IGF signaling directs ventricular cardiomyocyte proliferation during embryonic heart development

Development

Volumn 138, Issue 9, 2011, Pages 1795-1805

  Li, Peng ^a   Cavallero, Susana ^a   Gu, Ying ^a   Chen, Tim H P ^a   Hughes, Jennifer ^b   Hassan, A Bassim ^b   Brüning, Jens C ^c,d,e   Pashmforoush, Mohammad ^a   Sucov, Henry M ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Cardiomyocyte proliferation; Compact zone; Insulin like growth factor; Mouse; Ventricular chamber

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; RNA; SOMATOMEDIN B;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EPICARDIUM; GENE DISRUPTION; GENE EXPRESSION; GENE REPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; HYPOPLASIA; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VENTRICULAR CARDIOMYOCYTE; WESTERN BLOTTING;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEART; HEART VENTRICLES; INSULIN-LIKE GROWTH FACTOR II; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; MYOCARDIUM; MYOCYTES, CARDIAC; RECEPTOR, IGF TYPE 2; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 79955424835     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.054338     Document Type: Article

References (66)

1. Armstrong, M. T., Lee, D. Y. and Armstrong, P. B. (2000). Regulation of proliferation of the fetal myocardium. Dev. Dyn. 219, 226-236.
2. Austin, A. F., Compton, L. A., Love, J. D., Brown, C. B. and Barnett, J. V. (2008). Primary and immortalized mouse epicardial cells undergo differentiation in response to TGFbeta. Dev. Dyn. 237, 366-376.
3. Baker, J., Liu, J. P., Robertson, E. J. and Efstratiadis, A. (1993). Role of insulinlike growth factors in embryonic and postnatal growth. Cell 75, 73-82.
4. Belke, D. D., Betuing, S., Tuttle, M. J., Graveleau, C., Young, M. E., Pham, M., Zhang, D., Cooksey, R. C., McClain, D. A., Litwin, S. E. et al. (2002). Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J. Clin. Invest. 109, 629-639.
5. Bondy, C. A., Werner, H., Roberts, C. T. and LeRoith, D. (1990). Cellular pattern of insulin-like growth factor-I (IGF-I) and type I IGF receptor gene expression in early organogenesis: comparison with IGF-II gene expression. Mol. Endocrinol. 4, 1386-1398.
6. Brade, T., Kumar, S., Cunningham, T. J., Chatzi, C., Zhao, X., Cavallero, S., Li, P., Sucov, H. M., Ruiz-Lozano, P. and Duester, G. (2011). Retinoic acid stimulates myocardial expansion by induction of hepatic erythropoietin which activates epicardial Igf2. Development 138, 139-148.
7. Bushdid, P. B., Osinska, H., Waclaw, R. R., Molkentin, J. D. and Yutzey, K. E. (2003). NFATc3 and NFATc4 are required for cardiac development and mitochondrial function. Circ. Res. 92, 1305-1313.
8. Chen, J., Kubalak, S. W. and Chien, K. R. (1998). Ventricular muscle-restricted targeting of the RXRalpha gene reveals a non-cell-autonomous requirement in cardiac chamber morphogenesis. Development 125, 1943-1949.
9. Chen, T. H., Chang, T. C., Kang, J. O., Choudhary, B., Makita, T., Tran, C. M., Burch, J. B., Eid, H. and Sucov, H. M. (2002). Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor. Dev. Biol. 250, 198-207.
10. Corson, L. B., Yamanaka, Y., Lai, K. M. and Rossant, J. (2003). Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130, 4527-4537.
11. DeChiara, T. M., Efstratiadis, A. and Robertson, E. J. (1990). A growthdeficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345, 78-80.
12. DeChiara, T. M., Robertson, E. J. and Efstratiadis, A. (1991). Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849-859.
13. Dokic, D. and Dettman, R. W. (2006). VCAM-1 inhibits TGFbeta stimulated epithelial-mesenchymal transformation by modulating Rho activity and stabilizing intercellular adhesion in epicardial mesothelial cells. Dev. Biol. 299, 489-504.
14. Dupont, J. and Holzenberger, M. (2003). Biology of insulin-like growth factors in development. Birth Defects Res. C Embryo Today 69, 257-271.
