient high levels of viremia in patients with primary human immunodeficiency virus type 1 infection. N. Engl. J. Med. 324, 961-964.
16. De Maria, R., Boirivant, M., Cifone, M. G., Roncaioli, P., Hahne, M., Tschopp, J., Pallone, F., Santoni, A., and Testi, R. (1996). Functional expression of Fas and Fas ligand on human gut lamina propria T lymphocytes. J. Clin. Invest. 97, 316-322.
17. De Rossi, A., Masiero, S., Giaquinto, C., Ruga, E., Comar, M., Giacca, M., and Cheico-Bianchi, L. (1996). Dynamics of viral replication in infants with vertically acquired human immunodeficiency virus type 1 infection. J. Clin. Invest. 97, 323-330.
18. Desrosiers, R. C. (1990). The simian immunodeficiency viruses. Annu. Rev. Immunol. 8, 557-578.
19. smmPBj14. Nature 345, 636-640.
20. Dollard, S. C., James, H. J., Sharer, L. R., Epstein, L. G., Gelbard, H. A., and Dewhurst, S. (1995). Activation of nuclear factor κB in brains from children with HIV-1 encephalitis. Neuropathol. Appl. Neurobiol. 21, 518-528.
21. Estaquier, J., Idzoriek, T., De Bels, F., Barre-Sinoussi, F., Hurtrel, B., Aubertin, A. M., Venet, A., Mehtali, M., Muchmore, E., Michel, P., Mouton, Y., Girard, M., and Amiesen, J. C. (1994). PCD and AIDS: the significance of T-cell apoptosis in pathogenic and non-pathogenic models of lentiviral infection. Proc. Natl. Acad. Sci. USA 91, 9431-9435.
22. Finkel, T. H., Tudor-Williams, G., Banda, N. K., Cotton, M. R., Curiel, T., Monks, C., Baba, T. W., Ruprecht, R. M., and Kupfer, A. (1995). Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV-and SIV-infected lymph nodes. Nature Medicine 1, 129-134.
23. Fultz, P. N. (1991). Replication of an acutely lethal simian immunodeficiency virus activates and induces proliferation of lymphocytes. J. Virol. 65, 4902-4909.
24. Fultz, P. N., and Zack, P. (1994). Unique lentivirus-host interactions: SIVsmmPBj14 infection of macaques. Virus Res. 32, 205-225.
25. Fultz, P. N., McClure, H. M., Anderson, D. C., and Switzer, W. M. (1989). Identification and biologic characterization of an acutely lethal variant of simian immunodeficiency virus from sooty mangabeys (SIV/SMM). AIDS Res. Hum. Retroviruses 5, 397-409.
26. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell. Biol. 119, 493-501.
27. Gelbard, H. A., James, H. J., Sharer, L. R., Perry, S. W., Saito, Y., Kazee, A. M., Blumberg, B. M., and Epstein, L. G. (1995). Apoptotic neurons in brains from paediatric patients with HIV-1 encephalitis and progressive encephalopathy. Neuropathol. Appl. Neurobiol. 21, 208-217.
28. Ghosh, P., Tan, T.-H., Rice, N. R., Sica, A., and Young, H. A. (1993). The interleukin 2 CD28-responsive complex contains at least three members of the NFκB family: c-Rel, p50, and p65. Proc. Natl. Acad. Sci. USA 90, 1696-1700.
29. Groux, H., Torpier, G., Monte, D., Mouton, Y., Capron, A., and Amiesen, J. C. (1992). Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus asymptomatic individuals. J. Exp. Med. 175, 331-341.
30. smmPBj14 induces expression of a mucosal integrin on macaque lymphocytes. Virology 215, 97-100.
31. Henrard, D. R., Daar, E., Farzadegan, H., Clark, S. J., Phillips, J., Shaw, G. M., and Busch, M. P. (1995). Virologic and immunologic characterization of symptomatic and asymptomatic primary HIV-1 infection. J.A.I.D.S.H.R. 9, 305-310.
32. Hirsch, V. M., Dapolito, G., Johnson, P. R., Elkins, W. R., London, W. T., Montali, R. J., Goldstein, S., and Brown, C. (1995). Induction of AIDS by simian immunodeficiency virus from an African Green monkey: Species-specific variation in pathogenicity correlates with the extent of in vivo replication. J. Virol. 69, 955-967.
33. Hogervorst, E., Jurrianns, S., de Wolf, F., van Wijk, A., Wiersma, A., Valk, M., Roos, M., van Gemen, B., Coutinho, R., Miedema, F., and Goudsmit, J. (1995). Predictors for non-and slow progression in human immunodeficiency virus (HIV) type 1 infection: Low viral RNA copy numbers in serum and maintainance of high HIV-1 p24-specific but not V3-specific antibody levels. J. Infect. Dis. 171, 811-821.
34. smmPBj14 molecular clone 1.9 in macaques. AIDS Res. Hum. Retroviruses 9, 277-286.
35. Kerr, J. F. R., Wyllie, A. H., and Currie, A. R. (1972). Apoptosis: A basic biologic phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
36. Kent, K. A., Rud, E., Corcoran, C. Powell, C., Thiriart, C., Collignon, C., and Stott, E. J. (1992). Identification of two neutralizing and 8 non-neutralizing epitopes on simian immunodeficiency virus envelope using monoclonal antibodies. AIDS Res. Hum. Retroviruses 8, 1147-1151.
