Derivation and expansion of PAX7-positive muscle progenitors from human and mouse embryonic stem cells

Stem Cell Reports

Volumn 3, Issue 3, 2014, Pages 516-529

  Shelton, Michael ^a   Metz, Jeff ^a   Liu, Jun ^a   Carpenedo, Richard L ^a,b   Demers, Simon Pierre ^a,b   Stanford, William L ^a,b   Skerjanc, Ilona S ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR 2; MYOD1 PROTEIN; MYOGENIN; TRANSCRIPTION FACTOR NKX2.5; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR PAX7; 6 [[2 [[4 (2,4 DICHLOROPHENYL) 5 (4 METHYL 1H IMIDAZOL 2 YL) 2 PYRIMIDINYL]AMINO]ETHYL]AMINO]NICOTINONITRILE; GLYCOGEN SYNTHASE KINASE 3; PYRIDINE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL SELECTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MESODERM; MOUSE; MUSCLE DEVELOPMENT; MUSCLE STEM CELL; MYOTOME; MYOTUBE; NEURAL CREST CELL; NONHUMAN; PROTEIN EXPRESSION; SKELETAL MUSCLE; SOMITE; STEM CELL EXPANSION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCEDURES;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MESODERM; MICE; MUSCLE DEVELOPMENT; MUSCLE FIBERS, SKELETAL; PAX7 TRANSCRIPTION FACTOR; PYRIDINES; PYRIMIDINES;

EID: 84914149375     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.07.001     Document Type: Article

References (65)

1. H. Akazawa, and I. Komuro Cardiac transcription factor Csx/Nkx2-5: Its role in cardiac development and diseases Pharmacol. Ther. 107 2005 252 268
2. A.S. Al Madhoun, V. Mehta, G. Li, D. Figeys, N. Wiper-Bergeron, and I.S. Skerjanc Skeletal myosin light chain kinase regulates skeletal myogenesis by phosphorylation of MEF2C EMBO J. 30 2011 2477 2489
3. S. Albini, P. Coutinho, B. Malecova, L. Giordani, A. Savchenko, S.V. Forcales, and P.L. Puri Epigenetic reprogramming of human embryonic stem cells into skeletal muscle cells and generation of contractile myospheres Cell Reports 3 2013 661 670
4. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
5. R. Araki, M. Uda, Y. Hoki, M. Sunayama, M. Nakamura, S. Ando, M. Sugiura, H. Ideno, A. Shimada, A. Nifuji, and M. Abe Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells Nature 494 2013 100 104
6. T. Awaya, T. Kato, Y. Mizuno, H. Chang, A. Niwa, K. Umeda, T. Nakahata, and T. Heike Selective development of myogenic mesenchymal cells from human embryonic and induced pluripotent stem cells PLoS ONE 7 2012 e51638
7. T. Barberi, M. Bradbury, Z. Dincer, G. Panagiotakos, N.D. Socci, and L. Studer Derivation of engraftable skeletal myoblasts from human embryonic stem cells Nat. Med. 13 2007 642 648
8. B. Borchin, J. Chen, and T. Barberi Derivation and FACS-Mediated Purification of PAX3+/PAX7+ Skeletal Muscle Precursors from Human Pluripotent Stem Cells Stem Cell Rev. 1 2013 620 631
9. M. Buckingham Skeletal muscle progenitor cells and the role of Pax genes C. R. Biol. 330 2007 530 533
10. N. Cao, H. Liang, J. Huang, J. Wang, Y. Chen, Z. Chen, and H.-T. Yang Highly efficient induction and long-term maintenance of multipotent cardiovascular progenitors from human pluripotent stem cells under defined conditions Cell Res. 23 2013 1119 1132
11. H. Chang, M. Yoshimoto, K. Umeda, T. Iwasa, Y. Mizuno, S. Fukada, H. Yamamoto, N. Motohashi, Y. Miyagoe-Suzuki, and S. Takeda Generation of transplantable, functional satellite-like cells from mouse embryonic stem cells FASEB J. 23 2009 1907 1919
12. W.Y. Chang, J.R. Lavoie, S.Y. Kwon, Z. Chen, J.L. Manias, J. Behbahani, V. Ling, R.A. Kandel, D.J. Stewart, and W.L. Stanford Feeder-independent derivation of induced-pluripotent stem cells from peripheral blood endothelial progenitor cells Stem Cell Res. (Amst.) 10 2013 195 202
