The Envelope Glycoprotein Ectodomains Determine the Efficiency of CD4+ T Lymphocyte Depletion in Simian-human Immunodeficiency Virus-infected Macaques

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 1998 Sep 22

PMID 9743534

Citations 49

Authors

G B Karlsson

M Halloran

D Schenten

J Lee

P Racz

K Tenner-Racz

J Manola

R Gelman

B Etemad-Moghadam

E DESJARDINS

R Wyatt

N P Gerard

L Marcon

D Margolin

J Fanton

M K Axthelm

N L Letvin

J Sodroski

Affiliations

Soon will be listed here.

Abstract

CD4+ T lymphocyte depletion in human immunodeficiency virus type 1 (HIV-1)-infected humans underlies the development of acquired immune deficiency syndrome. Using a model in which rhesus macaques were infected with chimeric simian-human immunodeficiency viruses (SHIVs), we show that both the level of viremia and the structure of the HIV-1 envelope glycoprotein ectodomains individually contributed to the efficiency with which CD4(+) T lymphocytes were depleted. The envelope glycoproteins of recombinant SHIVs that efficiently caused loss of CD4(+) T lymphocytes exhibited increased chemokine receptor binding and membrane-fusing capacity compared with those of less pathogenic viruses. These studies identify the HIV-1 envelope glycoprotein ectodomains as determinants of CD4(+) T lymphocyte loss in vivo and provide a foundation for studying pathogenic mechanisms.

Citing Articles

Differential Pathogenicity of SHIV KB9 and 89.6 Env Correlates with Bystander Apoptosis Induction in CD4+ T cells.

Mehmetoglu-Gurbuz T, Joshi A, Garg H Viruses. 2019; 11(10).

PMID: 31581579 PMC: 6832477. DOI: 10.3390/v11100911.

Infection of rhesus macaques with a pool of simian immunodeficiency virus with the envelope genes from acute HIV-1 infections.

Krebs K, Tian M, Asmal M, Ling B, Nelson K, Henry K AIDS Res Ther. 2016; 13(1):41.

PMID: 27906032 PMC: 5124249. DOI: 10.1186/s12981-016-0125-8.

Single-cell RNA-seq reveals activation of unique gene groups as a consequence of stem cell-parenchymal cell fusion.

Freeman B, Jung J, Ogle B Sci Rep. 2016; 6:23270.

PMID: 26997336 PMC: 4800419. DOI: 10.1038/srep23270.

Viral-mediated fusion of mesenchymal stem cells with cells of the infarcted heart hinders healing via decreased vascularization and immune modulation.

Freeman B, Ogle B Sci Rep. 2016; 6:20283.

PMID: 26846200 PMC: 4742880. DOI: 10.1038/srep20283.

Viral envelope is a major determinant of enhanced fitness of a multidrug-resistant HIV-1 variant.

Mohri H, Prada N, Markowitz M J Acquir Immune Defic Syndr. 2015; 68(5):487-94.

PMID: 25622054 PMC: 4357569. DOI: 10.1097/QAI.0000000000000524.

References

Sodroski J, Goh W, Rosen C, Campbell K, Haseltine W . Role of the HTLV-III/LAV envelope in syncytium formation and cytopathicity. Nature. 1986; 322(6078):470-4. DOI: 10.1038/322470a0. View

Tenner-Racz K, Stellbrink H, van Lunzen J, Schneider C, Jacobs J, Raschdorff B . The unenlarged lymph nodes of HIV-1-infected, asymptomatic patients with high CD4 T cell counts are sites for virus replication and CD4 T cell proliferation. The impact of highly active antiretroviral therapy. J Exp Med. 1998; 187(6):949-59. PMC: 2212181. DOI: 10.1084/jem.187.6.949. View

Koga Y, Sasaki M, Nakamura K, Kimura G, Nomoto K . Intracellular distribution of the envelope glycoprotein of human immunodeficiency virus and its role in the production of cytopathic effect in CD4+ and CD4- human cell lines. J Virol. 1990; 64(10):4661-71. PMC: 247950. DOI: 10.1128/JVI.64.10.4661-4671.1990. View

Olshevsky U, Helseth E, Furman C, Li J, Haseltine W, Sodroski J . Identification of individual human immunodeficiency virus type 1 gp120 amino acids important for CD4 receptor binding. J Virol. 1990; 64(12):5701-7. PMC: 248709. DOI: 10.1128/JVI.64.12.5701-5707.1990. View

