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Role of ATP-Sensitive K+ Channels in Cardiac Preconditioning

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Potassium Channels in Cardiovascular Biology

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Abstract

Ischemic preconditioning (IPC) is a phenomenon by which a brief period of ischemia or hypoxia can result in an adaptive cardioprotective effect when the myocardium is subjected to a more prolonged ischemic insult. IPC occurs in all animals studied as well as in humans and has two phases, an early phase that lasts for 1–2 h following the IPC stimulus and a delayed phase or second window of protection (SWOP) that appears 12–24 h after IPC and lasts for 48–72 h (Przyklenk and Kloner, 1998). A number of mediators (i.e., adenosine, bradykinin, and opioids) and signaling pathways [i.e., tyrosine kinase (TK) and protein kinase C (PKC)] are involved in triggering the transduction of the preconditioning stimulus to the appropriate end effector in the heart. The end effector is most likely an enzyme, a small heat-shock protein (HSP), or an ion channel. The majority of evidence suggests that the ATP-sensitive potassium channel (KATP channel) is the end effector of both early and delayed IPC and pharmacologically induced preconditioning, and information will be presented to support this hypothesis. Recently, controversy has arisen as to whether the KATP channel subtype is responsible for the preconditioning effect is the surface or sarcolemmal channel (sarc KATP) or the mitochondrial channel (mito KATP), and evidence will be presented both for and against a role for these channel subtypes in classical or delayed IPC. Theories will also be presented concerning the mechanisms by which opening of the sarc KATP or mito KATP channels produces the cardioprotective effect of IPC. Finally, a comment will be made concerning future directions and questions that still need to be answered as to the role and function of the KATP channel in cardiac preconditioning.

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References

  • Aguilar-Bryan, L., Clement, J. P., IV, Gonzalez, G., Kunjilwar, K., Babenko, A., and Bryan, J., 1998, Toward understanding the assembly and structure of KATP channels, Physiol. Rev. 78:227–245.

    PubMed  CAS  Google Scholar 

  • Armstrong, S. C., Liu, G. S., Downey, J. M., and Ganote, C. E., 1995, Potassium channels and preconditioning of isolated rabbit cardiomyocytes: Effects of glyburide and pinacidil, J. Mol. Cell. Cardiol. 27:1765–1774.

    Article  PubMed  CAS  Google Scholar 

  • Auchampach, J. A., and Gross, G. J., 1993, Adenosine A1 receptors, KATP channels and ischemic preconditioning in dogs, Am. J. Physiol. 224:H1327–H1336.

    Google Scholar 

  • Auchampach, J. A., Grover, G. J., and Gross, G. J., 1992, Blockade of ischemic preconditioning in dogs by the novel ATP dependent potassium channel antagonist 5-hydroxydecanoate, Cardiovasc. Res. 26:1054–1062.

    Article  PubMed  CAS  Google Scholar 

  • Baxter, G. F., Marber, M. S., Patel, V. C., and Yellon, D. M., 1994, Adenosine receptor involvement in a delayed phase of protection 24 hours following ischemic preconditioning, Circulation 90:2993–3000.

    Article  PubMed  CAS  Google Scholar 

  • Cleveland, J. C., Jr., Meldrum, D. A. Rowland, R. T., Banerjee, A., and Harken, A. H., 1997a, Adenosine preconditioning of human myocardium is dependent upon the ATP-sensitive K+ channel, J. Mol. Cell. Cardiol. 29:175–182.

    Article  PubMed  CAS  Google Scholar 

  • Cleveland, J. C., Jr., Meldrum, D. R., Cain, B. S., Banerjee, A., and Harken A. H., 1997b,Oral sulfonylurea hypoglycemic agents prevent ischemic preconditioning in human myocardium, Circulation 96:29–32.

    Article  PubMed  CAS  Google Scholar 

  • Cole, W. G., McPherson, C. D., and Sontag, D., 1991, ATP-regulated K+ channels protect the myocardium against ischemia-reperfusion damage, Circ. Res. 69:571–581.

    Article  PubMed  CAS  Google Scholar 

  • Deutsch, E., Berger, M., Kussmaul, W. G., Hirshfeld, J. W., Jr., Herrmann, H. C., and Laskey, W. K., 1990, Adaptation to ischemia during percutaneous transluminal coronary angioplasty: Clinical, hemodynamic, and metabolic features, Circulation 82:2044–2051.

