Ontogenetic development of cardiac tolerance to oxygen deprivation - Possible mechanisms

Physiological Research

Volumn 58, Issue SUPPL.2, 2009, Pages 1-12

  Ostadal B ^a,b   Ostadalova I ^a,b   Kolar F ^a,b   Charvatova Z ^a,b   Netuka, I ^a,c  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^c INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

Cardiac protection; Cardiac tolerance; Hypoxia ischemia; Ontogenetic development

Indexed keywords

EID: 84865099848     PISSN: 08628408     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Short Survey

References (85)

1. ARTMAN M, MAHONY L, TEITEL DF: Regulation of myocyte contraction and relaxation. In: Neonatal Cardiology. M ARTMAN, L MAHONY, DF TEITEL (eds), McGraw Hill, New York, 2002, pp 19-38.
2. AWAD WI, SHATTOCK MJ, CHAMBERS DJ: Ischemic preconditioning in immature myocardium. Circulation 98: 206-213, 1998.
3. BAINES CP, KAISER RA, PURCELL NH, BLAIR NS, OSINSKA H, HAMBLETON MA, BRUNSKILL EW, SAYEN MR, GOTTLIEB RA, DORN GW, ROBBINS J, MOLKENTIN JD: Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434: 658-662, 2005.
4. BAKER EJ, BOERBOOM LE, OLINGER GN, BAKER JE: Tolerance of the developing heart to ischemia: impact of hypoxemia from birth. Am J Physiol 268: H1165-H1173, 1995.
5. BAKER JE, BOERBOOM LE, OLINGER GN: Age-related changes in the ability of hypothermia and cardioplegia to protect ischemic rabbit myocardium. J Thorac Cardiovasc Surg 96: 717-724, 1988.
6. BAKER JE, BOERBOOM LE, OLINGER GN: Is protection of ischemic neonatal myocardium by cardioplegia species dependent. J Thorac Cardiovasc Surg 99: 280-287, 1990.
7. BAKER JE, HOLMAN P, GROSS GJ: Preconditioning in immature rabbit hearts. Role of KATP channels. Circulation 99: 1249-1254, 1999.
8. BALASKA D, HALESTRAP AP, SULEIMAN M-S, GRIFFITHS EJ: Increased susceptibility to pore-opening in heart mitochondria from neonatal compared with adult rats. (abstract). J Mol Cell Cardiol 38: 1002, 2005.
9. BASS A, STEJSKALOVÁ M, STIEGLEROVÁ A, OŠŤÁDAL B, ŠAMÁNEK M: Ontogenetic development of energy-supplying enzymes in rat and guinea-pig heart. Physiol Res 50: 237-245, 2001.
10. BOLLI R: Preconditioning: a paradigm shift in the biology of myocardial ischemia. Am J Physiol 292: H19-H27, 2007.
11. BOUCEK RJ, SHELTON M, ARTMAN M, MUSHLIN PS, STARNES VA, OLSON RD: Comparative effect of verapamil, nifedipine and diltiazem on contractile function in the isolated immature and adult rabbit heart. Pediatr Res 18: 948-954, 1984.
12. CLARKE SJ, MCSTAY GP, HALESTRAP AP: Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem 277: 34793-34799, 2002.
13. DI LISA F, BERNARDI P: Mitochondrial function as a determinant of recovery or death in cell response to injury. Mol Cell Biochem 184: 379-391, 1998.
14. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 276: 2571-2575, 2001.
15. DI LISA F, BERNARDI P: Mitochondrial function and myocardial aging. A critical analysis of the role of permeability transition. Cardiovasc Res 66: 222-232, 2006.
16. DRAHOTA Z, MILEROVÁ M, STIEGLEROVÁ A, HOUŠTĚK J, OŠŤÁDAL B: Developmental changes of cytochrome c oxidase and citrate synthase in rat heart homogenate. Physiol Res 53: 119-122, 2004.
17. FABIATO A: Calcium-induced release of calcium from the sarcoplasmic reticulum. Am J Physiol 245: C1-C14, 1983.
18. FAZEKAS JF, ALEANDER FAD, HIMWICH HE: Tolerance of the newborn to anoxia. Am J Physiol 134: 281-285, 1941.
19. FEJFAR Z: Prevention against ischaemic heart disease: a critical review. In: Modern Trends in Cardiology - 3. M.F. OLIVER (ed), Butterworths, London, 1975, pp 465-499.
20. + channel in cardiac function and cardioprotection. Biochim Biophys Acta 1606: 1-21, 2003.
