Home LiteratureArticle Details
PMID: 16242146 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural

Proliferation of cardiomyocytes derived from human embryonic stem cells is mediated via the IGF/PI 3-kinase/Akt signaling pathway.

Journal of molecular and cellular cardiology ·Vol. 39 ·No. 6 ·2005-12-00 ·Pages 865-73

McDevitt TC, Laflamme MA, Murry CE

Abstract

Cardiomyocytes from common experimental animals rapidly exit the cell cycle upon isolation, impeding studies of basic cell biology and applications such as myocardial repair. Here we examined proliferation of cardiomyocytes derived from human and mouse embryonic stem (ES) cells. While mouse ES cell-derived cardiomyocytes showed little proliferation, human cardiomyocytes were highly proliferative under serum-free conditions (15-25% BrdU+/sarcomeric actin+). The cells exhibited only a small serum dose-response, and proliferation gradually slowed with increasing differentiation of the cells. Neither cell density nor different matrix attachment factors affected cardiomyocyte proliferation. Blockade of phosphatidylinositol 3-kinase (PI 3-kinase) and Akt significantly reduced cardiomyocyte proliferation, whereas MEK inhibition had no effect. Antibody blocking of the insulin-like growth factor-1 (IGF-1) receptor significantly inhibited cardiomyocyte proliferation, while addition of IGF-1 or IGF-2 stimulated cardiomyocyte proliferation in a dose-dependent manner. Thus, cardiomyocytes derived from human ES cells proliferate extensively in vitro, and their proliferation appears to be mediated primarily via the PI 3-kinase/Akt signaling pathway, using the IGF-1 receptor as one upstream activator. This system should permit identification of regulatory pathways for human cardiomyocyte proliferation and may facilitate expansion of cardiomyocytes from human ES cells for therapeutic purposes.

MeSH Terms
Animals Cell Proliferation/drug effects Cells, Cultured Dose-Response Relationship, Drug Embryo, Mammalian/cytology,physiology Heart Diseases/therapy Humans Insulin-Like Growth Factor I/metabolism,pharmacology Insulin-Like Growth Factor II/metabolism,pharmacology Mice Myocytes, Cardiac/cytology,physiology,transplantation Phosphatidylinositol 3-Kinases/metabolism Proto-Oncogene Proteins c-akt/metabolism Signal Transduction/drug effects,physiology Stem Cells/cytology,physiology
Chemicals
Insulin-Like Growth Factor I Insulin-Like Growth Factor II Phosphatidylinositol 3-Kinases Proto-Oncogene Proteins c-akt
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
McDevitt Todd C
Center for Cardiovascular Biology and Regenerative Medicine, University of Washington, 815 Mercer Street, Seattle, WA 98109, USA.
Laflamme Michael A
Murry Charles E
References (41)
41 references, click to expand
  1. Proliferation in vivo and in culture of differentiated adult atrial cardiomyocytes from transgenic mice.
    Am J Physiol. 1990 Dec;259(6 Pt 2):H1826-34 PMID: 2175567
  2. Inhibition of phosphatidylinositol-3-kinase blocks development of functional embryonic cardiomyocytes.
    Exp Cell Res. 1999 Feb 25;247(1):79-83 PMID: 10047449
  3. Cardiomyocyte proliferation in mice expressing alpha-cardiac myosin heavy chain-SV40 T-antigen transgenes.
    Am J Physiol. 1992 Jun;262(6 Pt 2):H1867-76 PMID: 1377879
  4. The IGF-1-IGF-1 receptor system modulates myocyte proliferation but not myocyte cellular hypertrophy in vitro.
    Exp Cell Res. 1994 Dec;215(2):273-83 PMID: 7982470
  5. Quantitative study of the myocardium in human embryos.
    Ann Anat. 1995 Mar;177(2):179-84 PMID: 7741280
  6. Down-regulation of the IGF-1 system parallels the attenuation in the proliferative capacity of rat ventricular myocytes during postnatal development.
    Lab Invest. 1995 Jun;72(6):646-55 PMID: 7783422
  7. Cardiomyocyte proliferation and hypertrophy in the human fetus: quantitative study of the myocyte nuclei.
    Bull Assoc Anat (Nancy). 1995 Sep;79(246):27-31 PMID: 8541608
  8. DNA synthesis and multinucleation in embryonic stem cell-derived cardiomyocytes.
    Am J Physiol. 1995 Dec;269(6 Pt 2):H1913-21 PMID: 8594899
  9. Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8630-5 PMID: 8710922
  10. Epidermal growth factor promotes a cardiomyoblastic phenotype in human fetal cardiac myocytes.
    Exp Cell Res. 1996 Nov 1;228(2):237-45 PMID: 8912716
  11. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):2979-84 PMID: 9501201
  12. Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I.
    Circ Res. 1998 Sep 7;83(5):516-22 PMID: 9734474
  13. Embryonic stem cell lines derived from human blastocysts.
    Science. 1998 Nov 6;282(5391):1145-7 PMID: 9804556
  14. Local insulin-like growth factor I expression induces physiologic, then pathologic, cardiac hypertrophy in transgenic mice.
    FASEB J. 1999 Nov;13(14):1923-9 PMID: 10544175
  15. Adenoviral gene transfer of activated phosphatidylinositol 3'-kinase and Akt inhibits apoptosis of hypoxic cardiomyocytes in vitro.
    Circulation. 1999 Dec 7;100(23):2373-9 PMID: 10587343
  16. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart.
    Circulation. 2000 Feb 15;101(6):660-7 PMID: 10673259
  17. Differentiation of cardiomyocytes in floating embryoid bodies is comparable to fetal cardiomyocytes.
    J Mol Cell Cardiol. 2000 May;32(5):839-51 PMID: 10775488
  18. The conserved phosphoinositide 3-kinase pathway determines heart size in mice.
    EMBO J. 2000 Jun 1;19(11):2537-48 PMID: 10835352
  19. Genetic dissection of cardiac growth control pathways.
    Annu Rev Physiol. 2000;62:289-319 PMID: 10845093
  20. Role of reactive oxygen species and phosphatidylinositol 3-kinase in cardiomyocyte differentiation of embryonic stem cells.
    FEBS Lett. 2000 Jul 7;476(3):218-23 PMID: 10913617
  21. Synthesis of extracellular matrix and adhesion through beta(1) integrins are critical for fetal ventricular myocyte proliferation.
    Circ Res. 2000 Sep 15;87(6):508-15 PMID: 10988244
  22. Expression of constitutively active phosphatidylinositol 3-kinase inhibits activation of caspase 3 and apoptosis of cardiac muscle cells.
    J Biol Chem. 2000 Dec 22;275(51):40113-9 PMID: 11007772
  23. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo.
    Circulation. 2001 Jul 17;104(3):330-5 PMID: 11457753
  24. Potential of embryonic stem cells.
    Mol Aspects Med. 2001 Jun;22(3):149-64 PMID: 11470141
  25. Cell proliferation in the growing human heart: MIB-1 immunostaining in preterm and term infants at autopsy.
    Cardiovasc Pathol. 2001 May-Jun;10(3):119-23 PMID: 11485855
  26. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes.
    J Clin Invest. 2001 Aug;108(3):407-14 PMID: 11489934
  27. Feeder-free growth of undifferentiated human embryonic stem cells.
    Nat Biotechnol. 2001 Oct;19(10):971-4 PMID: 11581665
  28. Akt/protein kinase B promotes organ growth in transgenic mice.
    Mol Cell Biol. 2002 Apr;22(8):2799-809 PMID: 11909972
  29. Cardiac-specific IGF-1 expression attenuates dilated cardiomyopathy in tropomodulin-overexpressing transgenic mice.
    Circ Res. 2002 Apr 5;90(6):641-8 PMID: 11934830
  30. Cardiomyocyte cell cycle regulation.
    Circ Res. 2002 May 31;90(10):1044-54 PMID: 12039793
  31. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells.
    Circ Res. 2002 Sep 20;91(6):501-8 PMID: 12242268
  32. Epicardial induction of fetal cardiomyocyte proliferation via a retinoic acid-inducible trophic factor.
    Dev Biol. 2002 Oct 1;250(1):198-207 PMID: 12297106
  33. Erythropoietin and retinoic acid, secreted from the epicardium, are required for cardiac myocyte proliferation.
    Dev Biol. 2003 Mar 15;255(2):334-49 PMID: 12648494
  34. Conditional expression of SV40 T-antigen in mouse cardiomyocytes facilitates an inducible switch from proliferation to differentiation.
    J Biol Chem. 2003 May 2;278(18):15927-34 PMID: 12590133
  35. Phosphoinositide 3-kinase(p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12355-60 PMID: 14507992
  36. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes.
    Am J Physiol Heart Circ Physiol. 2003 Dec;285(6):H2355-63 PMID: 14613910
  37. Extracellular signal-regulated kinase and phosphoinositol-3 kinase mediate IGF-1 induced proliferation of fetal sheep cardiomyocytes.
    Am J Physiol Regul Integr Comp Physiol. 2003 Dec;285(6):R1481-9 PMID: 12947030
  38. The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway.
    J Biol Chem. 2004 Feb 6;279(6):4782-93 PMID: 14597618
  39. Involvement of reactive oxygen species in cardiotrophin-1-induced proliferation of cardiomyocytes differentiated from murine embryonic stem cells.
    Exp Cell Res. 2004 Apr 1;294(2):313-24 PMID: 15023522
  40. Culture and characterization of fetal human atrial and ventricular cardiac muscle cells.
    In Vitro Cell Dev Biol. 1989 Dec;25(12):1114-20 PMID: 2532644
  41. Effects of subcultivation and culture medium on differentiation of human fetal cardiac myocytes.
    In Vitro Cell Dev Biol. 1992 Feb;28A(2):109-19 PMID: 1537751
Article Info
Journal
Journal of molecular and cellular cardiology
Abbr.
J Mol Cell Cardiol
ISSN
0022-2828
Published
2005-12-00
Epub
2005-00-19
Pages
865-73
Language
English
Region
England
NLM ID
0262322
PMCID
PMC3505759
Subset
IM
Grants
NHLBI NIH HHS · T32 HL007403-25 · United States
NHLBI NIH HHS · P01 HL003174-50 · United States
NIGMS NIH HHS · GM69983 · United States
NHLBI NIH HHS · R01 HL064387 · United States
NIGMS NIH HHS · P20 GM069983 · United States
NHLBI NIH HHS · P01 HL003174 · United States
NHLBI NIH HHS · HL3174 · United States
NHLBI NIH HHS · R24 HL064387 · United States
NHLBI NIH HHS · HL64387 · United States
NHLBI NIH HHS · HL07403-25 · United States
NIGMS NIH HHS · P20 GM069983-03 · United States
NHLBI NIH HHS · R01 HL061553 · United States
NHLBI NIH HHS · T32 HL007403 · United States
NHLBI NIH HHS · R01 HL061553-07 · United States
NHLBI NIH HHS · HL61553 · United States
NHLBI NIH HHS · R24 HL064387-05 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com