Skip to main content

Advertisement

SpringerLink
Log in

Myocardial remote ischemic preconditioning: from cell biology to clinical application

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Remote ischemic preconditioning (rIPC) is a cardioprotective phenomenon where brief periods of ischemia followed by reperfusion of one organ/tissue can confer subsequent protection against ischemia/reperfusion injury in other organs, such as the heart. It involves activation of humoral, neural or systemic communication pathways inducing different intracellular signals in the heart. The main purpose of this review is to summarize the possible mechanisms involved in the rIPC cardioprotection, and to describe recent clinical trials to establish the efficacy of these strategies in cardioprotection from lethal ischemia/reperfusion injury. In this sense, certain factors weaken the subcellular mechanisms of rIPC in patients, such as age, comorbidities, medication, and anesthetic protocol, which could explain the heterogeneity of results in some clinical trials. For these reasons, further studies, carefully designed, are necessary to develop a clearer understanding of the pathways and mechanism of early and late rIPC. An understanding of the pathways is important for translation to patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Przyklenk K, Bauer B, Ovize M, Kloner RA, Whittaker P (1993) Regional ischemic ‘preconditioning’ protects remote virgin myocardium from subsequent sustained coronary occlusion. Circulation 87:893–899. https://doi.org/10.1161/01.cir.87.3.893

    Article  CAS  PubMed  Google Scholar 

  2. Murry CE, Jennings RB, Reimer KA (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74:1124–1136. https://doi.org/10.1161/01.cir.74.5.1124

    Article  CAS  PubMed  Google Scholar 

  3. Kharbanda RK, Mortensen UM, White PA, Kristiansen SB, Schmidt MR, Hoschtitzky JA, Vogel M, Sorensen K, Redington AN, MacAllister R (2002) Transient limb ischemia induces remote ischemic preconditioning in vivo. Circulation 106:2881–2883. https://doi.org/10.1161/01.cir.0000043806.51912.9b

    Article  CAS  PubMed  Google Scholar 

  4. Lim SY, Hausenloy DJ (2012) Remote ischemic conditioning: from bench to bedside. Front Physiol 3:27. https://doi.org/10.3389/fphys.2012.00027

    Article  PubMed  PubMed Central  Google Scholar 

  5. Schoen M, Rotter R, Gierer P, Gradl G, Strauss U, Jonas L, Mittlmeier T, Vollmar B (2007) Ischemic preconditioning prevents skeletal muscle tissue injury, but not nerve lesion upon tourniquet-induced ischemia. J Trauma 63:788–797. https://doi.org/10.1097/01.ta.0000240440.85673.fc

    Article  PubMed  Google Scholar 

  6. Zarbock A, Van Aken H, Schmidt C (2015) Remote ischemic preconditioning and outcome: shall we all have an intermittent tourniquet? Curr Opin Anaesthesiol 28(2):165–171. https://doi.org/10.1097/ACO.0000000000000161

    Article  PubMed  Google Scholar 

  7. Stokfisz K, Ledakowicz-Polak A, Zagorski M, Zielinska M (2017) Ischaemic preconditioning–Current knowledge and potential future applications after 30 years of experience. Adv Med Sci 62(2):307–316. https://doi.org/10.1016/j.advms.2016.11.006

    Article  PubMed  Google Scholar 

  8. Hausenloy DJ, Yellon DM (2010) The second window of preconditioning (SWOP) where are we now? Cardiovasc Drugs Ther 24(3):235–254. https://doi.org/10.1007/s10557-010-6237-9

    Article  PubMed  Google Scholar 

  9. Walsh SR, Tang T, Sadat U, Dutka DP, Gaunt ME (2007) Cardioprotection by remote ischaemic preconditioning. Br J Anaesth 99:611–616. https://doi.org/10.1093/bja/aem273

    Article  CAS  PubMed  Google Scholar 

  10. Schmidt MR, Smerup M, Konstantinov IE, Shimizu M, Li J, Cheung M, White PA, Kristiansen SB, Sorensen K, Dzavik V, Redington AN, Kharbanda RK (2007) Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: first demonstration of remote ischemic perconditioning. Am J Physiol Heart Circ Physiol 292:H1883-1890. https://doi.org/10.1152/ajpheart.00617.2006

    Article  CAS  PubMed  Google Scholar 

  11. Dow J, Bhandari A, Simkhovich BZ, Hale SL, Kloner RA (2012) The effect of acute versus delayed remote ischemic preconditioning on reperfusion induced ventricular arrhythmias. J Cardiovasc Electrophysiol 23(12):1374–1383. https://doi.org/10.1111/j.1540-8167.2012.02397.x

