Bax is necessary for PGC1α pro-apoptotic effect in colorectal cancer cells

Cell Cycle

Volumn 10, Issue 17, 2011, Pages 2937-2945

  D'Errico, Ilenia ^a   Lo Sasso, Giuseppe ^a   Salvatore, Lorena ^a   Murzilli, Stefania ^a   Martelli, Nicola ^a   Cristofaro, Maricarmen ^a   Latorre, Dominga ^b   Villani, Gaetano ^b   Moschetta, Antonio ^a,b  

^a Laboratorio Angela Valenti dei Fattori Genetici e Ambientali di Rischio Trombotico   (Italy)

^b UNIVERSITY OF BARI   (Italy)

Author keywords

Apoptosis; Intestine; Mitochondria; Nuclear receptors; Reactive oxygen species (ROS)

Indexed keywords

MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN BAX; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL DEATH; COLORECTAL CANCER; HUMAN; HUMAN CELL; MITOCHONDRION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR GROWTH; XENOGRAFT;

EID: 80052400864     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.17.16791     Document Type: Article

References (55)

1. Kelly D.P., Scarpulla RC. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 2004; 18:357-68; PMID:15004004; DOI:10.1101/gad.1177604.
2. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999; 98:115-24; PMID:10412986; DOI:10.1016/S0092- 8674(00)80611-X.
3. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998; 92:829-39; PMID:9529258; DOI:10.1016/ S0092-8674(00)81410-5.
4. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., et al. Transcriptional co-activator PGC-1alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418:797-801; PMID:12181572; DOI:10.1038/ nature00904.
5. Puigserver P., Spiegelman BM. Peroxisome proliferatoractivated receptor-gamma coactivator 1alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003; 24:78-90; PMID:12588810; DOI:10.1210/er.2002-0012.
6. D'Errico I., Salvatore L., Murzilli S., Lo Sasso G., Latorre D., Martelli N., et al. Peroxisome proliferator-activated receptor-{gamma} coactivator 1-{alpha} (PGC1{alpha}) is a metabolic regulator of intestinal epithelial cell fate. Proc Natl Acad Sci USA 2011; 108:6603-8; PMID:21467224; DOI:10.1073/pnas.1016354108.
7. St. Pierre J., Lin J., Krauss S., Tarr P.T., Yang R., Newgard C.B., et al. Bioenergetic analysis of peroxisome proliferator- activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells. J Biol Chem 2003; 278:26597-603; PMID:12734177; DOI:10.1074/jbc.M301850200.
8. Valle I., Alvarez-Barrientos A., Arza E., Lamas S., Monsalve M. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc Res 2005; 66:562-73; PMID:15914121; DOI:10.1016/j.cardiores.2005.01.026.
9. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127:469-80; PMID:17081971; DOI:10.1016/j.cell.2006.10.018.
10. Pitari G.M., Li P., Lin J.E., Zuzga D., Gibbons A.V., Snook A.E., et al. The paracrine hormone hypothesis of colorectal cancer. Clin Pharmacol Ther 2007; 82:441- 7; PMID:17687268; DOI:10.1038/sj.clpt.6100325.
11. Turan A., Mahmood A. The profile of antioxidant systems and lipid peroxidation across the crypt-villus axis in rat intestine. Dig Dis Sci 2007; 52:1840-4; PMID:17393332; DOI:10.1007/s10620-006-9633-z.
12. Morin P.J., Vogelstein B., Kinzler KW. Apoptosis and APC in colorectal tumorigenesis. Proc Natl Acad Sci USA 1996; 93:7950-4; PMID:8755583; DOI:10.1073/pnas.93.15.7950.
13. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15:2922-2933; PMID:11711427.
14. Wolf B.B., Green DR. Apoptosis: letting slip the dogs of war. Curr Biol 2002; 12:177-9; PMID:11882308; DOI:10.1016/S0960-9822(02)00736-4.
15. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996; 86:147-57; PMID:8689682; DOI:10.1016/S0092- 8674(00)80085-9.
16. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997; 275:1132-6; PMID:9027315; DOI:10.1126/ science.275.5303.1132.
17. Lindsten T., Thompson CB. Cell death in the absence of Bax and Bak. Cell Death Differ 2006; 13:1272-6; PMID:16676001; DOI:10.1038/sj.cdd.4401953.
18. Tsujimoto Y. Cell death regulation by the Bcl-2 protein family in the mitochondria. J Cell Physiol 2003; 195:158-67; PMID:12652643; DOI:10.1002/ jcp.10254.
