Mitochondrial ROS and involvement of Bcl-2 as a mitochondrial ROS regulator

Mitochondrion

Volumn 19, Issue Part A, 2014, Pages 39-48

  Chong, Stephen Jun Fei ^a   Low, Ivan Cherh Chiet ^a   Pervaiz, Shazib ^a,b,c,d,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SINGAPORE MIT ALLIANCE   (Singapore)

^e National University Cancer Institute   (Singapore)

Author keywords

Bcl 2; Mitochondria; MitoROS; Phosphorylation; ROS; Superoxide

Indexed keywords

APRINOCARSEN; CISPLATIN; CYTOCHROME C OXIDASE; FLUOROURACIL; FOLINIC ACID; GLUTATHIONE; GOSSYPOL; PROTEIN BCL 2; PROTEIN KINASE C INHIBITOR; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); TEMOZOLOMIDE; UBIQUINOL CYTOCHROME C REDUCTASE; VINBLASTINE;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER THERAPY; CELL METABOLISM; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFICACY; ENZYME INHIBITION; HOMEOSTASIS; HUMAN; INHIBITION KINETICS; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PHASE 1 CLINICAL TRIAL (TOPIC); PROSTATE CARCINOMA; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; NEOPLASM; PHYSIOLOGY; PROTO ONCOGENE;

ANIMALS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, BCL-2; MITOCHONDRIA; NEOPLASMS; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES;

EID: 84911413325     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2014.06.002     Document Type: Article

References (173)

1. Anderson R.F., Hille R., Shinde S.S., Cecchini G. Electron transfer within complex II. Succinate:ubiquinone oxidoreductase of Escherichia coli. J. Biol. Chem. 2005, 280:33331-33337.
2. Armstrong J.S., Jones D.P. Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. FASEB J. 2002, 16:1263-1265.
3. Arsenijevic D., Onuma H., Pecqueur C., Raimbault S., Manning B.S., Miroux B., Couplan E., Alves-Guerra M.C., Goubern M., Surwit R., Bouillaud F., Richard D., Collins S., Ricquier D. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 2000, 26:435-439.
4. Asnaghi L., Calastretti A., Bevilacqua A., D'Agnano I., Gatti G., Canti G., Delia D., Capaccioli S., Nicolin A. Bcl-2 phosphorylation and apoptosis activated by damaged microtubules require mTOR and are regulated by Akt. Oncogene 2004, 23:5781-5791.
5. Bell E.L., Klimova T.A., Eisenbart J., Schumacker P.T., Chandel N.S. Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia. Mol. Cell. Biol. 2007, 27:5737-5745.
6. Berndtsson M., Hagg M., Panaretakis T., Havelka A.M., Shoshan M.C., Linder S. Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int. J. Cancer 2007, 120:175-180.
7. Boudny V., Nakano S. Src tyrosine kinase augments taxotere-induced apoptosis through enhanced expression and phosphorylation of Bcl-2. Br. J. Cancer 2002, 86:463-469.
8. Brand M.D. The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 2010, 45:466-472.
9. Brennan J.P., Bardswell S.C., Burgoyne J.R., Fuller W., Schroder E., Wait R., Begum S., Kentish J.C., Eaton P. Oxidant-induced activation of type I protein kinase A is mediated by RI subunit interprotein disulfide bond formation. J. Biol. Chem. 2006, 281:21827-21836.
10. Brichese L., Valette A. PP1 phosphatase is involved in Bcl-2 dephosphorylation after prolonged mitotic arrest induced by paclitaxel. Biochem. Biophys. Res. Commun. 2002, 294:504-508.
11. Bunn H.F., Poyton R.O. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 1996, 76:839-885.
12. Burgoyne J.R., Madhani M., Cuello F., Charles R.L., Brennan J.P., Schroder E., Browning D.D., Eaton P. Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science (New York, N.Y.) 2007, 317:1393-1397.
13. Burke P.V., Raitt D.C., Allen L.A., Kellogg E.A., Poyton R.O. Effects of oxygen concentration on the expression of cytochrome c and cytochrome c oxidase genes in yeast. J. Biol. Chem. 1997, 272:14705-14712.
14. Cadenas E., Boveris A., Ragan C.I., Stoppani A.O. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch. Biochem. Biophys. 1977, 180:248-257.
15. Cao D.X., Qiao B., Ge Z.Q., Yuan Y.J. Comparison of burst of reactive oxygen species and activation of caspase-3 in apoptosis of K562 and HL-60 cells induced by docetaxel. Cancer Lett. 2004, 214:103-113.
