Protocols and mechanisms for remote ischemic preconditioning: A novel method for reducing ischemia reperfusion injury

Transplantation

Volumn 84, Issue 4, 2007, Pages 445-458

  Kanoria, Sanjeev ^a   Jalan, Rajiv ^b   Seifalian, Alexander M ^a   Williams, Roger ^b   Davidson, Brian R ^a  

^a ROYAL FREE HOSPITAL   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Mechanism; Remote preconditioning; Review

Indexed keywords

1,4 DIHYDRO 2 METHYL 6 PHENYL 4 (2 PHENYLETHYNYL) 3,5 PYRIDINEDICARBOXYLIC ACID 5 BENZYL 3 ETHYL ESTER; 7 BENZYLIDENENALTREXONE; 8 (4 SULFOPHENYL)THEOPHYLLINE; ADENOSINE; ADENOSINE RECEPTOR BLOCKING AGENT; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; ICATIBANT; N(G) NITROARGININE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; S METHYLISOTHIOUREA SULFATE; TIOPRONIN; UNCLASSIFIED DRUG;

BRAIN ISCHEMIA; CELL PROTECTION; CLINICAL PROTOCOL; DRUG MECHANISM; EXPERIMENTAL STUDY; HEART MUSCLE ISCHEMIA; HUMAN; HUMORAL IMMUNITY; ISCHEMIA; KIDNEY ISCHEMIA; LIVER ISCHEMIA; MEDICAL RESEARCH; MEDLINE; NONHUMAN; PRIORITY JOURNAL; REMOTE ISCHEMIC PRECONDITIONING; REPERFUSION INJURY; REVIEW; SKELETAL MUSCLE; SKIN FLAP; STOMACH;

ANIMALS; HUMANS; ISCHEMIC PRECONDITIONING; ORGAN TRANSPLANTATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 34548147767     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.tp.0000228235.55419.e8     Document Type: Review

References (116)

1. Petrishchev NN, Vlasov TD. [Endothelium function in ischemiareperfusion (a literature review)]. Ross Fiziol Zh Im I M Sechenova 2000; 86: 148.
2. Goode HF, Webster NR, Howdle PD, et al. Reperfusion injury, antioxidants and hemodynamics during orthotopic liver transplantation. Hepatology 1994; 19: 354.
3. Langle F, Roth E, Steininger R, Winkler S, Muhlbacher F. Arginase release following liver reperfusion. Evidence of hemodynamic action of arginase infusions. Transplantation 1995; 59: 1542.
4. Gerlach J, Jorres A, Schon M, et al. Systemic liberation of interleukin-8 in the perioperative phase of liver transplantation. Transpl Int 1997; 10: 401.
5. Clavien PA, Camargo CA, Jr., Gorczynski R, et al. Acute reactant cytokines and neutrophil adhesion after warm ischemia in cirrhotic and noncirrhotic human livers. Hepatology 1996; 23: 1456.
6. Lentsch AB, Yoshidome H, Cheadle WG, et al. Chemokine involvement in hepatic ischemia/reperfusion injury in mice: Roles for macrophage inflammatory protein-2 and KC. Hepatology 1998; 27: 1172.
7. Colletti LM, Kunkel SL, Walz A, et al. Chemokine expression during hepatic ischemia/reperfusion-induced lung injury in the rat. The role of epithelial neutrophil activating protein. J Clin Invest 1995; 95: 134.
8. Boros P, Tarcsafalvi A, Wang L, et al. Intrahepatic expression and release of vascular endothelial growth factor following orthotopic liver transplantation in the rat. Transplantation 2001; 72: 805.
9. Neary P, Redmond HP. Ishaemia Reperfusion injury and the systemic inflammatory response syndrome. In: Grace PA, Mathie RT, eds. Ischemia reperfusion injury. London: Blackwell Science, 1999: 157.
10. Hardy KJ, McClure DN, Subwongcharoen S. Ischaemic preconditioning of the liver: A preliminary study. Aust N Z J Surg 1996; 66: 707.
11. Soncul H, Oz E, Kalaycioglu S. Role of ischemic preconditioning on ischemia-reperfusion injury of the lung. Chest 1999; 115: 1672.
12. Przyklenk K, Bauer B, Ovize M, et al. Regional ischemic 'preconditioning' protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 1993; 87: 893.
