PM&R
Volume 1, Issue 6 , Pages 547-559 , June 2009

Mesenchymal Stem Cells: Emerging Therapy for Duchenne Muscular Dystrophy

  • Chad D. Markert, PhD

      Affiliations

    • Department of Neurology, School of Medicine, and Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC†
    • ,
  • Anthony Atala, MD

      Affiliations

    • Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC‡
    • ,
  • Jennifer K. Cann, BA

      Affiliations

    • Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC§
    • ,
  • George Christ, PhD

      Affiliations

    • Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC
    • ,
  • Mark Furth, PhD

      Affiliations

    • Wake Forest Institute for Regenerative Medicine, Wake Forest University Health Sciences, Winston-Salem, NC∥
    • ,
  • Fabrisia Ambrosio, PT, PhD

      Affiliations

    • Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA#
    • ,
  • Martin K. Childers, DO, PhD

      Affiliations

    • Department of Neurology, School of Medicine, and Wake Forest University Health Sciences, Medical Center Boulevard, Winston-Salem, NC 27157-1078⁎⁎
    • Corresponding Author InformationAddress correspondence to: M.K.C.

Received 6 November 2008 ,Accepted 25 February 2009.

References 

  1. Hoffman EP, Brown RH, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 1987;51:919–928
  2. Petrof BJ. The molecular basis of activity-induced muscle injury in Duchenne muscular dystrophy. Mol Cell Biochem. 1998;179:111–123
  3. Petrof BJ. Molecular pathophysiology of myofiber injury in deficiencies of the dystrophin-glycoprotein complex. Am J Phys Med Rehabil. 2002;81:S162–S174
  4. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493–495
  5. Oexle K, Kohlschutter A. Cause of progression in Duchenne muscular dystrophy: impaired differentiation more probable than replicative aging. Neuropediatrics. 2001;32:123–129
  6. Lysaght MJ, Jaklenec A, Deweerd E. Great expectations: private sector activity in tissue engineering, regenerative medicine, and stem cell therapeutics. Tissue Eng Part A. 2008;14:305–315
  7. Daftary AS, Crisanti M, Kalra M, Wong B, Amin R. Effect of long-term steroids on cough efficiency and respiratory muscle strength in patients with Duchenne muscular dystrophy. Pediatrics. 2007;119:e320–e324
  8. Williams IA, Allen DG. Intracellular calcium handling in ventricular myocytes from mdx mice. Am J Physiol Heart Circ Physiol. 2007;292:H846–H855
  9. Nakatani M, Takehara Y, Sugino H, et al. Transgenic expression of a myostatin inhibitor derived from follistatin increases skeletal muscle mass and ameliorates dystrophic pathology in mdx mice. FASEB J. 2008;22:477–487
  10. Wagner KR, Fleckenstein JL, Amato AA, et al. A phase I/IItrial of MYO-029 in adult subjects with muscular dystrophy. Ann Neurol. 2008;63:561–571
  11. Hamed SA. Drug evaluation: PTC-124—a potential treatment of cystic fibrosis and Duchenne muscular dystrophy. IDrugs. 2006;9:783–789
  12. Hirawat S, Welch EM, Elfring GL, et al. Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J Clin Pharmacol. 2007;47:430–444
  13. Wilton S. PTC124, nonsense mutations and Duchenne muscular dystrophy. Neuromuscul Disord. 2007;17:719–720
  14. Badalamente MA, Stracher A. Delay of muscle degeneration and necrosis in mdx mice by calpain inhibition. Muscle Nerve. 2000;23:106–111
  15. Nonaka I, Ishiura S, Takagi A, Sugita H. Therapeutic trial with protease inhibitor (leupeptin) in chicken muscular dystrophy (A histologic and histochemical study). Acta Neuropathol. 1982;58:279–285
  16. Stracher A. Calpain inhibitors as therapeutic agents in nerve and muscle degeneration. Ann N Y Acad Sci. 1999;884:52–59
  17. Kajimoto H, Ishigaki K, