Activated protein C modulates cardiac metabolism and augments autophagy in the ischemic heart

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 9, 2012, Pages 1736-1744

  Costa, R ^a   Morrison, A ^a   Wang, J ^a   Manithody, C ^b   Li, J ^a   Rezaie, A R ^b  

^a UNIVERSITY AT BUFFALO   (United States)

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

Author keywords

AMPK; APC; Autophagy; Cardioprotection; GLUT4; Ischemia reperfusion

Indexed keywords

ACTIVATED PROTEIN C; ACTIVATED PROTEIN C 2CYS; FATTY ACID; GLUCOSE TRANSPORTER 4; MUTANT PROTEIN; UNCLASSIFIED DRUG; PROTEIN C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICOAGULATION; AUTOPHAGY; EX VIVO STUDY; GLUCOSE OXIDATION; GLUCOSE TRANSPORT; HEART MUSCLE FIBER MEMBRANE; HEART MUSCLE ISCHEMIA; HEART MUSCLE METABOLISM; HEART PROTECTION; IMMUNOBLOTTING; MALE; MOUSE; NONHUMAN; NOTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPERFUSION INJURY; SIGNAL TRANSDUCTION; ANIMAL; ARTICLE; HEART MUSCLE; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALS; HUMANS; MYOCARDIUM; PROTEIN C;

EID: 84865731953     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04833.x     Document Type: Note

References (57)