13. Verdouw PD, Gho BC, Koning MM, et al. Cardioprotection by ischemic and nonischemic myocardial stress and ischemia in remote organs. Implications for the concept of ischemic preconditioning. Ann N Y Acad Sci 1996; 793: 27.
14. Takaoka A, Nakae I, Mitsunami K, et al. Renal ischemia/reperfusion remotely improves myocardial energy metabolism during myocardial ischemia via adenosine receptors in rabbits: effects of "remote preconditioning." J Am Coll Cardiol 1999; 33: 556.
15. Gunaydin B, Cakici I, Soncul H, et al. Does remote organ ischaemia trigger cardiac preconditioning during coronary artery surgery? Pharmacol Res 2000; 41: 493.
16. Kharbanda RK, Mortensen UM, White PA, et al. Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 2002; 106: 2881.
17. Konstantinov IE, Arab S, Kharbanda RK, et al. The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans. Physiol Genomics 2004; 19: 143.
18. Kuntscher MV, Schirmbeck EU, Menke H, Klar E, Gebhard MM, Germann G. Ischemic preconditioning by brief extremity ischemia before flap ischemia in a rat model. Plast Reconstr Surg 2002; 109: 2398.
19. Kuntscher MV, Kastell T, Sauerbier M, et al. Acute remote ischemic preconditioning on a rat cremasteric muscle flap model. Microsurgery 2002; 22: 221.
20. Brzozowski T, Konturek PC, Konturek SJ, et al. Ischemic preconditioning of remote organs attenuates gastric ischemia-reperfusion injury through involvement of prostaglandins and sensory nerves. Eur J Pharmacol 2004; 499: 201.
21. Park KM, Kramers C, Vayssier-Taussat M, et al. Prevention of kidney ischemia/reperfusion-induced functional injury, MAPK and MAPK kinase activation, and inflammation by remote transient ureteral obstruction. J Biol Chem 2002; 277: 2040.
22. Park KM, Chen A, Bonventre JV. Prevention of kidney ischemia/ reperfusion-induced functional injury and JNK, p38, and MAPK kinase activation by remote ischemic pretreatment. J Biol Chem 2001; 276: 11870.
23. Ates E, Genc E, Erkasap N, et al. Renal protection by brief liver ischemia in rats. Transplantation 2002; 74: 1247.
24. Xia Z, Herijgers P, Nishida T, et al. Remote preconditioning lessens the deterioration of pulmonary function after repeated coronary artery occlusion and reperfusion in sheep. Can J Anaesth 2003; 50: 481.
25. Peralta C, Fernandez L, Panes J, et al. Preconditioning protects against systemic disorders associated with hepatic ischemia-reperfusion through blockade of tumor necrosis factor- induced P-selectin up-regulation in the rat. Hepatology 2001; 33: 100.
26. Harkin DW, Barros D'Sa AA, McCallion K, et al. Ischemic preconditioning before lower limb ischemia-reperfusion protects against acute lung injury. J Vasc Surg 2002; 35: 1264.
27. Kanoria S, Jalan R, Seifalian A, Williams R, Davidson B. Remote Ischemic preconditioning of hind limb reduces liver warm ischemia reperfusion injury in rabbit model. Hepatology 2003; 38: 474A.
28. Kanoria S, Jalan R, Davies NA, et al. Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. Br J Surg 2006; 93: 762.
29. Lai IR, Chang KJ, Chen CF, Tsai HW. Transient limb ischemia induces remote preconditioning in liver among rats: The protective role of heme oxygenase-1. Transplantation 2006; 81: 1311.
30. Dickson EW, Reinhardt CP, Renzi FP, et al. Ischemic preconditioning may be transferable via whole blood transfusion: Preliminary evidence. J Thromb Thrombolysis 1999; 8: 123.
31. Dickson EW, Lorbar M, Porcaro WA, et al. Rabbit heart can be "preconditioned" via transfer of coronary effluent. Am J Physiol 1999; 277: H2451.
32. McClanahan T, Nao B, Wolke L, et al. Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits. Faseb J 1993; 7: A118.
33. Pell TJ, Baxter GF, Yellon DM, Drew GM. Renal ischemia preconditions myocardium: Role of adenosine receptors and ATP-sensitive potassium channels. Am J Physiol 1998; 275: H1542.
