Chronic hypoxemia in late gestation decreases cardiomyocyte number but does not change expression of hypoxia-responsive genes

Journal of the American Heart Association

Volumn 3, Issue 4, 2014, Pages

  Botting, Kimberley J ^a,b   Caroline McMillen, I ^a,b   Forbes, Heather ^a   Nyengaard, Jens R ^c   Morrison, Janna L ^a,b  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Angiogenesis; Apoptosis; Hypoxia; Myocytes; Pregnancy

Indexed keywords

BECLIN 1; PROTEIN KINASE C EPSILON; APOPTOSIS REGULATORY PROTEIN; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 3; INDUCIBLE NITRIC OXIDE SYNTHASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; PROTEIN BAX; PROTEIN P53; VASCULOTROPIN A;

ADM GENE; ANG1 GENE; ANG2 GENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BAX GENE; BCL2 GENE; BECN1 GENE; BNIP3 GENE; CAPILLARY; CAPILLARY DENSITY; CELL COUNT; CONTROLLED STUDY; FEMALE; FETUS; FETUS WEIGHT; FLT1 GENE; GENE; GENE EXPRESSION REGULATION; GESTATIONAL AGE; GLUT1 GENE; GLUT3 GENE; HEART MUSCLE CELL; HYPOXEMIA; INOS GENE; LAMP1 GENE; MAP1LC3B GENE; NONHUMAN; OXYGEN CONSUMPTION; OXYGEN SATURATION; OXYGEN TENSION; PRIORITY JOURNAL; TIE2 GENE; TRANSCRIPTION REGULATION; VEGF GENE; ANIMAL; ANOXIA; CARDIAC MUSCLE CELL; CYTOLOGY; GENETICS; METABOLISM; PLACENTA INSUFFICIENCY; PREGNANCY; PROTO ONCOGENE; SHEEP;

ANIMALS; ANOXIA; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; CELL COUNT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, BCL-2; GLUCOSE TRANSPORTER TYPE 1; GLUCOSE TRANSPORTER TYPE 3; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MYOCYTES, CARDIAC; NITRIC OXIDE SYNTHASE TYPE II; PLACENTAL INSUFFICIENCY; PREGNANCY; RNA, MESSENGER; SHEEP; TUMOR SUPPRESSOR PROTEIN P53; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923211114     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.113.000531     Document Type: Article

References (54)