    Article  PubMed  Google Scholar 

  12. Konstantinov IE, Arab S, Li J, Coles JG, Boscarino C, Mori A, Cukerman E, Dawood F, Cheung M, Shimizu M, Liu P, Redington AN (2005) The remote ischemic preconditioning stimulus modifies gene expression in mouse myocardium. J Thorac Cardiovasc Surg 130:1326–1332. https://doi.org/10.1016/j.jtcvs.2005.03.050

    Article  CAS  PubMed  Google Scholar 

  13. Konstantinov IE, Arab S, Kharbanda RK, Cheung M, Cherepanov V, Downey GP, Liu P, Cukerman E, Coles JG, Redington AN (2004) The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans. Physiol Genom 19:143–150. https://doi.org/10.1152/physiolgenomics.00046.2004

    Article  CAS  Google Scholar 

  14. Liem DA, te Lintel HM, Manintveld OC, Boomsma F, Verdouw PD, Duncker DJ (2005) 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 288:H1165-1172. https://doi.org/10.1152/ajpheart.00899.2004

    Article  CAS  PubMed  Google Scholar 

  15. Gho BC, Schoemaker RG, van den Doel MA, Duncker DJ, Verdouw PD (1996) Myocardial protection by brief ischemia in noncardiac tissue. Circulation 94:2193–2200. https://doi.org/10.1161/01.cir.94.9.2193

    Article  CAS  PubMed  Google Scholar 

  16. Donato M, Buchholz B, Rodríguez M, Pérez V, Inserte J, García-Dorado D, Gelpi RJ (2013) Role of the parasympathetic nervous system in cardioprotection by remote hindlimb ischaemic preconditioning. Exp Physiol 98(2):425–434. https://doi.org/10.1113/expphysiol.2012.066217

    Article  PubMed  Google Scholar 

  17. Konstantinov IE, Li J, Cheung MM, Shimizu M, Stokoe J, Kharbanda RK, Redington AN (2005) Remote ischemic preconditioning of the recipient reduces myocardial ischemia reperfusion injury of the denervated donor heart via a Katp channel-dependent mechanism. Transplantation 79:1691–1695. https://doi.org/10.1097/01.tp.0000159137.76400.5d

    Article  PubMed  Google Scholar 

  18. Dickson EW, Blehar DJ, Carraway RE, Heard SO, Steinberg G, Przyklenk K (2001) Naloxone blocks transferred preconditioning in isolated rabbit hearts. J Mol Cell Cardiol 33:1751–1756. https://doi.org/10.1006/jmcc.2001.1436

    Article  CAS  PubMed  Google Scholar 

  19. Shimizu M, Tropak M, Diaz RJ, Suto F, Surendra H, Kuzmin E, Li J, Gross G, Wilson GJ, Callahan J, Redington AN (2009) Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond) 117:191–200. https://doi.org/10.1042/CS20080523

    Article  CAS  Google Scholar 

  20. Jensen RV, Stottrup NB, Kristiansen SB, Bøtker HE (2012) Release of a humoral circulating cardioprotective factor by remote ischemic preconditioning is dependent on preserved neural pathways in diabetic patients. Basic Res Cardiol 107:285. https://doi.org/10.1007/s00395-012-0285-1

    Article  CAS  PubMed  Google Scholar 

  21. José Alburquerque-Béjar J, Barba I, Valls-Lacalle L, Ruiz-Meana M, Pecoraro M, Rodríguez-Sinovas A, García-Dorado D (2017) Remote ischemic conditioning provides humoural cross-species cardioprotection through glycine receptor activation. Cardiovasc Res 113(1):52–60. https://doi.org/10.1093/cvr/cvw242

    Article  CAS  PubMed  Google Scholar 

  22. Albrecht M, Zitta K, Bein B, Wennemuth G, Broch O, Renner J, Schuett T, Lauer F, Maahs D, Hummitzsch L, Cremer J, Zacharowski K, Meybohm P (2013) Remote ischemic preconditioning regulates HIF-1α levels, apoptosis and inflammation in heart tissue of cardiosurgical patients: a pilot experimental study. Basic Res Cardiol 108(1):314. https://doi.org/10.1007/s00395-012-0314-0

    Article  CAS  PubMed  Google Scholar 

  23. Gao Y, Song J, Chen H, Cao C, Lee C (2015) TRPV1 activation is involved in the cardioprotection of remote limb ischemic postconditioning in ischemia-reperfusion injury rats. Biochem Biophys Res Commun 463:1034–1039. https://doi.org/10.1016/j.bbrc.2015.06.054

    Article  CAS  PubMed  Google Scholar 

  24. Liem DA, Verdouw PD, Ploeg H, Kazim S, Duncker D (2002) Sites of action of adenosine in interorgan preconditioning of the heart. Am J Physiol Heart Circ Physiol 283:H29–H37. https://doi.org/10.1152/ajpheart.01031.2001