34. Gho BC, Schoemaker RG, van den Doel MA, et al. Myocardial protection by brief ischemia in noncardiac tissue. Circulation 1996; 94: 2193.
35. Patel HH, Moore J, Hsu AK, Gross GJ. Cardioprotection at a distance: Mesenteric artery occlusion protects the myocardium via an opioid sensitive mechanism. J Mol Cell Cardiol 2002; 34: 1317.
36. Tokuno S, Hinokiyama K, Tokuno K, et al. Spontaneous ischemic events in the brain and heart adapt the hearts of severely atherosclerotic mice to ischemia. Arterioscler Thromb Vasc Biol 2002; 22: 995.
37. de Zeeuw S, Lameris TW, Duncker DJ, et al. Cardioprotection in pigs by exogenous norepinephrine but not by cerebral ischemia-induced release of endogenous norepinephrine. Stroke 2001; 32: 767.
38. Oxman T, Arad M, Klein R, et al. Limb ischemia preconditions the heart against reperfusion tachyarrhythmia. Am J Physiol 1997; 273: H1707.
39. Konstantinov IE, Li J, Cheung MM, et al. Remote ischemic preconditioning of the recipient reduces myocardial ischemia-reperfusion injury of the denervated donor heart via a Katp channel-dependent mechanism. Transplantation 2005; 79: 1691.
40. Weinbrenner C, Nelles M, Herzog N, et al. Remote preconditioning by infrarenal occlusion of the aorta protects the heart from infarction: A newly identified non-neuronal but PKC-dependent pathway. Cardiovasc Res 2002; 55: 590.
41. Nakano A, Heusch G, Cohen MV, Downey JM. Preconditioning one myocardial region does not neccessarily precondition the whole rabbit heart. Basic Res Cardiol 2002; 97: 35.
42. Vlasov TD, Smirnov DA, Nutfullina GM. [Adaptation of the rat small intestine to ischemia]. Ross Fiziol Zh Im I M Sechenova 2001; 87: 118.
43. Teoh N, Dela Pena A, Farrell G. Hepatic ischemic preconditioning in mice is associated with activation of NF-kappaB, p38 kinase, and cell cycle entry. Hepatology 2002; 36: 94.
44. Peralta C, Closa D, Xaus C, et al. Hepatic preconditioning in rats is defined by a balance of adenosine and xanthine. Hepatology 1998; 28: 768.
45. Carini R, De Cesaris MG, Splendore R, et al. Ischemic preconditioning reduces Na(+) accumulation and cell killing in isolated rat hepatocytes exposed to hypoxia. Hepatology 2000; 31: 166.
46. Goto M, Liu Y, Yang XM, et al. Role of bradykinin in protection of ischemic preconditioning in rabbit hearts. Circ Res 1995; 77: 611.
47. Birnbaum Y, Hale SL, Kloner RA. Ischemic preconditioning at a distance: reduction of myocardial infarct size by partial reduction of blood supply combined with rapid stimulation of the gastrocnemius muscle in the rabbit. Circulation 1997; 96: 1641.
48. Pang CY, Addison PD, Ashrafpour H, et al. Global protection against skeletal muscle infarction by non-invasive remote preconditioning. Circulation 2002; 106(Suppl-II): 133.
49. Moses MA, Addison PD, Neligan PC, et al. Mitochondrial KATP channels in hind limb remote ischemic preconditioning of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 2005; 288: H559.
50. Kanoria S, Glantzounis G, Jalan R, et al. A model to study total hepatic ischemia-reperfusion injury. Transplant Proc 2004; 36: 2586.
51. Peralta C, Bulbena O, Xaus C, et al. Ischemic preconditioning: a defense mechanism against the reactive oxygen species generated after hepatic ischemia reperfusion. Transplantation 2002; 73: 1203.
52. Fernandez L, Heredia N, Grande L, et al. Preconditioning protects liver and lung damage in rat liver transplantation: role of xanthine/xanthine oxidase. Hepatology 2002; 36: 562.
53. Waldow T, Alexiou K, Witt W, et al. Protection against acute porcine lung ischemia/reperfusion injury by systemic preconditioning via hind limb ischemia. Transpl Int 2005; 18: 198.
