Skip to main content
SpringerLink
Log in

Stem Cell Therapy in Muscle Degeneration

  • Chapter
  • First Online:
The Plasticity of Skeletal Muscle

  • 1141 Accesses

Abstract

Skeletal muscle is one of the largest tissues in humans, reaching around 38% of the body weight for men and 30% for women (Janssen I, et al, J Appl Physiol 89(1):81–88, 1985/2000). Muscle tissue finely regulates essential body movements, including respiration, equilibrium maintenance and ambulation. In addition, it controls body temperature and energy balance and restores blood glucose levels. Genetic or acquired alterations in these enzymes can lead to metabolic syndromes (McArdle’s syndrome (Vorgerd M, Neurotherapeutics 5(4):579–582 2008) or diabetes (DeFronzo RA, Tripathy D, Diabetes Care 32(Suppl 2):S157–S163 2009). Muscle tissue is originated during embryo development, from the fusion of mesoderm progenitors. During the neonatal and early juvenile period, even if the myofibre number remains constant, new postnatal multipotent cells, called satellite cells (SCs), can fuse and increase the number of nuclei per fibre (Biressi S, et al, Dev Biol 379(2):195–207, 2013). Adult skeletal muscle is organised in long fibres generated from the fusion of single cells into a unique syncytium able to collect thousands of nuclei and of myofibrils. Each myofibril contains multiple sarcomeres, formed by actin and myosin filaments to generate contraction and develop force. High heterogeneity is present among single fibres, including slow-contracting fatigue-resisting type I fibres (also known as slow-twitch, tonic or simply slow fibres) and fast-contracting fatigue-unresisting type II fibres (fast-twitch, phasic or fast fibres). To exert a good performance, the expression of specific contractile proteins and metabolic enzymes is necessary together with a regular connection to a single motor neuron and an efficient vascularisation. Myotendinous junctions connect myofibres from one side and bones in the skeleton on the other side, allowing transmission of contractions to other muscles. Daily wear and tear or excessive load and damage of the fibre integrity activate SCs that undergo fusion. The highly orchestrated process has been thoroughly studied. Nevertheless, understanding the role of local and circulating cell types in adult myogenesis still remains a matter of discussion (Relaix F, Zammit PS, Development 139(16):2845–2856, 2012). In this chapter after introducing the biological events occurring in acute and chronic skeletal muscle damages, cell and gene therapy approaches are considered as novel tools to preserve muscle function.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Janssen I et al (1985/2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89(1):81–88

    Google Scholar 

  2. Vorgerd M (2008) Therapeutic options in other metabolic myopathies. Neurotherapeutics 5(4):579–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. DeFronzo RA, Tripathy D (2009) Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care 32(Suppl 2):S157–S163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Biressi S et al (2013) Myf5 expression during fetal myogenesis defines the developmental progenitors of adult satellite cells. Dev Biol 379(2):195–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Relaix F, Zammit PS (2012) Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 139(16):2845–2856

    Article  CAS  PubMed  Google Scholar 

  6. Bansal D et al (2003) Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423(6936):168–172

    Article  CAS  PubMed  Google Scholar 

  7. Bushby KM (1995) Diagnostic criteria for the limb-girdle muscular dystrophies: report of the ENMC Consortium on Limb-Girdle Dystrophies. Neuromuscul Disord 5(1):71–74

    Article  CAS  PubMed  Google Scholar 

  8. Ciciliot S, Schiaffino S (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16(8):906–914

    Article  CAS  PubMed  Google Scholar 

  9. Angelini C, Di Mauro S, Margreth A (1968) Relationship of serum enzyme changes to muscle damage in vitamin E deficiency of the rabbit. Sperimentale 118(5):349–369

    CAS  PubMed  Google Scholar 

  10. Laterza OF et al (2009) Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem 55(11):1977–1983

    Article  CAS  PubMed  Google Scholar 

  11. Campana L et al (2014) Leukocyte HMGB1 is required for vessel remodeling in regenerating muscles. J Immunol 192(11):5257–5264

