Cardiomyocytes re-enter the cell cycle and contribute to heart development after differentiation from cardiac progenitors expressing Isl1 in chick embryo

Development Growth and Differentiation

Volumn 49, Issue 3, 2007, Pages 229-239

  Hayashi, Shinichi ^a   Inoue, Akio ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Cardiac progenitor; Cardiomyocyte; Differentiation; Isl1; Proliferation

Indexed keywords

BROXURIDINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL CYCLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CELL STRUCTURE; CHICK; CHROMOSOME; CONTROLLED STUDY; CYTOPLASM; DNA REPLICATION; EMBRYO; HEART CONTRACTION; HEART DEVELOPMENT; HEART MUSCLE CELL; IN VITRO STUDY; NONHUMAN; SARCOMERE; STEM CELL;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CHICK EMBRYO; DNA; HEART; HOMEODOMAIN PROTEINS; MITOSIS; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; ORGANOGENESIS; STEM CELLS;

EID: 33947386737     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2007.00923.x     Document Type: Article

References (66)

1. Armstrong, M. T., Lee, D. Y. & Armstrong, P. B. 2000. Regulation of proliferation of the fetal myocardium. Dev. Dyn. 219, 226-236.
2. Busk, P. K., Hinrichsen, R., Bartkova, J. et al. 2005. Cyclin D2 induces proliferation of cardiac myocytes and represses hypertrophy. Exp. Cell Res. 304, 149-161.
3. Cai, C. L., Liang, X., Shi, Y. et al. 2003. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5, 877-889.
4. Chang, C. P., Neilson, J. R., Bayle, J. H. et al. 2004. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis. Cell 118, 649-663.
5. Chaudhry, H. W., Dashoush, N. H., Tang, H. et al. 2004. Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J. Biol. Chem. 279, 35858-35866.
6. Collins, C. A., Olsen, I., Zammit, P. S. et al. 2005. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122, 289-301.
7. Davidson, B., Shi, W., Beh, J., Christiaen, L. & Levine, M. 2006. FGF signaling delineates the cardiac progenitor field in the simple chordate, Ciona intestinalis. Gene Dev. 20, 2728-2738.
8. Dodou, E., Verzi, M. P., Anderson, J. P., Xu, S. M. & Black, B. L. 2004. Mef2c is a direct transcriptional target of ISL1 and GATA factors in the anterior heart field during mouse embryonic development. Development 131, 3931-3942.
9. Ebelt, H., Hufnagel, N., Neuhaus, P. et al. 2005. Divergent siblings: E2F2 and E2F4 but not E2F1 and E2F3 induce DNA synthesis in cardiomyocytes without activation of apoptosis. Circ. Res. 96, 509-517.
10. Engel, F. B., Schebesta, M., Duong, M. T. et al. 2005. p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev. 19, 1175-1187.
11. Epstein, J., Li, J., Lang, D. et al. 2000. Migration of cardiac neural crest cells in splotch embryos. Development 127, 1869-1878.
12. Ericson, J., Thor, S., Edlund, T., Jessell, T. M. & Yamada, T. 1992. Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
13. Flink, I. L. 2002. Cell cycle reentry of ventricular and atrial cardiomyocytes and cells within the epicardium following amputation of the ventricular apex in the axolotl, Amblystoma mexicanum: confocal microscopic immunofluorescent image analysis of bromodeoxyuridine-labeled nuclei. Anat. Embryol. 205, 235-244.
14. Forouhar, A. S., Liebling, M., Hickerson, A. et al. 2006. The embryonic vertebrate heart tube is a dynamic suction pump. Science 312, 751-753.
15. Hamburger, V. & Hamilton, H. L. 1951. A series of normal stages in the development of the chick embryo. J. Morph. 88, 49-92.
16. van den Hoff, M. J. B., Kruithof, B. P. T. & Moorman, A. F. M. 2004. Making more heart muscle. Bioessays 26, 248-261.
17. van den Hoff, M. J. B., Moorman, A. F. M., Ruijter, J. M. et al. 1999. Myocardialization of the cardiac outflow tract. Dev. Biol. 212, 477-490.
18. Jung, J., Kim, T. G., Lyons, G. E., Kim, H. R. C. & Lee, Y. 2005. Jumonji regulates cardiomyocyte proliferation via interaction with retinoblastoma protein. J. Biol. Chem. 280, 30916-30923.