13. G. Chen, D.R. Gulbranson, Z. Hou, J.M. Bolin, V. Ruotti, M.D. Probasco, K. Smuga-Otto, S.E. Howden, N.R. Diol, and N.E. Propson Chemically defined conditions for human iPSC derivation and culture Nat. Methods 8 2011 424 429
14. L. Cheng, L.E. Alvares, M.U. Ahmed, A.S. El-Hanfy, and S. Dietrich The epaxial-hypaxial subdivision of the avian somite Dev. Biol. 274 2004 348 369
15. H. Clevers Wnt/beta-catenin signaling in development and disease Cell 127 2006 469 480
16. K.A. D'Amour, and F.H. Gage Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells Proc. Natl. Acad. Sci. USA 100 Suppl 1 2003 11866 11872
17. R. Darabi, K. Gehlbach, R.M. Bachoo, S. Kamath, M. Osawa, K.E. Kamm, M. Kyba, and R.C.R. Perlingeiro Functional skeletal muscle regeneration from differentiating embryonic stem cells Nat. Med. 14 2008 134 143
18. R. Darabi, F.N.C. Santos, A. Filareto, W. Pan, R. Koene, M.A. Rudnicki, M. Kyba, and R.C. Perlingeiro Assessment of the myogenic stem cell compartment following transplantation of Pax3/Pax7-induced embryonic stem cell-derived progenitors Stem Cells 29 2011 777 790
19. R. Darabi, W. Pan, D. Bosnakovski, J. Baik, M. Kyba, and R.C.R. Perlingeiro Functional myogenic engraftment from mouse iPS cells Stem Cell Rev. 7 2011 948 957
20. R. Darabi, R.W. Arpke, S. Irion, J.T. Dimos, M. Grskovic, M. Kyba, and R.C.R. Perlingeiro Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice Cell Stem Cell 10 2012 610 619
21. M. Denham, C. Bye, J. Leung, B.J. Conley, L.H. Thompson, and M. Dottori Glycogen synthase kinase 3β and activin/nodal inhibition in human embryonic stem cells induces a pre-neuroepithelial state that is required for specification to a floor plate cell lineage Stem Cells 30 2012 2400 2411
22. G. Diez-Roux, S. Banfi, M. Sultan, L. Geffers, S. Anand, D. Rozado, A. Magen, E. Canidio, M. Pagani, and I. Peluso A high-resolution anatomical atlas of the transcriptome in the mouse embryo PLoS Biol. 9 2011 e1000582
23. Y.V. Fedorov, N.C. Jones, and B.B. Olwin Regulation of myogenesis by fibroblast growth factors requires beta-gamma subunits of pertussis toxin-sensitive G proteins Mol. Cell. Biol. 18 1998 5780 5787
24. K. Gauthaman, C.-Y. Fong, and A. Bongso Effect of ROCK inhibitor Y-27632 on normal and variant human embryonic stem cells (hESCs) in vitro: its benefits in hESC expansion Stem Cell Rev. 6 2010 86 95
25. S. Goudenege, C. Lebel, N.B. Huot, C. Dufour, I. Fujii, J. Gekas, J. Rousseau, and J.P. Tremblay Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation Mol. Ther. 20 2012 2153 2167
26. J.K. Hall, G.B. Banks, J.S. Chamberlain, and B.B. Olwin Prevention of muscle aging by myofiber-associated satellite cell transplantation Sci. Transl. Med. 2 2010 57ra83
27. T. Hosoyama, J.V. McGivern, J.M. Van Dyke, A.D. Ebert, and M. Suzuki Derivation of myogenic progenitors directly from human pluripotent stem cells using a sphere-based culture Stem Cells Transl. Med. 3 2014 564 574
28. Y. Hwang, S. Suk, S. Lin, M. Tierney, B. Du, T. Seo, A. Mitchell, A. Sacco, and S. Varghese Directed in vitro myogenesis of human embryonic stem cells and their in vivo engraftment PLoS ONE 8 2013 e72023
29. S.J. Kattman, A.D. Witty, M. Gagliardi, N.C. Dubois, M. Niapour, A. Hotta, J. Ellis, and G. Keller Stage-specific optimization of activin/nodal and BMP signaling promotes cardiac differentiation of mouse and human pluripotent stem cell lines Cell Stem Cell 8 2011 228 240
30. K.A. Kennedy, T. Porter, V. Mehta, S.D. Ryan, F. Price, V. Peshdary, C. Karamboulas, J. Savage, T.A. Drysdale, and S.C. Li Retinoic acid enhances skeletal muscle progenitor formation and bypasses inhibition by bone morphogenetic protein 4 but not dominant negative beta-catenin BMC Biol. 7 2009 67
31. S. Kuang, K. Kuroda, F. Le Grand, and M.A. Rudnicki Asymmetric self-renewal and commitment of satellite stem cells in muscle Cell 129 2007 999 1010
32. X. Lian, C. Hsiao, G. Wilson, K. Zhu, L.B. Hazeltine, S.M. Azarin, K.K. Raval, J. Zhang, T.J. Kamp, and S.P. Palecek Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling Proc. Natl. Acad. Sci. USA 109 2012 E1848 E1857
33. X. Lian, J. Zhang, K. Zhu, T.J. Kamp, and S.P. Palecek Insulin inhibits cardiac mesoderm, not mesendoderm, formation during cardiac differentiation of human pluripotent stem cells and modulation of canonical Wnt signaling can rescue this inhibition Stem Cells 31 2013 447 457
34. P. Liu, M. Wakamiya, M.J. Shea, U. Albrecht, R.R. Behringer, and A. Bradley Requirement for Wnt3 in vertebrate axis formation Nat. Genet. 22 1999 361 365
35. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408
36. G.E. Lyons, S. Schiaffino, D. Sassoon, P. Barton, and M. Buckingham Developmental regulation of myosin gene expression in mouse cardiac muscle J. Cell Biol. 111 1990 2427 2436
37. A.P. Monaghan, K.H. Kaestner, E. Grau, and G. Schütz Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm Development 119 1993 567 578
38. D. Montarras, J. Morgan, C. Collins, F. Relaix, S. Zaffran, A. Cumano, T. Partridge, and M. Buckingham Direct isolation of satellite cells for skeletal muscle regeneration Science 309 2005 2064 2067
39. C.E. Murry, and G. Keller Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development Cell 132 2008 661 680
40. E. Nitzan, and C. Kalcheim Neural crest and somitic mesoderm as paradigms to investigate cell fate decisions during development Dev. Growth Differ. 55 2013 60 78
41. C.P. Ordahl, and N.M. Le Douarin Two myogenic lineages within the developing somite Development 114 1992 339 353
42. H. Petropoulos, and I.S. Skerjanc Beta-catenin is essential and sufficient for skeletal myogenesis in P19 cells J. Biol. Chem. 277 2002 15393 15399
43. M. Pick, L. Azzola, A. Mossman, E.G. Stanley, and A.G. Elefanty Differentiation of human embryonic stem cells in serum-free medium reveals distinct roles for bone morphogenetic protein 4, vascular endothelial growth factor, stem cell factor, and fibroblast growth factor 2 in hematopoiesis Stem Cells 25 2007 2206 2214
44. O. Pourquié, C.M. Fan, M. Coltey, E. Hirsinger, Y. Watanabe, C. Bréant, P. Francis-West, P. Brickell, M. Tessier-Lavigne, and N.M. Le Douarin Lateral and axial signals involved in avian somite patterning: a role for BMP4 Cell 84 1996 461 471
45. C. Pusch, E. Hustert, D. Pfeifer, P. Südbeck, R. Kist, B. Roe, Z. Wang, R. Balling, N. Blin, and G. Scherer The SOX10/Sox10 gene from human and mouse: sequence, expression, and transactivation by the encoded HMG domain transcription factor Hum. Genet. 103 1998 115 123
46. L. Rao, W. Tang, Y. Wei, L. Bao, J. Chen, H. Chen, L. He, P. Lu, J. Ren, and L. Wu Highly efficient derivation of skeletal myotubes from human embryonic stem cells Stem Cell Rev. 8 2012 1109 1119
47. A.C. Rios, O. Serralbo, D. Salgado, and C. Marcelle Neural crest regulates myogenesis through the transient activation of NOTCH Nature 473 2011 532 535
