Glutathionylation of UCP2 sensitizes drug resistant leukemia cells to chemotherapeutics

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 1, 2013, Pages 80-89

  Pfefferle, Aline ^a   Mailloux, Ryan J ^a   Adjeitey, Cyril Nii Klu ^a   Harper, Mary Ellen ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Chemotherapy; Drug resistance; Glutathionylation; Mitochondria; Proton leak; Uncoupling protein 2

Indexed keywords

ANTINEOPLASTIC AGENT; DIAMIDE; DOXORUBICIN; MENADIONE; PROTON; UNCOUPLING PROTEIN 2;

ARTICLE; BREATHING; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG EXPOSURE; DRUG INHIBITION; DRUG SENSITIVITY; GLUTATHIONYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMIA CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MODIFICATION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL SURVIVAL; DIAMIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GLUTATHIONE; HL-60 CELLS; HUMANS; ION CHANNELS; LEUKEMIA; MITOCHONDRIAL PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTON PUMPS; TUMOR CELLS, CULTURED;

EID: 84868590991     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.006     Document Type: Article

References (54)

1. Wallace D.C. Colloquium paper: bioenergetics, the origins of complexity, and the ascent of man. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(Suppl. 2):8947-8953.
2. Mailloux R.J., Harper M.E. Mitochondrial proticity and ROS signaling: lessons from the uncoupling proteins. Trends Endocrinol. Metab. 2012, 23:451-458.
3. Divakaruni A.S., Brand M.D. The regulation and physiology of mitochondrial proton leak. Physiology (Bethesda) 2011, 26:192-205.
4. Trenker M., Malli R., Fertschai I., Levak-Frank S., Graier W.F. Uncoupling proteins 2 and 3 are fundamental for mitochondrial Ca2+ uniport. Nat. Cell Biol. 2007, 9:445-452.
5. Lombardi A., Busiello R.A., Napolitano L., Cioffi F., Moreno M., de Lange P., Silvestri E., Lanni A., Goglia F. UCP3 translocates lipid hydroperoxide and mediates lipid hydroperoxide-dependent mitochondrial uncoupling. J. Biol. Chem. 2010, 285:16599-16605.
6. Negre-Salvayre A., Hirtz C., Carrera G., Cazenave R., Troly M., Salvayre R., Penicaud L., Casteilla L. A role for uncoupling protein-2 as a regulator of mitochondrial hydrogen peroxide generation. FASEB J. 1997, 11:809-815.
7. Giardina T.M., Steer J.H., Lo S.Z., Joyce D.A. Uncoupling protein-2 accumulates rapidly in the inner mitochondrial membrane during mitochondrial reactive oxygen stress in macrophages. Biochim. Biophys. Acta 2008, 1777:118-129.
8. Krauss S., Zhang C.Y., Scorrano L., Dalgaard L.T., St-Pierre J., Grey S.T., Lowell B.B. Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction. J. Clin. Investig. 2003, 112:1831-1842.
9. Feldmann H.M., Golozoubova V., Cannon B., Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009, 9:203-209.
10. 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.
11. Korshunov S.S., Skulachev V.P., Starkov A.A. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 1997, 416:15-18.
12. Pouvreau S. Superoxide flashes in mouse skeletal muscle are produced by discrete arrays of active mitochondria operating coherently. PLoS One 2010, 5.
13. Brand M.D., Esteves T.C. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab. 2005, 2:85-93.
14. Pi J., Collins S. Reactive oxygen species and uncoupling protein 2 in pancreatic beta-cell function. Diabetes Obes. Metab. 2010, 12(Suppl. 2):141-148.
15. Andrews Z.B., Liu Z.W., Walllingford N., Erion D.M., Borok E., Friedman J.M., Tschop M.H., Shanabrough M., Cline G., Shulman G.I., Coppola A., Gao X.B., Horvath T.L., Diano S. UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals. Nature 2008, 454:846-851.
16. 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.