1. Sugishita Y, Leifer DW, Agani F, Watanabe M, Fisher SA. Hypoxia-responsive signaling regulates the apoptosis-dependent remodeling of the embryonic avian cardiac outflow tract. Dev Biol. 2004;273:285-296.
2. Yue X, Tomanek RJ. Stimulation of coronary vasculogenesis/angiogenesis by hypoxia in cultured embryonic hearts. Dev Dyn. 1999;216:28-36.
3. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol. 2000;88:1474-1480.
4. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008;30:393-402.
5. An WG, Kanekal M, Simon MC, Maltepe E, Blagosklonny MV, Neckers LM. Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature. 1998;392:405-408.
6. Patterson AJ, Zhang L. Hypoxia and fetal heart development. Curr Mol Med. 2010;10:653-666.
7. Gagnon R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol. 2003;110(suppl 1):S99-S107.
8. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005;85:571-633.
9. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98-102.
10. Morrison JL. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol. 2008;35:730-743.
11. Bae S, Xiao Y, Li G, Casiano CA, Zhang L. Effect of maternal chronic hypoxic exposure during gestation on apoptosis in fetal rat heart. Am J Physiol Heart Circ Physiol. 2003;285:H983-H990.
12. 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 rat. J Soc Gynecol Investig. 2003;10:265-274.
13. Patterson AJ, Chen M, Xue Q, Xiao D, Zhang L. Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ Res. 2010;107:365-373.
14. Patterson AJ, Xiao D, Xiong F, Dixon B, Zhang L. Hypoxia-derived oxidative stress mediates epigenetic repression of PKCe gene in foetal rat hearts. Cardiovasc Res. 2012;93:302-310.
15. Li F, Wang X, Capasso JM, Gerdes AM. Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. J Mol Cell Cardiol. 1996;28:1737-1746.
16. Botting KJ, Wang KC, Padhee M, McMillen IC, Summers-Pearce B, Rattanatray L, Cutri N, Posterino GS, Brooks DA, Morrison JL. Early origins of heart disease: low birth weight and determinants of cardiomyocyte endowment. Clin Exp Pharmacol Physiol. 2012;39:814-823.
17. Bubb KJ, Cock ML, Black MJ, Dodic M, Boon WM, Parkington HC, Harding R, Tare M. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol. 2007;578:871-881.
18. Louey S, Jonker SS, Giraud GD, Thornburg KL. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol. 2007;580:639-648.
19. Morrison JL, Botting KJ, Dyer JL, Williams SJ, Thornburg KL, McMillen IC. Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol. 2007;293:R306-R313.
20. Simonetta G, Rourke AK, Owens JA, Robinson JS, McMillen IC. Impact of placental restriction on the development of the sympathoadrenal system. Pediatr Res. 1997;42:805-811.
21. Wang KC, Zhang L, McMillen IC, Botting KJ, Duffield JA, Zhang S, Suter CM, Brooks DA, Morrison JL. Fetal growth restriction and the programming of heart growth and cardiac insulin-like growth factor 2 expression in the lamb. J Physiol. 2011;589:4709-4722.
22. Muhlfeld C, Nyengaard JR, Mayhew TM. A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research. Cardiovasc Pathol. 2010;19:65-82.
23. Gundersen HJ. The smooth fractionator. J Microsc. 2002;207:191-210.
24. Nyengaard JR, Gundersen JG. The isector: a simple and direct method for generating isotropic, uniform random sections from small specimen. J Microsc. 1992;165:427-431.
25. Gundersen HJ. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc. 1986;143:3-45.
26. Bruel A, Oxlund H, Nyengaard JR. The total length of myocytes and capillaries, and total number of myocyte nuclei in the rat heart are time-dependently increased by growth hormone. Growth Horm IGF Res. 2005;15:256-264.
27. Passmore M, Nataatmadja M, Fraser JF. Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in Ovis aries. BMC Mol Biol. 2009;10:72.
28. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8:R19.
29. Soo PS, Hiscock J, Botting KJ, Roberts CT, Davey AK, Morrison JL. Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod Toxicol. 2012;33:374-381.
30. Gentili S, Morrison JL, McMillen IC. Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2, and HSDL1 mRNA in the sheep fetus in late gestation. Biol Reprod. 2009;80:1121-1127.
