Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 285, Issue 6 54-6, 2003, Pages

  Sundgren, Nathan C ^a   Giraud, George D ^a   Schultz, Jess M ^b   Lasarev, Michael R ^a   Stork, Philip J S ^a   Thornburg, Kent L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Hyperplasia; Hypertrophy; LY 294002; UO 126

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BROXURIDINE; INOSITOL PHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE 1; PHENYLEPHRINE; PHOSPHOTRANSFERASE INHIBITOR; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UO 126;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CELL SIZE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; DRUG EFFECT; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FETUS; HEART DEVELOPMENT; HEART HYPERTROPHY; HEART MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STIMULATION;

EID: 0345283345     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00232.2003     Document Type: Article

References (50)

1. Baker J, Liu JP, Robertson EJ, and Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75: 73-82, 1993.
2. Barbera A, Giraud GD, Reller MD, Maylie J, Morton MJ, and Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 279: R1157-R1164, 2000.
3. Barker DJ, Osmond C, and Law CM. The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Community Health 43: 237-240, 1989.
4. Baserga R and Rubin R. Cell cycle and growth control. Crit Rev Eukaryot Gene Expr 3: 47-61, 1993.
5. Condorelli G, Drusco A, Stassi G, Bellacosa A, Roncarati R, Iaccarino G, Russo MA, Gu Y, Dalton N, Chung C, Latronico MV, Napoli C, Sadoshima J, Croce CM, and Ross J Jr. Akt induces enhanced myocardial contractility and cell size in vivo in transgenic mice. Proc Natl Acad Sci USA 99: 12333-12338, 2002.
6. Coolican SA, Samuel DS, Ewton DZ, McWade FJ, and Florini JR. The mitogenic and myogenic actions of insulin-like growth factors utilize distinct signaling pathways. J Biol Chem 272: 6653-6662, 1997.
7. Crackower MA, Oudit GY, Kozieradzki I, Sarao R, Sun H, Sasaki T, Hirsch E, Suzuki A, Shioi T, Irie-Sasaki J, Sah R, Cheng HY, Rybin VO, Lembo G, Fratta L, Oliveira-dos-Santos AJ, Benovic JL, Kahn CR, Izumo S, Steinberg SF, Wymann MP, Backx PH, and Penninger JM. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 110: 737-749, 2002.
8. Delafontaine P. Insulin-like growth factor I and its binding proteins in the cardiovascular system. Cardiovasc Res 30: 825-834, 1995.
9. Han VK and Hill DJ. Growth factors in fetal growth. In: Textbook of Fetal Physiology, edited by Thorburn GD and Harding R. New York: Oxford Univ. Press, 1994, p. 48-69.
10. Harding J. The nutritional basis of the fetal origins of adult disease. Int J Epidemiol 30: 15-23, 2001.
11. He S, Cook BL, Deverman BE, Weihe U, Zhang F, Prachand V, Zheng J, and Weintraub SJ. E2F is required to prevent inappropriate S-phase entry of mammalian cells. Mol Cell Biol 20: 363-371, 2000.
12. Holm S. A simple sequentially rejective multiple test procedure. Scand J Stat 6: 65-70, 1979.
13. Hong F, Kwon SJ, Jhun BS, Kim SS, Ha J, Kim SJ, Sohn NW, Kang C, and Kang I. Insulin-like growth factor-1 protects H9c2 cardiac myoblasts from oxidative stress-induced apoptosis via phosphatidylinositol 3-kinase and extracellular signal-regulated kinase pathways. Life Sci 68: 1095-1105, 2001.
14. Ihaka R and Gentleman R. R: a language for data analysis and graphics. J Comput Graph Stat 5: 229-314, 1999.
