Ischemic and hypoxic preconditioning protect cardiac muscles via intracellular ROS signaling
Received date: 19 Mar 2012
Accepted date: 10 Apr 2012
Published date: 01 Jun 2013
Copyright
Oxidative stress can cause extensive damage to cardiac tissue under reperfusion conditions. However, preconditioning the myocardium may diminish these negative effects and alleviate reperfusion injury. There are a variety of preconditioning therapies, such as ischemic preconditioning (IPC) and hypoxic preconditioning (HPC), each targeting specific channels, receptors, and/or intracellular molecules. Ischemic preconditioning involves brief periods of ischemia followed by brief periods of reperfusion, thus strengthening the cardiac resistance for a longer period of ischemia. IPC involves complex mechanisms, some of which are still not completely understood today. Nevertheless, many studies have already established models of IPC. In addition, similar to IPC, HPC has also been recognized as preventing reperfusion injury. Reactive oxygen species (ROS) are known mediators of IPC and HPC. Particularly, mitochondria-generated ROS initiate activity of several beneficial preconditioning pathways. The role of ROS is paradoxical; low levels of ROS are key factors in signaling IPC/HPC, but high levels of ROS can contribute to increased oxidative stress on cardiomyocytes. Therefore, it is important to determine the molecular mechanism of IPC and HPC to avoid excessive accumulation of ROS to prevent cardiac injury. In this review, we will outline IPC and HPC, explaining the putative role of ROS in both pathways. We will also discuss preconditioning efficacy in certain conditions such as exercise and how the aging myocardium responds to preconditioning therapies.
Key words： hypoxia; ischemia-reperfusion; ROS; cardiomyocyte; preconditioning
Li ZUO , William J. ROBERTS , Rosa C. TOLOMELLO , Adam T. GOINS . Ischemic and hypoxic preconditioning protect cardiac muscles via intracellular ROS signaling[J]. Frontiers in Biology, 2013 , 8(3) : 305 -311 . DOI: 10.1007/s11515-012-1225-z
| 1 |
Abete P, Ferrara N, Cacciatore F, Madrid A, Bianco S, Calabrese C, Napoli C, Scognamiglio P, Bollella O, Cioppa A, Longobardi G, Rengo F (1997). Angina-induced protection against myocardial infarction in adult and elderly patients: a loss of preconditioning mechanism in the aging heart? J Am Coll Cardiol, 30(4): 947-954
|
| 2 |
Abrahamsson T, Almgren O, Carlsson L (1985). Ischemia-induced local release of myocardial noradrenaline. J Cardiovasc Pharmacol, 7(Suppl 5): S19-S22
|
| 3 |
Ambrosio G, Zweier J L, Duilio C, Kuppusamy P, Santoro G, Elia P P, Tritto I, Cirillo P, Condorelli M, Chiariello M (1993). Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. J Biol Chem, 268(25): 18532-18541
|
| 4 |
Ascensão A, Ferreira R, Magalhães J (2007). Exercise-induced cardioprotection—biochemical, morphological and functional evidence in whole tissue and isolated mitochondria. Int J Cardiol, 117(1): 16-30
|
| 5 |
Atsma D E, Bastiaanse E M, Jerzewski A, Van der Valk L J, Van der Laarse A (1995). Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during metabolic inhibition. Circ Res, 76(6): 1071-1078
|
| 6 |
Behling R W, Malone H J (1995). KATP-channel openers protect against increased cytosolic calcium during ischaemia and reperfusion. J Mol Cell Cardiol, 27(9): 1809-1817
|
| 7 |
Bélichard P, Pruneau D, Rochette L (1987). Arterial hypertension, myocardial hypertrophy and disorders of cardiac rhythm induced by ligation of the left coronary artery in the rat. Arch Mal Coeur Vaiss, 80(6): 883-887
|
| 8 |
Boengler K, Schulz R, Heusch G (2009). Loss of cardioprotection with ageing. Cardiovasc Res, 83(2): 247-261
|
| 9 |
Braunwald E, Kloner R A (1985). Myocardial reperfusion: a double-edged sword? J Clin Invest, 76(5): 1713-1719
|
| 10 |
Brookes P S, Yoon Y, Robotham J L, Anders M W, Sheu S S (2004). Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol, 287(4): C817-C833
|
| 11 |
Cai Z, Zhong H, Bosch-Marce M, Fox-Talbot K, Wang L, Wei C, Trush M A, Semenza G L (2008). Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1 alpha. Cardiovasc Res, 77(3): 463-470
|
| 12 |
Carlsson L, Abrahamsson T, Almgren O (1985). Local release of myocardial norepinephrine during acute ischemia: an experimental study in the isolated perfused rat heart. J Cardiovasc Pharmacol, 7(4): 791-798