21. GRIFFITHS EJ, HALESTRAP AP: Protection by cyclosporin A of ischemia/reperfusion-induced damage in isolated rat hearts. J Mol Cell Cardiol 25: 1461-1469, 1993.
22. HALESTRAP AP: Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans 34: 232-237, 2006.
23. HOERTER J: Changes in the sensitivity to hypoxia and glucose deprivation in the isolated perfused rabbit heart during perinatal development. Pflugers Arch 363: 1-6, 1976.
24. HOHL CM: Effect of respiratory inhibition and ischemia on nucleotide metabolism in newborn swine cardiac myocytes. In: The Developing Heart. B OŠŤÁDAL, M NAGANO, N TAKEDA, NS DHALLA (eds), Lippincott, Philadelphia, 1997, pp 393-406.
25. HURTADO A: Some clinical aspects of life at high altitudes. Ann Intern Med 53: 247-258, 1960.
26. JARMAKANI JM, NAGAMOTO T, NAKAZAWA M, LANGER GA: Effect of hypoxia on mechanical function in the neonatal mammalian heart. Am J Physiol 235: H469-H474, 1978a.
27. JARMAKANI JM, NAGAMOTO T, NAKAZAWA M, LANGER GA: Effect of hypoxia on myocardial high-energy phosphates in the neonatal mammalian heart. Am J Physiol 235: H475-H481, 1978b.
28. JARMAKANI JM, NAKANISHI T, GEORGE BL, BERS D: Effect of extracellular calcium on myocardial mechanical function in the neonatal rabbit. Dev Pharmacol Ther 5: 1-13, 1982.
29. JULIA P, KORFSKY ER, BUCKBERG GD, YOUNG HH, BUGYI HI: Studies of myocardial protection in the immature heart. I. Enhanced tolerance of immature versus adult myocardium to global ischemia with reference to metabolic differences. J Thorac Cardiovasc Surg 100: 879-887, 1990a.
30. JULIA P, YOUNG PP, BUCKBERG GD, KORFSKY ER, BUGYI HI: Studies of myocardial protection in the immature heart. II. Evidence for importance of amino acid metabolism in tolerance to ischemia. J Thorac Cardiovasc Res 100: 888-895, 1990b.
31. KOLÁŘ F, OŠŤÁDAL B, PROCHÁZKA J, PELOUCH V, WIDIMSKÝ J: Comparison of cardiopulmonary response to intermittent high-altitude hypoxia in young and adult rats. Respiration 56: 57-62, 1989.
32. KOLÁŘ F, OŠŤÁDAL B, PAPOUŠEK F: Effect of verapamil on contractile function of the isolated perfused heart. Basic Res Cardiol 85: 429-434, 1990.
33. KOLÁŘ F, OŠŤÁDAL B: Molecular mechanisms of cardiac protection by adaptation to chronic hypoxia. Physiol Res 53 (Suppl 1): S3-S13, 2004.
34. KUMA A, HATANO M, MATSUI M, YAMAMOTO A, NAKAYA H, YOSHIMORI T, OHSUMI Y, TOKUHISA T, MIZUSHIMA N: The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036, 2004.
35. LASKEY WK: Brief repetitive balloon occlusions enhance reperfusion during percutaneous coronary intervention for acute myocardial infarction; a pilot study. Catether Cardiovasc Interv 65: 361-367, 2005.
36. LEGATO MJ: Cellular mechanisms of normal growth in the mammalian heart. II. Qualitative and quantitative features of ventricular architecture in the dog from birth to live months of age. Circ Res 44: 263-279, 1979.
37. LI G, XIAO Y, ESTRELLA JL, DUCSAY CA, GILBERT RD, ZHANG L: Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult heart. J Soc Gynecol Investig 10: 265-274, 2003.
38. LI G, BAE S, ZHANG L: Effect of prenatal hypoxia on heat stress-mediated cardioprotection in adult rat heart. Am J Physiol 286: 1712-1719, 2004.
39. LOPASCHUK GD: Treating ischemic heart disease by pharmacologically improving cardiac energy metabolism. Presse Med 27: 2100-2104, 1998.
40. MILEROVÁ M, CHARVÁTOVÁ Z, ŠKÁRKA L, OŠŤÁDALOVÁ I, DRAHOTA Z, FIALOVÁ M, OŠŤÁDAL B: Neonatal cardiac mitochondria and ischemia/reperfusion injury. Mol Cell Biochem 2009; in press.
41. MORTOLA JP: Implications of hypoxic hypometabolism during mammalian ontogenesis. Respir Physiol Neurobiol 141: 345-356, 2004.
