Mechanisms for redox-regulation of protein kinase C

Frontiers in Pharmacology

Volumn 6, Issue JUN, 2015, Pages

  Steinberg, Susan F ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Oxidative stress; Post translational modifications; Protein kinase C; Src; Tyrosine phosphorylation

Indexed keywords

CALCIUM; CYSTEINE; DIACYLGLYCEROL; GROWTH FACTOR RECEPTOR; INOSITOL TRISPHOSPHATE; PHOSPHOLIPASE C GAMMA; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C DELTA; PROTEIN SH2; PROTEIN SH3; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR;

CELL COMPARTMENTALIZATION; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HEART FAILURE; HEART MUSCLE CONTRACTILITY; HUMAN; INTRACELLULAR SIGNALING; MITOCHONDRION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PROTEIN DOMAIN; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REVIEW; SARCOMERE;

EID: 84936944419     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00128     Document Type: Review

References (46)

1. Adwan, T. S., Ohm, A. M., Jones, D. N., Humphries, M. J., and Reyland, M. E. (2011). Regulated binding of importin-α to protein kinase C-δ in response to apoptotic signals facilitates nuclear import. J. Biol. Chem. 286, 35716-35724. doi: 10.1074/jbc.M111.255950
2. Andersson, D. C., Betzenhauser, M. J., Reiken, S., Meli, A. C., Umanskaya, A., Xie, W., et al. (2011). Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab. 14, 196-207. doi: 10.1016/j.cmet.2011.05.014
3. Benes, C. H., Wu, N., Elia, A. E., Dharia, T., Cantley, L. C., and Soltoff, S. P. (2005). The C2 domain of PKCδ is a phosphotyrosine binding domain. Cell 121, 271-280. doi: 10.1016/j.cell.2005.02.019
4. Churchill, E., Budas, G., Vallentin, A., Koyanagi, T., and Mochly-Rosen, D. (2008). PKC isozymes in chronic cardiac disease: possible therapeutic targets? Annu. Rev. Pharmacol. Toxicol. 48, 569-599. doi: 10.1146/annurev.pharmtox.48.121806.154902
5. Goldberg, M., Zhang, H. L., and Steinberg, S. F. (1997). Hypoxia alters the subcellular distribution of protein kinase C isoforms in neonatal rat ventricular myocytes. J. Clin. Invest. 99, 55-61. doi: 10.1172/JCI119133
6. Gong, J., Yao, Y., Zhang, P., Udayasuryan, B., Komissarova, E. V., Chen, J., et al. (2015). The C2 domain and altered ATP-binding loop phosphorylation at Ser359 mediate the redox-dependent increase in protein kinase C-δ activity. Mol. Cell. Biol. 35, 1727-1740. doi: 10.1128/MCB.01436-14
7. Guo, J., Gertsberg, Z., Ozgen, N., and Steinberg, S. F. (2009). p66Shc links alpha1-adrenergic receptors to a reactive oxygen species-dependent AKT-FOXO3A phosphorylation pathway in cardiomyocytes. Circ. Res. 104, 660-669. doi: 10.1161/CIRCRESAHA.108.186288
8. Hirotani, S., Otsu, K., Nishida, K., Higuchi, Y., Morita, T., Nakayama, H., et al. (2002). Involvement of nuclear factor-kappaB and apoptosis signal-regulating kinase 1 in G-protein-coupled receptor agonist-induced cardiomyocyte hypertrophy. Circulation 105, 509-515. doi: 10.1161/hc0402.102863
9. Humphries, K. M., Deal, M. S., and Taylor, S. S. (2005). Enhanced dephosphorylation of cAMP-dependent protein kinase by oxidation and thiol modification. J. Biol. Chem. 280, 2750-2758. doi: 10.1074/jbc.M410242200
10. Humphries, K. M., Juliano, C., and Taylor, S. S. (2002). Regulation of cAMP-dependent protein kinase activity by glutathionylation. J. Biol. Chem. 277, 43505-43511. doi: 10.1074/jbc.M207088200
11. Juhaszova, M., Zorov, D. B., Kim, S. H., Pepe, S., Fu, Q., Fishbein, K. W., et al. (2004). Glycogen synthase kinase-ß mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J. Clin. Invest. 113, 1535-1549. doi: 10.1172/JCI19906
12. Kambayashi, Y., Takekoshi, S., Tanino, Y., Watanabe, K., Nakano, M., Hitomi, Y., et al. (2007). Various molecular species of diacylglycerol hydroperoxide activate human neutrophils via PKC activation. J. Clin. Biochem. Nutr. 41, 68-75. doi: 10.3164/jcbn.2007009