15. Eggenschwiler, J., Ludwig, T., Fisher, P., Leighton, P. A., Tilghman, S. M. and Efstratiadis, A. (1997). Mouse mutant embryos overexpressing IGF-II exhibit phenotypic features of the Beckwith-Wiedemann and Simpson-Golabi-Behmel syndromes. Genes Dev. 11, 3128-3142.
16. Fraidenraich, D., Stillwell, E., Romero, E., Wilkes, D., Manova, K., Basson, C. T. and Benezra, R. (2004). Rescue of cardiac defects in id knockout embryos by injection of embryonic stem cells. Science 306, 247-252.
17. Gittenberger-de Groot, A. C., Vrancken Peeters, M. P., Bergwerff, M., Mentink, M. M. and Poelmann, R. E. (2000). Epicardial outgrowth inhibition leads to compensatory mesothelial outflow tract collar and abnormal cardiac septation and coronary formation. Circ. Res. 87, 969-971.
18. Gowan, L. K., Hampton, B., Hill, D. J., Schlueter, R. J. and Perdue, J. F. (1987). Purification and characterization of a unique high molecular weight form of insulin-like growth factor II. Endocrinology 121, 449-458.
19. Hakim, Z. S., DiMichele, L. A., Doherty, J. T., Homeister, J. W., Beggs, H. E., Reichardt, L. F., Schwartz, R. J., Brackhan, J., Smithies, O., Mack, C. P. et al. (2007). Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol. Cell. Biol. 27, 5352-5364.
20. He, T. C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W. and Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95, 2509-2514.
21. Hertig, C. M., Kubalak, S. W., Wang, Y. and Chien, K. R. (1999). Synergistic roles of neuregulin-1 and insulin-like growth factor-I in activation of the phosphatidylinositol 3-kinase pathway and cardiac chamber morphogenesis. J. Biol. Chem. 274, 37362-37369.
22. Ieda, M., Tsuchihashi, T., Ivey, K. N., Ross, R. S., Hong, T. T., Shaw, R. M. and Srivastava, D. (2009). Cardiac fibroblasts regulate myocardial proliferation through beta1 integrin signaling. Dev. Cell 16, 233-244.
23. Kang, J. O. and Sucov, H. M. (2005). Convergent proliferative response and divergent morphogenic pathways induced by epicardial and endocardial signaling in fetal heart development. Mech. Dev. 122, 57-65.
24. Kang, J., Gu, Y., Li, P., Johnson, B. L., Sucov, H. M. and Thomas, P. S. (2008). PDGF-A as an epicardial mitogen during heart development. Dev. Dyn. 237, 692-701.
25. Kastner, P., Grondona, J. M., Mark, M., Gansmuller, A., LeMeur, M., Decimo, D., Vonesch, J. L., Dolle, P. and Chambon, P. (1994). Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78, 987-1003.
26. Kastner, P., Messaddeq, N., Mark, M., Wendling, O., Grondona, J. M., Ward, S., Ghyselinck, N. and Chambon, P. (1997). Vitamin A deficiency and mutations of RXRalpha, RXRbeta and RARalpha lead to early differentiation of embryonic ventricular cardiomyocytes. Development 124, 4749-4758.
27. Kim, J., Wende, A. R., Sena, S., Theobald, H. A., Soto, J., Sloan, C., Wayment, B. E., Litwin, S. E., Holzenberger, M., LeRoith, D. et al. (2008). Insulin-like growth factor I receptor signaling is required for exercise-induced cardiac hypertrophy. Mol. Endocrinol. 22, 2531-2543.
28. Kim, J. K., Michael, M. D., Previs, S. F., Peroni, O. D., Mauvais-Jarvis, F., Neschen, S., Kahn, B. B., Kahn, C. R. and Shulman, G. I. (2000). Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J. Clin. Invest. 105, 1791-1797.
29. Kwee, L., Baldwin, H. S., Shen, H. M., Stewart, C. L., Buck, C., Buck, C. A. and Labow, M. A. (1995). Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121, 489-503.
30. Lau, M. M., Stewart, C. E., Liu, Z., Bhatt, H., Rotwein, P. and Stewart, C. L. (1994). Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev. 8, 2953-2963.