    Article  CAS  PubMed  Google Scholar 

  12. Hamer PW et al (2002) Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J Anat 200(Pt 1):69–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fanzani A et al (2012) Molecular and cellular mechanisms of skeletal muscle atrophy: an update. J Cachex Sarcopenia Muscle 3(3):163–179

    Article  Google Scholar 

  14. Nguyen HX, Lusis AJ, Tidball JG (2005) Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo. J Physiol 565(Pt 2):403–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Warren GL et al (2002) Physiological role of tumor necrosis factor alpha in traumatic muscle injury. FASEB J 16(12):1630–1632

    CAS  PubMed  Google Scholar 

  16. Horsley V et al (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113(4):483–494

    Article  CAS  PubMed  Google Scholar 

  17. Christov C et al (2007) Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell 18(4):1397–1409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chazaud B et al (2003) Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 163(5):1133–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Arnold L et al (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204(5):1057–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Perdiguero E et al (2011) p38/MKP-1-regulated AKT coordinates macrophage transitions and resolution of inflammation during tissue repair. J Cell Biol 195(2):307–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bosurgi L et al (2012) Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury. J Immunol 188(12):6267–6277

    Article  CAS  PubMed  Google Scholar 

  22. Sugama K et al (2012) IL-17, neutrophil activation and muscle damage following endurance exercise. Exerc Immunol Rev 18:116–127

    PubMed  Google Scholar 

  23. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214(2):199–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Loke P et al (2007) Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J Immunol 179(6):3926–3936

    Article  CAS  PubMed  Google Scholar 

  25. Bakkar N et al (2008) IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis. J Cell Biol 180(4):787–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Trendelenburg AU et al (2012) TAK-1/p38/nNFkappaB signaling inhibits myoblast differentiation by increasing levels of Activin A. Skelet Muscle 2(1):3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sierra-Filardi E et al (2011) Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 117(19):5092–5101

    Article  CAS  PubMed  Google Scholar 

  28. Londhe P, Davie JK (2011) Gamma interferon modulates myogenesis through the major histocompatibility complex class II transactivator, CIITA. Mol Cell Biol 31(14):2854–2866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mathur N, Pedersen BK (2008) Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm 2008:109502

    Article  CAS  Google Scholar 

  30. Broholm C et al (2012) Deficient leukemia inhibitory factor signaling in muscle precursor cells from patients with type 2 diabetes. Am J Physiol Endocrinol Metab 303(2):E283–E292

    Article  CAS  PubMed  Google Scholar 

  31. Steensberg A et al (2003) IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am J Physiol Endocrinol Metab 285(2):E433–E437

    Article  CAS  PubMed  Google Scholar 

  32. Pedersen BK (2012) Muscular interleukin-6 and its role as an energy sensor. Med Sci Sports Exerc 44(3):392–396

    Article  CAS  PubMed  Google Scholar 

  33. Bostrom P et al (2012) A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481(7382):463–468

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Whalen RG et al (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev Biol 141(1):24–40

    Article  CAS  PubMed  Google Scholar 

  35. Charge SB, Brack AS, Hughes SM (2002) Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy. Am J Phys Cell Phys 283(4):C1228–C1241

    Article  CAS  Google Scholar 

  36. von Maltzahn J et al (2013) Pax7 is critical for the normal function of satellite cells in adult skeletal muscle. Proc Natl Acad Sci U S A 110(41):16474–16479

    Article  Google Scholar 

  37. Cooper RN et al (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112(Pt 17):2895–2901

    CAS  PubMed  Google Scholar 

  38. Ustanina S et al (2007) The myogenic factor Myf5 supports efficient skeletal muscle regeneration by enabling transient myoblast amplification. Stem Cells 25(8):2006–2016

