Unexpected maturation of PI3K and MAPK-ERK signaling in fetal ovine cardiomyocytes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 8, 2014, Pages H1216-H1225

  Chattergoon, N N ^a   Louey, S ^a,b   Stork, P J ^a,c   Giraud, G D ^a,b,d   Thornburg, K L ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Cardiomyocyte proliferation; Fetal heart; MAPK; PI3K; Thyroid hormone

Indexed keywords

LIOTHYRONINE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; S6 KINASE; SOMATOMEDIN C; PROTEIN KINASE INHIBITOR; THYROID HORMONE;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL MATURATION; FETUS; GESTATIONAL AGE; HEART MUSCLE CELL; IN VITRO STUDY; NONHUMAN; SHEEP; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; FETUS HEART; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FETAL HEART; INSULIN-LIKE GROWTH FACTOR I; MAP KINASE SIGNALING SYSTEM; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SHEEP; THYROID HORMONES;

EID: 84908110190     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00833.2013     Document Type: Article

References (51)

1. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ, Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 279: R1157-R1164, 2000.
2. Barker DJ. Fetal origins of coronary heart disease. BMJ 311: 171-174, 1995.
3. Barker DJ, Osmond C, Law CM. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health 43: 237-240, 1989.
4. 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 274: 952-961, 2003.
5. Burton PB, Raff MC, Kerr P, Yacoub MH, Barton PJ. An intrinsic timer that controls cell-cycle withdrawal in cultured cardiac myocytes. Dev Biol 216: 659-670, 1999.
6. Chattergoon NN, Giraud GD, Louey S, Stork P, Fowden AL, Thornburg KL. Thyroid hormone drives fetal cardiomyocyte maturation. FASEB J 26: 397-408, 2012.
7. Chattergoon NN, Giraud GD, Thornburg KL. Thyroid hormone inhibits proliferation of fetal cardiac myocytes in vitro. J Endocrinol 192: R1-R8, 2007.
8. Chattergoon NN, Louey S, Stork P, Giraud GD, Thornburg KL. Mid-gestation ovine cardiomyocytes are vulnerable to mitotic suppression by thyroid hormone. Reprod Sci 19: 642-649, 2012.
9. Chopra IJ, Carlson HE, Solomon DH. Comparison of inhibitory effects of 3,5,3'-triiodothyronine (T3), thyroxine (T4), 3,3,',5'-triiodothyronine (rT3), and 3,3'-diiodothyronine (T2) on thyrotropin-releasing hormoneinduced release of thyrotropin in the rat in vitro. Endocrinology 103: 393-402, 1978.
10. Clubb FJ Jr., Bishop SP. Formation of binucleated myocardial cells in the neonatal rat An index for growth hypertrophy. Lab Invest 50: 571-577, 1984.
11. Delafontaine P. Insulin-like growth factor I and its binding proteins in the cardiovascular system. Cardiovasc Res 30: 825-834, 1995.
12. Forhead AJ, Curtis K, Kaptein E, Visser TJ, Fowden AL. Developmental control of iodothyronine deiodinases by cortisol in the ovine fetus and placenta near term. Endocrinology 147: 5988-5994, 2006.
13. Fowden AL, Mundy L, Silver M. Developmental regulation of glucogenesis in the sheep fetus during late gestation. J Physiol 508: 937-947, 1998.
14. Garcia-Silva S, Aranda A. The thyroid hormone receptor is a suppressor of ras-mediated transcription, proliferation, and transformation. Mol Cell Biol 24: 7514-7523, 2004.
15. 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.
16. Green NK, Gammage MD, Franklyn JA, Heagerty AM, Sheppard MC. Regulation of beta myosin heavy chain, c-myc and c-fos protooncogenes in thyroid hormone-induced hypertrophy of the rat myocardium. Clin Sci (Lond) 84: 61-67, 1993.
17. Green NK, Gammage MD, Franklyn JA, Sheppard MC. Regulation by thyroid status of c-myc, c-fos and H-ras mRNAs in the rat myocardium. J Endocrinol 130: 239-244, 1991.
18. Hopkins PS, Thorburn GD. The effects of foetal thyroidectomy on the development of the ovine foetus. J Endocrinol 54: 55-66, 1972.
19. Hu LW, Benvenuti LA, Liberti EA, Carneiro-Ramos MS, Barreto-Chaves ML. Thyroxine-induced cardiac hypertrophy: influence of adrenergic nervous system versus renin-angiotensin system on myocyte remodeling. Am J Physiol Regul Integr Comp Physiol 285: R1473-R1480, 2003.
20. Jonker SS, Faber JJ, Anderson DF, Thornburg KL, Louey S, Giraud GD. Sequential growth of fetal sheep cardiac myocytes in response to simultaneous arterial and venous hypertension. Am J Physiol Regul Integr Comp Physiol 292: R913-R919, 2007.
21. Jonker SS, Giraud MK, Giraud GD, Chattergoon NN, Louey S, Davis LE, Faber JJ, Thornburg KL. Cardiomyocyte enlargement, proliferation and maturation during chronic fetal anaemia in sheep. Exp Physiol 95: 131-139, 2010.
22. Jonker SS, Louey S, Thornburg KL, Faber JJ, Giraud GD. Cardiac myocyte growth dynamics change at birth. Reprod Sci 20, Suppl 3: 212A, 2013.
23. 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.
24. Kahaly GJ, Dillmann WH. Thyroid hormone action in the heart. Endocr Rev 26: 704-728, 2005.