    Article  PubMed  CAS  Google Scholar 

  • Elliott, G. T., Comerford, M. L., Smith, J. R., and Zhao, L., 1996, Myocardial ischemia/reperfusion protection using monophosphoryl lipid A is abrogated by the ATP-sensitive potassium channel blocker, gliben-clamide, Cardiovasc. Res. 32:1071–1080.

    Article  PubMed  CAS  Google Scholar 

  • Fryer, R. M., Schultz, J. J., Hsu, A. K., and Gross, G. J., 1998, Pretreatment with tyrosine kinase inhibitors partially attenuates ischemic preconditioning in rat hearts, Am. J. Physiol. 275:H2009–H2015.

    PubMed  CAS  Google Scholar 

  • Garlid, K. D., Paucek, P., Yarov-Yarovy, V., Murray, H. N., Darbenzio, R. B., D’Alonso, A. J., Lodge, N. J., Smith, M. A., and Grover, G. J., 1997, Cardioprotective effect of diazoxide and its interaction with mitochondrial ATP- sensitive K+ channels: Possible mechanism of cardioprotection, Circ. Res. 81:1072– 1082.

    Article  PubMed  CAS  Google Scholar 

  • Gogelein, H., Hartung, J., Englert, H. C., and Scholkens, B., 1998, HMR 1883, a novel cardioprotective inhibitor of the ATP-sensitive potassium channel. Part I: Effects on cardiomyocytes, coronary flow and pancreatic β-cells, J. Pharmacol. Exp. Ther. 286:1453–1464.

    PubMed  CAS  Google Scholar 

  • Grimmsmann, T., and Rustenbeck, I., 1998, Direct effects of diazoxide on mitochondria in pancreatic β-cells and on isolated liver mitochondria, Br. J. Pharmacol 123:781–788.

    Article  PubMed  CAS  Google Scholar 

  • Gross, G. J., and Auchampach, J. A., 1992, Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs, Circ. Res. 70:223–233.

    Article  PubMed  CAS  Google Scholar 

  • Grover, G. J., Sleph, P. G., and Dzwonczyk, S., 1992, Role of myocardial ATP-sensitive potassium channels in mediating preconditioning in the dog heart and their possible interaction with adenosine A1 receptors, Circulation 86:1310–1316.

    Article  PubMed  CAS  Google Scholar 

  • Grover, G. J., D’Alonso, A. J., Hess, T., Sleph, P. G., and Darbenzio, R. B., 1995, Glyburide-reversible cardioprotective effect of BMS-180448 is independent of action potential shortening, Cardiovasc. Res. 30:731–738.

    PubMed  CAS  Google Scholar 

  • Grover, G. J., D’Alonso, A. J., Dzwonczyk, S., Parham, C. S., and Darbenzio, R. B., 1996, Preconditioning is not abolished by the delayed rectifier K+ blocker dofetilide, Am. J. Physiol. 271:H1207–H1214.

    PubMed  CAS  Google Scholar 

  • Haessler, R., Kuzume, K., Chien, G. L., Wolff, R. A., Davis, R. F., and Van Winkle, D. M., 1994, Anaesthetics alter the magnitude of infarct limitation by ischaemic preconditioning, Cardiovasc. Res. 28:1574–1580.

    Article  PubMed  CAS  Google Scholar 

  • Hoag, J. B., Qian, Y. Z., Nayeem, M. A., D’Angelo, M., and Kukreja, R. C., 1997, ATP-sensitive potassium channel mediates delayed ischemic protection by heat stress in rabbit heart, Am. J. Physiol. 273:H2458–H2464.

    PubMed  CAS  Google Scholar 

  • Inoue, I., Nagase, H., Kishi, K., and Higuti, T., 1991, ATP-dependent K+ channel in the mitochondrial inner membrane, Nature 352:244–247.

    Article  PubMed  CAS  Google Scholar 

  • Jaburek, M., Yarov-Yarovoy, V., Paucek, P., and Garlid, K. D., 1998, State-dependent inhibition of the mitochondrial KATP channel by glyburide and 5-hydroxydecanoate, J. Biol Chem. 273:13578–13582.

    PubMed  CAS  Google Scholar 

  • Jovanovic, A., Jovanonvic, S., Lorenz, E., and Terzic, A., 1998, Recombinant cardiac ATP-sensitive K + channel subunits confer resistance to chemical hypoxia-reoxygenation injury, Circulation 98:1548–1555.

