Antiapoptotic mechanism of HIV protease inhibitors: Preventing mitochondrial transmembrane potential loss

Blood

Volumn 98, Issue 4, 2001, Pages 1078-1085

  Phenix, Barbara N ^a,b   Lum, Julian J ^a,b   Nie, Zehn ^a,b   Sanchez Dardon, Jaime ^a,b   Badley, Andrew D ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; FAS ANTIGEN; NELFINAVIR; PROTEINASE INHIBITOR; RITONAVIR; SAQUINAVIR; ZIDOVUDINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MEDIATOR RELEASE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0035883068     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood.V98.4.1078     Document Type: Article

References (69)

1. Richman DD. HIV therapeutics. Science. 1996;272:1886-1888.
2. Palella FJ, Delaney KM, Moorman A, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus syndrome. N Engl J Med. 1998;338:853-860.
3. Cameron DW, Hearth-Chiozzi M, Danner S, et al. Randomized placebo-controlled trial of ritonavir in advanced HIV-1 disease. Lancet. 1998;351:543-549.
4. Angel JB, Kumar A, Parato K, Filion LG, Diaz-Mitoma F, Daftarian P. Improvement in cell-mediated immune function during potent anti-human immunodeficiency virus therapy with ritonavir plus saquinavir. J Infect Dis. 1998;177:898-904.
5. Lederman MM, Connick E, Landay A, et al. Immunologic responses associated with 12 weeks of combination antiretroviral therapy consisting of zidovudine, lamivudine, and ritonavir: results of AIDS Clinical Trials Group Protocol 315. J Infect Dis. 1998;178:70-79.
6. Pakker NG, Notermans DW, de Boer RJ, et al. Biphasic kinetics of peripheral blood T cells after triple combination therapy in HIV-1 infection: a composite of redistribution and proliferation. Nat Med. 1998;4:208-214.
7. Autran B, Carcelain G, Li TS, Blanc C, Mathez D, Tubiana R. Positive effects of combined antiretroviral therapy on CD4+ T cell homeostasis and function in advanced HIV disease. Science. 1997;277:112-116.
8. Gorochov G, Neumann AU, Kereveur A, et al. Perturbation of CD4+ and CD8+ T-cell repertoires during progression to AIDS and regulation of the CD4+ repertoire during antiviral therapy. Nat Med. 1998;4:215-221.
9. Phenix BN, Angel JB, Mandy F, et al. Decreased HIV-associated T cell apoptosis by HIV protease inhibitors. AIDS Res Hum Retroviruses. 2000;16:559-567.
10. Collier AC, Coombs RW, Schoenfeld DA, et al. Treatment of human immunodeficiency virus infection with saquinavir, zidovudine, and zalcitabine. AIDS Clinical Trials Group. N Engl J Med. 1996;334:1011-1017.
11. Kaufmann D, Pantaleo G, Sudre P, Telenti A. CD4-cell count in HIV-1-infected individuals remaining viraemic with highly active antiretroviral therapy (HAART). Swiss HIV Cohort Study [letter]. Lancet. 1998;351:723-724.
12. Levitz SM. Improvement in CD4+ cell counts despite persistently detectable HIV load [letter]. N Engl J Med. 1998;338:1074-1075.
13. Piketty C, Castiel P, Belec L, et al. Discrepant responses to triple combination antiretroviral therapy in advanced HIV disease. AIDS. 1998;12:745-750.
14. Andre P, Groettrup M, Klenerman P, et al. An inhibitor of HIV-1 protease modulates proteasome activity, antigen presentation, and T cell responses. Proc Natl Acad Sci U S A. 1998;95:13120-13124.
15. Berthold HK, Parhofer KG, Ritter MM, et al. Influence of protease inhibitor therapy on lipoprotein metabolism. J Intern Med. 1999;246:567-575.
16. Gagnon AM, Angel JB, Sorisky A. Protease inhibitors and adipocyte differentiation in cell culture. Lancet. 1998;352:1032.
17. Zhang B, MacNaul K, Szalkowski D, Li Z, Berger J, Moller DE. Inhibition of adipocyte differentiation by HIV protease inhibitors. J Clin Endocrinol Metab. 1999;84:4274-4277.
18. Eagling VA, Back DJ, Barry MG. Differential inhibition of cytochrome P450 isoforms by the protease inhibitors, ritonavir, saquinavir and indinavir. Br J Clin Pharmacol. 1997;44:190-194.