25. Kajantie E, Phillips DI, Osmond C, Barker DJ, Forsen T, Eriksson JG. Spontaneous hypothyroidism in adult women is predicted by small body size at birth and during childhood. J Clin Endocrinol Metab 91: 4953-4956, 2006.
26. Kinugawa K, Jeong MY, Bristow MR, Long CS. Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol Endocrinol 19: 1618-1628, 2005.
27. Kuzman JA, Gerdes AM, Kobayashi S, Liang Q. Thyroid hormone activates Akt and prevents serum starvation-induced cell death in neonatal rat cardiomyocytes. J Mol Cell Cardiol 39: 841-844, 2005.
28. 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.
29. Mai W, Janier MF, Allioli N, Quignodon L, Chuzel T, Flamant F, Samarut J. Thyroid hormone receptor alpha is a molecular switch of cardiac function between fetal and postnatal life. Proc Natl Acad Sci USA 10332-10337, 2006.
30. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M. Regulation of Raf-Akt Cross-talk. J Biol Chem 277: 31099-31106, 2002.
31. O'Tierney PF, Chattergoon NN, Louey S, Giraud GD, Thornburg KL. Atrial natriuretic peptide inhibits angiotensin II-stimulated proliferation in fetal cardiomyocytes. J Physiol 558: 2879-2889, 2010.
32. Oliver MH, Harding JE, Breier BH, Gluckman PD. Fetal insulin-like growth factor (IGF)-I and IGF-II are regulated differently by glucose or insulin in the sheep fetus. Reprod Fertil Dev 8: 167-172, 1996.
33. Oliver MH, Harding JE, Breier BH, Gluckman PD. Fetal insulin-like growth factor (IGF)-I and IGF-II are regulated differently by glucose or insulin in the sheep fetus. Reprod Fertil Dev 8: 167-172, 1996.
34. Phillips DI, Cooper C, Fall C, Prentice L, Osmond C, Barker DJ, Rees SB. Fetal growth and autoimmune thyroid disease. Q J Med 86: 247-253, 1993.
35. Polk DH. Thyroid hormone metabolism during development. Reprod Fertil Dev 7: 469-477, 1995.
36. Polk DH, Wu SY, Wright C, Reviczky AL, Fisher DA. Ontogeny of thyroid hormone effect on tissue 5'-monodeiodinase activity in fetal sheep. Am J Physiol Endocrinol Metab 254: E337-E341, 1988.
37. Rakusan K. Cardiac growth, maturation, aging. In: Growth of the Heart in Health and Disease, edited by Zak R. New York: Raven, 1984, p. 131-164.
38. Ramos JW. The regulation of extracellular signal-regulated kinase (ERK) in mammalian cells. Int J Biochem Cell Biol 40: 2707-2719, 2008.
39. Scott PH, Belham CM, al Hafidh J, Chilvers ER, Peacock AJ, Gould GW, Plevin R. A regulatory role for cAMP in phosphatidylinositol 3-kinase/p70 ribosomal S6 kinase-mediated DNA synthesis in plateletderived-growth-factor-stimulated bovine airway smooth-muscle cells. Biochem J 318: 965-971, 1996.
40. Sedmera D, Pexieder T, Vuillemin M, Thompson RP, Anderson RH. Developmental patterning of the myocardium. Anat Rec 258: 319-337, 2000.
41. Soonpaa MH, Kim KK, Pajak L, Franklin M, Field LJ. Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol Heart Circ Physiol 271: H2183-H2189, 1996.
42. Soonpaa MH, Koh GY, Pajak L, Jing S, Wang H, Franklin MT, Kim KK, Field LJ. Cyclin D1 overexpression promotes cardiomyocyteDNAsynthesis and multinucleation in transgenic mice. J Clin Invest 99: 2644-2654, 1997.
43. Stork PJ, Schmitt JM. Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12: 258-266, 2002.
44. Sundgren NC, Giraud GD, Schultz JM, Lasarev MR, Stork PJ, Thornburg KL. Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes. Am J Physiol Regul Integr Comp Physiol 285: R1481-R1489, 2003.
45. Sundgren NC, Giraud GD, Stork PJ, Maylie JG, Thornburg KL. Angiotensin II stimulates hyperplasia but not hypertrophy in immature ovine cardiomyocytes. J Physiol 548: 881-891, 2003.
46. Thaler S, Hahnel PS, Schad A, Dammann R, Schuler M. RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEK-ERK pathway and inhibition of Akt. Cancer Res 69: 1748-1757, 2009.
47. Thorburn GD, Hopkins PS. Thyroid function in the foetal lamb. In: Foetal and Neonatal Physiology: Proceedings of the Sir Joseph Barcroft Centenary Symposium held at The Physiological Laboratory Cambridge, edited by Comline KS, Cross KW, Dawes GS, Nathanielsz PW. Texas: Cambridge Univ. Press, 1973, p. 488-507.
48. Thornburg K, Jonker S, O'Tierney P, Chattergoon N, Louey S, Faber J, Giraud G. Regulation of the cardiomyocyte population in the developing heart. Prog Biophys Mol Biol 106: 289-299, 2010.
49. Wang L, Gout I, Proud CG. Cross-talk between the ERK and p70 S6 kinase (S6K) signaling pathways. MEK-dependent activation of S6K2 in cardiomyocytes. J Biol Chem 276: 32670-32677, 2001.
50. Wu S, Polk D, Wong S, Reviczky A, Vu R, Fisher DA. Thyroxine sulfate is a major thyroid hormone metabolite and a potential intermediate in the monodeiodination pathways in fetal sheep. Endocrinology 131: 1751-1756, 1992.
51. Zhang L. Prenatal hypoxia and cardiac programming. J Soc Gynecol Investig 12: 2-13, 2005.