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Pluripotent Stem Cells for Gene Therapy of Hereditary Muscle Disorders

  • Thierry VandenDriesscheEmail author
  • Yoke Chin Chai
  • Dimitri Boon
  • Marinee K. ChuahEmail author
Chapter

Abstract

Stem cells and their myogenic derivatives offer unprecedented opportunities to treat degenerative muscular disorders by autologous or allogeneic cell-based therapy. This could be attributed to their self-renewal properties, their myogenic differentiation potential and their capacity to enhance muscle regeneration. In particular, different types of adult stem cells that participate in muscle regeneration have been explored for cell-based therapies of degenerative muscle disorders. Nevertheless, these adult stem cells cannot be expanded indefinitely due to cell exhaustion. To overcome this limitation, bona fide pluripotent stem cells could be used instead, such as embryonic stem (ES) cells and induced pluripotent stem (iPS) cells. They could be induced to differentiate into myogenic cells that contribute to muscle regeneration upon transplantation. Most importantly, patient-derived adult stem cells, ES and iPS cells, have been engineered by gene therapy, primarily using integrating vectors (with γ-retroviral, lentiviral or transposons). This allowed sustained expression of the therapeutic gene in the stem cells and their differentiated progeny. More recently, gene editing strategies have been explored (using either ZFNs, TALENs or CRISPR/Cas9) enabling site-specific gene correction. Proof-of-concept studies demonstrate the potential of gene-engineered adult or pluripotent stem cells for muscle regeneration in preclinical disease models, including Duchenne muscular dystrophy. Nevertheless, the overall efficacy of functional integration of gene-corrected myogenic cells into the degenerating muscle would need to be increased. In this review, we discuss some of the challenges that need to be addressed in order to harness the full potential of gene-engineered patient-specific pluripotent stem cells for regenerative medicine.

Keywords

Muscle stem cells iPS Gene therapy Gene editing Myogenic Muscular dystrophy Duchenne 

Notes

Acknowledgements

Some of the research described herein was conducted in the laboratories of TV and MC. This research was supported by grants from the Research Foundation of Flanders (FWO), Association Française contre les Myopathies (AFM), Walter Pyleman Fund (Koning Boudewijn Stichting), Willy Gepts grant (Vrije Universiteit Brussel, VUB), VUB Strategic Research Program ‘Groeier’, VUB Industrieel Onderzoeksfonds (Groups of Expertise in Applied Research grant), EU FP7-PERSIST grant and the EU Horizon 2020-PHC-14-2015-MYOCURE grant (Grant Agreement Number: 667751). DB is supported by an AAP mandate (VUB).

Conflict of Interest

The authors have no conflicts of interest to declare.

