Українська Русский English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2019; 65(3): 73-85


PROTECTIVE PROPERTIES OF OPENING ATP-SENSITIVE POTASSIUM CHANNELS

R.B. Strutynskyi

    O.O. Bogomoletz Institute of Physiology of National Academy of Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz65.03.073

Abstract

One of the main endogenous mechanisms of protection in reducing cellular energy resources is the system of ATPsensitive potassium (KATP) channels, which is considered a central metabolic cell sensor for its energy supply. These channels have neuro-, cerebro-, cardio-, nephroprotective effects, which are based on inhibition of excitability and metabolism, reduction of β-amyloid toxicity and normalization of bioenergetic processes with the preservation of high content of ATP. Their opening may have an analgesic effect, which is mediated by the release of endorphins, enkephalins and activation of opioid receptors, and may prevent morphine withdrawal syndrome. Also, the opening of these channels can be used to prevent hormonal disorders, elimination of bronchospasms and hyperactivity of the urinary system, and erectile dysfunction of neurogenic and vascular etiology, to improve hair growth and to normalize the work of skeletal muscles at hypokalemic paralysis. However, they have a special role in the cardiovascular system, because they implement the relationship between the energy resource of the heart, its electrical and contractile functions. At the base of their cardioprotective action are the inhibitory processes that occur due to changes in cardiohemodynamic and metabolism. In particular, moderate lowering of blood pressure, prevention of reperfusion increase of general-peripheral resistance and resistance of coronary vessels, and relative preservation of indicators of myocardial contractility during reperfusion. Also, the preventing a significant increase of excess NO by inducible (by iNOS) and by salvage (by NADH-dependent nitrate reductase) NO synthesis and, conversely, increasing the protective constitutive NO synthesis and the sphingosine content. Important for cardioprotection is significant inhibition of the formation of active forms of oxygen and nitrogen, and the preservation of a high activity of antioxidant enzymes, reduction of the formation of pathogenic in the conditions of myocardial ischemia LTC4 and ТхB2, inhibition of ATP degradation, stimulating of the heme oxygenase reaction, membrane protection and preventing opening of the mitochondrial permeability transition pore, and inhibition of apoptosis and necrosis of cardiomyocytes.

Keywords: ATP-sensitive potassium channels, cardioprotection

References

  1. Ngo AT, Riemann M, Holstein-Rathlou NH, TorpPedersen C, Jensen LJ. Significance of K(ATP) channels, L-type Ca²⁺ channels and CYP450-4A enzymes in oxygen sensing in mouse cremaster muscle arterioles in vivo. BMC Physiol. 2013 May 12;13-8. CrossRef PubMed PubMedCentral
  2.  
  3. Nichols CG. KATP channels as molecular sensors of cellular metabolism. Nature. 2006; 440(7083): 470-6. CrossRef PubMed
  4.  
  5. Olson TM, Terzic A. Human KATP channelopathies: diseases of metabolic homeostasis. Pflugers Arch. 2010 Jul;460(2):295-306. CrossRef PubMed PubMedCentral
  6.  
  7. Teshima Y, Akao M, Li RA, Chong TH, Baumgartner WA, Johnston MV, Marbán E. Mitochondrial ATP-sensitive potassium channel activation protects cerebellar granule neurons from apoptosis induced by oxidative stress. Stroke. 2003 Jul;34(7):1796-802. CrossRef PubMed
  8.  
  9. Wickenden AD. Potassium channels as anti-epileptic drug targets. Neuropharmacology. 2002 Dec;43(7):1055-60. CrossRef  
  10. Harel S, Cohen AS, Hussain K, Flanagan SE, SchladeBartusiak K, Patel M, et al. Alternating hypoglycemia and hyperglycemia in a toddler with a homozygous p.R1419H ABCC8 mutation: an unusual clinical picture. J Pediatr Endocrinol Metab. 2015 Mar;28(3-4):345-51. CrossRef PubMed
  11.  
  12. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK. A potassium channel mutation in neonatal human epilepsy. Science. 1998 Jan 16;279(5349):403-6. CrossRef PubMed
  13.  
