Skip to main content

Advertisement

Log in

Hypoxic Preconditioning – a Phenomenon Increasing the Tolerance of Cardiomyocytes to Hypoxia/Reoxygenation

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Most studies addressing the question of hypoxic preconditioning (HP) are performed on isolated cardiomyocytes. There are relatively few reports on delayed HP in vivo and only occasional studies have addressed early preconditioning in vivo. HP has been found to restrict necrosis and apoptosis of cardiomyocytes and to improve the contractility of the isolated heart in ischemia (hypoxia) and reperfusion (reoxygenation). Evidence has been obtained indicating that adenosine is a trigger for HP in vitro. NO is a trigger for HP in in vitro and in vivo experiments. Reactive oxygen species were also found to be triggers for hypoxic preconditioning. ERK1/2 and p38 kinase have been shown to play important roles in delayed HP in vitro. Data showing that Akt kinase and PI3 kinase are also involved in hypoxic preconditioning in vitro have been obtained. KATP channels and KCa channels may be mediators and, perhaps, end effectors of late HP. Hypoxic preconditioning activates the following transcription factors: HIF-1α, HIF-3α, GATA-4, and NF-κB. The end effectors of HP may be the proteins HSP90, GRP78, 14-3-3, Bcl-2, Bcl-xL, BAD, and iNOS.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. M. V. Bilenko, Ischemic and Reperfusion Damage to Organs [in Russian], Meditsina, Moscow (1989).

    Google Scholar 

  2. A. G. Portnichenko, M. I. Vasilenko, and A. A. Moibenko, “The effects of acute hypoxic hypoxia on the induction of nitric oxide synthase in rats,” Fiziol. Zh., 49, No. 3, 47–49 (2003).

    CAS  Google Scholar 

  3. A. G. Portnichenko, M. I. Vasilenko,V. I. Portnichenko, and A. A. Moibenko, “Acute hypoxic hypoxia as an inducer of delayed cardioprotection in rats,” in: Hypoxia, Automated Analysis of Hypoxic States. Collected Studies [in Russian], A. Z. Kolchinskaya (ed.), Nalchik, Moscow (2005), Vol. 1, pp. 185–190.

  4. A. G. Portnichenko, K. V. Rozova, M. I. Vasilenko, and O. O. Moibenko, “Age characteristics of ultrastructural changes in the myocardium in hypoxic preconditioning and ischemia-reperfusion of isolated rat hearts,” Fiziol. Zh., 53, No. 4, 27–34 (2007).

    Google Scholar 

  5. A. G. Portnichenko, M. I. Vasilenko, and O. O. Moibenko, “The role of potassium channels in the effector mechanisms of cardioprotection in late preconditioning of the rat heart,” Patologiya, 5, No. 3, 61–62 (2008).

    Google Scholar 

  6. A. G. Portnichenko, “The phenomenon of late preconditioning of the myocardium or phenotypic cardioprotection,” in: Endogenous Mechanisms of Cardioprotection as the Basis of the Pathogenetic Therapy of Heart Diseases [in Russian], A. A. Moibenko, V. E. Dosenko, and A. N. Parkhomenko (eds.), NVP Vidavnitstvo “Naukova Dumka,” Ukrainian National Academy of Sciences, Kiev (2008), pp. 305–331.

  7. A. Aries, P. Paradis, C. Lefebvre, R. J. Schwartz, and M. Nemer, “Essential role of GATA-4 in cell survival and drug-induced cardiotoxicity,” Proc. Natl. Acad. Sci. USA, 101, No. 18, 6975–6980 (2004).

    Article  PubMed  CAS  Google Scholar 

  8. M. A. Arstall, Y. Z. Zhao, L. Hornberger, S. P. Kennedy, R. A. Buchholz, R. Osathamondh, and R. A. Kelly, “Human ventricular myocytes in vitro exhibit both early and delayed preconditioning responses to simulated ischemia,” J. Mol. Cell. Cardiol., 30, No. 5, 1019–1025 (1998).

    Article  PubMed  CAS  Google Scholar 

  9. K. Ban, A. J. Cooper, S. Samuel, A. Bhatti, M. Patel, S. Izumo, J. M. Penninger, P. H. Backx, G. Y. Oudit, and R. G. Tsushima, “Phosphatidyinositol 3-kinase gamma is a critical mediator of myocardial ischemic and adenosine-mediated preconditioning,” Circ. Res., 103, No. 6, 643–653 (2008).