17. Diano S., Horvath T.L. Mitochondrial uncoupling protein 2 (UCP2) in glucose and lipid metabolism. Trends Mol. Med. 2012, 18:52-58.
18. Affourtit C., Jastroch M., Brand M.D. Uncoupling protein-2 attenuates glucose-stimulated insulin secretion in INS-1E insulinoma cells by lowering mitochondrial reactive oxygen species. Free Radic. Biol. Med. 2011, 50:609-616.
19. Mailloux R.J., Seifert E.L., Bouillaud F., Aguer C., Collins S., Harper M.E. Glutathionylation acts as a control switch for uncoupling proteins UCP2 and UCP3. J. Biol. Chem. 2011, 286:21865-21875.
20. Gallogly M.M., Mieyal J.J. Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr. Opin. Pharmacol. 2007, 7:381-391.
21. Santandreu F.M., Roca P., Oliver J. Uncoupling protein-2 knockdown mediates the cytotoxic effects of cisplatin. Free Radic. Biol. Med. 2010, 49:658-666.
22. Horimoto M., Fulop P., Derdak Z., Wands J.R., Baffy G. Uncoupling protein-2 deficiency promotes oxidant stress and delays liver regeneration in mice. Hepatology 2004, 39:386-392.
23. Derdak Z., Mark N.M., Beldi G., Robson S.C., Wands J.R., Baffy G. The mitochondrial uncoupling protein-2 promotes chemoresistance in cancer cells. Cancer Res. 2008, 68:2813-2819.
24. Baffy G., Derdak Z., Robson S.C. Mitochondrial recoupling: a novel therapeutic strategy for cancer?. Br. J. Cancer 2011, 105:469-474.
25. Harper M.E., Antoniou A., Villalobos-Menuey E., Russo A., Trauger R., Vendemelio M., George A., Bartholomew R., Carlo D., Shaikh A., Kupperman J., Newell E.W., Bespalov I.A., Wallace S.S., Liu Y., Rogers J.R., Gibbs G.L., Leahy J.L., Camley R.E., Melamede R., Newell M.K. Characterization of a novel metabolic strategy used by drug-resistant tumor cells. FASEB J. 2002, 16:1550-1557.
26. Mailloux R.J., Adjeitey C.N., Harper M.E. Genipin-induced inhibition of uncoupling protein-2 sensitizes drug-resistant cancer cells to cytotoxic agents. PLoS One 2010, 5:e13289.
27. Rial E., Rodriguez-Sanchez L., Aller P., Guisado A., Mar Gonzalez-Barroso M., Gallardo-Vara E., Redondo-Horcajo M., Castellanos E., Fernandez de la Pradilla R., Viso A. Development of chromanes as novel inhibitors of the uncoupling proteins. Chem. Biol. 2011, 18:264-274.
28. Ayyasamy V., Owens K.M., Desouki M.M., Liang P., Bakin A., Thangaraj K., Buchsbaum D.J., LoBuglio A.F., Singh K.K. Cellular model of Warburg effect identifies tumor promoting function of UCP2 in breast cancer and its suppression by genipin. PLoS One 2011, 6:e24792.
29. Samudio I., Fiegl M., Andreeff M. Mitochondrial uncoupling and the Warburg effect: molecular basis for the reprogramming of cancer cell metabolism. Cancer Res. 2009, 69:2163-2166.
30. Horimoto M., Resnick M.B., Konkin T.A., Routhier J., Wands J.R., Baffy G. Expression of uncoupling protein-2 in human colon cancer. Clin. Cancer Res. 2004, 10:6203-6207.
31. Carretero M.V., Torres L., Latasa U., Garcia-Trevijano E.R., Prieto J., Mato J.M., Avila M.A. Transformed but not normal hepatocytes express UCP2. FEBS Lett. 1998, 439:55-58.
32. Savagner F., Franc B., Guyetant S., Rodien P., Reynier P., Malthiery Y. Defective mitochondrial ATP synthesis in oxyphilic thyroid tumors. J. Clin. Endocrinol. Metab. 2001, 86:4920-4925.
33. Harker W.G., Slade D.L., Dalton W.S., Meltzer P.S., Trent J.M. Multidrug resistance in mitoxantrone-selected HL-60 leukemia cells in the absence of P-glycoprotein overexpression. Cancer Res. 1989, 49:4542-4549.
34. Mailloux R.J., Adjeitey C.N., Xuan J.Y., Harper M.E. Crucial yet divergent roles of mitochondrial redox state in skeletal muscle vs. brown adipose tissue energetics. FASEB J. 2012, 26:363-375.
35. Dalla Pozza E., Fiorini C., Dando I., Menegazzi M., Sgarbossa A., Costanzo C., Palmieri M., Donadelli M. Role of mitochondrial uncoupling protein 2 in cancer cell resistance to gemcitabine. Biochim. Biophys. Acta 2012, 1823:1856-1863.
