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* Divisions of Comparative Pathology and Microbiology, Tulane National Primate Research Center, Covington, LA 70433;
Department of Pathology,
Department of Microbiology and Immunology, School of Medicine, and
Department of Tropical Medicine, School of Public Health, Tulane University, New Orleans, LA 70112;
¶ Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545;
|| Human Immunology Section, Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892; and
# Department of Pathology, University of Pennsylvania School of Medicine, Philadelphia, PA 19107
The predictive value of acute gut-associated lymphoid tissue (GALT) CD4+ T cell depletion in lentiviral infections was assessed by comparing three animal models illustrative of the outcomes of SIV infection: pathogenic infection (SIVsmm infection of rhesus macaques (Rh)), persistent nonprogressive infection (SIVagm infection of African green monkeys (AGM)), and transient, controlled infection (SIVagm infection of Rh). Massive acute depletion of GALT CD4+ T cells was a common feature of acute SIV infection in all three models. The outcome of this mucosal CD4+ T cell depletion, however, differed substantially between the three models: in SIVsmm-infected Rh, the acute GALT CD4+ T cell depletion was persistent and continued with disease progression; in SIVagm, intestinal CD4+ T cells were partially restored during chronic infection in the context of normal levels of apoptosis and immune activation and absence of damage to the mucosal immunologic barrier; in SIVagm-infected Rh, complete control of viral replication resulted in restoration of the mucosal barrier and immune restoration. Therefore, our data support a revised paradigm wherein severe GALT CD4+ T cell depletion during acute pathogenic HIV and SIV infections of humans and Rh is necessary but neither sufficient nor predictive of disease progression, with levels of immune activation, proliferation and apoptosis being key factors involved in determining progression to AIDS.
The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1 This work was supported by Grants RO1 AI064066 and R21AI069935 (to I.P.), R01 AI49080 (to R.V.), R01 AI065325 and P20 RR020159 (to C.A.), RR06555 and AI28433 (to A.S.P.), RR18745 (to R.M.R.), and P51 RR000164 (to Tulane National Primate Research Center) from the National Institute of Allergy and Infectious Diseases and from the National Center for Research Resources. A part of this work was done under the auspices of contract DE-AC52-06NA25396 of the U.S. Department of Energy.
2 Address correspondence and reprint requests to Dr. Ivona Pandrea, Department of Comparative Pathology, Tulane National Primate Research Center, 18703 Three Rivers Road, Covington, LA 70433. E-mail address: ipandrea{at}tulane.edu
3 Abbreviations used in this paper: Rh, rhesus macaque; GALT, gut-associated lymphoid tissue; AGM, African green monkey; ISH, in situ hybridization; TCID, tissue culture-infective dose; p.i., postinfection; BAL, bronchoalveolar lavage; LN, lymph node; 7-AAD, 7-aminoactinomycin D.
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