Therapeutic peptides: Targeting the mitochondrion to modulate apoptosis

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1757, Issue 9-10, 2006, Pages 1312-1323

  Jacotot, Etienne ^a   Deniaud, Aurélien ^b   Borgne Sanchez, Annie ^a   Touat, Zahia ^b   Briand, Jean Paul ^c   Le Bras, Morgane ^b   Brenner, Catherine ^b  

^a Theraptosis SA   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Apoptosis; Bcl 2; Mitochondrion; Peptides; Permeability transition

Indexed keywords

1 [4 (1H IMIDAZOL 1 YL)BENZOYL] N METHYLCYCLOBUTANECARBOTHIOAMIDE; 2 AMINO 6 BROMO 4 (1 CYANO 2 ETHOXY 2 OXOETHYL) 4H CHROMENE 3 CARBOXYLIC ACID ETHYL ESTER; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 5 HYDROXYDECANOIC ACID; 6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; APOPTOSIS INDUCING FACTOR; BENZOPORPHYRIN DERIVATIVE; BETULIC ACID; BMS 191095; CASPASE; CATION; CYTOCHROME C; DIAZOXIDE; F 16; FINGOLIMOD; GLIBENCLAMIDE; ION TRANSPORT AFFECTING AGENT; N SEC BUTYL 1 (2 CHLOROPHENYL) N METHYL 3 ISOQUINOLINECARBOXAMIDE; NICORANDIL; PEPTIDE; PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN ENDOG; RESVERATROL; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI; SULFONAMIDE; SUPEROXIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CELL ORGANELLE; DRUG DESIGN; DRUG TARGETING; ENZYME RELEASE; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; HIGH THROUGHPUT SCREENING; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; TOXICITY TESTING;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL SWELLING; MOLECULAR SEQUENCE DATA; PEPTIDES; PERMEABILITY;

ANIMALIA;

EID: 33748953187     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2006.07.002     Document Type: Review

References (124)

1. Loffet A. Peptides as drugs: is there a market. J. Pept. Sci. 8 (2002) 1-7
2. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257
3. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 267 (1995) 1456-1462
4. Nicotera P., Leist M., Single B., and Volbracht C. Execution of apoptosis: converging or diverging pathways?. Biol. Chem. 380 (1999) 1035-1040
5. Klionsky D.J., and Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 290 (2000) 1717-1721
6. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., and Tsujimoto Y. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6 (2004) 1221-1228
7. Lum J.J., Bauer D.E., Kong M., Harris M.H., Li C., Lindsten T., and Thompson C.B. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120 (2005) 237-248
8. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120 (2005) 159-162
9. Schweichel J.U., and Merker H.J. The morphology of various types of cell death in prenatal tissues. Teratology 7 (1973) 253-266
10. Clarke P.G. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.) 181 (1990) 195-213
11. Lockshin R.A., and Zakeri Z. Apoptosis, autophagy, and more. Int. J. Biochem. Cell Biol. 36 (2004) 2405-2419
12. Levine B., and Yuan J. Autophagy in cell death: an innocent convict?. J. Clin. Invest. 115 (2005) 2679-2688
13. Yuan J., and Yankner B.A. Apoptosis in the nervous system. Nature 407 (2000) 802-809
14. Elmore S., Qian T., Grissom S.F., and Lemasters J.J. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15 (2001) 2286-2287
15. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., and Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122 (2005) 927-939
16. Warburg O. On the origin of cancer cells. Science 123 (1956) 309-314
17. Reed J.C. Dysregulation of apoptosis in cancer. Cancer J. Sci. Am. 4 Suppl. 1 (1998) S8-S14
18. Kroemer G., Zamzami N., and Susin S.A. Mitochondrial control of apoptosis. Immunol. Today 18 (1997) 44-51
19. Brenner C., and Kroemer G. Apoptosis. Mitochondria-The death signal integrators. Science 289 (2000) 1150-1151