48. J. Rohwedel, V. Maltsev, E. Bober, H.H. Arnold, J. Hescheler, and A.M. Wobus 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. 164 1994 87 101
49. A.J. Rufaihah, N.F. Huang, S. Jamé, J.C. Lee, H.N. Nguyen, B. Byers, A. De, J. Okogbaa, M. Rollins, and R. Reijo-Pera Endothelial cells derived from human iPSCS increase capillary density and improve perfusion in a mouse model of peripheral arterial disease Arterioscler. Thromb. Vasc. Biol. 31 2011 e72 e79
50. T. Ryan, J. Liu, A. Chu, L. Wang, A. Blais, and I.S. Skerjanc Retinoic acid enhances skeletal myogenesis in human embryonic stem cells by expanding the premyogenic progenitor population Stem Cell Rev. 8 2012 482 493
51. H. Sakurai, Y. Okawa, Y. Inami, N. Nishio, and K. Isobe Paraxial mesodermal progenitors derived from mouse embryonic stem cells contribute to muscle regeneration via differentiation into muscle satellite cells Stem Cells 26 2008 1865 1873
52. H. Sasaki, and B.L. Hogan Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo Development 118 1993 47 59
53. Y. Tahamtani, M. Azarnia, A. Farrokhi, A. Sharifi-Zarchi, N. Aghdami, and H. Baharvand Treatment of human embryonic stem cells with different combinations of priming and inducing factors toward definitive endoderm Stem Cells Dev. 22 2013 1419 1432
54. S. Takada, K.L. Stark, M.J. Shea, G. Vassileva, J.A. McMahon, and A.P. McMahon Wnt-3a regulates somite and tailbud formation in the mouse embryo Genes Dev. 8 1994 174 189
55. J.Y. Tan, G. Sriram, A.J. Rufaihah, K.G. Neoh, and T. Cao Efficient derivation of lateral plate and paraxial mesoderm subtypes from human embryonic stem cells through GSKi-mediated differentiation Stem Cells Dev. 22 2013 1893 1906
56. C.E. Thomas, A. Ehrhardt, and M.A. Kay Progress and problems with the use of viral vectors for gene therapy Nat. Rev. Genet. 4 2003 346 358
57. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
58. S. Ueno, G. Weidinger, T. Osugi, A.D. Kohn, J.L. Golob, L. Pabon, H. Reinecke, R.T. Moon, and C.E. Murry Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells Proc. Natl. Acad. Sci. USA 104 2007 9685 9690
59. D.M. Valenzuela, A.N. Economides, E. Rojas, T.M. Lamb, L. Nuñez, P. Jones, N.Y. Lp, R. Espinosa 3rd, C.I. Brannan, and D.J. Gilbert Identification of mammalian noggin and its expression in the adult nervous system J. Neurosci. 15 1995 6077 6084
60. E. Vasyutina, and C. Birchmeier The development of migrating muscle precursor cells Anat. Embryol. (Berl.) 211 Suppl 1 2006 37 41
61. X. Wang, and B. Seed A PCR primer bank for quantitative gene expression analysis Nucleic Acids Res. 31 2003 e154
62. J. Wong, V. Mehta, A. Voronova, J. Coutu, T. Ryan, M. Shelton, and I.S. Skerjanc β-catenin is essential for efficient in vitro premyogenic mesoderm formation but can be partially compensated by retinoic acid signalling PLoS ONE 8 2013 e57501
63. H.B. Wood, and V. Episkopou Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages Mech. Dev. 86 1999 197 201
64. Y. Wu, Z. Ai, K. Yao, L. Cao, J. Du, X. Shi, Z. Guo, and Y. Zhang CHIR99021 promotes self-renewal of mouse embryonic stem cells by modulation of protein-encoding gene and long intergenic non-coding RNA expression Exp. Cell Res. 319 2013 2684 2699
65. C. Xu, M. Tabebordbar, S. Iovino, C. Ciarlo, J. Liu, A. Castiglioni, E. Price, M. Liu, E.R. Barton, and C.R. Kahn A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species Cell 155 2013 909 921