15. Ito H, Hiroe M, Hirata Y, Tsujino M, Adachi S, Shichiri M, Koike A, Nogami A, and Marumo F. Insulin-like growth factor-I induces hypertrophy with enhanced expression of muscle specific genes in cultured rat cardiomyocytes. Circulation 87: 1715-1721, 1993.
16. Kajstura J, Cheng W, Reiss K, and Anversa P. The IGF-1-IGF-1 receptor system modulates myocyte proliferation but not myocyte cellular hypertrophy in vitro. Exp Cell Res 215: 273-283, 1994.
17. Kurihara S, Hakuno F, and Takahashi S. Insulin-like growth factor-I-dependent signal transduction pathways leading to the induction of cell growth and differentiation of human neuroblastoma cell line SH-SY5Y: the roles of MAP kinase pathway and PI 3-kinase pathway. Endocr J 47: 739-751, 2000.
18. Lavandero S, Foncea R, Perez V, and Sapag-Hagar M. Effect of inhibitors of signal transduction on IGF-1-induced protein synthesis associated with hypertrophy in cultured neonatal rat ventricular myocytes. FEBS Lett 422: 193-196, 1998.
19. Li F, Wang X, Bunger PC, and Gerdes AM. Formation of binucleated cardiac myocytes in rat heart. I. Role of actin-myosin contractile ring. J Mol Cell Cardiol 29: 1541-1551, 1997.
20. Li F, Wang X, and Gerdes AM. Formation of binucleated cardiac myocytes in rat heart. II. Cytoskeletal organisation. J Mol Cell Cardiol 29: 1553-1565, 1997.
21. Liu T, Lai H, Wu W, Chinn S, and Wang PH. Developing a strategy to define the effects of insulin-like growth factor-1 on gene expression profile in cardiomyocytes. Circ Res 88: 1231-1238, 2001.
22. Liu W, Liu Y, and Lowe JW Jr. The role of phosphatidylinositol 3-kinase and the mitogen-activated protein kinases in insulin-like growth factor-I-mediated effects in vascular endothelial cells. Endocrinology 142: 1710-1719, 2001.
23. Lok F, Owens JA, Mundy L, Robinson JS, and Owens PC. Insulin-like growth factor I promotes growth selectively in fetal sheep in late gestation. Am J Physiol Regul Integr Comp Physiol 270: R1148-R1155, 1996.
24. Marsh AC, Gibson KJ, Wu J, Owens PC, Owens JA, and Lumbers ER. Chronic effect of insulin-like growth factor I on renin synthesis, secretion, and renal function in fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R318-R326, 2001.
25. Mehrhof FB, Muller FU, Bergmann MW, Li P, Wang Y, Schmitz W, Dietz R, and von Harsdorf R. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositol-3-OH-kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation 104: 2088-2094, 2001.
26. Modesti PA, Vanni S, Bertolozzi I, Cecioni I, Polidori G, Paniccia R, Bandinelli B, Perna A, Liguori P, Boddi M, Galanti G, and Serneri GG. Early sequence of cardiac adaptations and growth factor formation in pressure- and volume-overload hypertrophy. Am J Physiol Heart Circ Physiol 279: H976-H985, 2000.
27. Moelling K, Schad K, Bosse M, Zimmermann S, and Schweneker M. Regulation of Raf-Akt cross-talk. J Biol Chem 277: 31099-31106, 2002.
28. Nadal-Ginard B, Kajstura J, Leri A, and Anversa P. Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ Res 92: 139-150, 2003.
29. Oliver MH, Harding JE, Breier BH, Evans PC, and Gluckman PD. Glucose but not a mixed amino acid infusion regulates plasma insulin-like growth factor-I concentrations in fetal sheep. Pediatr Res 34: 62-65, 1993.
30. Oliver MH, Harding JE, Breier BH, and 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.
31. Osgerby JC, Wathes DC, Howard D, and Gadd TS. The effect of maternal undernutrition on ovine fetal growth. J Endocrinol 173: 131-141, 2002.
32. Pardee AB. G1 events and regulation of cell proliferation. Science 246: 603-608, 1989.
