Impaired T-cell differentiation in the thymus at the early stages of acute pathogenic chimeric simian-human immunodeficiency virus (SHIV) infection in contrast to less pathogenic SHIV infection

Microbes and Infection

Volumn 8, Issue 6, 2006, Pages 1539-1549

  Motohara, Makiko ^a   Ibuki, Kentaro ^a   Miyake, Ariko ^a   Fukazawa, Yoshinori ^a   Inaba, Katsuhisa ^a   Suzuki, Hajime ^a   Masuda, Kyoko ^b,c   Minato, Nagahiro ^b   Kawamoto, Hiroshi ^c   Nakasone, Tadashi ^d   Honda, Mitsuo ^d   Hayami, Masanori ^a   Miura, Tomoyuki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

AIDS; Animal model; Rhesus monkey; SHIV; Thymopoiesis

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CHIMERA; CONTROLLED STUDY; EX VIVO STUDY; FETUS; HUMAN IMMUNODEFICIENCY VIRUS; INOCULATION; INVOLUTION; MACACA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN CULTURE; PRIORITY JOURNAL; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THYMUS; THYMUS ATROPHY; VIRUS INFECTION; VIRUS VIRULENCE;

ANIMALS; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; FEMALE; FLOW CYTOMETRY; HIV; HUMANS; MACACA MULATTA; MICE; MICE, INBRED C57BL; PREGNANCY; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; STEM CELLS; THYMUS GLAND; VIRAL LOAD;

MACACA; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

EID: 33745131124     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2006.01.011     Document Type: Article

References (30)