16. Casares C., Ramirez-Camacho R., Trinidad A., Roldan A., Jorge E., Garcia-Berrocal J.R. Reactive oxygen species in apoptosis induced by cisplatin: review of physiopathological mechanisms in animal models. Eur. Arch. Otorhinolaryngol. 2012, 269:2455-2459.
17. Cecchini G., Schroder I., Gunsalus R.P., Maklashina E. Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim. Biophys. Acta 2002, 1553:140-157.
18. Chakravarti A., Erkkinen M.G., Nestler U., Stupp R., Mehta M., Aldape K., Gilbert M.R., Black P.M., Loeffler J.S. Temozolomide-mediated radiation enhancement in glioblastoma: a report on underlying mechanisms. Clin. Cancer Res. 2006, 12:4738-4746.
19. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:11715-11720.
20. Chandel N.S., McClintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., Schumacker P.T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 2000, 275:25130-25138.
21. Chang T.S., Cho C.S., Park S., Yu S., Kang S.W., Rhee S.G. Peroxiredoxin III, a mitochondrion-specific peroxidase, regulates apoptotic signaling by mitochondria. J. Biol. Chem. 2004, 279:41975-41984.
22. Chen Z.X., Pervaiz S. Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ. 2007, 14:1617-1627.
23. Chen Z.X., Pervaiz S. BCL-2: pro- or anti-oxidant?. Front. Biosci. (Elite Ed.) 2009, 1:263-268.
24. Chen Z.X., Pervaiz S. Involvement of cytochrome c oxidase subunits Va and Vb in the regulation of cancer cell metabolism by Bcl-2. Cell Death Differ. 2010, 17:408-420.
25. Clement M.V., Hirpara J.L., Pervaiz S. Decrease in intracellular superoxide sensitizes Bcl-2-overexpressing tumor cells to receptor and drug-induced apoptosis independent of the mitochondria. Cell Death Differ. 2003, 10:1273-1285.
26. Cox A.G., Winterbourn C.C., Hampton M.B. Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochem. J. 2010, 425:313-325.
27. Cremers C.M., Jakob U. Oxidant sensing by reversible disulfide bond formation. J. Biol. Chem. 2013, 288:26489-26496.
28. Curtin J.F., Donovan M., Cotter T.G. Regulation and measurement of oxidative stress in apoptosis. J. Immunol. Methods 2002, 265:49-72.
29. Dagsgaard C., Taylor L.E., O'Brien K.M., Poyton R.O. Effects of anoxia and the mitochondrion on expression of aerobic nuclear COX genes in yeast: evidence for a signaling pathway from the mitochondrial genome to the nucleus. J. Biol. Chem. 2001, 276:7593-7601.
30. De Chiara G., Marcocci M.E., Torcia M., Lucibello M., Rosini P., Bonini P., Higashimoto Y., Damonte G., Armirotti A., Amodei S., Palamara A.T., Russo T., Garaci E., Cozzolino F. Bcl-2 Phosphorylation by p38 MAPK: identification of target sites and biologic consequences. J. Biol. Chem. 2006, 281:21353-21361.
31. Delpuech O., Griffiths B., East P., Essafi A., Lam E.W., Burgering B., Downward J., Schulze A. Induction of Mxi1-SR alpha by FOXO3a contributes to repression of Myc-dependent gene expression. Mol. Cell. Biol. 2007, 27:4917-4930.
32. Deng X., Ruvolo P., Carr B., May W.S. Survival function of ERK1/2 as IL-3-activated, staurosporine-resistant Bcl2 kinases. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1578-1583.
33. Deng X., Gao F., May W.S. Bcl2 retards G1/S cell cycle transition by regulating intracellular ROS. Blood 2003, 102:3179-3185.
34. Deng Y., Ren X., Yang L., Lin Y., Wu X. A JNK-dependent pathway is required for TNFalpha-induced apoptosis. Cell 2003, 115:61-70.
35. Deng X., Gao F., Flagg T., May W.S. Mono- and multisite phosphorylation enhances Bcl2's antiapoptotic function and inhibition of cell cycle entry functions. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:153-158.
36. Deng X., Gao F., May W.S. Protein phosphatase 2A inactivates Bcl2's antiapoptotic function by dephosphorylation and up-regulation of Bcl2-p53 binding. Blood 2009, 113:422-428.
