Role of protein kinase C in ischemic "conditioning": From first evidence to current perspectives

Journal of Cardiovascular Pharmacology and Therapeutics

Volumn 18, Issue 6, 2013, Pages 525-532

  Simkhovich, Boris Z ^a,b   Przyklenk, Karin ^c   Kloner, Robert A ^a,b  

^a GOOD SAMARITAN HOSPITAL   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ischemic preconditioning; postconditioning; protein kinase C; remote preconditioning

Indexed keywords

8 (4 SULFOPHENYL)THEOPHYLLINE; DELCASERTIB; DIAZOXIDE; GLIBENCLAMIDE; POLYMYXIN B; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; STAUROSPORINE;

CORONARY REPERFUSION; CYTOSOL; ENZYME ACTIVITY; HEART FUNCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; ISCHEMIC PRECONDITIONING; KIDNEY ARTERY STENOSIS; LEG ISCHEMIA; MESENTERIC ARTERY OCCLUSION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ISCHEMIC PRECONDITIONING; POSTCONDITIONING; PROTEIN KINASE C; REMOTE PRECONDITIONING;

ANIMALS; CYTOSOL; DIGLYCERIDES; HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING, MYOCARDIAL; PROTEIN ISOFORMS; PROTEIN KINASE C; PROTEIN KINASE C-EPSILON; PROTEIN TRANSPORT;

EID: 84887577572     PISSN: 10742484     EISSN: 19404034     Source Type: Journal    
DOI: 10.1177/1074248413494814     Document Type: Review

References (66)

1. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986 ; 74 (5). 1124-1136
2. Li Y, Whittaker P, Kloner RA. The transient nature of the effect of ischemic preconditioning. Circulation. 1992 ; 123 (2). 346-353
3. Schott RJ, Rochmann S, Braun ER, Schaper W. Ischemic preconditioning reduces infarct size in swine myocardium. Circ Res. 1990 ; 66 (4). 1133-1142
4. Liu GS, Thornton J, Van Winkle DM, Stanley AW, Olsson RA, Downey JM. Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart. Circulation. 1991 ; 84 (1). 350-356
5. Hale SL, Kloner RA. Effect of ischemic preconditioning on regional myocardial blood flow in the rabbit. Coron Artery Dis. 1992 ; 18 (2). 133-140
6. Liu GS, Richards SC, Olsson RA, Mullane K, Walsh RS, Downey JM. Evidence that adenosine A3 receptor may mediate the protection afforded by preconditioning in the isolated rabbit heart. Cardiovasc Res. 1994 ; 28 (7). 1057-1061
7. Wall TM, Sheehy R, Hartman JC. Role of bradykinin in myocardial preconditioning. J Pharmacol Exp Ther. 1994 ; 270 (2). 681-689
8. Miki T, Cohen MV, Downey JM. Opioid receptor contributes to ischemic preconditioning through protein kinase C activation in rabbits. Mol Cell Biochem. 1998 ; 186 (1-2). 3-12
9. Schultz JE, Hsu AK, Gross GJ. Ischemic preconditioning in the intact rat heart is mediated by δ1- but not μ- or κ-opioid receptors. Circulation. 1998 ; 97 (13). 1282-1289
10. Ytrehus K, Liu Y, Downey JM. Preconditioning protects ischemic rabbit heart by protein kinase C activation. Am J Physiol. 2004 ; 266 (3 pt 2). H1145 - H1152
11. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 1995 ; 9 (7). 484-496
12. Sugden PH, Bogoyevitch MA. Intracellular signaling through protein kinases in the heart. Cardiovasc Res. 1995 ; 30 (4). 478-492
13. Budas GR, Churchill EN, Mochly-Rosen D. Cardioprotective mechanisms of PKC-izozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury. Pharmacol Rev. 2007 ; 55 (6). 523-536
14. Steinberg SF. Cardiac action of protein kinase C isoforms. Physiology. 2012 ; 27 (3). 130-139
15. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM. Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol. 2004 ; 288 (2). H971 - H976
16. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the Reperfusion Injury Salvage Kinase (RISK)-pathway. Cardiovasc Res. 2004 ; 61 (3). 448-460
17. Downey JM, Davis AM, Cohen MV. Signaling pathways in ischemic preconditioning. Heart Fail Rev. 2007 ; 12 (3-4). 181-188
18. Cohen MV, Downey JM. Adenosine: trigger and mediator of cardioprotection. Basic Res Cardiol. 2008 ; 103 (3). 203-215
19. Downey JM, Cohen MV. Signal transduction in ischemic preconditioning. Z Kardiol. 1995 ; 84 (suppl 4). 77-86
20. Yellon DM, Baxter GF, Garcia-Dorado D, Heusch G, Sumeray MS. Ischaemic preconditioning: present position and future directions. Cardiovasc Res. 1998 ; 37 (1). 21-33
21. Sandhu R, Diaz RJ, Mao GD, Wilson GJ. Ischemic preconditioning. Differences in protection and susceptibility to blockade with single-cycle versus multicycle transient ischemia. Circulation. 1997 ; 96 (3). 984-995
22. Speechly-Dick ME, Mocanu MM, Yellon DM, Protein kinase C. Its role in ischemic preconditioning in the rat. Circ Res. 1994 ; 75 (3). 586-590
23. Li Y, Kloner RA. Does protein kinase C play a role in ischemic preconditioning in rat hearts. Am J Physiol. 1995 ; 268 (1 pt 2). H426 - H431
24. Okamura T, Miura T, Iwamoto H, et al. Ischemic preconditioning attenuates apoptosis through protein kinase C in rat hearts. Am J Physiol. 1999 ; 277 (5 pt 2). H1997 - H2001
25. Moolman JA, Genade S, Tromp E, Lochner A. No evidence for mediation of ischemic preconditioning by alpha 1-adrenergic signal transduction pathway or protein kinase C in the isolated rat heart. Cardiovasc Drugs Ther. 1996 ; 10 (2). 125-136
26. Kitakaze M, Node K, Minamino T, et al. Role of activation of protein kinase C in the infarct size-limiting effect of ischemic preconditioning through activation of ecto-5′-nucleotidase activity. Circulation. 1996 ; 93 (4). 781-791
