Enhancing myogenic differentiation of pluripotent stem cells with small molecule inducers

Cell and Bioscience

Volumn 3, Issue 1, 2013, Pages

  Chen, Jihong ^a   Li, Qiao ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Gene regulation; Histone acetylation; Myogenic differentiation; Nuclear receptor; Stem cells

Indexed keywords

EID: 84885131810     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-3-40     Document Type: Review

References (75)

1. Niederreither K, Dolle P. Retinoic acid in development: towards an integrated view. Nat Rev Genet 2008, 9:541-553.
2. Wilson JG, Roth CB, Warkany J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 1953, 92:189-217.
3. Chambon P. The nuclear receptor superfamily: a personal retrospect on the first two decades. Mol Endocrinol 2005, 19:1418-1428.
4. Folkers GE, van der Burg B, van der Saag PT. Promoter architecture, cofactors, and orphan receptors contribute to cell-specific activation of the retinoic acid receptor beta2 promoter. J Biol Chem 1998, 273:32200-32212.
5. Higazi A, Abed M, Chen J, Li Q. Promoter context determines the role of proteasome in ligand-dependent occupancy of retinoic acid responsive elements. Epigenetics 2011, 6:202-211.
6. Kurokawa R, DiRenzo J, Boehm M, Sugarman J, Gloss B, Rosenfeld MG, Heyman RA, Glass CK. Regulation of retinoid signalling by receptor polarity and allosteric control of ligand binding. Nature 1994, 371:528-531.
7. Li Q, Imhof A, Collingwood TN, Urnov FD, Wolffe AP. p300 stimulates transcription instigated by ligand-bound thyroid hormone receptor at a step subsequent to chromatin disruption. EMBO J 1999, 18:5634-5652.
8. Li Q, Sachs L, Shi YB, Wolffe AP. Modification of Chromatin Structure by the Thyroid Hormone Receptor. Trends Endocrinol Metab 1999, 10:157-164.
9. Li Q, Wrange O. Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Mol Cell Biol 1995, 15:4375-4384.
10. Li Q, Wrange O. Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. Genes Dev 1993, 7:2471-2482.
11. John S, Sabo PJ, Johnson TA, Sung MH, Biddie SC, Lightman SL, Voss TC, Davis SR, Meltzer PS, Stamatoyannopoulos JA, Hager GL. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 2008, 29:611-624.
12. Schild C, Claret FX, Wahli W, Wolffe AP. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. Embo J 1993, 12:423-433.
13. Wang Q, Carroll JS, Brown M. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell 2005, 19:631-642.
14. Gillespie RF, Gudas LJ. Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol 2007, 372:298-316.
15. Lee ER, Murdoch FE, Fritsch MK. High histone acetylation and decreased polycomb repressive complex 2 member levels regulate gene specific transcriptional changes during early embryonic stem cell differentiation induced by retinoic acid. Stem Cells 2007, 25:2191-2199.
16. Bhattacharyya N, Dey A, Minucci S, Zimmer A, John S, Hager G, Ozato K. Retinoid-induced chromatin structure alterations in the retinoic acid receptor beta2 promoter. Mol Cell Biol 1997, 17:6481-6490.
17. Langston AW, Thompson JR, Gudas LJ. Retinoic acid-responsive enhancers located 3' of the Hox A and Hox B homeobox gene clusters. Functional analysis. J Biol Chem 1997, 272:2167-2175.
18. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. Function of retinoic acid receptor gamma in the mouse. Cell 1993, 73:643-658.
19. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M, Chambon P. High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc Natl Acad Sci USA 1993, 90:7225-7229.
20. Grondona JM, Kastner P, Gansmuller A, Decimo D, Chambon P, Mark M. Retinal dysplasia and degeneration in RARbeta2/RARgamma2 compound mutant mice. Development 1996, 122:2173-2188.
21. Lohnes D, Mark M, Mendelsohn C, Dolle P, Dierich A, Gorry P, Gansmuller A, Chambon P. Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 1994, 120:2723-2748.
22. Wendling O, Ghyselinck NB, Chambon P, Mark M. Roles of retinoic acid receptors in early embryonic morphogenesis and hindbrain patterning. Development 2001, 128:2031-2038.
23. Wendling O, Dennefeld C, Chambon P, Mark M. Retinoid signaling is essential for patterning the endoderm of the third and fourth pharyngeal arches. Development 2000, 127:1553-1562.
24. Kastner P, Grondona JM, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch JL, Dolle P, Chambon P. Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 1994, 78:987-1003.
25. Krezel W, Dupe V, Mark M, Dierich A, Kastner P, Chambon P. RXR gamma null mice are apparently normal and compound RXR alpha +/-/RXR beta -/-/RXR gamma -/- mutant mice are viable. Proc Natl Acad Sci USA 1996, 93:9010-9014.
26. Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR, Evans RM. RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev 1994, 8:1007-1018.
27. Sapin V, Dolle P, Hindelang C, Kastner P, Chambon P. Defects of the chorioallantoic placenta in mouse RXRalpha null fetuses. Dev Biol 1997, 191:29-41.
28. Kastner P, Mark M, Ghyselinck N, Krezel W, Dupe V, Grondona JM, Chambon P. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 1997, 124:313-326.
29. Wendling O, Chambon P, Mark M. Retinoid X receptors are essential for early mouse development and placentogenesis. Proc Natl Acad Sci USA 1999, 96:547-551.
30. Tanaka T, De Luca LM. Therapeutic potential of "rexinoids" in cancer prevention and treatment. Cancer Res 2009, 69:4945-4947.
31. Ahuja HS, Szanto A, Nagy L, Davies PJ. The retinoid X receptor and its ligands: versatile regulators of metabolic function, cell differentiation and cell death. J Biol Regul Homeost Agents 2003, 17:29-45.
32. Heintzman ND, Ren B. Finding distal regulatory elements in the human genome. Curr Opin Genet Dev 2009, 19:541-549.
33. Wolffe AP. Histones, nucleosomes and the roles of chromatin structure in transcriptional control. Biochem Soc Trans 1997, 25:354-358.
34. Orkin SH, Hochedlinger K. Chromatin connections to pluripotency and cellular reprogramming. Cell 2011, 145:835-850.
35. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130:77-88.
36. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007, 39:311-318.
37. Asp P, Blum R, Vethantham V, Parisi F, Micsinai M, Cheng J, Bowman C, Kluger Y, Dynlacht BD. Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci USA 2011, 108:E149-158.
38. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
39. Dorschner MO, Hawrylycz M, Humbert R, Wallace JC, Shafer A, Kawamoto J, Mack J, Hall R, Goldy J, Sabo PJ, Kohli A, Li Q, McArthur M, Stamatoyannopoulos JA. High-throughput localization of functional elements by quantitative chromatin profiling. Nat Methods 2004, 1:219-225.
40. Berkes CA, Tapscott SJ. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 2005, 16:585-595.
41. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 1997, 89:127-138.
42. Francetic T, Li Q. Skeletal myogenesis and Myf5 activation. Transcription 2011, 2:109-114.
43. Roth JF, Shikama N, Henzen C, Desbaillets I, Lutz W, Marino S, Wittwer J, Schorle H, Gassmann M, Eckner R. Differential role of p300 and CBP acetyltransferase during myogenesis: p300 acts upstream of MyoD and Myf5. Embo J 2003, 22:5186-5196.
44. Martin GR, Evans MJ. The morphology and growth of a pluripotent teratocarcinoma cell line and its derivatives in tissue culture. Cell 1974, 2:163-172.
45. Martin GR, Evans MJ. Differentiation of clonal lines of teratocarcinoma cells: formation of embryoid bodies in vitro. Proc Natl Acad Sci USA 1975, 72:1441-1445.
46. Le May M, Mach H, Lacroix N, Hou C, Chen J, Li Q. Contribution of Retinoid X Receptor Signaling to the Specification of Skeletal Muscle Lineage. J Biol Chem 2011, 286:26806-26812.
47. McBurney MW, Rogers BJ. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev Biol 1982, 89:503-508.
48. Vidricaire G, Jardine K, McBurney MW. Expression of the Brachyury gene during mesoderm development in differentiating embryonal carcinoma cell cultures. Development 1994, 120:115-122.
49. McBurney MW, Jones-Villeneuve EM, Edwards MK, Anderson PJ. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 1982, 299:165-167.