37. Drose S., Brandt U. The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J. Biol. Chem. 2008, 283:21649-21654.
38. Ellerby L.M., Ellerby H.M., Park S.M., Holleran A.L., Murphy A.N., Fiskum G., Kane D.J., Testa M.P., Kayalar C., Bredesen D.E. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J. Neurochem. 1996, 67:1259-1267.
39. Emre Y., Hurtaud C., Nubel T., Criscuolo F., Ricquier D., Cassard-Doulcier A.M. Mitochondria contribute to LPS-induced MAPK activation via uncoupling protein UCP2 in macrophages. Biochem. J. 2007, 402:271-278.
40. Esposti M.D., Hatzinisiriou I., McLennan H., Ralph S. Bcl-2 and mitochondrial oxygen radicals. New approaches with reactive oxygen species-sensitive probes. J. Biol. Chem. 1999, 274:29831-29837.
41. Fan M., Goodwin M., Vu T., Brantley-Finley C., Gaarde W.A., Chambers T.C. Vinblastine-induced phosphorylation of Bcl-2 and Bcl-XL is mediated by JNK and occurs in parallel with inactivation of the Raf-1/MEK/ERK cascade. J. Biol. Chem. 2000, 275:29980-29985.
42. Ferber E.C., Peck B., Delpuech O., Bell G.P., East P., Schulze A. FOXO3a regulates reactive oxygen metabolism by inhibiting mitochondrial gene expression. Cell Death Differ. 2012, 19:968-979.
43. Finkel T. From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci. Signal. 2012, 5:pe10.
44. Fridovich I. Superoxide dismutases. Annu. Rev. Biochem. 1975, 44:147-159.
45. Friedman H.S., Kerby T., Calvert H. Temozolomide and treatment of malignant glioma. Clin. Cancer Res. 2000, 6:2585-2597.
46. Fujino G., Noguchi T., Matsuzawa A., Yamauchi S., Saitoh M., Takeda K., Ichijo H. Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell. Biol. 2007, 27:8152-8163.
47. Fujita N., Itoh T., Omori H., Fukuda M., Noda T., Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol. Biol. Cell 2008, 19:2092-2100.
48. Fukuda R., Zhang H., Kim J.W., Shimoda L., Dang C.V., Semenza G.L. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007, 129:111-122.
49. Gao P., Bauvy C., Souquere S., Tonelli G., Liu L., Zhu Y., Qiao Z., Bakula D., Proikas-Cezanne T., Pierron G., Codogno P., Chen Q., Mehrpour M. The Bcl-2 homology domain 3 mimetic gossypol induces both Beclin 1-dependent and Beclin 1-independent cytoprotective autophagy in cancer cells. J. Biol. Chem. 2010, 285:25570-25581.
50. Geiger T., Muller M., Dean N.M., Fabbro D. Antitumor activity of a PKC-alpha antisense oligonucleotide in combination with standard chemotherapeutic agents against various human tumors transplanted into nude mice. Anticancer Drug Des. 1998, 13:35-45.
51. Giorgi C., Agnoletto C., Baldini C., Bononi A., Bonora M., Marchi S., Missiroli S., Patergnani S., Poletti F., Rimessi A., Zavan B., Pinton P. Redox control of protein kinase C: cell- and disease-specific aspects. Antioxid. Redox Signal. 2010, 13:1051-1085.
52. Gleason C., Huang S., Thatcher L.F., Foley R.C., Anderson C.R., Carroll A.J., Millar A.H., Singh K.B. Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10768-10773.
53. Gordan J.D., Thompson C.B., Simon M.C. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007, 12:108-113.
54. Gotoh Y., Cooper J.A. Reactive oxygen species- and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-alpha signal transduction. J. Biol. Chem. 1998, 273:17477-17482.
55. Guo J., Lemire B.D. The ubiquinone-binding site of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase is a source of superoxide. J. Biol. Chem. 2003, 278:47629-47635.
56. Haldar S., Chintapalli J., Croce C.M. Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res. 1996, 56:1253-1255.
57. Halliwell B., Cross C.E. Oxygen-derived species: their relation to human disease and environmental stress. Environ. Health Perspect. 1994, 102(Suppl. 10):5-12.
58. Han D., Antunes F., Canali R., Rettori D., Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 2003, 278:5557-5563.
59. Hanada T., Noda N.N., Satomi Y., Ichimura Y., Fujioka Y., Takao T., Inagaki F., Ohsumi Y. The Atg12-Atg5 conjugate has a novel E3-like activity for protein lipidation in autophagy. J. Biol. Chem. 2007, 282:37298-37302.
