CaMKII and stress mix it up in mitochondria

Frontiers in Pharmacology

Volumn 5 MAY, Issue , 2014, Pages

  Joiner, Mei Ling A ^a   Koval, Olha M ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

CaMKII; CaMKIIN; Cell death; Mitochondria; Mitochondrial calcium uniporter

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II INHIBITOR; CALCIUM ION; CATECHOLAMINE; PROTEIN KINASE INHIBITOR; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; SODIUM ION; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELL STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; GENE OVEREXPRESSION; HEART FAILURE; HEART MITOCHONDRION; HEART OUTPUT; HUMAN; METABOLIC DISORDER; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; PROTEOMICS; REVIEW;

EID: 84904681715     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00067     Document Type: Review

References (57)

1. Antonarakis, S. E., Lyle, R., Dermitzakis, E. T., Reymond, A., and Deutsch, S. (2004). Chromosome 21 and down syndrome: from genomics to pathophysiology. Nat. Rev. Genet. 5, 725-738. doi: 10.1038/nrg1448.
2. Azarashvili, T., Odinokova, I., Bakunts, A., Ternovsky, V., Krestinina, O., Tyynelä, J., et al. (2014). Potential role of subunit c of F0F1-ATPase and subunit c of storage body in the mitochondrial permeability transition. Effect of the phosphorylation status of subunit c on pore opening. Cell Calcium 55, 69-77. doi: 10.1016/j.ceca.2013.12.002.
3. Baughman, J. M., Perocchi, F., Girgis, H. S., Plovanich, M., Belcher-Timme, C. A., Sancak, Y., et al. (2011). Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345. doi: 10.1038/nature10234.
4. Chang, B. H., Mukherji, S., and Soderling, T. R. (1998). Characterization of a calmodulin kinase II inhibitor protein in brain. Proc. Natl. Acad. Sci. U.S.A. 95, 10890-10895. doi: 10.1073/pnas.95.18.10890.
5. Chaudhuri, D., Sancak, Y., Mootha, V. K., and Clapham, D. E. (2013). MCU encodes the pore conducting mitochondrial calcium currents. Elife 2:e00704. doi: 10.7554/eLife.00704.
6. Clarke, S. J., Khaliulin, I., Das, M., Parker, J. E., Heesom, K. J., and Halestrap, A. P. (2008). Inhibition of mitochondrial permeability transition pore opening by ischemic preconditioning is probably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ. Res. 102, 1082-1090. doi: 10.1161/CIRCRESAHA.107.167072.
7. Covian, R., and Balaban, R. S. (2012). Cardiac mitochondrial matrix and respiratory complex protein phosphorylation. Am. J. Physiol. Heart Circ. Physiol. 303, H940-H966. doi: 10.1152/ajpheart.00077.2012.
8. Crompton, M., and Costi, A. (1988). Kinetic evidence for a heart mitochondrial pore activated by Ca2+, inorganic phosphate and oxidative stress. Eur. J. Biochem. 178, 489-501. doi: 10.1111/j.1432-1033.1988.tb14475.x.
9. Curran, J., Hinton, M. J., Ríos, E., Bers, D. M., and Shannon, T. R. (2007). Beta-adrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ. Res. 100, 391-398. doi: 10.1161/01.RES.0000258172.74570.e6.
10. De Stefani, D., Raffaello, A., Teardo, E., Szabo, I., and Rizzuto, R. (2011). A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340. doi: 10.1038/nature10230.
11. Dolga, A. M., Netter, M. F., Perocchi, F., Doti, N., Meissner, L., Tobaben, S., et al. (2013). Mitochondrial small conductance SK2 channels prevent glutamate-induced oxytosis and mitochondrial dysfunction. J. Biol. Chem. 288, 10792-10804. doi: 10.1074/jbc.M113.453522.