    Article  PubMed  CAS  Google Scholar 

  10. S. Banerjee, X. L. Tank, Y. Qiu, H. Takano, S. Manchikalapudi, B. Dawn, G. Shirk, and R. Bolli, “Nitroglycerin induces late preconditioning against myocardial stunning via a PKC-dependent pathway,” Am. J. Physiol., 277, No. 6, Part 2, H2488–H2494 (1999).

    PubMed  CAS  Google Scholar 

  11. P. C. Beguin, M. Joyeux-Faure, D. Godin-Ribuot, P. Lévy, and C. Ribuot, “Acute intermittent hypoxia improves rat myocardium tolerance to ischemia,” J. Appl. Physiol., 99, No. 3, 1064–1069 (2005).

    Article  PubMed  CAS  Google Scholar 

  12. P. C. Beguin, E. Belaidi, D. Godin-Ribuot, P. Lévy, and C. Ribuot, “Intermittent hypoxia-induced delayed cardioprotection is mediated by PKC and triggered by p38 MAP kinase and Erk1/2,” J. Mol. Cell. Cardiol., 42, No. 2, 343–351 (2007).

    Article  PubMed  CAS  Google Scholar 

  13. I. J. Benjamin and D. R. McMillan, “Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease,” Circ. Res., 83, No. 2, 117–132 (1998).

    PubMed  CAS  Google Scholar 

  14. M. Bernaudin and F. R. Sharp, “Methods to detect hypoxia-induced ischemic tolerance in the brain,” Meth. Enzymol., 381, 399–416 (2004).

    Article  PubMed  CAS  Google Scholar 

  15. W. M. Bernhardt, C. Warnecke, C. William, T. Tanaka, M. S. Wiesener, and K. U. Eckardt, “Organ protection by hypoxia and hypoxia-inducible factors,” Meth. Enzymol., 435, 221–245 (2007).

    PubMed  CAS  Google Scholar 

  16. I. Bin-Jaliah, H. I. Ammar, D. P. Mikhailidis, M. A. Dallak, F. H. Al-Hashem, M. A. Haidara, H. Z. Yassin, A. A. Bahnasi, L. A. Rashed, and E. R. Isenovic, “Cardiac adaptive responses after hypoxia in an experimental model,” Angiology, 61, No. 2, 145–156 (2010).

    Article  PubMed  CAS  Google Scholar 

  17. Z. Cai, D. J. Manalo, G. Wei, E. R. Rodriguez, K. Fox-Talbot, H. Lu, J. L. Zweier, and G. L. Semenza, “Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury,” Circulation, 108, No. 1, 79–85 (2003).

    Article  PubMed  CAS  Google Scholar 

  18. Z. Cai, H. Zhong, M. Bosch-Marce, K. Fox-Talbot, L. Wang, C. Wei, M. A. Trush, and G. L. Semenza, “Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1α,” Cardiovasc. Res., 77, No. 3, 463–470 (2008).

    Article  PubMed  CAS  Google Scholar 

  19. F. Charron, G. Tsimiklis, M. Arcand, L. Robitaille, Q. Liang, J. D. Molkentin, S. Meloche, and M. Nemer, “Tissue-specific GATA factors are transcriptional effectors of the small GTPase RhoA,” Genes Dev., 15, No. 20, 2702–2719 (2001).

    Article  PubMed  CAS  Google Scholar 

  20. H. P. Chen, M. He,Y. L. Xu, Q. R. Huang, G. H. Huang, G. H. Zeng, D. Liu, and Z. P. Liao, “Anoxic preconditioning up-regulates 14-3-3 protein expression in neonatal rat cardiomyocytes through extracellular signal-regulated kinase 1/2,” Life Sci., 81, No. 5, 372–379 (2007).

    Article  PubMed  CAS  Google Scholar 

  21. Y. Y. Chen and Q. Xia, “Evaluation of Gi/o protein signal transduction pathway in cardioprotection of hypoxic preconditioning,” Acta physiol. Sin., 52, No. 2, 93–97 (2000).

