Circulation Research. 2002;90:1044-1054
doi: 10.1161/01.RES.0000020201.44772.67
doi: 10.1161/01.RES.0000020201.44772.67
© 2002 American Heart Association, Inc.
Reviews |
Cardiomyocyte Cell Cycle Regulation
From the Wells Center for Pediatric Research and Krannert Institute of Cardiology, Indiana University School of Medicine, Indianapolis, Ind.
Correspondence to Loren J. Field, Herman B Wells Center for Pediatric Research, James Whitcomb Riley Hospital for Children, 702 Barnhill Dr, Room 2600, Indianapolis, IN 46202-5225. E-Mail ljfield{at}iupui.edu
Although rapid progress is being made in many areas of molecular cardiology, issues pertaining to the origins of heart-forming cells, the mechanisms responsible for cardiogenic induction, and the pathways that regulate cardiomyocyte proliferation during embryonic and adult life remain unanswered. In the present study, we review approaches and studies that have shed some light on cardiomyocyte cell cycle regulation. For reference, an initial description of cardiomyogenic induction and morphogenesis is provided, which is followed by a summary of published cell cycle analyses during these stages of cardiac ontology. A review of studies examining cardiomyocyte cell cycle analysis and de novo cardiomyogenic induction in the adult heart is then presented. Finally, studies in which cardiomyocyte cell cycle activity was experimentally manipulated in vitro and in vivo are reviewed. It is hoped that this compilation will serve to stimulate thought and experimentation in this intriguing area of cardiomyocyte cell biology.
Key Words: cardiomyocyte proliferation • cardiac myocyte apoptosis • heart regeneration • gene targeting • transgenic mice
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|
|
|
|
|
|
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|
|
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|
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|
|
|
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|
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|
|
|
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|
|
|
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|
|
|
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|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
M. Tamamori-Adachi, K. Hayashida, K. Nobori, C. Omizu, K. Yamada, N. Sakamoto, T. Kamura, K. Fukuda, S. Ogawa, K. I. Nakayama, et al. Down-regulation of p27Kip1 Promotes Cell Proliferation of Rat Neonatal Cardiomyocytes Induced by Nuclear Expression of Cyclin D1 and CDK4: EVIDENCE FOR IMPAIRED Skp2-DEPENDENT DEGRADATION OF p27 IN TERMINAL DIFFERENTIATION J. Biol. Chem., November 26, 2004; 279(48): 50429 - 50436. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
 |
|
 S. H. Ali, J. S. Kasper, T. Arai, and J. A. DeCaprio Cul7/p185/p193 Binding to Simian Virus 40 Large T Antigen Has a Role in Cellular Transformation J. Virol., March 15, 2004; 78(6): 2749 - 2757. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. A. Kulkarni, M. Sano, and M. D. Schneider Phosphorylation of RNA Polymerase II in Cardiac Hypertrophy: Cell Enlargement Signals Converge on Cyclin T/Cdk9 Recent Prog. Horm. Res., January 1, 2004; 59(1): 125 - 139. [Abstract] [Full Text]
|
|
|
|
|
|
M. Snir, I. Kehat, A. Gepstein, R. Coleman, J. Itskovitz-Eldor, E. Livne, and L. Gepstein Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes Am J Physiol Heart Circ Physiol, December 1, 2003; 285(6): H2355 - H2363. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. N. Olson and M. D. Schneider Sizing up the heart: development redux in disease Genes & Dev., August 15, 2003; 17(16): 1937 - 1956. [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
B. Nadal-Ginard, J. Kajstura, A. Leri, and P. Anversa Myocyte Death, Growth, and Regeneration in Cardiac Hypertrophy and Failure Circ. Res., February 7, 2003; 92(2): 139 - 150. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
 |
|
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|
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