  14. Alzheimer C, Ten Bruggencate G. Actions of BRL 34915 (Cromakalim) upon convulsive discharges in guinea pig hippocampal slices. Naunyn Schmiedebergs Arch Pharmacol. 1988 Apr;337(4):429-34. CrossRef PubMed
  15.  
  16. Chi X, Sutton ET, Hellermann G, Price JM. Potassium channel openers prevent beta-amyloid toxicity in bovine vascular endothelial cells. Neurosci Lett. 2000 Aug 18;290(1):9-12. CrossRef  
  17. Denysiuk O.M. A comparative influence of flokalin and mexidol on the course of bioenergetic processes in acute experimental cerebral ischemia. Buk Med Herald. 2011;15(1(57)):131-134. [Ukrainian].
  18.  
  19. Tricarico D, Servidei S, Tonali P, Jurkat-Rott K, Camerino DC. Impairment of skeletal muscle ATP-sensitive K+ channels in patients with hypokalemic periodic paralysis. J Clin Invest. 1999 Mar;103(5):675-82. CrossRef PubMed PubMedCentral
  20.  
  21. Campbell VC, Welch SP. The role of minoxidil on endogenous opioid peptides in the spinal cord: a putative co-agonist relationship between K-ATP openers and opioids. Eur J Pharmacol. 2001 Apr 6;417(1-2):91-8. CrossRef  
  22. Kang YM, Zhang ZH, Yang SW, Qiao JT, Dafny N. ATP-sensitive K+ channels are involved in the mediation of intrathecal norepinephrine- or morphine-induced antinociception at the spinal level: a study using EMG planimetry of flexor reflex in rats. Brain Res Bull. 1998;45(3):269-73. CrossRef  
  23. Robles LI, Barrios M, Baeyens JM. ATP-sensitive K+ channel openers inhibit morphine withdrawal. Eur J Pharmacol. 1994 Jan 4;251(1):113-5. CrossRef  
  24. Fozard JR, Manley PW. Potassium channel openers: agents for the treatment of airways hyperreactivity. In: Hansel TT, Barnes PJ, editors. New drugs for asthma, allergy and COPD. Prog. Respir. Res. 2001: 77-80. CrossRef  
  25. Fey TA, Gopalakrishnan M, Strake JG, et al. Effects of ATP-sensitive K+ channel openers and tolterodine on involuntary bladder contractions in a pig model of partial bladder outlet obstruction. Neurourol Urodyn. 2003;22:147-55. CrossRef PubMed
  26.  
  27. Bella AJ, Brock GB. Intracavernous pharmacotherapy for erectile dysfunction. Endocrine. 2004; 23:149-55. CrossRef  
  28. Filipets ND. Filipets OO. The state of homeostatic function of the kidneys after repeated activation of potassium channels with flocalin at salt load. Med Ukraine. 2012;1- 2:66-9. [Ukrainian].
  29.  
  30. Messenger AG, Rundegren J. Minoxidil: mechanisms of action on hair growth. Br J Dermatol. 2004;150:186-94. CrossRef PubMed
  31.  
  32. Hanley PJ, Daut J. K(ATP) channels and preconditioning: a re-examination of the role of mitochondrial K(ATP) channels and an overview of alternative mechanisms. J Mol Cell Cardiol. 2005 Jul;39(1):17-50. CrossRef PubMed
  33.  
  34. Zhang L, Cao S, Deng S, Yao G, Yu T. Ischemic postconditioning and pinacidil suppress calcium overload in anoxia-reoxygenation cardiomyocytes via downregulation of the calcium-sensing receptor. Peer J. 2016 Nov 1;4:e2612. CrossRef PubMed PubMedCentral
  35.  
  36. Aggarwal S, Randhawa PK, Singh N, Jaggi AS. Role of ATP-Sensitive Potassium Channels in Remote Ischemic Preconditioning Induced Tissue Protection. J Cardiovasc Pharmacol Ther. 2017 Sep;22(5):467-75. CrossRef PubMed
  37.  