31. Laustsen, P. G., Russell, S. J., Cui, L., Entingh-Pearsall, A., Holzenberger, M., Liao, R. and Kahn, C. R. (2007). Essential role of insulin and insulin-like growth factor 1 receptor signaling in cardiac development and function. Mol. Cell. Biol. 27, 1649-1664.
32. Lavine, K. J., Yu, K., White, A. C., Zhang, X., Smith, C., Partanen, J. and Ornitz, D. M. (2005). Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 8, 85-95.
33. Lavine, K. J., White, A. C., Park, C., Smith, C. S., Choi, K., Long, F., Hui, C. C. and Ornitz, D. M. (2006). Fibroblast growth factor signals regulate a wave of Hedgehog activation that is essential for coronary vascular development. Genes Dev. 20, 1651-1666.
34. Lavine, K. J., Schmid, G. J., Smith, C. S. and Ornitz, D. M. (2008). Novel tool to suppress cell proliferation in vivo demonstrates that myocardial and coronary vascular growth represent distinct developmental programs. Dev. Dyn. 237, 713-724.
35. Liu, Q., Yan, H., Dawes, N. J., Mottino, G. A., Frank, J. S. and Zhu, H. (1996). Insulin-like growth factor II induces DNA synthesis in fetal ventricular myocytes in vitro. Circ. Res. 79, 716-726.
36. Louvi, A., Accili, D. and Efstratiadis, A. (1997). Growth-promoting interaction of IGF-II with the insulin receptor during mouse embryonic development. Dev. Biol. 189, 33-48.
37. Lu, S. Y., Sheikh, F., Sheppard, P. C., Fresnoza, A., Duckworth, M. L., Detillieux, K. A. and Cattini, P. A. (2008). FGF-16 is required for embryonic heart development. Biochem. Biophys. Res. Commun. 373, 270-274.
38. Makita, T., Hernandez-Hoyos, G., Chen, T. H., Wu, H., Rothenberg, E. V. and Sucov, H. M. (2001). A developmental transition in definitive erythropoiesis: erythropoietin expression is sequentially regulated by retinoic acid receptors and HNF4. Genes Dev. 15, 889-901.
39. Manner, J. (1993). Experimental study on the formation of the epicardium in chick embryos. Anat. Embryol. (Berl.) 187, 281-289.
40. Manner, J., Schlueter, J. and Brand, T. (2005). Experimental analyses of the function of the proepicardium using a new microsurgical procedure to induce loss-of-proepicardial-function in chick embryos. Dev. Dyn. 233, 1454-1463.
41. Martinez-Estrada, O. M., Lettice, L. A., Essafi, A., Guadix, J. A., Slight, J., Velecela, V., Hall, E., Reichmann, J., Devenney, P. S., Hohenstein, P. et al. (2010). Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat. Genet. 42, 89-93.
42. Mellgren, A. M., Smith, C. L., Olsen, G. S., Eskiocak, B., Zhou, B., Kazi, M. N., Ruiz, F. R., Pu, W. T. and Tallquist, M. D. (2008). Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 103, 1393-1401.
43. Moses, K. A., DeMayo, F., Braun, R. M., Reecy, J. L. and Schwartz, R. J. (2001). Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31, 176-180.
44. Murrell, A., Heeson, S., Bowden, L., Constancia, M., Dean, W., Kelsey, G. and Reik, W. (2001). An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep. 2, 1101-1106.
45. Nanka, O., Krizova, P., Fikrle, M., Tuma, M., Blaha, M., Grim, M. and Sedmera, D. (2008). Abnormal myocardial and coronary vasculature development in experimental hypoxia. Anat. Rec. (Hoboken) 291, 1187-1199.
46. Ohmichi, M., Pang, L., Ribon, V., Gazit, A., Levitzki, A. and Saltiel, A. R. (1993). The tyrosine kinase inhibitor tyrphostin blocks the cellular actions of nerve growth factor. Biochemistry 32, 4650-4658.
47. Parrizas, M., Gazit, A., Levitzki, A., Wertheimer, E. and LeRoith, D. (1997). Specific inhibition of insulin-like growth factor-1 and insulin receptor tyrosine kinase activity and biological function by tyrphostins. Endocrinology 138, 1427-1433.
48. Peng, X., Wu, X., Druso, J. E., Wei, H., Park, A. Y., Kraus, M. S., Alcaraz, A., Chen, J., Chien, S., Cerione, R. A. et al. (2008). Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc. Natl. Acad. Sci. USA 105, 6638-6643.