54. Brzozowski T, Konturek PC, Pajdo R, et al. Importance of brain-gut axis in the gastroprotection induced by gastric and remote preconditioning. J Physiol Pharmacol 2004; 55: 165.
55. Vlasov TD, Korzhevskii DE, Poliakova EA. [Ischemic adaptation of the rat brain as a method for protection of endothelium from ischemic reperfusion injury]. Ross Fiziol Zh Im I M Sechenova 2004; 90: 40.
56. Kharbanda RK, Peters M, Walton B, et al. Ischemic preconditioning prevents endothelial injury and systemic neutrophil activation during ischemia-reperfusion in humans in vivo. Circulation 2001; 103: 1624.
57. Loukogeorgakis SP, Panagiotidou AT, Broadhead MW, et al. Remote ischemic preconditioning provides early and late protection against endothelial ischemia-reperfusion injury in humans: Role of the autonomic nervous system. J Am Coll Cardiol 2005; 46: 450.
58. Cheung MM, Kharbanda RK, Konstantinov IE, et al. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: First clinical application in humans. J Am Coll Cardiol 2006; 47: 2277.
59. Heusch G, Schulz R. Remote preconditioning. J Mol Cell Cardiol 2002; 34: 1279.
60. Schoemaker RG, van Heijningen CL. Bradykinin mediates cardiac preconditioning at a distance. Am J Physiol Heart Circ Physiol 2000; 278: H1571.
61. Tang ZL, Dai W, Li YJ, Deng HW. Involvement of capsaicin-sensitive sensory nerves in early and delayed cardioprotection induced by a brief ischaemia of the small intestine. Naunyn Schmiedebergs Arch Pharmacol 1999; 359: 243.
62. Wang Y, Xu H, Mizoguchi K, Oe M, Maeta H. Intestinal ischemia induces late preconditioning against myocardial infarction: A role for inducible nitric oxide synthase. Cardiovasc Res 2001; 49: 391.
63. Kuntscher MV, Kastell T, Engel H, et al. Late remote ischemic preconditioning in rat muscle and adipocutaneous flap models. Ann Plast Surg 2003; 51: 84.
64. Dickson EW, Porcaro WA, Fenton RA, et al. "Preconditioning at a distance" in the isolated rabbit heart. Acad Emerg Med 2000; 7: 311.
65. Dickson EW, Blehar DJ, Carraway RE, et al. Naloxone blocks transferred preconditioning in isolated rabbit hearts. J Mol Cell Cardiol 2001; 33: 1751.
66. Weinbrenner C, Schulze F, Sarvary L, Strasser RH. Remote preconditioning by infrarenal aortic occlusion is operative via delta1-opioid receptors and free radicals in vivo in the rat heart. Cardiovasc Res 2004; 61: 591.
67. Dickson EW, Tubbs RJ, Porcaro WA, et al. Myocardial preconditioning factors evoke mesenteric ischemic tolerance via opioid receptors and K(ATP) channels. Am J Physiol Heart Circ Physiol 2002; 283: H22.
68. Petrishchev NN, Vlasov TD, Sipovsky VG, et al. Does nitric oxide generation contribute to the mechanism of remote ischemic preconditioning? Pathophysiology 2001; 7: 271.
69. Peralta C, Prats N, Xaus C, et al. Protective effect of liver ischemic preconditioning on liver and lung injury induced by hepatic ischemiareperfusion in the rat. Hepatology 1999; 30: 1481.
70. Kuntscher MV, Kastell T, Altmann J, et al. Acute remote ischemic preconditioning II: The role of nitric oxide. Microsurgery 2002; 22: 227.
71. Kuntscher MV, Juran S, Altmann J, et al. Role of nitric oxide in the mechanism of preclamping and remote ischemic preconditioning of adipocutaneous flaps in a rat model. J Reconstr Microsurg 2003; 19: 55.
72. Li G, Labruto F, Sirsjo A, et al. Myocardial protection by remote preconditioning: The role of nuclear factor kappa-B p105 and inducible nitric oxide synthase. Eur J Cardiothorac Surg 2004; 26: 968.
73. Tokuno S, Chen F, Pernow J, et al. Effects of spontaneous or induced brain ischemia on vessel reactivity: The role of inducible nitric oxide synthase. Life Sci 2002; 71: 679.