    CAS  Google Scholar 

  22. D. V. Cuong, N. Kim, J. B. Youm, H. Joo, M. Warda, J. W. Lee, W. S. Park, T. Kim, S. Kang, H. Kim, and J. Han, “Nitric oxidecGMP-protein kinase G signaling pathway induces anoxic preconditioning through activation of ATP-sensitive K + channels in rat hearts,” Am. J. Physiol. Heart Circ. Physiol., 290, No. 5, H1808–H1817 (2006).

    Article  PubMed  Google Scholar 

  23. B. Dawn and R. Bolli, “Role of nitric oxide in myocardial preconditioning,” Ann. N.Y. Acad. Sci., 962, 18–41 (2002).

    Article  PubMed  CAS  Google Scholar 

  24. T. Eckjle, D. Köhler, R. Lehmann, K. El Kasmi, and H. K. Eltzschig, “Hypoxia-inducible factor-1 is central to cardioprotection: a new paradigm for ischemic preconditioning,” Circulation, 118, No. 2, 166–175 (2008).

    Article  Google Scholar 

  25. K. Z. Gong, Z. G. Zhang, A.H. Li, Y. F. Huang, P. Bu, F. Dong, and J. Liu, “ROS-mediated ERK activation in delayed protection from anoxic preconditioning in neonatal rat cardiomyocytes,” Chin. J. Med., 117, No. 3, 395–400 (2004).

    Google Scholar 

  26. Y. Honma, M. Tani, M. Takayama, K. Yamamura, and H. Hasegawa, “Aging abolishes the cardioprotective effect of combination heat shock and hypoxic preconditioning in reperfused rat hearts,” Basic Res. Cardiol., 67, No. 6, 489–495 (2002).

    Article  Google Scholar 

  27. Y. F. Huang, K. Z. Gong, and A. G. Zhang, “Different roles of ERK1/2 and p38 MAPKα/β in cellular signaling during cardiomyocyte anoxia preconditioning,” Acta Physiol. Sin., 55, No. 4, 454–458 (2003).

    CAS  Google Scholar 

  28. J. D. Jiao, V. Garg, B. Yang, and K. Hu, “Novel functional role of heat shock protein 90 in ATP-sensitive K + channel-mediated hypoxic preconditioning,” Cardiovasc. Res., 77, No. 1, 126–133 (2008).

    Article  PubMed  CAS  Google Scholar 

  29. A. Kalota, S. E. Shetzline, and A. M. Gewirtz, “Progress in the development of nucleic acid therapeutics for cancer,” Cancer Biol. Ther., 3, No. 1, 4–12 (2004).

    Article  PubMed  CAS  Google Scholar 

  30. R. Kerkala, S. Pikkarainen, T. Majalahti-Palviainen, H. Tokola, and H. Ruskoako, “Distinct roles of mitogen-activated protein kinase pathways in GATA-4 transcription factor-mediated regulation of B-type natriuretic peptide gene,” J. Biol. Chem., 277, No. 16, 13752–13760 (2002).

    Article  Google Scholar 

  31. J. Khoury, J. C. Ibla, A. S. Neish, and S. P. Colgun, “Antiinflammatory adaptation to hypoxia through adenosine-mediated cullin-1 deneddylation,” J. Clin. Invest., 117, No. 3, 703–711 (2007).

    Article  PubMed  CAS  Google Scholar 

  32. Y. Kim, A. G. Ma, K. Kitta, S. N. Fitch, T. Ideka,Y. Ihara, A. R. Simon, T. Evans, and Y. J. Suzuki, “Anthracycline-induced suppression of GATA-4 transcription factor: implication in the regulation of cardiac myocyte apoptosis,” Mol. Pharmacol., 63, No. 2, 368–377 (2003).

    Article  PubMed  CAS  Google Scholar 

  33. K. Kitta, S. A. Clément, J. Remeika, J. B. Blumberg, and Y. J. Suzuki, “Endothelin-1 induces phosphorylation of GATA-4 transcription factor in the HL-1 atrial-muscle cell line,” Biochem. J., 359, Part 2, 375–380 (2001).

    Article  PubMed  CAS  Google Scholar 

  34. K. Kitta, R. M. Day, Y. Kim, J. Torregroza, T. Evans, and Y. J. Suzuki, “Hepatocyte growth factor induces GATA-4 phosphorylation and cell survival in cardiac muscle cells,” J. Biol. Chem., 278, No. 7, 4705–4712 (2003).