12. Elrod, J. W., Wong, R., Mishra, S., Vagnozzi, R. J., Sakthievel, B., Goonasekera, S. A., et al. (2010). Cyclophilin D controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J. Clin. Invest. 120, 3680-3687. doi: 10.1172/JCI43171.
13. Erickson, J. R., Joiner, M. A., Guan, X., Kutschke, W., Yang, J., Oddis, C. V., et al. (2008). A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133, 462-474. doi: 10.1016/j.cell.2008.02.048.
14. Fieni, F., Bae Lee, S., Jan, Y. N., and Kirichok, Y. (2012). Activity of the mitochondrial calcium uniporter varies greatly between tissues. Nat. Commun. 3, 1317. doi: 10.1038/ncomms2325.
15. Fridovich, I. (1983). Superoxide radical: an endogenous toxicant. Annu. Rev. Pharmacol. Toxicol. 23, 239-257. doi: 10.1146/annurev.pa.23.040183.001323.
16. García-Rivas Gde, J., Carvajal, K., Correa, F., and Zazueta, C. (2006). Ru360, a specific mitochondrial calcium uptake inhibitor, improves cardiac post-ischaemic functional recovery in rats in vivo. Br. J. Pharmacol. 149, 829-837. doi: 10.1038/sj.bjp.0706932.
17. Giorgio, V., von Stockum, S., Antoniel, M., Fabbro, A., Fogolari, F., Forte, M., et al. (2013). Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc. Natl. Acad. Sci. U.S.A. 110, 5887-5892. doi: 10.1073/pnas.1217823110.
18. Griffiths, E. J., and Halestrap, A. P. (1993). Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol. 25, 1461-1469. doi: 10.1006/jmcc.1993.1162.
19. Gunter, T. E., and Pfeiffer, D. R. (1990). Mechanisms by which mitochondria transport calcium. Am. Cell Physiol. 258, C755-C786.
20. Halestrap, A., and Brenner, C. (2003). The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10, 1507-1525. doi: 10.2174/0929867033457278.
21. Halestrap, A. P. (2009). What is the mitochondrial permeability transition pore? J. Mol. Cell. Cardiol. 46, 821-831. doi: 10.1016/j.yjmcc.2009.02.021.
22. Hoffman, N. E., Chandramoorthy, H. C., Shamugapriya, S., Zhang, X., Rajan, S., Mallilankaraman, K., et al. (2013). MICU1 motifs define mitochondrial calcium uniporter binding and activity. Cell Rep. 5, 1576-1588. doi: 10.1016/j.celrep.2013.11.026.
23. Hornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B., et al. (2012). PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-D270. doi: 10.1093/nar/gkr1122.
24. Joiner, M. A., Koval, O., Li, J., He, B. J., Allamargot, C., Gao, Z., et al. (2012). CaMKII determines mitochondrial stress responses in heart. Nature 491, 269-273. doi: 10.1038/nature11444.
25. Kane, D. A., and Pavlov, E. V. (2013). Calculation of ion currents across the inner membrane of functionally intact mitochondria. Channels 7, 426-431. doi: 10.4161/chan.26290.
26. Kim, J.-S., Jin, Y., and Lemasters, J. J. (2006). Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 290, H2024-H2034. doi: 10.1152/ajpheart.00683.2005.
27. Kirichok, Y., Krapivinsky, G., and Clapham, D. E. (2004). The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427, 360-364. doi: 10.1038/nature02246.
28. Koc, E. C., and Koc, H. (2012). Regulation of mammalian mitochondrial translation by post-translational modifications. Biochim. Biophys. Acta 1819, 1055-1066. doi: 10.1016/j.bbagrm.2012.03.003.
29. Koval, O. M., Guan, X., Wu, Y., Joiner, M. A., Gao, Z., Chen, B., et al. (2010). CaV1.2 beta-subunit coordinates CaMKII-triggered cardiomyocyte death and afterdepolarizations. Proc. Natl. Acad. Sci. U.S.A. 107, 4996-5000. doi: 10.1073/pnas.0913760107.
