Skip to main content

Impact of Perinatal Chronic Hypoxia on Cardiac Tolerance to Acute Ischemia

  • Chapter
  • First Online:
Molecular Defects in Cardiovascular Disease

Abstract

Perinatal period is critical for the normal cardiac development, and different interventions imposed on the heart may significantly influence myocardial structure and function. Perinatal hypoxemia, although transient, may thus have serious early and late consequences on the cardiovascular system. Epidemiological and experimental studies have repeatedly suggested a possible link between perinatal hypoxia and increased sensitivity to ischemia/reperfusion (I/R) injury in adults. The mechanisms of this increased susceptibility are not known at present. It has been found that prenatal chronic hypoxia sensitizes the apoptosis pathway in the adult male heart in response to I/R stimulation. In addition, cardiac heat shock proteins (Hsp) 70 expression was significantly lower in prenatal hypoxic hearts than in controls; this fact may play a role in the increased susceptibility of the adult heart to I/R injury. The decreased eNOS levels in adult prenatal hypoxic hearts may also contribute to their increased sensitivity. These studies suggest that chronic hypoxic exposure during early development may cause in utero or neonatal programming of several genes which can play an important role in the increased susceptibility of the adult male heart to I/R injury. Furthermore, it has been observed in the rat model that late myocardial effects of chronic hypoxia, experienced in early life, may be sex-dependent. Unlike in males, perinatal exposure to chronic hypoxia significantly increased cardiac tolerance to acute I/R injury in adult females, expressed as the lower incidence of ischemic arrhythmias, decreased infarct size, decreased cardiac enzyme release, and increased postischemic recovery of left ventricular function. It was suggested that these sex-dependent changes may be due to differences in fetal programming of PKCε gene expression, which play a pivotal role in cardioprotection; down-regulation of PKCε function was observed in the hearts of adult male offspring only. These results would have important clinical implications, since cardiac sensitivity to oxygen deprivation in adult patients may be significantly influenced by perinatal hypoxia in a sex-dependent manner.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Barker DJ, Osmond C, Golding J, et al. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298:564–7.

    Article  PubMed  CAS  Google Scholar 

  2. Xue Q, Zhang L. Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischaemia and reperfusion injury in adult male offspring: role of protein kinase Cε. J Pharmacol Exp Therap. 2009;330:624–32.

    Article  CAS  Google Scholar 

  3. Giussani DA, Phillips PS, Anstee S, et al. Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res. 2001;49:490–4.

    Article  PubMed  CAS  Google Scholar 

  4. Rohlicek CV, Matsuoka T, Saiki C. Cardiovascular response to acute hypoxemia in adult rats hypoxemic neonatally. Cardiovasc Res. 2002;53:263–70.

    Article  PubMed  CAS  Google Scholar 

  5. Nollert G, Fischlein T, Bouterwek S, et al. Long-term survival in patients with repair of tetralogy of Fallot: 36-year follow-up of 490 survivors of the first year after surgical repair. J Am Coll Cardiol. 1997;30:1374–83.

    Article  PubMed  CAS  Google Scholar 

  6. Netuka I, Szarszoi O, Maly J, et al. Effect of perinatal hypoxia on cardiac tolerance to acute ischaemia in adult male and female rats. Clin Exp Pharmacol Physiol. 2006;33:714–9.

    Article  PubMed  CAS  Google Scholar 

  7. Krecek J. The weanling period as a critical period of development. In: Krecek J, editor. The post-natal development of phenotype. Prague: Academia; 1970. p. 33–44.

    Google Scholar 

  8. Eastman NJ. Mount Everest in utero. President’s address. Am J Obstet Gynecol. 1954;67:701–11.

    PubMed  CAS  Google Scholar 

  9. Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004;432:1032–6.

    Article  PubMed  CAS  Google Scholar 

  10. Mühlfeld C, Singer D, Engelhardt N, et al. Electron microscopy and microcalorimetry of the postnatal rat heart (Rattus norvegicus). Comp Biochem Physiol A Mol Integr Physiol. 2005;141:310–8.

