Activated protein C protects against myocardial ischemic/reperfusion injury through AMP-activated protein kinase signaling

Journal of Thrombosis and Haemostasis

Volumn 9, Issue 7, 2011, Pages 1308-1317

  Wang, J ^a   Yang, L ^b   Rezaie, A R ^b   Li, J ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activated protein C; AMPK signaling; Cardioprotection; Endothelial protein C receptor; Ischemia reperfusion; PAR 1

Indexed keywords

ACTIVATED PROTEIN C; CALCIUM ION; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; IN VIVO STUDY; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; SIGNAL TRANSDUCTION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CELLS, CULTURED; HEART; MAP KINASE SIGNALING SYSTEM; MICE; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NF-KAPPA B; PROTEIN C; SIGNAL TRANSDUCTION;

EID: 79959817748     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04331.x     Document Type: Article

References (42)

1. Esmon CT. Molecular events that control the protein C anticoagulant pathway. Thromb Haemost 1993; 70: 29-35.
2. Walker FJ, Fay PJ. Regulation of blood coagulation by the protein C system. FASEB J 1992; 6: 2561-7.
3. Taylor FB Jr, Chang A, Esmon CT, D'Angelo A, Vigano-D'Angelo S, Blick KE. Protein C prevents the coagulopathic and lethal effects of Escherichia coli infusion in the baboon. J Clin Invest 1987; 79: 918-25.
4. Taylor FB Jr, Stearns-Kurosawa DJ, Kurosawa S, Ferrell G, Chang AC, Laszik Z, Kosanke S, Peer G, Esmon CT. The endothelial cell protein C receptor aids in host defense against Escherichia coli sepsis. Blood 2000; 95: 1680-6.
5. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 2002; 296: 1880-2.
6. Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007; 109: 3161-72.
7. Joyce DE, Grinnell BW. Recombinant human activated protein C attenuates the inflammatory response in endothelium and monocytes by modulating nuclear factor-kappaB. Crit Care Med 2002; 30 (5 Suppl.): S288-93.
8. Finigan JH, Dudek SM, Singleton PA, Chiang ET, Jacobson JR, Camp SM, Ye SQ, Garcia JG. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 2005; 280: 17286-93.
9. Nick JA, Coldren CD, Geraci MW, Poch KR, Fouty BW, O'Brien J, Gruber M, Zarini S, Murphy RC, Kuhn K, Richter D, Kast KR, Abraham E. Recombinant human activated protein C reduces human endotoxin-induced pulmonary inflammation via inhibition of neutrophil chemotaxis. Blood 2004; 104: 3878-85.
10. Elphick GF, Sarangi PP, Hyun YM, Hollenbaugh JA, Ayala A, Biffl WL, Chung HL, Rezaie AR, McGrath JL, Topham DJ, Reichner JS, Kim M. Recombinant human activated protein C inhibits integrin-mediated neutrophil migration. Blood 2009; 113: 4078-85.
11. Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood 2005; 105: 3178-84.
12. Cheng T, Liu D, Griffin JH, Fernandez JA, Castellino F, Rosen ED, Fukudome K, Zlokovic BV. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat Med 2003; 9: 338-42.
13. Griffin JH, Fernandez JA, Liu D, Cheng T, Guo H, Zlokovic BV. Activated protein C and ischemic stroke. Crit Care Med 2004; 32 (5 Suppl.): S247-53.
14. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, Fisher CJ Jr. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001; 344: 699-709.
15. Guo H, Liu D, Gelbard H, Cheng T, Insalaco R, Fernandez JA, Griffin JH, Zlokovic BV. Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 2004; 41: 563-72.
16. Iwaki T, Cruz DT, Martin JA, Castellino FJ. A cardioprotective role for the endothelial protein C receptor in lipopolysaccharide-induced endotoxemia in the mouse. Blood 2005; 105: 2364-71.
17. Kerschen EJ, Fernandez JA, Cooley BC, Yang XV, Sood R, Mosnier LO, Castellino FJ, Mackman N, Griffin JH, Weiler H. Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C. J Exp Med 2007; 204: 2439-48.
18. Niessen F, Furlan-Freguia C, Fernandez JA, Mosnier LO, Castellino FJ, Weiler H, Rosen H, Griffin JH, Ruf W. Endogenous EPCR/aPC-PAR1 signaling prevents inflammation-induced vascular leakage and lethality. Blood 2009; 113: 2859-66.
19. Pirat B, Muderrisoglu H, Unal MT, Ozdemir H, Yildirir A, Yucel M, Turkoglu S. Recombinant human-activated protein C inhibits cardiomyocyte apoptosis in a rat model of myocardial ischemia-reperfusion. Coron Artery Dis 2007; 18: 61-6.
