Early regeneration of thymic progenitors in rhesus macaques infected with simian immunodeficiency virus

Journal of Experimental Medicine

Volumn 187, Issue 11, 1998, Pages 1767-1776

  Wykrzykowska, Joanna J ^a   Rosenzweig, Michael ^a   Veazey, Ronald S ^a   Simon, Meredith A ^a   Halvorsen, Katherine ^b   Desrosiers, Ronald C ^a   Johnson, R Paul ^a   Lackner, Andrew A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SMITH COLLEGE   (United States)

Author keywords

AIDS; Animal model; Apoptosis; Pathogenesis; T cell homeostasis

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; IMMUNE RESPONSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; STEM CELL; T LYMPHOCYTE SUBPOPULATION; TARGET CELL; VIRUS INFECTION; VIRUS LOAD;

ANIMALS; APOPTOSIS; CELL DIVISION; MACACA MULATTA; MALE; REGENERATION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; STEM CELLS; THYMUS GLAND;

EID: 0032101595     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.187.11.1767     Document Type: Article

References (51)

1. Spits, H., L.L. Lanier, and J.H. Phillips. 1995. Development of human T and natural killer cells. Blood. 85:2654-2670.
2. Haynes, B.F., S.M. Denning, P.T. Le, and K.H. Singer. 1990. Human intrathymic T cell differentiation. Semin. Immunol. 2:67-77.
3. Schuurman, H.J., W.J.A. Krone, R. Broekhuizen, J.V. Baarlen, P. vanVeen, A.L. Goldstein, J. Huber, and J. Goudsmit. 1989. The thymus in acquired immune deficiency syndrome: comparison with other types of immunodeficiency disease and presence of components of human immunodeficiency virus type 1. Am. J. Pathol. 134:1329-1334.
4. Burke, A.P., D. Anderson, W. Benson, R. Turnicky, P. Mannan, Y.H. Liang, J. Smialek, and R. Virmani. 1995. Localization of human immunodeficiency virus 1 RNA in thymic tissues from asymptomatic drug addicts. Arch. Pathol. Lab. Med. 119:36-41.
5. + (T4) lymphocyte depletion. Proc. Natl. Acad. Sci. USA. 87:7727-7731.
6. Su, L., H. Kaneshima, M. Bonyhadi, S. Salimi, D. Kraft, L. Rabin, and J.M. McCune. 1995. HIV-1-induced thymocyte depletion is associated with indirect cytopathogenicity and infection of progenitor cells in vivo. Immunity. 2:25-36.
7. Rosenzweig, M., D.P. Clark, and G.N. Gaulton. 1993. Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS. 7:1601-1605.
8. Stanley, S.K., J.M. McCune, H. Kaneshima, J.S. Justement, M. Sullivan, E. Boone, M. Baseler, J. Adelsberger, M. Bonyhadi, J. Orenstein, et al. 1993. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID-hu mouse. J. Exp. Med. 178:1151-1163.
9. Mitler, J.E., B.R. Levin, and R. Antia. 1996. T-cell homeostasis, competition and drift: AIDS as HIV-accelerated senescence of the immune repertoire. J. Acquired Immune Defic. Syndr. 12:233-248.
10. Wei, X., S.K. Ghosh, M.E. Taylor, V.A. Johnson, E.A. Emini, P. Deutsch, J.D. Lifson, S. Bonhoeffer, M.A. Nowak, B.H. Hahn, et al. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:117-122.
11. Mackall, C.L., T.A. Gleisher, M.R. Brown, M.P. Andrich, C.C. Chen, I.M. Feuerstein, M.E. Horowitz, I.T. Magrath, A.T. Shad, S.M. Steinberg, et al. 1995. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N. Engl. J. Med. 332:143-149.
12. Ho, D., A.U. Neumann, A.S. Perelson, W. Chen, J.M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373:123-126.
13. Mackall, C.L., V.C. Bare, L.A. Granger, S.O. Sharrow, J.A. Titus, and R.E. Gress. 1996. Thymic-independent T cell regeneration occurs via antigen-driven expansion of peripheral T cells resulting in a repertoire that is limited in diversity and prone to skewing. J. Immunol. 156:4609-1616.
14. Heitger, A., N. Neu, H. Kern, E.R. Panzer-Grumayer, H. Greinix, D. Nachbaur, D. Niederwieser, and F.M. Fink. 1997. Essential role of the thymus to reconstitute naive (CD45RA+) T-helper cells after human allogeneic bone marrow transplantation. Blood. 90:850-857.
15. Bonyhadi, M.L., L. Rabin, S. Salimi, D.A. Brown, J. Kosek, J.M. McCune, and H. Kanesha. 1993. HIV induces thymus depletion in vivo. Nature. 363:728-732.