    Article  PubMed  Google Scholar 

  11. Ostadalova I, Charvatova Z, Wilhelm J. Lipofuscin-like pigments in the rat heart during early postnatal development: effect of selenium supplementation. Physiol Res. 2010;59:881–6.

    PubMed  CAS  Google Scholar 

  12. Ostadal B, Wachtlova M, Bily J, et al. Weight of the heart in the rats before and after birth. Physiol bohemoslov. 1967;16:111–9.

    Google Scholar 

  13. Ostadalova I, Kolar F, Ostadal B, et al. Early postnatal development of contractile performance and responsiveness to Ca2+, verapamil and ryanodine in the isolated rat heart. J Mol Cell Cardiol. 1993;25:733–40.

    Article  PubMed  CAS  Google Scholar 

  14. Li F, Wang X, Capasso JM, et al. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol. 1996;28:1737–46.

    Article  PubMed  CAS  Google Scholar 

  15. Rakusan K. Vascularization of the heart during normal and pathological growth. Adv Org Biol. 1999;7:130–53.

    Google Scholar 

  16. Skarka L, Bardova K, Brauner P, et al. Expression of mitochondrial uncoupling protein 3 and adenine nucleotide translocase 1 genes in developing rat heart: putative involvement in control of mitochondrial membrane potential. J Mol Cell Cardiol. 2003;35:321–30.

    Article  PubMed  CAS  Google Scholar 

  17. Nijjar MS, Dhalla NS. Biochemical basis of calcium handling in developing myocardium. In: Ostadal B, Nagano M, Takeda N, Dhalla NS, editors. The developing heart. Philadelphia, P.A.: Lippincott; 1997. p. 189–217.

    Google Scholar 

  18. Ostadal B, Ostadalova I, Dhalla NS. Development of cardiac sensitivity to oxygen deficiency: comparative and ontogenetic aspects. Physiol Rev. 1999;79:635–59.

    PubMed  CAS  Google Scholar 

  19. Ostadalova I, Ostadal B, Kolar F. Effect of prenatal hypoxia on contractile performance and responsiveness to Ca2+ in the isolated perinatal rat heart. Physiol Res. 1995;44:135–7.

    PubMed  CAS  Google Scholar 

  20. Babicky A, Ostadalova I, Parizek J, et al. Initial solid food intake and growth of young rats in nests of different sizes. Physiol Bohemoslov. 1973;22:557–66.

    PubMed  CAS  Google Scholar 

  21. Gilbert RD. Fetal myocardial responses to long-term hypoxemia. Comp Biochem Physiol. 1998;3:669–74.

    Google Scholar 

  22. Ohtsuka T, Gilbert RD. Cardiac enzyme activities in fetal and adult pregnant and non pregnant sheep exposed to high altitude hypoxemia. J Appl Physiol. 1995;79:1286–9.

    PubMed  CAS  Google Scholar 

  23. Murotsuki J, Challis JR, Han VK, et al. Chronic fetal placental embolization and hypoxaemia cause hypertension and myocardial hypertrophy in fetal sheep. Am J Physiol Regul Integr Comp Physiol. 1997;272:R201–7.

    CAS  Google Scholar 

  24. Martin C, Yu AY, Jiang BH, et al. Cardiac hypertrophy in chronically anemic fetal sheep: increased vascularization is associated with increased myocardial expression of vascular endothelial growth factor and hypoxia-inducible factor 1. Am J Obstet Gynecol. 1998;178:527–34.

    Article  PubMed  CAS  Google Scholar 

  25. Han HC, Austin KJ, Nathanielsz PVV, et al. Maternal nutrient restriction alters gene expression in the ovine fetal heart. J Physiol. 2004;555:111–21.

    Article  Google Scholar 

  26. Bae S, Xiao Y, Li G, et al. Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am J Physiol Heart Circ Physiol. 2003;285:H983–90.

