Cardiomyogenesis is controlled by the miR-99a/let-7c cluster and epigenetic modifications

Stem Cell Research

Volumn 12, Issue 2, 2014, Pages 323-337

  Coppola, Antonietta ^a   Romito, Antonio ^b   Borel, Christelle ^c   Gehrig, Corinne ^c   Gagnebin, Maryline ^c   Falconnet, Emilie ^c   Izzo, Antonella ^d   Altucci, Lucia ^a   Banfi, Sandro ^a,b   Antonarakis, Stylianos E ^c   Minchiotti, Gabriella ^e   Cobellis, Gilda ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESP 1 PROTEIN; MESSENGER RNA PRECURSOR; MICRORNA 99A; MICRORNA LET 7C; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2C; NODAL SIGNALING PROTEIN; SMAD2 PROTEIN; SMARCA5 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR TBX5; UNCLASSIFIED DRUG; MICRORNA; MIRN99 MICRORNA, HUMAN; MIRN99 MICRORNA, MOUSE; MIRNLET7 MICRORNA, HUMAN; MIRNLET7 MICRORNA, MOUSE;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CHROMATIN; CHROMOSOME 21; CONTROLLED STUDY; DOWN SYNDROME; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; EPIGENETICS; FETUS; FETUS HEART; GENE CLUSTER; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HEART MUSCLE CELL; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MESODERM; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; UPREGULATION; ANIMAL; CYTOLOGY; GENETIC EPIGENESIS; GENETIC TRANSFECTION; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HUMANS; MICE; MICRORNAS; MYOCYTES, CARDIAC; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84890819225     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.11.008     Document Type: Article

References (48)

1. Antonarakis S.E., et al. Chromosome 21 and down syndrome: from genomics to pathophysiology. Nat. Rev. Genet. 2004, 5(10):725-738.
2. Araki K., et al. Efficiency of recombination by Cre transient expression in embryonic stem cells: comparison of various promoters. J. Biochem. 1997, 122(5):977-982.
3. Barrero M.J., et al. Epigenetic mechanisms that regulate cell identity. Cell Stem Cell 2010, 7(5):565-570.
4. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136(2):215-233.
5. Bernstein E., et al. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 2006, 26(7):2560-2569.
6. Burridge P.W., et al. Production of de novo cardiomyocytes: human pluripotent stem cell differentiation and direct reprogramming. Cell Stem Cell 2012, 10(1):16-28.
7. Caretti G., et al. The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev. 2004, 18(21):2627-2638.
8. Chen J.F., et al. Targeted deletion of Dicer in the heart leads to dilated cardiomyopathy and heart failure. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(6):2111-2116.
9. Colas A.R., et al. Whole-genome microRNA screening identifies let-7 and mir-18 as regulators of germ layer formation during early embryogenesis. Genes Dev. 2012, 26(23):2567-2579.
10. Corona D.F., Tamkun J.W. Multiple roles for ISWI in transcription, chromosome organization and DNA replication. Biochim. Biophys. Acta 2004, 1677(1-3):113-119.
11. da Costa Martins P.A., et al. Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 2008, 118(15):1567-1576.
12. D'Aniello C., et al. G protein-coupled receptor APJ and its ligand apelin act downstream of Cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circ. Res. 2009, 105(3):231-238.
13. De Cegli R., et al. A mouse embryonic stem cell bank for inducible overexpression of human chromosome 21 genes. Genome Biol. 2010, 11(6):R64.
14. Delgado-Olguin P., et al. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat. Genet. 2012, 44(3):343-347.
15. Dirscherl S., Krebs J.E. Functional diversity of ISWI complexes. Biochem. Cell Biol. 2004, 82(4):482-489.
16. Erdel F., et al. Human ISWI chromatin-remodeling complexes sample nucleosomes via transient binding reactions and become immobilized at active sites. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(46):19873-19878.
17. Fei T., et al. Smad2 mediates Activin/Nodal signaling in mesendoderm differentiation of mouse embryonic stem cells. Cell Res. 2010, 20(12):1306-1318.
18. Frankenberg S., et al. Primitive endoderm differentiates via a three-step mechanism involving Nanog and RTK signaling. Dev. Cell 2011, 21(6):1005-1013.
19. Gennarino V.A., et al. Identification of microRNA-regulated gene networks by expression analysis of target genes. Genome Res. 2012, 22(6):1163-1172.
20. Gentleman R.C., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5(10):R80.
21. Guo H., et al. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466(7308):835-840.
22. He A., Pu W.T. Mature cardiomyocytes recall their progenitor experience via polycomb repressive complex 2. Circ. Res. 2012, 111(2):162-164.
23. He A., et al. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ. Res. 2012, 110(3):406-415.
24. Iorio M.V., Croce C.M. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 2012, 4(3):143-159.
25. Juan A.H., et al. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes Dev. 2011, 25(8):789-794.
26. Kanellopoulou C., et al. Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 2005, 19(4):489-501.
27. Kitamura R., et al. Stage-specific role of endogenous Smad2 activation in cardiomyogenesis of embryonic stem cell. Circ. Res. 2007, 101(1):78-87.
28. Kong D., et al. Loss of let-7 up-regulates EZH2 in prostate cancer consistent with the acquisition of cancer stem cell signatures that are attenuated by BR-DIM. PLoS ONE 2012, 7(3):e33729.
29. Laible G., et al. Mammalian homologues of the polycomb-group gene enhancer of zeste mediate gene silencing in Drosophila heterochromatin and at S. cerevisiae telomeres. EMBO J. 1997, 16(11):3219-3232.
30. Liu N., Olson E.N. MicroRNA regulatory networks in cardiovascular development. Dev. Cell 2010, 18(4):510-525.
31. Masui S., et al. An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic Acids Res. 2005, 33(4):e43.
32. McLendon P.M., Robbins J. Desmin-related cardiomyopathy: an unfolding story. Am. J. Physiol. Heart Circ. Physiol. 2011, 301(4):H1220-H1228.
33. Mulder K.W., et al. Diverse epigenetic strategies interact to control epidermal differentiation. Nat. Cell Biol. 2012, 14(7):753-763.
34. Murry C.E., Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008, 132(4):661-680.
35. Nadiminty N., et al. MicroRNA let-7c is downregulated in prostate cancer and suppresses prostate cancer growth. PLoS ONE 2012, 7(3):e32832.
36. Nadiminty N., et al. MicroRNA let-7c suppresses androgen receptor expression and activity via regulation of Myc expression in prostate cancer cells. J. Biol. Chem. 2012, 287(2):1527-1537.
37. O'Carroll D., et al. The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 2001, 21(13):4330-4336.
38. Ozsolak F., et al. Chromatin structure analyses identify miRNA promoters. Genes Dev. 2008, 22(22):3172-3183.
39. Roush S., Slack F.J. The let-7 family of microRNAs. Trends Cell Biol. 2008, 18(10):505-516.
40. Sauvageau M., Sauvageau G. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 2010, 7(3):299-313.
41. Sher F., et al. Dynamic changes in Ezh2 gene occupancy underlie its involvement in neural stem cell self-renewal and differentiation towards oligodendrocytes. PLoS ONE 2012, 7(7):e40399.
42. Stopka T., Skoultchi A.I. The ISWI ATPase Snf2h is required for early mouse development. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(24):14097-14102.
43. Sun D., et al. miR-99 family of MicroRNAs suppresses the expression of prostate-specific antigen and prostate cancer cell proliferation. Cancer Res. 2011, 71(4):1313-1324.
44. Tarantino C., et al. miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J. 2010, 24(9):3255-3263.
45. Turcatel G., et al. MIR-99a and MIR-99b modulate TGF-beta induced epithelial to mesenchymal plasticity in normal murine mammary gland cells. PLoS ONE 2012, 7(1):e31032.
46. Vandesompele J., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3(7).
47. Zhao Y., et al. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005, 436(7048):214-220.
48. Zhao Y., et al. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 2007, 129(2):303-317.