Regulation of mitochondrial metabolism: Yet another facet in the biology of the oncoprotein Bcl-2

Biochemical Journal

Volumn 435, Issue 3, 2011, Pages 545-551

  Krishna, Shefali ^a   Low, Ivan Cherh Chiet ^a,b   Pervaiz, Shazib ^a,b,c,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SINGAPORE MIT ALLIANCE   (Singapore)

Author keywords

Apoptosis; B cell lymphocytic leukaemia proto oncogene 2 (Bcl 2); Mitochondrion; Reactive oxygen species (ROS)

Indexed keywords

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; CISPLATIN; DAUNORUBICIN; ETOPOSIDE; FLAVOPIRIDOL; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; RESVERATROL;

APOPTOSIS; BIOLOGY; CANCER CHEMOTHERAPY; CARCINOGENESIS; CELL DEATH; HUMAN; LYMPHOMA; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW;

GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 79954459921     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101996     Document Type: Review

References (58)

1. Spierings, D., McStay, G., Saleh, M., Bender, C., Chipuk, J., Maurer, U. and Green, D. R. (2005) Connected to death: the (unexpurgated) mitochondrial pathway of apoptosis. Science 310, 66-67
2. Reed, J. C. (2008) Bcl-2-family proteins and hematologic malignancies: history and future prospects. Blood 111, 3322-3330
3. Tsujimoto, Y., Gorham, J., Cossman, J., Jaffe, E. and Croce, C. M. (1985) The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229, 1390-1393
4. Chen, Z. X. and Pervaiz, S. (2009) BCL-2: pro-or anti-oxidant? Front. Biosci. 1, 263-268
5. Vaux, D. L., Cory, S. and Adams, J. M. (1988) Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335, 440-442
6. McDonnell, T. J., Deane, N., Platt, F. M., Nunez, G., Jaeger, U., McKearn, J. P. and Korsmeyer, S. J. (1989) Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57, 79-88 (Pubitemid 19098870)
7. Chen, Z. X. and Pervaiz, S. (2007) Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ. 14, 1617-1627 (Pubitemid 47278847)
8. Andreyev, A. Y., Kushnareva, Y. E. and Starkov, A. A. (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry 70, 200-214
9. Hockenbery, D. M., Oltvai, Z. N., Yin, X. M., Milliman, C. L. and Korsmeyer, S. J. (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75, 241-251 (Pubitemid 23320288)
10. Chen, Z. X. and Pervaiz, S. (2010) Involvement of cytochrome c oxidase subunits Va and Vb in the regulation of cancer cell metabolism by Bcl-2. Cell Death Differ. 17, 408-420
11. Vaux, D. L. and Korsmeyer, S. J. (1999) Cell death in development. Cell 96, 245-254 (Pubitemid 29059354)
12. Savill, J., Fadok, V., Henson, P. and Haslett, C. (1993) Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14, 131-136 (Pubitemid 23068298)
13. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H. and Peter, M. E. (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17, 1675-1687
14. Reed, J. C. and Kroemer, G. (2000) Mechanisms of mitochondrial membrane permeabilization. Cell Death Differ. 7, 1145 (Pubitemid 32042220)
15. Chipuk, J. E., Bouchier-Hayes, L. and Green, D. R. (2006) Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13, 1396-1402
16. Chipuk, J. E., Moldoveanu, T., Llambi, F., Parsons, M. J. and Green, D. R. (2010) The BCL-2 family reunion. Mol. Cell 37, 299-310
17. Kvansakul, M., Yang, H., Fairlie, W. D., Czabotar, P. E., Fischer, S. F., Perugini, M. A., Huang, D. C. and Colman, P. M. (2008) Vaccinia virus anti-apoptotic F1L is a novel Bcl-2-like domain-swapped dimer that binds a highly selective subset of BH3-containing death ligands. Cell Death Differ. 15, 1564-1571
18. Adams, J. M. and Cory, S. (2007) The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26, 1324-1337 (Pubitemid 46328466)
19. Wei, M. C., Zong, W. X., Cheng, E. H., Lindsten, T., Panoutsakopoulou, V., Ross, A. J., Roth, K. A., MacGregor, G. R., Thompson, C. B. and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730 (Pubitemid 32385543)
20. Zhivotovsky, B., Galluzzi, L., Kepp, O. and Kroemer, G. (2009) Adenine nucleotide translocase: a component of the phylogenetically conserved cell death machinery. Cell Death Differ. 16, 1419-1425
21. Madesh, M., Zong, W. X., Hawkins, B. J., Ramasamy, S., Venkatachalam, T., Mukhopadhyay, P., Doonan, P. J., Irrinki, K. M., Rajesh, M., Pacher, P. and Thompson, C. B. (2009) Execution of superoxide-induced cell death by the proapoptotic Bcl-2-related proteins Bid and Bak. Mol. Cell. Biol. 29, 3099-3112
22. Letai, A., Bassik, M. C., Walensky, L. D., Sorcinelli, M. D., Weiler, S. and Korsmeyer, S. J. (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2, 183-192 (Pubitemid 41043974)
23. Kowaltowski, A. J. and Fiskum, G. (2005) Redox mechanisms of cytoprotection by Bcl-2. Antioxid. Redox Signaling 7, 508-514 (Pubitemid 40279819)
24. Clement, M. V., Hirpara, J. L. and Pervaiz, S. (2003) Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria. Cell Death Differ. 10, 1273-1285 (Pubitemid 37407129)
25. Low, I. C., Chen, Z. X. and Pervaiz, S. (2010) Bcl-2 modulates resveratrol-induced ROS production by regulating mitochondrial respiration in tumor cells. Antioxid. Redox Signaling 13, 807-819
26. Halliwell, B. and Gutteridge, J. M. C. (2007) Free Radicals in Biology and Medicine. Oxford University Press, Oxford
27. Burdon, R. H. (1995) Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radical Biol. Med. 18, 775-794
28. Clement, M. V. and Pervaiz, S. (2001) Intracellular superoxide and hydrogen peroxide concentrations: a critical balance that determines survival or death. Redox Rep. 6, 211-214
29. Irani, K. and Goldschmidt-Clermont, P. J. (1998) Ras, superoxide and signal transduction. Biochem. Pharmacol. 55, 1339-1346
30. Naughton, R., Quiney, C., Turner, S. D. and Cotter, T. G. (2009) Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia 23, 1432-1440
31. Bubici, C., Papa, S., Pham, C. G., Zazzeroni, F. and Franzoso, G. (2006) The NF-κB-mediated control of ROS and JNK signaling. Histol. Histopathol. 21, 69-80
32. Hirpara, J. L., Clement, M. V. and Pervaiz, S. (2001) Intracellular acidification triggered by mitochondrial-derived hydrogen peroxide is an effector mechanism for drug-induced apoptosis in tumor cells. J. Biol. Chem. 276, 514-521
33. Clement, M. V., Ponton, A. and Pervaiz, S. (1998) Apoptosis induced by hydrogen peroxide is mediated by decreased superoxide anion concentration and reduction of intracellular milieu. FEBS Lett. 440, 13-18 (Pubitemid 28558725)
34. Ahmad, K. A., Clement, M. V., Hanif, I. M. and Pervaiz, S. (2004) Resveratrol inhibits drug-induced apoptosis in human leukemia cells by creating an intracellular milieu nonpermissive for death execution. Cancer Res. 64, 1452-1459 (Pubitemid 38235616)
35. Pervaiz, S. and Clement, M. V. (2002) A permissive apoptotic environment: function of a decrease in intracellular superoxide anion and cytosolic acidification. Biochem. Biophys. Res. Commun. 290, 1145-1150
36. Roy, S., Bayly, C. I., Gareau, Y., Houtzager, V. M., Kargman, S., Keen, S. L., Rowland, K., Seiden, I. M., Thornberry, N. A. and Nicholson, D. W. (2001) Maintenance of caspase-3 proenzyme dormancy by an intrinsic 'safety catch' regulatory tripeptide. Proc. Natl. Acad. Sci. U.S.A. 98, 6132-6137
37. Grivennikova, V. G. and Vinogradov, A. D. (2006) Generation of superoxide by the mitochondrial Complex I. Biochim. Biophys. Acta 1757, 553-561
38. Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L. and Lesnefsky, E. J. (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278, 36027-36031
39. Dowhan, W., Bibus, C. R. and Schatz, G. (1985) The cytoplasmically-made subunit IV is necessary for assembly of cytochrome c oxidase in yeast. EMBO J. 4, 179-184