16. Kaneshima, H., L. Su, M.L. Bonyhadi, R.I. Connor, D.D. Ho, and J.M. McCune. 1994. Rapid-high, syncytium-inducing isolates of human immunodeficiency virus type 1 induce cytopathicity in the human thymus of the SCID-hu mouse. J. Virol. 68:8188-8192.
17. Aldrovandi, G.M., G. Feuer, L. Gao, B. Jamieson, M. Kristeva, I.S.Y. Chen, and J.A. Zack. 1993. The SCID-hu mouse as a model For HIV-1 infection. Nature. 363:732-736.
18. Namikawa, R., H. Kaneshima, M. Liberman, I.L. Weissman, and J.M. McCune. 1988. Infection of the SCID-hu mouse by HIV-1. Science. 242:1684-1686.
19. Desrosiers, R.C. 1990. The simian immunodeficiency viruses. Annu. Rev. Immunol. 8:557-578.
20. Watson, A., J. Ranchalis, B. Travis, J. McClure, W. Sutton, P.R. Johnson, S.L. Hu, and N.L. Haigwood. 1997. Plasma viremia in macaques infected with simian immunodeficiency virus: plasma viral load early in infection predicts survival. J. Virol. 71:284-290.
21. Hirsch, V.M., T.R. Fuerst, G. Sutter, M.W. Carroll, L.C. Yang, S. Goldstein, M. Piatak, W.R. Elkins, W.G. Alvord, D.C. Montefiori, et al. 1996. Patterns of viral replication correlate with outcome in simian immunodeficiency virus (SIV)-infected macaques: effect of prior immunization with a trivalent SIV vaccine in modified vaccinia virus Ankara. J. Virol. 70:3741-3752.
22. Kestler, H., T. Kodama, D. Ringler, M. Marthas, N. Pedersen, A. Lackner, D. Regier, P. Sehgal, M. Daniel, N. King, and R. Desrosiers. 1990. Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science. 248:1109-1112.
23. Kestler, H.W., D.J. Ringler, K. Mori, D.L. Panicali, P.K. Sehgal, M.D. Daniel, and R.C. Desrosiers. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell. 65:651-662.
24. Gibbs, J.S., A.A. Lackner, S.M. Lang, M.A. Simon, P.K. Sehgal, M.D. Daniel, and R.C. Desrosiers. 1995. Progression to AIDS in the absence of a gene for vpr or vpx. J. Virol. 69:2378-2383.
25. Daniel, M.D., Y. Li, Y.M. Naidu, P.J. Durda, D.K. Schmidt, C.D. Finger, D.P. Silva, J.J. MacKey, H.W. Kestler, P.K. Sehgal, et al. 1988. Simian immunodeficiency viruses from African green monkeys. J. Virol. 62:4123-4128.
26. Kawai, T., J. Wong, J. MacLean, A.B. Cosimi, and S. Wee. 1994. Characterization of a monoclonal antibody recognizing the cynomolgus monkey CD3 antigen. Transplant. Proc. 26: 1845-1846.
27. Ilyinskii, P.O., M.D. Daniel, M.A. Simon, A.A. Lackner, and R.C. Desrosiers. 1994. The role of upstream U3 sequences in the pathogenesis of SIV-induced AIDS in rhesus monkeys. J. Virol. 68:5933-5944.
28. Horvath, C.J., R.D. Hunt, M.A. Simon, P.K. Sehgal, and D.J. Ringler. 1993. An immunohistologic study of granulomatous inflammation in SIV-infected rhesus monkeys. J. Leukocyte Biol. 53:532-540.
29. Lackner, A.A., M. Schiødt, G.C. Armitage, P.F. Moore, R.J. Munn, P.A. Marx, M.B. Gardner, and L.J. Lowenstine. 1989. Mucosal epithelial cells and Langerhans cells are targets for infection by the immunosuppressive type D simian AIDS retrovirus serotype 1. J. Med. Primatol. 18:195-207.
30. Ringler, D.J., D.G. Walsh, L.V. Chalifoux, J.J. MacKey, M.D. Daniel, R.C. Desrosiers, N.W. King, and W.W. Hancock. 1990. Soluble and membrane-associated interleukin 2 receptor-alpha expression in rhesus monkeys infected with simian immunodeficiency virus. Lab. Invest. 62:435-143.
31. Sasseville, V.G., Z. Du, L.V. Chalifoux, D.R. Pauley, H.L. Young, P.K. Sehgal, R.C. Desrosiers, and A.A. Lackner. 1996. Induction of lymphocyte proliferation and severe gastrointestinal disease in macaques by a nef gene variant of SIVmac239. Am. J. Pathol. 149:163-176.
32. Keshgeian, A.A., and A. Cnaan. 1995. Proliferation markers in breast carcinoma: mitotic figure count, S-phase fraction, proliferating cell nuclear antigen, Ki-67 and MIB-1. Am. J. Clin. Pathol. 104:42-49.
33. Kelleher, L,. H.M. Magee, and P.A. Dervan. 1994. Evaluation of cell-proliferation antibodies reactive in paraffin sections. Appl. Immunohistochem. 2:164-170.