30. Lee, J., Xu, Y., Chen, Y., Sprung, R., Kim, S. C., Xie, S., et al. (2007). Mitochondrial phosphoproteome revealed by an improved IMAC method and MS/MS/MS. Mol. Cell. Proteomics 6, 669-676. doi: 10.1074/mcp.M600218-MCP200.
31. Lemasters, J. J., Theruvath, T. P., Zhong, Z., and Nieminen, A.-L. (2009). Mitochondrial calcium and the permeability transition in cell death. Biochim. Biophys. Acta 1787, 1395-1401. doi: 10.1016/j.bbabio.2009.06.009.
32. Luo, M., Guan, X., Luczak, E. D., Lang, D., Kutschke, W., Gao, Z., et al. (2013). Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J. Clin. Invest. 123, 1262-1274. doi: 10.1172/JCI65268.
33. Maack, C., Cortassa, S., Aon, M. A., Ganesan, A. N., Liu, T., and O'Rourke, B. (2006). Elevated cytosolic Na+ decreases mitochondrial Ca2+ Uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ. Res. 99, 172-182. doi: 10.1161/01.RES.0000232546.92777.05.
34. Miller, S. G., and Kennedy, M. B. (1986). Regulation of brain Type II Ca2+calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch. Cell 44, 861-870. doi: 10.1016/0092-8674(86)90008-5.
35. Miura, T., Tanno, M., and Sato, T. (2010). Mitochondrial kinase signalling pathways in myocardial protection from ischaemia/reperfusion-induced necrosis. Cardiovasc. Res. 88, 7-15. doi: 10.1093/cvr/cvq206.
36. Moon, S. H., Jenkins, C. M., Kiebish, M. A., Sims, H. F., Mancuso, D. J., and Gross, R. W. (2012). Genetic ablation of calcium-independent phospholipase A2gamma (iPLA2gamma) attenuates calcium-induced opening of the mitochondrial permeability transition pore and resultant cytochrome c release. J. Biol. Chem. 287, 29837-29850. doi: 10.1074/jbc.M112.373654.
37. Nicolli, A., Basso, E., Petronilli, V., Wenger, R. M., and Bernardi, P. (1996). Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin a-sensitive channel. J. Biol. Chem. 271, 2185-2192.
38. Ozcan, L., and Tabas, I. (2010). Pivotal role of calcium/calmodulin-dependent protein kinase II in ER stress-induced apoptosis. Cell Cycle 9, 223-224. doi: 10.4161/cc.9.2.10596.
39. Pan, X., Liu, J., Nguyen, T., Liu, C., Sun, J., Teng, Y., et al. (2013). The physiological role of mitochondrial calcium revealed by mice lacking the mitochondrial calcium uniporter. Nat. Cell Biol. 15, 1464-1472. doi: 10.1038/ncb2868.
40. Perocchi, F., Gohil, V. M., Girgis, H. S., Bao, X. R., McCombs, J. E., Palmer, A. E., et al. (2010). MICU1 encodes a mitochondrial EF hand protein required for Ca2+ uptake. Nature 467, 291-296. doi: 10.1038/nature09358.
41. Piot, C., Croisille, P., Staat, P., Thibault, H., Rioufol, G., Mewton, N., et al. (2008). Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N. Engl. J. Med. 359, 473-481. doi: 10.1056/NEJMoa071142.
42. Purohit, A., Rokita, A. G., Guan, X., Chen, B., Koval, O. M., Voigt, N., et al. (2013). Oxidized ca2+/calmodulin-dependent protein kinase II triggers atrial fibrillation. Circulation 128, 1748-1757. doi: 10.1161/CIRCULATIONAHA.113.003313.
43. Rose, A. J., Frøsig, C., Kiens, B., Wojtaszewski, F. P. Jr., and Richter, E. A. (2007). Effect of endurance exercise training on Ca2+ calmodulin-dependent protein kinase II expression and signalling in skeletal muscle of humans. J. Physiol. 583, 785-795. doi: 10.1113/jphysiol.2007.138529.