Clark S, Saag M, DECKER W, Roberson J, Veldkamp P, Kappes J . High titers of cytopathic virus in plasma of patients with symptomatic primary HIV-1 infection. N Engl J Med. 1991; 324(14):954-60. DOI: 10.1056/NEJM199104043241404. View

Daar E, Moudgil T, Meyer R, Ho D . Transient high levels of viremia in patients with primary human immunodeficiency virus type 1 infection. N Engl J Med. 1991; 324(14):961-4. DOI: 10.1056/NEJM199104043241405. View

Culp J, Johansen H, Hellmig B, Beck J, Matthews T, Delers A . Regulated expression allows high level production and secretion of HIV-1 gp120 envelope glycoprotein in Drosophila Schneider cells. Biotechnology (N Y). 1991; 9(2):173-7. DOI: 10.1038/nbt0291-173. View

Li J, Lord C, Haseltine W, Letvin N, Sodroski J . Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus that expresses the HIV-1 envelope glycoproteins. J Acquir Immune Defic Syndr (1988). 1992; 5(7):639-46. View

Letvin N . Animal models for the study of human immunodeficiency virus infections. Curr Opin Immunol. 1992; 4(4):481-5. DOI: 10.1016/s0952-7915(06)80043-9. View

10.

Reimann K, Tenner-Racz K, Racz P, Montefiori D, Yasutomi Y, Lin W . Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J Virol. 1994; 68(4):2362-70. PMC: 236713. DOI: 10.1128/JVI.68.4.2362-2370.1994. View

11.

Chakrabarti L, Cumont M, Montagnier L, Hurtrel B . Variable course of primary simian immunodeficiency virus infection in lymph nodes: relation to disease progression. J Virol. 1994; 68(10):6634-43. PMC: 237084. DOI: 10.1128/JVI.68.10.6634-6643.1994. View

12.

Burton D, Pyati J, Koduri R, Sharp S, Thornton G, Parren P . Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science. 1994; 266(5187):1024-7. DOI: 10.1126/science.7973652. View

13.

Reimann K, Waite B, Lee-Parritz D, Lin W, Uchanska-Ziegler B, Oconnell M . Use of human leukocyte-specific monoclonal antibodies for clinically immunophenotyping lymphocytes of rhesus monkeys. Cytometry. 1994; 17(1):102-8. DOI: 10.1002/cyto.990170113. View

14.

Igarashi T, Shibata R, Hasebe F, Ami Y, Shinohara K, Komatsu T . Persistent infection with SIVmac chimeric virus having tat, rev, vpu, env and nef of HIV type 1 in macaque monkeys. AIDS Res Hum Retroviruses. 1994; 10(8):1021-9. DOI: 10.1089/aid.1994.10.1021. View

15.

Wei X, Ghosh S, Taylor M, Johnson V, Emini E, Deutsch P . Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 1995; 373(6510):117-22. DOI: 10.1038/373117a0. View

16.

Ho D, Neumann A, Perelson A, Chen W, Leonard J, Markowitz M . Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 1995; 373(6510):123-6. DOI: 10.1038/373123a0. View

17.

Pachl C, Todd J, Kern D, Sheridan P, Fong S, Stempien M . Rapid and precise quantification of HIV-1 RNA in plasma using a branched DNA signal amplification assay. J Acquir Immune Defic Syndr Hum Retrovirol. 1995; 8(5):446-54. DOI: 10.1097/00042560-199504120-00003. View

18.

Voss G, Li J, Manson K, Wyand M, Sodroski J, Letvin N . Human immunodeficiency virus type 1 envelope glycoprotein-specific cytotoxic T lymphocytes in simian-human immunodeficiency virus-infected rhesus monkeys. Virology. 1995; 208(2):770-5. DOI: 10.1006/viro.1995.1209. View

19.

Sullivan N, Sun Y, Li J, Hofmann W, Sodroski J . Replicative function and neutralization sensitivity of envelope glycoproteins from primary and T-cell line-passaged human immunodeficiency virus type 1 isolates. J Virol. 1995; 69(7):4413-22. PMC: 189183. DOI: 10.1128/JVI.69.7.4413-4422.1995. View

20.

Luciw P, Shaw K, Levy J, Cheng-Mayer C . Persistent infection of rhesus macaques with T-cell-line-tropic and macrophage-tropic clones of simian/human immunodeficiency viruses (SHIV). Proc Natl Acad Sci U S A. 1995; 92(16):7490-4. PMC: 41365. DOI: 10.1073/pnas.92.16.7490. View