    Article  CAS  PubMed  Google Scholar 

  39. Kassar-Duchossoy L et al (2004) Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431(7007):466–471

    Article  CAS  PubMed  Google Scholar 

  40. Timmerman KL et al (2008) Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise? J Leukoc Biol 84(5):1271–1278

    Article  CAS  PubMed  Google Scholar 

  41. Gussoni E et al (1994) Specific T cell receptor gene rearrangements at the site of muscle degeneration in Duchenne muscular dystrophy. J Immunol 153(10):4798–4805

    CAS  PubMed  Google Scholar 

  42. Farini A et al (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(2):229–238

    Article  CAS  PubMed  Google Scholar 

  43. Pagel CN et al (2014) Osteopontin, inflammation and myogenesis: influencing regeneration, fibrosis and size of skeletal muscle. J Cell Commun Signal 8(2):95–103

    Article  PubMed  Google Scholar 

  44. Mojumdar K et al (2014) Inflammatory monocytes promote progression of Duchenne muscular dystrophy and can be therapeutically targeted via CCR2. EMBO Mol Med 6(11):1476–1492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Radley HG et al (2007) Duchenne muscular dystrophy: focus on pharmaceutical and nutritional interventions. Int J Biochem Cell Biol 39(3):469–477

    Article  CAS  PubMed  Google Scholar 

  46. Buyse GM et al (2007) CINRG pilot trial of oxatomide in steroid-naive Duchenne muscular dystrophy. Eur J Paediatr Neurol 11(6):337–340

    Article  PubMed  Google Scholar 

  47. Vidal B et al (2008) Fibrinogen drives dystrophic muscle fibrosis via a TGFbeta/alternative macrophage activation pathway. Genes Dev 22(13):1747–1752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Vidal B et al (2012) Amelioration of Duchenne muscular dystrophy in mdx mice by elimination of matrix-associated fibrin-driven inflammation coupled to the alphaMbeta2 leukocyte integrin receptor. Hum Mol Genet 21(9):1989–2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Abdel-Hamid H, Clemens PR (2012) Pharmacological therapies for muscular dystrophies. Curr Opin Neurol 25(5):604–608

    Article  PubMed  Google Scholar 

  50. Sundrud MS et al (2009) Halofuginone inhibits TH17 cell differentiation by activating the amino acid starvation response. Science 324(5932):1334–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Hodgetts S et al (2006) Reduced necrosis of dystrophic muscle by depletion of host neutrophils, or blocking TNFalpha function with Etanercept in mdx mice. Neuromuscul Disord 16(9–10):591–602

    Article  PubMed  Google Scholar 

  52. Munoz-Canoves P, Serrano AL (2015) Macrophages decide between regeneration and fibrosis in muscle. Trends Endocrinol Metab 26(9):449–450

    Article  CAS  PubMed  Google Scholar 

  53. Gattazzo F et al (2014) Cyclosporin A promotes in vivo myogenic response in collagen VI-deficient myopathic mice. Front Aging Neurosci 6:244

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Merlini L et al (2011) Cyclosporine A in Ullrich congenital muscular dystrophy: long-term results. Oxidative Med Cell Longev 2011:139194

    Article  CAS  Google Scholar 

  55. Wehling M, Spencer MJ, Tidball JG (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155(1):123–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lluis F et al (2005) E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. EMBO J 24(5):974–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Zetser A, Gredinger E, Bengal E (1999) p38 mitogen-activated protein kinase pathway promotes skeletal muscle differentiation. Participation of the Mef2c transcription factor. J Biol Chem 274(8):5193–5200

    Article  CAS  PubMed  Google Scholar 

  58. Gillespie MA et al (2009) p38-{gamma}-dependent gene silencing restricts entry into the myogenic differentiation program. J Cell Biol 187(7):991–1005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Palacios D et al (2010) TNF/p38alpha/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7(4):455–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Price DM et al (2014) The effect of age and medical comorbidities on in vitro myoblast expansion in women with and without pelvic organ prolapse. Female Pelvic Med Reconstr Surg 20(5):281–286

