Rapid CD4(+) T-cell Loss Induced by Human Immunodeficiency Virus Type 1(NC) in Uninfected and Previously Infected Chimpanzees

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2001 Jan 11

PMID 11152525

Citations 19

Authors

F J Novembre

J de Rosayro

S Nidtha

S P ONeil

T R Gibson

C E Hart

H M McClure

Affiliations

Soon will be listed here.

Abstract

To investigate the pathogenicity of a virus originating in a chimpanzee with AIDS (C499), two chimpanzees were inoculated with a plasma-derived isolate termed human immunodeficiency virus type 1(NC) (HIV-1(NC)). A previously uninfected chimpanzee, C534, experienced rapid peripheral CD4(+) T-cell loss to fewer than 26 cells/microl by 14 weeks after infection. CD4(+) T-cell depletion was associated with high plasma HIV-1 loads but a low virus burden in the peripheral lymph node. The second chimpanzee, C459, infected 13 years previously with HIV-1(LAV), experienced a more protracted course of peripheral CD4(+) T-cell loss after HIV-1(NC) inoculation, resulting in fewer than 200 cells/microl by 96 weeks postinoculation. The quantities of viral RNA in the plasma and peripheral lymph node from C459 were below the lower limits of detection prior to inoculation with HIV-1(NC) but were significantly and persistently increased after superinfection, with HIV-1(NC) representing the predominant viral genotype. These results show that viruses derived from C499 are more pathogenic for chimpanzees than any other HIV-1 isolates described to date.

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References

Veazey R, Lackner A . The gastrointestinal tract and the pathogenesis of AIDS. AIDS. 1998; 12 Suppl A:S35-42. View

Veazey R, Demaria M, Chalifoux L, Shvetz D, Pauley D, Knight H . Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science. 1998; 280(5362):427-31. DOI: 10.1126/science.280.5362.427. View

Alter H, Eichberg J, Masur H, Saxinger W, Gallo R, Macher A . Transmission of HTLV-III infection from human plasma to chimpanzees: an animal model for AIDS. Science. 1984; 226(4674):549-52. DOI: 10.1126/science.6093251. View

Francis D, Feorino P, Broderson J, McClure H, Getchell J, McGrath C . Infection of chimpanzees with lymphadenopathy-associated virus. Lancet. 1984; 2(8414):1276-7. DOI: 10.1016/s0140-6736(84)92824-1. View

Fultz P, McClure H, Swenson R, McGrath C, Brodie A, Getchell J . Persistent infection of chimpanzees with human T-lymphotropic virus type III/lymphadenopathy-associated virus: a potential model for acquired immunodeficiency syndrome. J Virol. 1986; 58(1):116-24. PMC: 252883. DOI: 10.1128/JVI.58.1.116-124.1986. View

Murphey-Corb M, Martin L, RANGAN S, Baskin G, Gormus B, Wolf R . Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature. 1986; 321(6068):435-7. DOI: 10.1038/321435a0. View

Fultz P, McClure H, Anderson D, Swenson R, Anand R, Srinivasan A . Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys). Proc Natl Acad Sci U S A. 1986; 83(14):5286-90. PMC: 323936. DOI: 10.1073/pnas.83.14.5286. View

Benveniste R, Arthur L, Tsai C, Sowder R, Copeland T, Henderson L . Isolation of a lentivirus from a macaque with lymphoma: comparison with HTLV-III/LAV and other lentiviruses. J Virol. 1986; 60(2):483-90. PMC: 288916. DOI: 10.1128/JVI.60.2.483-490.1986. View

Nara P, HATCH W, Kessler J, Kelliher J, Carter S . The biology of human immunodeficiency virus-1 IIIB infection in the chimpanzee: in vivo and in vitro correlations. J Med Primatol. 1989; 18(3-4):343-55. View

10.

Nicol I, Dubouch P, Bernard J, Snart R, Jouffre R, Reveil B . Persistent HIV-2 infection of rhesus macaque, baboon, and mangabeys. Intervirology. 1989; 30(5):258-67. DOI: 10.1159/000150101. View

11.

Zarling J, Ledbetter J, Sias J, Fultz P, EICHBERG J, Gjerset G . HIV-infected humans, but not chimpanzees, have circulating cytotoxic T lymphocytes that lyse uninfected CD4+ cells. J Immunol. 1990; 144(8):2992-8. View

12.

Castro B, Walker C, Eichberg J, Levy J . Suppression of human immunodeficiency virus replication by CD8+ cells from infected and uninfected chimpanzees. Cell Immunol. 1991; 132(1):246-55. DOI: 10.1016/0008-8749(91)90023-5. View

13.

McCune J, KANESHIMA H, Krowka J, Namikawa R, Outzen H, Peault B . The SCID-hu mouse: a small animal model for HIV infection and pathogenesis. Annu Rev Immunol. 1991; 9:399-429. DOI: 10.1146/annurev.iy.09.040191.002151. View

14.

Ghosh S, Fultz P, Keddie E, Saag M, Sharp P, Hahn B . A molecular clone of HIV-1 tropic and cytopathic for human and chimpanzee lymphocytes. Virology. 1993; 194(2):858-64. DOI: 10.1006/viro.1993.1331. View

15.

Gougeon M, Garcia S, Heeney J, Tschopp R, Lecoeur H, Guetard D . Programmed cell death in AIDS-related HIV and SIV infections. AIDS Res Hum Retroviruses. 1993; 9(6):553-63. DOI: 10.1089/aid.1993.9.553. View

16.

Fultz P . Nonhuman primate models for AIDS. Clin Infect Dis. 1993; 17 Suppl 1:S230-5. DOI: 10.1093/clinids/17.supplement_1.s230. View

17.

Schuitemaker H, Meyaard L, Kootstra N, Dubbes R, Otto S, Tersmette M . Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. J Infect Dis. 1993; 168(5):1140-7. DOI: 10.1093/infdis/168.5.1140. View

18.

Mwaengo D, Novembre F . Molecular cloning and characterization of viruses isolated from chimpanzees with pathogenic human immunodeficiency virus type 1 infections. J Virol. 1998; 72(11):8976-87. PMC: 110315. DOI: 10.1128/JVI.72.11.8976-8987.1998. View

19.

Connor R, Montefiori D, Binley J, Moore J, Bonhoeffer S, Gettie A . Temporal analyses of virus replication, immune responses, and efficacy in rhesus macaques immunized with a live, attenuated simian immunodeficiency virus vaccine. J Virol. 1998; 72(9):7501-9. PMC: 109989. DOI: 10.1128/JVI.72.9.7501-7509.1998. View

20.

Ferrari G, Place C, Ahearne P, Nigida Jr S, Arthur L, Bolognesi D . Comparison of anti-HIV-1 ADCC reactivities in infected humans and chimpanzees. J Acquir Immune Defic Syndr (1988). 1994; 7(4):325-31. View