    Article  CAS  PubMed  Google Scholar 

  25. Hildebrandt HA, Kreienkamp V, Gent S, Kahlert P, Heusch G, Kleinbongard P (2016) Kinetics and signal activation properties of circulating factor(s) from healthy volunteers undergoing remote ischemic pre-conditioning. JACC Basic Transl Sci 1(1–2):3–13. https://doi.org/10.1016/j.jacbts.2016.01.007

    Article  PubMed  PubMed Central  Google Scholar 

  26. Basalay MV, Mastitskaya S, Mrochek A, Ackland GL, Del Arroyo AG, Sanchez J, Sjoquist PO, Pernow J, Gourine AV, Gourine A (2016) Glucagon-like peptide-1 (GLP-1) mediates cardioprotection by remote ischaemic conditioning. Cardiovasc Res 112(3):669–676. https://doi.org/10.1093/cvr/cvw216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rassaf T, Totzeck M, Hendgen-Cotta UB, Shiva S, Heusch G, Kelm M (2014) Circulating nitrite contributes to cardioprotection by remote ischemic preconditioning. Circ Res 114(10):1601–1610. https://doi.org/10.1161/CIRCRESAHA.114.303822

    Article  CAS  PubMed  Google Scholar 

  28. Heusch G (2015) Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ Res 116:674–699. https://doi.org/10.1161/CIRCRESAHA.116.305348

    Article  CAS  PubMed  Google Scholar 

  29. Shimizu M, Tropak M, Diaz RJ, Suto F, Surendra H, Kuzmin E, Li J, Gross G, Wilson GJ, Callahan J, Redington AN (2009) Transient limb ischaemia remotely preconditions through a humoral mechanism acting directly on the myocardium: evidence suggesting cross-species protection. Clin Sci (Lond) 117(5):191–200. https://doi.org/10.1042/CS20080523

    Article  CAS  Google Scholar 

  30. Wever KE, Menting TP, Maroeska Rovers J, van der Vliet A, Rongen GA, Masereeuw R, Ritskes-Hoitinga M, Hooijmans CR, Warlé M (2012) Ischemic preconditioning in the animal kidney, a systematic review and meta-analysis. PLoS ONE 7(2):e32296. https://doi.org/10.1371/journal.pone.0032296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Johnsen J, Pryds K, Salman R, Løfgren B, Kristiansen SB, Bøtker HE (2016) The remote ischemic preconditioning algorithm: effect of number of cycles, cycle duration and effector organ mass on efficacy of protection. Basic Res Cardiol 111(2):10. https://doi.org/10.1007/s00395-016-0529-6

    Article  PubMed  Google Scholar 

  32. Basalay MV, Davidson SM, Gourine AV, Yellon DM (2018) Neural mechanisms in remote ischaemic conditioning in the heart and brain: mechanistic and translational aspects. Basic Res Cardiol 113(4):25. https://doi.org/10.1007/s00395-018-0684-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Donato M, Goyeneche MA, Garces M, Marchini T, Pérez V, Del Mauro J, Höcht C, Rodríguez M, Evelson P, Gelpi RJ (2016) Myocardial triggers involved in activation of remote ischaemic preconditioning. Exp Physiol 101(6):708–716. https://doi.org/10.1113/EP085535

    Article  CAS  PubMed  Google Scholar 

  34. Mastitskaya S, Marina N, Gourine A, Gilbey MP, Spyer KM, Teschemacher AG, Kasparov S, Trapp S, Ackland GL, Gourine AV (2012) Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal pre-ganglionic neurones. Cardiovasc Res 95(4):487–494. https://doi.org/10.1093/cvr/cvs212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hausenloy DJ, Bøtker HE, Ferdinandy P, Heusch G, Ng GA, Redington A, Garcia-Dorado D (2019) Cardiac innervation in acute myocardial ischaemia/reperfusion injury and cardioprotection. Cardiovasc Res 115(7):1167–1177. https://doi.org/10.1093/cvr/cvz053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kingma JG, Simard D, Rouleau JR (2017) Influence of cardiac nerve status on cardiovascular regulation and cardioprotection. World J Cardiol 9(6):508–520. https://doi.org/10.4330/wjc.v9.i6.508

    Article  PubMed  PubMed Central  Google Scholar 

  37. Jia J, Li J, Jiang L, Zhang J, Chen S, Wang L, Zhou Y, Xie H, Zhou L, Zheng S (2015) Protective effect of remote limb ischemic perconditioning on the liver grafts of rats with a novel model. PLoS ONE 10(3):e0121972. https://doi.org/10.1371/journal.pone.0121972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Li G, Labruto F, Sirsjo A, Chen F, Vaage J, Valen G (2004) Myocardial protection by remote preconditioning: the role of nuclear factor kappa-B p105 and inducible nitric oxide synthase. Eur J Cardiothorac Surg 26:968–973. https://doi.org/10.1016/j.ejcts.2004.06.015