60. Hirst J., Carroll J., Fearnley I.M., Shannon R.J., Walker J.E. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta 2003, 1604:135-150.
61. Hirst J., King M.S., Pryde K.R. The production of reactive oxygen species by complex I. Biochem. Soc. Trans. 2008, 36:976-980.
62. Hochman A., Sternin H., Gorodin S., Korsmeyer S., Ziv I., Melamed E., Offen D. Enhanced oxidative stress and altered antioxidants in brains of Bcl-2-deficient mice. J. Neurochem. 1998, 71:741-748.
63. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.
64. Hofmann F., Feil R., Kleppisch T., Schlossmann J. Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol. Rev. 2006, 86:1-23.
65. Horsefield R., Yankovskaya V., Sexton G., Whittingham W., Shiomi K., Omura S., Byrne B., Cecchini G., Iwata S. Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction. J. Biol. Chem. 2006, 281:7309-7316.
66. Huang L.H., Hu J.Q., Tao W.Q., Li Y.H., Li G.M., Xie P.Y., Liu X.S., Jiang J. Gossypol inhibits phosphorylation of Bcl-2 in human leukemia HL-60 cells. Eur. J. Pharmacol. 2010, 645:9-13.
67. Hwang I.T., Chung Y.M., Kim J.J., Chung J.S., Kim B.S., Kim H.J., Kim J.S., Yoo Y.D. Drug resistance to 5-FU linked to reactive oxygen species modulator 1. Biochem. Biophys. Res. Commun. 2007, 359:304-310.
68. Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science (New York, N.Y.) 1997, 275:90-94.
69. Imoto K., Kukidome D., Nishikawa T., Matsuhisa T., Sonoda K., Fujisawa K., Yano M., Motoshima H., Taguchi T., Tsuruzoe K., Matsumura T., Ichijo H., Araki E. Impact of mitochondrial reactive oxygen species and apoptosis signal-regulating kinase 1 on insulin signaling. Diabetes 2006, 55:1197-1204.
70. Ito T., Deng X., Carr B., May W.S. Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem. 1997, 272:11671-11673.
71. Itoh T., Terazawa R., Kojima K., Nakane K., Deguchi T., Ando M., Tsukamasa Y., Ito M., Nozawa Y. Cisplatin induces production of reactive oxygen species via NADPH oxidase activation in human prostate cancer cells. Free Radic. Res. 2011, 45:1033-1039.
72. Jiang Y., Sun Y., Yuan Y. Mechanism of temozolomide-induced anti-tumor effects on glioblastoma cells in vitro is via ROS-dependent SIRT1 signaling pathway. Zhonghua Zhong Liu Za Zhi 2012, 34:734-738.
73. Kagan V.E., Tyurin V.A., Jiang J., Tyurina Y.Y., Ritov V.B., Amoscato A.A., Osipov A.N., Belikova N.A., Kapralov A.A., Kini V., Vlasova I.I., Zhao Q., Zou M., Di P., Svistunenko D.A., Kurnikov I.V., Borisenko G.G. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat. Chem. Biol. 2005, 1:223-232.
74. Kamata H., Honda S., Maeda S., Chang L., Hirata H., Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005, 120:649-661.
75. Kane D.J., Sarafian T.A., Anton R., Hahn H., Gralla E.B., Valentine J.S., Ord T., Bredesen D.E. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science (New York, N.Y.) 1993, 262:1274-1277.
76. Kang Y.H., Lee S.J. The role of p38 MAPK and JNK in Arsenic trioxide-induced mitochondrial cell death in human cervical cancer cells. J. Cell. Physiol. 2008, 217:23-33.
77. Kim J.W., Tchernyshyov I., Semenza G.L., Dang C.V. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006, 3:177-185.
78. Kops G.J., Dansen T.B., Polderman P.E., Saarloos I., Wirtz K.W., Coffer P.J., Huang T.T., Bos J.L., Medema R.H., Burgering B.M. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002, 419:316-321.
79. Kowaltowski A.J., Fiskum G. Redox mechanisms of cytoprotection by Bcl-2. Antioxid. Redox Signal. 2005, 7:508-514.
80. Kowaltowski A.J., Cosso R.G., Campos C.B., Fiskum G. Effect of Bcl-2 overexpression on mitochondrial structure and function. J. Biol. Chem. 2002, 277:42802-42807.
