Cortisol stimulates proliferation and apoptosis in the late gestation fetal heart: Differential effects of mineralocorticoid and glucocorticoid receptors

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 305, Issue 4, 2013, Pages

  Feng, Xiaodi ^a   Reini, Seth A ^a   Richards, Elaine ^a   Wood, Charles E ^a   Keller Wood, Maureen ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cardiomyocyte; Caspase 3; Purkinje fiber; Sheep; Stress

Indexed keywords

CANRENOIC ACID; CASPASE 3; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; KI 67 ANTIGEN; MIFEPRISTONE; MINERALOCORTICOID RECEPTOR; STEM CELL FACTOR; CANRENOATE POTASSIUM; MINERALOCORTICOID ANTAGONIST; STEM CELL FACTOR RECEPTOR; MICROTUBULE ASSOCIATED PROTEIN 2;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FETUS; FETUS HEART; HEART CONDUCTION; HEART WEIGHT; NONHUMAN; PRIORITY JOURNAL; PURKINJE FIBER; STAINING; ANIMAL; CARDIOMEGALY; CARDIOMYOCYTE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; GESTATIONAL AGE; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PREGNANCY; SHEEP; STEM CELL; STRESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RETRIEVAL; AUTOPSY; BODY WEIGHT; CELL POPULATION; ELECTRIC CONDUCTIVITY; ENZYME ACTIVATION; HEART LEFT VENTRICLE; HEART RIGHT VENTRICLE; HYDROCORTISONE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; ONCOGENE C KIT; PRENATAL EXPOSURE; THIRD TRIMESTER PREGNANCY;

CARDIOMYOCYTE; CASPASE-3; PURKINJE FIBER; SHEEP; STRESS;

ANIMALS; APOPTOSIS; CANRENOATE POTASSIUM; CARDIOMEGALY; CASPASE 3; CELL PROLIFERATION; FEMALE; FETAL HEART; GESTATIONAL AGE; HYDROCORTISONE; INFUSIONS, INTRAVENOUS; KI-67 ANTIGEN; MIFEPRISTONE; MINERALOCORTICOID RECEPTOR ANTAGONISTS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-KIT; PURKINJE FIBERS; RECEPTORS, GLUCOCORTICOID; RECEPTORS, MINERALOCORTICOID; SHEEP; STEM CELLS;

EID: 84881625037     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00112.2013     Document Type: Article

References (62)