    Article  PubMed  Google Scholar 

  39. Kim YM, Kim TH, Seol DW, Talanian RV, Billiar TR (1998) Nitric oxide suppression of apoptosis occurs in association with an inhibition of Bcl-2 cleavage and cytochrome c release. J Biol Chem 273:31437–31441. https://doi.org/10.1074/jbc.273.47.31437

    Article  CAS  PubMed  Google Scholar 

  40. Kim YM, Talanian RV, Li J, Billiar T (1998) Nitric oxide prevents IL-1beta and IFN-gamma-inducing factor (IL-18) release from macrophages by inhibiting caspase-1 (IL-1beta-converting enzyme). J Immunol 161:4122–4128

    CAS  PubMed  Google Scholar 

  41. Yamaguchi T, Izumi Y, Nakamura Y, Yamazaki T, Shiota M, Sano S, Tanaka M, Osada-Oka M, Shimada K, Miura K, Yoshiyama M, Iwao H (2015) Repeated remote ischemic conditioning attenuates left ventricular remodeling via exosome-mediated intercellular communication on chronic heart failure after myocardial infarction. Int J Cardiol 178:239–246. https://doi.org/10.1016/j.ijcard.2014.10.144

    Article  PubMed  Google Scholar 

  42. Wei M, Xin P, Li S, Tao J, Li Y, Li J, Liu M, Li J, Zhu W, Redington AN (2011) Repeated remote ischemic postconditioning protects against adverse left ventricular remodeling and improves survival in a rat model of myocardial infarction. Circ Res 108(10):1220–1225. https://doi.org/10.1161/CIRCRESAHA.110.236190

    Article  CAS  PubMed  Google Scholar 

  43. Pilz PM, Hamza O, Gidlöf O, Gonçalves IF, Tretter EV, Trojanek S, Abraham D, Heber S, Haller PM, Podesser BK, Kiss A (2019) Remote ischemic perconditioning attenuates adverse cardiac remodeling and preserves left ventricular function in a rat model of reperfused myocardial infarction. Int J Cardiol 285:72–79. https://doi.org/10.1016/j.ijcard.2019.03.003

    Article  PubMed  Google Scholar 

  44. Chen H, Jing X-Y, Shen Y-J, Wang T-L, Ou C, Lu S-F, Cai Y, Li Q, Chen X, Ding Y-J, Yu X-C, Zhu B-M (2018) Stat5-dependent cardioprotection in late remote ischaemia preconditioning. Cardiovasc Res 114:679–689. https://doi.org/10.1093/cvr/cvy014

    Article  CAS  PubMed  Google Scholar 

  45. Heusch G, Musiolik J, Kottenberg E, Peters J, Jakob H, Thielmann M (2012) STAT5 activation and cardioprotection by remote ischemic preconditioning in humans: short communication. Circ Res 110:111–115. https://doi.org/10.1093/cvr/cvy014

    Article  CAS  PubMed  Google Scholar 

  46. Billah M, Ridiandries A, Rayner BS, Allahwala UK, Dona A, Khachigian LM, Bhindi R (2019) Egr-1 functions as a master switch regulator of remote ischemic preconditioning-induced cardioprotection. Basic Res Cardiol 115:3–3. https://doi.org/10.1007/s00395-019-0763-9

    Article  CAS  PubMed  Google Scholar 

  47. Chen C, Jiang W, Liu Z, Li F, Yang J, Zhao Y, Ran Y, Meng Y, Ji X, Geng X, Du H, Hu X (2018) Splenic responses play an important role in remote ischemic preconditioning-mediated neuroprotection against stroke. J Neuroinflamm 15:167. https://doi.org/10.1186/s12974-018-1190-9

    Article  CAS  Google Scholar 

  48. Pearce L, Davidson SM, Yellon DM (2021) Does remote ischaemic conditioning reduce inflammation? A focus on innate immunity and cytokine response. Basic Res Cardiol 116:12. https://doi.org/10.1007/s00395-021-00852-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Manukyan MC, Alvernaz CH, Poynter JA, Wang Y, Brewster BD, Weil BR, Abarbanell AM, Herrmann JL, Crowe BJ, Keck AC, Meldrum DR (2011) Interleukin-10 protects the ischemic heart from reperfusion injury via the STAT3 pathway. Surgery 150:231–239. https://doi.org/10.1016/j.surg.2011.05.017

