Mechanism of HIV-1 viral protein R-induced apoptosis

Biochemical and Biophysical Research Communications

Volumn 304, Issue 3, 2003, Pages 583-592

  Muthumani, Karuppiah ^a   Choo, Andrew Y ^a   Hwang, Daniel S ^a   Chattergoon, Michael A ^a   Dayes, Nathanael N ^a   Zhang, Donghui ^a   Lee, Mark D ^a   Duvvuri, Umaheswar ^a   Weiner, David B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

AIF; Apoptosis; Caspase; Cytochrome c; HIV 1 Vpr; Mitochondrial membrane potential; NF B

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; APOPTOSIS INDUCING FACTOR; CASPASE 3; CASPASE 9; CD4 ANTIGEN; CYTOCHROME C; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL XL; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPR PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL MEMBRANE POTENTIAL; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MITOCHONDRIAL MEMBRANE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS PARTICLE; VIRUS PATHOGENESIS; VIRUS REPLICATION;

FORMICIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0037427469     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(03)00631-4     Document Type: Article

References (54)

1. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell. 102:2000;1-4.
2. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Jeonard L.M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373:1995;123-126.
3. Wei X., Ghosh S.K., Taylor M.E., Johnson V.A., Emini E.A., Deutsch P., Lifson J.D., Bonhoeffer S., Nowak M.A., Hahn B.H. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:1995;117-122.
4. Finkel T.H., Tudor-Williams G., Banda N.K., Cotton M.F., Curiel T., Monks C., Baba T.W., Ruprecht R.M., Kupfer A. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1:1995;129-134.
5. Muro-Cacho C.A., Pantaleo G., Fauci A.S. Analysis of apoptosis in lymph nodes of HIV-infected persons. Intensity of apoptosis correlates with the general state of activation of the lymphoid tissue and not with stage of disease or viral burden. J. Immunol. 154:1995;5555-5566.
6. + T cells by a Fas-independent mechanism. J. Exp. Med. 187:1998;1113-1122.
7. Cohen E.A., Dehni G., Sodroski J.G., Haseltine W.A. Human immunodeficiency virus vpr product is a virion-associated regulatory protein. J. Virol. 64:1990;3097-3099.
8. Subbramanian R.A., Kessous-Elbaz A., Lodge R., Forget J., Yao X.J., Bergeron D., Cohen E.A. Human immunodeficiency virus type 1 Vpr is a positive regulator of viral transcription and infectivity in primary human macrophages. J. Exp. Med. 187:1998;1103-1111.
9. Ayyavoo V., Mahboubi A., Mahalingam S., Ramalingam R., Kudchodkar S., Williams W.V., Green D.R., Weiner D.B. HIV-1 Vpr suppresses immune activation and apoptosis through regulation of nuclear factor κ B. Nat. Med. 3:1997;1117-1123.
10. Levy D.N., Refaeli Y., Weiner D.B. Extracellular Vpr protein increases cellular permissiveness to human immunodeficiency virus replication and reactivates virus from latency. J. Virol. 69:1995;1243-1252.
11. Muthumani K., Hwang D.S., Desai B.M., Zhang D., Dayes N., Green D.R., Weiner D.B. HIV-1 Vpr induces apoptosis through caspase 9 in T cells and peripheral blood mononuclear cells. J. Biol. Chem. 277:2002;37820-37831.
12. Roumier T., Vieira H.L., Castedo M., Ferri K.F., Boya P., Andreau K., Druillennec S., Joza N., Penninger J.M., Roques B., Kroemer G. The C-terminal moiety of HIV-1 Vpr induces cell death via a caspase-independent mitochondrial pathway. Cell Death Differ. (11):2002;1212-1219.
13. Levy D.N., Refaeli Y., MacGregor R.R., Weiner D.B. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA. 91:1994;10873-10877.
