Cardiac vulnerability to ischemia/reperfusion injury drastically increases in late pregnancy

Basic Research in Cardiology

Volumn 107, Issue 4, 2012, Pages

  Li, Jingyuan ^a   Umar, Soban ^a   Iorga, Andrea ^a   Youn, Ji Youn ^a   Wang, Yibin ^a   Regitz Zagrosek, Vera ^b   Cai, Hua ^a   Eghbali, Mansoureh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Heart hypertrophy; Ischemia reperfusion; MPTP; Pregnancy; ROS

Indexed keywords

CALCIUM ION; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STAT3 PROTEIN; SUPEROXIDE; CALCIUM; CARRIER PROTEIN; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; HEART INFARCTION SIZE; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; IN VIVO STUDY; ISOLATED HEART; MITOCHONDRIAL PERMEABILITY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; THIRD TRIMESTER PREGNANCY; ANIMAL; C57BL MOUSE; CONVALESCENCE; DISEASE MODEL; DISEASE PREDISPOSITION; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART VENTRICLE PRESSURE; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PREGNANCY; PREGNANCY COMPLICATION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; CALCIUM; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEMALE; GLYCOGEN SYNTHASE KINASE 3; MICE; MICE, INBRED C57BL; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; OXIDATIVE STRESS; PHOSPHORYLATION; PREGNANCY; PREGNANCY COMPLICATIONS, CARDIOVASCULAR; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECOVERY OF FUNCTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR PRESSURE;

EID: 84861469940     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0271-7     Document Type: Article

References (72)