    Article  PubMed  Google Scholar 

  50. Hausenloy DJ, Yellon DM (2008) Remote ischaemic preconditioning: underlying mechanisms and clinical application. Cardiovasc Res 79:377–386. https://doi.org/10.1093/cvr/cvn114

    Article  CAS  PubMed  Google Scholar 

  51. Crowley LE, McIntyre CW (2013) Remote ischaemic conditioning—therapeutic opportunities in renal medicine. Nat Rev Nephrol 9:739–746. https://doi.org/10.1038/nrneph.2013.226

    Article  PubMed  Google Scholar 

  52. Wever KE, Menting TP, Rovers M, van der Vliet JA, Rongen GA, Masereeuw R, Ritskes-Hoitinga M, Hooijmans CR, Warlé M (2012) Ischemic preconditioning in the animal kidney, a systematic review and meta-analysis. PLoS ONE 7(2):e32296. https://doi.org/10.1371/journal.pone.0032296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Jan WC, Chen CH, Tsai PS, Huang CJ (2011) Limb ischemic preconditioning mitigates lung injury induced by haemorrhagic shock/resuscitation in rats. Resuscitation 82:760–766. https://doi.org/10.1016/j.resuscitation.2011.02.010

    Article  PubMed  Google Scholar 

  54. Peralta C, Fernandez L, Panes J, Prats N, Sans M, Pique JM, Gelpi E, Rosello-Catafau J (2001) 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 33:100–113. https://doi.org/10.1053/jhep.2001.20529

    Article  CAS  PubMed  Google Scholar 

  55. Olguner C, Koca U, Kar A, Karci A, Islekel H, Canyilmaz M, Mavioglu O, Kizildag S, Unlu G, Elar Z (2006) Ischemic preconditioning attenuates the lipid peroxidation and remote lung injury in the rat model of unilateral lower limb ischemia reperfusion. Acta anaesthesiol Scand 50:150–155. https://doi.org/10.1111/j.1399-6576.2006.00938.x

    Article  CAS  PubMed  Google Scholar 

  56. Xia Z, Herijgers P, Nishida T, Ozaki S, Wouters P, Flameng W (2003) Remote preconditioning lessens the deterioration of pulmonary function after repeated coronary artery occlusion and reperfusion in sheep. Can J Anaesth 50:481–488. https://doi.org/10.1007/BF03021061

    Article  PubMed  Google Scholar 

  57. Lai IR, Chang KJ, Chen CF, Tsai HW (2006) Transient limb ischemia induces remote preconditioning in liver among rats: the protective role of heme oxygenase-1. Transplantation 81:1311–1317. https://doi.org/10.1097/01.tp.0000203555.14546.63

    Article  CAS  PubMed  Google Scholar 

  58. Gustafsson BI, Friman S, Wallin M, Heiman J, Delbro DS (2006) Effect of remote preconditioning on mild or severe ischemia-reperfusion injury to rat liver. Transplant Proc 38:2708–2709. https://doi.org/10.1016/j.transproceed.2006.07.044

    Article  CAS  PubMed  Google Scholar 

  59. Wang F, Birch SE, He R, Tawadros P, Szaszi K, Kapus A, Rotstein OD (2010) Remote ischemic preconditioning by hindlimb occlusion prevents liver ischemic/reperfusion injury: the role of high mobility group-box 1. Ann Surg 251:292–299. https://doi.org/10.1097/SLA.0b013e3181bfda8c

    Article  PubMed  Google Scholar 

  60. Kanoria S, Jalan R, Davies NA, Seifalian AM, Williams R, Davidson BR (2006) Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. Br J Surg 93:762–768. https://doi.org/10.1002/bjs.5331

    Article  CAS  PubMed  Google Scholar 

  61. Meng R, Asmaro K, Meng L, Liu Y, Ma C, Xi C, Li G, Ren C, Luo Y, Ling F, Jia J, Hua Y, Wang X, Ding Y, Lo EH, Ji X (2012) Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 79(18):1853–1861. https://doi.org/10.1212/WNL.0b013e318271f76a

    Article  PubMed  Google Scholar 

  62. Walsh SR, Nouraei SA, Tang TY, Sadat U, Carpenter RH, Gaunt ME (2010) Remote ischemic preconditioning for cerebral and cardiac protection during carotid endarterectomy: results from a pilot randomized clinical trial. Vascul Endovasc Surg 44:434–439. https://doi.org/10.1177/1538574410369709

    Article  Google Scholar 

  63. Chen C, Jiang W, Liu Z, Li F, Yang J, Zhao Y, Ran Y, Meng Y, Ji X, Geng X, Du H, Hu X (2018) Splenic responses play an important role in remote ischemic preconditioning-mediated neuroprotection against stroke. J Neuroinflamm 15(1):167. https://doi.org/10.1186/s12974-018-1190-9