|
| 13 |
Carrasco A J, Dzeja P P, Alekseev A E, Pucar D, Zingman L V, Abraham M R, Hodgson D, Bienengraeber M, Puceat M, Janssen E, Wieringa B, Terzic A (2001). Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc Natl Acad Sci USA, 98(13): 7623-7628
|
| 14 |
Chen C F, Tsai S Y, Ma M C, Wu M S (2003). Hypoxic preconditioning enhances renal superoxide dismutase levels in rats. J Physiol, 552(2): 561-569
|
| 15 |
Crawford R M, Ranki H J, Botting C H, Budas G R, Jovanovic A (2002). Creatine kinase is physically associated with the cardiac ATP-sensitive K+ channel in vivo. FASEB J, 16(1): 102-104
|
| 16 |
Davies K J (1995). Oxidative stress: the paradox of aerobic life. Biochem Soc Symp, 61: 1-31
|
| 17 |
Dhalla N S, Elmoselhi A B, Hata T, Makino N (2000a). Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res, 47(3): 446-456
|
| 18 |
Dhalla N S, Temsah R M, Netticadan T (2000b). Role of oxidative stress in cardiovascular diseases. J Hypertens, 18(6): 655-673
|
| 19 |
Downey J M, Krieg T, Cohen M V (2008). Mapping preconditioning’s signaling pathways: an engineering approach. Ann N Y Acad Sci, 1123(1): 187-196
|
| 20 |
Duranteau J, Chandel N S, Kulisz A, Shao Z, Schumacker P T (1998). Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J Biol Chem, 273(19): 11619-11624
|
| 21 |
Elmoselhi A B, Lukas A, Ostadal P, Dhalla N S (2003). Preconditioning attenuates ischemia-reperfusion-induced remodeling of Na+-K+-ATPase in hearts. Am J Physiol Heart Circ Physiol, 285(3): H1055-H1063
|
| 22 |
Fryer R M, Eells J T, Hsu A K, Henry M M, Gross G J (2000). Ischemic preconditioning in rats: role of mitochondrial K(ATP) channel in preservation of mitochondrial function. Am J Physiol Heart Circ Physiol, 278(1): H305-H312
|
| 23 |
Garlid K D, Paucek P, Yarov-Yarovoy V, Sun X, Schindler P A (1996). The mitochondrial KATP channel as a receptor for potassium channel openers. J Biol Chem, 271(15): 8796-8799
|
| 24 |
Giordano F J (2005). Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest, 115(3): 500-508
|
| 25 |
Gopalakrishna R, Anderson W B (1989). Ca2+- and phospholipid-independent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc Natl Acad Sci USA, 86(17): 6758-6762
|
| 26 |
Gross G J, Hsu A, Falck J R, Nithipatikom K (2007). Mechanisms by which epoxyeicosatrienoic acids (EETs) elicit cardioprotection in rat hearts. J Mol Cell Cardiol, 42(3): 687-691
|
| 27 |
Halestrap A P (1989). The regulation of the matrix volume of mammalian mitochondria in vivo and in vitro and its role in the control of mitochondrial metabolism. Biochim Biophys Acta, 973(3): 355-382
|
| 28 |
Hamilton K L, Staib J L, Phillips T, Hess A, Lennon S L, Powers S K (2003). Exercise, antioxidants, and HSP72: protection against myocardial ischemia/reperfusion. Free Radic Biol Med, 34(7): 800-809
|
| 29 |
Hekimi S, Lapointe J, Wen Y (2011). Taking a “good” look at free radicals in the aging process. Trends Cell Biol, 21(10): 569-576
|
| 30 |
Huang Y, Hickey R P, Yeh J L, Liu D, Dadak A, Young L H, Johnson R S, Giordano F J (2004). Cardiac myocyte-specific HIF-1alpha deletion alters vascularization, energy availability, calcium flux, and contractility in the normoxic heart. FASEB J, 18(10): 1138-1140
|
| 31 |
Jaffe M D, Quinn N K (1980). Warm-up phenomenon in angina pectoris. Lancet, 316(8201): 934-936
|
| 32 |
Juhaszova M, Zorov D B, Kim S H, Pepe S, Fu Q, Fishbein K W, Ziman B D, Wang S, Ytrehus K, Antos C L, Olson E N, Sollott S J (2004). Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest, 113(11): 1535-1549
|
| 33 |
Kim M S, Akera T (1987). O2 free radicals: cause of ischemia-reperfusion injury to cardiac Na+-K+-ATPase. Am J Physiol, 252(2 Pt 2): H252-H257
|
| 34 |
Kloner R A, Jennings R B (2001). Consequences of brief ischemia: stunning, preconditioning, and their clinical implications: part 2. Circulation, 104(25): 3158-3167
|
| 35 |
Lemasters J J, Theruvath T P, Zhong Z, Nieminen A L (2009). Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta, 1787(11): 1395-1401
|
| 36 |
Light P E, Sabir A A, Allen B G, Walsh M P, French R J (1996). Protein kinase C-induced changes in the stoichiometry of ATP binding activate cardiac ATP-sensitive K+ channels. A possible mechanistic link to ischemic preconditioning. Circ Res, 79(3): 399-406
|
| 37 |