    Article  PubMed  CAS  Google Scholar 

  • Joyeux, M., Godin-Ribuot, D., and Ribuot, C., 1998, Resistance to myocardial infarction induced by heat stress and the effect of ATP-sensitive potassium channel blockade in the rat isolated heart, Br. J. Pharmacol 123:1085–1088.

    Article  PubMed  CAS  Google Scholar 

  • Kersten, J. R., Gross, G. J., Pagel, P. S., and Warltier, D. C, 1998, Activation of adenosine triphosphate- regulated potassium channels: Mediation of cellular and organ protection, Anesthesiology 88:495–513.

    Article  PubMed  CAS  Google Scholar 

  • Kitakaze, M. Minamino, T., Node, K., Komamura, K., Shinozaki, Y., Chujo, M., Mori, H., Inoue, M., Hori, M., and Kamada, T., 1996, Role of activation of ectosolic 5’-nucleotidase in the cardioprotection mediated by opening of K+ channels, Am. J. Physiol. 270:H1744–H1756.

    PubMed  CAS  Google Scholar 

  • Kloner, R. A., Shook, T., Przyklenk, K., Davis, V. G., Junio, L. Mathews, R. V., Burstein, S., Gibson, C. M., Poole, W. K., Cannon, C. P., McCabe, C. H., and Braunwald, E., 1995, Previous angina alters in-hospital outcome in TIMI 4: A clinical correlate to preconditioning, Circulation 91:37–47.

    Article  PubMed  CAS  Google Scholar 

  • Kouchi, I., Murakami T., Nawada, R., Akao, M., and Sasayama, S., 1998, KATP channels are common mediators of ischemic and calcium preconditioning in rabbits, Am. J. Physiol. 274:H1106–H1112.

    PubMed  CAS  Google Scholar 

  • Kuzuya, T., Hoshida, S., Yamashita, N., Fuji, H., Oe, H., Hori, M., Kamada, T., and Tada, M., 1993, Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia, Circ. Res. 72:1293–1299.

    Article  PubMed  CAS  Google Scholar 

  • Liang, B. T., 1996, Direct preconditioning of cardiac ventricular myocytes via adenosine A1 receptor and KATP channel, Am. J. Physiol. 271:H1769–H1777.

    PubMed  CAS  Google Scholar 

  • Linz, W., Jung, O., Scholkens, B., and Englert, H., 1998, Different effects of KATP channel blockers on ischemic preconditioning, J. Mol. Cell. Cardiol. 30:A18 (abstract).

    Google Scholar 

  • Liu, G. S., Thornton, J. D., Van Winkle, D. M., Stanley, A. W. H., Olsson, R. A., and Downey, J. M., 1991, Protection against infarction afforded by preconditioning is mediated via A1 adenosine receptors in rabbit heart, Circulation 84:350–356.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Ytrehus, K., and Downey, J. M., 1994, Evidence that translocation of protein kinase C is a key event during ischemic preconditioning of rabbit myocardium, J. Mol. Cell. Cardiol. 26:661–668.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Y., Sato, T., O’Rourke, B., and Marban, E., 1998, Mitochondrial ATP-dependent potassium channels: Novel effectors of cardioprotection, Circulation 97:2463–2469.

    Article  PubMed  CAS  Google Scholar 

  • Marber, M. S., Latchman, D. S., Walker, J. M., and Yellon, D. M., 1993, Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction, Circulation 88:1264–1272.

    Article  PubMed  CAS  Google Scholar 

  • Mei, D. A., Elliott, G. T., and Gross, G. J., 1996, KATP channels mediate late preconditioning against infarction produced by monophosphoryl lipid A, Am. J. Physiol. 271:H2723–H2729.

    PubMed  CAS  Google Scholar 

  • Miura, K., Kano, S., Nakai, T., Satoh, K., Hoshi, K., and Ichihara, K., 1997, Inhibitory effects of glibenclamide and pertussis toxin on the attenuation of ischemia-induced myocardial acidosis following ischemic preconditioning in dogs, Jpn. Circ. J. 61:709–714.

    Article  PubMed  CAS  Google Scholar 

  • Mizumura, T., Nithipatikom, K., and Gross, G. J., 1995, Bimakalim, an ATP-sensitive potassium channel opener, mimics the effects of ischemic preconditioning to reduce infarct size, adenosine release and neutrophil function in dogs. Circulation 92:1236–1245.