References

  1. 1.
    Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495CrossRefGoogle Scholar
  2. 2.
    Loperfido M, Steele-Stallard HB, Tedesco FS, VandenDriessche T (2015) Pluripotent stem cells for gene therapy of degenerative muscle diseases. Curr Gene Ther 15(4):364–380CrossRefGoogle Scholar
  3. 3.
    Blau HM, Webster C, Pavlath GK (1983) Defective myoblasts identified in Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 80(15):4856–4860CrossRefGoogle Scholar
  4. 4.
    Cassano M, Dellavalle A, Tedesco FS, Quattrocelli M, Crippa S, Ronzoni F, Salvade A, Berardi E, Torrente Y, Cossu G, Sampaolesi M (2011) Alpha sarcoglycan is required for FGF-dependent myogenic progenitor cell proliferation in vitro and in vivo. Development 138(20):4523–4533.  https://doi.org/10.1242/dev.070706 CrossRefPubMedGoogle Scholar
  5. 5.
    Cohn RD, Henry MD, Michele DE, Barresi R, Saito F, Moore SA, Flanagan JD, Skwarchuk MW, Robbins ME, Mendell JR, Williamson RA, Campbell KP (2002) Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110(5):639–648CrossRefGoogle Scholar
  6. 6.
    Kudryashova E, Kramerova I, Spencer MJ (2012) Satellite cell senescence underlies myopathy in a mouse model of limb-girdle muscular dystrophy 2H. J Clin Invest 122(5):1764–1776.  https://doi.org/10.1172/JCI59581 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, Partridge T, Buckingham M (2005) Direct isolation of satellite cells for skeletal muscle regeneration. Science 309(5743):2064–2067.  https://doi.org/10.1126/science.1114758 CrossRefGoogle Scholar
  8. 8.
    Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, Kraft P, Shkreli M, Delp S, Pomerantz JH, Artandi SE, Blau HM (2010) Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143(7):1059–1071.  https://doi.org/10.1016/j.cell.2010.11.039 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    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(140):140ra189.  https://doi.org/10.1126/scitranslmed.3003541 CrossRefGoogle Scholar
  10. 10.
    Benedetti S, Hoshiya H, Tedesco FS (2013) Repair or replace? Exploiting novel gene and cell therapy strategies for muscular dystrophies. FEBS J 280(17):4263–4280.  https://doi.org/10.1111/febs.12178 CrossRefPubMedGoogle Scholar
  11. 11.
    Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154–156CrossRefGoogle Scholar
  12. 12.
    Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147CrossRefGoogle Scholar
  13. 13.
    Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676.  https://doi.org/10.1016/j.cell.2006.07.024 CrossRefPubMedGoogle Scholar
  14. 14.
    Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872.  https://doi.org/10.1016/j.cell.2007.11.019 CrossRefGoogle Scholar
  15. 15.
    Costamagna D, Berardi E, Ceccarelli G, Sampaolesi M (2015) Adult stem cells and skeletal muscle regeneration. Curr Gene Ther 15(4):348–363CrossRefGoogle Scholar
  16. 16.
    Mercuri E, Muntoni F (2013) Muscular dystrophies. Lancet 381(9869):845–860.  https://doi.org/10.1016/S0140-6736(12)61897-2 CrossRefPubMedGoogle Scholar
  17. 17.
    Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G (2010) Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 120(1):11–19.  https://doi.org/10.1172/JCI40373 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    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(6203):176–179.  https://doi.org/10.1038/337176a0 CrossRefPubMedGoogle Scholar
  19. 19.
    Skuk D, Tremblay JP (2014) Clarifying misconceptions about myoblast transplantation in myology. Mol Ther 22(5):897–898.  https://doi.org/10.1038/mt.2014.57 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Perie S, Mamchaoui K, Mouly V, Blot S, Bouazza B, Thornell LE, St Guily JL, Butler-Browne G (2006) Premature proliferative arrest of cricopharyngeal myoblasts in oculo-pharyngeal muscular dystrophy: therapeutic perspectives of autologous myoblast transplantation. Neuromuscul Disord 16(11):770–781.  https://doi.org/10.1016/j.nmd.2006.07.022 CrossRefPubMedGoogle Scholar
  21. 21.