27. Przyklenk K, Sussman MA, Simkhovich BZ, Kloner RA. Does ischemic preconditioning trigger translocation of protein kinase C in the canine mode?. Circulation. 1995 ; 92 (6). 1546-1557
28. Vogh AM, Htun P, Arras M, Elsasser A, Podzuweit T, Schaper W. Intramyocardial infusion of tool drugs for the study of molecular mechanisms in ischemic preconditioning. Basic Res Cardiol. 1996 ; 91 (5). 389-400
29. Vahlhaus C, Schultz R, Post H, Onallch R, Heusch G. No prevention of ischemic preconditioning by protein kinase C inhibitor staurosporine in swine. Circ Res. 1996 ; 79 (3). 407-414
30. Simkhovich BZ, Przyklenk K, Hale SL, Patterson M, Kloner RA. Direct evidence that ischemic preconditioning does not cause protein kinase C translocation in rabbit heart. Cardiovasc Res. 1996 ; 32 (6). 1064-1070
31. Banerjee A, Gamboni-Robertson F, Mitchell MB, et al. Stress-induced cardioadaptation reveals a code linking hormone receptors and spatial redistribution of PKC isoforms. Ann N Y Acad Sci. 1996 ; 793: 226-239
32. Ping P, Zhang J, Qiu Y, et al. Ischemic preconditioning induces selective translocation of protein kinase C isoforms â̂Š and η in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res. 1997 ; 81 (3). 404-414
33. Yoshida K, Kawamura S, Mizukami Y, Kitakaze M. Implication of protein kinase C-α, δ and â̂Š isoforms in ischemic preconditioning in perfused rat hearts. J Biochem. 1997 ; 122 (3). 506-511
34. Saurin AT, Pennington DJ, Raat NJ, Latchman DS, Owen MJ, Marber MS. Targeted disruption of the protein kinase C epsilon gene abolishes the infarct size reduction that follows ischaemic preconditioning of isolated buffer-perfused mouse hearts. Cardiovasc Res. 2002 ; 55 (3). 672-680
35. Liu GS, Cohen MV, Mochly-Rosen D, Downey JM. Protein kinase C-â̂Š is responsible for the protection of preconditioning in rabbit cardiomyocytes. J Mol Cell Cardiol. 1999 ; 31 (10). 1937-1948
36. Gregory KN, Hahn H, Haglighi K, et al. Increased particulate partitioning of PKCâ̂Š reverses susceptibility of phospholamban knockout hearts to ischemic injury. J Mol Cell Cardiol. 2003 ; 36 (2). 313-318
37. Kawamura S, Yoshida K, Miura T, Muzikami Y, Matsuzaki M. Ischemic preconditioning translocates PKC-δ and -â̂Š, which mediate functional protection in isolated rat heart. Am J Physiol. 1998 ; 275 (6 pt 2). H2266 - H2271
38. Wang Y, Kyoji H, Muhammad A. Activation of mitochondrial ATP-sensitive K+ channel for cardiac protection against ischemic injury is dependent on protein kinase C activity. Circ Res. 1999 ; 85 (8). 731-741
39. Zhao J, Renner L, Wightman L, et al. The expression of constitutively active isotypes of protein kinase C to investigate preconditioning. J Biol Chem. 1998 ; 273 (36). 23072-23079
40. Kolar F, Jezkova J, Balkova P, et al. Role of oxidative stress in PKC-δ upregulation and cardioprotection induced by chronic intermittent hypoxia. Am J Physiol Heart Circ Physiol. 2007 ; 292 (1). H224 - H230
41. Mayr M, Metzler B, Chung YL, et al. Ischemic preconditioning exaggerates cardiac damage in PKC-δ null mice. Am J Physiol. 2004 ; 287 (2). H946 - H956
42. Fryer RM, Hsu AK, Wang Y, Henry M, Eels J, Gross GJ. PKC-δ inhibition does not block preconditioning-induced preservation in mitochondrial ATP synthesis and infarct size reduction in rats. Basic Res Cardiol. 2002 ; 97 (1). 47-54
43. Sivaraman V, Hausenloy DJ, Kolvekar S, et al. The divergent roles of protein kinase C epsilon and delta in simulated ischaemia-reperfusion injury in human myocardium. J Mol Cell Cardiol. 2009 ; 46 (5). 758-764
44. Churchill EN, Ferreira JC, Brum PC, Szweda LI, Mochly-Rosen D. Ischaemic preconditioning improves proteasomal activity and increases the degradation of δPKC during reperfusion. Cardiovasc Res. 2010 ; 85 (2). 385-394
45. Inagaki K, Chen L, Ikeno F, et al. Inhibition of δ-protein kinase C protects against reperfusion injury of the ischemic heart in vivo. Circulation. 2003 ; 108 (19). 2304-2307