1. Abdallah Y, Gkatzoflia A, Gligorievski D et al (2006) Insulin protects cardiomyocytes against reoxygenation-induced hypercontracture by a survival pathway targeting SR Ca2? storage. Cardiovasc Res 70(2):346-353. doi:10.1016/j.cardiores.2006. 02.020
2. Birnbaum Y, Long B, Qian J, Perez-Polo JR, Ye Y (2011) Pioglitazone limits myocardial infarct size, activates Akt, and upregulates cPLA2 and COX-2 in a PPAR-gamma-independent manner. Basic Res Cardiol 106(3):431-446. doi:10.1007/ s00395-011-0162-3
3. Boengler K, Buechert A, Heinen Y et al (2008) Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res 102(1):131-135. doi:10.1007/s00395-010-0124-1
4. Boengler K, Hilfiker-Kleiner D, Drexler H, Heusch G, Schulz R (2008) The myocardial JAK/STAT pathway: From protection to failure. Pharmacol Ther 120(2):172-185. doi:10.1007/s00395-010-0124-1
5. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105(6):771-785. doi:10.1007/s00395-010-0124-1
6. Bopassa JC, Eghbali M, Toro L, Stefani E (2010) A novel estrogen receptor GPER inhibits mitochondria permeability transition pore opening and protects the heart against ischemiareperfusion injury. Am J Physiol Heart Circ Physiol 298(1):H16-H23. doi:10.1152/ajpheart.00588.2009
7. Breivik L, Helgeland E, Aarnes EK, Mrdalj J, Jonassen AK (2011) Remote postconditioning by humoral factors in effluent from ischemic preconditioned rat hearts is mediated via PI3K/ Akt-dependent cell-survival signaling at reperfusion. Basic Res Cardiol 106(1):135-145
8. Callies F, Stromer H, Schwinger RH et al (2003) Administration of testosterone is associated with a reduced susceptibility to myocardial ischemia. Endocrinology 144(10):4478-4483
9. Cantor EJ, Babick AP, Vasanji Z, Dhalla NS, Netticadan T (2005) A comparative serial echocardiographic analysis of cardiac structure and function in rats subjected to pressure or volume overload. J Mol Cell Cardiol 38(5):777-786. doi:10.1016/j. yjmcc.2005.02.012
10. Cao W, Xie YH, Li XQ et al (2011) Burn-induced apoptosis of cardiomyocytes is survivin dependent and regulated by PI3K/Akt, p38 MAPK and ERK pathways. Basic Res Cardiol 106(6): 1207-1220. doi:10.1007/s00395-011-0199-3
11. Carabello BA (2002) Concentric versus eccentric remodeling. J Card Fail 8(6 Suppl):S258-S263. doi:10.1054/jcaf.2002.129250
12. Chalupsky K, Cai H (2005) Endothelial dihydrofolate reductase: Critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 102(25):9056-9061. doi:10.1073/pnas.0409594102
13. Chapman AB, Abraham WT, Zamudio S et al (1998) Temporal relationships between hormonal and hemodynamic changes in early human pregnancy. Kidney Int 54(6):2056-2063
14. Christian TF, Schwartz RS, Gibbons RJ (1992) Determinants of infarct size in reperfusion therapy for acute myocardial infarction. Circulation 86(1):81-90. doi:10.1161/01.CIR.86.1.81
15. Cohen MV, Yang XM, Downey JM (2008) Acidosis, oxygen, and interference with mitochondrial permeability transition pore formation in the early minutes of reperfusion are critical to postconditioning's success. Basic Res Cardiol 103(5):464-471. doi: 10.1007/s00395-008-0737-9
16. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem J 341(Pt 2):233-249
17. Daniels SR, Meyer RA, Liang YC, Bove KE (1988) Echocardiographically determined left ventricular mass index in normal children, adolescents and young adults. J Am Coll Cardiol 12(3):703-708
18. Eghbali M, Deva R, Alioua A et al (2005) Molecular and functional signature of heart hypertrophy during pregnancy. Circ Res 96(11):1208-1216. doi:10.1161/01.RES.0000170652.71414.16
19. Eghbali M, Wang Y, Toro L, Stefani E (2006) Heart hypertrophy during pregnancy: A better functioning heart? Trends Cardiovasc Med 16(8):285-291. doi:10.1016/j.tcm.2006.07.001
20. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K (2000) Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101(6):660-667. doi:10.1161/01.CIR.101.6.660
21. Ghaboura N, Tamareille S, Ducluzeau PH et al (2011) Diabetes mellitus abrogates erythropoietin-induced cardioprotection against ischemic-reperfusion injury by alteration of the RISK/ GSK-3beta signaling. Basic Res Cardiol 106(1):147-162. doi: 10.1007/s00395-010-0130-3
22. Gomez L, Paillard M, Thibault H, Derumeaux G, Ovize M (2008) Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 117(21):2761-2768. doi:10.1161/ CIRCULATIONAHA.107.755066
23. Halestrap AP, Clarke SJ, Javadov SA (2004) Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 61(3):372-385. doi: 10.1016/S0008-6363(03) 00533-9
24. Halestrap AP, Kerr PM, Javadov S, Woodfield KY (1998) Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim Biophys Acta 1366(1-2):79-94