    Article  PubMed  Google Scholar 

  61. Penna F et al (2010) Muscle wasting and impaired myogenesis in tumor bearing mice are prevented by ERK inhibition. PLoS One 5(10):e13604

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. He WA et al (2013) NF-kappaB-mediated Pax7 dysregulation in the muscle microenvironment promotes cancer cachexia. J Clin Invest 123(11):4821–4835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Heredia JE et al (2013) Type 2 innate signals stimulate fibro/adipogenic progenitors to facilitate muscle regeneration. Cell 153(2):376–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Saccone V et al (2014) HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibro-adipogenic progenitors in dystrophic muscles. Genes Dev 28(8):841–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Mozzetta C et al (2013) Fibroadipogenic progenitors mediate the ability of HDAC inhibitors to promote regeneration in dystrophic muscles of young, but not old Mdx mice. EMBO Mol Med 5(4):626–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fry CS et al (2015) Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 21(1):76–80

    Article  CAS  PubMed  Google Scholar 

  67. Sousa-Victor P et al (2014) Geriatric muscle stem cells switch reversible quiescence into senescence. Nature 506(7488):316–321

    Article  CAS  PubMed  Google Scholar 

  68. Tierney MT et al (2014) STAT3 signaling controls satellite cell expansion and skeletal muscle repair. Nat Med 20(10):1182–1186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Brack AS et al (2007) Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 317(5839):807–810

    Article  CAS  PubMed  Google Scholar 

  70. Costamagna D et al (2015) Role of inflammation in muscle homeostasis and myogenesis. Mediat Inflamm 2015:805172

    Article  CAS  Google Scholar 

  71. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Morgan JE, Partridge TA (2003) Muscle satellite cells. Int J Biochem Cell Biol 35(8):1151–1156

    Article  CAS  PubMed  Google Scholar 

  73. Lepper C, Partridge TA, Fan CM (2011) An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Development 138(17):3639–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Boldrin L, Muntoni F, Morgan JE (2010) Are human and mouse satellite cells really the same? J Histochem Cytochem 58(11):941–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Seale P et al (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102(6):777–786

    Article  CAS  PubMed  Google Scholar 

  76. Ratajczak MZ et al (2003) Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells 21(3):363–371

    Article  CAS  PubMed  Google Scholar 

  77. Bockhold KJ, Rosenblatt JD, Partridge TA (1998) Aging normal and dystrophic mouse muscle: analysis of myogenicity in cultures of living single fibers. Muscle Nerve 21(2):173–183

    Article  CAS  PubMed  Google Scholar 

  78. Lindstrom M, Thornell LE (2009) New multiple labelling method for improved satellite cell identification in human muscle: application to a cohort of power-lifters and sedentary men. Histochem Cell Biol 132(2):141–157

    Article  PubMed  CAS  Google Scholar 

  79. Zheng B et al (2007) Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25(9):1025–1034

    Article  CAS  PubMed  Google Scholar 

  80. Mouly V et al (2005) The mitotic clock in skeletal muscle regeneration, disease and cell mediated gene therapy. Acta Physiol Scand 184(1):3–15

    Article  CAS  PubMed  Google Scholar 

  81. 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 

  82. Partridge TA et al (1989) Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337(6203):176–179

    Article  CAS  PubMed  Google Scholar 

  83. 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(6 Pt 1):2437–2449

    Google Scholar 

  84. Kinoshita I, Huard J, Tremblay JP (1994) Utilization of myoblasts from transgenic mice to evaluate the efficacy of myoblast transplantation. Muscle Nerve 17(9):975–980

    Article  CAS  PubMed  Google Scholar 

  85. Huard J et al (1994) High efficiency of muscle regeneration after human myoblast clone transplantation in SCID mice. J Clin Invest 93(2):586–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Palmieri B, Tremblay JP, Daniele L (2010) Past, present and future of myoblast transplantation in the treatment of Duchenne muscular dystrophy. Pediatr Transplant 14(7):813–819