81. Kushnareva Y., Murphy A.N., Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 2002, 368:545-553.
82. Kutuk O., Letai A. Regulation of Bcl-2 family proteins by posttranslational modifications. Curr. Mol. Med. 2008, 8:102-118.
83. Kwon J., Lee S.R., Yang K.S., Ahn Y., Kim Y.J., Stadtman E.R., Rhee S.G. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16419-16424.
84. Lai B., Zhang L., Dong L.Y., Zhu Y.H., Sun F.Y., Zheng P. Impact of inhibition of Qo site of mitochondrial complex III with myxothiazol on persistent sodium currents via superoxide and protein kinase C in rat hippocampal CA1 cells. Neurobiol. Dis. 2006, 21:206-216.
85. Lambert A.J., Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 2004, 279:39414-39420.
86. Lee S.R., Yang K.S., Kwon J., Lee C., Jeong W., Rhee S.G. Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 2002, 277:20336-20342.
87. Li Z., Zhang G., Feil R., Han J., Du X. Sequential activation of p38 and ERK pathways by cGMP-dependent protein kinase leading to activation of the platelet integrin alphaIIb beta3. Blood 2006, 107:965-972.
88. Li L., Chen Y., Gibson S.B. Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cell. Signal. 2013, 25:50-65.
89. Li X., Fang P., Mai J., Choi E.T., Wang H., Yang X.F. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 2013, 6:19.
90. Lin D., Takemoto D.J. Oxidative activation of protein kinase Cgamma through the C1 domain. Effects on gap junctions. J. Biol. Chem. 2005, 280:13682-13693.
91. Lin S.S., Bassik M.C., Suh H., Nishino M., Arroyo J.D., Hahn W.C., Korsmeyer S.J., Roberts T.M. PP2A regulates BCL-2 phosphorylation and proteasome-mediated degradation at the endoplasmic reticulum. J. Biol. Chem. 2006, 281:23003-23012.
92. Liu H., Lo C.R., Czaja M.J. NF-kappaB inhibition sensitizes hepatocytes to TNF-induced apoptosis through a sustained activation of JNK and c-Jun. Hepatology (Baltimore, Md.) 2002, 35:772-778.
93. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 2002, 80:780-787.
94. Liu Y., Yang Y., Ye Y.C., Shi Q.F., Chai K., Tashiro S., Onodera S., Ikejima T. Activation of ERK-p53 and ERK-mediated phosphorylation of Bcl-2 are involved in autophagic cell death induced by the c-Met inhibitor SU11274 in human lung cancer A549 cells. J. Pharmacol. Sci. 2012, 118:423-432.
95. Low I.C., Chen Z.X., Pervaiz S. Bcl-2 modulates resveratrol-induced ROS production by regulating mitochondrial respiration in tumor cells. Antioxid. Redox Signal. 2010, 13:807-819.
96. Low I.C., Kang J., Pervaiz S. Bcl-2: a prime regulator of mitochondrial redox metabolism in cancer cells. Antioxid. Redox Signal. 2011, 15:2975-2987.
97. Madesh M., Hajnoczky G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 2001, 155:1003-1015.
98. Mailloux R.J., Harper M.E. Uncoupling proteins and the control of mitochondrial reactive oxygen species production. Free Radic. Biol. Med. 2011, 51:1106-1115.
99. Mani S., Rudin C.M., Kunkel K., Holmlund J.T., Geary R.S., Kindler H.L., Dorr F.A., Ratain M.J. Phase I clinical and pharmacokinetic study of protein kinase C-alpha antisense oligonucleotide ISIS 3521 administered in combination with 5-fluorouracil and leucovorin in patients with advanced cancer. Clin. Cancer Res. 2002, 8:1042-1048.
100. Marklund S.L. Extracellular superoxide dismutase in human tissues and human cell lines. J. Clin. Invest. 1984, 74:1398-1403.
101. Marullo R., Werner E., Degtyareva N., Moore B., Altavilla G., Ramalingam S.S., Doetsch P.W. Cisplatin induces a mitochondrial-ROS response that contributes to cytotoxicity depending on mitochondrial redox status and bioenergetic functions. PLoS One 2013, 8:e81162.
102. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7:961-967.
103. May W.S., Tyler P.G., Ito T., Armstrong D.K., Qatsha K.A., Davidson N.E. Interleukin-3 and bryostatin-1 mediate hyperphosphorylation of BCL2 alpha in association with suppression of apoptosis. J. Biol. Chem. 1994, 269:26865-26870.