20. Loubele ST, Spek CA, Leenders P, van Oerle R, Aberson HL, Hamulyak K, Ferrell G, Esmon CT, Spronk HM, ten Cate H. Activated protein C protects against myocardial ischemia/reperfusion injury via inhibition of apoptosis and inflammation. Arterioscler Thromb Vasc Biol 2009; 29: 1087-92.
21. Medina P, Navarro S, Corral J, Zorio E, Roldan V, Estelles A, Santamaria A, Marin F, Rueda J, Bertina RM, Espana F. Endothelial protein C receptor polymorphisms and risk of myocardial infarction. Haematologica 2008; 93: 1358-63.
22. Li J, Miller EJ, Ninomiya-Tsuji J, Russell RR III, Young LH. AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing recruitment of p38 MAPK to TAB 1 in the ischemic heart. Circ Res 2005; 97: 872-9.
23. Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R, Young LH. Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 2008; 451: 578-82.
24. Jensen TE, Rose AJ, Jorgensen SB, Brandt N, Schjerling P, Wojtaszewski JF, Richter EA. Possible CaMKK-dependent regulation of AMPK phosphorylation and glucose uptake at the onset of mild tetanic skeletal muscle contraction. Am J Physiol Endocrinol Metab 2007; 292: E1308-17.
25. Zhao P, Wang J, Ma H, Xiao Y, He L, Tong C, Wang Z, Zheng Q, Dolence EK, Nair S, Ren J, Li J. A newly synthetic chromium complex-Chromium (d-phenylalanine)(3) activates AMP-activated protein kinase and stimulates glucose transport. Biochem Pharmacol 2009; 77: 1002-10.
26. Dong F, Zhang X, Yang X, Esberg LB, Yang H, Zhang Z, Culver B, Ren J. Impaired cardiac contractile function in ventricular myocytes from leptin-deficient ob/ob obese mice. J Endocrinol 2006; 188: 25-36.
27. Bae JS, Yang L, Manithody C, Rezaie AR. Engineering a disulfide bond to stabilize the calcium-binding loop of activated protein C eliminates its anticoagulant but not its protective signaling properties. J Biol Chem 2007; 282: 9251-9.
28. Yang L, Bae JS, Manithody C, Rezaie AR. Identification of a specific exosite on activated protein C for interaction with protease-activated receptor 1. J Biol Chem 2007; 282: 25493-500.
29. Young LH, Li J, Baron SJ, Russell RR. AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc Med 2005; 15: 110-8.
30. Domotor E, Benzakour O, Griffin JH, Yule D, Fukudome K, Zlokovic BV. Activated protein C alters cytosolic calcium flux in human brain endothelium via binding to endothelial protein C receptor and activation of protease activated receptor-1. Blood 2003; 101: 4797-801.
31. Bretschneider E, Uzonyi B, Weber AA, Fischer JW, Pape R, Lotzer K, Schror K. Human vascular smooth muscle cells express functionally active endothelial cell protein C receptor. Circ Res 2007; 100: 255-62.
32. Hurley RL, Anderson KA, Franzone JM, Kemp BE, Means AR, Witters LA. The Ca2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J Biol Chem 2005; 280: 29060-6.
33. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2005; 2: 21-33.
34. Ren J, Privratsky JR, Yang X, Dong F, Carlson EC. Metallothionein alleviates glutathione depletion-induced oxidative cardiomyopathy in murine hearts. Crit Care Med 2008; 36: 2106-16.
35. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2005; 2: 9-19.
36. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001; 108: 1167-1174.
37. Liu Y, Shepherd EG, Nelin LD. MAPK phosphatases - regulating the immune response. Nat Rev Immunol 2007; 7: 202-12.
38. Young LH. AMP-activated protein kinase conducts the ischemic stress response orchestra. Circulation 2008; 117: 832-40.
39. Mizutani A, Okajima K, Uchiba M, Noguchi T. Activated protein C reduces ischemia/reperfusion-induced renal injury in rats by inhibiting leukocyte activation. Blood 2000; 95: 3781-7.
40. Swantek JL, Cobb MH, Geppert TD. Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-alpha) translation: glucocorticoids inhibit TNF-alpha translation by blocking JNK/SAPK. Mol Cell Biol 1997; 17: 6274-82.
41. Mosnier LO, Zampolli A, Kerschen EJ, Schuepbach RA, Banerjee Y, Fernandez JA, Yang XV, Riewald M, Weiler H, Ruggeri ZM, Griffin JH. Hyperantithrombotic, noncytoprotective Glu149Ala-activated protein C mutant. Blood 2009; 113: 5970-8.
42. Guo H, Singh I, Wang Y, Deane R, Barrett T, Fernandez JA, Chow N, Griffin JH, Zlokovic BV. Neuroprotective activities of activated protein C mutant with reduced anticoagulant activity. Eur J Neurosci 2009; 29: 1119-30.