    PubMed  CAS  Google Scholar 

  27. Patterson AJ, Chen M, Xue Q, et al. Chronic prenatal hypoxia induces epigenetic programming of PKCε gene expression in rat hearts. Circulation Res. 2010;107:365–73.

    Article  PubMed  CAS  Google Scholar 

  28. Verburg BO, Jaddoe VW, Wladimiroff JW, et al. Fetal hemodynamic adaptive changes related to intrauterine growth: the generation R study. Circulation. 2008;117:649–59.

    Article  PubMed  Google Scholar 

  29. Chvojkova Z, Ostadalova I, Ostadal B. Low body weight and cardiac tolerance to ischemia in neonatal rats. Physiol Res. 2005;54:357–62.

    PubMed  CAS  Google Scholar 

  30. Mortola JP, Xu L, Lauzon A-M. Body growth, lung and heart weight, and DNA content in newborn rats exposed to different levels of chronic hypoxia. Can J Physiol Pharmacol. 1990;68:1590–4.

    Article  PubMed  CAS  Google Scholar 

  31. Naye RL. Organ and cellular development in mice growing at simulated high altitude. Lab Invest. 1966;15:700–6.

    Google Scholar 

  32. Bai SL, Campbell SE, Moore JA, et al. Influence of age, growth, and sex on cardiac myocyte size and number in rats. Anat Rec. 1990;226:207–12.

    Article  PubMed  CAS  Google Scholar 

  33. Bell JM, Slotkin TA. Postnatal nutritional status influences development of cardiac adrenergic receptor binding sites. Brain Res Bull. 1988;21:893–6.

    Article  PubMed  CAS  Google Scholar 

  34. Ostadalova I, Ostadal B. Ontogenetic differences in isoproterenol induced 85 Sr uptake in the myocardium. In: Nagano M, Takeda N, Dhalla NS, editors. The cardiomyopathic heart. New York: Raven; 1994. p. 395–400.

    Google Scholar 

  35. Bell JM, Whitmore WL, Queen KL, et al. Biochemical determinants of growth sparing during neonatal deprivation or enhancement: ornithine decarboxylase, polyamines, and macromolecules in brain regions and heart. Pediatr Res. 1987;22:599–604.

    Article  PubMed  CAS  Google Scholar 

  36. Brodsky VY, Pelouch V, Arefyeva AM, et al. Lack of proportionality between gene dosage and total muscle protein content in the rat heart. Int J Dev Biol. 1992;36:339–42.

    PubMed  CAS  Google Scholar 

  37. Pelouch V, Kolar F, Milerova M, et al. Effect of preweanling nutritional state on the cardiac protein profile and functional performance of the rat heart. Mol Cell Biochem. 1997;177:221–8.

    Article  PubMed  CAS  Google Scholar 

  38. Dowell RT, Martin AF. Perinatal nutritional modification of weanling rat heart contractile protein. Am J Physiol Heart Circ Physiol. 1984;247:H967–72.

    CAS  Google Scholar 

  39. Rakusan K, Poupa O. Differences in capillary supply of hypertrophied and hyperplastic hearts. Cardiologia. 1966;49:293–8.

    Article  PubMed  CAS  Google Scholar 

  40. Neffgen F, Korecky B. Cellular hyperplasia and hypertrophy in cardiomegalies induced by anaemia in young and adult rats. Circulation Res. 1972;30:104–13.

    PubMed  CAS  Google Scholar 

  41. Hollenberg M, Honbo N, Samorodin AJ. Effects of hypoxia on cardiac growth in neonatal rats. Am J Physiol. 1976;231:1445–50.

    PubMed  CAS  Google Scholar 

  42. Wachtlova M, Mares V, Ostadal B. DNA synthesis in the ventricular myocardium of young rats exposed to intermittent high altitude (IHA) hypoxia. Virchows Arch B Cell Path. 1977;24:335–42.

    CAS  Google Scholar 

  43. Samanek M, Bass A, Ostadal B, et al. Effect of hypoxaemia on enzymes supplying myocardial energy in children with congenital heart disease. Int J Cardiol. 1989;25:265–70.