    Article  CAS  Google Scholar 

  64. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN (2006) Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol 47:2277–2282. https://doi.org/10.1016/j.jacc.2006.01.066

    Article  PubMed  Google Scholar 

  65. Hausenloy DJ, Mwamure PK, Venugopal V, Harris J, Barnard M, Grundy E, Ashley E, Vichare S, Di Salvo C, Kolvekar S, Hayward M, Keogh B, MacAllister RJ, Yellon DM (2007) Effect of remote ischaemic preconditioning on myocardial injury in patients undergoing coronary artery bypass graft surgery: a randomised controlled trial. Lancet 370:575–579. https://doi.org/10.1016/S0140-6736(07)61296-3

    Article  PubMed  Google Scholar 

  66. Hausenloy DJ (2013) Cardioprotection techniques: preconditioning, postconditioning and remote conditioning (basic science). Curr Pharm Des 19(25):4544–4563. https://doi.org/10.2174/1381612811319250004

    Article  CAS  PubMed  Google Scholar 

  67. Pickard JM, Bøtker HE, Crimi G, Davidson B, Davidson SM, Dutka D, Ferdinandy P, Ganske R, Garcia-Dorado D, Giricz Z, Gourine AV, Heusch G, Kharbanda R, Kleinbongard P, MacAllister R, McIntyre C, Meybohm P, Prunier F, Redington A, Robertson NJ, Suleiman MS, Vanezis A, Walsh S, Yellon DM, Hausenloy DJ (2015) Remote ischemic conditioning: from experimental observation to clinical application: report from the 8th Biennial Hatter Cardiovascular Institute workshop. Basic Res Cardiol 110(1):453. https://doi.org/10.1007/s00395-014-0453-6

    Article  PubMed  Google Scholar 

  68. Hausenloy DJ, Garcia-Dorado D, Bøtker HE, Davidson SM, Downey J, Engel FB, Jennings R, Lecour S, Leor J, Madonna R, Ovize M, Perrino C, Prunier F, Schulz R, Sluijter JPG, Van Laake LW, Vinten-Johansen J, Yellon DM, Ytrehus K, Heusch G, Ferdinandy P (2017) Novel targets and future strategies for acute cardioprotection: position paper of the European Society of Cardiology working group on cellular biology of the heart. Cardiovasc Res 113(6):564–585. https://doi.org/10.1093/cvr/cvx049

    Article  CAS  PubMed  Google Scholar 

  69. Hong DM, Lee EH, Kim HJ, Min JJ, Chin JH, Choi DK, Bahk JH, Sim JY, Choi IC, Jeon Y (2014) Does remote ischaemic preconditioning with postconditioning improve clinical outcomes of patients undergoing cardiac surgery? Remote ischaemic preconditioning with postconditioning outcome trial. Eur Heart J 35(3):176–183. https://doi.org/10.1093/eurheartj/eht346

    Article  PubMed  Google Scholar 

  70. Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, Knight R, Kunst G, Laing C, Nicholas J, Pepper J, Robertson S, Xenou M, Clayton T, Yellon DM, Trial Investigators ERICCA (2015) Remote ischemic preconditioning and outcomes of cardiac surgery. N Engl J Med 373(15):1408–1417. https://doi.org/10.1056/NEJMoa1413534

    Article  CAS  PubMed  Google Scholar 

  71. Meybohm P, Bein B, Brosteanu O, Cremer J, Gruenewald M, Stoppe C, Coburn M, Schaelte G, Böning A, Niemann B, Roesner J, Kletzin F, Strouhal U, Reyher C, Laufenberg-Feldmann R, Ferner M, Brandes IF, Bauer M, Stehr SN, Kortgen A, Wittmann M, Baumgarten G, Meyer-Treschan T, Kienbaum P, Heringlake M, Schön J, Sander M, Treskatsch S, Smul T, Wolwender E, Schilling T, Fuernau G, Hasenclever D, Zacharowski K, RIPHeart Study Collaborators (2015) A multicenter trial of remote ischemic preconditioning for heart surgery. N Engl J Med 373(15):1397–1407. https://doi.org/10.1056/NEJMoa1413579

    Article  CAS  PubMed  Google Scholar 

  72. Kottenberg E, Thielmann M, Bergmann L, Heine T, Jakob H, Heusch G, Peters J (2012) Protection by remote ischemic preconditioning during coronary artery bypass graft surgery with isoflurane but not propofol - a clinical trial. Acta Anaesthesiol Scand 56:30–38. https://doi.org/10.1111/j.1399-6576.2011.02585.x