25. Hausenloy DJ, Lecour S, Yellon DM (2011) Reperfusion injury salvage kinase and survivor activating factor enhancement prosurvival signaling pathways in ischemic postconditioning: Two sides of the same coin. Antioxid Redox Signal 14(5):893-907. doi:10.1089/ars.2010.3360
26. Hausenloy DJ, Ong SB, Yellon DM (2009) The mitochondrial permeability transition pore as a target for preconditioning and postconditioning. Basic Res Cardiol 104(2):189-202. doi: 10.1007/s00395-009-0010-x
27. Hausenloy DJ, Tsang A, Mocanu MM, Yellon DM (2005) Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288(2):H971-H976. doi:10.1152/ajpheart.00374.2004
28. Heusch G, Boengler K, Schulz R (2010) Inhibition of mitochondrial permeability transition pore opening: The Holy Grail of cardioprotection. Basic Res Cardiol 105(2):151-154. doi: 10.1007/s00395-009-0080-9
29. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: Nitric oxide, protein kinases, and mitochondria. Circulation 118(19): 1915-1919. doi:10.1161/CIRCULATIONAHA.108.805242
30. Heusch G, Musiolik J, Gedik N, Skyschally A (2011) Mitochondrial STAT3 activation and cardioprotection by ischemic postconditioning in pigs with regional myocardial ischemia/ reperfusion. Circ Res 109(11):1302-1308. doi:10.1161/ CIRCRESAHA.111.255604
31. Hilfiker-Kleiner D, Kaminski K, Podewski E et al (2007) A cathepsin D-cleaved 16 kDa form of prolactin mediates postpartum cardiomyopathy. Cell 128(3):589-600. doi:10.1016/j. cell.2006.12.036
32. James AH, Jamison MG, Biswas MS, Brancazio LR, Swamy GK, MyersER(2006)Acutemyocardial infarction in pregnancy: AUnited States population-based study. Circulation 113(12):1564-1571. doi: 10.1161/ CIRCULATIONAHA.105.576751
33. James PR (2001) Drugs in pregnancy. Cardiovascular disease. Best Pract Res Clin Obstet Gynaecol 15(6):903-911. doi: 10.1053/beog.2001.0237
34. Jin ZQ, Goetzl EJ, Karliner JS (2004) Sphingosine kinase activation mediates ischemic preconditioning in murine heart. Circulation 110(14):1980-1989. doi:10.1161/01.CIR.0000143632. 06471.93
35. Kam KW, Qi JS, Chen M, Wong TM (2004) Estrogen reduces cardiac injury and expression of beta1-adrenoceptor upon ischemic insult in the rat heart. J Pharmacol Exp Ther 309(1):8-15. doi:10.1124/jpet.103.058339
36. Keeley EC, Boura JA, Grines CL (2003) Primary angioplasty versus intravenous thrombolytic therapy for acute myocardial infarction: A quantitative review of 23 randomised trials. Lancet 361(9351):13-20. doi:10.1016/S0140- 6736(03)12113-7
37. Kelly RF, Lamont KT, Somers S et al (2010) Ethanolamine is a novel STAT-3 dependent cardioprotective agent. Basic Res Cardiol 105(6):763-770. doi:10.1007/s00395-010-0125-0
38. Kevin LG, Novalija E, Stowe DF (2005) Reactive oxygen species as mediators of cardiac injury and protection: The relevance to anesthesia practice. Anesth Analg 101(5):1275-1287. doi: 10.1213/01.ANE.0000180999.81013
39. Korge P, Ping P, Weiss JN (2008) Reactive oxygen species production in energized cardiac mitochondria during hypoxia/ reoxygenation: Modulation by nitric oxide. Circ Res 103(8):873-880. doi:10.1161/CIRCRESAHA.108.180869
40. Kuch M, Janiszewski M, Mamcarz A, Cudnoch-Jedrzejewska A, Dluzniewski M (2009) Major adverse cardiac event predictors in survivors of myocardial infarction with asymptomatic left ventricular dysfunction or chronic heart failure. Med Sci Monit 15(6):H40-H48
41. Lacerda L, Somers S, Opie LH, Lecour S (2009) Ischaemic postconditioning protects against reperfusion injury via the SAFE pathway. Cardiovasc Res 84(2):201-208. doi:10.1093/cvr/cvp274
42. Ladner HE, Danielsen B, Gilbert WM (2005) Acute myocardial infarction in pregnancy and the puerperium: A population-based study. Obstet Gynecol 105(3):480-484. doi:10.1097/01.AOG. 0000151998.50852.31
43. Lecour S (2009) Multiple protective pathways against reperfusion injury: A SAFE path without Aktion? J Mol Cell Cardiol 46(5): 607-609. doi:10.1016/j.yjmcc.2009.01.003
44. Lemasters JJ, Qian T, He L et al (2002) Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal 4(5):769-781. doi: 10.1089/152308602760598918
45. Madamanchi NR, Runge MS (2007) Mitochondrial dysfunction in atherosclerosis. Circ Res 100(4):460-473. doi:10.1161/01. RES.0000258450.44413. 96
46. Matsui T, Tao J, del Monte F et al (2001) Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation 104(3):330-335. doi:10.1161/01. CIR.104.3.330
47. Nahrendorf M, Frantz S, Hu K et al (2003) Effect of testosterone on post-myocardial infarction remodeling and function. Cardiovasc Res 57(2):370-378. doi:10.1016/S0008-6363(02)00701-0
48. Nam UH, Wang M, Crisostomo PR et al (2007) The effect of chronic exogenous androgen on myocardial function following acute ischemia-reperfusion in hosts with different baseline levels of sex steroids. J Surg Res 142(1):113-118. doi:10.1016/j.jss. 2006.11.019
49. Oak JH, Cai H (2007) Attenuation of angiotensin II signaling recouples eNOS and inhibits nonendothelial NOX activity in diabetic mice. Diabetes 56(1):118-126
50. Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ (2010) Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 121(18): 2012-2022. doi:10.1161/CIRCULATIONAHA.109.906610
51. Pedretti S, Raddatz E (2011) STAT3alpha interacts with nuclear GSK3beta and cytoplasmic RISK pathway and stabilizes rhythm in the anoxic-reoxygenated embryonic heart. Basic Res Cardiol 106(3):355-369. doi:10.1007/s00395-011-0152-5
52. Penpargkul S, Scheuer J (1970) The effect of physical training upon the mechanical and metabolic performance of the rat heart. J Clin Invest 49(10):1859-1868
53. Pluim BM, Zwinderman AH, van der Laarse A, van der Wall EE (2000) The athlete's heart. A meta-analysis of cardiac structure and function. Circulation 101(3):336-344. doi:10.1161/01.CIR. 101.3.336
54. Rahman S, Li J, Bopassa JC et al (2011) Phosphorylation of GSK-3beta mediates intralipid-induced cardioprotection against ischemia/reperfusion injury. Anesthesiology 115(2):242-253. doi:10.1097/ALN.0b013e318223b8b9
55. Riedhammer HH, Rafflenbeul W, Weihe WH, Krayenbuhl HP (1976) Left ventricle contractile function in trained dogs with cardial hypertrophy. Basic Res Cardiol 71(3):297-308
56. Robson SC, Dunlop W, Moore M, Hunter S (1987) Combined Doppler and echocardiographic measurement of cardiac output: Theory and application in pregnancy. Br J Obstet Gynaecol 94(11):1014-1027
57. Roth A, Elkayam U (1996) Acute myocardial infarction associated with pregnancy. Ann Intern Med 125(9):751-762
58. Roth A, Elkayam U (2008) Acute myocardial infarction associated with pregnancy. J Am Coll Cardiol 52(3):171-180. doi: 10.1016/j.jacc.2008.03.049
59. Rottlaender D, Boengler K, Wolny M et al (2010) Connexin 43 acts as a cytoprotective mediator of signal transduction by stimulating mitochondrial KATP channels in mouse cardiomyocytes. J Clin Invest 120(5):1441-1453. doi:10.1172/JCI40927
60. Rottlaender D, Boengler K, Wolny M et al (2012) Glycogen synthase kinase 3beta transfers cytoprotective signaling through connexin 43 onto mitochondrial ATP-sensitive K? channels. Proc Natl Acad Sci USA 109(5):E242-E251. doi:10.1073/pnas. 1107479109
61. Saito T, Ciobotaru A, Bopassa JC, Toro L, Stefani E, Eghbali M (2009) Estrogen contributes to gender differences in mouse ventricular repolarization. Circ Res 105(4):343-352. doi: 10.1161/CIRCRESAHA.108.190041
62. Schannwell CM, Zimmermann T, Schneppenheim M, Plehn G, Marx R, Strauer BE (2002) Left ventricular hypertrophy and diastolic dysfunction in healthy pregnant women. Cardiology 97(2):73-78
63. Skyschally A, van Caster P, Boengler K et al (2009) Ischemic postconditioning in pigs: No causal role for RISK activation. Circ Res 104(1):15-18. doi:10.1161/CIRCRESAHA.108.186429
64. Suleman N, Somers S, Smith R, Opie LH, Lecour SC (2008) Dual activation of STAT-3 and Akt is required during the trigger phase of ischaemic preconditioning. Cardiovasc Res 79(1):127-133. doi:10.1093/cvr/cvn067
65. Tamareille S, Ghaboura N, Treguer F et al (2009) Myocardial reperfusion injury management: Erythropoietin compared with postconditioning. Am J Physiol Heart Circ Physiol 297(6): H2035-H2043. doi:10.1152/ajpheart.00472.2009
66. Toescu V, Nuttall SL, Martin U, Kendall MJ, Dunne F (2002) Oxidative stress and normal pregnancy. Clin Endocrinol (Oxf) 57(5):609-613. doi:10.1046/j.1365-2265.2002.01638.x
67. Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: Shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681(2-3):134-149. doi:10.1016/j.mrrev. 2008.06.004
68. Yang XM, Krieg T, Cui L, Downey JM, Cohen MV (2004) NECA and bradykinin at reperfusion reduce infarction in rabbit hearts by signaling through PI3K, ERK, and NO. J Mol Cell Cardiol 36(3):411-421. doi:10.1016/j.yjmcc.2003.12.008
69. Youn JY, Wang T, Cai H (2009) An ezrin/calpain/PI3K/AMPK/ eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circ Res 104(1):50-59. doi: 10.1161/CIRCRESAHA.108.178467
70. Zhang J, Cai H (2010) Netrin-1 prevents ischemia/reperfusioninduced myocardial infarction via a DCC/ERK1/2/eNOS s1177/ NO/DCC feed-forward mechanism. J Mol Cell Cardiol 48(6):1060-1070. doi:10.1016/j.yjmcc.2009.11.020
71. Zhuo C, Wang Y, Wang X, Wang Y, Chen Y (2011) Cardioprotection by ischemic postconditioning is abolished in depressed rats: Role of Akt and signal transducer and activator of transcription-3. Mol Cell Biochem 346(1-2):39-47. doi:10.1007/ s11010-010-0589-0
72. Zoratti M, Szabo I (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241(2):139-176. doi:10.1016/ 0304-4157(95)00003-A