  38. Nakaya H. Role of ATP-sensitive K+ channels in cardiac arrhythmias. J Cardiovasc Pharmacol Ther. 2014;19(3):237-243. CrossRef PubMed
  39.  
  40. Strutyns'kyĭ RB. Cardioprotective effects of fluorinecontaining activator of adenosine triphosphate-dependent potassium channels flokalin. Fiziol Zh. 2009;55(4):83-90. [Ukrainian].
  41.  
  42. Das B, Sarkar C. MitochondrialKATP channel activation is important in the antiarrhythmic and cardioprotective effects of non-hypotensive doses of nicorandil and cromakalim during ischemia/reperfusion: a study in an intact anesthetized rabbit model. Pharmacol Res. 2003;47:447-61. CrossRef  
  43. Flagg TP, Nichols CG. Sarcolemmal KATP channels: what do we really know? J Mol Cell Cardiol. 2005;39:61-70. CrossRef PubMed
  44.  
  45. Jahandir A, Terzic A. KATP channel therapeutics at the bedsise. J Mol Cell Cardiol. 2005 Jul;39(1):99-112. CrossRef PubMed PubMedCentral
  46.  
  47. Jang Z, Shi G, Wang H, Liu K, Liu Y. Electrophysiologic effects of nicorandil on the guinea pig long QT1 syndrome model. J Cardiovasc Electrophysiol. 2004 Jul;15(7):815-20. CrossRef PubMed
  48.  
  49. Ueda H, Nakayama Y, Tsumura K, Yoshimaru K, Hayashi T, Yoshikawa J. Intravenous nicorandil can reduce the occurrence of ventricular fibrillation and QT dispersion in patients with successful coronary angioplasty in acute myocardial infarction. Can J Cardiol. 2004;20:625-9.
  50.  
  51. Liu XK, Yamada S, Kane GC, AlekseevAV, Hodgson DM, O'Cochlain F, Jahangir A, Miki T, Seino S, Terzic A. Genetic disruption of Kir.6.2, the pore-forming subunit of ATP-sensitive K+ channels, predisposes to catecholamine-indused ventricular dysrhythmia. Diabetes. 2004 Dec;53 Suppl 3:S165-8. CrossRef PubMed
  52.  
  53. Sun JM, Wang CM, Guo Z, Hao YY, Xie YJ, Gu J, Wang AL. Reduction of isoproterenol-induced cardiac hypertrophy and modulation of myocardial connexin43 by a KATP channel agonist. Mol Med Rep. 2015 Mar;11(3):1845-50. CrossRef PubMed
  54.  
  55. Strutyns'kyĭ RB, Rovenets' RA, Neshcheret OP, Tumanovs'ka LV, Boĭchuk TM, Dzhuran BV, Moĭbenko OO. Effect of medical form of flocalin on the course of myocardial reperfusion injury. Fiziol Zh. 2011;57(1):55-65. [Ukrainian].
  56.  
  57. Mazur I, Voronkov L, Dosenko V, Strutynskyi R, Gorovenko N. Impact of KCNJ11 gene polymorphisms of ATP-sensitive potassium channel on left ventricular end-diastolic volume and mass in chronic systolic heart failure. Europ J Heart Failure. 2016;18(1):284.
  58.  
  59. Strutynskyi RB, Neshcheret AP, Tumanovska LV, Rovenets RA, Moibenko AA Cardioprotective effects of flocalin in in vivo experiments: influence of the hemodynamic and on the damage of myocardium under ischemia-reperfusion. Int J Physiol Pathophysiol. 2010;1(3):211-8. CrossRef  
  60. Park WS Alteration of ATP-sensitive K+ channels in rabbit aortic smooth muscle during left ventricular hypertrophy. Park WS, Hong DH, Son YK, Kim MH, Jeong SH, Kim HK, Kim N, Han J. Am J Physiol Cell Physiol. 2012 303(2):C170-178. CrossRef PubMed
  61.  