40. Nijtmans, L. G., Taanman, J. W., Muijsers, A. O., Speijer, D. and Van Den Bogert, C. (1998) Assembly of cytochrome-c oxidase in cultured human cells. Eur. J. Biochem. 254, 389-394
41. Wu, H., Rao, G. N., Dai, B. and Singh, P. (2000) Autocrine gastrins in colon cancer cells up-regulate cytochrome c oxidase Vb and down-regulate efflux of cytochrome c and activation of caspase-3. J. Biol. Chem. 275, 32491-32498
42. Reference deleted
43. Ahmad, K. A., Iskandar, K. B., Hirpara, J. L., Clement, M. V. and Pervaiz, S. (2004) Hydrogen peroxide-mediated cytosolic acidification is a signal for mitochondrial translocation of Bax during drug-induced apoptosis of tumor cells. Cancer Res. 64, 7867-7878 (Pubitemid 39446920)
44. Herrmann, P. C., Gillespie, J. W., Charboneau, L., Bichsel, V. E., Paweletz, C. P., Calvert, V. S., Kohn, E. C., Emmert-Buck, M. R., Liotta, L. A. and Petricoin, III, E. F. (2003) Mitochondrial proteome: altered cytochrome c oxidase subunit levels in prostate cancer. Proteomics 3, 1801-1810 (Pubitemid 37129826)
45. Campian, J. L., Gao, X., Qian, M. and Eaton, J. W. (2007) Cytochrome C oxidase activity and oxygen tolerance. J. Biol. Chem. 282, 12430-12438
46. Bensaad, K. and Vousden, K. H. (2007) p53: new roles in metabolism. Trends Cell Biol. 17, 286-291
47. Matoba, S., Kang, J. G., Patino, W. D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P. J., Bunz, F. and Hwang, P. M. (2006) p53 regulates mitochondrial respiration. Science 312, 1650-1653
48. Warburg, O. (1956) On respiratory impairment in cancer cells. Science 124, 269-270
49. Zu, X. L. and Guppy, M. (2004) Cancer metabolism: facts, fantasy, and fiction. Biochem. Biophys. Res. Commun. 313, 459-465
50. Elwood, J. C., Lin, Y. C., Cristofalo, V. J., Weinhouse, S. and Morris, H. P. (1963) Glucose utilization in homogenates of the morris hepatoma 5123 and related tumors. Cancer Res. 23, 906-913
51. Rodriguez-Enriquez, S., Vital-Gonzalez, P. A., Flores-Rodriguez, F. L., Marin-Hernandez, A., Ruiz-Azuara, L. and Moreno-Sanchez, R. (2006) Control of cellular proliferation by modulation of oxidative phosphorylation in human and rodent fast-growing tumor cells. Toxicol. Appl. Pharmacol. 215, 208-217
52. Fang, J., Nakamura, H. and Iyer, A. K. (2007) Tumor-targeted induction of oxystress for cancer therapy. J. Drug Target. 15, 475-486
53. Shenoy, K., Wu, Y. and Pervaiz, S. (2009) LY303511 enhances TRAIL sensitivity of SHEP-1 neuroblastoma cells via hydrogen peroxide-mediated mitogen-activated protein kinase activation and up-regulation of death receptors. Cancer Res. 69, 1941-1950
54. Jansen, B., Schlagbauer-Wadl, H., Brown, B. D., Bryan, R. N., van Elsas, A., Muller, M., Wolff, K., Eichler, H. G. and Pehamberger, H. (1998) Bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat. Med. 4, 232-234
55. Howard, A. N., Bridges, K. A., Meyn, R. E. and Chandra, J. (2009) ABT-737, a BH3 mimetic, induces glutathione depletion and oxidative stress. Cancer Chemother. Pharmacol. 65, 41-54
56. Wang, J. L., Liu, D., Zhang, Z. J., Shan, S., Han, X., Srinivasula, S. M., Croce, C. M., Alnemri, E. S. and Huang, Z. (2000) Structure-based discovery of an organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc. Natl. Acad. Sci. U.S.A. 97, 7124-7129
57. Pei, X. Y., Dai, Y. and Grant, S. (2004) The small-molecule Bcl-2 inhibitor HA14-1 interacts synergistically with flavopiridol to induce mitochondrial injury and apoptosis in human myeloma cells through a free radical-dependent and Jun NH2-terminal kinase-dependent mechanism. Mol. Cancer Ther. 3, 1513-1524
58. Decker, R. H., Dai, Y. and Grant, S. (2001) The cyclin-dependent kinase inhibitor flavopiridol induces apoptosis in human leukemia cells (U937) through the mitochondrial rather than the receptor-mediated pathway. Cell Death Differ. 8, 715-724