19. Kelly, R. G., Brown, N. A. & Buckingham, M. E. 2001. The arterial pole of the mouse heart forms from fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1, 435-440.
20. Kelly, A. M. & Chacko, S. 1976. Myofibril organisation and mitosis in cultured cardiac muscle cells. Dev. Biol. 48, 421-430.
21. Kim, C. F. B., Jackson, E. L., Woolfenden, A. E. et al. 2005. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121, 823-835.
22. Laugwitz, K. L., Moretti, A., Lam, J. et al. 2005. Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433, 647-653.
23. Lavine, K., J. Yu, K. White, A. C. et al. 2005. Endocardial and epicardial derived FGF signals regulate myocardial proliferation and differentiation in vivo. Dev. Cell 8, 85-95.
24. Ledda-Columbano, G. M., Molotzu, F., Pibiri, M., Cossu, C., Perra, A. & Columbano, A. 2006. Thyroid hormone induces cyclin D1 nuclear translocation and DNA synthesis in adult rat cardiomyocytes. FASEB J. 20, 87-94.
25. Lin, Q., Schwarz, J., Bucana, C. & Olson, E. N. 1997. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science 276, 1404-1407.
26. Liu, S., Liu, F., Schneider, A. E., St. Amand, T., Epstein, J. A. & Gutstein, D. E. 2006. Distinct cardiac malformations caused by absence of connexin 43 in the neural crest and in the non-crest neural tube. Development 133, 2063-2073.
27. Martinsen, B. J. 2005. Reference guide to the stages of chick heart embryology. Dev. Dyn. 233, 1217-1237.
28. Mjaatvedt. C. H., Nakaoka, T., Moreno-Rodriguez, R. et al. 2001. The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol. 238, 97-109.
29. Monzen, K., Hiroi, Y., Kudoh, S. et al. 2001. Smad, TAK1, and their common target ATF-2 play a critical role in cardiomyocytes differentiation. J. Cell Biol. 153, 687-698.
30. Moreno-Rodriguez, R. A., Krug, E. L., Reyes, L., Villavicencio, L., Mjaatvedt, C. H. & Markwald, R. R. 2006. Bidirectional fusion of the heart-forming fields in the developing chick embryo. Dev. Dyn. 235, 191-202.
31. Nonaka, S., Shiratori, H., Saijoh, Y. & Hamada, H. 2002. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99.
32. Parisi, S., D'Andrea, D., Lago, C. T., Adamson, E. D., Persico, M. G. & Minchiotti, G. 2003. Nodal-dependent Cripto signaling promotes cardiomyogenesis and redirects the neural fate of embryonic stem cells. J. Cell Biol. 163, 303-314.
33. Park, E. J., Ogaden, L. A., Talbot, A. et al. 2006. Required, tissue-specific roles for fgf8 in outflow tract formation and remodeling. Development 133, 2419-2433.
34. Pasumarthi, K. B. S. & Field, L. J. 2002. Cardiomyocyte cell cycle regulation. Circ. Res. 90, 1044-1054.
35. Pasumarthi, K. B. S., Nakajima, H., Nakajima, H. O., Soonpaa, M. H. & Field, L. J. 2005. Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ. Res. 96, 110-118.
36. Pennisi, D. J., Ballard, V. L. T. & 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.
37. Perez-Pomares, J. M., Phelps, A., Sedmerova, M. et al. 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.
38. Portiansky, E. L., Barbeito, C. G., Gimeno, E. J., Zuccolilli, G. O. & Goya, R. G. 2006. Loss of NeuN immunoreactivity in rat spinal cord neurons during aging. Exp. Neurol. 202, 519-521.
39. Poss, K. D., Wilson, L. G. & Keating, M. T. 2002. Heart regeneration in zebrafish. Science 298, 2188-2190.
40. Ramsdell, A. F. 2005. Left-right asymmetry and congenital cardiac defects: getting to the heart of the matter in vertebrate left-right axis determination. Dev. Biol. 288, 1-20.
41. Relaix, F., Rocancourt, D., Mansouri, A. & Buckingham, M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953.
42. Rhee, H., Polak, L. & Fuchs, E. 2006. Lhx2 maintains stem cell character in hair follicles. Science 312, 1946-1949.
43. Rhodes, K. E., Moon, L. D. F. & Fawcett, J. W. 2003. Inhibiting cell proliferation during formation of the glial scar: effects on axon regeneration in the CNS. Neuroscience 120, 41-56.
44. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. & Inoue, T. 1999. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126, 3437-3447.