    Perie S, Trollet C, Mouly V, Vanneaux V, Mamchaoui K, Bouazza B, Marolleau JP, Laforet P, Chapon F, Eymard B, Butler-Browne G, Larghero J, St Guily JL (2014) Autologous myoblast transplantation for oculopharyngeal muscular dystrophy: a phase I/IIa clinical study. Mol Ther 22(1):219–225.  https://doi.org/10.1038/mt.2013.155 CrossRefPubMedGoogle Scholar
  22. 22.
    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(5):1008–1017.  https://doi.org/10.1038/mt.2014.26 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    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(6):646–657.  https://doi.org/10.1016/j.stem.2007.09.016 CrossRefPubMedGoogle Scholar
  24. 24.
    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 Transplant 16(6):563–577CrossRefGoogle Scholar
  25. 25.
    Mitchell KJ, Pannerec A, Cadot B, Parlakian A, Besson V, Gomes ER, Marazzi G, Sassoon DA (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12(3):257–266.  https://doi.org/10.1038/ncb2025 CrossRefPubMedGoogle Scholar
  26. 26.
    Rouger K, Larcher T, Dubreil L, Deschamps JY, Le Guiner C, Jouvion G, Delorme B, Lieubeau B, Carlus M, Fornasari B, Theret M, Orlando P, Ledevin M, Zuber C, Leroux I, Deleau S, Guigand L, Testault I, Le Rumeur E, Fiszman M, Cherel Y (2011) Systemic delivery of allogenic muscle stem cells induces long-term muscle repair and clinical efficacy in duchenne muscular dystrophy dogs. Am J Pathol 179(5):2501–2518.  https://doi.org/10.1016/j.ajpath.2011.07.022 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Vauchez K, Marolleau JP, Schmid M, Khattar P, Chapel A, Catelain C, Lecourt S, Larghero J, Fiszman M, Vilquin JT (2009) Aldehyde dehydrogenase activity identifies a population of human skeletal muscle cells with high myogenic capacities. Mol Ther 17(11):1948–1958.  https://doi.org/10.1038/mt.2009.204 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cappellari O, Cossu G (2013) Pericytes in development and pathology of skeletal muscle. Circ Res 113(3):341–347.  https://doi.org/10.1161/CIRCRESAHA.113.300203 CrossRefPubMedGoogle Scholar
  29. 29.
    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.  https://doi.org/10.1038/ncomms1508 CrossRefPubMedGoogle Scholar
  30. 30.
    Minasi MG, Riminucci M, De Angelis L, Borello U, Berarducci B, Innocenzi A, Caprioli A, Sirabella D, Baiocchi M, De Maria R, Boratto R, Jaffredo T, Broccoli V, Bianco P, Cossu G (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129(11):2773–2783PubMedGoogle Scholar
  31. 31.
    Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, Bottinelli R, Cossu G (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301(5632):487–492.  https://doi.org/10.1126/science.1082254 CrossRefPubMedGoogle Scholar
  32. 32.
    Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy I, Perani L, Mantero S, Guttinger M, Pansarasa O, Rinaldi C, Cusella De Angelis MG, Torrente Y, Bordignon C, Bottinelli R, Cossu G (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444(7119):574–579.  https://doi.org/10.1038/nature05282 CrossRefPubMedGoogle Scholar
  33. 33.
    Gargioli C, Coletta M, De Grandis F, Cannata SM, Cossu G (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat Med 14(9):973–978.  https://doi.org/10.1038/nm.1852 CrossRefPubMedGoogle Scholar
  34. 34.
    Diaz-Manera J, Touvier T, Dellavalle A, Tonlorenzi R, Tedesco FS, Messina G, Meregalli M, Navarro C, Perani L, Bonfanti C, Illa I, Torrente Y, Cossu G (2010) Partial dysferlin reconstitution by adult murine mesoangioblasts is sufficient for full functional recovery in a murine model of dysferlinopathy. Cell Death Dis 1:e61.  https://doi.org/10.1038/cddis.2010.35 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    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(96):96ra78.  https://doi.org/10.1126/scitranslmed.3002342 CrossRefPubMedGoogle Scholar
  36. 36.
    Giannotta M, Benedetti S, Tedesco FS, Corada M, Trani M, D'Antuono R, Millet Q, Orsenigo F, Galvez BG, Cossu G, Dejana E (2014) Targeting endothelial junctional adhesion molecule-A/EPAC/Rap-1 axis as a novel strategy to increase stem cell engraftment in dystrophic muscles. EMBO Mol Med 6(2):239–258.  https://doi.org/10.1002/emmm.201302520 CrossRefPubMedGoogle Scholar
