Protein kinase C-α activation promotes recovery of mitochondrial function and cell survival following oxidant injury in renal cells

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 4, 2012, Pages

  Nowak, Grazyna ^a   Bakajsova, Diana ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

ATP; Complex I; Complex IV; Cytochrome oxidase; Electron transport chain; Mitochondrial dysfunction; Reactive oxygen species; Renal proximal tubular cells; Respiration

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; MUTANT PROTEIN; PROTEIN KINASE C ALPHA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); TERT BUTYL HYDROPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; GENE OVEREXPRESSION; HYPERPOLARIZATION; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE;

EID: 84865132210     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00072.2012     Document Type: Article

References (44)

1. Agudo-López A, Miguel BG, Fernández I, Martínez AM. Role of protein kinase C and mitochondrial permeability transition pore in the neuroprotective effect of ceramide in ischemia-induced cell death. FEBS Lett 585: 99-103, 2011.
2. Bouwman RA, Musters RJP, van Beek-Harmsen BJ, de Lange JJ, Lamberts RR, Loer SA, Boer C. Sevoflurane-induced cardioprotection depends on PKC-α activation via production of reactive oxygen species. Br J Anaesth 99: 639-645, 2007.
3. Bradshaw D, Hill CH, Nixon JS, Wilkinson SE. Therapeutic potential of protein kinase C inhibitors. Agents Actions 38: 135-147, 1993.
4. Breitkreutz D, Braiman-Wiksman L, Daum N, Denning M, Tennenbaum T. Protein kinase C family: on the crossroads of cell signaling in skin and tumor epithelium. J Cancer Res Clin Oncol 133: 793-808, 2007.
5. Carpenter L, Cordery D, Biden TJ. Protein kinase Cδ activation by interleukin-1β stabilizes inducible nitric-oxide synthase mRNA in pancreatic β-cells. J Biol Chem 276: 5368-5374, 2001.
6. Cerioni L, Palomba L, Brüne B, Cantoni O. Peroxynitrite-induced mitochondrial translocation of PKCα causes U937 cell survival. Biochem Biophys Res Commun 339: 126-131, 2006.
7. Costa ADT, Jakob R, Costa CL, Andrukhiv K, West IC, Garlid KD. The mechanism by which the mitochondrial ATP-sensitive K+ channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem 281: 20801-20808, 2006.
8. Dong L, Stevens JL, Fabbro D, Jaken S. Regulation of protein kinase C isozymes in kidney regeneration. Cancer Res 53: 4542-4549, 1993.
9. Fang J, Prabu SK, Sepuri NB, Raza H, Anandatheerthavarada HK, Galati D, Spear J, Avadhani NG. Site specific phosphorylation of cytochrome c oxidase subunits I, IVi1 and Vb in rabbit hearts subjected to ischemia/reperfusion. FEBS Lett 581: 1302-1310, 2007.
10. Fernández E, Cuenca N, García M, De Juan J. Two types of mitochondria are evidenced by protein kinase C immunoreactivity in the Müller cells of the carp retina. Neurosci Lett 183: 202-205, 1995.
11. Gopalakrishna R, Chen ZH, Gundimeda U. Tobacco smoke tumor promoters, catechol and hydroquinone, induce oxidative regulation of protein kinase C and influence invasion and metastasis of lung carcinoma cells. Proc Natl Acad Sci USA 91: 12233-12237, 1994.
12. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med 28: 1349-1361, 2000.
13. Gopalakrishna R, Gundimeda U. Antioxidant regulation of protein kinase C in cancer prevention. J Nutr 132: 3819S-3823S, 2002.
14. Kuo T, Huang W, Guh J. WJ9708012 exerts anticancer activity through PKC-α related crosstalk of mitochondrial and endoplasmic reticulum stresses in human hormone-refractory prostate cancer cells. Acta Pharmacol Sinica 32: 89-98, 2011.
15. Law RH, Manon S, Devenish RJ, Nagley P. ATP synthase from Saccharomyces cerevisiae. Methods Enzymol 260: 133-163, 1995.
16. Liu X, Godwin ML, Nowak G. Protein kinase C-α inhibits the repair of oxidative phosphorylation after S-(1,2-dichlorovinyl)-L-cysteine injury in renal cells. Am J Physiol Renal Physiol 287: F64-F73, 2004.
17. Lu N, Wang W, Liu J, Wong C. Protein kinase C epsilon affects mitochondrial function through estrogen-related receptor alpha. Cell Signal 23: 1473-1478, 2011.
18. Nishihara M, Miura T, Ohori K, Miki T, Shimamoto K. GSK-3β phosphorylated by PKC and Akt inhibits ANT-cyclophilin-D interaction: a possible mechanism of cardiomyocyte protection. J Mol Cell Cardiol 44: 441-442, 2008.
19. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607-614, 1992.
20. Nowak G. Protein kinase C mediates repair of mitochondrial and transport functions after toxicant-induced injury in renal cells. J Pharmacol Exp Ther 306: 157-165, 2003.
21. Nowak G. Protein kinase C-α and ERK1/2 mediate mitochondrial dysfunction, decreases in active Na+ transport, and cisplatin-induced apoptosis in renal cells. J Biol Chem 277: 43377-43388, 2002.
22. Nowak G, Bakajsova D, Clifton GL. Protein kinase C-PPmodulates mitochondrial function and active Na+ transport after oxidant injury in renal cells. Am J Physiol Renal Physiol 286: F307-F316, 2004.
23. Nowak G, Clifton GL, Godwin ML, Bakajsova D. Activation of ERK1/2 pathway mediates oxidant-induced decreases in mitochondrial function in renal cells. Am J Physiol Renal Physiol 291: F840-F855, 2006.
24. Nowak G, Schnellmann RG. Autocrine production and TGF-β1-mediated effects on metabolism and viability in renal cells. Am J Physiol Renal Fluid Electrolyte Physiol 271: F689-F697, 1996.
25. Nowak G, Schnellmann RG. L-Ascorbic acid regulates growth and metabolism of renal cells: improvements in cell culture. Am J Physiol Cell Physiol 271: C2072-C2080, 1996.
26. Nowak G, Schnellmann RG. Improved culture conditions stimulate gluconeogenesis in primary cultures of renal proximal tubule cells. Am J Physiol Cell Physiol 268: C1053-C1061, 1995.
27. Nowak G, Bakajsova D, Hayes C, Hauer-Jensen M, Compadre CM. γ-Tocotrienol protects against mitochondrial dysfunction and renal cell death. J Pharmacol Exp Ther 340: 330-338, 2012.
28. Nowak G, Bakajsova D, Samarel AM. Protein kinase C-PPactivation induces mitochondrial dysfunction and fragmentation in renal proximal tubules. Am J Physiol Renal Physiol 301: F197-F208, 2011.
29. Padanilam BJ. Induction and subcellular localization of protein kinase C isozymes following renal ischemia. Kidney Int 59: 1789-1797, 2001.
30. Perletti GP, Smeraldi C, Porro D, Piccinini F. Involvement of the α isoenzyme of protein kinase C in the growth inhibition induced by phorbol esters in MH1C1 hepatoma cells. Biochem Biophys Res Commun 205: 1589-1594, 1994.
31. Porter MJ, Heidkamp MC, Scully BT, Patel N, Martin JL, Samarel AM. Isoenzyme-selective regulation of SERCA2 gene expression by protein kinase C in neonatal rat ventricular myocytes. Am J Physiol Cell Physiol 285: C39-C47, 2003.
32. Prabu SK, Anandatheerthavarada HK, Raza H, Srinivasan S, Spear JF, Avadhani NG. Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J Biol Chem 281: 2061-2070, 2006.
33. Rasmo DD, Palmisano G, Scacco S, Technikova-Dobrova Z, Panelli D, Cocco T, Sardanelli AM, Gnoni A, Micelli L, Trani A, Luccia AD, Papa S. Phosphorylation pattern of the NDUFS4 subunit of complex I of the mammalian respiratory chain. Mitochondrion 10: 464-471, 2010.
34. Rosivatz E, Woscholski R. Removal or masking of phosphatidylinositol-(4,5)bisphosphate from the outer mitochondrial membrane causes mitochondrial fragmentation. Cell Signal 23: 478-486, 2011.
35. Ruvolo PP, Deng X, Carr BK, May WS. A functional role for mitochondrial protein kinase Cα in Bcl2 phosphorylation and suppression of apoptosis. J Biol Chem 273: 25436-25442, 1998.
36. Serlachius E, Svennilson J, Schalling M, Aperia A. Protein kinase C in the developing kidney: Isoform expression and effects of ceramide and PKC inhibitors. Kidney Int 52: 901-910, 1997.
37. Shaik ZP, Fifer EK, Nowak G. Akt activation improves oxidative phosphorylation in renal proximal tubular cells following nephrotoxicant injury. Am J Physiol Renal Physiol 294: F423-F432, 2008.
38. Shaik ZP, Fifer EK, Nowak G. Protein kinase B/Akt modulates nephrotoxicant-induced necrosis in renal cells. Am J Physiol Renal Physiol 292: F292-F303, 2007.
39. Technikova-Dobrova Z, Sardanelli AM, Speranza F, Scacco S, Signorile A, Lorusso V, Papa S. Cyclic adenosine monophosphate-dependent phosphorylation of mammalian mitochondrial proteins: enzyme and substrate characterization and functional role. Biochemistry 40: 13941-13947, 2001.
40. Vijayan K, Szotek EL, Martin JL, Samarel AM. Protein kinase C-α-induced hypertrophy of neonatal rat ventricular myocytes. Am J Physiol Heart Circ Physiol 287: H2777-H2789, 2004.
41. Wang W, Yeh S, Yi-Kung Huang E, Lu Y, Wang C, Huang CF, Lin W. Mitochondrial anchoring of PKCα by PICK1 confers resistance to etoposide-induced apoptosis. Apoptosis 12: 1857-1871, 2007.
42. Wang W, Yeh S, Chang Y, Hsiao S, Lian W, Lin C, Huang CF, Lin W. PICK1, an anchoring protein that specifically targets protein kinase Cα to mitochondria selectively upon serum stimulation in NIH 3T3 Cells. J Biol Chem 278: 37705-37712, 2003.
43. Wang Y, Biswas G, Prabu SK, Avadhani NG. Modulation of mitochondrial metabolic function by phorbol 12-myristate 13-acetate through increased mitochondrial translocation of protein kinase Cα in C2C12 myocytes. Biochem Pharmacol 72: 881-892, 2006.
44. Wu Q, Liu S, Ding L, Ye X, Su W. PKCα translocation from mitochondria to nucleus is closely related to induction of apoptosis in gastric cancer cells. Sci China C Life Sci 45: 237-244, 2002.