Isolation of progenitors that exhibit myogenic/osteogenic bipotency in vitro by fluorescence-activated cell sorting from human fetal muscle

Stem Cell Reports

Volumn 2, Issue 1, 2014, Pages 92-106

  Castiglioni, Alessandra ^a,b,c   Hettmer, Simone ^a,b,d   Lynes, Matthew D ^b   Rao, Tata Nageswara ^a,b   Tchessalova, Daria ^a,b   Sinha, Indranil ^e   Lee, Bernard T ^f   Tseng, Yu Hua ^b   Wagers, Amy J ^a,b  

^a Harvard University   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTE; ARTICLE; BONE; CELL DIFFERENTIATION; CELL ISOLATION; CELL TYPE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; MUSCLE CELL; PRIORITY JOURNAL; SKELETAL MUSCLE; STEM CELL; ADIPOGENESIS; ANIMAL; BONE DEVELOPMENT; CELL CULTURE; CELL LINEAGE; CYTOLOGY; FETUS; FLOW CYTOMETRY; METABOLISM; MOUSE; MUSCLE DEVELOPMENT; STEM CELL TRANSPLANTATION; XENOGRAFT;

ALPHA INTEGRIN; ALPHA7 INTEGRIN; LEUKOCYTE ANTIGEN; PAX7 PROTEIN, HUMAN; TRANSCRIPTION FACTOR PAX7;

ADIPOGENESIS; ANIMALS; ANTIGENS, CD; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; FETUS; FLOW CYTOMETRY; HUMANS; INTEGRIN ALPHA CHAINS; MICE; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; OSTEOGENESIS; PAX7 TRANSCRIPTION FACTOR; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84892608848     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2013.12.006     Document Type: Article

References (40)

1. A. Andukuri, Y.D. Sohn, C.P. Anakwenze, D.J. Lim, B.C. Brott, Y.S. Yoon, and H.W. Jun Enhanced human endothelial progenitor cell adhesion and differentiation by a bioinspired multifunctional nanomatrix Tissue Eng. Part C Methods 19 2013 375 385
2. J.R. Beauchamp, L. Heslop, D.S. Yu, S. Tajbakhsh, R.G. Kelly, A. Wernig, M.E. Buckingham, T.A. Partridge, and P.S. Zammit Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells J. Cell Biol. 151 2000 1221 1234
3. R. Berry, and M.S. Rodeheffer Characterization of the adipocyte cellular lineage in vivo Nat. Cell Biol. 15 2013 302 308
4. D. Bosnakovski, Z. Xu, W. Li, S. Thet, O. Cleaver, R.C. Perlingeiro, and M. Kyba Prospective isolation of skeletal muscle stem cells with a Pax7 reporter Stem Cells 26 2008 3194 3204
5. G. Bulfield, W.G. Siller, P.A. Wight, and K.J. Moore X chromosome-linked muscular dystrophy (mdx) in the mouse Proc. Natl. Acad. Sci. USA 81 1984 1189 1192
6. M. Cerletti, S. Jurga, C.A. Witczak, M.F. Hirshman, J.L. Shadrach, L.J. Goodyear, and A.J. Wagers Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles Cell 134 2008 37 47
7. M. Cerletti, Y.C. Jang, L.W. Finley, M.C. Haigis, and A.J. Wagers Short-term calorie restriction enhances skeletal muscle stem cell function Cell Stem Cell 10 2012 515 519
8. J.V. Chakkalakal, K.M. Jones, M.A. Basson, and A.S. Brack The aged niche disrupts muscle stem cell quiescence Nature 490 2012 355 360
9. I.M. Conboy, M.J. Conboy, G.M. Smythe, and T.A. Rando Notch-mediated restoration of regenerative potential to aged muscle Science 302 2003 1575 1577
10. M.J. Conboy, M. Cerletti, A.J. Wagers, and I.M. Conboy Immuno-analysis and FACS sorting of adult muscle fiber-associated stem/precursor cells Methods Mol. Biol. 621 2010 165 173
11. M. Crisan, L. Casteilla, L. Lehr, M. Carmona, A. Paoloni-Giacobino, S. Yap, B. Sun, B. Léger, A. Logar, and L. Pénicaud et al. A reservoir of brown adipocyte progenitors in human skeletal muscle Stem Cells 26 2008 2425 2433
12. R. Darabi, R.W. Arpke, S. Irion, J.T. Dimos, M. Grskovic, M. Kyba, and R.C. 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
13. S. Doulatov, F. Notta, E. Laurenti, and J.E. Dick Hematopoiesis: a human perspective Cell Stem Cell 10 2012 120 136
14. J. Ehrhardt, K. Brimah, C. Adkin, T. Partridge, and J. Morgan Human muscle precursor cells give rise to functional satellite cells in vivo Neuromuscul. Disord. 17 2007 631 638
15. H. Ema, Y. Morita, S. Yamazaki, A. Matsubara, J. Seita, Y. Tadokoro, H. Kondo, H. Takano, and H. Nakauchi Adult mouse hematopoietic stem cells: purification and single-cell assays Nat. Protoc. 1 2006 2979 2987
16. S. Fukada, S. Higuchi, M. Segawa, K. Koda, Y. Yamamoto, K. Tsujikawa, Y. Kohama, A. Uezumi, M. Imamura, and Y. Miyagoe-Suzuki et al. Purification and cell-surface marker characterization of quiescent satellite cells from murine skeletal muscle by a novel monoclonal antibody Exp. Cell Res. 296 2004 245 255
17. G.E. Glass, J.K. Chan, A. Freidin, M. Feldmann, N.J. Horwood, and J. Nanchahal TNF-alpha promotes fracture repair by augmenting the recruitment and differentiation of muscle-derived stromal cells Proc. Natl. Acad. Sci. USA 108 2011 1585 1590
18. N. Hashimoto, T. Kiyono, M.R. Wada, R. Umeda, Y. Goto, I. Nonaka, S. Shimizu, S. Yasumoto, and M. Inagawa-Ogashiwa Osteogenic properties of human myogenic progenitor cells Mech. Dev. 125 2008 257 269
19. A.W. Joe, L. Yi, A. Natarajan, F. Le Grand, L. So, J. Wang, M.A. Rudnicki, and F.M. Rossi Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis Nat. Cell Biol. 12 2010 153 163
20. 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
21. S. Lecourt, J.P. Marolleau, O. Fromigué, K. Vauchez, R. Andriamanalijaona, B. Ternaux, M.N. Lacassagne, I. Robert, K. Boumédiene, and F. Chéreau et al. Characterization of distinct mesenchymal-like cell populations from human skeletal muscle in situ and in vitro Exp. Cell Res. 316 2010 2513 2526
22. I.W. McKinnell, J. Ishibashi, F. Le Grand, V.G. Punch, G.C. Addicks, J.F. Greenblatt, F.J. Dilworth, and M.A. Rudnicki Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex Nat. Cell Biol. 10 2008 77 84
23. 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
24. T. Oishi, A. Uezumi, A. Kanaji, N. Yamamoto, A. Yamaguchi, H. Yamada, and K. Tsuchida Osteogenic differentiation capacity of human skeletal muscle-derived progenitor cells PLoS ONE 8 2013 e56641
25. Y. Okuno, H. Iwasaki, C.S. Huettner, H.S. Radomska, D.A. Gonzalez, D.G. Tenen, and K. Akashi Differential regulation of the human and murine CD34 genes in hematopoietic stem cells Proc. Natl. Acad. Sci. USA 99 2002 6246 6251
26. M. Osawa, K. Hanada, H. Hamada, and H. Nakauchi Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell Science 273 1996 242 245
27. N. Ozeki, M. Lim, C.C. Yao, M. Tolar, and R.H. Kramer alpha7 integrin expressing human fetal myogenic progenitors have stem cell-like properties and are capable of osteogenic differentiation Exp. Cell Res. 312 2006 4162 4180
28. A. Pasut, P. Oleynik, and M.A. Rudnicki Isolation of muscle stem cells by fluorescence activated cell sorting cytometry Methods Mol. Biol. 798 2012 53 64
29. D.F. Pisani, N. Clement, A. Loubat, M. Plaisant, S. Sacconi, J.Y. Kurzenne, C. Desnuelle, C. Dani, and C.A. Dechesne Hierarchization of myogenic and adipogenic progenitors within human skeletal muscle Stem Cells 28 2010 2182 2194
30. D.F. Pisani, C.A. Dechesne, S. Sacconi, S. Delplace, N. Belmonte, O. Cochet, N. Clement, B. Wdziekonski, A.P. Villageois, and C. Butori et al. Isolation of a highly myogenic CD34-negative subset of human skeletal muscle cells free of adipogenic potential Stem Cells 28 2010 753 764
31. W.J. Racki, L. Covassin, M. Brehm, S. Pino, R. Ignotz, R. Dunn, J. Laning, S.K. Graves, A.A. Rossini, L.D. Shultz, and D.L. Greiner NOD-scid IL2rgamma(null) mouse model of human skin transplantation and allograft rejection Transplantation 89 2010 527 536
32. P. Rocheteau, B. Gayraud-Morel, I. Siegl-Cachedenier, M.A. Blasco, and S. Tajbakhsh A subpopulation of adult skeletal muscle stem cells retains all template DNA strands after cell division Cell 148 2012 112 125
33. A. Sacco, R. Doyonnas, P. Kraft, S. Vitorovic, and H.M. Blau Self-renewal and expansion of single transplanted muscle stem cells Nature 456 2008 502 506
34. P. Seale, L.A. Sabourin, A. Girgis-Gabardo, A. Mansouri, P. Gruss, and M.A. Rudnicki Pax7 is required for the specification of myogenic satellite cells Cell 102 2000 777 786
35. R.I. Sherwood, J.L. Christensen, I.M. Conboy, M.J. Conboy, T.A. Rando, I.L. Weissman, and A.J. Wagers Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle Cell 119 2004 543 554
36. O. Tanaka, H. Shinohara, M. Oguni, and T. Yoshioka Ultrastructure of developing muscle in the upper limbs of the human embryo and fetus Anat. Rec. 241 1995 417 424
37. K.K. Tanaka, J.K. Hall, A.A. Troy, D.D. Cornelison, S.M. Majka, and B.B. Olwin Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration Cell Stem Cell 4 2009 217 225
38. A. Uezumi, S. Fukada, N. Yamamoto, S. Takeda, and K. Tsuchida Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle Nat. Cell Biol. 12 2010 143 152
39. Y.X. Wang, and M.A. Rudnicki Satellite cells, the engines of muscle repair Nat. Rev. Mol. Cell Biol. 13 2012 127 133
40. B. Zheng, B. Cao, M. Crisan, B. Sun, G. Li, A. Logar, S. Yap, J.B. Pollett, L. Drowley, and T. Cassino et al. Prospective identification of myogenic endothelial cells in human skeletal muscle Nat. Biotechnol. 25 2007 1025 1034