74. Xiao L, Lu R, Hu CP, et al. Delayed cardioprotection by intestinal preconditioning is mediated by calcitonin gene-related peptide. Eur J Pharmacol 2001; 427: 131.
75. Gislason H, Varhaug P, Sorbye H, et al. Role of adenosine and nitric oxide in the hyperemic response to superficial and deep gastric mucosal injury and H+ back-diffusion in cats. Scand J Gastroenterol 1996; 31: 14.
76. Arai M, Thurman RG, Lemasters JJ. Contribution of adenosine A(2) receptors and cyclic adenosine monophosphate to protective ischemic preconditioning of sinusoidal endothelial cells against Storage/Reperfusion injury in rat livers. Hepatology 2000; 32: 297.
77. Liem DA, Verdouw PD, Ploeg H, et al. Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol 2002; 283: H29.
78. Liem DA, te Lintel Hekkert M, Manintveld OC, et al. Myocardium tolerant to an adenosine-dependent ischemic preconditioning stimulus can still be protected by stimuli that employ alternative signaling pathways. Am J Physiol Heart Circ Physiol 2005; 288: H1165.
79. Ishida T, Yarimizu K, Gute DC, Korthuis RJ. Mechanisms of ischemic preconditioning. Shock 1997; 8: 86.
80. Papanastasiou S, Estdale SE, Homer-Vanniasinkam S, Mathie RT. Protective effect of preconditioning and adenosine pretreatment in experimental skeletal muscle reperfusion injury. Br J Surg 1999; 86: 916.
81. Pasini FL, Capecchi PL, Perri TD. Adenosine and chronic ischemia of the lower limbs. Vasc Med 2000; 5: 243.
82. Wang WZ, Guo SZ, Anderson GL, Miller FN. The initiating factors of late preconditioning in skeletal muscle. J Surg Res 2001; 99: 92.
83. Schulz R, Post H, Vahlhaus C, Heusch G. Ischemic preconditioning in pigs: A graded phenomenon: its relation to adenosine and bradykinin. Circulation 1998; 98: 1022.
84. Tanaka M, Fujiwara H, Yamasaki K, et al. Expression of heat shock protein after ischemic preconditioning in rabbit hearts. Jpn Circ J 1998; 62: 512.
85. Patel A, van de Poll MC, Greve JW, et al. Early stress protein gene expression in a human model of ischemic preconditioning. Transplantation 2004; 78: 1479.
86. Liauw SK, Rubin BB, Lindsay TF, et al. Sequential ischemia/reperfusion results in contralateral skeletal muscle salvage. Am J Physiol 1996; 270: H1407.
87. Kukoba TV, Moibenko OO. [Heme oxygenase and carbon monoxide: The protection or the injury of cells?]. Fiziol Zh 2002; 48: 79.
88. Amersi F, Buelow R, Kato H, et al. Upregulation of heme oxygenase-1 protects genetically fat Zucker rat livers from ischemia/reperfusion injury. J Clin Invest 1999; 104: 1631.
89. Teoh N, Leclercq I, Pena AD, Farrell G. Low-dose TNF-alpha protects against hepatic ischemia-reperfusion injury in mice: Implications for preconditioning. Hepatology 2003; 37: 118.
90. Lecour S, Rochette L, Opie L. Free radicals trigger TNF alpha-induced cardioprotection. Cardiovasc Res 2005; 65: 239.
91. Yamashita N, Hoshida S, Otsu K, et al. The involvement of cytokines in the second window of ischaemic preconditioning. Br J Pharmacol 2000; 131: 415.
92. Ren X, Wang Y, Jones WK. TNF-alpha is required for late ischemic preconditioning but not for remote preconditioning of trauma. J Surg Res 2004; 121: 120.
93. Chen YS, Chien CT, Ma MC, et al. Protection "outside the box" (skeletal remote preconditioning) in rat model is triggered by free radical pathway. J Surg Res 2005; 126: 92.
94. Arad M, Oxman T, Leor R, Rabinowitz B. Prostaglandins and the antiarrhythmic effect of preconditioning in the isolated rat heart. Mol Cell Biochem 1996; 160-161: 249.
95. Singh D, Chopra K. Evidence of the role of angiotensin AT(1) receptors in remote renal preconditioning of myocardium. Meth Find Exp Clin Pharmacol 2004; 26: 117.