49. Pennisi, D. J., Ballard, V. L. and Mikawa, T. (2003). Epicardium is required for the full rate of myocyte proliferation and levels of expression of myocyte mitogenic factors FGF2 and its receptor, FGFR-1, but not for transmural myocardial patterning in the embryonic chick heart. Dev. Dyn. 228, 161-172.
50. Perez-Pomares, J. M., Phelps, A., Sedmerova, M., Carmona, R., Gonzalez-Iriarte, M., Munoz-Chapuli, R. and Wessels, A. (2002). Experimental studies on the spatiotemporal expression of WT1 and RALDH2 in the embryonic avian heart: a model for the regulation of myocardial and valvuloseptal development by epicardially derived cells (EPDCs). Dev. Biol. 247, 307-326.
51. Powell-Braxton, L., Hollingshead, P., Warburton, C., Dowd, M., Pitts-Meek, S., Dalton, D., Gillett, N. and Stewart, T. A. (1993). IGF-I is required for normal embryonic growth in mice. Genes Dev. 7, 2609-2617.
52. Qin, X. F., An, D. S., Chen, I. S. and Baltimore, D. (2003). Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc. Natl. Acad. Sci. USA 100, 183-188.
53. Sedmera, D. and Thomas, P. S. (1996). Trabeculation in the embryonic heart. BioEssays 18, 607.
54. Sengbusch, J. K., He, W., Pinco, K. A. and Yang, J. T. (2002). Dual functions of [alpha]4[beta]1 integrin in epicardial development: initial migration and longterm attachment. J. Cell Biol. 157, 873-882.
55. Shai, S. Y., Harpf, A. E., Babbitt, C. J., Jordan, M. C., Fishbein, M. C., Chen, J., Omura, M., Leil, T. A., Becker, K. D., Jiang, M. et al. (2002). Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 90, 458-464.
56. Stachelscheid, H., Ibrahim, H., Koch, L., Schmitz, A., Tscharntke, M., Wunderlich, F. T., Scott, J., Michels, C., Wickenhauser, C., Haase, I. et al. (2008). Epidermal insulin/IGF-1 signalling control interfollicular morphogenesis and proliferative potential through Rac activation. EMBO J. 27, 2091-2101.
57. Stuckmann, I., Evans, S. and Lassar, A. B. (2003). Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol. 255, 334-349.
58. Stylianopoulou, F., Efstratiadis, A., Herbert, J. and Pintar, J. (1988). Pattern of the insulin-like growth factor II gene expression during rat embryogenesis. Development 103, 497-506.
59. Sucov, H. M., Dyson, E., Gumeringer, C. L., Price, J., Chien, K. R. and Evans, R. M. (1994). RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev. 8, 1007-1018.
60. Sucov, H. M., Gu, Y., Thomas, S., Li, P. and Pashmforoush, M. (2009). Epicardial control of myocardial proliferation and morphogenesis. Pediatr. Cardiol. 30, 617-625.
61. Sun, Y., Gao, D., Liu, Y., Huang, J., Lessnick, S. and Tanaka, S. (2006). IGF2 is critical for tumorigenesis by synovial sarcoma oncoprotein SYT-SSX1. Oncogene 25, 1042-1052.
62. Viragh, S. and Challice, C. E. (1981). The origin of the epicardium and the embryonic myocardial circulation in the mouse. Anat. Rec. 201, 157-168.
63. Wang, Z. Q., Fung, M. R., Barlow, D. P. and Wagner, E. F. (1994). Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372, 464-467.
64. Wu, H., Lee, S. H., Gao, J., Liu, X. and Iruela-Arispe, M. L. (1999). Inactivation of erythropoietin leads to defects in cardiac morphogenesis. Development 126, 3597-3605.
65. Zamora, M., Manner, J. and Ruiz-Lozano, P. (2007). Epicardium-derived progenitor cells require beta-catenin for coronary artery formation. Proc. Natl. Acad. Sci. USA 104, 18109-18114.
66. Zapf, J., Futo, E., Peter, M. and Froesch, E. R. (1992). Can "big" insulin-like growth factor II in serum of tumor patients account for the development of extrapancreatic tumor hypoglycemia? J. Clin. Invest. 90, 2574-2584.