50. Edwards MK, McBurney MW. The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol 1983, 98:187-191.
51. Edwards MK, Harris JF, McBurney MW. Induced muscle differentiation in an embryonal carcinoma cell line. Mol Cell Biol 1983, 3:2280-2286.
52. Jones-Villeneuve EM, Rudnicki MA, Harris JF, McBurney MW. Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol Cell Biol 1983, 3:2271-2279.
53. Kennedy KA, Porter T, Mehta V, Ryan SD, Price F, Peshdary V, Karamboulas C, Savage J, Drysdale TA, Li SC, Bennett SA, Skerjanc IS. Retinoic acid enhances skeletal muscle progenitor formation and bypasses inhibition by bone morphogenetic protein 4 but not dominant negative beta-catenin. BMC Biol 2009, 7:67.
54. Armour C, Garson K, McBurney MW. Cell-cell interaction modulates myoD-induced skeletal myogenesis of pluripotent P19 cells in vitro. Exp Cell Res 1999, 251:79-91.
55. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
56. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981, 78:7634-7638.
57. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R. 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, 87:27-45.
58. Williams RL, Hilton DJ, Pease S, Willson TA, Stewart CL, Gearing DP, Wagner EF, Metcalf D, Nicola NA, Gough NM. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 1988, 336:684-687.
59. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, Stahl M, Rogers D. Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 1988, 336:688-690.
60. Rohwedel J, Maltsev V, Bober E, Arnold HH, Hescheler J, Wobus AM. Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Dev Biol 1994, 164:87-101.
61. Wobus AM, Rohwedel J, Maltsev V, Hescheler J. In vitro differentiation of embryonic stem cells into cardiomyocytes or skeletal muscle cells is specifically modulated by retinoic acid. Roux's Arch Dev Biol 1994, 204:36-45.
62. Bajard L, Relaix F, Lagha M, Rocancourt D, Daubas P, Buckingham ME. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev 2006, 20:2450-2464.
63. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell 2000, 102:777-786.
64. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomes D, Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 2005, 19:1426-1431.
65. Relaix F, Rocancourt D, Mansouri A, Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 2005, 435:948-953.
66. Darabi R, Gehlbach K, Bachoo RM, Kamath S, Osawa M, Kamm KE, Kyba M, Perlingeiro RC. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med 2008, 14:134-143.
67. Darabi R, Santos FN, Filareto A, Pan W, Koene R, Rudnicki MA, Kyba M, Perlingeiro RC. Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors. Stem Cells 2011, 29:777-790.
68. Ridgeway AG, Skerjanc IS. Pax3 is essential for skeletal myogenesis and the expression of Six1 and Eya2. J Biol Chem 2001, 276:19033-19039.
69. Petropoulos H, Gianakopoulos PJ, Ridgeway AG, Skerjanc IS. Disruption of Meox or Gli activity ablates skeletal myogenesis in P19 cells. J Biol Chem 2004, 279:23874-23881.
70. Francetic T, Le May M, Hamed M, Mach H, Meyers D, Cole PA, Chen J, Li Q. Regulation of Myf5 early enhancer by histone acetyltransferase p300 during stem cell differentiation. Mol Biol 2012, 1:103.
71. Hamed M, Khilji S, Chen J, Li Q. Stepwise acetyltransferase association and histone acetylation at the Myod1 locus during myogenic differentiation. Sci Rep 2013, 3:2390.
72. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, Goodyear LJ, Wagers AJ. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 2008, 134:37-47.
73. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM. Self-renewal and expansion of single transplanted muscle stem cells. Nature 2008, 456:502-506.
74. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M. Direct isolation of satellite cells for skeletal muscle regeneration. Science 2005, 309:2064-2067.
75. Shi X, Garry DJ. Muscle stem cells in development, regeneration, and disease. Genes Dev 2006, 20:1692-1708.