1. Abel MH, Bass FG, Krane EJ, Thomas AL, Liggins GC. Pituitary stalk-section and some of its effects on endocrine function in the fetal lamb. Q J Exp Physiol Cogn Med Sci 63: 211-219, 1978.
2. Airey JA, Almeida-Porada G, Colletti EJ, Porada CD, Chamberlain J, Movsesian M, Sutko JL, Zanjani ED. Human mesenchymal stem cells form Purkinje fibers in fetal sheep heart. Circulation 109: 1401-1407, 2004.
3. Al Jarallah AS. Reversible cardiomyopathy caused by an uncommon form of congenital adrenal hyperplasia. Pediatr Cardiol 25: 675-676, 2004.
4. Almeida OF, Conde GL, Crochemore C, Demeneix BA, Fischer D, Hassan AH, Meyer M, Holsboer F, Michaelidis TM. Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corti-costeroid receptors decide neuronal fate. FASEB J 14: 779-790, 2000.
5. Anacker C, Cattaneo A, Luoni A, Musaelyan K, Zunszain PA, Milanesi E, Rybka J, Berry A, Cirulli F, Thuret S, Price J, Riva MA, Gennarelli M, Pariante CM. Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology 38: 872-883, 2013.
6. Aoyama N, Yamashina S, Poelmann RE, Gittenberger-De Groot AC, Izumi T, Soma K, Ohwada T. Conduction system abnormalities in rat embryos induced by maternal hyperthermia. Anat Rec 267: 213-219, 2002.
7. Arriza JL, Weinberger C, Cerelli G, Glaser TM, Handelin BL, Housman DE, Evans RM. Cloning of human mineralocorticoid receptor complementary DNA: structural and functional kinship with the glucocor-ticoid receptor. Science 237: 268-275, 1987.
8. Atkinson A, Inada S, Li J, Tellez JO, Yanni J, Sleiman R, Allah EA, Anderson RH, Zhang H, Boyett MR, Dobrzynski H. Anatomical and molecular mapping of the left and right ventricular His-Purkinje conduction networks. J Mol Cell Cardiol 51: 689-701, 2011.
9. Bassett JM, Thorburn GD. Foetal plasma corticosteroids and the initiation of parturition in sheep. J Endocrinol 44: 285-286, 1969.
10. Boeuf B, Maragnes P, Belzic I, Lacotte J, Bonte JB, Guillois B. [Glucocorticoid-induced hypertrophic cardiomyopathy in premature infants: apropos of 4 cases]. Arch Pediatr 4: 152-157, 1997.
11. Caceres A, Payne MR, Binder LI, Steward O. Immunocytochemical localization of actin and microtubule-associated protein MAP2 in dendritic spines. Proc Natl Acad Sci USA 80: 1738-1742, 1983.
12. Canale E, Smolich JJ, Campbell GR. Differentiation and innervation of the atrioventricular bundle and ventricular Purkinje system in sheep heart. Development 100: 641-651, 1987.
13. Cottrell EC, Seckl JR. Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci 3: 19, 2009.
14. Crochemore C, Lu J, Wu Y, Liposits Z, Sousa N, Holsboer F, Almeida OF. Direct targeting of hippocampal neurons for apoptosis by glucocor-ticoids is reversible by mineralocorticoid receptor activation. Mol Psychiatry 10: 790-798, 2005.
15. Davis EP, Glynn LM, Waffarn F, Sandman CA. Prenatal maternal stress programs infant stress regulation. J Child Psychol Psychiatry 52: 119-129, 2011.
16. de Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev 19: 269-301, 1998.
17. Di Meglio F, Castaldo C, Nurzynska D, Romano V, Miraglia R, Bancone C, Langella G, Vosa C, Montagnani S. Epithelial-mesenchy-mal transition of epicardial mesothelium is a source of cardiac CD117-positive stem cells in adult human heart. J Mol Cell Cardiol 49: 719-727, 2010.
18. Entringer S, Buss C, Swanson JM, Cooper DM, Wing DA, Waffarn F, Wadhwa PD. Fetal programming of body composition, obesity, and metabolic function: the role of intrauterine stress and stress biology. J Nutr Metab 2012: 632548, 2012.
19. Fayol L, Masson P, Millet V, Simeoni U. Cushing's syndrome in pregnancy and neonatal hypertrophic obstructive cardiomyopathy. Acta Paediatr 93: 1400-1402, 2004.
20. Federico C. Natriuretic Peptide system and cardiovascular disease. Heart Views 11: 10-15, 2010.