    Article  PubMed  Google Scholar 

  87. Neumeyer AM, DiGregorio DM, Brown RH Jr (1992) Arterial delivery of myoblasts to skeletal muscle. Neurology 42(12):2258–2262

    Article  CAS  PubMed  Google Scholar 

  88. Dellavalle A et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9(3):255–267

    Article  CAS  PubMed  Google Scholar 

  89. Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21(2):193–215

    Article  CAS  PubMed  Google Scholar 

  90. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97(6):512–523

    Article  CAS  PubMed  Google Scholar 

  91. Diaz-Flores L et al (2009) Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24(7):909–969

    CAS  PubMed  Google Scholar 

  92. Crisan M et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3):301–313

    Article  CAS  PubMed  Google Scholar 

  93. Chen WC et al (2014) Isolation of blood-vessel-derived multipotent precursors from human skeletal muscle. J Vis Exp 90:e51195

    Google Scholar 

  94. De Angelis L et al (1999) Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147(4):869–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Sampaolesi M et al (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301(5632):487–492

    Article  CAS  PubMed  Google Scholar 

  96. Tonlorenzi R et al (2007) Isolation and characterization of mesoangioblasts from mouse, dog, and human tissues. Curr Protoc Stem Cell Biol. Chapter 2: p. Unit 2B 1

    Google Scholar 

  97. Sampaolesi M et al (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444(7119):574–579

    Article  CAS  PubMed  Google Scholar 

  98. Minasi MG et al (2002) The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development 129(11):2773–2783

    CAS  PubMed  Google Scholar 

  99. Quattrocelli M et al (2010) Cell therapy strategies and improvements for muscular dystrophy. Cell Death Differ 17(8):1222–1229

    Article  CAS  PubMed  Google Scholar 

  100. Quattrocelli M et al (2012) Mouse and human mesoangioblasts: isolation and characterization from adult skeletal muscles. Methods Mol Biol 798:65–76

    Article  CAS  PubMed  Google Scholar 

  101. Caplan AI (2008) All MSCs are pericytes? Cell Stem Cell 3(3):229–230

    Article  CAS  PubMed  Google Scholar 

  102. English K et al (2013) Mesoangioblasts suppress T cell proliferation through IDO and PGE-2-dependent pathways. Stem Cells Dev 22(3):512–523

    Article  CAS  PubMed  Google Scholar 

  103. Tedesco FS et al (2011) Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Sci Transl Med 3(96):96ra78

    Article  CAS  PubMed  Google Scholar 

  104. Costamagna D et al (2016) Smad1/5/8 are myogenic regulators of murine and human mesoangioblasts. J Mol Cell Biol 8(1):73–87

    Article  PubMed  Google Scholar 

  105. Loperfido M et al (2016) piggyBac transposons expressing full-length human dystrophin enable genetic correction of dystrophic mesoangioblasts. Nucleic Acids Res 44(2):744–760

    Article  CAS  PubMed  Google Scholar 

  106. Cossu G et al (2015) Intra-arterial transplantation of HLA-matched donor mesoangioblasts in Duchenne muscular dystrophy. EMBO Mol Med 7(12):1513–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Cao B et al (2003) Muscle stem cells differentiate into haematopoietic lineages but retain myogenic potential. Nat Cell Biol 5(7):640–646

    Article  CAS  PubMed  Google Scholar 

  108. Qu-Petersen Z et al (2002) Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157(5):851–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Ota S et al (2011) Intramuscular transplantation of muscle-derived stem cells accelerates skeletal muscle healing after contusion injury via enhancement of angiogenesis. Am J Sports Med 39(9):1912–1922

    Article  PubMed  Google Scholar 

  110. Vauchez K et al (2009) Aldehyde dehydrogenase activity identifies a population of human skeletal muscle cells with high myogenic capacities. Mol Ther 17(11):1948–1958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Rouger K et al (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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Mitchell KJ et al (2010) Identification and characterization of a non-satellite cell muscle resident progenitor during postnatal development. Nat Cell Biol 12(3):257–266