13. Kang, M. Y., Zhang, Y., Matkovich, S. J., Diwan, A., Chishti, A. H., and Dorn, G. W. (2010). Receptor-independent cardiac protein kinase C-α activation by calpain-mediated truncation of regulatory domains. Circ. Res. 107, 903-912. doi: 10.1161/CIRCRESAHA.110.220772
14. Kishimoto, A., Mikawa, K., Hashimoto, K., Yasuda, I., Tanaka, S., Tominaga, M., et al. (1989). Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J. Biol. Chem. 264, 4088-4092.
15. Knapp, L. T., and Klann, E. (2000). Superoxide-induced stimulation of protein kinase C via thiol modification and modulation of zinc content. J. Biol. Chem. 275, 24136-24145. doi: 10.1074/jbc.M002043200
16. Knock, G. A., and Ward, J. P. (2011). Redox regulation of protein kinases as a modulator of vascular function. Antioxid. Redox Signal. 15, 1531-1547. doi: 10.1089/ars.2010.3614
17. Konishi, H., Tanaka, M., Takemura, Y., Matsuzaki, H., Ono, Y., Kikkawa, U., et al. (1997). Activation of protein kinase C by tyrosine phosphorylation in response to H2O2. Proc. Natl. Acad. Sci. U.S.A. 94, 11233-11237. doi: 10.1073/pnas.94.21.11233
18. Konishi, H., Yamauchi, E., Taniguchi, H., Yamamoto, T., Matsuzaki, H., Takemura, Y., et al. (2001). Phosphorylation sites of protein kinase Cδ in H2O2-treated cells and its activation by tyrosine kinase in vitro. Proc. Natl. Acad. Sci. U.S.A. 98, 6587-6592. doi: 10.1073/pnas.111158798
19. Korichneva, I., Hoyos, B., Chua, R., Levi, E., and Hammerling, U. (2002). Zinc release from protein kinase C as the common event during activation by lipid second messenger or reactive oxygen. J. Biol. Chem. 277, 44327-44331. doi: 10.1074/jbc.M205634200
20. Kuster, G. M., Pimentel, D. R., Adachi, T., Ido, Y., Brenner, D. A., Cohen, R. A., et al. (2005). Alpha-adrenergic receptor-stimulated hypertrophy in adult rat ventricular myocytes is mediated via thioredoxin-1-sensitive oxidative modification of thiols on Ras. Circulation 111, 1192-1198. doi: 10.1161/01.CIR.0000157148.59308.F5
21. Lu, W., Finnis, S., Xiang, C., Lee, H. K., Markowitz, Y., Okhrimenko, H., et al. (2007). Tyrosine311 is phosphorylated by c-Abl and promotes the apoptotic effect of PKCδ in glioma cells. Biochem. Biophys. Res. Commun. 352, 431-436. doi: 10.1016/j.bbrc.2006.11.028
22. MacKay, C. E., and Knock, G. A. (2014). Control of vascular smooth muscle function by Src-family kinases and reactive oxygen species in health and disease. J. Physiol. doi: 10.1113/jphysiol.2014.285304 [Epub ahead of print].
23. Mayr, M., Metzler, B., Chung, Y. L., Mcgregor, E., Mayr, U., Troy, H., et al. (2004). Ischemic preconditioning exaggerates cardiac damage in PKCδ null mice. Am. J. Physiol. Heart Circ. Physiol. 287, H946-H956. doi: 10.1152/ajpheart.00878.2003
24. Nakamura, K., Fushimi, K., Kouchi, H., Mihara, K., Miyazaki, M., Ohe, T., et al. (1998). Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation 98, 794-799. doi: 10.1161/01.CIR.98.8.794
25. Nakashima, H., Frank, G. D., Shirai, H., Hinoki, A., Higuchi, S., Ohtsu, H., et al. (2008). Novel role of protein kinase C-d Tyr311 phosphorylation in vascular smooth muscle cell hypertrophy by angiotensin II. Hypertension 51, 232-238. doi: 10.1161/HYPERTENSIONAHA.107.101253
26. Ohmori, S., Shirai, Y., Sakai, N., Fujii, M., Konishi, H., Kikkawa, U., et al. (1998). Three distinct mechanisms for translocation and activation of the delta subspecies of protein kinase C. Mol. Cell. Biol. 18, 5263-5271.
27. Paulsen, C. E., Truong, T. H., Garcia, F. J., Homann, A., Gupta, V., Leonard, S. E., et al. (2012). Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8, 57-64. doi: 10.1038/nchembio.736
28. Roussel, J., Thireau, J., Brenner, C., Saint, N., Scheuermann, V., Lacampagne, A., et al. (2015). Palmitoyl-carnitine increases RyR2 oxidation and sarcoplasmic reticulum Ca2+ leak in cardiomyocytes: role of adenine nucleotide translocase. Biochim. Biophys. Acta 1852, 749-758. doi: 10.1016/j.bbadis.2015.01.011
29. Russell, B., Curtis, M. W., Koshman, Y. E., and Samarel, A. M. (2010). Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J. Mol. Cell. Cardiol. 48, 817-823. doi: 10.1016/j.yjmcc.2010.02.016