  62. Muntean DM, Kiss L, Jost N, Baczko I. ATP-sensitive potassium channel modulators and cardiac arrhythmias: an update. Curr Pharm Des. 2015;21(8):1091-102. CrossRef PubMed
  63.  
  64. Konstantinov IE, Li J, Cheung MM, Shimizu M, Stokoe J, Kharbanda RK, Redington AN. Remote ischemic preconditioning of the recipient reduces myocardial ischemiareperfusion injury of the denervated donor heart via a Katp channel-dependent mechanism. Transplantation. 2005 Jun 27;79(12):1691-5. CrossRef PubMed
  65.  
  66. Smith KJ, Chadburn AJ, Adomaviciene A, Minoretti P, Vignali L, Emanuele E, Tammaro P. Coronary spasm and acute myocardial infarction due to a mutation (V734I) in the nucleotide binding domain 1 of ABCC9 Int J Cardiol. 2013 Oct 9;168(4):3506-13. CrossRef PubMed
  67.  
  68. Rosenblum WI. ATP-sensitive potassium channels in the cerebral circulation. Stroke. 2003 Jun;34(6):1547-52. CrossRef PubMed
  69.  
  70. Strutynsk'kyĭ R B, Moĭbenko OO. Modeling of K+ATP channel activity in normotensive and hypertensive animals. Fiziol. Zh. 2000; 46(6):54-60. [Ukrainian].
  71.  
  72. Sica DA. Minoxidil: an underused vasodilator for resistant or severe hypertension. J Clin Hypertens (Greenwich). 2004 May;6(5):283-7. CrossRef PubMed
  73.  
  74. Saito S, Mizumura T, Takayama T, Honye J, Fukui T, Kamata T, Moriuchi M, Hibiya K, Tamura Y, Ozawa Y, et al. Antiischemic effects of nicorandil during coronary angioplasty in humans. Cardiovasc Drugs Ther. 1995 Mar;9 Suppl 2:257-63. CrossRef PubMed
  75.  
  76. Bonev AD, Nelson MT. ATP-sensitive potassium channels in smooth muscle cells from guinea-pig urinary bladder. Am J Physiol. 1993 May;264(5 Pt 1):C1190-200. CrossRef PubMed
  77.  
  78. Teramoto N, McMurray G, Brading AF. Effects of levcromacalim and nucleotide diphosphates on glibenclamide-sensitive K+ channels in pig uretal myocytes. Br J Pharmacol. 1997 Apr;120(7):1229-40. CrossRef PubMed PubMedCentral
  79.  
  80. Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial muscle. Am J Physiol. 1995 Apr;268(4 Pt 1):C799-822. CrossRef PubMed
  81.  
  82. Quayle JM, Nelson MT, Standen NB. ATP-sensitive and inwardly rectifying potassium channels in smooth muscle. Physiol Rev. 1997 Oct;77(4):1165-232. CrossRef PubMed
  83.  
  84. Clapp LH, Gurney AM. ATP-sensitive K+ channels regulate resting potential of pulmonary arterial smooth muscle cells. Am J Physiol. 1992 Mar;262(3 Pt 2):H916-20. CrossRef PubMed
  85.  
  86. Clapp LH, Gurney AM, Standen NB, Langton PD. Properties of the ATP-sensitive K+ current activated by levcromakalim in isolated pulmonary arterial myocytes. J Membr Biol. 1994 Jun;140(3):205-13. CrossRef PubMed
  87.  
  88. Xu X, Lee KS. Characterization of the ATP-inhibited K+ current in canine coronary smooth muscle cell. Pflugers Arch. 1994 May;427(1-2):110-20. CrossRef PubMed
  89.  
  90. Yokoshiki H, Sunagawa M, Seki T, Sperelakis N. ATPsensitive K+ channels in pancreatic, cardiac, and vascular smooth muscle cells. Am J Physiol. 1998 Jan;274(1 Pt 1):C25-37. CrossRef PubMed
  91.  
  92. Beech DJ, Zhang H, Nakao K, Bolton TB. K channel activation by nucleotide diphosphates and its inhibition by glibenclamide in vascular smooth muscle cells / D.J. Beech, H. Zhang, K. Nakao, T.B. Bolton. Br J Pharmacol. 1993 Oct;110(2):573-82. CrossRef PubMed PubMedCentral
  93.  