42. MÜHLFELD C, SINGER D, ENGELHARDT N, RICHTER J, SCHMIEDL A: Electron microscopy and microcalorimetry of the postnatal rat heart (Rattus norvegicus). Comp Biochem Physiol A Mol Integr Physiol 141: 310-318, 2005.
43. MURRY CE, JENNINGS RB, REIMER KA: Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124-1136, 1986.
44. NAKAGAWA T, SHIMIZU S, WATANABE T, YAMAGUCHI O, OTSU K, YAMAGATA H, INOHARA H, KUBO T, TSUJIMOTO Y: Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434: 652-658, 2005.
45. NAKANISHI T, OKUDO H, NAKAZAWA M, TAKAO A: Effect of acidosis on contractile function in the newborn rabbit heart. Pediatr Res 19: 482-488, 1985.
46. NECKÁŘ J, PAPOUŠEK F, NOVÁKOVÁ O, OŠŤÁDAL B, KOLÁŘ F: Cardioprotective effects of chronic hypoxia and ischaemic preconditioning are not additive. Basic Res Cardiol 97: 161-167, 2002.
47. NECKÁŘ J, SZÁRSZOI O, KOTEN L, PAPOUŠEK F, OŠŤÁDAL B, GROVER GJ, KOLÁŘ F: Effects of mitochondrial KATP modulators on cardioprotection induced by chronic high altitude hypoxia in rats. Cardiovasc Res 55: 567-575, 2002.
48. NETUKA I, SZARSZOI O, MALÝ J, BEŠÍK J, NECKÁŘ J, KOLÁŘ F, OŠŤÁDALOVÁ I, PIRK J, OŠŤÁDAL B: Effect of perinatal hypoxia on cardiac tolerance to acute ischaemia in adult male and female rats. Clin Exp Pharmacol Physiol 33: 714-719, 2006.
49. NIJJAR MS, DHALLA NS: Biochemical basis of calcium handling in developing myocardium. In: The Developing Heart. B OŠŤÁDAL, M NAGANO, N TAKEDA, NS DHALLA (eds), Lippincott, Philadelphia, 1997, pp 189-217.
50. NOLLERT G, FISCHLEIN T, BOUTERWEK S, BOHMER C, KLINNER W, REICHART B: 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 30: 1374-1383, 1997.
51. OLIVETTI G, ANVERSA P, LOUD AV: Morphometric study of early postnatal development in the left and right ventricular myocardium of the rat. II. Tissue composition, capillary growth and sarcoplasmic alterations. Circ Res 46: 503-512, 1980.
52. OŠŤÁDAL B, SCHIEBLER TH: Die terminale Strombahn in Herzen der Schildkröte (Testudo Hermanni). Z Anat Entwickl-Gesch 134: 111-116, 1971.
53. OŠŤÁDAL B, PROCHÁZKA J, JANATOVÁ T, PELOUCH V, KRAUSE EG: Developmental aspects of cardiac resistance to hypoxia. Ber Humboldt Univ Berlin 24: 52-58, 1982.
54. OŠŤÁDAL B, KOLÁŘ F, PELOUCH V, WIDIMSKÝ J: Ontogenetic differences in cardiopulmonary adaptation to chronic hypoxia. Physiol Res 44: 45-51, 1995.
55. OŠŤÁDAL B, OŠŤÁDALOVÁ I, DHALLA NS: Development of cardiac sensitivity to oxygen deficiency: comparative and ontogenetic aspects. Physiol Rev 79: 635-659, 1999.
56. OŠŤÁDAL B, KOLÁŘ F: Cardiac adaptation to chronic high altitude hypoxia. Respir Physiol Neurobiol 158: 224-236, 2007.
57. OŠŤÁDAL B, NETUKA I, MALÝ J, BEŠÍK J, OŠŤÁDALOVÁ I: Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp Biol Med 234: 1011-1019, 2009.
58. OŠŤÁDAL B, CHARVÁTOVÁ Z, OŠŤÁDALOVÁ I, KOLÁŘ F, NETUKA I: Development of cardiac tolerance to oxygen deprivation - experimental aspects. (in Czech) Cor Vasa 51: 691-697, 2009.
59. OŠŤÁDALOVÁ I, OŠŤÁDAL B: Ontogenetic differences in isoproterenol-induced 85Sr uptake in the myocardium. In: The Developing Heart. B OŠŤÁDAL, M NAGANO, N TAKEDA, NS DHALLA (eds), Lippincott, Philadelphia, 1997, pp 395-400.
60. 2+ in the isolated perinatal rat heart. Physiol Res 44: 135-137, 1995.
61. OŠŤÁDALOVÁ I, OŠŤÁDAL B, KOLÁŘ F, PARRATT JR, WILSON S: Tolerance to ischemia and ischaemic preconditioning in neonatal rat heart. J Mol Cell Cardiol 30: 857-865, 1998.
62. OŠŤÁDALOVÁ I, OŠŤÁDAL B, JARKOVSKÁ D, KOLÁŘ F: Ischemic preconditioning in chronically hypoxic neonatal rat heart. Pediatr Res 52: 561-567, 2002.
63. RAKUSAN K: Vascularization of the heart during normal and pathological growth. Adv Org Biol 7: 130-153, 1999.