20. Desagher S., and Martinou J.C. Mitochondria as the central control point of apoptosis. Trends Cell. Biol. 10 (2000) 369-377
21. Henry-Mowatt J., Dive C., Martinou J.C., and James D. Role of mitochondrial membrane permeabilization in apoptosis and cancer. Oncogene 23 (2004) 2850-2860
22. Reed J.C. Apoptosis-based therapies. Nat. Rev., Drug Discov. 1 (2002) 111-121
23. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
24. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
25. Armstrong J. Mitochondrial membrane permeabilization: the sine qua non for cell death. BioEssays 28 (2006) 253-260
26. Garlid K., and Paucek P. Mitochondrial potassium transport: the K(+) cycle. Biochim. Biophys. Acta 1606 (2003) 23-41
27. Ardehali H., and O'Rourke B. Mitochondrial K(ATP) channels in cell survival and death. J. Mol. Cell Cardiol. 39 (2005) 7-16
28. Marzo I., Brenner C., Zamzami N., Susin S.A., Beutner G., Brdiczka D., Remy R., Xie Z.H., Reed J.C., and Kroemer G. The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J. Exp. Med. 187 (1998) 1261-1271
29. Woodfield K., Ruck A., Brdiczka D., and Halestrap A.P. Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem. J. 336 (1998) 287-290
30. Letai A. Pharmacological manipulation of Bcl-2 family members to control cell death. J. Clin. Invest. 115 (2005) 2648-2655
31. Willis S., and Adams J. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17 (2005) 617-625
32. Chen L., Willis S., Wei A., Smith B., Fletcher J., Hinds M., Colman P., Day C., Adams J., and Huang D. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell 17 (2005) 393-403
33. Decaudin D., Marzo I., Brenner C., and Kroemer G. Mitochondria in chemotherapy-induced apoptosis: a prospective novel target of cancer therapy. Int. J. Oncol. 12 (1998) 141-152
34. Debatin K.M., Poncet D., and Kroemer G. Chemotherapy: targeting the mitochondrial cell death pathway. Oncogene 21 (2002) 8786-8803
35. Bouchier-Hayes L., Lartigue L., and Newmeyer D.D. Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest. 115 (2005) 2640-2647
36. Ichas F., Jouaville L., and Mazat J. Mitochondria are excitable organelles capable of generating and conveying electrical and calcium signals. Cell 89 (1997) 1145-1153
37. Clement M.V., and Pervaiz S. Reactive oxygen intermediates regulate cellular response to apoptotic stimuli: an hypothesis. Free Radical Res. 30 (1999) 247-252
38. Marzo I., Susin S.A., Petit P.X., Ravagnan L., Brenner C., Larochette N., Zamzami N., and Kroemer G. Caspases disrupt mitochondrial membrane barrier function. FEBS Lett. 427 (1998) 198-202
39. Ricci J., Gottlieb R., and Green D. Caspase-mediated loss of mitochondrial function and generation of reactive oxygen species during apoptosis. J. Cell Biol. 160 (2003) 65-75
40. Green D.R., and Kroemer G. Pharmacological manipulation of cell death: clinical applications in sight?. J. Clin. Invest. 115 (2005) 2610-2617
41. Calamita G., Ferri D., Gena P., Liquori G.E., Cavalier A., Thomas D., and Svelto M. The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water. J. Biol. Chem. 280 (2005) 17149-17153
42. Tsujimoto Y., Finger L.R., Yunis J., Nowell P.C., and Croce C.M. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226 (1984) 1097-1099
43. Reed J.C., Jurgensmeier J.M., and Matsuyama S. Bcl-2 family proteins and mitochondria. Biochim. Biophys. Acta 1366 (1998) 127-137
44. Antonsson B., Montessuit S., Lauper S., Eskes R., and Martinou J.C. Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem. J. 345 (2000) 271-278
45. Shimizu S., Ide T., Yanagida T., and Tsujimoto Y. Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J. Biol. Chem. 275 (2000) 12321-12325
46. Marzo I., Brenner C., Zamzami N., Jurgensmeier J.M., Susin S.A., Vieira H.L., Prevost M.C., Xie Z., Matsuyama S., Reed J.C., and Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281 (1998) 2027-2031
47. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., and Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75 (1993) 241-251
48. Thomenius M.J., Wang N.S., Reineks E.Z., Wang Z., and Distelhorst C.W. Bcl-2 on the endoplasmic reticulum regulates Bax activity by binding to BH3-only proteins. J. Biol. Chem. 278 (2003) 6243-6250
49. Bassik M.C., Scorrano L., Oakes S.A., Pozzan T., and Korsmeyer S.J. Phosphorylation of BCL-2 regulates ER Ca2+ homeostasis and apoptosis. EMBO J. 23 (2004) 1207-1216
50. Chen R., Valencia I., Zhong F., McColl K.S., Roderick H.L., Bootman M.D., Berridge M.J., Conway S.J., Holmes A.B., Mignery G.A., Velez P., and Distelhorst C.W. Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J. Cell Biol. 166 (2004) 193-203
51. Zou H., Henzel W.J., Liu X., Lutschg A., and Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90 (1997) 405-413
52. Desagher S., Osen-Sand A., Nichols A., Eskes R., Montessuit S., Lauper S., Maundrell K., Antonsson B., and Martinou J.C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144 (1999) 891-901
53. Degterev A., Boyce M., and Yuan J. The channel of death. J. Cell Biol. 155 (2001) 695-698
54. Qian J., Voorbach M.J., Huth J.R., Coen M.L., Zhang H., Ng S.C., Comess K.M., Petros A.M., Rosenberg S.H., Warrior U., and Burns D.J. Discovery of novel inhibitors of Bcl-xL using multiple high-throughput screening platforms. Anal. Biochem. 328 (2004) 131-138
55. Reed J., Stein C., Subasinghe C., Haldar S., Croce C., Yum S., and Cohen J. Antisense-mediated inhibition of BCL2 protooncogene expression and leukemic cell growth and survival: comparisons of phosphodiester and phosphorothioate oligodeoxynucleotides. Cancer Res. 50 (1990) 6565-6570
56. Tzung S., Kim K., Basanez G., Giedt C., Simon J., Zimmerberg J., Zhang K., and Hockenbery D. Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3. Nat. Cell Biol. 3 (2001) 183-191
57. Zoratti M., and Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241 (1995) 139-176
58. Halestrap A.P., and Brenner C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10 (2003) 1507-1525
59. Zoratti M., and Szabo I. Electrophysiology of the inner mitochondrial membrane. J. Bioenerg. Biomembr. 26 (1994) 543-553
60. Lemasters J.J., Nieminen A.L., Qian T., Trost L.C., Elmore S.P., Nishimura Y., Crowe R.A., Cascio W.E., Bradham C.A., Brenner D.A., and Herman B. The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim. Biophys. Acta 1366 (1998) 177-196
61. Kroemer G., and Reed J.C. Mitochondrial control of cell death. Nat. Med. 6 (2000) 513-519
62. De Giorgi F., Lartigue L., Bauer M.K., Schubert A., Grimm S., Hanson G.T., Remington S.J., Youle R.J., and Ichas F. The permeability transition pore signals apoptosis by directing Bax translocation and multimerization. FASEB J. 16 (2002) 607-609
63. Belzacq A.S., Vieira H.L., Kroemer G., and Brenner C. The adenine nucleotide translocator in apoptosis. Biochimie 84 (2002) 167-176
64. Brenner C., Cadiou H., Vieira H.L., Zamzami N., Marzo I., Xie Z., Leber B., Andrews D., Duclohier H., Reed J.C., and Kroemer G. Bcl-2 and Bax regulate the channel activity of the mitochondrial adenine nucleotide translocator. Oncogene 19 (2000) 329-336
65. Scorrano L., Ashiya M., Buttle K., Weiler S., Oakes S.A., Mannella C.A., and Korsmeyer S.J. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell 2 (2002) 55-67
66. Crompton M., Barksby E., Johnson N., and Capano M. Mitochondrial intermembrane junctional complexes and their involvement in cell death. Biochimie 84 (2002) 143-152
67. Halestrap A.P., McStay G.P., and Clarke S.J. The permeability transition pore complex: another view. Biochimie 84 (2002) 153-166
68. C. Brenner, S. Grimm, The permeability transition proe complex and cell death, Oncogene (in press).
69. Ko Y.H., Delannoy M., Hullihen J., Chiu W., and Pedersen P.L. Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J. Biol. Chem. 278 (2003) 12305-12309
70. Faustin B., Rossignol R., Rocher C., Benard G., Malgat M., and Letellier T. Mitochondrial ATP synthasome. Cristae-enriched membranes and a multiwell detergent screening assay yield dispersed single complexes containing the ATP synthase and carriers for Pi and ADP/ATP. J. Biol. Chem. 279 (2004) 20411-20421
71. Beutner G., Ruck A., Riede B., Welte W., and Brdiczka D. Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett. 396 (1996) 189-195
72. Verrier F., Deniaud A., LeBras M., Metivier D., Kroemer G., Mignotte B., Jan G., and Brenner C. Dynamic evolution of the adenine nucleotide translocase interactome during chemotherapy-induced apoptosis. Oncogene 23 (2004) 8049-8064
73. Kokoszka J.E., Waymire K.G., Levy S.E., Sligh J.E., Cai J., Jones D.P., MacGregor G.R., and Wallace D.C. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427 (2004) 461-465
74. Halestrap A.P. Mitochondrial permeability: dual role for the ADP/ATP translocator?. Nature 430 (2004) 1-983
75. Nakagawa T., Shimizu S., Watanabe T., Yamaguchi O., Otsu K., Yamagata H., Inohara H., Kubo T., and Tsujimoto Y. Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434 (2005) 652-658
76. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., Brunskill E.W., Sayen M.R., Gottlieb R.A., Dorn G.W., Robbins J., and Molkentin J.D. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
77. Basso E., Fante L., Fowlkes J., Petronilli V., Forte M.A., and Bernardi P. Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. J. Biol. Chem. 280 (2005) 18558-18561
78. Capano M., and Crompton M. Biphasic translocation of Bax to mitochondria. Biochem. J. 367 (2002) 169-178
79. Cao G., Minami M., Pei W., Yan C., Chen D., O'Horo C., Graham S.H., and Chen J. Intracellular Bax translocation after transient cerebral ischemia: implications for a role of the mitochondrial apoptotic signaling pathway in ischemic neuronal death. J. Cereb. Blood Flow Metab. 21 (2001) 321-333
80. Cheng E., Sheiko T., Fisher J., Craigen W., and Korsmeyer S. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301 (2003) 513-517
81. Danial N., Gramm C., Scorrano L., Zhang C., Krauss S., Ranger A., Datta S., Greenberg M., Licklide R.L., Lowell B.B., Gygi S., and Korsmeyer S. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424 (2003) 952-956
82. Belzacq A., Vieira H., Verrier F., Vandecasteele G., Cohen I., Prevost M., Larquet E., Pariselli F., Petit P., Kahn A., Rizzuto R., Brenner C., and Kroemer G. Bcl-2 and Bax modulate adenine nucleotide translocase activity. Cancer Res. 63 (2003) 541-546
83. Machida K., Ohta Y., and Osada H. Suppression of apoptosis by cyclophilin D via stabilization of hexokinase II mitochondrial binding in cancer cells. J. Biol. Chem. 281 (2006) 14314-14320
84. Belzacq A.S., and Brenner C. The adenine nucleotide translocator: a new potential chemotherapeutic target. Curr. Drug Targets 4 (2003) 517-524
85. Brenner C., Marzo I., de Araujo Vieira H.L., and Kroemer G. Purification and liposomal reconstitution of permeability transition pore complex. Methods Enzymol. 322 (2000) 243-252
86. Belzacq A.S., Vieira H.L., Verrier F., Vandecasteele G., Cohen I., Prevost M.C., Larquet E., Pariselli F., Petit P.X., Kahn A., Rizzuto R., Brenner C., and Kroemer G. Bcl-2 and Bax modulate adenine nucleotide translocase activity. Cancer Res. 63 (2003) 541-546
87. Zamzami N., El Hamel C., Maisse C., Brenner C., Munoz-Pinedo C., Belzacq A.S., Costantini P., Vieira H., Loeffler M., Molle G., and Kroemer G. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 19 (2000) 6342-6350
88. Vieira H.L., Belzacq A.S., Haouzi D., Bernassola F., Cohen I., Jacotot E., Ferri K.F., El Hamel C., Bartle L.M., Melino G., Brenner C., Goldmacher V., and Kroemer G. The adenine nucleotide translocator: a target of nitric oxide, peroxynitrite, and 4-hydroxynonenal. Oncogene 20 (2001) 4305-4316
89. Costantini P., Belzacq A.S., Vieira H.L., Larochette N., de Pablo M.A., Zamzami N., Susin S.A., Brenner C., and Kroemer G. Oxidation of a critical thiol residue of the adenine nucleotide translocator enforces Bcl-2-independent permeability transition pore opening and apoptosis. Oncogene 19 (2000) 307-314
90. 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., and Kroemer G. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2. J. Exp. Med. 193 (2001) 509-519
91. 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., and Kroemer G. The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 191 (2000) 33-46
92. Goldmacher V.S., Bartle L.M., Skaletskaya A., Dionne C.A., Kedersha N.L., Vater C.A., Han J., Lutz R.J., Watanabe S., McFarland E.D., Kieff E.D., Mocarski E.S., and Chittenden T. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 12536-12541
93. Jan G., Belzacq A.S., Haouzi D., Rouault A., Metivier D., Kroemer G., and Brenner C. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ. 9 (2002) 179-188
94. Belzacq A.S., Jacotot E., Vieira H.L., Mistro D., Granville D.J., Xie Z., Reed J.C., Kroemer G., and Brenner C. Apoptosis induction by the photosensitizer verteporfin: identification of mitochondrial adenine nucleotide translocator as a critical target. Cancer Res. 61 (2001) 1260-1264
95. Belzacq A.S., El Hamel C., Vieira H.L., Cohen I., Haouzi D., Metivier D., Marchetti P., Brenner C., and Kroemer G. Adenine nucleotide translocator mediates the mitochondrial membrane permeabilization induced by lonidamine, arsenite and CD437. Oncogene 20 (2001) 7579-7587
96. Weaver J.G.R., Tarze A., Moffat T.C., Le Bras M., Deniaud A., Brenner C., Bren G.D., Phenix B., Miller B., Dong L., Jiang S.X., Moffat T., Sim V., Zurakowski B., Lallier J., Hardin H., Wettstein P., van Heeswijk R.P.G., Douen A., Kroemer R., Miller B., Hou S.T., Bennet S.A.L., Lynch D.H., Kroemer G., and Badley A.D. Inhibition of adenine nucleotide translocator pore function and protection against apoptosis in vivo by an HIV protease inhibitor. J. Clin. Invest. 115 (2005) 1828-1838
97. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trezeguet V., Lauquin G.J., and Brandolin G. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426 (2003) 39-44
98. Tsujimoto Y., and Shimizu S. Bcl-2 family: life-or-death switch. FEBS Lett. 466 (2000) 6-10
99. Wallace D. Mitochondrial diseases in man and mouse. Science 283 (1999) 1482-1488
100. Leist M., Single B., Castoldi A.F., Kuhnle S., and Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185 (1997) 1481-1486
101. Nishimura G., Proske R., Doyama H., and Higuchi M. Regulation of apoptosis by respiration: cytochrome c release by respiratory substrates. FEBS Lett. 505 (2001) 399-404
102. Krippner A., Matsuno-Yagi A., Gottlieb R.A., and Babior B.M. Loss of function of cytochrome c in Jurkat cells undergoing fas-mediated apoptosis. J. Biol. Chem. 271 (1996) 21629-21636
103. Schulzeosthoff K., Ferrari D., Los M., Wesselborg S., and Peter M.E. Apoptosis signaling by death receptors. Eur. J. Biochem. 254 (1998) 439-459
104. Fontaine E., Eriksson O., Ichas F., and Bernardi P. Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex I. J. Biol. Chem. 273 (1998) 12662-12668
105. Martinucci S., Szabo I., Tombola F., and Zoratti M. Ca2+-reversible inhibition of the mitochondrial megachannel by ubiquinone analogues. FEBS Lett. 480 (2000) 89-94
106. Walter L., Nogueira X., Heitz M., Bernardi P., and Fontaine E. Three classes of ubiquinone analogs regulate the mitochondrial permeability transition pore through a common site. J. Biol. Chem. 275 (2000) 29521-29527