19. Gutmann H, Fricker G, Drewe J, Toeroek M, Miller DS. Interactions of HIV protease inhibitors with ATP-dependent drug export proteins. Mol Pharmacol. 1999;56:383-389.
20. Weichold FF, Bryant JL, Pati S, Barabitskaya O, Gallo RC, Reitz MS Jr. HIV-1 protease inhibitor ritonavir modulates susceptibility to apoptosis of uninfected T cells. J Hum Virol. 1999;2:261-269.
21. Sloand EM, Kumar PN, Kim S, Chaudhuri A, Weichold FF, Young NS. Human immunodeficiency virus type 1 protease inhibitor modulates activation of peripheral blood CD4(+) T cells and decreases their susceptibility to apoptosis in vitro and in vivo. Blood. 1999;94:1021-1027.
22. Sloand EM, Maciejewski J, Kumar P, Kim S, Chaudhuri A, Young N. Protease inhibitors stimulate hematopoiesis and decrease apoptosis and ICE expression in CD34+ cells. Blood. 2000;96:2735-2739.
23. Johnson N, Parkin JM. Anti-retroviral therapy reverses HIV-associated abnormalities in lymphocyte apoptosis. Clin Exp Immunol. 1998;113:229-234.
24. Badley AD, Parato K, Cameron DW, et al. Dynamic correlation of apoptosis and immune activation during treatment of HIV infection. Cell Death Differ. 1999;6:420-432.
25. Badley AD, Dockrell DH, Algeciras A, et al. In vivo analysis of Fas/FasL interactions in HIV-infected patients. J Clin Invest. 1998;102:79-87.
26. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods. 1995;184:39-51.
27. Marzo I, Brenner C, Zamzami N, et al. The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med. 1998;187:1261-1271.
28. Medema JP, Scaffidi C, Kischkel FC, et al. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 1997;16:2794-2804.
29. Evans EK, Kuwana T, Strum SL, Smith JJ, Newmeyer DD, Kornbluth S. Reaper-induced apoptosis in a vertebrate system. EMBO J. 1997;16:7372-7381.
30. Marchenko ND, Zika A, Moll UM. Signal-induced localization of P53 protein to mitochondria. J Biol Chem. 2000;275:16202-16212.
31. Sims NR. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J Neurochem. 1990;55:698-707.
32. Reinhart PH, Taylor WM, Bygrave FL. A procedure for the rapid preparation of mitochondria from rat liver. J Biochem. 1982;204:731-735.
33. Flexner C. HIV-protease inhibitors. N Engl J Med. 1998;338:1281-1292.
34. Jarvis B, Faulds D. Nelfinavir. A review of its therapeutic efficacy in HIV infection. Drugs. 1998;56:147-167.
35. Markowitz M, Conant M, Hurley A, et al. A preliminary evaluation of nelfinavir mesylate, an inhibitor of human immunodeficiency virus (HIV)-1 protease, to treat HIV infection. J Infect Dis. 1998;177:1533-1540.
36. Pithavala YK, Zhang M, Knowles M, Dniels R, Anderson R, Kerr B. Virologic response-plasma drug concentration relationship in a phase III study of nelfinavir mesylate. 12th World AIDS Conference. Geneva, Switzerland; 1998.
37. Aweeka F, Jayewardene A, Staprans S, et al. Failure to detect nelfinavir in the cerebrospinal fluid of HIV-1-infected patients with and without AIDS dementia complex. J Acquir Immune Defic Syndr Hum Retrovirol. 1999;20:39-43.
38. Petit PX, Zamzami N, Vanyssiere JL, Mignotte B, Kroemer G, Castedo M. Implication of mitochondria in apoptosis. Mol Cell Biochem. 1997;174:185-188.
39. Lemasters JJ, Qian T, Trost LC, et al. Confocal microscopy of the mitochondrial permeability transition in necrotic and apoptotic cell death. Biochem Soc Symp. 1999;66:205-222.
40. Costantini P, Jacotot E, Decaudin D, Kroemer G. Mitochondrion as a novel target of anticancer chemotherapy. J Natl Cancer Inst. 2000;92:1042-1053.
41. Daugas E, Nochy D, Ravagnan L, et al. Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 2000;476:118-123.
42. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281:1309-1312.
43. Li P, Nijhawan D, Budihardjo I, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91:479-489.
44. Green DR. Apoptotic pathways: the roads to ruin. Cell. 1998;94:695-698.