  37. 37.
    Cossu G, Previtali SC, Napolitano S, Cicalese MP, Tedesco FS, Nicastro F, Noviello M, Roostalu U, Natali Sora MG, Scarlato M, De Pellegrin M, Godi C, Giuliani S, Ciotti F, Tonlorenzi R, Lorenzetti I, Rivellini C, Benedetti S, Gatti R, Marktel S, Mazzi B, Tettamanti A, Ragazzi M, Imro MA, Marano G, Ambrosi A, Fiori R, Sormani MP, Bonini C, Venturini M, Politi LS, Torrente Y, Ciceri F (2015) Intra-arterial transplantation of HLA-matched donor mesoangioblasts in Duchenne muscular dystrophy. EMBO Mol Med 7(12):1513–1528.  https://doi.org/10.15252/emmm.201505636 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78(12):7634–7638CrossRefGoogle Scholar
  39. 39.
    Yamanaka S (2012) Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10(6):678–684.  https://doi.org/10.1016/j.stem.2012.05.005 CrossRefPubMedGoogle Scholar
  40. 40.
    Darabi R, Arpke RW, Irion S, Dimos JT, Grskovic M, Kyba M, Perlingeiro RC (2012) Human ES- and iPS-derived myogenic progenitors restore DYSTROPHIN and improve contractility upon transplantation in dystrophic mice. Cell Stem Cell 10(5):610–619.  https://doi.org/10.1016/j.stem.2012.02.015 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Biasco L, Baricordi C, Aiuti A (2012) Retroviral integrations in gene therapy trials. Mol Ther 20(4):709–716.  https://doi.org/10.1038/mt.2011.289 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458(7239):771–775.  https://doi.org/10.1038/nature07864 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945–949.  https://doi.org/10.1126/science.1162494 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Drukker M, Katz G, Urbach A, Schuldiner M, Markel G, Itskovitz-Eldor J, Reubinoff B, Mandelboim O, Benvenisty N (2002) Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci U S A 99(15):9864–9869.  https://doi.org/10.1073/pnas.142298299 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Swijnenburg RJ, Tanaka M, Vogel H, Baker J, Kofidis T, Gunawan F, Lebl DR, Caffarelli AD, de Bruin JL, Fedoseyeva EV, Robbins RC (2005) Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 112(9 Suppl):I166–I172.  https://doi.org/10.1161/CIRCULATIONAHA.104.525824 CrossRefPubMedGoogle Scholar
  46. 46.
    Zhao T, Zhang ZN, Rong Z, Xu Y (2011) Immunogenicity of induced pluripotent stem cells. Nature 474(7350):212–215.  https://doi.org/10.1038/nature10135 CrossRefPubMedGoogle Scholar
  47. 47.
    Li O, English K, Tonlorenzi R, Cossu G, Saverio Tedesco F, Wood KJ (2013) Human iPSC-derived mesoangioblasts, like their tissue-derived counterparts, suppress T cell proliferation through IDO- and PGE-2-dependent pathways. F1000Res 2:24.  https://doi.org/10.12688/f1000research.2-24.v1 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Ye L, Muench MO, Fusaki N, Beyer AI, Wang J, Qi Z, Yu J, Kan YW (2013) Blood cell-derived induced pluripotent stem cells free of reprogramming factors generated by Sendai viral vectors. Stem Cells Transl Med 2(8):558–566.  https://doi.org/10.5966/sctm.2013-0006 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Zhou T, Benda C, Dunzinger S, Huang Y, Ho JC, Yang J, Wang Y, Zhang Y, Zhuang Q, Li Y, Bao X, Tse HF, Grillari J, Grillari-Voglauer R, Pei D, Esteban MA (2012) Generation of human induced pluripotent stem cells from urine samples. Nat Protoc 7(12):2080–2089.  https://doi.org/10.1038/nprot.2012.115 CrossRefPubMedGoogle Scholar
  50. 50.
    Kuang S, Gillespie MA, Rudnicki MA (2008) Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2(1):22–31.  https://doi.org/10.1016/j.stem.2007.12.012 CrossRefPubMedGoogle Scholar
  51. 51.
    Pannerec A, Marazzi G, Sassoon D (2012) Stem cells in the hood: the skeletal muscle niche. Trends Mol Med 18(10):599–606.  https://doi.org/10.1016/j.molmed.2012.07.004 CrossRefPubMedGoogle Scholar
  52. 52.
    Wang YX, Rudnicki MA (2011) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13(2):127–133.  https://doi.org/10.1038/nrm3265 CrossRefPubMedGoogle Scholar