107. Matter A. Tumor angiogenesis as a therapeutic target. Drug Discov. Today 6 (2001) 1005-1024
108. Ellerby H.M., Arap W., Ellerby L.M., Kain R., Andrusiak R., Rio G.D., Krajewski S., Lombardo C.R., Rao R., Ruoslahti E., Bredesen D.E., and Pasqualini R. Anti-cancer activity of targeted pro-apoptotic peptides. Nat. Med. 5 (1999) 1032-1038
109. Arap W., Haedicke W., Bernasconi M., Kain R., Rajotte D., Krajewski S., Ellerby H., Bredesen D., Pasqualini R., and Ruoslahti E. Targeting the prostate for destruction through a vascular address. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 1527-1531
110. Reed J. Bcl-2 family proteins. Oncogene 17 (1998) 3225-3236
111. Brewis N., Phelan A., Normand N., Choolun E., and O'Hare P. Particle assembly incorporating a VP22-BH3 fusion protein, facilitating intracellular delivery, regulated release, and apoptosis. Mol. Ther. 7 (2003) 262-270
112. Schimmer A., Hedley D., Chow S., Pham N., Chakrabartty A., Bouchard D., Mak T., Trus M., and Minden M. The BH3 domain of BAD fused to the Antennapedia peptide induces apoptosis via its alpha helical structure and independent of Bcl-2. Cell Death Differ. 8 (2001) 725-733
113. Vieira H.L., Boya P., Cohen I., El Hamel C., Haouzi D., Druillenec S., Belzacq A.S., Brenner C., Roques B., and Kroemer G. Cell permeable BH3-peptides overcome the cytoprotective effect of Bcl-2 and Bcl-X(L). Oncogene 21 (2002) 1963-1977
114. Cory S., and Adams J. Killing cancer cells by flipping the Bcl-2/Bax switch. Cancer Cell 8 (2005) 5-6
115. Walensky L., Kung A., Escher I., Malia T., Barbuto S., Wright R., Wagner G., Verdine G., and Korsmeyer S. Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science 305 (2004) 1466-1470
116. Oltersdorf T., Elmore S., Shoemaker A., Armstrong R., Augeri D., Belli B., Bruncko M., Deckwerth T.L., Dinges J., Hajduk P.J., Joseph M.K., Katida S., Korsmeyer S.J., Kunzer A.R., Letai A., Li C., Mitten M.J., Nettesheim D.G., Ng S., Nimmer P.M., O'Connor J.M., Oleksijew A., Petros A.M., Reed J.C., Shen W., Tahir S.K., Thompson C.B., Tomaselli K.J., Wang B., Wendt M.D., Zhang H., Fesik S.W., and Rosenberg S.H. An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435 (2005) 677-681
117. Shimizu S., Konishi A., Kodama T., and Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3100-3105
118. Klein D., Ribeiro M., Mendoza V., Jayaraman S., Kenyon N., Pileggi A., Molano R., Inverardi L., Ricordi C., and Pastori R. Delivery of Bcl-XL or its BH4 domain by protein transduction inhibits apoptosis in human islets. Biochem. Biophys. Res. Commun. 323 (2004) 473-478
119. Cantara S., Donnini S., Giachetti A., Thorpe P., and Ziche M. Exogenous BH4/Bcl-2 peptide reverts coronary endothelial cell apoptosis induced by oxidative stress. J. Vasc. Res. 41 (2004) 202-207
120. Ono M., Sawa Y., Ryugo M., Alechine A., Shimizu S., Sugioka R., Tsujimoto Y., and Matsuda H. BH4 peptide derivative from Bcl-xL attenuates ischemia/reperfusion injury thorough anti-apoptotic mechanism in rat hearts. Eur. J. Cardio-thorac. Surg. 27 (2005) 117-121
121. Deniaud A., Brenner C., and Kroemer G. Mitochondrial membrane permeabilization by HIV-1 Vpr. Mitochondrion 4 (2004) 223-233
122. 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., and Kroemer G. Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2. J. Exp. Med. 193 (2001) 509-520
123. Sabbah E., Druillennec S., Morellet N., Bouaziz S., Kroemer G., and Roques B. Interaction between the HIV-1 protein Vpr and the adenine nucleotide translocator. Chem. Biol. Drug Des. (2006) 145-154
124. Lecoeur H., Langonne A., Baux L., Rebouillat D., Rustin P., Prevost M.C., Brenner C., Edelman L., and Jacotot E. Real-time flow cytometry analysis of permeability transition in isolated mitochondria. Exp. Cell Res. 294 (2004) 106-117