36. Halestrap A.P., Woodfield K.Y., Connern C.P. Oxidative stress, thiol reagents, and membrane potential modulate the mitochondrial permeability transition by affecting nucleotide binding to the adenine nucleotide translocase. J. Biol. Chem. 1997, 272:3346-3354.
37. Kushnareva Y.E., Sokolove P.M. Prooxidants open both the mitochondrial permeability transition pore and a low-conductance channel in the inner mitochondrial membrane. Arch. Biochem. Biophys. 2000, 376:377-388.
38. Chen X., Zhong Z., Xu Z., Chen L., Wang Y. 2',7'-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radic. Res. 2010, 44:587-604.
39. Coffey R.N., Watson R.W., Hegarty N.J., O'Neill A., Gibbons N., Brady H.R., Fitzpatrick J.M. Thiol-mediated apoptosis in prostate carcinoma cells. Cancer 2000, 88:2092-2104.
40. Pastore A., Piemonte F. S-Glutathionylation signaling in cell biology: progress and prospects. Eur. J. Pharm. Sci. 2012, 46:279-292.
41. Navarro J., Obrador E., Carretero J., Petschen I., Avino J., Perez P., Estrela J.M. Changes in glutathione status and the antioxidant system in blood and in cancer cells associate with tumour growth in vivo. Free Radic. Biol. Med. 1999, 26:410-418.
42. Kawiak A., Piosik J., Stasilojc G., Gwizdek-Wisniewska A., Marczak L., Stobiecki M., Bigda J., Lojkowska E. Induction of apoptosis by plumbagin through reactive oxygen species-mediated inhibition of topoisomerase II. Toxicol. Appl. Pharmacol. 2007, 223:267-276.
43. Beer S.M., Taylor E.R., Brown S.E., Dahm C.C., Costa N.J., Runswick M.J., Murphy M.P. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant DEFENSE. J. Biol. Chem. 2004, 279:47939-47951.
44. Cooper A.J., Pinto J.T., Callery P.S. Reversible and irreversible protein glutathionylation: biological and clinical aspects. Expert Opin. Drug Metabol. Toxicol. 2011, 7:891-910.
45. Hill B.G., Higdon A.N., Dranka B.P., Darley-Usmar V.M. Regulation of vascular smooth muscle cell bioenergetic function by protein glutathiolation. Biochim. Biophys. Acta 2010, 1797:285-295.
46. Conte da Frota M.L., Gomes da Silva E., Behr G.A., Roberto de Oliveira M., Dal-Pizzol F., Klamt F., Moreira J.C. All-trans retinoic acid induces free radical generation and modulate antioxidant enzyme activities in rat sertoli cells. Mol. Cell. Biochem. 2006, 285:173-179.
47. Doroshow J.H. Anthracycline antibiotic-stimulated superoxide, hydrogen peroxide, and hydroxyl radical production by NADH dehydrogenase. Cancer Res. 1983, 43:4543-4551.
48. Mailloux R.J., Beriault R., Lemire J., Singh R., Chenier D.R., Hamel R.D., Appanna V.D. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS One 2007, 2:e690.
49. Ying W. NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid. Redox Signal. 2008, 10:179-206.
50. Finkel T. Signal transduction by reactive oxygen species. J. Cell Biol. 2011, 194:7-15.
51. de Luca A., Moroni N., Serafino A., Primavera A., Pastore A., Pedersen J.Z., Petruzzelli R., Farrace M.G., Pierimarchi P., Moroni G., Federici G., Sinibaldi Vallebona P., Lo Bello M. Treatment of doxorubicin-resistant MCF7/Dx cells with nitric oxide causes histone glutathionylation and reversal of drug resistance. Biochem. J. 2011, 440:175-183.
52. Townsend D.M., He L., Hutchens S., Garrett T.E., Pazoles C.J., Tew K.D. NOV-002, a glutathione disulfide mimetic, as a modulator of cellular redox balance. Cancer Res. 2008, 68:2870-2877.
53. Ladas E.J., Jacobson J.S., Kennedy D.D., Teel K., Fleischauer A., Kelly K.M. Antioxidants and cancer therapy: a systematic review. J. Clin. Oncol. 2004, 22:517-528.
54. Seifried H.E., McDonald S.S., Anderson D.E., Greenwald P., Milner J.A. The antioxidant conundrum in cancer. Cancer Res. 2003, 63:4295-4298.