Skeletal muscle cell transplantation: models and methods

Abstract

Xenografts of skeletal muscle are used to study muscle repair and regeneration, mechanisms of muscular dystrophies, and potential cell therapies for musculoskeletal disorders. Typically, xenografting involves using an immunodeficient host that is pre-injured to create a niche for human cell engraftment. Cell type and method of delivery to muscle depend on the specific application, but can include myoblasts, satellite cells, induced pluripotent stem cells, mesangioblasts, immortalized muscle precursor cells, and other multipotent cell lines delivered locally or systemically. Some studies follow cell engraftment with interventions to enhance cell proliferation, migration, and differentiation into mature muscle fibers. Recently, several advances in xenografting human-derived muscle cells have been applied to study and treat Duchenne muscular dystrophy and Facioscapulohumeral muscular dystrophy. Here, we review the vast array of techniques available to aid researchers in designing future experiments aimed at creating robust muscle xenografts in rodent hosts.

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References

  1. Ambrosio F, Ferrari RJ, Fitzgerald GK, Carvell G, Boninger ML, Huard J (2009) Functional overloading of dystrophic mice enhances muscle-derived stem cell contribution to muscle contractile capacity. Arch Phys Med Rehabil 90:66–73

    PubMed  PubMed Central  Google Scholar 

  2. Ambrosio F, Ferrari RJ, Distefano G, Plassmeyer JM, Carvell GE, Deasy BM, Boninger ML, Fitzgerald GK, Huard J (2010) The synergistic effect of treadmill running on stem-cell transplantation to heal injured skeletal muscle. Tissue Eng A 16:839–849

    CAS  Google Scholar 

  3. Arandel L, Polay Espinoza M, Matloka M, Bazinet A, De Dea Diniz D, Naouar N, Rau F, Jollet A, Edom-Vovard F, Mamchaoui K, Tarnopolsky M, Puymirat J, Battail C, Boland A, Deleuze JF, Mouly V, Klein AF, Furling D (2017) Immortalized human myotonic dystrophy muscle cell lines to assess therapeutic compounds. Dis Model Mech 10:487–497

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Arpke RW, Darabi R, Mader TL, Zhang Y, Toyama A, Lonetree CL, Nash N, Lowe DA, Perlingeiro RC, Kyba M (2013) A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells 31:1611–1620

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Asakura A, Seale P, Girgis-Gabardo A, Rudnicki MA (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159:123–134

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Baker HB, Passipieri JA, Siriwardane M, Ellenburg MD, Vadhavkar M, Bergman CR, Saul JM, Tomblyn S, Burnett L, Christ GJ (2017) Cell and growth factor-loaded keratin hydrogels for treatment of volumetric muscle loss in a mouse model. Tissue Eng A 23:572–584

    CAS  Google Scholar 

  7. Barthelemy F, Wein N (2018) Personalized gene and cell therapy for duchenne muscular dystrophy. Neuromuscul Disord 28:803–824

    PubMed  Google Scholar 

  8. Beck AJ, Vitale JM, Zhao Q, Schneider JS, Chang C, Altaf A, Michaels J, Bhaumik M, Grange R, Fraidenraich D (2011) Differential requirement for utrophin in the induced pluripotent stem cell correction of muscle versus fat in muscular dystrophy mice. PLoS ONE 6:e20065

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Benabdallah BF, Bouchentouf M, Rousseau J, Bigey P, Michaud A, Chapdelaine P, Scherman D, Tremblay JP (2008) Inhibiting myostatin with follistatin improves the success of myoblast transplantation in dystrophic mice. Cell Transpl 17:337–350

    Google Scholar 

  10. Benchaouir R, Meregalli M, Farini A, D’Antona G, Belicchi M, Goyenvalle A, Battistelli M, Bresolin N, Bottinelli R, Garcia L, Torrente Y (2007) Restoration of human dystrophin following transplantation of exon-skipping-engineered DMD patient stem cells into dystrophic mice. Cell Stem Cell 1:646–657

    CAS  PubMed  Google Scholar 

  11. Bencze M, Negroni E, Vallese D, Yacoub-Youssef H, Chaouch S, Wolff A, Aamiri A, Di Santo JP, Chazaud B, Butler-Browne G, Savino W, Mouly V, Riederer I (2012) Proinflammatory macrophages enhance the regenerative capacity of human myoblasts by modifying their kinetics of proliferation and differentiation. Mol Ther 20:2168–2179

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Benedetti S, Uno N, Hoshiya H, Ragazzi M, Ferrari G, Kazuki Y, Moyle LA, Tonlorenzi R, Lombardo A, Chaouch S, Mouly V, Moore M, Popplewell L, Kazuki K, Katoh M, Naldini L, Dickson G, Messina G, Oshimura M, Cossu G, Tedesco FS (2018) Reversible immortalisation enables genetic correction of human muscle progenitors and engineering of next-generation human artificial chromosomes for Duchenne muscular dystrophy. EMBO Mol Med 10:254–275

    CAS  PubMed  Google Scholar 

  13. Boldrin L, Morgan JE (2012) Human satellite cells: identification on human muscle fibres. PLoS Curr 3:Rrn1294

    PubMed  PubMed Central  Google Scholar 

  14. Boldrin L, Neal A, Zammit PS, Muntoni F, Morgan JE (2012) Donor satellite cell engraftment is significantly augmented when the host niche is preserved and endogenous satellite cells are incapacitated. Stem Cells 30:1971–1984

    PubMed  PubMed Central  Google Scholar 

  15. Brimah K, Ehrhardt J, Mouly V, Butler-Browne GS, Partridge TA, Morgan JE (2004) Human muscle precursor cell regeneration in the mouse host is enhanced by growth factors. Hum Gene Ther 15:1109–1124