21. Ferreira-Martins J, Ogãrek B, Cappetta D, Matsuda A, Signore S, D'Amario D, Kostyla J, Steadman E, Ide-Iwata N, Sanada F, Iaffal-dano G, Ottolenghi S, Hosoda T, Leri A, Kajstura J, Anversa P, Rota M. Cardiomyogenesis in the developing heart is regulated by c-kit-positive cardiac stem cells. Circ Res 110: 701-715, 2012.
22. Forsgren S, Thornell LE. The development of Purkinje fibres and ordinary myocytes in the bovine fetal heart. An ultrastructural study. Anat Embryol (Berl) 162: 127-136, 1981.
23. Giraud GD, Louey S, Jonker S, Schultz J, Thornburg KL. Cortisol Stimulates Cell Cycle Activity in the Cardiomyocyte of the Sheep Fetus. Endocrinology 147: 3643-3649, 2006.
24. Gittenberger-De Groot AC, Winter EM, Bartelings MM, Goumans MJ, Deruiter MC, Poelmann RE. The arterial and cardiac epicardium in development, disease and repair. Differentiation 84: 41-53, 2012.
25. Guo C, Martinez-Vasquez D, Mendez GP, Toniolo MF, Yao TM, Oestreicher EM, Kikuchi T, Lapointe N, Pojoga L, Williams GH, Ricchiuti V, Adler GK. Mineralocorticoid receptor antagonist reduces renal injury in rodent models of types 1 and 2 diabetes mellitus. Endocrinology 147: 5363-5373, 2006.
26. Harris A, Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59: 279-289, 2011.
27. Hou J, Wang L, Jiang J, Zhou C, Guo T, Zheng S, Wang T. Cardiac stem cells and their roles in myocardial infarction. Stem Cell Rev 2012.
28. Jensen E, Wood CE, Keller-Wood M. Chronic alterations in ovine maternal corticosteroid levels influence uterine blood flow and placental and fetal growth. Am J Physiol Regul Integr Comp Physiol 288: R54-R61, 2005.
29. Jerse M, Zidar N. Apoptosis in the developing human heart resembles apoptosis in epithelial tissues. Cell Tissue Res 343: 537-543, 2011.
30. Jonker SS, Zhang L, Louey S, Giraud GD, Thornburg KL, Faber JJ. Myocyte enlargement, differentiation, and proliferation kinetics in the fetal sheep heart. J Appl Physiol 102: 1130-1142, 2007.
31. Keller-Wood M. Inhibition of stimulated and basal ACTH by cortisol during ovine pregnancy. Am J Physiol Regul Integr Comp Physiol 271: R130-R136, 1996.
32. Lai M, Horsburgh K, Bae SE, Carter RN, Stenvers DJ, Fowler JH, Yau JL, Gomez-Sanchez CE, Holmes MC, Kenyon CJ, Seckl JR, Macleod MR. Forebrain mineralocorticoid receptor overexpression enhances memory, reduces anxiety and attenuates neuronal loss in cerebral ischaemia. Eur J Neurosci 25: 1832-1842, 2007.
33. Liggins GC. Adrenocortical-related maturational events in the fetus. Am J Obstet Gynecol 126: 931, 1976.
34. Liggins GC, Howie RN. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics 50: 515-525, 1972.
35. Louey S, Jonker SS, Giraud GD, Thornburg KL. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol 580: 639-648, 2007.
36. Lumbers ER, Boyce AC, Joulianos G, Kumarasamy V, Barner E, Segar JL, Burrell JH. Effects of cortisol on cardiac myocytes and on expression of cardiac genes in fetal sheep. Am J Physiol Regul Integr Comp Physiol 288: R567-R574, 2005.
37. Manasek FJ. Myocardial cell death in the embryonic chick ventricle. J Embryol Exp Morphol 21: 271-284, 1969.
38. Martinerie L, Munier M, Le MD, Meduri G, Viengchareun S, Lombes M. The mineralocorticoid signaling pathway throughout development: Expression, regulation and pathophysiological implications. Biochimie 95: 148-157, 2013.
39. Mikawa T, Gourdie RG, Takebayashi-Suzuki K, Kanzawa N, Hyer J, Pennisi DJ, Poma CP, Shulimovich M, Diaz KG, Layliev J, Prasad A. Induction and patterning of the Purkinje fibre network. Novartis Found Symp 250: 142-153, 2003.
40. Mildenhall L, Battin M, Bevan C, Kuschel C, Harding JE. Repeat prenatal corticosteroid doses do not alter neonatal blood pressure or myocardial thickness: randomized, controlled trial. Pediatrics 123: e646-e652, 2009.
41. 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 293: R306-R313, 2007.
42. Murphy BE, Clark SJ, Donald IR, Pinsky M, Vedady D. Conversion of maternal cortisol to cortisone during placental transfer to the human fetus. Am J Obstet Gynecol 118: 538-541, 1974.