    Article  PubMed  CAS  Google Scholar 

  35. S. Kobayashi, T. Lackey,Y. Huang, E. Bisping,W. T. Pu, L. M. Boxer, and Q. Liang, “Transcription factor GATA4 regulates BCL2 gene expression in vitro and in vivo,” FASEB J., 20, No. 6, 800–802 (2006).

    PubMed  CAS  Google Scholar 

  36. F. Kolar, J. Jezková, P. Balková, J. Breh, F. Neckár, F. Novák, O. Nováková, H. Tomásová, M. Srbová, B. Ost’ádal, J. Wilhelm, and J. Herget, “Role of oxidative stress in PKC-δ upregulation and cardioprotection induced by chronic intermittent hypoxia,” Am. J. Physiol. Heart Circ. Physiol., 292, No. 1, H224–H230 (2007).

    Article  PubMed  CAS  Google Scholar 

  37. G. Kroemer, L. Galluzzi, and C. Brenner, “Mitochondrial membrane permeabilization in cell death,” Physiol. Rev., 87, No. 1, 99–163 (2007).

    Article  PubMed  CAS  Google Scholar 

  38. J. Kurreck, “Antisense technologies. Improvement through novel chemical modifications,” Eur. J. Biochem., 270, No. 8, 1628–1644 (2003).

    Article  PubMed  CAS  Google Scholar 

  39. R. D. Lasley, G. M. Anderson, and R. M. Mentzer, “Ischaemic and hypoxic preconditioning enhance postischaemic recovery in the rat heart,” Cardiovasc. Res., 27, No. 4, 565–570 (1993).

    Article  PubMed  CAS  Google Scholar 

  40. X. Liu, X. Wu, L. Cai, C. Tang, and J. Su, “Hypoxic preconditioning of cardiomyocytes and cardioprotection: phosphorylation of HIF-1α induced by p42/p44 mitogen-activated protein kinases is involved,” Pathophysiology, 9, No. 4, 201–205 (2003).

    Article  PubMed  CAS  Google Scholar 

  41. L. D. Lukyanova, E. L. Germanova, and R. A. Kopaladze, “Development of resistance of an organism under various conditions of hypoxic preconditioning: role of the hypoxic period and reoxygenation,” Bull. Exp. Biol. Med., 147, No. 4, 400–404 (2009).

    Article  PubMed  CAS  Google Scholar 

  42. S. C. Masters, R. R. Subramanian, A. Truong, H. Yang, K. Fujii, H. Zhang, and H. Fu, “Survival-promoting functions of 14-3-3 proteins,” Biochem. Soc. Trans., 30, No. 4, 360–365 (2002).

    Article  PubMed  CAS  Google Scholar 

  43. N. Maulik, R. M. Engelman, J. A. Rousou, J. E. Flack, D. Deaton, and D. K. Das, “Ischemic preconditioning reduces apoptosis by upregulating anti-death gene Bcl-2,” Circulation, 100, No. 10, Supplement, II369–II375 (1999).

    PubMed  CAS  Google Scholar 

  44. T. Morimoto, K. Hasegawa, T. Kakita, H. Wada, T. Yanazume, and S. Sasayama, “Phosphorylation of GATA-4 is involved in α1-adrenergic agonist-responsive transcription of the endothelin-1 gene in cardiac myocytes,” J. Biol. Chem., 275, No. 18, 13721–13726 (2000).

    Article  PubMed  CAS  Google Scholar 

  45. S. Munro, and H. R. Pelham, “An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein,” Cell, 46, No. 2, 291–300 (1986).

    Article  PubMed  CAS  Google Scholar 

  46. M. Nojiri, K. Tanonaka, K. Yabe, K. Kawana, T. Iwai, M. Yamane, H. Yoshida, J. Hayashi, and S. Takeo, “Involvement of adenosine receptor, potassium channel and protein kinase C in hypoxic preconditioning of isolated cardiomyocytes of adult rat,” Jap. J. Pharmacol., 80, No. 1, 15–23 (1999).

    Article  PubMed  CAS  Google Scholar 

  47. M. Ogbi and J. A. Johnson, “Protein kinase Cε interacts with cytochrome oxidase subunit IV and enhances cytochrome c oxidase activity in neonatal cardiac myocyte preconditioning,” Biochem. J., 393, Part 1, 191–199 (2006).