    CAS  PubMed  Google Scholar 

  113. Bonfanti C et al (2015) PW1/Peg3 expression regulates key properties that determine mesoangioblast stem cell competence. Nat Commun 6:6364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Penton CM et al (2013) Muscle side population cells from dystrophic or injured muscle adopt a fibro-adipogenic fate. PLoS One 8(1):e54553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Tanaka KK et al (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4(3):217–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Berardi E et al (2014) Molecular and cell-based therapies for muscle degenerations: a road under construction. Front Physiol 5:119

    Article  PubMed  PubMed Central  Google Scholar 

  117. Gussoni E et al (1999) Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401(6751):390–394

    CAS  PubMed  Google Scholar 

  118. Joe AW et al (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12(2):153–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Uezumi A et al (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12(2):143–152

    Article  CAS  PubMed  Google Scholar 

  120. Bianco P et al (2010) “Mesenchymal” stem cells in human bone marrow (skeletal stem cells): a critical discussion of their nature, identity, and significance in incurable skeletal disease. Hum Gene Ther 21(9):1057–1066

    Article  CAS  PubMed  Google Scholar 

  121. Chamberlain G et al (2007) Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25(11):2739–2749

    Article  CAS  PubMed  Google Scholar 

  122. Dominici M et al (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8(4):315–317

    Article  CAS  PubMed  Google Scholar 

  123. Caplan AI (2007) Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213(2):341–347

    Article  CAS  PubMed  Google Scholar 

  124. Rodriguez AM et al (2005) Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 201(9):1397–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Meng J et al (2010) The contribution of human synovial stem cells to skeletal muscle regeneration. Neuromuscul Disord 20(1):6–15

    Article  PubMed  Google Scholar 

  126. Jackson WM, Nesti LJ, Tuan RS (2010) Potential therapeutic applications of muscle-derived mesenchymal stem and progenitor cells. Expert Opin Biol Ther 10(4):505–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Ferrari G et al (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279(5356):1528–1530

    Article  CAS  PubMed  Google Scholar 

  128. Dezawa M et al (2005) Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309(5732):314–317

    Article  CAS  PubMed  Google Scholar 

  129. Torrente Y et al (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114(2):182–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Torrente Y et al (2007) Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients. Cell Transplant 16(6):563–577

    Article  CAS  PubMed  Google Scholar 

  131. Negroni E et al (2009) In vivo myogenic potential of human CD133+ muscle-derived stem cells: a quantitative study. Mol Ther 17(10):1771–1778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Benchaouir R et al (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

    Article  CAS  PubMed  Google Scholar 

  133. Thomson JA et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145–1147

    Article  CAS  PubMed  Google Scholar 

  134. Takahashi K et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872

    Article  CAS  PubMed  Google Scholar 

  135. Ostrovidov S et al (2015) Stem cell differentiation toward the myogenic lineage for muscle tissue regeneration: a focus on muscular dystrophy. Stem Cell Rev 11(6):866–884

    Article  CAS  PubMed  Google Scholar 

  136. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292(5819):154–156

    Article  CAS  PubMed  Google Scholar 

  137. Bodnar MS et al (2004) Propagation and maintenance of undifferentiated human embryonic stem cells. Stem Cells Dev 13(3):243–253

    Article  CAS  PubMed  Google Scholar 

  138. Barberi T et al (2007) Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med 13(5):642–648

    Article  CAS  PubMed  Google Scholar 

  139. Darabi R et al (2011) Functional myogenic engraftment from mouse iPS cells. Stem Cell Rev 7(4):948–957

    Article  PubMed  PubMed Central  Google Scholar 

  140. Darabi R et al (2009) Engraftment of embryonic stem cell-derived myogenic progenitors in a dominant model of muscular dystrophy. Exp Neurol 220(1):212–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Zheng JK et al (2006) Skeletal myogenesis by human embryonic stem cells. Cell Res 16(8):713–722

    Article  CAS  PubMed  Google Scholar 

  142. Yamanaka S et al (2008) Pluripotency of embryonic stem cells. Cell Tissue Res 331(1):5–22

    Article  PubMed  Google Scholar 

  143. Kim D et al (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4(6):472–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Okita K et al (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322(5903):949–953

    Article  CAS  PubMed  Google Scholar 

  145. Judson RL et al (2009) Embryonic stem cell-specific microRNAs promote induced pluripotency. Nat Biotechnol 27(5):459–461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Park IH et al (2008) Disease-specific induced pluripotent stem cells. Cell 134(5):877–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Yamanaka S (2010) Patient-specific pluripotent stem cells become even more accessible. Cell Stem Cell 7(1):1–2

    Article  CAS  PubMed  Google Scholar 

  148. Mizuno Y et al (2010) Generation of skeletal muscle stem/progenitor cells from murine induced pluripotent stem cells. FASEB J 24(7):2245–2253

    Article  CAS  PubMed  Google Scholar 

  149. Kazuki Y et al (2010) Complete genetic correction of ips cells from Duchenne muscular dystrophy. Mol Ther 18(2):386–393

    Article  CAS  PubMed  Google Scholar 

  150. Young CS et al (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

    Article  CAS  PubMed  Google Scholar 

  151. Fairclough LC et al (2015) Tumour necrosis factor receptor I blockade shows that TNF-dependent and TNF-independent mechanisms synergise in TNF receptor associated periodic syndrome. Eur J Immunol 45(10):2937–2944

    Article  CAS  PubMed  Google Scholar 

  152. Foster TC et al (2008) Viral vector-mediated delivery of estrogen receptor-alpha to the hippocampus improves spatial learning in estrogen receptor-alpha knockout mice. Mol Ther 16(9):1587–1593

    Article  CAS  PubMed Central  Google Scholar 

  153. Bachrach E et al (2004) Systemic delivery of human microdystrophin to regenerating mouse dystrophic muscle by muscle progenitor cells. Proc Natl Acad Sci U S A 101(10):3581–3586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Ikemoto M et al (2007) Autologous transplantation of SM/C-2.6(+) satellite cells transduced with micro-dystrophin CS1 cDNA by lentiviral vector into mdx mice. Mol Ther 15(12):2178–2185

    Article  CAS  Google Scholar 

  155. Hacein-Bey-Abina S et al (2008) Insertional oncogenesis in 4 patients after retrovirus-mediated gene therapy of SCID-X1. J Clin Invest 118(9):3132–3142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Hollinger K, Chamberlain JS (2015) Viral vector-mediated gene therapies. Curr Opin Neurol 28(5):522–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Buning H et al (2003) AAV-based gene transfer. Curr Opin Mol Ther 5(4):367–375

    PubMed  Google Scholar 

  158. Louboutin JP, Wang L, Wilson JM (2005) Gene transfer into skeletal muscle using novel AAV serotypes. J Gene Med 7(4):442–451

    Article  CAS  PubMed  Google Scholar 

  159. Bowles DE et al (2012) Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther 20(2):443–455

    Article  CAS  PubMed  Google Scholar 

  160. Yang Q et al (2012) AAV-based shRNA silencing of NF-kappaB ameliorates muscle pathologies in mdx mice. Gene Ther 19(12):1196–1204

    Article  CAS  PubMed  Google Scholar 

  161. Reay DP et al (2012) Effect of nuclear factor kappaB inhibition on serotype 9 adeno-associated viral (AAV9) minidystrophin gene transfer to the mdx mouse. Mol Med 18:466–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Aartsma-Rus A (2012) Overview on DMD exon skipping. Methods Mol Biol 867:97–116