14. Jacotot E., Ravagnan L., Loeffler M., Ferri K.F., Vieira H.L., Zamzami N., Costantini P., Druillennec S., Hoebeke J., Briand J.P., Irinopoulou T., Daugas E., Susin S.A., Cointe D., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. J. Exp. Med. 191:2000;33-46.
15. Jacotot E., Ferri K.F., El Hamel C., Brenner C., Druillennec S., Hoebeke J., Rustin P., Metivier D., Lenoir C., Geuskens M., Vieira H.L., Loeffler M., Belzacq A.S., Briand J.P., Zamzami N., Edelman L., Xie Z.H., Reed J.C., Roques B.P., Kroemer G. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 193:2001;509-519.
16. Stewart S.A., Poon B., Song J.Y., Chen I.S. Human immunodeficiency virus type 1 vpr induces apoptosis through caspase activation. J. Virol. 74:2000;3105-3111.
17. Rogel M.E., Wu L.I., Emerman M. The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection. J. Virol. 69:1995;882-888.
18. Re F., Braaten D., Franke E.K., Luban J. nodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. J. Virol. 69:1995;6859-6864.
19. Jowett J.B., Planelles V., Poon B., Shah N.P., Chen M.L., Chen I.S. The human immunodeficiency virus type 1 vpr gene arrests infected T cells in the G2. + M phase of the cell cycle J. Virol. 69:1995;6304-6313.
20. He J., Choe S., Walker R., Di Marzio P., Morgan D.O., Landau N.R. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 69:1995;6705-6711.
21. Zhao Y., Cao J., O'Gorman M.R., Yu M., Yogev R. Effect of human immunodeficiency virus type 1 protein R (vpr) gene expression on basic cellular function of fission yeast Schizosaccharomyces pombe. J. Virol. 70:1996;5821-5826.
22. Poon B., Grovit-Ferbas K., Stewart S.A., Chen I.S. Cell cycle arrest by Vpr in HIV-1 virions and insensitivity to antiretroviral agents. Science. 281:1998;266-269.
23. Mahalingam S., Ayyavoo V., Patel M., Kieber-Emmons T., Kao G.D., Muschel R.J., Weiner D.B. HIV-1 Vpr interacts with a human 34-kDa mov34 homologue, a cellular factor linked to the G2/M phase transition of the mammalian cell cycle. Proc. Natl. Acad. Sci. USA. 95:1998;3419-3424.
24. Goh W.C., Rogel M.E., Kinsey C.M., Michael S.F., Fultz P.N., Nowak M.A., Hahn B.H., Emerman M. HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo. Nat. Med. 4:1998;65-71.
25. Muthumani K., Zhang D., Hwang D.S., Kudchodkar S., Dayes N.S., Desai B.M., Malik A.S., Yang J.S., Chattergoon M.A., Maguire H.C. Jr., Weiner D.B. Adenovirus encoding HIV-1 Vpr activates caspase 9 and induces apoptotic cell death in both p53 positive and negative human tumor cell lines. Oncogene. 21:2002;4613-4625.
26. Alnemri E.S., Livingston D.J., Nicholson D.W., Salvesen G., Thornberry N.A., Wong W.W., Yuan J. Human ICE/CED-3 protease nomenclature. Cell. 87:1996;171.
27. Yang X., Chang H.Y., Baltimore D. Autoproteolytic activation of pro-caspases by oligomerization. Mol. Cell. 1:1998;319-325.
28. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
29. Navon G., Navon R., Shulman R.G., Yamane T. Phosphate metabolites in lymphoid, Friend erythroleukemia, and HeLa cells observed by high-resolution 31P nuclear magnetic resonance. Proc. Natl. Acad. Sci. USA. 75:1978;891-895.
30. Beg A.A., Sha W.C., Bronson R.T., Ghosh S., Baltimore D. Constitutive NF-κB activation, enhanced granulopoiesis, and neonatal lethality in I-κB α-deficient mice. Nature. 376:1995;167-170.
31. Beg A.A., Baltimore D. An essential role for NF-κB in preventing TNF-α-induced cell death. Science. 274:1996;782-784.
32. Wang C.Y., Mayo M.W., Baldwin A.S. Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-κB. Science. 274:1996;784-787.
33. Liu Z.G., Hsu H., Goeddel D.V., Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-κB activation prevents cell death. Cell. 87:1996;565-576.