    Article  PubMed  CAS  Google Scholar 

  48. B. Ostadal and F. Kolar, Cardiac Ischemia: from Injury to Protection, Kluwer Academic Publishers, Boston, Dordrecht, London (1999).

    Google Scholar 

  49. Y. X. Pan, L. Lin, A. J. Ren, H. Chen, C. S. Tang, and W. J. Yuan, “HSP70 and FRP78 induced by endothelin-1 pretreatment enhance tolerance to hypoxia in cultured neonatal rat cardiomyocytes,” J. Cardiovasc. Pharmacol., 44, Supplement 1, S117–S120 (2004).

    Article  PubMed  CAS  Google Scholar 

  50. Y. X. Pan, A. J. Ren, J. Zheng, W. F. Rong, H. Chen, X. H. Yan, C. Wu, W. J. Yuan, and L. Lin, “Delayed cytoprotection induced by hypoxic preconditioning in cultured neonatal rat cardiomyocytes: role of GRP78,” Life Sci., 81, No. 13, 1042–1049 (2007).

    Article  PubMed  CAS  Google Scholar 

  51. A. M. Park, H. Nagase, S. Vinod Kumar, and Y. J. Suzuki, “Acute intermittent hypoxia activates myocardial cell survival signaling,” Am. J. Physiol. Heart Circ. Physiol., 29, No. 2, H751–H757 (2007).

    Google Scholar 

  52. A. G. Portnychenko,V. E. Dosenko,V. I. Portnichenko, and O. O. Moybenko, “Expression of HIF-1α and HIF-3α differentially changed in rat heart ventricles after hypoxic preconditioning,” in : Proceedings of the XXVII European Section Meeting of the ISHR, Athens, Greece, May 28–31, 2008, Medimond Inter. Proc. (2008), pp. 61–64.

  53. S. Rane, M. He, D. Sayed, H. Vashistha, A. Malhotra, J. Sadoshima, D. E. Vatner, S. F. Vatner, and M. Abdellatif, “Downregulation of miR-199a depresses hypoxia-inducible factor-1α and sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes,” Circ. Res., 104, No. 7, 879–886 (2009).

    Article  PubMed  CAS  Google Scholar 

  54. T. Ravingerova, J. E. Løkebø, J. Munch-Ellingsen, R. Sundset, P. Tande, and K. Ytrehus, “Mechanism of hypoxic preconditioning in guinea pig papillary muscles,” Mol. Cell. Biochem., 186, No. 1–2, 53–60 (1998).

    Article  PubMed  CAS  Google Scholar 

  55. A. Rizvi, X. L. Tang, Y. Qiu, Y. T. Xuan, H. Takano, A. K. Jadoon, and R. Bolli, “Increased protein synthesis is necessary for the development of late preconditioning signal against myocardial stunning,” Am. J. Physiol., 277, No. 3, Part 2, H874–H884 (1999).

    PubMed  CAS  Google Scholar 

  56. M. Rosenquist, “14-3-3 proteins in apoptosis,” Braz. J. Med. Biol. Res., 36, No. 4, 403–408 (2003).

    Article  PubMed  CAS  Google Scholar 

  57. G. L. Semenza, “HIF-1: mediator of physiological and pathophysiological responses to hypoxia,” J. Appl. Physiol., 88, No. 4, 1474–1480 (2000).

    PubMed  CAS  Google Scholar 

  58. G. L. Semenza, P. H. Roth, H. M. Fang, and G. L. Wang, “Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1,” J. Biol. Chem., 269, No. 38, 23757–23763 (1994).

    PubMed  CAS  Google Scholar 

  59. K. Shinmura,Y. T. Xuan, X. L. Tang, E. Kodani, H. Han,Y. Zhu, and R. Boli, “Inducible nitric oxide synthase modulates cyclooxygenase-2 activity in the heart of conscious rabbits during the late phase of ischemic preconditioning,” Circ. Res., 90, No. 5, 602–608 (2002).

    Article  PubMed  CAS  Google Scholar 

  60. K. Shintani-Ishida, M. Nakajima, K. Uemura, and K. Yoshida, “Ischemic preconditioning protects cardiomyocytes against ischemic injury by inducing GRP78,” Biochem. Biophys. Res. Commun., 345, No. 4, 1600–1605 (2006).