    Article  CAS  PubMed  Google Scholar 

  163. Wein N et al (2010) Efficient bypass of mutations in dysferlin deficient patient cells by antisense-induced exon skipping. Hum Mutat 31(2):136–142

    Article  CAS  PubMed  Google Scholar 

  164. Kinali M et al (2009) Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8(10):918–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Vila MC et al (2015) Elusive sources of variability of dystrophin rescue by exon skipping. Skelet Muscle 5:44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  166. Mendell JR et al (2016) Longitudinal effect of eteplirsen versus historical control on ambulation in Duchenne muscular dystrophy. Ann Neurol 79(2):257–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Haas M et al (2015) European Medicines Agency review of ataluren for the treatment of ambulant patients aged 5 years and older with Duchenne muscular dystrophy resulting from a nonsense mutation in the dystrophin gene. Neuromuscul Disord 25(1):5–13

    Article  PubMed  Google Scholar 

  168. Quenneville SP et al (2007) Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: human cells and primate models. Mol Ther 15(2):431–438

    Article  CAS  PubMed  Google Scholar 

  169. Le Guiner C et al (2014) Forelimb treatment in a large cohort of dystrophic dogs supports delivery of a recombinant AAV for exon skipping in Duchenne patients. Mol Ther 22(11):1923–1935

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Chapdelaine P et al (2010) Meganucleases can restore the reading frame of a mutated dystrophin. Gene Ther 17(7):846–858

    Article  CAS  PubMed  Google Scholar 

  171. Ousterout DG et al (2013) Reading frame correction by targeted genome editing restores dystrophin expression in cells from Duchenne muscular dystrophy patients. Mol Ther 21(9):1718–1726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Jinek M et al (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821

    Article  CAS  PubMed  Google Scholar 

  173. Mali P et al (2013) RNA-guided human genome engineering via Cas9. Science 339(6121):823–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Long C et al (2014) Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science 345(6201):1184–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Long C et al (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351(6271):400–403

    Article  CAS  PubMed  Google Scholar 

  177. Godfrey C et al (2015) How much dystrophin is enough: the physiological consequences of different levels of dystrophin in the mdx mouse. Hum Mol Genet 24(15):4225–4237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to apologise to all authors whose work has not been reported here due to space limitations. This work has been supported with the contribution of “Opening The Future” Campaign [EJJ-OPTFUT-02010] CARIPLO 2015_0634, FWO (#G088715N, #G060612N, #G0A8813N), GOA (EJJ-C2161-GOA/11/012), IUAP-VII/07 (EJJ-C4851-17/07-P) and OT#09-053 (EJJ-C0420-OT/09/053) grants. We would also like to thank Rondoufonds voor Duchenne Onderzoek for kind donations.

Author information

Authors and Affiliations

  1. Translational Cardiomyology Lab, Stem Cell Institute Leuven, Stem Cell Biology and Embryology Unit, Department of Development and Regeneration, KU Leuven, Leuven, Belgium

    Robin Duelen, Domiziana Costamagna & Maurilio Sampaolesi

  2. Division of Human Anatomy, Department of Public Health, Experimental and Forensic Medicine, University of Pavia, Pavia, Italy

    Maurilio Sampaolesi

Authors
  1. Robin Duelen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Domiziana Costamagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurilio Sampaolesi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maurilio Sampaolesi .

Editor information

Editors and Affiliations

  1. Institute for Liberal Arts, Environment and Society, Tokyo Institute of Technology, Tokyo, Japan

    Kunihiro Sakuma

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Duelen, R., Costamagna, D., Sampaolesi, M. (2017). Stem Cell Therapy in Muscle Degeneration. In: Sakuma, K. (eds) The Plasticity of Skeletal Muscle. Springer, Singapore. https://doi.org/10.1007/978-981-10-3292-9_3

Download citation

  • DOI: https://doi.org/10.1007/978-981-10-3292-9_3

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-10-3291-2

  • Online ISBN: 978-981-10-3292-9

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation