Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4

Journal of Clinical Investigation

Volumn 116, Issue 8, 2006, Pages 2161-2172

  Espert, Lucile ^a   Denizot, Mélanie ^a   Grimaldi, Marina ^a   Robert Hebmann, Véronique ^a   Gay, Bernard ^a   Varbanov, Mihayl ^a   Codogno, Patrice ^b   Biard Piechaczyk, Martine ^a  

^a CNRS   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; BAFILOMYCIN A1; CHEMOKINE RECEPTOR CXCR4; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 160; GLYCOPROTEIN GP 41; PROTEIN KINASE LCK; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; AUTOPHAGY; CD4+ T LYMPHOCYTE; CELL DEATH; CELL LINE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN BINDING; T LYMPHOCYTE; VIRUS REPLICATION; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CELL DEATH; CELL LINE; COCULTURE TECHNIQUES; GENE PRODUCTS, ENV; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; KIDNEY; RECEPTORS, CXCR4; T-LYMPHOCYTES;

EID: 33746691954     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI26185     Document Type: Article

References (82)

1. Maldarelli, F., Sato, H., Berthold, E., Orenstein, J., and Martin, M.A. 1995. Rapid induction of apoptosis by cell-to-cell transmission of human immunodeficiency virus type 1. J. Virol. 69:6457-6465.
2. + T cells. J. Gen. Virol. 76:681-690.
3. Laurent-Crawford, A.G., et al. 1993. Membrane expression of HIV envelope glycoproteins triggers apoptosis in CD4 cells. AIDS Res. Hum. Retroviruses. 9:761-773.
4. Garcia, E., et al. 2005. HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic. 6:488-501.
5. Jolly, C., Kashefi, K., Hollinshead, M., and Sattentau, Q.J. 2004. HIV-1 cell to cell transfer across an Env-induced, actin-dependent synapse. J. Exp. Med. 199:283-293.
6. Nobile, C., et al. 2005. Covert human immunodeficiency virus replication in dendritic cells and in DC-SIGN-expressing cells promotes long-term transmission to lymphocytes. J. Virol. 79:5386-5399.
7. Sivard, P., et al. 2004. HIV-1 infection of Langerhans cells in a reconstructed vaginal mucosa. J. Infect. Dis. 190:227-235.
8. Ferri, K.F., et al. 2000. Apoptosis control in syncytia induced by the HIV type 1-envelope glycoprotein complex. Role of mitochondria and caspases. J. Exp. Med. 192:1081-1092.
9. Roggero, R., et al. 2001. Binding of human immunodeficiency virus type 1 gp120 to CXCR4 induces mitochondrial transmembrane depolarization and cytochrome c-mediated apoptosis independently of Fas signaling. J. Virol. 75:7637-7650.
10. Blanco, J., et al. 1999. The implication of the chemokine receptor CXCR4 in HIV-1 envelope protein-induced apoptosis is independent of the G protein-mediated signalling. AIDS. 13:909-917.
11. Hazenberg, M.D., et al. 2003. Depletion of naive CD4 T cells by CXCR4-using HIV-1 variants occurs mainly through increased T-cell death and activation. AIDS. 17:1419-1424.
12. Nishimura, Y., et al. 2004. 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. 101:12324-12329.
13. Bursch, W., Ellinger, A., Gerner, C., Frohwein, U., and Schulte-Hermann, R. 2000. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann. N. Y. Acad. Sci. 926:1-12.
14. Lockshin, R.A., Osborne, B., and Zakeri, Z. 2000. Cell death in the third millennium. Cell Death Differ. 7:2-7.
15. Clarke, P.G. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.). 181:195-213.
16. Baehrecke, E.H. 2003. Caspase activation finds fertile ground. Dev. Cell. 4:608-609.
17. Gonzalez-Polo, R.A., et al. 2005. The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J. Cell Sci. 118:3091-3102.
18. Yoshimori, T. 2004. Autophagy: a regulated bulk degradation process inside cells. Biochem. Biophys. Res. Commun. 313:453-458.
19. Mizushima, N., Sugita, H., Yoshimori, T., and Ohsumi, Y. 1998. A new protein conjugation system in human. The counterpart of the yeast Apg12p conjugation system essential for autophagy. J. Biol. Chem. 273:33889-33892.
20. Ohsumi, Y. 2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2:211-216.
21. Tanida, I., Ueno, T., and Kominami, E. 2004. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36:2503-2518.
22. Kabeya, Y., et al. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
23. Kihara, A., Kabeya, Y., Ohsumi, Y., and Yoshimori, T. 2001. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:330-335.
24. Liang, X.H., et al. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402:672-676.
25. Kuma, A., et al. 2004. The role of autophagy during the early neonatal starvation period. Nature. 432:1032-1036.
26. Lum, J.J., et al. 2005. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell. 120:237-248.
27. Boya, P., et al. 2005. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25:1025-1040.
28. Pattingre, S., et al. 2005. Bcl-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell. 122:927-939.
29. Shimizu, S., et al. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6:1221-1228.
30. Yue, Z., Jin, S., Yang, C., Levine, A.J., and Heintz, N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U. S. A. 100:15077-15082.
31. Baehrecke, E.H. 2003. Autophagic programmed cell death in Drosophila. Cell Death Differ. 10:940-945.
32. Debnath, J., Baehrecke, E.H., and Kroemer, G. 2005. Does autophagy contribute to cell death? Autophagy. 1:66-74.
33. Levine, B., and Yuan, J. 2005. Autophagy in cell death: an innocent convict? J. Clin. Invest. 115:2679-2688. doi:10.1172/JCI26390.
34. Lamparska-Przybysz, M., Gajkowska, B., and Motyl, T. 2005. Cathepsins and BID are involved in the molecular switch between apoptosis and autophagy in breast cancer MCF-7 cells exposed to camptothecin. J. Physiol. Pharmacol. 56(Suppl. 3):159-179.
35. Furuya, D., Tsuji, N., Yagihashi, A., and Watanabe, N. 2005. Beclin 1 augmented cis-diamminedichloroplatinum induced apoptosis via enhancing caspase-9 activity. Exp. Cell Res. 307:26-40.
36. Liang, X.H., et al. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72:8586-8596.
37. Takacs-Vellai, K., et al. 2005. Inactivation of the autophagy gene bec-1 triggers apoptotic cell death in C. elegans. Curr. Biol. 15:1513-1517.
38. Yu, L., et al. 2004. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science. 304:1500-1502.
39. Melendez, A., et al. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science. 301:1387-1391.
40. Petiot, A., Ogier-Denis, E., Blommaart, E.F., Meijer, A.J., and Codogno, P. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
41. Rusten, T.E., et al. 2004. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell. 7:179-192.
42. Daido, S., et al. 2004. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64:4286-4293.
43. Scarlatti, F., et al. 2004. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of beclin 1. J. Biol. Chem. 279:18384-18391.
44. Kirkegaard, K., Taylor, M.P., and Jackson, W.T. 2004. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2:301-314.
45. Prentice, E., Jerome, W.G., Yoshimori, T., Mizushima, N., and Denison, M.R. 2004. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279:10136-10141.
46. Jackson, W.T., et al. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156.
47. Talloczy, Z., et al. 2002. Regulation of starvationand virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 99:190-195.
48. Schlegel, A., Giddings, T.H., Jr., Ladinsky, M.S., and Kirkegaard, K. 1996. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 70:6576-6588.
49. Suhy, D.A., Giddings, T.H., Jr., and Kirkegaard, K. 2000. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J. Virol. 74:8953-8965.
50. Levine, B. 2005. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell. 120:159-162.
51. Paludan, C., et al. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science. 307:593-596.
52. Guillerm, C., Coudronnière, N., Robert-Hebmann, V., and Devaux, C. 1998. Delayed human immunodeficiency virus type 1-induced apoptosis in cells expressing truncated forms of CD4. J. Virol. 72:1754-1761.
53. lck tyrosine protein kinase. Mol. Cell. Biol. 10:1853-1862.
54. Yang, X.P., Gallo, M., Ngan, I., Nocerini, M., and Chen, M.M. 2002. Use of CMFDA and CMTMR fluorescent dyes in FACS-based antibody screening. Biotechniques. 32:678-680, 682.
55. Benkirane, M., Jeang, K.-T., and Devaux, C. 1994. The cytoplasmic domain of CD4 plays a critical role during the early stages of HIV infection in T-cells. EMBO J. 13:5559-5569.
56. Biard-Piechaczyk, M., et al. 2000. Caspase-dependent apoptosis of cells expressing the chemokine receptor CXCR4 is induced by cell membrane-associated Human Immunodeficiency Virus type 1 envelope glycoprotein (gp120). Virology. 268:329-344.
57. Donzella, G.A., et al. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
58. Blanco, J., et al. 2000. The CXCR4 antagonist AMD3100 efficiently inhibits cell-surface-expressed human immunodeficiency virus type 1 envelopeinduced apoptosis. Antimicrob. Agents Chemother. 44:51-56.
59. Fantini, J., et al. 1997. Synthetic soluble analogs of galactosylceramide (GalCer) bind to the V3 domain of HIV-1 gp120 and inhibit HIV-1-induced fusion and entry. J. Biol. Chem. 272:7245-7252.
60. Perfettini, J.L., et al. 2005. Mechanisms of apoptosis induction by the HIV-1 envelope. Cell Death Differ. 12(Suppl. 1):916-923.
61. Seglen, P.O., and Gordon, P.B. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 79:1889-1892.
62. Blommaart, E.F., Krause, U., Schellens, J.P., Vreeling-Sindelarova, H., and Meijer, A.J. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243:240-246.
63. Lockshin, R.A., and Zakeri, Z. 2004. Apoptosis, autophagy, and more. Int. J. Biochem. Cell Biol. 36:2405-2419.
64. Bowman, E.J., Siebers, A., and Altendorf, K. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. U. S. A. 85:7972-7976.
65. Yamamoto, A., et al. 1998. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23:33-42.
66. Hesselgesser, J., et al. 1998. Neuronal apoptosis induced by HIV-1 gp120 and the chemokine SDF-1α is mediated by the chemokine receptor CXCR4. Curr. Biol. 8:595-598.
67. Canu, N., et al. 2005. Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92:1228-1242.
68. Guimaraes, C.A., Benchimol, M., Amarante-Mendes, G.P., and Linden, R. 2003. Alternative programs of cell death in developing retinal tissue. J. Biol. Chem. 278:41938-41946.
69. Jia, L., et al. 1997. Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br. J. Haematol. 98:673-685.
70. Uchiyama, Y. 2001. Autophagic cell death and its execution by lysosomal cathepsins. Arch. Histol. Cytol. 64:233-246.
71. Hoyer-Hansen, M., Bastholm, L., Mathiasen, I.S., Elling, F., and Jaattela, M. 2005. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ. 12:1297-1309.
72. Xue, L., Fletcher, G.C., and Tolkovsky, A.M. 1999. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14:180-198.
73. Shao, Y., Gao, Z., Marks, P.A., and Jiang, X. 2004. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc. Natl. Acad. Sci. U. S. A. 101:18030-18035.
74. Kosta, A., et al. 2004. Autophagy gene disruption reveals a non-vacuolar cell death pathway in Dictyostelium. J. Biol. Chem. 279:48404-48409.
75. Priault, M., et al. 2005. Impairing the bioenergetic status and the biogenesis of mitochondria triggers mitophagy in yeast. Cell Death Differ. 12:1613-1621.
76. Bras, M., Queenan, B., and Susin, S.A. 2005. Programmed cell death via mitochondria: different modes of dying. Biochemistry (Mosc.). 70:231-239.
77. Castino, R., Isidoro, C., and Murphy, D. 2005. Autophagy-dependent cell survival and cell death in an autosomal dominant familial neurohypophyseal diabetes insipidus in vitro model. FASEB J. 19:1024-1026.
78. Broker, L.E., Kruyt, F.A., and Giaccone, G. 2005. Cell death independent of caspases: a review. Clin. Cancer Res. 11:3155-3162.
79. Golstein, P., and Kroemer, G. 2005. Redundant cell death mechanisms as relics and backups. Cell Death Differ. 12(Suppl. 2):1490-1496.
80. Bedinger, P., et al. 1988. Internalization of the human immunodeficiency virus does not require the cytoplasmic domain of CD4. Nature. 334:162-165.
81. Charret, R., and Fauré-Fremiet, E. 1967. Technique de rassemblement de micro-organismes: préinclusion dans un caillot de fibrine. J. Microsc. 6:1063-1066.
82. Zar, J.H. 1996. Biostatistical analysis. 3rd edition. Prentice Hall. Upper Saddle River, New Jersey, USA. 662 pp.