    Article  PubMed  CAS  Google Scholar 

  44. Fitzpatrick CM, Shi Y, Hutchins WC, et al. Cardioprotection in chronically hypoxic rabbits on exposure to normoxia: role of NOS and KATP channels. Am J Physiol Heart Circ Physiol. 2005;288:H62–8.

    Article  PubMed  CAS  Google Scholar 

  45. Ostadal B, Kolar F. Cardiac ischemia: from injury to protection. Boston: Kluwer Academic; 1999.

    Google Scholar 

  46. Ostadal B, Netuka I, Maly J, et al. Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp Biol Med. 2009;234:1011–9.

    Article  CAS  Google Scholar 

  47. Riva A, Hearse DJ. Age-dependent changes in myocardial succeptibility to ischemic injury. Cardioscience. 2009;4:85–92.

    Google Scholar 

  48. Ostadalova I, Ostadal B, Kolar F, et al. Tolerance to ischemia and ischaemic preconditioning in neonatal rat heart. J Mol Cell Cardiol. 1998;30:857–65.

    Article  PubMed  CAS  Google Scholar 

  49. Baker EJ, Boerboom LE, Olinger GN, et al. Tolerance of the developing heart to ischemia: impact of hypoxemia from birth. Am J Physiol. 1998;268:H1165–73.

    Google Scholar 

  50. Hoerter J. Changes in the sensitivity to hypoxia and glucose deprivation in the isolated perfused rabbit heart during perinatal development. Pflugers Arch. 1976;363:1–6.

    Article  PubMed  CAS  Google Scholar 

  51. Julia P, Young PP, Buckberg GD, et al. Studies of myocardial protection in the immature heart. II. Evidence for importance of amino acid metabolism in tolerance to ischemia. J Thorac Cardiovasc Res. 1990;100:888–95.

    CAS  Google Scholar 

  52. Hohl CM. Effect of respiratory inhibition and ­ischemia on nucleotide metabolism in newborn swine ­cardiac myocytes. In: Ostadal B, Nagano M, Takeda N, Dhalla NS, editors. The developing heart. Philadelphia, PA: Lippincott; 1997. p. 393–406.

    Google Scholar 

  53. Vetter R, Studer R, Reinecke H, et al. Reciprocal changes in the postnatal expression of the sarcolemmal Na+-Ca2+-exchanger and SERCA2 in rat heart. J Mol Cell Cardiol. 1995;27:1689–701.

    Article  PubMed  CAS  Google Scholar 

  54. Schagger H, Noack H, Halangk W, et al. Cytochrome c oxidase in developing rat heart. Enzymic properties and amino-terminal sequences suggest identity of the fetal heart and the adult liver isoform. Eur J Biochem. 1995;230:235–41.

    Article  PubMed  CAS  Google Scholar 

  55. Drahota Z, Milerova M, Stieglerova A, et al. Developmental changes of cytochrome c oxidase and citrate synthase in rat heart homogenate. Physiol Res. 2004;53:119–22.

    PubMed  CAS  Google Scholar 

  56. Di Lisa F, Bernardi P. Mitochondrial function as a determinant of recovery or death in cell response to injury. Mol Cell Biochem. 1998;184:379–91.

    Article  PubMed  Google Scholar 

  57. Di Lisa F, Bernardi P. Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition. Cardiovasc Res. 2006;66:222–32.

    Article  Google Scholar 

  58. Di Lisa F, Menabo R, Canton M, et al. Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem. 2001;276:2571–5.

    Article  PubMed  Google Scholar 

  59. Milerova M, Charvatova Z, Skarka L, et al. Neonatal cardiac mitochondria and ischemia/reperfusion injury. Mol Cell Biochem. 2010;335:147–53.