McArdle F, Spiers S, Aldemir H, Vasilaki A, Beaver A, Iwanejko L, McArdle A, Jackson M J (2004). Preconditioning of skeletal muscle against contraction-induced damage: the role of adaptations to oxidants in mice. J Physiol, 561(1): 233-244
|
| 38 |
Murphy E, Steenbergen C (2007). Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res, 75(3): 478-486
|
| 39 |
Nayler W G, Elz J S (1986). Reperfusion injury: laboratory artifact or clinical dilemma? Circulation, 74(2): 215-221
|
| 40 |
Opie L H (1992). Cardiac metabolism—emergence, decline, and resurgence`. Part II. Cardiovasc Res, 26(9): 817-830
|
| 41 |
Osada M, Takeda S, Sato T, Komori S, Tamura K (1994). The protective effect of preconditioning on reperfusion-induced arrhythmia is lost by treatment with superoxide dismutase. Jpn Circ J, 58(4): 259-263
|
| 42 |
Pagliaro P, Gattullo D, Rastaldo R, Losano G (2001). Ischemic preconditioning: from the first to the second window of protection. Life Sci, 69(1): 1-15
|
| 43 |
Park J W, Chun Y S, Kim Y H, Kim C H, Kim M S (1997). Ischemic preconditioning reduces Op6 generation and prevents respiratory impairment in the mitochondria of post-ischemic reperfused heart of rat. Life Sci, 60(24): 2207-2219
|
| 44 |
Peternelj T T, Coombes J S (2011). Antioxidant supplementation during exercise training: beneficial or detrimental? Sports Med, 41(12): 1043-1069
|
| 45 |
Rose G, Crocco P, De Rango F, Montesanto A, Passarino G (2011). Further support to the uncoupling-to-survive theory: the genetic variation of human UCP genes is associated with longevity. PLoS ONE, 6(12): e29650
|
| 46 |
Saini H K, Machackova J, Dhalla N S (2004). Role of reactive oxygen species in ischemic preconditioning of subcellular organelles in the heart. Antioxid Redox Signal, 6(2): 393-404
|
| 47 |
Sanada S, Komuro I, Kitakaze M (2011). Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures. Am J Physiol Heart Circ Physiol, 301(5): H1723-H1741
|
| 48 |
Stubbs S L, Hsiao S T, Peshavariya H, Lim S Y, Dusting G J, Dilley R J (2012) Hypoxic preconditioning enhances survival of human adipose-derived stem cells and conditions endothelial cells in vitro. Stem Cells Dev, Available online in Januaryβ27, 2012
|
| 49 |
Suzuki M, Sasaki N, Miki T, Sakamoto N, Ohmoto-Sekine Y, Tamagawa M, Seino S, Marbán E, Nakaya H (2002). Role of sarcolemmal K(ATP) channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest, 109(4): 509-516
|
| 50 |
Tanaka M, Fujiwara H, Yamasaki K, Sasayama S (1994). Superoxide dismutase and N-2-mercaptopropionyl glycine attenuate infarct size limitation effect of ischaemic preconditioning in the rabbit. Cardiovasc Res, 28(7): 980-986
|
| 51 |
Turrell H E, Rodrigo G C, Norman R I, Dickens M, Standen N B (2011). Phenylephrine preconditioning involves modulation of cardiac sarcolemmal K(ATP) current by PKC delta, AMPK and p38 MAPK. J Mol Cell Cardiol, 51(3): 370-380
|
| 52 |
Vanden Hoek T L, Becker L B, Shao Z, Li C, Schumacker P T (1998). Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem, 273(29): 18092-18098
|
| 53 |
Wojtovich A P, Brookes P S (2008). The endogenous mitochondrial complex II inhibitor malonate regulates mitochondrial ATP-sensitive potassium channels: implications for ischemic preconditioning. Biochim Biophys Acta, 1777(7-8): 882-889
|
| 54 |
Wojtovich A P, Nadtochiy S M, Brookes P S, Nehrke K (2012). Ischemic preconditioning: the role of mitochondria and aging. Exp Gerontol, 47(1): 1-7
|
| 55 |
Yang X, Cohen M V, Downey J M (2010). Mechanism of cardioprotection by early ischemic preconditioning. Cardiovasc Drugs Ther, 24(3): 225-234
|
| 56 |
Yuan G J, Ma J C, Gong Z J, Sun X M, Zheng S H, Li X (2005). Modulation of liver oxidant-antioxidant system by ischemic preconditioning during ischemia/reperfusion injury in rats. World J Gastroenterol, 11(12): 1825-1828
|
| 57 |
Zuo L, Chen Y R, Reyes L A, Lee H L, Chen C L, Villamena F A, Zweier J L (2009). The radical trap 5,5-dimethyl-1-pyrroline N-oxide exerts dose-dependent protection against myocardial ischemia-reperfusion injury through preservation of mitochondrial electron transport. J Pharmacol Exp Ther, 329(2): 515-523
|
| 58 |
Zuo L, Pasniciuc S, Wright V P, Merola A J, Clanton T L (2003). Sources for superoxide release: lessons from blockade of electron transport, NADPH oxidase, and anion channels in diaphragm. Antioxid Redox Signal, 5(5): 667-675
|
/
| 〈 |
|
〉 |