37. Kestler, H. W., Ringler, D. J., Mori, K., Panicali, D. L., Sehgal, P. K., Daniel, M. D., and Desrosiers, R. C. (1991). Importance of the nef gene for maintainance of high virus loads and for development of AIDS. Cell 65, 651-662.
38. Lackner, A. A., Vogel, P., Ramos, R. A., Kluge, J. D., and Marthas, M. (1994). Early events in tissues during infection with pathogenic (SIV-mac239) and nonpathogenic (SIVmac1A11) molecular clones of simian immunodeficiency virus. Am. J. Pathol. 145, 428-439.
39. Leist, M., Gartner, F., Bohlinger, I., Tiegs, G., and Wendel, A. (1994). Application of the cell death detection ELISA for the detection of tumor necrosis factor-induced DNA fragmentation in murine models of inflammatory organ failure. Biochemica (BMB) 11, 20-22.
40. Letvin, N. L., and King, N. W. (1990). Immunologic and pathologic manifestations of the infection of rhesus monkeys with simian immunodeficiency virus of macaques. J.A.I.D.S. 3, 1023-1040.
41. smmPBj14) isolate from sooty mangabeys. AIDS Res. Hum. Retroviruses 8, 1631-1639.
42. Li, C. J., Friedman, D. J., Wang, C., Metelev, V., and Pardee, A. B. (1995). Induction of apoptosis in uninfected lymphocytes by HIV-1 tat protein. Science 268, 429-432.
43. Lu, W., Salerno-Goncalves, R., Yuan, J., Sylvie, D., Han, D.-S., and Andrieu, J.-M. (1995). Glucocorticoids rescue CD4+ Tlymphocytes from activation-induced apoptosis triggered by HIV-1: implications for pathogenesis and therapy. AIDS 9, 35-42.
44. Mahalingam, M., Peakman, M., Davies, E. T., Pozniak, A., McManus, T. J., and Vergani, D. (1993). T cell activation and disease severity in HIV infection. Clin. Exp. Immunol. 93, 337-343.
45. Mellors, J. W., Kingsley, L. A., Rinaldo, C. R., Todd, J. A., Hoo, B. S., Kokka, R. P., and Gupta, P. (1995). Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann. Intern. Med. 122, 573-579.
46. Meyaard, L., Otto, S. A., Jonker, R. R., Mijnster, M. J., Keet, R. P. M., and Miedema, F. (1992). Programmed death of T cells in HIV-1 infection. Science 257, 217-219.
47. Muro-Cacho, C. A., Pantaleo, G., and Fauci, A. S. (1995). Analysis of apoptosis in lymph nodes of HIV-infected persons. J. Immunol. 154, 5555-5566.
48. Nabel, G., and Baltimore, D. (1987). An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature 326, 711-713.
49. smmPBj variant. J. Virol. 67, 2466-2474.
50. Papaevangelou, V., Pollack, H., Rigaud, M., Arlievsky, N., Lu, M.-L., Rochford, G., Krasinski, K., and Borkowsky, W. (1996). The amount of early p24 antigenemia and not the time of first detection of virus predicts the clinical outcome of infants vertically infected with human immunodeficiency virus. J. Infect. Dis. 173, 574-578.
51. Reimann, K. A., Tenner-Racz, K., Racz, P., Montefiori, D. C., Yasutomi, Y., Lin, W., Ransil, B. J., and Letvin, N. L. (1994). Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J. Virol. 68, 2362-2370.
52. Rice, N. R., and Ernst, M. K. (1993). In vivo control of NF-κB activation by IκBα. EMBO J. 12, 4685-4695.
53. smmPBj14: correlation between in vitro and in vivo events. J. Virol. 68, 5538-5547.
54. Sekigawa, I., Hishikawa, T., Kaneko, H., Hashimoto, H., Hirose, S., Ingaki, Y., and Yamamoto, N. (1994). FK506 can inhibit apoptotic cell death induced by the HIV-1 envelope glycoprotein gp120. AIDS 8, 1623-1624.
55. Talley, A. K., Dewhurst, S., Perry, S., Dollard, S. C., Gummuluru, S., Fine, S. M., New, D., Epstein, L. G., Gendelman, H. E., Genis, P., and Gelbard, H. A. (1995). Tumor necrosis factor alpha induces apoptosis in human neuronal cells: protection by the antioxidant N-acetylcysteine and the genes bcl-2 and crmA. Mol. Cell. Biol. 15, 2359-2366.
56. Terai, C., Kornbluth, R. S., Pauza, C. D., Richman, D. D., and Carson, D. A. (1991). Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J. Clin. Invest. 87, 1710-1715.
57. Weissman, D., Barker, T. D., and Fauci, A. S. (1996). The efficiency of acute infection of CD4+ T cells is markedly enhanced in the setting of antigen-specific immune activation. J. Exp. Med. 183, 687-692.
58. Westendorp, M. O., Frank, R., Ochsenbauer, C., Stricker, K., Dhein, J., Walczak, H., Debatin, K.-M., and Krammer, P. H. (1995). Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375, 497-500.
59. Wyllie, A. H., Morris, R. G., Smith, A. L., and Dunlop, D. (1984). Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142, 67-77.
60. Zack, J. A., Arrigo, S. J., Weitsman, S. R., Go, A. S., Haislip, A., and Chen, I. S. Y. (1990). HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61, 213-222.
61. Zheng, L., Fisher, G., Miller, R. E., Peschon, J., Lynch, D. H., and Lenardo, M. J. (1995). Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377, 348-351.