    Article  PubMed  CAS  Google Scholar 

  • Mizumura, T., Auchampach, J. A., Linden, J., Bruns, R. F., and Gross, G. J., 1996, PD 81723, allosteric enhancer of the A1 adenosine receptor, lowers the threshold for ischemic preconditioning in dogs, Circ. Res. 79:415–423.

    Article  PubMed  CAS  Google Scholar 

  • Moritani, K., Miyazaki, T., Miyoshi, S., Asanagi, M., Zhao, L. S., Mitamura, H., and Ogawa, S., 1994, Blockade of ATP-sensitive potassium channels by 5-hydroxydecanoate suppresses monophasic action potential shortening during regional myocardial ischemia, Cardiovasc. Drugs Ther. 8:749–756.

    Article  PubMed  CAS  Google Scholar 

  • Murry, C. E., Jennings, A. B., and Reimer, K. A., 1986, Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium, Circulation 74:1124–1136.

    Article  PubMed  CAS  Google Scholar 

  • Noma, A., 1983, ATP-regulated K+ channels in cardiac muscle, Nature 305:147–148.

    Article  PubMed  CAS  Google Scholar 

  • Okuyama, Y., Yamada, M., Kondo, C., Satoh, E., Isomoto, S., Shindo, T., Horio, Y., Kitakaze, M., Hori, M., and Kurachi, Y., 1998, The effects of nucleotides and potassium channel openers on the SUR 2A/Kir6.2 complex K+ channel expressed in a mammalian cell line, HEK 293 T cells, Pflügers Arch. 435:595–603.

    Article  PubMed  CAS  Google Scholar 

  • Ottani, F., Galvani, M., Ferrini, D., Sorbello, F., Limonetti, P., Pantoli, D., and Rusticali, F., 1995, Prodromal angina limits infarct size: A role for ischemic preconditioning, Circulation 91:291–297.

    Article  PubMed  CAS  Google Scholar 

  • Paucek, P., Mironova, G., Mahdi, F., Beavis, A. D., Woldegiorgis, G., and Garlid, K. D., 1992, Reconstitution and partial purification of the glibenclamide-sensitive, ATP-dependent K+ channel from rat liver, and beef heart mitochrondria, J. Biol. Chem. 267:26062–26069.

    PubMed  CAS  Google Scholar 

  • Pell, T. J., Yellon, D. M., Goodwin, R. W., and Baxter, G. F., 1997, Myocardial ischemic tolerance following heat stress is abolished by ATP-sensitive potassium channel blockade, Cardiovasc. Drugs Ther. 11:679–686.

    Article  PubMed  CAS  Google Scholar 

  • Przyklenk, K., and Kloner, R. A., 1998, Ischemic preconditioning: Exploring the paradox, Prog. Cardiovasc. Dis. 40:517–547.

    Article  PubMed  CAS  Google Scholar 

  • Rohmann, S., Weygandt, H., Schelling, P., Soei, L. K., Verdouw, P. D., and Lues, I., 1994, Involvement of ATP-sensitive potassium channels in preconditioning protection, Basic Res. Cardiol. 89:563–576.

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto, K., Yamazaki, J., and Nagao, T., 1998, 5-Hydroxydecanoate selectively reduces the initial increase in extracellular K+ in ischemic guinea-pig heart, Eur. J. Pharmacol. 348:31–35.

    Article  PubMed  CAS  Google Scholar 

  • Sato, T., O’Rourke, B., and Marban, E., 1998, Modulation of mitochondrial ATP-dependent K+ channels by protein kinase C, Circ. Res. 83:110–114.

    Article  PubMed  CAS  Google Scholar 

  • Schultz, J. J., Rose, E., Yao, Z., and Gross, G. J., 1995, Evidence for involvement of opioid receptors in ischemic preconditioning in rat hearts, Am. J. Physiol. 268:H2157–2161.

    PubMed  CAS  Google Scholar 

  • Schultz, J. J., Yao, Z., Cavero, I., and Gross, G. J., 1997, Glibenclamide-induced blockade of ischemic preconditioning is time dependent in intact rat heart, Am. J. Physiol. 272:H2607–H2615.

    PubMed  CAS  Google Scholar 

  • Schulz, R., Rose, J., and Heusch, G., 1994, Involvement of activation of ATP-dependent potassium channels in ischemic preconditioning in swine, Am. J. Physiol. 267:H1341–H1352.

