CD4+ T-cell Death Induced by Infectious and Noninfectious HIV-1: Role of Type 1 Interferon-dependent, TRAIL/DR5-mediated Apoptosis

Overview

Journal Blood

Publisher Elsevier

Specialty Hematology

Date 2005 Jul 28

PMID 16046522

Citations 118

Authors

Jean-Philippe Herbeuval

Jean-Charles Grivel

Adriano Boasso

Andrew W Hardy

Claire Chougnet

Matthew J Dolan

Hideo Yagita

Jeffrey D Lifson

Gene M Shearer

Affiliations

Soon will be listed here.

Abstract

It has been proposed that direct and indirect mechanisms contribute to the unresolved issue of CD4(+) T-cell depletion that results from HIV-1 infection. We recently reported that plasma levels of tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL) are elevated in HIV-1-infected patients and that they correlate with viral load. The present study investigates the expression of TRAIL death receptor 5 (DR5) in the peripheral-blood mononuclear cells (PBMCs) of HIV-1-infected patients and its role in CD4(+) T-cell death. DR5 expression was elevated and associated with the apoptotic marker annexin V. Apoptosis was reduced in CD4(+) T cells when cultured with anti-DR5 antibody. CD4(+), but not CD8(+), T cells from uninfected donors expressed TRAIL, DR5, and activated caspase-3 when cultured with infectious or noninfectious HIV-1, resulting in preferential apoptosis of CD4(+) T cells. TRAIL, caspase-3 expression, and apoptosis were type 1 interferon (IFN) dependent. Induction of apoptosis and DR5 expression required glycoprotein 120 (gp120)-CD4 interaction. Finally, we analyzed DR5 expression by CD4(+) T cells in highly active antiretroviral therapy (HAART)-treated patients. The decreased viral loads and increased CD4 counts of HAART-responsive patients were associated with a decrease in DR5 mRNA expression by CD4(+) T lymphocytes. We propose a novel model in which a type 1 IFN-regulated TRAIL /DR5 mechanism induces apoptosis of HIV-1-exposed CD4(+) T cells.

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References

Abel K, Rothaeusler K, Marthas M, Miller C . The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFN-alpha/beta) and IFN-alpha/beta-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. J Virol. 2002; 76(16):8433-45. PMC: 155165. DOI: 10.1128/jvi.76.16.8433-8445.2002. View

Katsikis P, Torres-Roca J, Tijoe I, Smith C, Herzenberg L . Interleukin-1 beta converting enzyme-like protease involvement in Fas-induced and activation-induced peripheral blood T cell apoptosis in HIV infection. TNF-related apoptosis-inducing ligand can mediate activation-induced T cell death in HIV.... J Exp Med. 1997; 186(8):1365-72. PMC: 2199088. DOI: 10.1084/jem.186.8.1365. View

Yang Y, Tikhonov I, Ruckwardt T, Djavani M, Zapata J, Pauza C . Monocytes treated with human immunodeficiency virus Tat kill uninfected CD4(+) cells by a tumor necrosis factor-related apoptosis-induced ligand-mediated mechanism. J Virol. 2003; 77(12):6700-8. PMC: 156176. DOI: 10.1128/jvi.77.12.6700-6708.2003. View

Takaoka A, Hayakawa S, Yanai H, Stoiber D, Negishi H, Kikuchi H . Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence. Nature. 2003; 424(6948):516-23. DOI: 10.1038/nature01850. View

Vilcek J . Boosting p53 with interferon and viruses. Nat Immunol. 2003; 4(9):825-6. DOI: 10.1038/ni0903-825. View

Ryan L, Peng H, Erichsen D, Huang Y, Persidsky Y, Zhou Y . TNF-related apoptosis-inducing ligand mediates human neuronal apoptosis: links to HIV-1-associated dementia. J Neuroimmunol. 2004; 148(1-2):127-39. DOI: 10.1016/j.jneuroim.2003.11.019. View

Lichtner M, Maranon C, Vidalain P, Azocar O, Hanau D, Lebon P . HIV type 1-infected dendritic cells induce apoptotic death in infected and uninfected primary CD4 T lymphocytes. AIDS Res Hum Retroviruses. 2004; 20(2):175-82. DOI: 10.1089/088922204773004897. View

Dianzani U, Bensi T, Savarino A, Sametti S, Indelicato M, Mesturini R . Role of FAS in HIV infection. Curr HIV Res. 2004; 1(4):405-17. DOI: 10.2174/1570162033485131. View

Vasilescu A, Heath S, Diop G, Do H, Hirtzig T, Hendel H . Genomic analysis of Fas and FasL genes and absence of correlation with disease progression in AIDS. Immunogenetics. 2004; 56(1):56-60. DOI: 10.1007/s00251-004-0664-3. View

10.

Fonteneau J, Larsson M, Beignon A, McKenna K, DaSilva I, Amara A . Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol. 2004; 78(10):5223-32. PMC: 400371. DOI: 10.1128/jvi.78.10.5223-5232.2004. View

11.

Mehandru S, Poles M, Tenner-Racz K, Horowitz A, Hurley A, Hogan C . Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med. 2004; 200(6):761-70. PMC: 2211967. DOI: 10.1084/jem.20041196. View

12.

Brenchley J, Schacker T, Ruff L, Price D, Taylor J, Beilman G . CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004; 200(6):749-59. PMC: 2211962. DOI: 10.1084/jem.20040874. View

13.

Harper M, Marselle L, Gallo R, Wong-Staal F . Detection of lymphocytes expressing human T-lymphotropic virus type III in lymph nodes and peripheral blood from infected individuals by in situ hybridization. Proc Natl Acad Sci U S A. 1986; 83(3):772-6. PMC: 322947. DOI: 10.1073/pnas.83.3.772. View

14.

Yamamoto J, Barre-Sinoussi F, Bolton V, Pedersen N, Gardner M . Human alpha- and beta-interferon but not gamma- suppress the in vitro replication of LAV, HTLV-III, and ARV-2. J Interferon Res. 1986; 6(2):143-52. DOI: 10.1089/jir.1986.6.143. View

15.

Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162(1):156-9. DOI: 10.1006/abio.1987.9999. View

16.

Schnittman S, Psallidopoulos M, Lane H, Thompson L, Baseler M, Massari F . The reservoir for HIV-1 in human peripheral blood is a T cell that maintains expression of CD4. Science. 1989; 245(4915):305-8. DOI: 10.1126/science.2665081. View

17.

Chaudhary P, Eby M, Jasmin A, Bookwalter A, Murray J, Hood L . Death receptor 5, a new member of the TNFR family, and DR4 induce FADD-dependent apoptosis and activate the NF-kappaB pathway. Immunity. 1998; 7(6):821-30. DOI: 10.1016/s1074-7613(00)80400-8. View

18.

Jeremias I, Herr I, Boehler T, Debatin K . TRAIL/Apo-2-ligand-induced apoptosis in human T cells. Eur J Immunol. 1998; 28(1):143-52. DOI: 10.1002/(SICI)1521-4141(199801)28:01<143::AID-IMMU143>3.0.CO;2-3. View

19.

Zagury D, Lachgar A, Chams V, Fall L, Bernard J, Zagury J . Interferon alpha and Tat involvement in the immunosuppression of uninfected T cells and C-C chemokine decline in AIDS. Proc Natl Acad Sci U S A. 1998; 95(7):3851-6. PMC: 19926. DOI: 10.1073/pnas.95.7.3851. View

20.

Esser M, Bess Jr J, Suryanarayana K, Chertova E, Marti D, Carrington M . Partial activation and induction of apoptosis in CD4(+) and CD8(+) T lymphocytes by conformationally authentic noninfectious human immunodeficiency virus type 1. J Virol. 2001; 75(3):1152-64. PMC: 114021. DOI: 10.1128/JVI.75.3.1152-1164.2001. View