19. Zong W.X., Lindsten T., Ross A.J., MacGregor G.R., Thompson CB. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 2001; 15:1481- 6; PMID:11410528; DOI:10.1101/gad.897601.
20. Ruiz-Vela A., Opferman J.T., Cheng E.H., Korsmeyer SJ. Proapoptotic BAX and BAK control multiple initiator caspases. EMBO Rep 2005; 6:379-85; PMID:15776018; DOI:10.1038/sj.embor.7400375.
21. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292:727-30; PMID:11326099; DOI:10.1126/science.1059108.
22. Cheng E.H., Wei M.C., Weiler S., Flavell R.A., Mak T.W., Lindsten T., et al. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAKmediated mitochondrial apoptosis. Mol Cell 2001; 8:705-11; PMID:11583631; DOI:10.1016/S1097- 2765(01)00320-3.
23. Chandrika B.B., Maney S.K., Lekshmi S.U., Joseph J., Seervi M, KSP, et al. Bax deficiency mediated drug resistance can be reversed by endoplasmic reticulum stress induced death signaling. Biochem Pharmacol 2010; 79:1589-99; PMID:20138027; DOI:10.1016/j. bcp.2010.01.032.
24. Kirkland R.A., Windelborn J.A., Kasprzak J.M., Franklin JL. A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death. J Neurosci 2002; 22:6480-6490; PMID:12151527.
25. Peyerl F.W., Dai S., Murphy G.A., Crawford F., White J., Marrack P., et al. Elucidation of some Bax conformational changes through crystallization of an antibodypeptide complex. Cell Death Differ 2007; 14:447-52; PMID:16946732; DOI:10.1038/sj.cdd.4402025.
26. Boohaker R.J., Zhang G., Carlson A.L., Nemec K.N., Khaled AR. Bax supports the mitochondrial network, promoting bioenergetics in non-apoptotic cells. Am J Physiol Cell Physiol 2011; 300:1466-78; PMID:21289292; DOI:10.1152/ajpcell.00325.2010.
27. D'Alessio M., De Nicola M., Coppola S., Gualandi G., Pugliese L., Cerella C., et al. Oxidative Bax dimerization promotes its translocation to mitochondria independently of apoptosis. FASEB J 2005; 19:1504-1506; PMID:15972297.
28. Nie C., Tian C., Zhao L., Petit P.X., Mehrpour M., Chen Q. Cysteine 62 of Bax is critical for its conformational activation and its proapoptotic activity in response to H2O2-induced apoptosis. J Biol Chem 2008; 283:15359-69; PMID:18344566; DOI:10.1074/jbc. M800847200.
29. Zhang L., Yu J., Park B.H., Kinzler K.W., Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 2000; 290:989-92; PMID:11062132; DOI:10.1126/science.290.5493.989.
30. Von Ahsen O., Waterhouse N.J., Kuwana T., Newmeyer D.D., Green DR. The 'harmless' release of cytochrome c. Cell Death Differ 2000; 7:1192-9; PMID:11175256; DOI:10.1038/sj.cdd.4400782.
31. Vigneron A., Vousden K.H. p53, ROS and senescence in the control of aging. Aging (Albany NY) 2010; 2:471-474; PMID:20729567.
32. Huang Y., Ratovitski E.A. Phospho-DeltaNp63alpha/ Rpn13-dependent regulation of LKB1 degradation modulates autophagy in cancer cells. Aging (Albany NY) 2010; 2:959-968; PMID:21191146.
33. Feilchenfeldt J., Brundler M.A., Soravia C., Totsch M., Meier CA. Peroxisome proliferator-activated receptors (PPARs) and associated transcription factors in colon cancer: reduced expression of PPARgammacoactivator 1 (PGC-1). Cancer Lett 2004; 203:25-33; PMID:14670614; DOI:10.1016/j.canlet.2003.08.024.
34. Jiang W.G., Douglas-Jones A., Mansel RE. Expression of peroxisome-proliferator activated receptor-gamma (PPARgamma) and the PPARgamma co-activator, PGC-1, in human breast cancer correlates with clinical outcomes. Int J Cancer 2003; 106:752-7; PMID:12866036; DOI:10.1002/ijc.11302.
35. Watkins G., Douglas-Jones A., Mansel R.E., Jiang W.G. The localisation and reduction of nuclear staining of PPARgamma and PGC-1 in human breast cancer. Oncol Rep 2004; 12:483-488; PMID:15254719.
36. Jeong A.Y., Lee M.Y., Lee S.H., Park J.H., Han HJ. PPARdelta agonist-mediated ROS stimulates mouse embryonic stem cell proliferation through cooperation of p38 MAPK and Wnt/beta-catenin. Cell Cycle 2009; 8:611-9; PMID:19197156; DOI:10.4161/ cc.8.4.7752.
