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PMID: 15861132 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Interplay between the retinoblastoma protein and LEK1 specifies stem cells toward the cardiac lineage.

The EMBO journal ·Vol. 24 ·No. 9 ·2005-05-04 ·Pages 1750-61

Papadimou E, Ménard C, Grey C, Pucéat M

Abstract

The molecular mechanisms governing early cardiogenesis are still largely unknown. Interestingly, the retinoblastoma protein (Rb), a regulator of cell cycle, has recently emerged as a new candidate regulating cell differentiation. Rb-/- mice die at midgestation and mice lacking E2f1/E2f3, downstream components of the Rb-dependent transcriptional pathway, die of heart failure. To gain insight into the function of Rb pathway in early cardiogenesis, we used Rb-/- embryonic stem (ES) cells differentiating into cardiomyocytes. Rb-/- cells displayed a dramatic delay in expression of cardiac-specific transcription factors and in turn in the whole process of cardiac differentiation. The phenotype of Rb-/- ES cell-derived cardiomyocytes was rescued by reintroducing Rb in cardiac progenitors, by stimulating the BMP-dependent cardiogenic pathway or by overexpression of Nkx2.5. ES cells deficient in the recently identified factor LEK1, a murine homolog of the cardiomyogenic factor 1, or specific disruption of Rb-LEK1 interaction into the nucleus of differentiating ES cells recapitulated the delay in cardiac differentiation of Rb-/- ES cells. Thus, we provide evidence for a novel Rb/LEK1-dependent and BMP-independent transcriptional program, which plays a pivotal role in priming ES cells toward a cardiac fate.

MeSH Terms
Animals Cell Differentiation/physiology Cell Lineage/physiology Chromosomal Proteins, Non-Histone/deficiency,metabolism Mice Microfilament Proteins Myocardial Contraction Myocardium/cytology Myocytes, Cardiac/cytology,metabolism NIH 3T3 Cells Retinoblastoma Protein/deficiency,metabolism,physiology Stem Cells/cytology,physiology
Chemicals
Chromosomal Proteins, Non-Histone Microfilament Proteins Retinoblastoma Protein centromere protein F
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Papadimou Evangelia
CRBM, CNRS FRE 2593, Montpellier, France.
Ménard Claudine
Grey Corinne
Pucéat Michel
References (51)
51 references, click to expand
  1. Characterization of cardiac muscle factor 1 sequence motifs: retinoblastoma protein binding and nuclear localization.
    Gene. 2002 Jan 9;282(1-2):53-64 PMID: 11814677
  2. Stem cell differentiation requires a paracrine pathway in the heart.
    FASEB J. 2002 Oct;16(12):1558-66 PMID: 12374778
  3. Acquisition of essential somatic cell cycle regulatory protein expression and implied activity occurs at the second to third cell division in mouse preimplantation embryos.
    FEBS Lett. 2005 Jan 17;579(2):398-408 PMID: 15642350
  4. Sizing up the heart: development redux in disease.
    Genes Dev. 2003 Aug 15;17(16):1937-56 PMID: 12893779
  5. Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents.
    Circ Res. 1994 Aug;75(2):233-44 PMID: 8033337
  6. Analysis of CMF1 reveals a bone morphogenetic protein-independent component of the cardiomyogenic pathway.
    J Biol Chem. 2000 Jul 14;275(28):21453-9 PMID: 10747923
  7. Shared role of the pRB-related p130 and p107 proteins in limb development.
    Genes Dev. 1996 Jul 1;10(13):1633-44 PMID: 8682294
  8. BMP2 is required for early heart development during a distinct time period.
    Mech Dev. 2000 Mar 1;91(1-2):259-70 PMID: 10704850
  9. Potential role of helix-loop-helix proteins in cardiac gene expression.
    Circ Res. 1993 Sep;73(3):569-78 PMID: 8394227
  10. Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene.
    Development. 1998 Dec;125(23):4669-79 PMID: 9806916
  11. E2F3 contributes both to the inappropriate proliferation and to the apoptosis arising in Rb mutant embryos.
    Genes Dev. 2001 Feb 15;15(4):386-91 PMID: 11230146
  12. Targeted disruption of p107: functional overlap between p107 and Rb.
    Genes Dev. 1996 Jul 1;10(13):1621-32 PMID: 8682293
  13. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells.
    J Biol Chem. 1999 Jul 9;274(28):19838-45 PMID: 10391928
  14. Inhibition of E2F abrogates the development of cardiac myocyte hypertrophy.
    J Biol Chem. 2003 Jun 13;278(24):21388-94 PMID: 12682052
  15. Rb function in extraembryonic lineages suppresses apoptosis in the CNS of Rb-deficient mice.
    Proc Natl Acad Sci U S A. 2003 May 27;100(11):6546-51 PMID: 12732721
  16. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins.
    Nature. 2000 Oct 5;407(6804):592-8 PMID: 11034201
  17. Identification of a novel cardiac-specific transcript critical for cardiac myocyte differentiation.
    Development. 1996 Sep;122(9):2779-89 PMID: 8787752
  18. The retinoblastoma protein and cell cycle control.
    Cell. 1995 May 5;81(3):323-30 PMID: 7736585
  19. Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation.
    J Exp Zool. 1999 Jun 15;284(1):67-81 PMID: 10368935
  20. Src family tyrosine kinase regulates intracellular pH in cardiomyocytes.
    J Cell Biol. 1998 Jun 29;141(7):1637-46 PMID: 9647655
  21. Extra-embryonic function of Rb is essential for embryonic development and viability.
    Nature. 2003 Feb 27;421(6926):942-7 PMID: 12607001
  22. Tumor suppressor gene expression during normal and pathologic myocardial growth.
    J Biol Chem. 1994 Sep 9;269(36):22607-13 PMID: 8077211
  23. LEK1 is a potential inhibitor of pocket protein-mediated cellular processes.
    J Biol Chem. 2004 Jan 2;279(1):664-76 PMID: 14555653
  24. Cell cycle control mechanisms and their role in cardiac growth.
    Cardiovasc Res. 1995 Oct;30(4):557-69 PMID: 8575004
  25. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart.
    Dev Cell. 2003 Dec;5(6):877-89 PMID: 14667410
  26. Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor beta and bone morphogenetic protein.
    Mol Cell Biol. 2004 May;24(10):4241-54 PMID: 15121845
  27. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium.
    J Embryol Exp Morphol. 1985 Jun;87:27-45 PMID: 3897439
  28. Skeletal muscle cells lacking the retinoblastoma protein display defects in muscle gene expression and accumulate in S and G2 phases of the cell cycle.
    J Cell Biol. 1996 Oct;135(2):441-56 PMID: 8896600
  29. A new mathematical model for relative quantification in real-time RT-PCR.
    Nucleic Acids Res. 2001 May 1;29(9):e45 PMID: 11328886
  30. A fluorescent reporter gene as a marker for ventricular specification in ES-derived cardiac cells.
    FEBS Lett. 2000 Jul 28;478(1-2):151-8 PMID: 10922488
  31. Patterning the vertebrate heart.
    Nat Rev Genet. 2002 Jul;3(7):544-56 PMID: 12094232
  32. The retinoblastoma gene family in differentiation and development.
    Oncogene. 1999 Dec 20;18(55):7873-82 PMID: 10630640
  33. Identification of upstream regulatory regions in the heart-expressed homeobox gene Nkx2-5.
    Development. 1999 Feb;126(4):839-49 PMID: 9895330
  34. Signaling networks that link cell proliferation and cell fate.
    J Biol Chem. 2002 Apr 5;277(14):11617-20 PMID: 11805123
  35. The cardiac cell cycle, pocket proteins, and p300.
    Trends Cardiovasc Med. 1995 Nov-Dec;5(6):230-5 PMID: 21232265
  36. A system for stable expression of short interfering RNAs in mammalian cells.
    Science. 2002 Apr 19;296(5567):550-3 PMID: 11910072
  37. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis.
    Nature. 1992 Sep 24;359(6393):288-94 PMID: 1406932
  38. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells.
    Science. 1994 Jun 3;264(5164):1467-71 PMID: 8197461
  39. Mutant mouse models reveal the relative roles of E2F1 and E2F3 in vivo.
    Mol Cell Biol. 2002 Apr;22(8):2663-72 PMID: 11909960
  40. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs.
    Genes Dev. 1996 Nov 1;10(21):2794-804 PMID: 8946919
  41. Role of the retinoblastoma protein in differentiation and senescence.
    Cancer Biol Ther. 2003 Mar-Apr;2(2):124-30 PMID: 12750549
  42. Requirement for a functional Rb-1 gene in murine development.
    Nature. 1992 Sep 24;359(6393):328-30 PMID: 1406937
  43. Rb is required for progression through myogenic differentiation but not maintenance of terminal differentiation.
    J Cell Biol. 2004 Sep 13;166(6):865-76 PMID: 15364961
  44. Effects of an Rb mutation in the mouse.
    Nature. 1992 Sep 24;359(6393):295-300 PMID: 1406933
  45. Id proteins at the cross-road of development and cancer.
    Oncogene. 2001 Dec 20;20(58):8326-33 PMID: 11840325
  46. E2F-dependent histone acetylation and recruitment of the Tip60 acetyltransferase complex to chromatin in late G1.
    Mol Cell Biol. 2004 May;24(10):4546-56 PMID: 15121871
  47. The RB and p53 pathways in cancer.
    Cancer Cell. 2002 Aug;2(2):103-12 PMID: 12204530
  48. The C-terminal domain of c-fos is required for activation of an AP-1 site specific for jun-fos heterodimers.
    Mol Cell Biol. 1998 Sep;18(9):5073-81 PMID: 9710591
  49. The retinoblastoma gene family is differentially expressed during embryogenesis.
    Oncogene. 1997 Apr 17;14(15):1789-97 PMID: 9150384
  50. The cloning and analysis of LEK1 identifies variations in the LEK/centromere protein F/mitosin gene family.
    J Biol Chem. 1999 Jun 25;274(26):18597-604 PMID: 10373470
  51. A genetic blueprint for cardiac development.
    Nature. 2000 Sep 14;407(6801):221-6 PMID: 11001064
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2005-05-04
Epub
2005-00-21
Pages
1750-61
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1142583
Subset
IM
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