    Article  PubMed  CAS  Google Scholar 

  61. Y. Shizukuda, R. T. Mallet, S. C. Lee, and H. F. Downey, “Hypoxic preconditioning of ischaemic canine myocardium,” Cardiovasc. Res., 26, No. 5, 534–542 (1992).

    Article  PubMed  CAS  Google Scholar 

  62. Y. Shizukuda, T. Iwamoto, R. T. Mallet, and H. F. Downey, “Hypoxic preconditioning attenuates stunning caused by repeated coronary artery occlusions in dog heart,” Cardiovasc. Res., 27, No. 4, 559–564 (1993).

    Article  PubMed  CAS  Google Scholar 

  63. D. Singh, A. Sharma, and M. Singh, “Effect of actinomycin D and cycloheximide on ischemic preconditioning-induced delayed cardioprotective effect in rats,” Indian J. Exp. Biol., 38, No. 10, 982–987 (2000).

    PubMed  CAS  Google Scholar 

  64. A. Skyschally, P. van Caster, K. Boengler, P. Gres, J. Musiolik, D. Schilawa, R. Schulz, and G. Heusch, “Ischemic postconditioning in pigs: no causal role for RISK activation,” Circ. Res., 104, No. 1, 15–18 (2009).

    Article  PubMed  CAS  Google Scholar 

  65. L. H. Snoeckx, R. N. Cornelussen, F. A. van Nieuwenhoven, R. S. Reneman, and G. J. Van der Vusse, “Heat shock proteins and cardiovascular pathophysiology,” Physiol. Rev., 81, No. 4, 1461–1497 (2001).

    PubMed  CAS  Google Scholar 

  66. R. R. Subramanian, S. C. Masters, H. Zhang, and H. Fu, “Functional conservation of 14-3-3 isoforms in inhibiting bad-induced apoptosis,” Exp. Cell Res., 271, No. 1, 142–151 (2001).

    Article  PubMed  CAS  Google Scholar 

  67. H. Y. Sun, N. P. Wang, F. Kerendi, M. Halkos, H. Kin, R. A. Guyton, J. Vinten-Johansen, and Z. Q. Zhao, “Hypoxic postconditioning reduces cardiomyocyte loss by inhibiting ROS generation intracellular Ca2+ overload,” Am. J. Physiol. Heart Circ. Physiol., 288, No. 4, H1900–H1908 (2005).

    Article  PubMed  CAS  Google Scholar 

  68. M. Tani, Y. Suganuma, M. Takayama, H. Hasegawa, K. Shinmura, Y. Ebihara, and K. Tamaki, “Low concentrations of adenosine receptor blocker decrease protection by hypoxic preconditioning in ischemic rat hearts,” J. Mol. Cell. Cardiol., 30, No. 3, 617–626 (1998).

    Article  PubMed  CAS  Google Scholar 

  69. M. Tani, Y. Honma, M. Takayama, H. Hasegawa, K. Shinmura, Y. Ebihara, and K. Tamaki, “Loss of protection by hypoxic preconditioning in aging Fischer 344 rat hearts related to myocardial glycogen content and Na + imbalance,” Cardiovasc. Res., 41, No. 3, 594–602 (1999).

    Article  PubMed  CAS  Google Scholar 

  70. G. Testoni, S. Cerruti, P. Kade, M. Carregal, A. Varela, and E. A. Savino, “Effects of hypoxic preconditioning on the hypoxic-reoxygenated atria from fed and fasted rats,” J. Physiol. Biochem., 56, No. 4, 321–328 (2000).

    Article  PubMed  CAS  Google Scholar 

  71. T. Uchiyama, R. M. Engelman, N. Maulik, and D. K. Das, “Role of Akt signaling in mitochondrial survival pathways triggered by hypoxic preconditioning,” Circulation, 109, No. 24, 3042–3049 (2004).

    Article  PubMed  CAS  Google Scholar 

  72. T. L. Vanden Hoek, L. B. Becker, Z. Shao, C. Li, and P. T. Schumacker, “Reactive oxygen species released from mitochondria during brief hypoxia preconditioning in cardiomyocytes,” J. Biol. Chem., 273, No. 29, 18092–18098 (1998).