31. Corstius HB, Zimanyi MA, Maka N, Herath T, Thomas W, van der Laarse A, Wreford NG, Black MJ. Effect of intrauterine growth restriction on the number of cardiomyocytes in rat hearts. Pediatr Res. 2005;57:796-800.
32. 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: H1712-H1719.
33. Burrell JH, Boyn AM, Kumarasamy V, Hsieh A, Head SI, Lumbers ER. Growth and maturation of cardiac myocytes in fetal sheep in the second half of gestation. Anat Rec A Discov Mol Cell Evol Biol. 2003;274:952-961.
34. Thornburg KL, Louey S, Giraud GD. The role of growth in heart development. Nestle Nutr Workshop Ser Pediatr Program. 2008;61:39-51.
35. Porrello ER, Widdop RE, Delbridge LM. Early origins of cardiac hypertrophy: does cardiomyocyte attrition programme for pathological 'catch-up' growth of the heart? Clin Exp Pharmacol Physiol. 2008;35:1358-1364.
36. Porrello ER, Bell JR, Schertzer JD, Curl CL, McMullen JR, Mellor KM, Ritchie RH, Lynch GS, Harrap SB, Thomas WG, Delbridge LM. Heritable pathologic cardiac hypertrophy in adulthood is preceded by neonatal cardiac growth restriction. Am J Physiol Regul Integr Comp Physiol. 2009;296:R672-R680.
37. Harrap SB, Danes VR, Ellis JA, Griffiths CD, Jones EF, Delbridge LM. The hypertrophic heart rat: a new normotensive model of genetic cardiac and cardiomyocyte hypertrophy. Physiol Genomics. 2002;9:43-48.
38. Stacy V, De Matteo R, Brew N, Sozo F, Probyn ME, Harding R, Black MJ. The influence of naturally occurring differences in birthweight on ventricular cardiomyocyte number in sheep. Anat Rec (Hoboken). 2009;292:29-37.
39. Takagi-Morishita Y, Yamada N, Sugihara A, Iwasaki T, Tsujimura T, Terada N. Mouse uterine epithelial apoptosis is associated with expression of mitochondrial voltage-dependent anion channels, release of cytochrome C from mitochondria, and the ratio of Bax to Bcl-2 or Bcl-X. Biol Reprod. 2003;68:1178-1184.
40. Sermeus A, Michiels C. Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis. 2011;2:e164.
41. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature. 1996;379:88-91.
42. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol. 2008;9:402-412.
43. Wang EY, Gang H, Aviv Y, Dhingra R, Margulets V, Kirshenbaum LA. p53 Mediates autophagy and cell death by a mechanism contingent on BNIP3. Hypertension. 2013;62:70-77.
44. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA. 2002;99:12825-12830.
45. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, Hakem R, Greenberg AH. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol. 2000;20:5454-5468.
46. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB. Response to myocardial ischemia/reperfusion injury involves BNIP3 and autophagy. Cell Death Differ. 2007;14:146-157.
47. Masschelein E, Van Thienen R, D'Hulst G, Hespel P, Thomis M, Deldicque L. Acute environmental hypoxia induces LC3 lipidation in a genotype-dependent manner. FASEB J. 2014;28:1022-1034.
48. Ishihara M, Urushido M, Hamada K, Matsumoto T, Shimamura Y, Ogata K, Inoue K, Taniguchi Y, Horino T, Fujieda M, Fujimoto S, Terada Y. Sestrin-2 and BNIP3 regulate autophagy and mitophagy in renal tubular cells in acute kidney injury. Am J Physiol Renal Physiol. 2013;305:F495-F509.
49. de Theije CC, Langen RC, Lamers WH, Schols AM, Kohler SE. Distinct responses of protein turnover regulatory pathways in hypoxia-and semistarvation-induced muscle atrophy. Am J Physiol Lung Cell Mol Physiol. 2013;305:L82-L91.
50. Wang J, Pan XL, Ding LJ, Liu DY, Da-Peng L, Jin T. Aberrant expression of Beclin-1 and LC3 correlates with poor prognosis of human hypopharyngeal squamous cell carcinoma. PLoS One. 2013;8:e69038.
51. Escobar ML, Echeverria OM, Sanchez-Sanchez L, Mendez C, Pedernera E, Vazquez-Nin GH. Analysis of different cell death processes of prepubertal rat oocytes in vitro. Apoptosis. 2010;15:511-526.
52. Ginouves A, Ilc K, Macias N, Pouyssegur J, Berra E. PHDs overactivation during chronic hypoxia "desensitizes" HIFalpha and protects cells from necrosis. Proc Natl Acad Sci USA. 2008;105:4745-4750.
53. Le Moine CM, Morash AJ, McClelland GB. Changes in HIF-1alpha protein, pyruvate dehydrogenase phosphorylation, and activity with exercise in acute and chronic hypoxia. Am J Physiol Regul Integr Comp Physiol. 2011;301: R1098-R1104.
54. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med. 2003;9:677-684.