  94. Noack T, Deitmer P, Edwards G, Weston AH. Characterization of potassium currents modulated by BRL 38227 in rat portal vein. Br J Pharmacol. 1992 Jul;106(3):717-26. CrossRef PubMed PubMedCentral
  95.  
  96. Hiraoka M, Furukawa T. Functional modulation of cardiac ATP-sensitive K+ channels. News Physiol Sci. 1998 Jun;13:131-7. CrossRef  
  97. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8-14;305(5930):147-8. CrossRef PubMed
  98.  
  99. Sanada S, Kitakaze M, Asanuma H, Harada K, Ogita H, Node K, Takashima S, Sakata Y, Asakura M, Shinozaki Y, Mori H, Kuzuya T, Hori M. Role of mitochondrial and sarcolemmal KATP channels in ischemic preconditioning of the canine heart. Am J Physiol Heart Circ Physiol. 2001 Jan;280(1):H256-63. CrossRef PubMed
  100.  
  101. Pyvovar SM, Strutyns'kyĭ RB, Iagupol's'kyĭ LM, Moĭbenko OO. Study of the mechanism of action of novel fluoro-containing analogs of diazoxide on the vascular tonus. Fiziol Zh. 2004;50(2):27-33. [Ukrainian].
  102.  
  103. Wang Y, Kudo M, Xu M, Ayub A, Ashraf M. Mitochondrial K(ATP) channel as an end effector of cardioprotection during late preconditioning: triggering role of nitric oxide. J Mol Cell Cardiol. 2001 Nov;33(11):2037-46. CrossRef PubMed
  104.  
  105. Donato M, Evelson P, Gelpi RJ. Protecting the heart from ischemia/reperfusion injury: an update on remote ischemic preconditioning and postconditioning. Curr Opin Cardiol. 2017 Nov;32(6):784-90. CrossRef PubMed
  106.  
  107. Zhou X, Zhai X, Ashraf M. Direct evidence that initial oxidative stress triggered by preconditioning contributes to a second window of protection by endogenous antioxidant enzymes in myocytes. Circulation. 1996 Mar 15;93(6):1177-84. CrossRef PubMed
  108.  
  109. Pain T, Yang XM, Critz SD, Yue Y, Nakano A, Liu GS, Heusch G, Cohen MV, Downey JM. Opening of mitochondrial KATP channel triggers the preconditioned state by generating free radicals Circ Res. 2000 Sep 15;87(6):460-6. CrossRef PubMed
  110.  
  111. Wang Y, Ashraf M. Role of protein kinase C in mitochondrial KATP channel-mediated protection against Ca2+ overload injury in rat myocardium Circ Res. 1999 May 28;84(10):1156-65. CrossRef PubMed
  112.  
  113. Otani H. Reactive oxygen species as mediators of signal transduction in ischemic preconditioning. Antioxid Redox Signal. 2004; 6(2):449-69. CrossRef PubMed
  114.  
  115. Lasley RD, Keith BJ, Kristo G, Yoshimura Y, Mentzer RM Jr. Delayed adenosine A1 receptor preconditioning in rat myocardium is MAPK dependent but iNOS independent Am J Physiol Heart Circ Physiol. 2005 Aug;289(2):H785-91. CrossRef PubMed
  116.  
  117. Andrukhiv A, Costa AD, West IC, Garlid KD Opening mitoKATP increases superoxide generation from Complex I of the electron transport chain. Am J Physiol Heart Circ Physiol. 2006 Nov;291(5):H2067-74. CrossRef PubMed
  118.  
  119. Strutyns'kyĭ RB, Kotsiuruba AV, Rovenets' RA, Strutyns'ka NA, Iagupols'kyĭ IuL, Sagach VF, Moĭbenko OO. Biochemical mechanisms of the cardioprotective effect of the K(ATP) channels opener flocalin (medicinal form) in ischemia-reperfusion of myocardium. Fiziol Zh. 2013;59(4):16-27. [Ukrainian].