96. Ferdinandy P, Csont T, Csonka C, et al. Capsaicin-sensitive local sensory innervation is involved in pacing-induced preconditioning in rat hearts: role of nitric oxide and CGRP? Naunyn Schmiedebergs Arch Pharmacol 1997; 356: 356.
97. Wolfrum S, Nienstedt J, Heidbreder M, et al. Calcitonin gene related peptide mediates cardioprotection by remote preconditioning. Regul Pept 2005; 127: 217.
98. Huda R, Chung DH, Mathru M. Ischemic preconditioning at a distance: Altered gene expression in mouse heart and other organs following brief occlusion of the mesenteric artery. Heart Lung Circ 2005; 14: 36.
99. Boku K, Ohno T, Saeki T, et al. Adaptive cytoprotection mediated by prostaglandin I(2) is attributable to sensitization of CRGP-containing sensory nerves. Gastroenterology 2001; 120: 134.
100. Wang YP, Maeta H, Mizoguchi K, et al. Intestinal ischemia preconditions myocardium: Role of protein kinase C and mitochondrial K(ATP) channel. Cardiovasc Res 2002; 55: 576.
101. Wolfrum S, Schneider K, Heidbreder M, et al. Remote preconditioning protects the heart by activating myocardial PKC-epsilon-isoform. Cardiovasc Res 2002; 55: 583.
102. Pagliaro P, Gattullo D, Rastaldo R, Losano G. Involvement of nitric oxide in ischemic preconditioning. Ital Heart J 2001; 2: 660.
103. Kristiansen SB, Henning O, Kharbanda RK, et al. Remote preconditioning reduces ischemia-reperfusion injury in the explanted heart by a KATP channel-dependent mechanism. Am J Physiol Heart Circ Physiol 2005; 288: H1252.
104. Moses MA, Addison PD, Neligan PC, et al. Inducing late phase of infarct protection in skeletal muscle by remote preconditioning: Efficacy and mechanism. Am J Physiol Regul Integr Comp Physiol 2005; 289: R1609.
105. Moses MA, Addison PD, Neligan PC, et al. Mitochondrial KATP channels in hindlimb remote ischemic preconditioning of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 2005; 288: H559.
106. O'Rourke B. Myocardial K(ATP) channels in preconditioning. Circ Res 2000; 87: 845.
107. Murata M, Akao M, O'Rourke B, Marban E. Mitochondrial ATP-sensitive potassium channels attenuate matrix Ca(2+) overload during simulated ischemia and reperfusion: Possible mechanism of cardioprotection. Circ Res 2001; 89: 891.
108. Kowaltowski AJ, Seetharaman S, Paucek P, Garlid KD. Bioenergetic consequences of opening the ATP-sensitive K(+) channel of heart mitochondria. Am J Physiol Heart Circ Physiol 2001; 280: H649.
109. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 2003; 284: G15.
110. Konstantinov IE, Arab S, Li J, et al. The remote ischemic preconditioning stimulus modifies gene expression in mouse myocardium. J Thorac Cardiovasc Surg 2005; 130: 1326.
111. Przyklenk K, Darling CE, Dickson EW, Whittaker P. Cardioprotection 'outside the box'-the evolving paradigm of remote preconditioning. Basic Res Cardiol 2003; 98: 149.
112. Verdouw PD, Gho BC, Koning MM, et al. Cardioprotection by ischemic and nonischemic myocardial stress and ischemia in remote organs. Implications for the concept of ischemic preconditioning. Ann N Y Acad Sci 1996;793: 27.
113. Wang WZ, Stepheson LL, Fang XH, Khiabani KT, Zamboni WA. Ischemic preconditioning-induced microvascular protection at a distance. J Reconstr Microsurg 2004; 20: 175.
114. Kristiansen SB, Henning O, Kharbanda RK, et al. Remote preconditioning reduces ischemic injury in the explanted heart by a KATP channel-dependent mechanism. Am J Physiol Heart Circ Physiol 2005; 288: H1252.
115. Addison PD, Neligan PC, Ashrafpour H, et al. Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction. Am J Physiol Heart Circ Physiol 2003; 285: H1435.
116. Mabanta L, Valane P, Bourne J, Frame MD. Initiation of remote microvascular preconditioning requires K(ATP) channel activity. Am J Physiol Heart Circ Physiol 2006; 290: H264.