43. Ouvrard-Pascaud A, Sainte-Marie Y, Benitah JP, Perrier R, Souka-seum C, Nguyen Dinh CA, Royer A, Le QK, Charpentier F, Demolombe S, Mechta-Grigoriou F, Beggah AT, Maison-Blanche P, Oblin ME, Delcayre C, Fishman GI, Farman N, Escoubet B, Jaisser F. Conditional mineralocorticoid receptor expression in the heart leads to life-threatening arrhythmias. Circulation 111: 3025-3033, 2005.
44. Pitt B, Williams G, Remme W, Martinez F, Lopez-Sendon J, Zannad F, Neaton J, Roniker B, Hurley S, Burns D, Bittman R, Kleiman J. The EPHESUS trial: eplerenone in patients with heart failure due to systolic dysfunction complicating acute myocardial infarction. Eplerenone Post-AMI Heart Failure Efficacy and Survival Study. Cardiovasc Drugs Ther 15: 79-87, 2001.
45. Rashid S, Lewis GF. The mechanisms of differential glucocorticoid and mineralocorticoid action in the brain and peripheral tissues. Clin Biochem 38: 401-409, 2005.
46. Reini SA, Dutta G, Wood CE, Keller-Wood M. Cardiac corticosteroid receptors mediate the enlargement of the ovine fetal heart induced by chronic increases in maternal cortisol. J Endocrinol 198: 419-427, 2008.
47. Reini SA, Wood CE, Jensen E, Keller-Wood M. Increased maternal cortisol in late gestation ewes decreases fetal cardiac expression of 11fS-HSD2 mRNA and the ratio of AT1 to AT2 receptor mRNA. Am J Physiol Regul Integr Comp Physiol 291: R1708-R1716, 2006.
48. Ren R, Oakley RH, Cruz-Topete D, Cidlowski JA. Dual role for glucocorticoids in cardiomyocyte hypertrophy and apoptosis. Endocrinology 153: 5346-5360, 2012.
49. Rogalska J, Kang P, Wotherspoon W, Macleod MR, Lai M. Effect of hyperthermia and anoxia on glucocorticoid and mineralocorticoid receptor expression in neonatal rat hippocampus. Neurosci Lett 450: 196-200, 2009.
50. Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 23: 291-299, 2001.
51. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675, 2012.
52. Scire G, D'Anella G, Cristofori L, Mazzuca V, Cianfarani S. Marked left ventricular hypertrophy mimicking hypertrophic cardiomyopathy associated with steroid therapy for congenital adrenal hyperplasia. J Cardiovasc Med (Hagerstown) 8: 465-467, 2007.
53. Sohn HJ, Yoo KH, Jang GY, Lee JH, Choi BM, Lee JH, Bae IS, Yim HE, Son CS, Lee JW. Aldosterone modulates cell proliferation and apoptosis in the neonatal rat heart. J Korean Med Sci 25: 1296-1304, 2010.
54. Winter EM, Gittenberger-De Groot AC. Epicardium-derived cells in cardiogenesis and cardiac regeneration. Cell Mol Life Sci 64: 692-703, 2007.
55. Winter EM, Grauss RW, Hogers B, van Tuyn J, van der Geest R, Lie-Venema H, Steijn RV, Maas S, Deruiter MC, deVries AA, Steendijk P, Doevendans PA, Van Der Laarse A, Poelmann RE, Schalij MJ, Atsma DE, Gittenberger-De Groot AC. Preservation of left ventricular function and attenuation of remodeling after transplantation of human epicardium-derived cells into the infarcted mouse heart. Circulation 116: 917-927, 2007.
56. Wong EY, Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci 22: 785-792, 2005.
57. Wood CE. Negative-feedback inhibition of fetal ACTH secretion by maternal cortisol. Am J Physiol Regul Integr Comp Physiol 252: R743-R748, 1987.
58. Woolley CS, Gould E, Sakai RR, Spencer RL, McEwen BS. Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res 554: 312-315, 1991.
59. Wu SM, Chien KR, Mummery C. Origins and fates of cardiovascular progenitor cells. Cell 132: 537-543, 2008.
60. Yim HE, Yoo KH, Bae IS, Jang GY, Hong YS, Lee JW. Aldosterone regulates cellular turnover and mitogen-activated protein kinase family expression in the neonatal rat kidney. J Cell Physiol 219: 724-733, 2009.
61. Young MJ, Lam EY, Rickard AJ. Mineralocorticoid receptor activation and cardiac fibrosis. Clin Sci (Lond) 112: 467-475, 2007.
62. Yunis KA, Bitar FF, Hayek P, Mroueh SM, Mikati M. Transient hypertrophic cardiomyopathy in the newborn following multiple doses of antenatal corticosteroids. Am J Perinatol 16: 17-21, 1999.