    Article  PubMed  CAS  Google Scholar 

  73. T. L. Vanden Hoek, L. B. Becker, Z. H. Zhao, C. Q. Li, and P. T. Schumacker, “Preconditioning in cardiomyocytes protects by attenuating oxidant stress at reperfusion,” Circ. Res., 86, No. 5, 541–548 (2000).

    PubMed  CAS  Google Scholar 

  74. H. C. Wang, H. F. Zhang, W. Y. Guo, H. Su, K. R. Zhang, Q. X. Li, W. Yan, X. L. Ma, B. L. Lopez, T. A. Christopher, and F. Gao, “Hypoxic preconditioning enhances the survival and inhibits apoptosis of cardiomyocytes following reoxygenation: role of peroxynitrite formation,” Apoptosis, 11, No. 8, 1453–1460 (2006).

    Article  PubMed  CAS  Google Scholar 

  75. D. Wasserfuhr, S. M. Cetin, J. Yang, P. Freitag, S. Frede, H. Jakob, and P. Massoudy, “Protection of the right ventricle from ischemia and reperfusion by preceding hypoxia,” Naunyn-Schmiedeberg’s Arch. Pharmacol., 378, No. 1, 27–32 (2008).

    Article  CAS  Google Scholar 

  76. R. A. White, L. L. Dowler, L. M. Pasztor, L. L. Gatson, L. R. Adkison, S. V. Angelonik, and D. B. Wilson, “Assignment of the transcription factor GATA4 gene to human chromosome 8 and mouse chromosome 145: Gata4 is a candidate gene for Ds (disorganization),” Genomics, 27, No. 1, 20–26 (1995).

    Article  PubMed  CAS  Google Scholar 

  77. X. Wu, X. Liu, X. Zhu, and C. Tang, “Hypoxic preconditioning induces delayed cardioprotection through p38 MAPK-mediated calreticulin upregulation,” Shock, 27, No. 5, 572–577 (2007).

    Article  PubMed  CAS  Google Scholar 

  78. L. Xi, D. Tekin, E. Gursoy, F. Salloum, J. E. Levasseur, and R. C. Kukreja, “Evidence that NOS2 acts as a trigger and mediator of late preconditioning induced by acute systemic hypoxia,” Am. J. Physiol. Heart Circ. Physiol., 283, No. 1, H5–H12 (2002).

    PubMed  CAS  Google Scholar 

  79. F. F. Xu, X. H. Liu, and L. R. Cai, “Role of hypoxia-inducible factor-1α in the prevention of cardiomyocyte injury induced by hypoxic preconditioning,” Acta Physiol. Sin., 56, No. 5, 609–614 (2004).

    CAS  Google Scholar 

  80. X. M. Yang, Y. Liu, N. Tandon, J. Kambayashi, J. M. Downey, and M. V. Cohen, “Attenuation of infarction in cynomolgus monkeys: preconditioning and postconditioning,” Basic Res. Cardiol., 105, No. 1, 119–128 (2010).

    Article  PubMed  Google Scholar 

  81. D. M. Yellon and J. M. Downey, “Preconditioning the myocardium: from cellular physiology to clinical cardiology,” Physiol. Rev., 83, No. 4, 1113–1151 (2003).

    PubMed  CAS  Google Scholar 

  82. J. G. Zhuang, Y. Zhang, and Z. N. Zhou, “Hypoxic preconditioning upregulates KATP channels through activation of protein kinase C in rat ventricular myocytes,” Acta Pharmacol. Sin., 21, No. 9, 845–849 (2000).

    PubMed  CAS  Google Scholar 

  83. X. M. Zhu, X. H. Liu, L. R. Cai, and F. F. Zu, “Hypoxic preconditioning induces endoplasmic reticulum stress-related cardioprotection mediated by p38 mitogen-activated protein kinase,” Acta Physiol. Sin., 58, No. 5, 463–470 (2006).

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 96, No. 12, pp. 1170–1189, December, 2010.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maslov, L.N., Lishmanov, Y.B., Kolar, F. et al. Hypoxic Preconditioning – a Phenomenon Increasing the Tolerance of Cardiomyocytes to Hypoxia/Reoxygenation. Neurosci Behav Physi 42, 380–391 (2012). https://doi.org/10.1007/s11055-012-9577-z

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-012-9577-z

Keywords

Navigation