  53. 53.
    Borchin B, Chen J, Barberi T (2013) Derivation and FACS-mediated purification of PAX3+/PAX7+ skeletal muscle precursors from human pluripotent stem cells. Stem Cell Reports 1(6):620–631.  https://doi.org/10.1016/j.stemcr.2013.10.007 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Vaskova EA, Stekleneva AE, Medvedev SP, Zakian SM (2013) “Epigenetic memory” phenomenon in induced pluripotent stem cells. Acta Nat 5(4):15–21Google Scholar
  55. 55.
    Shtrichman R, Germanguz I, Itskovitz-Eldor J (2013) Induced pluripotent stem cells (iPSCs) derived from different cell sources and their potential for regenerative and personalized medicine. Curr Mol Med 13(5):792–805CrossRefGoogle Scholar
  56. 56.
    Quattrocelli M, Palazzolo G, Floris G, Schoffski P, Anastasia L, Orlacchio A, VandenDriessche T, Chuah MK, Cossu G, Verfaillie C, Sampaolesi M (2011) Intrinsic cell memory reinforces myogenic commitment of pericyte-derived iPSCs. J Pathol 223(5):593–603.  https://doi.org/10.1002/path.2845 CrossRefPubMedGoogle Scholar
  57. 57.
    Sanchez-Freire V, Lee AS, Hu S, Abilez OJ, Liang P, Lan F, Huber BC, Ong SG, Hong WX, Huang M, Wu JC (2014) Effect of human donor cell source on differentiation and function of cardiac induced pluripotent stem cells. J Am Coll Cardiol 64(5):436–448.  https://doi.org/10.1016/j.jacc.2014.04.056 CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Wu C, Hong SG, Winkler T, Spencer DM, Jares A, Ichwan B, Nicolae A, Guo V, Larochelle A, Dunbar CE (2014) Development of an inducible caspase-9 safety switch for pluripotent stem cell-based therapies. Mol Ther Methods Clin Dev 1:14053.  https://doi.org/10.1038/mtm.2014.53 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Schuldiner M, Itskovitz-Eldor J, Benvenisty N (2003) Selective ablation of human embryonic stem cells expressing a “suicide” gene. Stem Cells 21(3):257–265.  https://doi.org/10.1634/stemcells.21-3-257 CrossRefPubMedGoogle Scholar
  60. 60.
    Sicari BM, Agrawal V, Siu BF, Medberry CJ, Dearth CL, Turner NJ, Badylak SF (2012) A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng Part A 18(19–20):1941–1948.  https://doi.org/10.1089/ten.TEA.2012.0475 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Criswell TL, Corona BT, Wang Z, Zhou Y, Niu G, Xu Y, Christ GJ, Soker S (2013) The role of endothelial cells in myofiber differentiation and the vascularization and innervation of bioengineered muscle tissue in vivo. Biomaterials 34(1):140–149.  https://doi.org/10.1016/j.biomaterials.2012.09.045 CrossRefPubMedGoogle Scholar
  62. 62.
    Fuoco C, Rizzi R, Biondo A, Longa E, Mascaro A, Shapira-Schweitzer K, Kossovar O, Benedetti S, Salvatori ML, Santoleri S, Testa S, Bernardini S, Bottinelli R, Bearzi C, Cannata SM, Seliktar D, Cossu G, Gargioli C (2015) In vivo generation of a mature and functional artificial skeletal muscle. EMBO Mol Med 7(4):411–422.  https://doi.org/10.15252/emmm.201404062 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kazuki Y, Hiratsuka M, Takiguchi M, Osaki M, Kajitani N, Hoshiya H, Hiramatsu K, Yoshino T, Kazuki K, Ishihara C, Takehara S, Higaki K, Nakagawa M, Takahashi K, Yamanaka S, Oshimura M (2010) Complete genetic correction of ips cells from Duchenne muscular dystrophy. Mol Ther 18(2):386–393.  https://doi.org/10.1038/mt.2009.274 CrossRefPubMedGoogle Scholar
  64. 64.
    Loperfido M, Jarmin S, Dastidar S, Di Matteo M, Perini I, Moore M, Nair N, Samara-Kuko E, Athanasopoulos T, Tedesco FS, Dickson G, Sampaolesi M, VandenDriessche T, Chuah MK (2016) piggyBac transposons expressing full-length human dystrophin enable genetic correction of dystrophic mesoangioblasts. Nucleic Acids Res 44(2):744–760.  https://doi.org/10.1093/nar/gkv1464 CrossRefPubMedGoogle Scholar
  65. 65.
    Filareto A, Parker S, Darabi R, Borges L, Iacovino M, Schaaf T, Mayerhofer T, Chamberlain JS, Ervasti JM, McIvor RS, Kyba M, Perlingeiro RC (2013) An ex vivo gene therapy approach to treat muscular dystrophy using inducible pluripotent stem cells. Nat Commun 4:1549.  https://doi.org/10.1038/ncomms2550 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4(12):1441–1444.  https://doi.org/10.1038/4033 CrossRefPubMedGoogle Scholar
