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.
Similar content being viewed by others
References
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
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
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
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
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
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
Barthelemy F, Wein N (2018) Personalized gene and cell therapy for duchenne muscular dystrophy. Neuromuscul Disord 28:803–824
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
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
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
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
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
Boldrin L, Morgan JE (2012) Human satellite cells: identification on human muscle fibres. PLoS Curr 3:Rrn1294
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
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
Burks TN, Cohn RD (2011) Role of TGF-beta signaling in inherited and acquired myopathies. Skelet Muscle 1:19
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
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
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
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
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
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
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
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
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
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
Danisovic L, Culenova M, Csobonyeiova M (2018) Induced pluripotent stem cells for duchenne muscular dystrophy modeling and therapy. Cells 7:253
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
Daxinger L, Tapscott SJ, van der Maarel SM (2015) Genetic and epigenetic contributors to FSHD. Curr Opin Genet Dev 33:56–61
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
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
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
DeSimone AM, Pakula A, Lek A, Emerson CP Jr (2017) Facioscapulohumeral muscular dystrophy. Compr Physiol 7:1229–1279
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
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
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
Fakhfakh R, Lamarre Y, Skuk D, Tremblay JP (2012a) Losartan enhances the success of myoblast transplantation. Cell Transplant 21:139–152
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
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
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
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
Gerard C, Forest MA, Beauregard G, Skuk D, Tremblay JP (2012) Fibrin gel improves the survival of transplanted myoblasts. Cell Transpl 21:127–137
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
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
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
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
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
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
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
Hamel J, Tawil R (2018) Facioscapulohumeral muscular dystrophy: update on pathogenesis and future treatments. Neurotherapeutics 15:863–871
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
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
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
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
Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928
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
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
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
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
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
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
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
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
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
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
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
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
Lee KY, Peters MC, Anderson KW, Mooney DJ (2000) Controlled growth factor release from synthetic extracellular matrices. Nature 408:998–1000
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
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
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
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
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
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
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
Lovik M (1995) The SCID (severe combined immunodeficiency) mouse–its biology and use in immunotoxicological research. Arch Toxicol Suppl 17:455–467
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Nakajima T, Sakurai H, Ikeya M (2019) In vitro generation of somite derivatives from human induced pluripotent stem cells. J Vis Exp 146:e59359
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
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
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
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
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
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
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
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
Pourquie O, Al Tanoury Z, Chal J (2018) The long road to making muscle in vitro. Curr Top Dev Biol 129:123–142
Quenneville SP, Tremblay JP (2006) Ex vivo modification of cells to induce a muscle-based expression. Curr Gene Ther 6:625–632
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
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
Richardson TP, Peters MC, Ennett AB, Mooney DJ (2001) Polymeric system for dual growth factor delivery. Nat Biotechnol 19:1029–1034
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
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
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
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
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
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
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
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
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
Sharma V, Harafuji N, Belayew A, Chen YW (2013) DUX4 differentially regulates transcriptomes of human rhabdomyosarcoma and mouse C2C12 cells. PLoS ONE 8:e64691
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
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
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
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
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
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
Smythe GM, Hodgetts SI, Grounds MD (2000) Immunobiology and the future of myoblast transfer therapy. Mol Ther 1:304–313
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
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
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
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
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
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
Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:R345–R353
Tidball JG (2011) Mechanisms of muscle injury, repair, and regeneration. Compr Physiol 1:2029–2062
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
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
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
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
Urciuolo A, De Coppi P (2018) Decellularized tissue for muscle regeneration. Int J Mol Sci 19:2392
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
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
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
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
Walz PC, Hiatt KK, Naidu M, Halum SL (2008) Characterization of laryngeal muscle stem cell survival and proliferation. Laryngoscope 118:1422–1426
Xia G, Terada N, Ashizawa T (2018) Human iPSC models to study orphan diseases: muscular dystrophies. Curr Stem Cell Rep 4:299–309
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
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
Yang W, Hu P (2018) Skeletal muscle regeneration is modulated by inflammation. J Orthop Transl 13:25–32
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
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
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
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
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10974-019-09550-w