    Article  CAS  PubMed  Google Scholar 

  73. Kottenberg E, Musiolik J, Thielmann M, Jakob H, Peters J, Heusch G (2014) Interference of propofol with signal transducer and activator of transcription 5 activation and cardioprotection by remote ischemic preconditioning during coronary artery bypass grafting. J Thorac Cardiovasc Surg 147(1):376–382. https://doi.org/10.1016/j.jtcvs.2013.01.005

    Article  CAS  PubMed  Google Scholar 

  74. Venugopal V, Ludman A, Yellon DM, Hausenloy DJ (2009) ‘Conditioning’ the heart during surgery. Eur J Cardiothorac Surg 35(6):977–987. https://doi.org/10.1016/j.ejcts.2009.02.014

    Article  PubMed  Google Scholar 

  75. Dezfulian C, Taft M, Corey C, Hill G, Krehel N, Rittenberger JC, Guyette FX, Shiva S (2017) Biochemical signaling by remote ischemic conditioning of the arm versus thigh: is one raise of the cuff enough? Redox Biol 12:491–498. https://doi.org/10.1016/j.redox.2017.03.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Yellon DM, Ackbarkhan AK, Balgobin V, Bulluck H, Deelchand A, Dhuny MR, Domah N, Gaoneadry D, Jagessur RK, Joonas N, Kowlessur S, Lutchoo J, Nicholas JM, Pauvaday K, Shamloll O, Walker JM, Hausenloy DJ (2015) Remote ischemic conditioning reduces myocardial infarct size in STEMI patients treated by thrombolysis. J Am Coll Cardiol 65(25):2764. https://doi.org/10.1016/j.jacc.2015.02.082

    Article  PubMed  Google Scholar 

  77. Gong R, Wu YQ (2019) Remote ischemic conditioning during primary percutaneous coronary intervention in patients with ST-segment elevation myocardial infarction: a systematic review and meta-analysis. J Cardiothorac Surg 14(1):14. https://doi.org/10.1186/s13019-019-0834-x

    Article  PubMed  PubMed Central  Google Scholar 

  78. Wang X, Kong N, Zhou C, Mungun D, Iyan Z, Guo Y, Yang Z (2017) Effect of remote ischemic preconditioning on perioperative cardiac events in patients undergoing elective percutaneous coronary intervention: a meta-analysis of 16 randomized trials. Cardiol Res Pract 2017:6907167. https://doi.org/10.1155/2017/6907167

    Article  PubMed  PubMed Central  Google Scholar 

  79. Manchurov V, Ryazankina N, Khmara T, Skrypnik D, Reztsov R, Vasilieva E, Shpektor A (2014) Remote ischemic preconditioning and endothelial function in patients with acute myocardial infarction and primary PCI. Am J Med 127(7):670–673. https://doi.org/10.1016/j.amjmed.2014.02.012

    Article  PubMed  Google Scholar 

  80. Hausenloy DJ, Kharbanda RK, Møller UK, Ramlall M, Aarøe J, Butler R, Bulluck H, Clayton T, Dana A, Dodd M, Engstrom T, Evans R, Lassen JF, Christensen EF, Garcia-Ruiz JM, Gorog DA, Hjort J, Houghton RF, Ibanez B, Knight R, Lippert FK, Lønborg JT, Maeng M, Milasinovic D, More R, Nicholas JM, Jensen LO, Perkins A, Radovanovic N, Rakhit RD, Ravkilde J, Ryding AD, Schmidt MR, Riddervold IS, Sørensen HT, Stankovic G, Varma M, Webb I, Terkelsen CJ, Greenwood JP, Yellon DM, Bøtker HE, CONDI-2/ERIC-PPCI Investigators (2019) Effect of remote ischaemic conditioning on clinical outcomes in patients with acute myocardial infarction (CONDI-2/ERIC-PPCI): a single-blind randomised controlled trial. Lancet 394(10207):1415–1424. https://doi.org/10.1016/S0140-6736(19)32039-2

    Article  PubMed  PubMed Central  Google Scholar 

  81. Boengler K, Schulz R, Heusch G (2009) Loss of cardioprotection with ageing. Cardiovasc Res 83:247–261

    Article  CAS  Google Scholar 

  82. Jensen RV, Zachara NE, Nielsen PH, Kimose HH, Kristiansen SB, Bøtker HE (2013) Impact of O-GlcNAc on cardioprotection by remote ischaemic preconditioning in non-diabetic and diabetic patients. Cardiovasc Res 97(2):369–378. https://doi.org/10.1093/cvr/cvp033

    Article  CAS  PubMed  Google Scholar 

  83. Kristiansen SB, Lofgren B, Nielsen JM, Stottrup NB, Buhl ES, Nielsen-Kudsk JE, Nielsen TT, Rungby J, Flyvbjerg A, Bøtker HE (2011) Comparison of two sulfonylureas with high and low myocardial K (ATP) channel affinity on myocardial infarct size and metabolism in a rat model of type 2 diabetes. Diabetologia 54:451–458. https://doi.org/10.1007/s00125-010-1970-y