46. Lincoff AM. Selective inhibition of delta protein kinase C to reduce infarct size after primary percutaneous intervention for acute myocardial infarction; the PROTECTION-AMI phase IIb clinical trial. Presented at: American College of Cardiology Meeting; April 2-5, 2011; New Orleans, LA.
47. Ping P, Zhang J, Cao X, et al. PKC-dependent activation of p44/p42 MAPKs during myocardial ischemia-reperfusion in conscious rabbits. Am J Physiol. 1999 ; 276 (5 pt 2). H1468 - H1481
48. Ping P, Zhang J, Huang S, et al. PKC-dependent activation of p46/p54 JNKs during ischemic preconditioning in conscious rabbits. Am J Physiol. 1999 ; 277 (5 pt 2). H1771 - H1785
49. Baines CP, Zhang J, Wang GW, et al. Mitochondrial PKCâ̂ Š and MAPK form signaling module in the murine heart: enhanced mitochondrial PKCâ̂Š-MAPK interactions and differential MAPK activation in PKCâ̂Š-induced cardioprotection. Circ Res. 2002 ; 90 (4). 390-397
50. Pain T, Yang XM, Critz SD, et al. Opening of mitochondrial KATP channels triggers the preconditioned state by generating free radicals. Circ Res. 2000 ; 87 (6). 460-466
51. Le Good JA, Ziegler WH, Parekh DB, Alessi DR, Cohen P, Parker PJ. Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science. 1998 ; 281 (5385). 2042-2045
52. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation. 1993 ; 83 (3). 893-899
53. Birnbaum Y, Hale SL. Kloner RA. "Ischemic preconditioning at a distance": reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in rabbits. Circulation. 1997 ; 96 (5). 1641-1646
54. Gho BC, Schoemaker RG, van Den Doel MA, Duncker DJ, Verdouw PD. Myocardial protection by brief ischemia in noncardiac tissue. Circulation. 1996 ; 94 (9). 2193-2220
55. Hausenloy DJ, Iliodromitis EK, Andreadou I, et al. Investigating the signal transduction pathways underlying remote ischemic conditioning in the porcine heart. Cardiovasc Drugs Ther. 2012 ; 26 (2). 87-93
56. Zhao ZQ, Corvera JS, Halkos ME, et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol. 2003 ; 285 (2). H579 - H588
57. Heusch G. Postconditioning: old wine in a new bottle?. J Am Coll Cardiol. 2004 ; 44 (5). 1111-1112
58. Kerendi F, Kin H, Halkos ME, et al. Remote postconditioning. Brief renal ischemia and reperfusion applied before coronary artery reperfusion reduces myocardial infarct size via endogenous activation of adenosine receptors. Basic Res Cardiol. 2005 ; 100 (5). 404-412
59. Schmidt MR, Smerup M, Konstantinov IE, et al. Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: first demonstration of remote ischemic perconditioning. Am J Physiol. 2007 ; 292 (4). H1883 - H1890
60. Haunsenloy DJ, Mwamure P, Venugopal V, et al. Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomized controlled trial. Lancet. 2007 ; 370 (9587). 575-579
61. Bøtker HE, Kharbanda R, Schmidt MR, et al. Remote ischaemic conditioning before hospital admission as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomized trial. Lancet. 2010 ; 375 (9716). 727-734
62. Heush G. Cardioprotection: chances and challenges of its translation to the clinic. Lancet. 2013 ; 381 (9861). 166-175
63. Wolfrum S, Schneider K, Heidbreder M, Nienstedt J, Dominiak P, Dendorfer A. Remote preconditioning protects the heart by activating myocardial PKCâ̂Š -isoform. Cardiovasc Res. 2002 ; 55 (3). 590-601
64. Weinbrenner C, Nelles M, Herzog N, Sarvary L, Strasser RH. Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: a newly identified non-neuronal but PKC-dependent pathway. Cardiovasc Res. 2002 ; 55 (3). 590-601
65. Zatta AJ, Kin H, Lee G, et al. Infarct-sparing effect of myocardial postconditioning is dependent on protein kinase C signaling. Cardiovasc Res. 2006 ; 70 (2). 315-324
66. Philipp S, Yang XM, Cui L, Davis AM, Downey JM, Cohen MV. Postconditioning protects rabbit heart through a protein kinase C-adenosine A2b receptor cascade. Cardiovasc Res. 2006 ; 70 (2). 308-314