34. Tanaka M., Fuentes M.E., Yamaguchi K., Durnin M.H., Dalrymple S.A., Hardy K.L., Goeddel D.V. Embryonic lethality, liver degeneration, and impaired NF-κB activation in IKK-β-deficient mice. Immunity. 10:1999;421-429.
35. Li Z.W., Chu W., Hu Y., Delhase M., Deerinck T., Ellisman M., Johnson R., Karin M. The IKKβ subunit of I-κB kinase (IKK) is essential for nuclear factor κB activation and prevention of apoptosis. J. Exp. Med. 189:1999;1839-1845.
36. Stehlik C., de Martin R., Kumabashiri I., Schmid J.A., Binder B.R., Lipp J. Nuclear factor (NF)-κB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor α-induced apoptosis. J. Exp. Med. 188:1998;211-216.
37. Wang C.Y., Mayo M.W., Korneluk R.G., Goeddel D.V., Baldwin A.S. Jr. NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science. 281:1998;1680-1683.
38. Deveraux Q.L., Takahashi R., Salvesen G.S., Reed J.C. X-linked IAP is a direct inhibitor of cell-death proteases. Nature. 388:1997;300-304.
39. Deveraux Q.L., Roy N., Stennicke H.R., Van Arsdale T., Zhou Q., Srinivasula S.M., Alnemri E.S., Salvesen G.S., Reed J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17:1998;2215-2223.
40. Chen C., Edelstein L.C., Gelinas C. The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell. Biol. 20:2000;2687-2695.
41. Vander Heiden M.G., Chandel N.S., Williamson E.K., Schumacker P.T., Thompson C.B. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 91:1997;627-637.
42. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
43. Wong B.R., Josien R., Lee S.Y., Sauter B., Li H.L., Steinman R.M., Choi Y. TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J. Exp. Med. 186:1997;2075-2080.
44. Levy D.N., Fernandes L.S., Williams W.V., Weiner D.B. Induction of cell differentiation by human immunodeficiency virus 1 vpr. Cell. 72:1993;541-550.
45. Refaeli Y., Levy D.N., Weiner D.B. The glucocorticoid receptor type II complex is a target of the HIV-1 vpr gene product. Proc. Natl. Acad. Sci. USA. 92:1995;3621-3625.
46. Heinzinger N.K., Bukinsky M.I., Haggerty S.A., Ragland A.M., Kewalramani V., Lee M.A., Gendelman H.E., Ratner L., Stevenson M., Emerman M. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc. Natl. Acad. Sci. USA. 91(15):1994;7311-7315.
47. Vodicka M.A., Koepp D.M., Silver P.A., Emerman M. HIV-1 Vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev. 12(2):1998;175-185.
48. + T cells. J. Exp. Med. 194:2001;1407-1419.
49. de Noronha C.M., Sherman M.P., Lin H.W., Cavrois M.V., Moir R.D., Goldman R.D., Greene W.C. Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science. 294:2001;1105-1108.
50. Somasundaran M., Sharkey M., Brichacek B., Luzuriaga K., Emerman M., Sullivan J.L., Stevenson M. Evidence for a cytopathogenicity determinant in HIV-1 Vpr. Proc. Natl. Acad. Sci. USA. 14:2002;9503-9508.
51. Sherman M.P., Schubert U., Williams S.A., de Noronha C.M., Kreisberg J.F., Henklein P., Greene W.C. HIV-1 Vpr displays natural protein-transducing properties: implications for viral pathogenesis. Virology. 302:2002;95-105.
52. Kino T., Gragerov A., Kopp J.B., Stauber R.H., Pavlakis G.N., Chrousos G.P. The HIV-1 virion-associated protein vpr is a coactivator of the human glucocorticoid receptor. J. Exp. Med. 189:1999;51-62.
53. Yao X.J., Lemay J., Rougeau N., Clement M., Kurtz S., Belhumeur P., Cohen E.A. Genetic selection of peptide inhibitors of human immunodeficiency virus type 1 vpr. J. Biol. Chem. 277:2002;48816-48826.
54. Phenix B.N., Lum J.J., Nie Z., Sanchez-Dardon J., Badley A.D. Antiapoptotic mechanism of HIV protease inhibitors: preventing mitochondrial transmembrane potential loss. Blood. 98:2001;1078-1085.