64. RAKUSAN K, CHVOJKOVA Z, OLIVIERO P, OSTADALOVA I, KOLAR F, CHASSAGNE C, SAMUEL J-L, OSTADAL B: ANG II type 1 receptor antagonist irbesartan inhibits coronary angiogenesis stimulated by chronic intermittent hypoxia in neonatal rats. Am J Physiol 292: H1-H8, 2007.
65. RIVA A, HEARSE DJ: Age-dependent changes in myocardial succeptibility to ischemic injury. Cardioscience 4: 85-92, 1993.
66. ROHLICEK CV, VIAU S, TRIEU P, HÉBERT TE: Effects of neonatal hypoxia in the rat on inotropic stimulation of the adult heart. Cardiovasc Res 65: 861-868, 2005.
67. SCHAGGER H, NOACK H, HALANGK W, BRANDT U, VON JAGOW G: 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 230: 235-241, 1995.
68. SCHONFELD P, SCHILD L, BOHNENSACK R: Expression of the ADP/ATP carrier and expansion of the mitochondrial (ATP+ADP) pool contribute to postnatal maturation of the rat heart. Eur J Biochem 241: 895-900, 1996.
69. SINGER D: Metabolic adaptation to hypoxia: cost and benefit of being small. Respir Physiol Neurobiol 141: 215-228, 2004.
70. SNOECKX LH, CORNELUSSEN RN, VAN NIEUWENHOVEN FA, RENEMAN RS, VAN DER VUSSE GJ: Heat shock proteins and cardiovascular pathophysiology. Physiol Rev 81: 1461-1497, 2001.
71. SOLARO RJ, LEE JA, KENTISH JC, ALLEN DG: Effect of acidosis on ventricular muscle from adult neonatal rats. Circ Res 63: 779-787, 1988.
72. SOUTHWORTH R, SHATTOCK MJ, KELLY FJ: Age-related difference in the cardiac response to ischemia and free radical production on reperfusion. In: The Developing Heart. B OŠŤÁDAL, M NAGANO, N TAKEDA, NS DHALLA (eds), Lippincott, Philadelphia, 1997, pp 427-441.
73. SU JY, FRIEDMAN WF: Comparison of the responses of fetal and adult cardiac muscle to hypoxia. Am J Physiol 224: 1249-1253, 1973.
74. ŠAMÁNEK M, BASS A, OŠŤÁDAL B, HUČÍN B, STEJSKALOVÁ M: Effect of hypoxaemia on enzymes supplying myocardial energy in children with congenital heart disease. Int J Cardiol 25: 265-270, 1989.
75. ŠAMÁNEK M, URBANOVÁ Z: Prevention of Atherosclerosis in Children. (in Czech) Galén, Praha, 2003, 226 p.
76. ŠKÁRKA L, BARDOVÁ K, BRAUNER, FLACHS P, JARKOVSKÁ D, KOPECKÝ J, OŠŤÁDAL B: 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 35: 321-330, 2003.
77. ŠKOVRÁNEK J, OŠŤÁDAL B, PELOUCH V, PROCHÁZKA J: Ontogenetic differences in cardiac sensitivity to verapamil in rats. Pediatr Cardiol 7: 25-29, 1986.
78. 2+-exchanger and SERCA2 in rat heart. J Mol Cell Cardiol 27: 1689-1701, 1995.
79. VINTEN-JOHANSEN J: Postconditioning: a mechanical maneuver that triggers biological and molecular cardioprotective responses to reperfusion Heart Fail Rev 12: 235-244, 2007
80. VORNANEN M: Postnatal changes in cardiac calcium regulation. In: The Developing Heart. B OŠŤÁDAL, M NAGANO, N TAKEDA, NS DHALLA (eds), Lippincott, Philadelphia, 1997, pp 219-229.
81. WIBO M, BRAVO G, GODFRAIND T: Postnatal maturation of excitation-contraction coupling in rat ventricle in relation to the subcellular localization and surface density of 1,4-dihydropyridine and ryanodine receptors. Circ Res 68: 662-673, 1991.
82. WIBO M, KOLÁŘ F, ZHENG L, GODFRAIND T: Influence of thyroid status on postnatal maturation of calcium channels, β-adrenoceptors and cation transport ATPases in rat ventricular tissue. J Mol Cell Cardiol 27: 1731-1743, 1995.
83. XU Y, WILLIAMS SJ, O'BRIEN D, DAVIDGE ST: Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J 20: 1251-1253, 2006.
84. YELLON DM, DOWNEY JM: Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 83: 1113-1151, 2003.
85. YOUNG HH, SHIMIZU T, NISHIOKA K, NAKANISHI T, JARMAKANI JM: Effect of hypoxia and reoxygenation on mitochondrial function in neonatal myocardium. Am J Physiol 245: H998-H1006, 1983.