    Article  CAS  PubMed  Google Scholar 

  84. Kottenberg E, Thielmann M, Kleinbongard P, Frey UH, Heine T, Jakob H, Heusch G, Peters J (2014) Myocardial protection by remote ischaemic pre-conditioning is abolished in sulphonylurea-treated diabetics undergoing coronary revascularisation. Acta Anaesthesiol Scand 58:453–462. https://doi.org/10.1111/aas.12278

    Article  CAS  PubMed  Google Scholar 

  85. Ye Y, Perez-Polo JR, Aguilar D, Birnbaum Y (2011) The potential effects of anti-diabetic medications on myocardial ischemia-reperfusion injury. Basic Res Cardiol 106:925–952. https://doi.org/10.1007/s00395-011-0216-6

    Article  CAS  PubMed  Google Scholar 

  86. Kloner RA, Nesto RW (2008) Glucose-insulin-potassium for acute myocardial infarction: continuing controversy over cardioprotection. Circulation 117:2523–2533. https://doi.org/10.1161/CIRCULATIONAHA.107.697979

    Article  PubMed  Google Scholar 

  87. Lexis CPH, Wieringa WG, Hiemstra B, van Deursen V, Lipsic E, van der Harst P, van Veldhuisen DJ, van der Horst IC (2014) Chronic metformin treatment is associated with reduced myocardial infarct size in diabetic patients with ST-segment elevation myocardial infarction. Cardiovasc Drugs Ther 28:163–171. https://doi.org/10.1007/s10557-013-6504-7

    Article  CAS  PubMed  Google Scholar 

  88. Alburquerque-Béjar JJ, Barba I, Inserte J, Miró-Casas E, Ruiz-Meana M, Poncelas M, Vilardosa Ú, Valls-Lacalle L, Rodríguez-Sinovas A, Garcia-Dorado D (2015) Combination therapy with remote ischaemic conditioning and insulin or exenatide enhances infarct size limitation in pigs. Cardiovasc Res 107(2):246–254. https://doi.org/10.1093/cvr/cvv171

    Article  CAS  PubMed  Google Scholar 

  89. Lim VG, Bell RM, Arjun S, Kolatsi-Joannou M, Long DA, Yellon DM (2019) SGLT2 Inhibitor, canagliflozin, attenuates myocardial infarction in the diabetic and nondiabetic heart. J Am Col Cardiol Basic Transl Sci 4:15–26. https://doi.org/10.1016/j.jacbts.2018.10.002

    Article  Google Scholar 

Download references

Funding

This work was supported by a research grant from National Agency for Scientific and Technological Promotion [ANPCyT, PICT 2017-1447] and the University of Buenos Aires [UBACYT 20020150100105BA].

Author information

Author notes

  1. Martín Donato, Verónica D´Annunzio, and Ricardo J. Gelpi are Members of the National Council of Scientific and Technological Research (CONICET).

Authors and Affiliations

  1. Department of Pathology, Faculty of Medicine, Institute of Cardiovascular Pathophysiology (INFICA), University of Buenos Aires, 950 J. E. Uriburu, 2nd floor, C1114AAD, Buenos Aires, Argentina

    Martín Donato, Eliana P. Bin, Verónica D´Annunzio & Ricardo J. Gelpi

  2. Institute of Biochemistry and Molecular Medicine (IBIMOL, UBA-CONICET), Buenos Aires, Argentina

    Martín Donato, Eliana P. Bin, Verónica D´Annunzio & Ricardo J. Gelpi

Authors
  1. Martín Donato
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eliana P. Bin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Verónica D´Annunzio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo J. Gelpi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MD, VD´A, and RJG conceived and designed the review. EPB designed the review and the figures.

Corresponding author

Correspondence to Ricardo J. Gelpi.

Ethics declarations

Conflict of interest

The authors have not conflict of interest.

Ethics approval

The procedures used in the mentioned studies, in which we are authors were approved by the Animal Care and Research Committee of the University of Buenos Aires (Protocol number 2948/10) and were in compliance with the Guide for the Care and Use of Laboratory Animals published by the US National Institutes of Health in 2011.

Informed consent

All the authors gave their consent to participate and publish the review.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Donato, M., Bin, E.P., D´Annunzio, V. et al. Myocardial remote ischemic preconditioning: from cell biology to clinical application. Mol Cell Biochem 476, 3857–3867 (2021). https://doi.org/10.1007/s11010-021-04192-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-021-04192-4

Keywords

Search

Navigation