33. Pene F, Claessens YE, Muller O, Viguie F, Mayeux P, Dreyfus F, Lacombe C, and Bouscary D. Role of the phosphatidylinositol 3-kinase/Akt and mTOR/P70S6-kinase pathways in the proliferation and apoptosis in multiple myeloma. Oncogene 21: 6587-6597, 2002.
34. Penheiro JC and Baudler S. Mixed-Effects Models in S and S-Plus. New York: Springer, 2000.
35. Quinn LS, Steinmetz B, Maas A, Ong L, and Kaleko M. Type-1 insulin-like growth factor receptor overexpression produces dual effects on myoblast proliferation and differentiation. J Cell Physiol 159: 387-398, 1994.
36. Reiss K, Cheng W, Ferber A, Kajstura J, Li P, Li B, Olivetti G, Homcy CJ, Baserga R, and Anversa P. Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice. Proc Natl Acad Sci USA 93: 8630-8635, 1996.
37. Rommel C, Clarke BA, Zimmermann S, Nunez L, Rossman R, Reid K, Moelling K, Yancopoulos GD, and Glass DJ. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science 286: 1738-1741, 1999.
38. Sadoshima J, Aoki H, and Izumo S. Angiotensin II and serum differentially regulate expression of cyclins, activity of cyclin-dependent kinases, and phosphorylation of retinoblastoma gene product in neonatal cardiac myocytes. Circ Res 80: 228-241, 1997.
39. Schoenfeld JR, Vasser M, Jhurani P, Ng P, Hunter JJ, Ross J Jr, Chien KR, and Lowe DG. Distinct molecular phenotypes in murine cardiac muscle development, growth, and hypertrophy. J Mol Cell Cardiol 30: 2269-2280, 1998.
40. Shioi T, Kang PM, Douglas PS, Hampe J, Yballe CM, Lawitts J, Cantley LC, and Izumo S. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J 19: 2537-2548, 2000.
41. Shioi T, McMullen JR, Kang PM, Douglas PS, Obata T, Franke TF, Cantley LC, and Izumo S. Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol 22: 2799-2809, 2002.
42. Smolich JJ, Walker AM, Campbell GR, and Adamson TM. Left and right ventricular myocardial morphometry in fetal, neonatal, and adult sheep. Am J Physiol Heart Circ Physiol 257: H1-H9, 1989.
43. Stewart CE, James PL, Fant ME, and Rotwein P. Overexpression of insulin-like growth factor-II induces accelerated myoblast differentiation. J Cell Physiol 169: 23-32, 1996.
44. Stewart CE and Rotwein P. Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol Rev 76: 1005-1026, 1996.
45. Sundgren NC, Giraud GD, Stork PJ, Maylie JG, and Thornburg KL. Angiotensin II stimulates hyperplasia but not hypertrophy in immature ovine cardiomyocytes. J Physiol 548: 881-891, 2003.
46. Thornburg KL and Morton MJ. Filling and arterial pressures as determinants of RV stroke volume in the sheep fetus. Am J Physiol Heart Circ Physiol 244: H656-H663, 1983.
47. Ueyama T, Kawashima S, Sakoda T, Rikitake Y, Ishida T, Kawai M, Yamashita T, Ishido S, Hotta H, and Yokoyama M. Requirement of activation of the extracellular signal-regulated kinase cascade in myocardial cell hypertrophy. J Mol Cell Cardiol 32: 947-960, 2000.
48. Yu CF, Liu ZX, and Cantley LG. ERK negatively regulates the epidermal growth factor-mediated interaction of Gab1 and the phosphatidylinositol 3-kinase. J Biol Chem 277: 19382-19388, 2002.
49. Yue TL, Gu JL, Wang C, Reith AD, Lee JC, Mirabile RC, Kreutz R, Wang Y, Maleeff B, Parsons AA, and Ohlstein EH. Extracellular signal-regulated kinase plays an essential role in hypertrophic agonists, endothelin-1 and phenylephrine-induced cardiomyocyte hypertrophy. J Biol Chem 275: 37895-37901, 2000.
50. Zimmermann S and Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science 286: 1741-1744, 1999.