30. Rybin, V. O., Guo, J., Sabri, A., Elouardighi, H., Schaefer, E., and Steinberg, S. F. (2004). Stimulus-specific differences in protein kinase C-δ localization and activation mechanisms in cardiomyocytes. J. Biol. Chem. 279, 19350-19361. doi: 10.1074/jbc.M311096200
31. Santos, C. X., Anilkumar, N., Zhang, M., Brewer, A. C., and Shah, A. M. (2011). Redox signaling in cardiac myocytes. Free Radic. Biol. Med. 50, 777-793. doi: 10.1016/j.freeradbiomed.2011.01.003
32. Santulli, G., Pagano, G., Sardu, C., Xie, W., Reiken, S., D'ascia, S. L., et al. (2015). Calcium release channel RyR2 regulates insulin release and glucose homeostasis. J. Clin. Invest. 125, 1968-1978. doi: 10.1172/JCI79273
33. Stahelin, R. V., Kong, K. F., Raha, S., Tian, W., Melowic, H. R., Ward, K. E., et al. (2012). Protein kinase C-δ C2 domain is a phosphotyrosine binding module that plays a key role in its activation. J. Biol. Chem. 287, 30518-30528. doi: 10.1074/jbc.M112.391557
34. Steinberg, S. F. (2008). Structural basis of protein kinase C isoform function. Physiol. Rev. 88, 1341-1378. doi: 10.1152/physrev.00034.2007
35. Steinberg, S. F. (2012). Cardiac actions of protein kinase C isoforms. Physiology (Bethesda) 27, 130-139. doi: 10.1152/physiol.00009.2012
36. Sumandea, M. P., Rybin, V. O., Hinken, A. C., Wang, C., Kobayashi, T., Harleton, E., et al. (2008). Tyrosine phosphorylation modifies PKCδ-dependent phosphorylation of cardiac troponin I. J. Biol. Chem. 283, 22680-22689. doi: 10.1074/jbc.M802396200
37. Tocchetti, C. G., Molinaro, M., Angelone, T., Lionetti, V., Madonna, R., Mangiacapra, F., et al. (2015). Nitroso-Redox Balance and Modulation of Basal Myocardial Function: an Update from the Italian Society of Cardiovascular Research (SIRC). Curr. Drug Targets doi: 10.2174/1389450116666150304103517 [Epub ahead of print].
38. Truong, T. H., and Carroll, K. S. (2012). Redox regulation of epidermal growth factor receptor signaling through cysteine oxidation. Biochemistry 51, 9954-9965. doi: 10.1021/bi301441e
39. Umanskaya, A., Santulli, G., Xie, W., Andersson, D. C., Reiken, S. R., and Marks, A. R. (2014). Genetically enhancing mitochondrial antioxidant activity improves muscle function in aging. Proc. Natl. Acad. Sci. U.S.A. 111, 15250-15255. doi: 10.1073/pnas.1412754111
40. Wang, X., Mccullough, K. D., Franke, T. F., and Holbrook, N. J. (2000). Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J. Biol. Chem. 275, 14624-14631. doi: 10.1074/jbc.275.19.14624
41. Wang, X. T., Mccullough, K. D., Wang, X. J., Carpenter, G., and Holbrook, N. J. (2001). Oxidative stress-induced phospholipase C-gamma 1 activation enhances cell survival. J. Biol. Chem. 276, 28364-28371. doi: 10.1074/jbc.M102693200
42. Xu, W., Doshi, A., Lei, M., Eck, M. J., and Harrison, S. C. (1999). Crystal structures of c-Src reveal features of its autoinhibitory mechanism. Mol. Cell 3, 629-638. doi: 10.1016/S1097-2765(00)80356-1
43. Yamakawa, H., Banno, Y., Nakashima, S., Yoshimura, S., Sawada, M., Nishimura, Y., et al. (2001). Crucial role of calpain in hypoxic PC12 cell death: calpain, but not caspases, mediates degradation of cytoskeletal proteins and protein kinase C-α and -δ. Neurol. Res. 23, 522-530. doi: 10.1179/016164101101198776
44. Zalk, R., Lehnart, S. E., and Marks, A. R. (2007). Modulation of the ryanodine receptor and intracellular calcium. Annu. Rev. Biochem. 76, 367-385. doi: 10.1146/annurev.biochem.76.053105.094237
45. Zhang, H., Davies, K. J., and Forman, H. J. (2015). TGFbeta1 rapidly activates Src through a non-canonical redox signaling mechanism. Arch. Biochem. Biophys. 568, 1-7. doi: 10.1016/j.abb.2015.01.001
46. Zhang, Y., Matkovich, S. J., Duan, X., Diwan, A., Kang, M. Y., and Dorn, G. W. II. (2011). Receptor-independent protein kinase C-α (PKCα) signaling by calpain-generated free catalytic domains induces HDAC5 nuclear export and regulates cardiac transcription. J. Biol. Chem. 286, 26943-26951. doi: 10.1074/jbc.M111.234757