    PubMed  CAS  Google Scholar 

  • Speechly-Dick, M. E., Grover, G. J., and Yellon, D. M., 1995, Does ischemic preconditioning in the human involve protein kinase C and the ATP-dependent K+ channel? Studies of contractile function after simulated ischemia in an atrial in vitro model, Circ. Res. 77:1030–1035.

    Article  PubMed  CAS  Google Scholar 

  • Tan, H. L., Mazon, P., Verberne, H. J., Sleeswijk, M. E., Coronel, R., Opthof, T., and Janse, M., 1993, Ischaemic preconditioning delays ischemia-induced cellular electrical uncoupling in rabbit myocardium by activation of ATP-sensitive potassium channels, Cardiovasc. Res. 27:644–651.

    Article  PubMed  CAS  Google Scholar 

  • Thornton, J. D., Thornton, C. S., Sterling, D. L., and Downey, J. M., 1993, Blockade of ATP-sensitive potassium channels increases infarct size but does not prevent preconditioning in rabbit hearts, Circ. Res. 72:44–49.

    Article  PubMed  CAS  Google Scholar 

  • Tomai, F., Crea, F., Gaspardone, A., Versaci, F., De Paulis, R., Penta de Peppo, A., Chiariello, L., and Gioffre, P. A., 1994, Ischemic preconditioning during coronary angioplasty is prevented by glibenclamide, a selective ATP-sensitive K+ channel blocker, Circulation 90:700–705.

    Article  PubMed  CAS  Google Scholar 

  • Toombs, C. F., Moore, T. L., and Shebuski, R. J., 1993, Limitation of infarct size in the rabbit by ischaemic preconditioning is reversible with glibenclamide, Cardiovasc. Res. 27:617–622.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Z., and Gross, G. J., 1994b, Effects of the KATP channel opener bimakalim on coronary blood flow, monophasic action potential duration and infarct size in dogs., Circulation 89:1769–1775.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Z., and Gross, G. J., 1993a, Role of nitric oxide, muscarinic receptors and the ATP-sensitive K+ channel in mediating the effects of acetylcholine to mimic preconditioning in dogs, Circ. Res. 73:1193–1201.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Z., and Gross, G. J., 1994a, A comparison of adenosine-induced cardio-protection and ischemic preconditioning in dogs, Circulation 89:1229–1236.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Z., and Gross, G. J., 1994b, Activation of ATP-sensitive potassium channels lowers the threshold for ischemic preconditioning in dogs, Am. J. Physiol. 267:H1888–H1894.

    PubMed  CAS  Google Scholar 

  • Yao, Z., Auchampach, J. A., Pieper, G. M., and Gross, G. J., 1993b, Cardioprotective effect of monophos-phoryl lipid A, a novel endotoxin analogue, in dogs, Cardiovasc. Res. 27:832–838.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Z., Cavero, I., and Gross, G. J., 1993c, Activation of cardiac KATP channels: an endogenous protective mechanism during repetitive ischemic, Am. J. Physiol. 264:H495–H504.

    PubMed  CAS  Google Scholar 

  • Yao, Z., Mizumura, T., Mei, D. A., and Gross, G. J., 1997, KATP channels and memory of ischemic preconditioning in dogs: Synergism between adenosine and KATP channels. Am. J. Physiol. 272:H334–H342.

    PubMed  CAS  Google Scholar 

  • Zhou, X., Zhai, X., and Ashraf, M., 1996, Direct evidence that initial oxidative stress triggered by preconditioning contributes to second window of protection by endogenous antioxidant enzyme in myocytes, Circulation 93:1177–1184.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Pharmacology & Toxicology, The Medical College of Wisconsin, Milwaukee, Wisconsin, 53226, USA

    Garrett J. Gross

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  1. Garrett J. Gross
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Editors and Affiliations

  1. Walter McKenzie Health Science Centre, University of Alberta Hospital, Edmonton, Alberta, Canada

    Stephen L. Archer

  2. Medical College of Wisconsin, Milwaukee, Wisconsin, USA

    Nancy J. Rusch

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Gross, G.J. (2001). Role of ATP-Sensitive K+ Channels in Cardiac Preconditioning. In: Archer, S.L., Rusch, N.J. (eds) Potassium Channels in Cardiovascular Biology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1303-2_38

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  • DOI: https://doi.org/10.1007/978-1-4615-1303-2_38

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