104. Mayer B., Oberbauer R. Mitochondrial regulation of apoptosis. News Physiol. Sci. 2003, 18:89-94.
105. Messner K.R., Imlay J.A. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J. Biol. Chem. 1999, 274:10119-10128.
106. Messner K.R., Imlay J.A. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J. Biol. Chem. 2002, 277:42563-42571.
107. Mirkovic N., Voehringer D.W., Story M.D., McConkey D.J., McDonnell T.J., Meyn R.E. Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 1997, 15:1461-1470.
108. Mizushima N. The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ. 2005, 12(Suppl. 2):1535-1541.
109. Mizushima N. Autophagy: process and function. Genes Dev. 2007, 21:2861-2873.
110. Moreno-Sanchez R., Hernandez-Esquivel L., Rivero-Segura N.A., Marin-Hernandez A., Neuzil J., Ralph S.J., Rodriguez-Enriquez S. Reactive oxygen species are generated by the respiratory complex II-evidence for lack of contribution of the reverse electron flow in complex I. FEBS J. 2013, 280:927-938.
111. Muller F., Crofts A.R., Kramer D.M. Multiple Q-cycle bypass reactions at the Qo site of the cytochrome bc1 complex. Biochemistry 2002, 41:7866-7874.
112. Muller F.L., Roberts A.G., Bowman M.K., Kramer D.M. Architecture of the Qo site of the cytochrome bc1 complex probed by superoxide production. Biochemistry 2003, 42:6493-6499.
113. Muller F.L., Liu Y., Van Remmen H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J. Biol. Chem. 2004, 279:49064-49073.
114. Muller F.L., Liu Y., Abdul-Ghani M.A., Lustgarten M.S., Bhattacharya A., Jang Y.C., Van Remmen H. High rates of superoxide production in skeletal-muscle mitochondria respiring on both complex I- and complex II-linked substrates. Biochem. J. 2008, 409:491-499.
115. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
116. Myers K.M., Fiskum G., Liu Y., Simmens S.J., Bredesen D.E., Murphy A.N. Bcl-2 protects neural cells from cyanide/aglycemia-induced lipid oxidation, mitochondrial injury, and loss of viability. J. Neurochem. 1995, 65:2432-2440.
117. Neuzil J., Weber T., Schroder A., Lu M., Ostermann G., Gellert N., Mayne G.C., Olejnicka B., Negre-Salvayre A., Sticha M., Coffey R.J., Weber C. Induction of cancer cell apoptosis by alpha-tocopheryl succinate: molecular pathways and structural requirements. FASEB J. 2001, 15:403-415.
118. Nijtmans L.G., Taanman J.W., Muijsers A.O., Speijer D., Van den Bogert C. Assembly of cytochrome-c oxidase in cultured human cells. Eur. J. Biochem. 1998, 254:389-394.
119. Ojala P.M., Yamamoto K., Castanos-Velez E., Biberfeld P., Korsmeyer S.J., Makela T.P. The apoptotic v-cyclin-CDK6 complex phosphorylates and inactivates Bcl-2. Nat. Cell Biol. 2000, 2:819-825.
120. Owusu-Ansah E., Banerjee U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature 2009, 461:537-541.
121. Paduch R., Kandefer-Szerszen M., Piersiak T. The importance of release of proinflammatory cytokines, ROS, and NO in different stages of colon carcinoma growth and metastasis after treatment with cytotoxic drugs. Oncol. Res. 2010, 18:419-436.
122. Paranagama M.P., Sakamoto K., Amino H., Awano M., Miyoshi H., Kita K. Contribution of the FAD and quinone binding sites to the production of reactive oxygen species from Ascaris suum mitochondrial complex II. Mitochondrion 2010, 10:158-165.
123. Pathan N., Aime-Sempe C., Kitada S., Basu A., Haldar S., Reed J.C. Microtubule-targeting drugs induce bcl-2 phosphorylation and association with Pin1. Neoplasia 2001, 3:550-559.
124. Pervaiz S., Clement M.V. Superoxide anion: oncogenic reactive oxygen species?. Int. J. Biochem. Cell Biol. 2007, 39:1297-1304.
125. Poyton R.O., Burke P.V. Oxygen regulated transcription of cytochrome c and cytochrome c oxidase genes in yeast. Biochim. Biophys. Acta 1992, 1101:252-256.