1. Douek D. Thymic output and HIV infection; on the right TREC. Immunity 21 (2004) 744-745
2. Kaneshima H., Su L., Bonyhadi M.L., Connor R.I., Ho D.D., and McCune J.M. 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 (1994) 8188-8192
3. Rosenzweig M., Clark D.P., and Gaulton G.N. Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS 7 (1993) 1601-1605
4. Joshi V.V., Oleske J.M., Minnefor A.B., Singh R., Bokhari T., and Rapkin R.H. Pathology of suspected acquired immune deficiency syndrome in children: a study of eight cases. Pediatr. Pathol. 2 (1984) 71-87
5. Douek D.C., Betts M.R., Hill B.J., Little S.J., Lempicki R., Metcalf J.A., Casazza J., Yoder C., Adelsberger J.W., Stevens R.A., Baseler M.W., Keiser P., Richman D.D., Davey R.T., and Koup R.A. Evidence for increased T cell turnover and decreased thymic output in HIV infection. J. Immunol. 167 (2001) 6663-6668
6. Sodora D.L., Douek D.C., Silvestri G., Montgomery L., Rosenzweig M., Igarashi T., Bernacky B., Johnson R.P., Feinberg M.B., Martin M.A., and Koup R.A. Quantification of thymic function by measuring T cell receptor excision circles within peripheral blood and lymphoid tissues in monkeys. Eur. J. Immunol. 30 (2000) 1145-1153
7. Sodora D.L., Milush J.M., Ware F., Wozniakowski A., Montgomery L., McClure H.M., Lackner A.A., Marthas M., Hirsch V., Johnson R.P., Douek D.C., and Koup R.A. Decreased levels of recent thymic emigrants in peripheral blood of simian immunodeficiency virus-infected macaques correlate with alterations within the thymus. J. Virol. 76 (2002) 9981-9990
8. Weiss R.A., Clapham P.R., Weber J.N., Dalgleish A.G., Lasky L.A., and Berman P.W. Variable and conserved neutralization antigens of human immunodeficiency virus. Nature 324 (1986) 572-575
9. Shibata R., Kawamura M., Sakai H., Hayami M., Ishimoto A., and Adachi A. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J. Virol. 65 (1991) 3514-3520
10. Reimann K.A., Li J.T., Veazey R., Halloran M., Park I.W., Karlsson G.B., Sodroski J., and Letvin N.L. A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J. Virol. 70 (1996) 6922-6928
11. Harouse J.M., Gettie A., Tan R.C., Blanchard J., and Cheng-Mayer C. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284 (1999) 816-819
12. Shinohara K., Sakai K., Ando S., Ami Y., Yoshino N., Takahashi E., Someya K., Suzaki Y., Nakasone T., Sasaki Y., Kaizu M., Lu Y., and Honda M. A highly pathogenic simian/human immunodeficiency virus with genetic changes in cynomolgus monkey. J. Gen. Virol. 80 Pt 5 (1999) 1231-1240
13. Reyes R.A., Canfield D.R., Esser U., Adamson L.A., Brown C.R., Cheng-Mayer C., Gardner M.B., Harouse J.M., and Luciw P.A. Induction of simian AIDS in infant rhesus macaques infected with CCR5- or CXCR4-utilizing simian-human immunodeficiency viruses is associated with distinct lesions of the thymus. J. Virol. 78 (2004) 2121-2130
14. Ho S.H., Shek L., Gettie A., Blanchard J., and Cheng-Mayer C. V3 loop-determined coreceptor preference dictates the dynamics of CD4+-T-cell loss in simian-human immunodeficiency virus-infected macaques. J. Virol. 79 (2005) 12296-12303
15. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., Nguyen P.L., Khoruts A., Larson M., Haase A.T., and Douek D.C. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200 (2004) 749-759
16. Mehandru S., Poles M.A., Tenner-Racz K., Horowitz A., Hurley A., Hogan C., Boden D., Racz P., and Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200 (2004) 761-770
17. Berger E.A., Murphy P.M., and Farber J.M. Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu. Rev. Immunol. 17 (1999) 657-700
18. Kozyrev I.L., Ibuki K., Shimada T., Kuwata T., Takemura T., Hayami M., and Miura T. Characterization of less pathogenic infectious molecular clones derived from acute-pathogenic SHIV-89.6p stock virus. Virology 282 (2001) 6-13
19. Kawamoto H., Ohmura K., Hattori N., and Katsura Y. Hemopoietic progenitors in the murine fetal liver capable of rapidly generating T cells. J. Immunol. 158 (1997) 3118-3124
20. Neben K., Heidbreder M., Muller J., Marxer A., Petry H., Didier A., Schimpl A., Hunig T., and Kerkau T. Impaired thymopoietic potential of immature CD3(-)CD4(+)CD8(-) T cell precursors from SIV-infected rhesus monkeys. Int. Immunol. 11 (1999) 1509-1518
21. Kuwata T., Igarashi T., Ido E., Jin M., Mizuno A., Chen J., and Hayami M. Construction of human immunodeficiency virus 1/simian immunodeficiency virus strain mac chimeric viruses having vpr and/or nef of different parental origins and their in vitro and in vivo replication. J. Gen. Virol. 76 Pt 9 (1995) 2181-2191
22. Shimada T., Suzuki H., Motohara M., Kuwata T., Ibuki K., Ui M., Iida T., Fukumoto M., Miura T., and Hayami M. Comparative histopathological studies in the early stages of acute pathogenic and nonpathogenic SHIV-infected lymphoid organs. Virology 306 (2003) 334-346
23. Evans J.T., Okamoto Y., Douek D.C., McFarland R.D., Gatlin J., Koup R.A., and Garcia J.V. Thymocyte differentiation from lentivirus-marked CD34(+) cells in infant and adult human thymus. J. Immunol. Methods 245 (2000) 31-43
24. Yamakami K., Honda M., Takei M., Ami Y., Kitamura N., Nishinarita S., Sawada S., and Horie T. Early bone marrow hematopoietic defect in simian/human immunodeficiency virus C2/1-infected macaques and relevance to advance of disease. J. Virol. 78 (2004) 10906-10910
25. Valentin H., Nugeyre M.T., Vuillier F., Boumsell L., Schmid M., Barre-Sinoussi F., and Pereira R.A. Two subpopulations of human triple-negative thymic cells are susceptible to infection by human immunodeficiency virus type 1 in vitro. J. Virol. 68 (1994) 3041-3050
26. Nishimura Y., Igarashi T., Donau O.K., Buckler-White A., Buckler C., Lafont B.A., Goeken R.M., Goldstein S., Hirsch V.M., and Martin M.A. Highly pathogenic SHIVs and SIVs target different CD4+ T cell subsets in rhesus monkeys, explaining their divergent clinical courses. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 12324-12329
27. Veazey R.S., DeMaria M., Chalifoux L.V., Shvetz D.E., Pauley D.R., Knight H.L., Rosenzweig M., Johnson R.P., Desrosiers R.C., and Lackner A.A. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280 (1998) 427-431
28. Miyake A., Ibuki K., Enose Y., Suzuki H., Horiuchi R., Motohara M., Saito N., Nakasone T., Honda M., Watanabe T., Miura T., and Hayami M. Rapid dissemination of a pathogenic simian/human immunodeficiency virus to systemic organs and active replication in lymphoid tissues following intrarectal infection. J. Gen. Virol. 87 (2006) 1311-1320
29. Arron S.T., Ribeiro R.M., Gettie A., Bohm R., Blanchard J., Yu J., Perelson A.S., Ho D.D., and Zhang L. Impact of thymectomy on the peripheral T cell pool in rhesus macaques before and after infection with simian immunodeficiency virus. Eur. J. Immunol. 35 (2005) 46-55
30. Hazenberg M.D., Otto S.A., de Pauw E.S., Roelofs H., Fibbe W.E., Hamann D., and Miedema F. T-cell receptor excision circle and T-cell dynamics after allogeneic stem cell transplantation are related to clinical events. Blood 99 (2002) 3449-3453