  120.  
  121. Jones SP, Bolli R.The ubiquitous role of nitric oxide in cardioprotection. J Mol Cell Cardiol. 2006;40(1):16-23. CrossRef PubMed
  122.  
  123. Naitoh K, Ichikawa Y, Miura T, Nakamura Y, Miki T, Ikeda Y, Kobayashi H, Nishihara M, Ohori K, Shimamoto K. MitoKATP channel activation suppresses gap junction permeability in the ischemic myocardium by an ERK-dependent mechanism. Cardiovasc Res. 2006 May 1;70(2):374-83. CrossRef PubMed
  124.  
  125. Penna C, Pasqua T, Perrelli MG, Pagliaro P, Cerra MC, Angelone T. Postconditioning with glucagon like peptide-2 reduces ischemia/reperfusion injury in isolated rat hearts: role of survival kinases and mitochondrial KATP channels Basic Res Cardiol. 2012 Jul;107(4):272. CrossRef PubMed
  126.  
  127. Perrelli MG, Tullio F, Angotti C, Cerra MC, Angelone T, Tota B, Alloatti G, Penna C, Pagliaro P. Catestatin reduces myocardial ischaemia/reperfusion injury: involvement of PI3K/Akt, PKCs, mitochondrial KATP channels and ROS signaling. Pflugers Arch. 2013 Jul;465(7):1031-40. CrossRef PubMed
  128.  
  129. Yang XM, Proctor JB, Cui L, Krieg T, Downey JM, Cohen MV. Multiple, brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways. J Am Coll Cardiol. 2004 Sep 1;44(5):1103-10. CrossRef PubMed
  130.  
  131. Zhang SJ, Yang XM, Liu GS, Cohen MV, Pemberton K, Downey JM. CGX-1051, a peptide from Conus snail venom, attenuates infarction in rabbit hearts when administered at reperfusion. J Cardiovasc Pharmacol. 2003 Dec;42(6):764-71. CrossRef PubMed
  132.  
  133. Nichols CG, Singh GK, Grange DK. KATP channels and cardiovascular disease: suddenly a syndrome. Circ Res. 2013 Mar 29;112(7):1059-72. CrossRef PubMed PubMedCentral
  134.  
  135. Voitychuk OI, Strutynskyi RB, Yagupolskii LM, Tinker A, Moibenko OO, Shuba YM. Sarcolemmal cardiac K(ATP) channels as a target for the cardioprotective effects of the fluorine-containing pinacidil analogue, flocalin. Br J Pharmacol. 2011 Feb;162(3):701-11. CrossRef PubMed PubMedCentral
  136.  
  137. Strutyns'kyĭ RB, Kotsiuruba AV, Neshcheret OP, Rovenets' RA, Moĭbenko OO. The changes of metabolism in myocardium at ischemia-reperfusion and activating of the ATP-sensitive potassium channels. Fiziol Zh. 2012;58(1):13-26. [Ukrainian].
  138.  
  139. Moybenko OO, Strutynskyi RB, Yagupolskii LM, Mohort MA, Shalamai AS. Organization of industrial production of flokalin - new myotropic spasmolytic and cardioprotector. Nauka Innov. 2013; 9(1): 55-63. [Ukrainian].
  140. CrossRef  
  141. Strutyns'kyĭ RB, Pyvovar SM, Rovenets' RA, Piskun OV, Iahupol's'kyĭ LM, Moĭbenko OO. Effect of adenosine triphosphate-sensitve potassium channel activator flokalin on the isolated heart functions. Fiziol Zh. 2005;51(6):18-24. [Ukrainian].
  142.  
  143. Strutyns'kyĭ RB. The vasodilation effects of flokalin, a fluorine-containing K(ATP) channel opener. Fiziol Zh. 2010;56(4):59-65. [Ukrainian].
  144.  