45. Jacotot E, Ravagnan L, Loeffler M, et al. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J Exp Med. 2000;191:33-46.
46. Zamzami N, Susin SA, Marchetti P, et al. Mitochondrial control of nuclear apoptosis [see comments]. J Exp Med. 1996;183:1533-1544.
47. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998;17:1675-1687.
48. Scaffidi C, Schmitz I, Zha J, Korsmeyer SJ, Krammer PH, Peter ME. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J Biol Chem. 1999;274:22532-22538.
49. Peter ME, Krammer PH. Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr Opin Immunol. 1998;10:545-551.
50. Hertzberg RP, Caranfa MJ, Hecht SM. On the mechanism of topoisomerase I inhibition by camptothecin: evidence for binding to an enzyme-DNA complex. Biochemistry. 1989;30:4629-4638.
51. Dalgleish AG, Beverley PC, Clapham PR, Crawford DH, Greaves MF, Weiss RA. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984;312:763-767.
52. Klatzmann D, Champagne E, Chamaret S, et al. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 1984;312:767-768.
53. Peng C, Ho BK, Chang TW, Chang NT. Role of human immunodeficiency virus type 1-specific protease in core protein maturation and viral infectivity. J Virol. 1989;63:2550-2556.
54. Kaplan AH, Swanstrom R. Human immunodeficiency virus type 1 Gag proteins are processed in two cellular compartments. Proc Natl Acad Sci U S A. 1991;88:4528-4532.
55. Patick AK, Mo H, Markowitz M, et al. Antiviral and resistance studies of AG1343, an orally bioavailable inhibitor of human immunodeficiency virus protease [published erratum appears in Antimicrob Agents Chemother. 1996;40:1575]. Antimicrob Agents Chemother. 1996;40:292-297.
56. Fernandes RS, McGowan AJ, Cotter TG. Mutant H-ras overexpression inhibits drug and U.V. induced apoptosis. Anticancer Res. 1996;16:1691-1705.
57. Itoh N, Yonehara S, Ishii A, et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell. 1991;26:233-243.
58. Zoratti M, Szabo I. Electrophysiology of the inner mitochondrial membrane. J Bioenerg Biomembr. 1994;26:543-553.
59. Bernardi P, Broekemeie KM, Pfeiffer DR. Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr. 1994;26:509-517.
60. Zamzami N, Marchetti P, Castedo M, et al. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med. 1995;182:367-377.
61. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis [published erratum appears in Nat Med. 1997;3:934]. Nat Med. 1997;3:614-620.
62. Marchetti P, Castedo M, Susin SA, et al. Mitochondrial permeability transition is a central coordinating event of apoptosis. J Exp Med. 1996;184:1155-1160.
63. Kantrow SP, Piantadosi CA. Release of cytochrome c from liver mitochondria during permeability transition. Biochem Biophys Res Commun. 1997;232:669-671.
64. Susin SA, Lorenzo HK, Zamzami N, et al. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J Exp Med. 1999;189:381-383.
65. Susin SA, Zamzami N, Castedo M, et al. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med. 1996;184:1331-1341.
66. Wood E, Yip B, Hogg RS, et al. Full suppression of viral load is needed to achieve an optimal CD4 cell count response among patients on triple drug antiretroviral therapy. AIDS. 2000;14:1955-1960.
67. Kravcik S, Magill A, Sanghvi B, et al. Comparative CD4 T cell responses of protease inhibitor containing and sparing antiretroviral regimes. HIV Clin Trials. 2001;2:160-170.
68. Carr A, Chuah J, Hudson J, et al. A randomised, open-label comparison of three highly active antiretroviral therapy regimens including two nucleoside analogues and indinavir for previously untreated HIV-1 infection: the OzCombo1 study. AIDS. 2000;14:1171-1180.
69. Hawley-Foss N, Mbisa G, Lum JJ, et al. Effects of therapy cessation during a discordant response to HAART; implications for scheduled therapeutic interruptions. Clin Infect Dis. In Press.