  67. 67.
    Tanaka A, Woltjen K, Miyake K, Hotta A, Ikeya M, Yamamoto T, Nishino T, Shoji E, Sehara-Fujisawa A, Manabe Y, Fujii N, Hanaoka K, Era T, Yamashita S, Isobe K, Kimura E, Sakurai H (2013) Efficient and reproducible myogenic differentiation from human iPS cells: prospects for modeling Miyoshi myopathy in vitro. PLoS One 8(4):e61540.  https://doi.org/10.1371/journal.pone.0061540 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Ma N, Liao B, Zhang H, Wang L, Shan Y, Xue Y, Huang K, Chen S, Zhou X, Chen Y, Pei D, Pan G (2013) Transcription activator-like effector nuclease (TALEN)-mediated gene correction in integration-free beta-thalassemia induced pluripotent stem cells. J Biol Chem 288(48):34671–34679.  https://doi.org/10.1074/jbc.M113.496174 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Choi SM, Kim Y, Shim JS, Park JT, Wang RH, Leach SD, Liu JO, Deng C, Ye Z, Jang YY (2013) Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 57(6):2458–2468.  https://doi.org/10.1002/hep.26237 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Osborn MJ, Starker CG, McElroy AN, Webber BR, Riddle MJ, Xia L, DeFeo AP, Gabriel R, Schmidt M, von Kalle C, Carlson DF, Maeder ML, Joung JK, Wagner JE, Voytas DF, Blazar BR, Tolar J (2013) TALEN-based gene correction for epidermolysis bullosa. Mol Ther 21(6):1151–1159.  https://doi.org/10.1038/mt.2013.56 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    VandenDriessche T, Chuah MK (2016) CRISPR/Cas9 flexes its muscles: in vivo somatic gene editing for muscular dystrophy. Mol Ther 24(3):414–416.  https://doi.org/10.1038/mt.2016.29 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Ousterout DG, Perez-Pinera P, Thakore PI, Kabadi AM, Brown MT, Qin X, Fedrigo O, Mouly V, Tremblay JP, Gersbach CA (2013) Reading frame correction by targeted genome editing restores dystrophin expression in cells from Duchenne muscular dystrophy patients. Mol Ther 21(9):1718–1726.  https://doi.org/10.1038/mt.2013.111 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Ousterout DG, Kabadi AM, Thakore PI, Perez-Pinera P, Brown MT, Majoros WH, Reddy TE, Gersbach CA (2015) Correction of dystrophin expression in cells from Duchenne muscular dystrophy patients through genomic excision of exon 51 by zinc finger nucleases. Mol Ther 23(3):523–532.  https://doi.org/10.1038/mt.2014.234 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Ousterout DG, Kabadi AM, Thakore PI, Majoros WH, Reddy TE, Gersbach CA (2015) Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun 6:6244.  https://doi.org/10.1038/ncomms7244 CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    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 Reports 4(1):143–154.  https://doi.org/10.1016/j.stemcr.2014.10.013 CrossRefPubMedGoogle Scholar
  76. 76.
    Cyranoski D (2014) Japanese woman is first recipient of next-generation stem cells. Nature.  https://doi.org/10.1038/nature.2014.15915
  77. 77.
    Kamao H, Mandai M, Okamoto S, Sakai N, Suga A, Sugita S, Kiryu J, Takahashi M (2014) Characterization of human induced pluripotent stem cell-derived retinal pigment epithelium cell sheets aiming for clinical application. Stem Cell Reports 2(2):205–218.  https://doi.org/10.1016/j.stemcr.2013.12.007 CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Nakano-Okuno M, Borah BR, Nakano I (2014) Ethics of iPSC-based clinical research for age-related macular degeneration: patient-centered risk-benefit analysis. Stem Cell Rev 10(6):743–752.  https://doi.org/10.1007/s12015-014-9536-x CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Gene Therapy & Regenerative Medicine, Faculty of Medicine and PharmacyVrije Universiteit Brussel (VUB)BrusselsBelgium
  2. 2.Center for Molecular & Vascular Biology, Department of Cardiovascular SciencesUniversity of LeuvenLeuvenBelgium

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