  145. Strutynskyi RB, Kotsuruba AV, Neshcheret AP, Shysh AN, Rovenets RA, Moibenko AA. Cardioprotective Effects of ATP-Sensitive Potassium Channels Activation in Experiments in Vivo: Influence on Biochemical Parameters of Blood Following Ischemia-Reperfusion of Myocardium. Int J Physiol Pathophysiol. 2010;1(4):305-313. CrossRef  
  146. Strutyns'kyĭ RB, Rovenets' RA, Strutyns'ka NA, Neshcheret OP, Moĭbenko OO. The influence of activation of the ATP-sensitive potassium channels by flocalin on the function of the cardiovascular system. Fiziol Zh. 2013;59(1):11-6. [Ukrainian].
  147.  
  148. Strutyns'kyĭ RB, Pyvovar SM, Tumanovs'ka LV, Moĭbenko OO. Cardioprotective effects of flokalin: relative role of activation of sarcolemmal and mitochondrial adenosine triphosphate-dependent potassium channels. Fiziol Zh. 2008;54(6):15-23. [Ukrainian].
  149.  
  150. Strutyns'kyĭ RB, Neshcheret OP, Tumanovs'ka LV, Rovenets' RA, Moĭbenko OO. Cardioprotective effects of flokalin in experiments in vivo: influence on hemodynamic and myocardial lesions in ischemiareperfusion. Fiziol Zh. 2009;55(5):9-16. [Ukrainian].
  151.  
  152. Mironova GD, Kachayeva YeV, Krylova IB, Rodionova OM, BolinaMI, Yevdokimova NR, Sapronov NS. Mitochondrial ATP-dependent potassium channel. 2. The role of the channel inprotection of the heart against ischemia. Bul Rus AMS. 2007; 2: 44-50. [Russian].
  153.  
  154. Holmuhamedov EL, Jovanović S, Dzeja PP, Jovanović A, Terzic A. Mitochondrial ATP-sensitive K+ channels modulate cardiac mitochondrial function. Am J Physiol. 1998 Nov;275(5 Pt 2):H1567-76. CrossRef PubMed
  155.  
  156. Storey NM, Stratton RC, Rainbow RD, Standen NB, Lodwick D. Kir6.2 limits Ca(2+) overload and mitochondrial oscillations of ventricular myocytes in response to metabolic stress. Am J Physiol Heart Circ Physiol. 2013 Nov 15;305(10):H1508-18. CrossRef PubMed PubMedCentral
  157.  
  158. Murata M, Akao M, O'Rourke B, Marbán E.Mitochondrial ATP-Sensitive potassium channels attenuate matrix Ca2+ overload during simulated ischemia and reperfusion: Possible mechanism of cardioprotection. Circ Res. 2001 Nov 9;89(10):891-8.
  159.  
  160. Strutynska NA, Strutynskyi RB, Chorna SV, Semenykhina OM, Mys LA, Moibenko OO, Sahach VF. New FluorineContaining Openers of ATP-sensitive Potassium Channels Flocalin and Tioflocalin Inhibit CalciumInduced Mitochondrial Pore Opening in Rat Hearts. Int J Physiol Pathophysiol. 2014;5(3):231-44.
  161.  
  162. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion - a target for cardioprotection. Cardiovasc Res. 2004 Feb 15;61(3):372-85. CrossRef  
  163. O'Rourke B. Myocardial KATP channels in preconditioning. Circ Res. 2000 Nov 10;87(10):845-55. CrossRef PubMed
  164.  
  165. Strutyns'kyĭ RB, Nagibin VS, Strutyns'ka NA, Ianchiĭ OR, Moĭbenko OO. Influence of flocalin on development of apoptosis and necrosis at anoxia-reoxygenation of culture rats neonatal cardiomyocytes. Fiziol Zh. 2013;59(3):3-9. [Ukrainian]. CrossRef  
  166. Dunne MJ, Aynsley-Green A, Lindley KJ. Nature's KATP channels knockout. News Physiol Sci. 1997;12:197-203. CrossRef  
  167. Khmil NV, Gorbacheva OS, Strutinskiy RB, Korobeynikova MO, Belosludtseva NV, Kolomytkin OV, and Mironova GD. A study of the effects of flocalin on respiration and potassium transport of rat - heart and liver mitochondria. Biophysics. 2016; 61(6): 888-92. CrossRef  
  168. Gorbacheva OS, Strutynskyi RB, Khmil NV, Belosludtseva NV, Mursaeva SV, Korobeynikova MO, Alilova GA, Lezhnev EI, Mironova GD. Study of the influence of flocalin on the energy and ion exchanges in rat liver mitochondria. Biological Motility, Pushchino. 2016: 73-7.