    CAS  PubMed  Google Scholar 

  16. Burks TN, Cohn RD (2011) Role of TGF-beta signaling in inherited and acquired myopathies. Skelet Muscle 1:19

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Cai WF, Huang W, Wang L, Wang JP, Zhang L, Ashraf M, Wu S, Wang Y (2016) Induced pluripotent stem cells derived muscle progenitors effectively mitigate muscular dystrophy through restoring the dystrophin distribution. J Stem Cell Res Ther 6:1000361

    PubMed  PubMed Central  Google Scholar 

  18. Caiozzo VJ, Giedzinski E, Baker M, Suarez T, Izadi A, Lan M, Cho-Lim J, Tseng BP, Limoli CL (2010) The radiosensitivity of satellite cells: cell cycle regulation, apoptosis and oxidative stress. Radiat Res 174:582–589

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Charville GW, Cheung TH, Yoo B, Santos PJ, Lee GK, Shrager JB, Rando TA (2015) Ex vivo expansion and in vivo self-renewal of human muscle stem cells. Stem Cell Rep 5:621–632

    CAS  Google Scholar 

  20. Chen JC, King OD, Zhang Y, Clayton NP, Spencer C, Wentworth BM, Emerson CP Jr, Wagner KR (2016) Morpholino-mediated knockdown of DUX4 toward facioscapulohumeral muscular dystrophy therapeutics. Mol Ther 24:1405–1411

    PubMed  PubMed Central  Google Scholar 

  21. Chicha L, Tussiwand R, Traggiai E, Mazzucchelli L, Bronz L, Piffaretti JC, Lanzavecchia A, Manz MG (2005) Human adaptive immune system Rag2-/-gamma(c)-/- mice. Ann N Y Acad Sci 1044:236–243

    CAS  PubMed  Google Scholar 

  22. Chien KY, Chiang CM, Hseu YC, Vyas AA, Rule GS, Wu W (1994) Two distinct types of cardiotoxin as revealed by the structure and activity relationship of their interaction with zwitterionic phospholipid dispersions. J Biol Chem 269:14473–14483

    CAS  PubMed  Google Scholar 

  23. Chirieleison SM, Feduska JM, Schugar RC, Askew Y, Deasy BM (2012) Human muscle-derived cell populations isolated by differential adhesion rates: phenotype and contribution to skeletal muscle regeneration in Mdx/SCID mice. Tissue Eng A 18:232–241

    CAS  Google Scholar 

  24. Cooper RN, Irintchev A, Di Santo JP, Zweyer M, Morgan JE, Partridge TA, Butler-Browne GS, Mouly V, Wernig A (2001) A new immunodeficient mouse model for human myoblast transplantation. Hum Gene Ther 12:823–831

    CAS  PubMed  Google Scholar 

  25. Cooper RN, Thiesson D, Furling D, Di Santo JP, Butler-Browne GS, Mouly V (2003) Extended amplification in vitro and replicative senescence: key factors implicated in the success of human myoblast transplantation. Hum Gene Ther 14:1169–1179

    CAS  PubMed  Google Scholar 

  26. Cudre-Mauroux C, Occhiodoro T, Konig S, Salmon P, Bernheim L, Trono D (2003) Lentivector-mediated transfer of Bmi-1 and telomerase in muscle satellite cells yields a duchenne myoblast cell line with long-term genotypic and phenotypic stability. Hum Gene Ther 14:1525–1533

    CAS  PubMed  Google Scholar 

  27. Danisovic L, Culenova M, Csobonyeiova M (2018) Induced pluripotent stem cells for duchenne muscular dystrophy modeling and therapy. Cells 7:253

    CAS  PubMed Central  Google Scholar 

  28. Darabi R, Pan W, Bosnakovski D, Baik J, Kyba M, Perlingeiro RC (2011) Functional myogenic engraftment from mouse iPS cells. Stem Cell Rev 7:948–957

    PubMed Central  Google Scholar 

  29. Daxinger L, Tapscott SJ, van der Maarel SM (2015) Genetic and epigenetic contributors to FSHD. Curr Opin Genet Dev 33:56–61

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Decary S, Mouly V, Hamida CB, Sautet A, Barbet JP, Butler-Browne GS (1997) Replicative potential and telomere length in human skeletal muscle: implications for satellite cell-mediated gene therapy. Hum Gene Ther 8:1429–1438

    CAS  PubMed  Google Scholar 

  31. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9:255–267

    CAS  PubMed  Google Scholar 

  32. Dellavalle A, Maroli G, Covarello D, Azzoni E, Innocenzi A, Perani L, Antonini S, Sambasivan R, Brunelli S, Tajbakhsh S, Cossu G (2011) Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat Commun 2:499

    CAS  PubMed  Google Scholar 

  33. DeSimone AM, Pakula A, Lek A, Emerson CP Jr (2017) Facioscapulohumeral muscular dystrophy. Compr Physiol 7:1229–1279

    PubMed  Google Scholar 

  34. Ehrhardt J, Brimah K, Adkin C, Partridge T, Morgan J (2007) Human muscle precursor cells give rise to functional satellite cells in vivo. Neuromuscul Disord 17:631–638

    PubMed  Google Scholar 

  35. Eidahl JO, Giesige CR, Domire JS, Wallace LM, Fowler AM, Guckes SM, Garwick-Coppens SE, Labhart P, Harper SQ (2016) Mouse Dux is myotoxic and shares partial functional homology with its human paralog DUX4. Hum Mol Genet 25:4577–4589

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Fakhfakh R, Michaud A, Tremblay JP (2011) Blocking the myostatin signal with a dominant negative receptor improves the success of human myoblast transplantation in dystrophic mice. Mol Ther 19:204–210

    CAS  PubMed  Google Scholar 

  37. Fakhfakh R, Lamarre Y, Skuk D, Tremblay JP (2012a) Losartan enhances the success of myoblast transplantation. Cell Transplant 21:139–152

    PubMed  Google Scholar 

  38. Fakhfakh R, Lee SJ, Tremblay JP (2012b) Administration of a soluble activin type IIB receptor promotes the transplantation of human myoblasts in dystrophic mice. Cell Transplant 21:1419–1430

    PubMed  PubMed Central  Google Scholar 

  39. Farini A, Meregalli M, Belicchi M, Battistelli M, Parolini D, D’Antona G, Gavina M, Ottoboni L, Constantin G, Bottinelli R, Torrente Y (2007) T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse. J Pathol 213:229–238

    CAS  PubMed  Google Scholar 

  40. Fishman JM, Tyraskis A, Maghsoudlou P, Urbani L, Totonelli G, Birchall MA, De Coppi P (2013) Skeletal muscle tissue engineering: which cell to use? Tissue Eng B Rev 19:503–515

    CAS  Google Scholar 

  41. Gavina M, Belicchi M, Rossi B, Ottoboni L, Colombo F, Meregalli M, Battistelli M, Forzenigo L, Biondetti P, Pisati F, Parolini D, Farini A, Issekutz AC, Bresolin N, Rustichelli F, Constantin G, Torrente Y (2006) VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133 + stem cells after intra-arterial transplantation. Blood 108:2857–2866

    CAS  PubMed  Google Scholar 

  42. Gerard C, Forest MA, Beauregard G, Skuk D, Tremblay JP (2012) Fibrin gel improves the survival of transplanted myoblasts. Cell Transpl 21:127–137

    Google Scholar 

  43. Goldman JP, Blundell MP, Lopes L, Kinnon C, Di Santo JP, Thrasher AJ (1998) Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain. Br J Haematol 103:335–342

    CAS  PubMed  Google Scholar 

  44. Goudenege S, Lebel C, Huot NB, Dufour C, Fujii I, Gekas J, Rousseau J, Tremblay JP (2012) Myoblasts derived from normal hESCs and dystrophic hiPSCs efficiently fuse with existing muscle fibers following transplantation. Mol Ther 20:2153–2167

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Gross JG, Bou-Gharios G, Morgan JE (1999) Potentiation of myoblast transplantation by host muscle irradiation is dependent on the rate of radiation delivery. Cell Tissue Res 298:371–375

    CAS  PubMed  Google Scholar 

  46. Guigal N, Rodriguez M, Cooper RN, Dromaint S, Di Santo JP, Mouly V, Boutin JA, Galizzi JP (2002) Uncoupling protein-3 (UCP3) mRNA expression in reconstituted human muscle after myoblast transplantation in RAG2-/-/gamma c/C5(-) immunodeficient mice. J Biol Chem 277:47407–47411

    CAS  PubMed  Google Scholar 

  47. Hagan M, Ashraf M, Kim IM, Weintraub NL, Tang Y (2018) Effective regeneration of dystrophic muscle using autologous iPSC-derived progenitors with CRISPR-Cas9 mediated precise correction. Med Hypotheses 110:97–100

    CAS  PubMed  Google Scholar 

  48. Hall MN, Hall JK, Cadwallader AB, Pawlikowski BT, Doles JD, Elston TL, Olwin BB (2017) Transplantation of Skeletal Muscle Stem Cells. Methods Mol Biol 1556:237–244

    PubMed  Google Scholar 

  49. Halum SL, Hiatt KK, Naidu M, Sufyan AS, Clapp DW (2008) Optimization of autologous muscle stem cell survival in the denervated hemilarynx. Laryngoscope 118:1308–1312

    PubMed  Google Scholar 

  50. Hamel J, Tawil R (2018) Facioscapulohumeral muscular dystrophy: update on pathogenesis and future treatments. Neurotherapeutics 15:863–871

    PubMed  PubMed Central  Google Scholar 

  51. Hardy D, Besnard A, Latil M, Jouvion G, Briand D, Thepenier C, Pascal Q, Guguin A, Gayraud-Morel B, Cavaillon JM, Tajbakhsh S, Rocheteau P, Chretien F (2016) Comparative study of injury models for studying muscle regeneration in mice. PLoS ONE 11:e0147198

    PubMed  PubMed Central  Google Scholar 

  52. Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113(Pt 12):2299–2308

    CAS  PubMed  Google Scholar 

  53. Himeda CL, Jones TI, Virbasius CM, Zhu LJ, Green MR, Jones PL (2018) Identification of epigenetic regulators of DUX4-fl for targeted therapy of facioscapulohumeral muscular dystrophy. Mol Ther 26:1797–1807

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Hodges SJ, Agbaji AS, Harvey AL, Hider RC (1987) Cobra cardiotoxins. Purification, effects on skeletal muscle and structure/activity relationships [published errtum appears in Eur J Biochem 1988 Feb 1;171(3):727]. Eur J Biochem 165:373–383

    CAS  PubMed  Google Scholar 

  55. Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928

    CAS  PubMed  Google Scholar 

  56. Huard J, Verreault S, Roy R, Tremblay M, Tremblay JP (1994) High efficiency of muscle regeneration after human myoblast clone transplantation in SCID mice. J Clin Invest 93:586–599

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Incitti T, Magli A, Darabi R, Yuan C, Lin K, Arpke RW, Azzag K, Yamamoto A, Stewart R, Thomson JA, Kyba M, Perlingeiro RCR (2019) Pluripotent stem cell-derived myogenic progenitors remodel their molecular signature upon in vivo engraftment. Proc Natl Acad Sci USA 116(10):4346–4351

    CAS  PubMed  Google Scholar 

  58. Ishii K, Sakurai H, Suzuki N, Mabuchi Y, Sekiya I, Sekiguchi K, Akazawa C (2018) Recapitulation of extracellular LAMININ environment maintains stemness of satellite cells in vitro. Stem Cell Rep 10:568–582

    CAS  Google Scholar 

  59. Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397:164–168

    CAS  PubMed  Google Scholar 

  60. Jiwlawat N, Lynch EM, Napiwocki BN, Stempien A, Ashton RS, Kamp TJ, Crone WC, Suzuki M (2019) Micropatterned substrates with physiological stiffness promote cell maturation and Pompe disease phenotype in human induced pluripotent stem cell-derived skeletal myocytes. Biotechnol Bioeng. https://doi.org/10.1002/bit.27075

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kim J, Lee J (2017) Role of transforming growth factor-beta in muscle damage and regeneration: focused on eccentric muscle contraction. J Exerc Rehabil 13:621–626

    PubMed  PubMed Central  Google Scholar 

  62. Kim JH, Ko IK, Atala A, Yoo JJ (2016) Progressive muscle cell delivery as a solution for volumetric muscle defect repair. Sci Rep 6:38754

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Kim EY, Barefield DY, Vo AH, Gacita AM, Schuster EJ, Wyatt EJ, Davis JL, Dong B, Sun C, Page P, Dellefave-Castillo L, Demonbreun A, Zhang HF, McNally EM (2019) Distinct pathological signatures in human cellular models of myotonic dystrophy subtypes. JCI Insight 4:e122686

    PubMed Central  Google Scholar 

  64. Kuhn MA, Black AB, Siddiqui MT, Nolta JA, Belafsky PC (2017) Novel murine xenograft model for the evaluation of stem cell therapy for profound dysphagia. Laryngoscope 127:E359-e63

    Google Scholar 

  65. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, Dupras SK, Reinecke H, Xu C, Hassanipour M, Police S, O’Sullivan C, Collins L, Chen Y, Minami E, Gill EA, Ueno S, Yuan C, Gold J, Murry CE (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015–1024

    CAS  PubMed  Google Scholar 

  66. Lavasani M, Lu A, Thompson SD, Robbins PD, Huard J, Niedernhofer LJ (2013) Isolation of muscle-derived stem/progenitor cells based on adhesion characteristics to collagen-coated surfaces. Methods Mol Biol 976:53–65

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Lavasani M, Thompson SD, Pollett JB, Usas A, Lu A, Stolz DB, Clark KA, Sun B, Peault B, Huard J (2014) Human muscle-derived stem/progenitor cells promote functional murine peripheral nerve regeneration. J Clin Invest 124:1745–1756

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Lee KY, Peters MC, Anderson KW, Mooney DJ (2000) Controlled growth factor release from synthetic extracellular matrices. Nature 408:998–1000

    CAS  PubMed  Google Scholar 

  69. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D’Amore PA, Langer R (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23:879–884

    CAS  PubMed  Google Scholar 

  70. Li HL, Fujimoto N, Sasakawa N, Shirai S, Ohkame T, Sakuma T, Tanaka M, Amano N, Watanabe A, Sakurai H, Yamamoto T, Yamanaka S, Hotta A (2015) Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Rep 4:143–154

    CAS  Google Scholar 

  71. Liu X, Liu Y, Zhao L, Zeng Z, Xiao W, Chen P (2017) Macrophage depletion impairs skeletal muscle regeneration: the roles of regulatory factors for muscle regeneration. Cell Biol Int 41:228–238

    CAS  PubMed  Google Scholar 

  72. Liu X, Zeng Z, Zhao L, Xiao W, Chen P (2018) Changes in inflammatory and oxidative stress factors and the protein synthesis pathway in injured skeletal muscle after contusion. Exp Ther Med 15:2196–2202

    CAS  PubMed  Google Scholar 

  73. Liu X, Zhen L, Zhou Y, Chen Y, Chen P, Xiao W (2019) BMSC transplantation aggravates inflammation, oxidative stress, and fibrosis and impairs skeletal muscle regeneration. Front Physiol 10:87

    PubMed  PubMed Central  Google Scholar 

  74. Loperfido M, Steele-Stallard HB, Tedesco FS, VandenDriessche T (2015) Pluripotent stem cells for gene therapy of degenerative muscle diseases. Curr Gene Ther 15:364–380

    CAS  PubMed  Google Scholar 

  75. Lorant J, Saury C, Schleder C, Robriquet F, Lieubeau B, Negroni E, Leroux I, Chabrand L, Viau S, Babarit C, Ledevin M, Dubreil L, Hamel A, Magot A, Thorin C, Guevel L, Delorme B, Pereon Y, Butler-Browne G, Mouly V, Rouger K (2018) Skeletal muscle regenerative potential of human mustem cells following transplantation into injured mice muscle. Mol Ther 26:618–633

    CAS  PubMed  Google Scholar 

  76. Lovik M (1995) The SCID (severe combined immunodeficiency) mouse–its biology and use in immunotoxicological research. Arch Toxicol Suppl 17:455–467

    CAS  PubMed  Google Scholar 

  77. Maffioletti SM, Noviello M, English K, Tedesco FS (2014) Stem cell transplantation for muscular dystrophy: the challenge of immune response. Biomed Res Int 2014:964010

    PubMed  PubMed Central  Google Scholar 

  78. Mamchaoui K, Trollet C, Bigot A, Negroni E, Chaouch S, Wolff A, Kandalla PK, Marie S, Di Santo J, St Guily JL, Muntoni F, Kim J, Philippi S, Spuler S, Levy N, Blumen SC, Voit T, Wright WE, Aamiri A, Butler-Browne G, Mouly V (2011) Immortalized pathological human myoblasts: towards a universal tool for the study of neuromuscular disorders. Skelet Muscle 1:34

    PubMed  PubMed Central  Google Scholar 

  79. Martinez-Sarra E, Montori S, Gil-Recio C, Nunez-Toldra R, Costamagna D, Rotini A, Atari M, Luttun A, Sampaolesi M (2017) Human dental pulp pluripotent-like stem cells promote wound healing and muscle regeneration. Stem Cell Res Ther 8:175

    PubMed  PubMed Central  Google Scholar 

  80. McGreevy JW, Hakim CH, McIntosh MA, Duan D (2015) Animal models of Duchenne muscular dystrophy: from basic mechanisms to gene therapy. Dis Model Mech 8:195–213

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Meng J, Adkin CF, Xu SW, Muntoni F, Morgan JE (2011) Contribution of human muscle-derived cells to skeletal muscle regeneration in dystrophic host mice. PLoS ONE 6:e17454

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Meng J, Chun S, Asfahani R, Lochmuller H, Muntoni F, Morgan J (2014) Human skeletal muscle-derived CD133(+) cells form functional satellite cells after intramuscular transplantation in immunodeficient host mice. Mol Ther 22:1008–1017

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Meng J, Bencze M, Asfahani R, Muntoni F, Morgan JE (2015) The effect of the muscle environment on the regenerative capacity of human skeletal muscle stem cells. Skelet Muscle 5:11

    PubMed  PubMed Central  Google Scholar 

  84. Meng J, Muntoni F, Morgan J (2018) CD133 + cells derived from skeletal muscles of Duchenne muscular dystrophy patients have a compromised myogenic and muscle regenerative capability. Stem Cell Res 30:43–52

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Mir R, Sinha M, Sharma S, Singh N, Kaur P, Srinivasan A, Singh TP (2008) Isolation, purification, crystallization and preliminary crystallographic studies of sagitoxin, an oligomeric cardiotoxin from the venom of Naja naja saggitifera. Acta Crystallogr F 64:545–547

    CAS  Google Scholar 

  86. Mizuno Y, Chang H, Umeda K, Niwa A, Iwasa T, Awaya T, Fukada S, Yamamoto H, Yamanaka S, Nakahata T, Heike T (2010) Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. Faseb J 24:2245–2253

    CAS  PubMed  Google Scholar 

  87. Mokri B, Engel AG (1975) Duchenne dystrophy: electron microscopic findings pointing to a basic or early abnormality in the plasma membrane of the muscle fiber. Neurology 25:1111–1120

    CAS  PubMed  Google Scholar 

  88. Morgan JE, Hoffman EP, Partridge TA (1990) Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J Cell Biol 111:2437–2449

    CAS  PubMed  Google Scholar 

  89. Morgan JE, Gross JG, Pagel CN, Beauchamp JR, Fassati A, Thrasher AJ, Di Santo JP, Fisher IB, Shiwen X, Abraham DJ, Partridge TA (2002) Myogenic cell proliferation and generation of a reversible tumorigenic phenotype are triggered by preirradiation of the recipient site. J Cell Biol 157:693–702

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Morosetti R, Mirabella M, Gliubizzi C, Broccolini A, Sancricca C, Pescatori M, Gidaro T, Tasca G, Frusciante R, Tonali PA, Cossu G, Ricci E (2007) Isolation and characterization of mesoangioblasts from facioscapulohumeral muscular dystrophy muscle biopsies. Stem Cells 25:3173–3182

    CAS  PubMed  Google Scholar 

  91. Morosetti R, Gidaro T, Broccolini A, Gliubizzi C, Sancricca C, Tonali PA, Ricci E, Mirabella M (2011) Mesoangioblasts from facioscapulohumeral muscular dystrophy display in vivo a variable myogenic ability predictable by their in vitro behavior. Cell Transpl 20:1299–1313

    Google Scholar 

  92. Morrison J, Lu QL, Pastoret C, Partridge T, Bou-Gharios G (2000) T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab Invest 80:881–891

    CAS  PubMed  Google Scholar 

  93. Mouly V, Aamiri A, Perie S, Mamchaoui K, Barani A, Bigot A, Bouazza B, Francois V, Furling D, Jacquemin V, Negroni E, Riederer I, Vignaud A, St Guily JL, Butler-Browne GS (2005) Myoblast transfer therapy: is there any light at the end of the tunnel? Acta Myol 24:128–133

    CAS  PubMed  Google Scholar 

  94. Mueller AL, O’Neill A, Jones TI, Llach A, Rojas LA, Sakellariou P, Stadler G, Wright WE, Eyerman D, Jones PL, Bloch RJ (2019) Muscle xenografts reproduce key molecular features of facioscapulohumeral muscular dystrophy. Exp Neurol 320:113011

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Nakajima T, Sakurai H, Ikeya M (2019) In vitro generation of somite derivatives from human induced pluripotent stem cells. J Vis Exp 146:e59359

    Google Scholar 

  96. Negroni E, Riederer I, Chaouch S, Belicchi M, Razini P, Di Santo J, Torrente Y, Butler-Browne GS, Mouly V (2009) In vivo myogenic potential of human CD133 + muscle-derived stem cells: a quantitative study. Mol Ther 17:1771–1778

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Negroni E, Gidaro T, Bigot A, Butler-Browne GS, Mouly V, Trollet C (2015) Invited review: stem cells and muscle diseases: advances in cell therapy strategies. Neuropathol Appl Neurobiol 41:270–287

    CAS  PubMed  Google Scholar 

  98. O’Connor MS, Carlson ME, Conboy IM (2009) Differentiation rather than aging of muscle stem cells abolishes their telomerase activity. Biotechnol Prog 25:1130–1137

    PubMed  PubMed Central  Google Scholar 

  99. Pareja-Galeano H, Sanchis-Gomar F, Emanuele E, Gallardo ME, Lucia A (2016) IPSCs, a promising tool to restore muscle atrophy. J Cell Physiol 231:259–260

    CAS  PubMed  Google Scholar 

  100. Partridge TA, Morgan JE, Coulton GR, Hoffman EP, Kunkel LM (1989) Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337:176–179

    CAS  PubMed  Google Scholar 

  101. Pearson T, Shultz LD, Miller D, King M, Laning J, Fodor W, Cuthbert A, Burzenski L, Gott B, Lyons B, Foreman O, Rossini AA, Greiner DL (2008) Non-obese diabetic-recombination activating gene-1 (NOD-Rag1 null) interleukin (IL)-2 receptor common gamma chain (IL2r gamma null) null mice: a radioresistant model for human lymphohaematopoietic engraftment. Clin Exp Immunol 154:270–284

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Piga D, Salani S, Magri F, Brusa R, Mauri E, Comi GP, Bresolin N, Corti S (2019) Human induced pluripotent stem cell models for the study and treatment of Duchenne and Becker muscular dystrophies. Ther Adv Neurol Disord 12:1756286419833478

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Porter GA, Dmytrenko GM, Winkelmann JC, Bloch RJ (1992) Dystrophin colocalizes with beta-spectrin in distinct subsarcolemmal domains in mammalian skeletal muscle. J Cell Biol 117:997–1005

    CAS  PubMed  Google Scholar 

  104. Pourquie O, Al Tanoury Z, Chal J (2018) The long road to making muscle in vitro. Curr Top Dev Biol 129:123–142

    CAS  PubMed  Google Scholar 

  105. Quenneville SP, Tremblay JP (2006) Ex vivo modification of cells to induce a muscle-based expression. Curr Gene Ther 6:625–632

    CAS  PubMed  Google Scholar 

  106. Rao L, Qian Y, Khodabukus A, Ribar T, Bursac N (2018) Engineering human pluripotent stem cells into a functional skeletal muscle tissue. Nat Commun 9:126

    PubMed  PubMed Central  Google Scholar 

  107. Reimann J, Brimah K, Schroder R, Wernig A, Beauchamp JR, Partridge TA (2004) Pax7 distribution in human skeletal muscle biopsies and myogenic tissue cultures. Cell Tissue Res 315:233–242

    PubMed  Google Scholar 

  108. Richardson TP, Peters MC, Ennett AB, Mooney DJ (2001) Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029–1034

    CAS  PubMed  Google Scholar 

  109. Riederer I, Negroni E, Bigot A, Bencze M, Di Santo J, Aamiri A, Butler-Browne G, Mouly V (2008) Heat shock treatment increases engraftment of transplanted human myoblasts into immunodeficient mice. Transpl Proc 40:624–630

    CAS  Google Scholar 

  110. Riederer I, Negroni E, Bencze M, Wolff A, Aamiri A, Di Santo JP, Silva-Barbosa SD, Butler-Browne G, Savino W, Mouly V (2012) Slowing down differentiation of engrafted human myoblasts into immunodeficient mice correlates with increased proliferation and migration. Mol Ther 20:146–154

    CAS  PubMed  Google Scholar 

  111. Rodriguez AM, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne JY, Wdziekonski B, Villageois A, Bagnis C, Breittmayer JP, Groux H, Ailhaud G, Dani C (2005) Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 201:1397–1405

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Rozkalne A, Adkin C, Meng J, Lapan A, Morgan JE, Gussoni E (2014) Mouse regenerating myofibers detected as false-positive donor myofibers with anti-human spectrin. Hum Gene Ther 25:73–81

    CAS  PubMed  Google Scholar 

  113. Sacco A, Doyonnas R, Kraft P, Vitorovic S, Blau HM (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456:502–506

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Sakellariou P, O’Neill A, Mueller AL, Stadler G, Wright WE, Roche JA, Bloch RJ (2016) Neuromuscular electrical stimulation promotes development in mice of mature human muscle from immortalized human myoblasts. Skelet Muscle 6:4

    PubMed  PubMed Central  Google Scholar 

  115. Salani S, Donadoni C, Rizzo F, Bresolin N, Comi GP, Corti S (2012) Generation of skeletal muscle cells from embryonic and induced pluripotent stem cells as an in vitro model and for therapy of muscular dystrophies. J Cell Mol Med 16:1353–1364

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Saxena AK, Marler J, Benvenuto M, Willital GH, Vacanti JP (1999) Skeletal muscle tissue engineering using isolated myoblasts on synthetic biodegradable polymers: preliminary studies. Tissue Eng 5:525–532

    CAS  PubMed  Google Scholar 

  117. Schafer R, Knauf U, Zweyer M, Hogemeier O, de Guarrini F, Liu X, Eichhorn HJ, Koch FW, Mundegar RR, Erzen I, Wernig A (2006) Age dependence of the human skeletal muscle stem cell in forming muscle tissue. Artif Organs 30:130–140

    PubMed  Google Scholar 

  118. Sharma V, Harafuji N, Belayew A, Chen YW (2013) DUX4 differentially regulates transcriptomes of human rhabdomyosarcoma and mouse C2C12 cells. PLoS ONE 8:e64691

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Shimizu-Motohashi Y, Miyatake S, Komaki H, Takeda S, Aoki Y (2016) Recent advances in innovative therapeutic approaches for Duchenne muscular dystrophy: from discovery to clinical trials. Am J Transl Res 8:2471–2489

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Shimizu-Motohashi Y, Komaki H, Motohashi N, Takeda S, Yokota T, Aoki Y (2019) Restoring dystrophin expression in duchenne muscular dystrophy: current status of therapeutic approaches. J Pers Med 9:1

    PubMed Central  Google Scholar 

  121. Silva-Barbosa SD, Butler-Browne GS, Di Santo JP, Mouly V (2005) Comparative analysis of genetically engineered immunodeficient mouse strains as recipients for human myoblast transplantation. Cell Transpl 14:457–467

    Google Scholar 

  122. Silva-Barbosa SD, Butler-Browne GS, de Mello W, Riederer I, Di Santo JP, Savino W, Mouly V (2008) Human myoblast engraftment is improved in laminin-enriched microenvironment. Transplantation 85:566–575

    PubMed  Google Scholar 

  123. Skuk D, Tremblay JP (2015) Cell therapy in muscular dystrophies: many promises in mice and dogs, few facts in patients. Expert Opin Biol Ther 15:1307–1319

    PubMed  Google Scholar 

  124. Skuk D, Furling D, Bouchard JP, Goulet M, Roy B, Lacroix Y, Vilquin JT, Tremblay JP, Puymirat J (1999) Transplantation of human myoblasts in SCID mice as a potential muscular model for myotonic dystrophy. J Neuropathol Exp Neurol 58:921–931

    CAS  PubMed  Google Scholar 

  125. Smythe GM, Hodgetts SI, Grounds MD (2000) Immunobiology and the future of myoblast transfer therapy. Mol Ther 1:304–313

    CAS  PubMed  Google Scholar 

  126. Stadler G, Chen JC, Wagner K, Robin JD, Shay JW, Emerson CP Jr, Wright WE (2011) Establishment of clonal myogenic cell lines from severely affected dystrophic muscles—CDK4 maintains the myogenic population. Skelet Muscle 1:12

    PubMed  PubMed Central  Google Scholar 

  127. Steele-Stallard HB, Pinton L, Sarcar S, Ozdemir T, Maffioletti SM, Zammit PS, Tedesco FS (2018) Modeling skeletal muscle laminopathies using human induced pluripotent stem cells carrying pathogenic LMNA mutations. Front Physiol 9:1332

    PubMed  PubMed Central  Google Scholar 

  128. Swartz EW, Baek J, Pribadi M, Wojta KJ, Almeida S, Karydas A, Gao FB, Miller BL, Coppola G (2016) A novel protocol for directed differentiation of C9orf72-associated human induced pluripotent stem cells into contractile skeletal myotubes. Stem Cells Transl Med 5:1461–1472

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Tassin A, Laoudj-Chenivesse D, Vanderplanck C, Barro M, Charron S, Ansseau E, Chen YW, Mercier J, Coppee F, Belayew A (2013) DUX4 expression in FSHD muscle cells: how could such a rare protein cause a myopathy? J Cell Mol Med 17:76–89

    CAS  PubMed  Google Scholar 

  130. Tedesco FS, Hoshiya H, D’Antona G, Gerli MF, Messina G, Antonini S, Tonlorenzi R, Benedetti S, Berghella L, Torrente Y, Kazuki Y, Bottinelli R, Oshimura M, Cossu G (2011) Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Sci Transl Med 3:96ra78

    CAS  PubMed  Google Scholar 

  131. Tedesco FS, Gerli MF, Perani L, Benedetti S, Ungaro F, Cassano M, Antonini S, Tagliafico E, Artusi V, Longa E, Tonlorenzi R, Ragazzi M, Calderazzi G, Hoshiya H, Cappellari O, Mora M, Schoser B, Schneiderat P, Oshimura M, Bottinelli R, Sampaolesi M, Torrente Y, Broccoli V, Cossu G (2012) Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4:140ra89

    PubMed  Google Scholar 

  132. Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345–R353

    CAS  PubMed  Google Scholar 

  133. Tidball JG (2011) Mechanisms of muscle injury, repair, and regeneration. Compr Physiol 1:2029–2062

    PubMed  Google Scholar 

  134. Torihashi S, Ho M, Kawakubo Y, Komatsu K, Nagai M, Hirayama Y, Kawabata Y, Takenaka-Ninagawa N, Wanachewin O, Zhuo L, Kimata K (2015) Acute and temporal expression of tumor necrosis factor (TNF)-alpha-stimulated gene 6 product, TSG6, in mesenchymal stem cells creates microenvironments required for their successful transplantation into muscle tissue. J Biol Chem 290:22771–22781

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Torrente Y, Tremblay JP, Pisati F, Belicchi M, Rossi B, Sironi M, Fortunato F, El Fahime M, D’Angelo MG, Caron NJ, Constantin G, Paulin D, Scarlato G, Bresolin N (2001) Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol 152:335–348

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, D’Antona G, Tonlorenzi R, Porretti L, Gavina M, Mamchaoui K, Pellegrino MA, Furling D, Mouly V, Butler-Browne GS, Bottinelli R, Cossu G, Bresolin N (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114:182–195

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Torrente Y, Belicchi M, Marchesi C, D’Antona G, Cogiamanian F, Pisati F, Gavina M, Giordano R, Tonlorenzi R, Fagiolari G, Lamperti C, Porretti L, Lopa R, Sampaolesi M, Vicentini L, Grimoldi N, Tiberio F, Songa V, Baratta P, Prelle A, Forzenigo L, Guglieri M, Pansarasa O, Rinaldi C, Mouly V, Butler-Browne GS, Comi GP, Biondetti P, Moggio M, Gaini SM, Stocchetti N, Priori A, D’Angelo MG, Turconi A, Bottinelli R, Cossu G, Rebulla P, Bresolin N (2007) Autologous transplantation of muscle-derived CD133 + stem cells in Duchenne muscle patients. Cell Transpl 16:563–577

    CAS  Google Scholar 

  138. Urciuolo A, De Coppi P (2018) Decellularized tissue for muscle regeneration. Int J Mol Sci 19:2392

    PubMed Central  Google Scholar 

  139. Vallese D, Negroni E, Duguez S, Ferry A, Trollet C, Aamiri A, Vosshenrich CA, Fuchtbauer EM, Di Santo JP, Vitiello L, Butler-Browne G, Mouly V (2013) The Rag2(-)Il2rb(-)Dmd(-) mouse: a novel dystrophic and immunodeficient model to assess innovating therapeutic strategies for muscular dystrophies. Mol Ther 21:1950–1957

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Vieira NM, Valadares M, Zucconi E, Secco M, Bueno CR Jr, Brandalise V, Assoni A, Gomes J, Landini V, Andrade T, Caetano HV, Vainzof M, Zatz M (2012) Human adipose-derived mesenchymal stromal cells injected systemically into GRMD dogs without immunosuppression are able to reach the host muscle and express human dystrophin. Cell Transpl 21:1407–1417

    CAS  Google Scholar 

  141. Vilquin JT, Marolleau JP, Sacconi S, Garcin I, Lacassagne MN, Robert I, Ternaux B, Bouazza B, Larghero J, Desnuelle C (2005) Normal growth and regenerating ability of myoblasts from unaffected muscles of facioscapulohumeral muscular dystrophy patients. Gene Ther 12:1651–1662

    CAS  PubMed  Google Scholar 

  142. Walsh S, Nygren J, Ponten A, Jovinge S (2011) Myogenic reprogramming of bone marrow derived cells in a W(4)(1)Dmd(mdx) deficient mouse model. PLoS ONE 6:e27500

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Walz PC, Hiatt KK, Naidu M, Halum SL (2008) Characterization of laryngeal muscle stem cell survival and proliferation. Laryngoscope 118:1422–1426

    PubMed  Google Scholar 

  144. Xia G, Terada N, Ashizawa T (2018) Human iPSC models to study orphan diseases: muscular dystrophies. Curr Stem Cell Rep 4:299–309

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Xiao W, Liu Y, Chen P (2016) Macrophage depletion impairs skeletal muscle regeneration: the roles of pro-fibrotic factors, inflammation, and oxidative stress. Inflammation 39:2016–2028

    CAS  PubMed  Google Scholar 

  146. Xu X, Wilschut KJ, Kouklis G, Tian H, Hesse R, Garland C, Sbitany H, Hansen S, Seth R, Knott PD, Hoffman WY, Pomerantz JH (2015) Human satellite cell transplantation and regeneration from diverse skeletal muscles. Stem Cell Rep 5:419–434

    CAS  Google Scholar 

  147. Yang W, Hu P (2018) Skeletal muscle regeneration is modulated by inflammation. J Orthop Transl 13:25–32

    Google Scholar 

  148. Young CS, Hicks MR, Ermolova NV, Nakano H, Jan M, Younesi S, Karumbayaram S, Kumagai-Cresse C, Wang D, Zack JA, Kohn DB, Nakano A, Nelson SF, Miceli MC, Spencer MJ, Pyle AD (2016) A single CRISPR-Cas9 deletion strategy that targets the majority of DMD patients restores dystrophin function in hiPSC-derived muscle cells. Cell Stem Cell 18:533–540

    CAS  PubMed  PubMed Central  Google Scholar 

  149. Zhang Y, King OD, Rahimov F, Jones TI, Ward CW, Kerr JP, Liu N, Emerson CP Jr, Kunkel LM, Partridge TA, Wagner KR (2014) Human skeletal muscle xenograft as a new preclinical model for muscle disorders. Hum Mol Genet 23:3180–3188

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Zhao C, Farruggio AP, Bjornson CR, Chavez CL, Geisinger JM, Neal TL, Karow M, Calos MP (2014) Recombinase-mediated reprogramming and dystrophin gene addition in mdx mouse induced pluripotent stem cells. PLoS ONE 9:e96279

    PubMed  PubMed Central  Google Scholar 

  151. Zhu CH, Mouly V, Cooper RN, Mamchaoui K, Bigot A, Shay JW, Di Santo JP, Butler-Browne GS, Wright WE (2007) Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: consequences in aging muscle and therapeutic strategies for muscular dystrophies. Aging Cell 6:515–523

    CAS  PubMed  Google Scholar 

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Mueller, A.L., Bloch, R.J. Skeletal muscle cell transplantation: models and methods. J Muscle Res Cell Motil 41, 297–311 (2020). https://doi.org/10.1007/s10974-019-09550-w

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Keywords

  • Xenograft
  • Transplantation
  • Muscular dystrophy
  • FSHD
  • Satellite cell
  • Myoblast transfer therapy