126. Pua H.H., Guo J., Komatsu M., He Y.W. Autophagy is essential for mitochondrial clearance in mature T lymphocytes. J. Immunol. 2009, 182:4046-4055.
127. Qi Y., Tian X., Liu J., Han Y., Graham A.M., Simon M.C., Penninger J.M., Carmeliet P., Li S. Bnip3 and AIF cooperate to induce apoptosis and cavitation during epithelial morphogenesis. J. Cell Biol. 2012, 198:103-114.
128. Quinlan C.L., Gerencser A.A., Treberg J.R., Brand M.D. The mechanism of superoxide production by the antimycin-inhibited mitochondrial Q-cycle. J. Biol. Chem. 2011, 286:31361-31372.
129. Quinlan C.L., Orr A.L., Perevoshchikova I.V., Treberg J.R., Ackrell B.A., Brand M.D. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J. Biol. Chem. 2012, 287:27255-27264.
130. Ralph S.J., Rodriguez-Enriquez S., Neuzil J., Saavedra E., Moreno-Sanchez R. The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation - why mitochondria are targets for cancer therapy. Mol. Asp. Med. 2010, 31:145-170.
131. Rao S., Watkins D., Cunningham D., Dunlop D., Johnson P., Selby P., Hancock B.W., Fegan C., Culligan D., Schey S., Morris T.C., Lissitchkov T., Oliver J.W., Holmlund J.T. Phase II study of ISIS 3521, an antisense oligodeoxynucleotide to protein kinase C alpha, in patients with previously treated low-grade non-Hodgkin's lymphoma. Ann. Oncol. 2004, 15:1413-1418.
132. Ray R.M., Bhattacharya S., Johnson L.R. Protein phosphatase 2A regulates apoptosis in intestinal epithelial cells. J. Biol. Chem. 2005, 280:31091-31100.
133. Ray P.D., Huang B.W., Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 2012, 24:981-990.
134. Reed J.C., Cuddy M., Slabiak T., Croce C.M., Nowell P.C. Oncogenic potential of bcl-2 demonstrated by gene transfer. Nature 1988, 336:259-261.
135. Ruvolo P.P., Deng X., Carr B.K., May W.S. A functional role for mitochondrial protein kinase Calpha in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 1998, 273:25436-25442.
136. Ruvolo P.P., Deng X., Ito T., Carr B.K., May W.S. Ceramide induces Bcl2 dephosphorylation via a mechanism involving mitochondrial PP2A. J. Biol. Chem. 1999, 274:20296-20300.
137. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998, 17:2596-2606.
138. Scherz-Shouval R., Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem. Sci. 2011, 36:30-38.
139. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007, 26:1749-1760.
140. Selimovic D., Badura H.E., El-Khattouti A., Soell M., Porzig B.B., Spernger A., Ghanjati F., Santourlidis S., Haikel Y., Hassan M. Vinblastine-induced apoptosis of melanoma cells is mediated by Ras homologous A protein (Rho A) via mitochondrial and non-mitochondrial-dependent mechanisms. Apoptosis 2013, 18:980-997.
141. Selivanov V.A., Votyakova T.V., Pivtoraiko V.N., Zeak J., Sukhomlin T., Trucco M., Roca J., Cascante M. Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain. PLoS Comput. Biol. 2011, 7:e1001115.
142. Sena L.A., Chandel N.S. Physiological roles of mitochondrial reactive oxygen species. Mol. Cell 2012, 48:158-167.
143. Seo J.H., Ahn Y., Lee S.R., Yeol Yeo C., Chung Hur K. The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol. Biol. Cell 2005, 16:348-357.
144. Starkov A.A., Fiskum G. Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 2003, 86:1101-1107.
145. Steinman H.M. The Bcl-2 oncoprotein functions as a pro-oxidant. J. Biol. Chem. 1995, 270:3487-3490.
146. St-Pierre J., Buckingham J.A., Roebuck S.J., Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 2002, 277:44784-44790.
147. Sun J., Trumpower B.L. Superoxide anion generation by the cytochrome bc1 complex. Arch. Biochem. Biophys. 2003, 419:198-206.
148. Tal M.C., Sasai M., Lee H.K., Yordy B., Shadel G.S., Iwasaki A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2770-2775.
149. Tello D., Balsa E., Acosta-Iborra B., Fuertes-Yebra E., Elorza A., Ordonez A., Corral-Escariz M., Soro I., Lopez-Bernardo E., Perales-Clemente E., Martinez-Ruiz A., Enriquez J.A., Aragones J., Cadenas S., Landazuri M.O. Induction of the mitochondrial NDUFA4L2 protein by HIF-1alpha decreases oxygen consumption by inhibiting complex I activity. Cell Metab. 2011, 14:768-779.