  169.  
  170. Costa AD, Quinlan CL, Andrukhiv A, West IC, Jaburek M, Garlid KD. The direct physiological effects of mitoK(ATP) opening on heart mitochondria. Am J Physiol Heart Circ Physiol. 2006; 290(1):406-15. CrossRef PubMed
  171.  
  172. Belisle E, Kowaltowski AJ. Opening of mitochondrial K+ channels increases ATP levels by preventing hydrolysis. J Bioenerg Biomembr. 2002 Aug;34(4):285-98. CrossRef  
  173. Dzeja PP, Bast P, Ozcan C, Valverde A, Holmuhamedov EL, Van Wylen DG, Terzic A. Targeting nucleotiderequiring enzymes: implications for diazoxide-induced cardioprotection. Am J Physiol Heart Circ Physiol. 2003 Apr;284(4):H1048-56. CrossRef PubMed
  174.  
  175. Maslov LN, Lishmanov YuB, Solenkova NV. Adaptation of Myocardium to Ischemia. The Early Phase of Ischemic Preconditioning. Succes Physiol Sci 2006; 37(3): 25-41.
  176.  
  177. McPherson CD, Pierce GN, Cole WC. Ischemic cardioprotection by ATP-sensitive K+ channels involves high-energy phosphate preservation. Am J Physiol. 1993 Nov;265(5 Pt 2):H1809-18. CrossRef PubMed
  178.  
  179. Crestanello JA, Doliba NM, Babsky AM, Doliba NM, Niibori K, Whitman GJ, Osbakken MD. Ischemic preconditioning improves mitochondrial tolerance to experimental calcium overload. J Surg Res. 2002 Apr;103(2):243-51. CrossRef PubMed
  180.  
  181. Eells JT, Henry MM, Gross GJ, Baker JE. Increased mitochondrial KATP channel activity during chronic myocardial hypoxia. Is cardioprotection mediated by improved bioenergetics? Circ Res. 2000 Nov 10;87(10):915-21. CrossRef PubMed
  182.  
  183. Jilkina O, Kuzio B, Grover GJ, Kupriyanov VV. Effects of K(ATP) channel openers, P-1075, pinacidil, and diazoxide, on energetics and contractile function in isolated rat hearts. J Mol Cell Cardiol. 2002 Apr;34(4):427-40. CrossRef PubMed
  184.  
  185. Lembert N, Idahl LA, Ammon HP. K-ATP channel independent effects of pinacidil on ATP production in isolated cardiomyocyte or pancreatic β-cell mitochondria. Biochem Pharmacol. 2003 Jun 1;65(11):1835-41. CrossRef  
  186. Strutynskyi RB. Mechanisms of cardioprotective action of activation of SUR receptors of potassium channels: dissert. Doctor of Biological Sciences; 03.00.13; Kyiv 2018:440. [Ukrainian].
  187.  
  188. Marletta MA. Another activation switch for endothelial nitric oxide synthase: why does it have to be so complicated? Trends Biochem Sci. 2001 Sep;26(9):519-21. CrossRef  
  189. Ozcan C, Bienengraeber M, Dzeja PP, Terzic A. Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. Am J Physiol Heart Circ Physiol. 2002 Feb;282(2):H531-9. CrossRef PubMed
  190.  
  191. Kim HH, Choi S. Therapeutic Aspects of Carbon Monoxide in Cardiovascular Disease. Int J Mol Sci. 2018 Aug 13;19(8). pii: E2381. CrossRef PubMed PubMedCentral
  192.  

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2020.