    Article  PubMed  CAS  Google Scholar 

  60. Heath D, Williams DR. High altitude medicine and pathology. Oxford: Oxford University Press; 1995.

    Google Scholar 

  61. Ostadal B, Kolar F. Cardiac adaptation to chronic high altitude hypoxia. Respir Physiol Neurobiol. 2007;158:224–36.

    Article  PubMed  CAS  Google Scholar 

  62. Neckar J, Papousek F, Novakova O, et al. Cardioprotective effects of chronic hypoxia and ischaemic preconditioning are not additive. Basic Res Cardiol. 2002;97:161–7.

    Article  PubMed  Google Scholar 

  63. Neckar J, Szarszoi O, Koten L, et al. Effects of mitochondrial KATP modulators on cardioprotection induced by chronic high altitude hypoxia in rats. Cardiovasc Res. 2002;55:567–75.

    Article  PubMed  CAS  Google Scholar 

  64. Asemu G, Papousek F, Ostadal B, et al. Adaptation to high altitude hypoxia protects the rat heart against ischemia-induced arrhythmias. Involvement of mitochondrial KATP channel. J Mol Cell Cardiol. 1999;31:821–31.

    Article  Google Scholar 

  65. Szarszoi O, Asemu G, Ostadal B, et al. Effects of melatonin on ischemia and reperfusion injury of the rat heart. Cardiovasc Drugs Ther. 2001;15:251–7.

    Article  PubMed  CAS  Google Scholar 

  66. Kolar F, Ostadal B. Molecular mechanisms of cardiac protection by adaptation to chronic hypoxia. Physiol Res. 2004;53 Suppl 1:S3–13.

    PubMed  CAS  Google Scholar 

  67. Ostadal B, Kolar F, Pelouch V, et al. Ontogenetic ­differences in cardiopulmonary adaptation to chronic hypoxia. Physiol Res. 1995;44:45–51.

    PubMed  CAS  Google Scholar 

  68. Ostadalova I, Ostadal B, Jarkovska D, et al. Ischemic preconditioning in chronically hypoxic neonatal rat heart. Pediatr Res. 2002;52:561–7.

    Article  PubMed  CAS  Google Scholar 

  69. Ostadal B, Ostadalova I, Kolar F, et al. Ontogenetic development of cardiac tolerance to oxygen deprivation – possible mechanisms. Physiol Res. 2009;58 Suppl 2:S1–12.

    PubMed  Google Scholar 

  70. Rakusan K, Chvojkova Z, Oliviero P, et al. ANG II type 1 receptor antagonist irbesartan inhibits coronary angiogenesis stimulated by chronic intermittent hypoxia in neonatal rats. Am J Physiol Heart Circ Physiol. 2007;292:H1–8.

    Google Scholar 

  71. Barker DJ. In utero programming of cardiovascular disease. Theriogenology. 2000;53:555–74.

    Article  PubMed  CAS  Google Scholar 

  72. Sallout B, Walker M. The fetal origin of adult disease. J Obstet Gynaecol. 2003;23:555–60.

    Article  PubMed  CAS  Google Scholar 

  73. Osmond C, Barker DJP, Winter PD, et al. Early growth and death from cardiovascular disease in women. BMJ. 1993;307:1519–24.

    Article  PubMed  CAS  Google Scholar 

  74. Rich-Edwards JW, Stampfer MJ, Manson JE, et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ. 1997;315:396–400.

    PubMed  CAS  Google Scholar 

  75. Leon DA, Lithell HO, Vagero D, et al. Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15  000 Swedish men and women born 1915–1929. BMJ. 1998;317:241–5.

    PubMed  CAS  Google Scholar 

  76. Eriksson JG, Forsen T, Toumilehto J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ. 1999;318:427–31.

    PubMed  CAS  Google Scholar 

  77. Crispi F, Bijnens B, Figueras F, et al. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation. 2010;121:2427–36.

    Article  PubMed  Google Scholar 

  78. Li G, Xiao Y, Estrella JL, et al. Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult heart. J Soc Gynecol Investig. 2003;10:265–74.

    Article  PubMed  CAS  Google Scholar 

  79. Li G, Bae S, Zhang L. Effect of prenatal hypoxia on heat stress-mediated cardioprotection in adult rat heart. Am J Physiol Heart Circ Physiol. 2004;286:1712–9.