150. Thomas A., Giesler T., White E. p53 mediates bcl-2 phosphorylation and apoptosis via activation of the Cdc42/JNK1 pathway. Oncogene 2000, 19:5259-5269.
151. Tormos K.V., Anso E., Hamanaka R.B., Eisenbart J., Joseph J., Kalyanaraman B., Chandel N.S. Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab. 2011, 14:537-544.
152. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
153. Turrens J.F., Alexandre A., Lehninger A.L. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 1985, 237:408-414.
154. Uchida T., Rossignol F., Matthay M.A., Mounier R., Couette S., Clottes E., Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J. Biol. Chem. 2004, 279:14871-14878.
155. van Loo G., Saelens X., van Gurp M., MacFarlane M., Martin S.J., Vandenabeele P. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 2002, 9:1031-1042.
156. Veis D.J., Sorenson C.M., Shutter J.R., Korsmeyer S.J. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 1993, 75:229-240.
157. Velaithan R., Kang J., Hirpara J.L., Loh T., Goh B.C., Le Bras M., Brenner C., Clement M.V., Pervaiz S. The small GTPase Rac1 is a novel binding partner of Bcl-2 and stabilizes its antiapoptotic activity. Blood 2011, 117:6214-6226.
158. Voss V., Senft C., Lang V., Ronellenfitsch M.W., Steinbach J.P., Seifert V., Kogel D. The pan-Bcl-2 inhibitor (-)-gossypol triggers autophagic cell death in malignant glioma. Mol. Cancer Res. 2010, 8:1002-1016.
159. Wallace D.C. Mitochondria and cancer: Warburg addressed. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:363-374.
160. Wang J., Yi J. Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol. Ther. 2008, 7:1875-1884.
161. Wang S., Vrana J.A., Bartimole T.M., Freemerman A.J., Jarvis W.D., Kramer L.B., Krystal G., Dent P., Grant S. Agents that down-regulate or inhibit protein kinase C circumvent resistance to 1-beta-d-arabinofuranosylcytosine-induced apoptosis in human leukemia cells that overexpress Bcl-2. Mol. Pharmacol. 1997, 52:1000-1009.
162. Wei Y., Pattingre S., Sinha S., Bassik M., Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 2008, 30:678-688.
163. Williams S.L., Valnot I., Rustin P., Taanman J.W. Cytochrome c oxidase subassemblies in fibroblast cultures from patients carrying mutations in COX10, SCO1, or SURF1. J. Biol. Chem. 2004, 279:7462-7469.
164. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 2008, 45:549-561.
165. Yamamoto K., Ichijo H., Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 1999, 19:8469-8478.
166. Yankovskaya V., Horsefield R., Tornroth S., Luna-Chavez C., Miyoshi H., Leger C., Byrne B., Cecchini G., Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science (New York, N.Y.) 2003, 299:700-704.
167. Zamzami N., Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2001, 2:67-71.
168. Zelivianski S., Spellman M., Kellerman M., Kakitelashvilli V., Zhou X.W., Lugo E., Lee M.S., Taylor R., Davis T.L., Hauke R., Lin M.F. ERK inhibitor PD98059 enhances docetaxel-induced apoptosis of androgen-independent human prostate cancer cells. Int. J. Cancer 2003, 107:478-485.
169. Zhang L., Yu L., Yu C.A. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J. Biol. Chem. 1998, 273:33972-33976.
170. Zhang J., Frerman F.E., Kim J.J. Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16212-16217.
171. Zhang J., Khvorostov I., Hong J.S., Oktay Y., Vergnes L., Nuebel E., Wahjudi P.N., Setoguchi K., Wang G., Do A., Jung H.J., McCaffery J.M., Kurland I.J., Reue K., Lee W.N., Koehler C.M., Teitell M.A. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J. 2011, 30:4860-4873.
172. Zhong L.T., Sarafian T., Kane D.J., Charles A.C., Mah S.P., Edwards R.H., Bredesen D.E. bcl-2 inhibits death of central neural cells induced by multiple agents. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:4533-4537.
173. Zimmermann A.K., Loucks F.A., Schroeder E.K., Bouchard R.J., Tyler K.L., Linseman D.A. Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria. J. Biol. Chem. 2007, 282:29296-29304.