44. Ryu, S.-Y., Beutner, G., Dirksen, R. T., Kinnally, K. W., and Sheu, S.-S. (2010). Mitochondrial ryanodine receptors and other mitochondrial Ca2+ permeable channels. FEBS Lett. 584, 1948-1955. doi: 10.1016/j.febslet.2010.01.032.
45. Salas, M. A., Valverde, C. A., Sanchez, G., Said, M., Rodriguez, J. S., Portiansky, E. L., et al. (2009). The signalling pathway of CaMKII-mediated apoptosis and necrosis in the ischemia/reperfusion injury. J. Mol. Cell. Cardiol. 48, 1298-1306. doi: 10.1016/j.yjmcc.2009.12.015.
46. Sancak, Y., Markhard, A. L., Kitami, T., Kovács-Bogdán, E., Kamer, K. J., Udeshi, N. D., et al. (2013). EMRE Is an essential component of the mitochondrial calcium uniporter complex. Science 342, 1379-1382. doi: 10.1126/science.1242993.
47. Sepúlveda, M., Gonano, L. A., Back, T. G., Chen, S. R. W., and Vila Petroff, M. (2013). Role of CaMKII and ROS in rapid pacing-induced apoptosis. J. Mol. Cell. Cardiol. 63, 135-145. doi: 10.1016/j.yjmcc.2013.07.013.
48. Sharma, V., Abraham, T., So, A., Allard, M., and McNeill, J. (2010). Functional effects of protein kinases and peroxynitrite on cardiac carnitine palmitoyltransferase-1 in isolated mitochondria. Mol. Cell. Biochem. 337, 223-237. doi: 10.1007/s11010-009-0303-2.
49. Sugawara, K., Fujikawa, M., and Yoshida, M. (2013). Screening of protein kinase inhibitors and knockdown experiments identified four kinases that affect mitochondrial ATP synthesis activity. FEBS Lett. 587, 3843-3847. doi: 10.1016/j.febslet.2013.10.012.
50. Timmins, J. M., Ozcan, L., Seimon, T. A., Li, G., Malagelada, C., Backs, J., et al. (2009). Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways. J. Clin. Invest. 119, 2925-2941. doi: 10.1172/JCI38857.
51. Wagner, S., Dybkova, N., Rasenack, E. C., Jacobshagen, C., Fabritz, L., Kirchhof, P., et al. (2006). Ca2+/calmodulin-dependent protein kinase II regulates cardiac Na+ channels. J. Clin. Invest. 116, 3127-3138. doi: 10.1172/JCI26620.
52. Wei, A.-C., Liu, T., Winslow, R. L., and O'Rourke, B. (2012). Dynamics of matrix-free Ca2+ in cardiac mitochondria: two components of Ca2+ uptake and role of phosphate buffering. J. Gen. Physiol. 139, 465-478. doi: 10.1085/jgp.201210784.
53. Witze, E. S., Old, W. M., Resing, K. A., and Ahn, N. G. (2007). Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4, 798-806. doi: 10.1038/nmeth1100.
54. Yang, Y., Zhu, W.-Z., Joiner, M., Zhang, R., Oddis, C. V., Hou, Y., et al. (2006). Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. Am. J. Physiol. Heart Circ. Physiol. 291, H3065-H3075. doi: 10.1152/ajpheart.00353.2006.
55. Yun, B., Lee, H., Ghosh, M., Cravatt, B. F., Hsu, K.-L., Bonventre, J. V., et al. (2013). Serine hydrolase inhibitors block necrotic cell death by preventing calcium overload of the mitochondria and permeability transition pore formation. J. Biol. Chem. 289, 1491-1504. doi: 10.1074/jbc.M113.497651.
56. Zhang, T., Guo, T., Mishra, S., Dalton, N. D., Kranias, E. G., Peterson, K. L., et al. (2010). Phospholamban ablation rescues sarcoplasmic reticulum Ca2+ handling but exacerbates cardiac dysfunction in CaMKII{delta}C transgenic mice. Circ. Res. 106, 354-362. doi: 10.1161/CIRCRESAHA.109.207423.
57. Zhao, X., León, I. R., Bak, S., Mogensen, M., Wrzesinski, K., Højlund, K., et al. (2011). Phosphoproteome analysis of functional mitochondria isolated from resting human muscle reveals extensive phosphorylation of inner membrane protein complexes and enzymes. Mol. Cell. Proteomics 10:M110.000299. doi: 10.1074/mcp.M110.000299.