34. Barbareschi, M., S. Girlando, F.M. Mauri, S. Forti, C. Eccher, F.A. Mauri, R. Togni, P.D. Palma, and C. Doglioni. 1994. Quantitative growth fraction evaluation with MIB1 and Ki67 antibodies in breast carcinomas. Am. J. Clin. Pathol. 102:171-175.
35. Landberg, G., E.M. Tan, and G. Roos. 1990. Flow cytometric multiparameter analysis of proliferating cell nuclear antigen/cyclin and Ki-67 antigen: a new view of the cell cycle. Exp. Cell. Res. 187:111-118.
36. Sarli, G., C. Benazzi, R. Preziosi, and P.S. Marcato. 1994. Proliferative activity assessed by anti-PCNA and Ki67 monoclonal antibodies in canine testicular tumours. J. Comp. Path. 110:357-368.
37. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
38. Tenner-Racz, K., P. Racz, C. Thomé, C.G. Meyer, P.J. Anderson, S.F. Schlossman, and N.L. Letvin. 1993. Cytotoxic effector cell granules recognized by the monoclonal antibody TIA-1 are present in CD8+ lymphocytes in lymph nodes of human immunodeficiency virus-1-infected patients. Am. J. Pathol. 142:1750-1758.
39. Meehan, S.M., R.T. McCluskey, M. Pascual, F.L. Preffer, P. Anderson, S.F. Schlossman, and R.B. Colvin. 1997. Cytotoxicity and apoptosis in human renal allografts: Identification, distribution, and quantitation of cells with a cytotoxic granule protein GMP-17 (TIA-1) and cells with fragmented nuclear DNA. Lab. Invest. 76:639-649.
40. Lackner, A.A., P. Vogel, R.A. Ramos, J.D. Kluge, and M. Marthas. 1994. Early events in tissues during infection with pathogenic (SIVmac239) and nonpathogenic (SIVmac1A11) molecular clones of simian immunodeficiency virus. Am. J. Pathol. 145:428-439.
41. Zhang, J., L.N. Martin, E.A. Watson, R.C. Montelaro, M. West, L. Epstein, and M. Murphey-Corb. 1988. Simian immunodeficiency virus/delta-induced immunodeficiency disease in rhesus monkeys: relation of antibody response and antigenemia. J. Infect. Dis. 158:1277-1286.
42. Daniel, M.D., F. Kirchoff, S.C. Czajak, P.K. Sehgal, and R.C. Desrosiers. 1992. Protective effects of a live attenuated SIV vaccine with a deletion in the nef gene. Science. 258: 1938-1941.
43. Baskin, G.B., M. Murphey-Corb, L.N. Martin, B. Davison-Fairburn, F.-S. Hu, and D. Kuebler. 1991. Thymus in simian immunodeficiency virus-infected rhesus monkeys. Lab. Invest. 65:400-407.
44. Terstappen, L.W., S. Huang, and L.J. Picker. 1992. Flow cytometric assessment of human T-cell differentiation in thymus and bone marrow. Blood. 79:666-677.
45. Kourtis, A.P., C. Ibegbu, A.J. Nahmias, F.K. Lee, W.S. Clark, M.K. Sawyer, and S. Nesheim. 1996. Early progression of disease in HIV-infected infants with thymic dysfunction. N. Engl. J. Med. 335:1431-1436.
46. Connors, M., J.A. Kovacs, S. Krevat, J.C. Gea-Banacloche, M.C. Sneller, M. Flanigan, J.A. Metcalf, R.E. Walker, J. Falloon, M. Baseler, et al. 1997. HIV induces changes in CD4+ T-cell phenotype and depletions within the CD4+ T-cell repertoire that are not immediately restored by antiviral or immune-based therapies. Nat. Med. 3:533-540.
47. Autran, B., C. Carcelain, T.S. Li, C. Blanc, D. Mathez, R. Tubiana, C. Katlama, P. Debré, and J. Leibowitch. 1997. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science. 277:112-116.
48. Jacobson, M.A., F. Kramer, P.R. Pavan, S. Owens, R. Pollard, and N.A.P. Team. 1997. Failure of highly active antiretroviral therapy (HAART) to prevent CMV retinitis despite marked CD4 count increase. Proceedings of the 4th Conference on Retroviruses and Opportunistics Infections. 129:353. (Abstr.)
49. Gilquin, J., C. Piketty, V. Thomas, G. GonzaJes-Canali, and M.D. Kazatchkine. 1997. Acute CMV infection in AIDS patients receiving combination therapy including protease inhibitors. Proceedings of the 4th Conference on Retroviruses and Opportunistic Infections. 129:354 (Abstr.)
50. + T lymphocyte turnover in simion immunodeficiency virus-infected macaques. Proc. NAtl. Acad. Sci. USA. In press.
51. Du, Z.J., S.M. Lang, V.G. Sasseville, A.A. Lackner, P.O. Ilyinskii, M.D. Daniel, J.U. Jung, and R.C. Desrosiers. 1995. Identification of a nef allele that causes lymphocyte activation and acute disease in macaque monkeys. Cell. 82:665-674.