Top

Published in:

01-07-2009 | Riley Symposium

Insights into the Characteristics of Mammalian Cardiomyocyte Terminal Differentiation Shown Through the Study of Mice with a Dysfunctional c-Kit

Authors: Nawazish Naqvi, Ming Li, Eiji Yahiro, Robert M. Graham, Ahsan Husain

Published in: Pediatric Cardiology | Issue 5/2009

Abstract

Mammalian cardiomyocytes withdraw from the cell cycle soon after birth. This process is called terminal differentiation. The c-kit, a receptor tyrosine kinase, is expressed on cardiomyocytes immediately after birth but for only a few days. In mice with genetic c-kit dysfunction, adult cardiomyocytes are phenotypically indistinguishable from those of wild type mice, except that they are capable of proliferation in vivo after acute pressure overload. This review explores the idea that postnatal cardiomyocyte differentiation and cell cycle withdrawal are distinct processes and that terminal differentiation may not simply be due to altered expression of genes that regulate the cell cycle but could involve c-kit induced epigenetic change.

Ahuja P, Sdek P, MacLellan WR (2007) Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 87:521–544PubMedCrossRef

Ausma J, Schaart G, Thoné F et al (1995) Chronic ischemic viable myocardium in man: aspects of dedifferentiation. Cardiovasc Pathol 4:29–37CrossRef

Chaudhry HW, Dashoush NH, Tang H et al (2004) Cyclin A2 mediates cardiomyocyte mitosis in the postmitotic myocardium. J Biol Chem 279:35858–35866PubMedCrossRef

Ehler E, Rothen BM, Hämmerle SP et al (1999) Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line, and the thick filaments. J Cell Sci 112:1529–1539PubMed

Engel FB, Schebesta M, Duong MT et al (2005) p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytes. Genes Dev 19:1175–1187PubMedCrossRef

Esposito G, Rapacciuolo A, Naga Prasad SV et al (2002) Genetic alterations that inhibit in vivo pressure-overload hypertrophy prevent cardiac dysfunction despite increased wall stress. Circulation 105:85–92PubMedCrossRef

Gulick J, Subramaniam A, Neumann J, Robbins J (1991) Isolation and characterization of the mouse cardiac myosin heavy chain genes. J Biol Chem 266:9180–9185PubMed

Herget GW, Neuburger M, Plagwitz R, Adler CP (1997) DNA content, ploidy level, and number of nuclei in the human heart after myocardial infarction. Cardiovasc Res 36:45–51PubMedCrossRef

Hirschy A, Schatzmann F, Ehler E, Perriard JC (2006) Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol 289:430–441PubMedCrossRef

10.

Hubbard SR (2004) Juxtamembrane autoinhibition in receptor tyrosine kinases. Nat Rev Mol Cell Biol 5:464–471PubMedCrossRef

11.

Li M, Naqvi N, Yahiro E, Liu K et al (2008) C-kit is required for cardiomyocyte terminal differentiation. Circ Res 102:677–685PubMedCrossRef

12.

Mol CD, Lim KB, Sridhar V et al (2003) Structure of a c-kit product complex reveals the basis for kinase transactivation. J Biol Chem 278:31461–31464PubMedCrossRef

13.

Mol CD, Dougan DR, Schneider TR et al (2004) Structural basis for the autoinhibition and STI-571 inhibition of c-kit tyrosine kinase. J Biol Chem 279:31655–31663PubMedCrossRef

14.

Ng WA, Grupp IL, Subramaniam A, Robbins J (1991) Cardiac myosin heavy chain mRNA expression and myocardial function in the mouse heart. Circ Res 68:1742–1750PubMed

15.

Nocka K, Majumder S, Chabot B, Ray P et al (1989) Expression of c-kit gene products in known cellular targets of W mutations in normal and W mutant mice: evidence for an impaired c-kit kinase in mutant mice. Genes Dev 3:816–826PubMedCrossRef

16.

Nocka K, Tan JC, Chiu E et al (1990) Molecular bases of dominant negative and loss of function mutations at the murine c-kit/white spotting lOCUS: W37, W′, W41, and W. EMBO J 9:1805–1813PubMed

17.

Oberpriller JO, Oberpriller JC (1974) Response of the adult newt ventricle to injury. J Exp Zool 187:249–253PubMedCrossRef

18.

Pasumarthi KB, Nakajima H, Nakajima HO et al (2005) Targeted expression of cyclin D2 results in cardiomyocyte DNA synthesis and infarct regression in transgenic mice. Circ Res 96:110–118PubMedCrossRef

19.

Poolman RA, Brooks G (1998) Expressions and activities of cell cycle regulatory molecules during the transition from myocyte hyperplasia to hypertrophy. J Mol Cell Cardiol 10:2121–2135CrossRef

20.

Poolman RA, Gilchrist R, Brooks G (1998) Cell cycle profiles and expressions of p21CIP1 AND P27KIP1 during myocyte development. Int J Cardiol 67:133–142PubMedCrossRef

21.

Poolman RA, Li JM, Durand B, Brooks G (1999) Altered expression of cell cycle proteins and prolonged duration of cardiac myocyte hyperplasia in p27KIP1 knockout mice. Circ Res 85:117–127PubMed

22.

Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298:2188–2190PubMedCrossRef

23.

Rumyantsev PP (1977) Interrelations of the proliferation and differentiation processes during cardiact myogenesis and regeneration. Int Rev Cytol 51:186–273PubMed

24.

Soonpaa MH, Field LJ (1997) Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. Am J Physiol 272:H220–H226PubMed

25.

Soonpaa MH, Kim KK, Pjak L et al (1996) Cardiomyocyte DNA synthesis and binucleation during murine development. Am J Physiol 271:2183–2189

26.

Soonpaa MH, Koh GY, Pajak L et al (1997) Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. J Clin Invest 99:2644–2654PubMedCrossRef

27.

Zeller R, Bloch KD, Williams BS et al (1987) Localized expression of the atrial natriuretic factor gene during cardiac embryogenesis. Genes Dev 1:693–698PubMedCrossRef

Title: Insights into the Characteristics of Mammalian Cardiomyocyte Terminal Differentiation Shown Through the Study of Mice with a Dysfunctional c-Kit
Authors: Nawazish Naqvi
Ming Li
Eiji Yahiro
Robert M. Graham
Ahsan Husain
Publication date: 01-07-2009
Publisher: Springer-Verlag
Published in: Pediatric Cardiology / Issue 5/2009
Print ISSN: 0172-0643
Electronic ISSN: 1432-1971
DOI: https://doi.org/10.1007/s00246-008-9366-1

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Insights into the Characteristics of Mammalian Cardiomyocyte Terminal Differentiation Shown Through the Study of Mice with a Dysfunctional c-Kit

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 5/2009

Concepts of Cardiac Development in Retrospect

2008 Riley Heart Center Symposium on Cardiac Development: Growth and Morphogenesis of the Ventricular Wall

Monitoring Clonal Growth in the Developing Ventricle

Stem Cells from In- or Outside of the Heart: Isolation, Characterization, and Potential for Myocardial Tissue Regeneration

Multipotent Progenitor Cells in Regenerative Cardiovascular Medicine

Analysis of Ventricular Hypertrabeculation and Noncompaction Using Genetically Engineered Mouse Models

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page