37. Lefebvre A.M., Chen I., Desreumaux P., Najib J., Fruchart J.C., Geboes K., et al. Activation of the peroxisome proliferator-activated receptor gamma promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat Med 1998; 4:1053-7; PMID:9734399; DOI:10.1038/2036.
38. Saez E., Tontonoz P., Nelson M.C., Alvarez J.G., Ming U.T., Baird S.M., et al. Activators of the nuclear receptor PPARgamma enhance colon polyp formation. Nat Med 1998; 4:1058-61; PMID:9734400; DOI:10.1038/2042.
39. Park B.H., Breyer B., He TC. Peroxisome proliferatoractivated receptors: roles in tumorigenesis and chemoprevention in human cancer. Curr Opin Oncol 2001; 13:78-83; PMID:11148691; DOI:10.1097/00001622- 200101000-00015.
40. Rumi M.A., Ishihara S., Kazumori H., Kadowaki Y., Kinoshita Y. Can PPARgamma ligands be used in cancer therapy? Curr Med Chem Anticancer Agents 2004; 4:465-77; PMID:15579013; DOI:10.2174/1568011043352678.
41. Koeffler H.P. Peroxisome proliferator-activated receptor gamma and cancers. Clin Cancer Res 2003; 9:1-9; PMID:12538445.
42. Zhang Y., Ba Y., Liu C., Sun G., Ding L., Gao S., et al. PGC-1alpha induces apoptosis in human epithelial ovarian cancer cells through a PPARgamma-dependent pathway. Cell Res 2007; 17:363-73; PMID:17372612; DOI:10.1038/cr.2007.11.
43. Priault M., Bessoule J.J., Grelaud-Coq A., Camougrand N., Manon S. Bax-induced cell death in yeast depends on mitochondrial lipid oxidation. Eur J Biochem 2002; 269:5440-50; PMID:12423342; DOI:10.1046/ j.1432-033.2002.03234.x.
44. Trédan O., Galmarini C.M., Patel K., Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007; 99:1441-54; PMID:17895480; DOI:10.1093/jnci/djm135.
45. Vaupel P., Thews O., Hoeckel M. Treatment resistance of solid tumors: role of hypoxia and anemia. Med Oncol 2001; 18:243-59; PMID:11918451; DOI:10.1385/ MO:18:4:243.
46. LeBlanc H., Lawrence D., Varfolomeev E., Totpal K., Morlan J., Schow P., et al. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002; 8:274-81; PMID:11875499; DOI:10.1038/nm0302-274.
47. Jansson A., Sun XF. Bax expression decreases significantly from primary tumor to metastasis in colorectal cancer. J Clin Oncol 2002; 20:811-6; PMID:11821465; DOI:10.1200/JCO.20.3.811.
48. Duckworth C.A., Pritchard DM. Suppression of apoptosis, crypt hyperplasia and altered differentiation in the colonic epithelia of bak-null mice. Gastroenterology 2009; 136:943-52; PMID:19185578; DOI:10.1053/j. gastro.2008.11.036.
49. Kim B.J., Ryu S.W., Song BJ. JNK- and p38 kinasemediated phosphorylation of Bax leads to its activation and mitochondrial translocation and to apoptosis of human hepatoma HepG2 cells. J Biol Chem 2006; 281:21256-65; PMID:16709574; DOI:10.1074/jbc. M510644200.
50. Hsieh C.C., Kuro-o M., Rosenblatt K.P., Brobey R., Papaconstantinou J. The ASK1-Signalosome regulates p38 MAPK activity in response to levels of endogenous oxidative stress in the Klotho mouse models of aging. Aging (Albany NY) 2010; 2:597-611; PMID:20844314.
51. Huang F., Nie C., Yang Y., Yue W., Ren Y., Shang Y., et al. Selenite induces redox-dependent Bax activation and apoptosis in colorectal cancer cells. Free Radic Biol Med 2009; 46:1186-96; PMID:19439215; DOI:10.1016/j. freeradbiomed.2009.01.026.
52. Chan S.L., Yu VC. Proteins of the bcl-2 family in apoptosis signalling: from mechanistic insights to therapeutic opportunities. Clin Exp Pharmacol Physiol 2004; 31:119-28; PMID:15008953; DOI:10.1111/j.1440- 681.2004.03975.x.
53. Lindsten T., Ross A.J., King A., Zong W.X., Rathmell J.C., Shiels H.A., et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 2000; 6:1389-99; PMID:11163212; DOI:10.1016/ S1097-2765(00)00136-2.
54. Zong W.X., Ditsworth D., Bauer D.E., Wang Z.Q., Thompson CB. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 2004; 18:1272-82; PMID:15145826; DOI:10.1101/ gad.1199904.
55. Shimizu S., Kanaseki T., Mizushima N., Mizuta T., Arakawa-Kobayashi S., Thompson C.B., et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 2004; 6:1221-8; PMID:15558033; DOI:10.1038/ ncb1192.