1. Bangalore S, Cohen DJ, Kleiman NS, Regev-Beinart T, Rao SV, Pencina MJ, Mauri L. Bleeding risk comparing targeted low-dose heparin with bivalirudin in patients undergoing percutaneous coronary intervention: results from a propensity score-matched analysis of the Evaluation of Drug-Eluting Stents and Ischemic Events (EVENT) registry. Circ Cardiovasc Interv 2011; 4: 463-73.
2. Ferdinandy P, Schulz R, Baxter GF. Interaction of cardiovascular risk factors with myocardial ischemia/reperfusion injury, preconditioning, and postconditioning. Pharmacol Rev 2007; 59: 418-58.
3. 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: 110-18.
4. Morrison A, Yan X, Tong C, Li J. Acute rosiglitazone treatment is cardioprotective against ischemia-reperfusion injury by modulating AMPK, Akt, and JNK signaling in nondiabetic mice. Am J Physiol Heart Circ Physiol 2011; 301: H895-902.
5. Turer AT, Hill JA. Pathogenesis of myocardial ischemia-reperfusion injury and rationale for therapy. Am J Cardiol 2010; 106: 360-8.
6. Wang J, Yang L, Rezaie AR, Li J. Activated protein C protects against myocardial ischemic/reperfusion injury through AMP-activated protein kinase signaling. J Thromb Haemost 2011; 9: 1308-17.
7. Rezaie AR. Exosite-dependent regulation of the protein C anticoagulant pathway. Trends Cardiovasc Med 2003; 13: 8-15.
8. Oganesyan V, Oganesyan N, Terzyan S, Qu D, Dauter Z, Esmon NL, Esmon CT. The crystal structure of the endothelial protein C receptor and a bound phospholipid. J Biol Chem 2002; 277: 24851-4.
9. Fukudome K, Kurosawa S, Stearns-Kurosawa DJ, He X, Rezaie AR, Esmon CT. The endothelial cell protein C receptor. Cell surface expression and direct ligand binding by the soluble receptor. J Biol Chem 1996; 271: 17491-8.
10. 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.
11. Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007; 109: 3161-72.
12. Russell RR III, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ, Young LH. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest 2004; 114: 495-503.
13. Kudo N, Gillespie JG, Kung L, Witters LA, Schulz R, Clanachan AS, Lopaschuk GD. Characterization of 5′AMP-activated protein kinase activity in the heart and its role in inhibiting acetyl-CoA carboxylase during reperfusion following ischemia. Biochim Biophys Acta 1996; 1301: 67-75.
14. Jorgensen SB, Nielsen JN, Birk JB, Olsen GS, Viollet B, Andreelli F, Schjerling P, Vaulont S, Hardie DG, Hansen BF, Richter EA, Wojtaszewski JF. The alpha2-5′AMP-activated protein kinase is a site 2 glycogen synthase kinase in skeletal muscle and is responsive to glucose loading. Diabetes 2004; 53: 3074-81.
15. Russell RR III, Bergeron R, Shulman GI, Young LH. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 1999; 277: H643-9.
16. Hardie DG, Carling D. The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur J Biochem 1997; 246: 259-73.
17. Nishida K, Kyoi S, Yamaguchi O, Sadoshima J, Otsu K. The role of autophagy in the heart. Cell Death Differ 2009; 16: 31-8.
18. He C, Bassik MC, Moresi V, Sun K, Wei Y, Zou Z, An Z, Loh J, Fisher J, Sun Q, Korsmeyer S, Packer M, May HI, Hill JA, Virgin HW, Gilpin C, Xiao G, Bassel-Duby R, Scherer PE, Levine B. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012; 481: 511-15.
19. Jaswal JS, Keung W, Wang W, Ussher JR, Lopaschuk GD. Targeting fatty acid and carbohydrate oxidation - a novel therapeutic intervention in the ischemic and failing heart. Biochim Biophys Acta 2011; 1813: 1333-50.
20. Lopaschuk GD, Barr R, Thomas PD, Dyck JR. Beneficial effects of trimetazidine in ex vivo working ischemic hearts are due to a stimulation of glucose oxidation secondary to inhibition of long-chain 3-ketoacyl coenzyme A thiolase. Circ Res 2003; 93: e33-7.
21. 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.
22. 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.
23. Miller EJ, Li J, Sinusas KM, Holman GD, Young LH. Infusion of a biotinylated bis-glucose photolabel: a new method to quantify cell surface GLUT4 in the intact mouse heart. Am J Physiol Endocrinol Metab 2007; 292: E1922-8.
24. Lopaschuk GD, Barr RL. Measurements of fatty acid and carbohydrate metabolism in the isolated working rat heart. Mol Cell Biochem 1997; 172: 137-47.
25. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19: 5720-8.
26. 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.
27. 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.
28. Matsui T, Tao J, del Monte F, Lee KH, Li L, Picard M, Force TL, Franke TF, Hajjar RJ, Rosenzweig A. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation 2001; 104: 330-5.
29. Rowland AF, Fazakerley DJ, James DE. Mapping insulin/GLUT4 circuitry. Traffic 2011; 12: 672-81.
30. Young LH. AMP-activated protein kinase conducts the ischemic stress response orchestra. Circulation 2008; 117: 832-40.
31. Behrend AM, Harding CO, Shoemaker JD, Matern D, Sahn DJ, Elliot DL, Gillingham MB. Substrate oxidation and cardiac performance during exercise in disorders of long chain fatty acid oxidation. Mol Genet Metab 2012; 105: 110-15.
32. Sciarretta S, Hariharan N, Monden Y, Zablocki D, Sadoshima J. Is autophagy in response to ischemia and reperfusion protective or detrimental for the heart? Pediatr Cardiol 2011; 32: 275-81.
33. Wang J, Ma H, Tong C, Zhang H, Lawlis GB, Li Y, Zang M, Ren J, Nijland MJ, Ford SP, Nathanielsz PW, Li J. Overnutrition and maternal obesity in sheep pregnancy alter the JNK-IRS-1 signaling cascades and cardiac function in the fetal heart. FASEB J 2010; 24: 2066-76.
34. Alers S, Loffler AS, Wesselborg S, Stork B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 2012; 32: 2-11.
35. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13: 132-41.
36. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011; 331: 456-61.
37. 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.
38. 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.
39. 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.
40. 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.
41. Kim AS, Miller EJ, Young LH. AMP-activated protein kinase: a core signalling pathway in the heart. Acta Physiol (Oxf) 2009; 196: 37-53.
42. Ramanjaneya M, Conner AC, Brown JE, Chen J, Digby JE, Barber TM, Randeva HS. Adiponectin (15-36) stimulates steroidogenic acute regulatory (StAR) protein expression and cortisol production in human adrenocortical cells: role of AMPK and MAPK kinase pathways. Biochim Biophys Acta 2011; 1813: 802-9.
43. Marsin AS, Bertrand L, Rider MH, Deprez J, Beauloye C, Vincent MF, van den Berghe G, Carling D, Hue L. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr Biol 2000; 10: 1247-55.
44. Kovacic S, Soltys CL, Barr AJ, Shiojima I, Walsh K, Dyck JR. Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. J Biol Chem 2003; 278: 39422-7.
45. Bae JS, Yang L, Rezaie AR. Receptors of the protein C activation and activated protein C signaling pathways are colocalized in lipid rafts of endothelial cells. Proc Natl Acad Sci USA 2007; 104: 2867-72.
46. Bae JS, Yang L, Manithody C, Rezaie AR. The ligand occupancy of endothelial protein C receptor switches the protease-activated receptor 1-dependent signaling specificity of thrombin from a permeability-enhancing to a barrier-protective response in endothelial cells. Blood 2007; 110: 3909-16.
47. Madhusudhan T, Wang H, Straub BK, Grone E, Zhou Q, Shahzad K, Muller-Krebs S, Schwenger V, Gerlitz B, Grinnell BW, Griffin JH, Reiser J, Grone HJ, Esmon CT, Nawroth PP, Isermann B. Cytoprotective signaling by activated protein C requires protease-activated receptor-3 in podocytes. Blood 2012; 119: 874-83.
48. Yang XV, Banerjee Y, Fernández JA, Deguchi H, Xu X, Mosnier LO, Urbanus RT, de Groot PG, White-Adams TC, McCarty OJ, Griffin JH. Activated protein C ligation of ApoER2 (LRP8) causes Dab1-dependent signaling in U937 cells. Proc Natl Acad Sci USA 2009; 106: 274-9.
49. Minhas N, Xue M, Fukudome K, Jackson CJ. Activated protein C utilizes the angiopoietin/Tie2 axis to promote endothelial barrier function. FASEB J 2010; 24: 873-81.
50. Morrison A, Li J. PPAR-gamma and AMPK - advantageous targets for myocardial ischemia/reperfusion therapy. Biochem Pharmacol 2011; 82: 195-200.
51. Makinde AO, Gamble J, Lopaschuk GD. Upregulation of 5′-AMP-activated protein kinase is responsible for the increase in myocardial fatty acid oxidation rates following birth in the newborn rabbit. Circ Res 1997; 80: 482-9.
52. Kantor PF, Lucien A, Kozak R, Lopaschuk GD. The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ Res 2000; 86: 580-8.
53. McCormack JG, Barr RL, Wolff AA, Lopaschuk GD. Ranolazine stimulates glucose oxidation in normoxic, ischemic, and reperfused ischemic rat hearts. Circulation 1996; 93: 135-42.
54. van Bilsen M, van Nieuwenhoven FA, van der Vusse GJ. Metabolic remodelling of the failing heart: beneficial or detrimental? Cardiovasc Res 2009; 81: 420-8.
55. Jin S, Zhou F, Katirai F, Li PL. Lipid raft redox signaling: molecular mechanisms in health and disease. Antioxid Redox Signal 2011; 15: 1043-83.
56. Hardie DG. AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 2011; 25: 1895-908.
57. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K. Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 2012; 485: 251-5.