45. Sakabe, M., Matsui, H., Sakata, H., Ando, K., Yamagishi, T. & Nakajima, Y. 2005. Understanding heart development and congenital heart defects through developmental biology: a segmental approach. Congenit. Anom. (Kyoto) 45, 107-118.
46. Satou, Y., Imai, K. S. & Satou, N. 2004. The ascidian Mesp gene specifies heart precursor cells. Development 131, 2533-2541.
47. Schultheiss, T., Xydas, S. & Lassar, A. 1995. Induction of avian cardiac myogenesis by anterior endoderm. Development 121, 4203-4214.
48. Sheikh, F., Fandrich, R. R., Kardami, E. & Cattini, P. A. 1999. Overexpression of long or short FGFR-1 results in FGF-2-mediated proliferation in neonatal cardiac myocyte cultures. Cardiovasc. Res. 42, 696-705.
49. Shen, Q., Goderie, S. K., Jin, L. et al. 2004. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340.
50. Shiratori, H., Yashiro, K., Shen, M. M. & Hamada, H. 2006. Conserved regulation and role of Pitx2 in situs-specific morphogenesis of visceral organs. Development 133, 3015-3025.
51. Soonpaa, M. H., Kim, K. K., Pajak, L., Franklin, M. & Field, L. J. 1996. Cardiomyocyte DNA synthesis and binucleation during murine development. Am. J. Physiol. 271, H2183-H2189.
52. Soufan, A. T., van den Berg, G., Ruijter, J. M., de Boer, P. A. J., van den Hoff, M. J. B. & Moorman, A. F. M. 2006. Regionalized sequence of myocardial cell growth and proliferation characterizes early chamber formation. Circ. Res. 99, 545-552.
53. Stuckmann, I., Evans, S. & Lassar, A. B. 2003. Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation. Dev. Biol. 255, 334-349.
54. Takeuchi, J. K., Mileikovskaia, M., Koshiba-Takeuchi, K. et al. 2005. Tbx20 dose-dependently regulates transcription factor networks required for mouse heart and motoneuron development. Development 132, 2463-2474.
55. Tamamori-Adachi, M., Hayashida, K., Nobori, K. et al. 2004. Down-regulation of p27Kip1 promotes cell proliferation of rat neonatal cardiomyocytes induced by nuclear expression of Cyclin D1 and CDK4: evidence for impaired Skp2-development degradation of p27 in terminal differentiation. J. Biol. Chem. 279, 50429-50436.
56. Tamamori-Adachi, M., Ito, H., Sumrejkanchanakij, P. et al. 2003. Critical role of cyclin D1 nuclear import in cardiomyocyte proliferation. Circ. Res. 92, 12e-19.
57. Tamaoki, M., Imanaka-Yoshida, K., Yokoyama, K. et al. 2005. Tenascin-C regulates recruitment of myofibroblasts during tissue repair after myocardial injury. Am. J. Pathol. 167, 71-80.
58. Thaler, J. P., Koo, S. J., Kania, A. et al. 2004. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41, 337-350.
59. Tirosh-Finkel, L., Elhanany, H., Rinon, A. & Tzahor, E. 2006. Mesoderm progenitor cells of common origin contribute to the head musculature and the cardiac outflow tract. Development 133, 1943-1953.
60. Vong, L., Bi, W., O'Connor-Halligan, K. E., Li, C., Cserjesi, P. & Schwarz, J. J. 2006. MEF2C is required for the normal allocation of cells between the ventricular and sinoatrial precursors of the primary heart field. Dev. Dyn. 235, 1809-1821.
61. Waldo, K. L., Hutson, M. R., Stadt, H. A., Zdanowicz, M., Zdanowicz, J. & Kirby, M. L. 2005a. Cardiac neural crest is necessary for normal addition of the myocardium to the arterial pole from the secondary heart field. Dev. Biol. 281, 66-77.
62. Waldo, K. L., Hutson, M. R., Ward, C. C. et al. 2005b. Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev. Biol. 281, 78-90.
63. Waldo, K. L., Kumiski, D. H., Wallis, K. T. et al. 2001. Conotruncal myocardium arises from a secondary heart field. Development 128, 3179-3188.
64. Xin, M., Davis, C. A., Molkentin, J. D. et al. 2006. A threshold of GATA4 and GATA6 expression is required for cardiovascular development. Proc. Natl. Acad. Sci. USA 103, 11189-11194.
65. Zaffran, S., Kelly, R. G., Meilhac, S. M., Buckingham, M. E. & Brown, N. A. 2004. Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95, 261-268.
66. Zeisberg, E. M., Ma, Q., Juraszek, A. L. et al. 2005. Morphogenesis of the right ventricle requires myocardial expression of Gata4. J. Clin. Invest. 115, 1522-1531.