    Article  Google Scholar 

  80. Xu Y, Williams SJ, O’Brien D, et al. Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J. 2006;20:1251–3.

    Article  PubMed  CAS  Google Scholar 

  81. Peyronnet J, Dalmaz Y, Ehrstrom M. Long-lasting adverse effects of prenatal hypoxia on developing autonomic nervous system and cardiovascular parameters in rats. Pflugers Arch. 2002;443:858–65.

    Article  PubMed  CAS  Google Scholar 

  82. Hampl V, Herget J. Perinatal hypoxia increases hypoxic pulmonary vasoconstriction in adult rats recovering from chronic exposure to hypoxia. Am Rev Respir Dis. 1990;142:619–24.

    PubMed  CAS  Google Scholar 

  83. Hampl V, Bibova J, Ostadalova I, et al. Gender differences in the long-term effects of perinatal hypoxia on pulmonary circulation in rats. Am J Physiol Lung Cell Mol Physiol. 2003;285:L386–92.

    PubMed  CAS  Google Scholar 

  84. Snoeckx LH, Cornelussen RN, Van Nieuwenhoven FA, et al. Heat shock proteins and cardiovascular pathophysiology. Physiol Rev. 2001;81:1461–97.

    PubMed  CAS  Google Scholar 

  85. Di Lisa F. A female way to protect the heart. Say NO to calcium. Circ Res. 2006;98:298–300.

    Article  PubMed  Google Scholar 

  86. Sun J, Picht E, Ginsburg KS, et al. Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha 1 subunit and reduced ischemia-reperfusion injury. Circ Res. 2006;98:403–11.

    Article  PubMed  CAS  Google Scholar 

  87. Johnson MS, Moore RL, Brown DA. Sex differences in myocardial infarct size are abolished by sarcolemmal KATP channel blocade in rat. Am J Physiol Heart Circ Physiol. 2006;290:H2644–7.

    Article  PubMed  CAS  Google Scholar 

  88. Lee TM, Su SF, Tsai CC, et al. Cardioprotective effects of 17 beta-estradiol produced by activation of mitochondrial ATP-sensitive K+ channels in canine hearts. J Mol Cell Cardiol. 2000;32:1147–58.

    Article  PubMed  CAS  Google Scholar 

  89. Bae S, Zhang L. Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts: focus on Akt and protein kinase C signaling. J Pharmacol Exp Therap. 2005;315:1125–35.

    Article  CAS  Google Scholar 

  90. Cross HR, Murphy E, Steenbergen C. Ca2+ loading and adrenergic stimulation reveal male/female differences in susceptibility to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2002;283:H481–9.

    PubMed  CAS  Google Scholar 

  91. Lagranha CJ, Deschamps A, Aponte A, et al. Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res. 2010;106:1681–91.

    Article  PubMed  CAS  Google Scholar 

  92. Murriel CL, Mochly-Rosen D. Opposing roles of delta and epsilon PKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch Biochem Biophys. 2003;420:246–54.

    Article  PubMed  CAS  Google Scholar 

  93. Kolar F, Novak F, Neckar J, et al. Role of protein kinases in chronic intermittent hypoxia-induced cardioprotection. In: Xi L, Serebrovskaya TV, editors. Intermittent hypoxia. New York: Nova Science; 2009. p. 213–30.

    Google Scholar 

Download references

Acknowledgments

This study was supported by grants MSMT 1 M0510 and AVOZ 50110509.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bohuslav Ostadal .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Ostadal, B., Ostadalova, I., Kolar, F., Netuka, I., Szarszoi, O. (2011). Impact of Perinatal Chronic Hypoxia on Cardiac Tolerance to Acute Ischemia. In: Dhalla, N., Nagano, M., Ostadal, B. (eds) Molecular Defects in Cardiovascular Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7130-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-7130-2_5

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-7129-6

  • Online ISBN: 978-1-4419-7130-2

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics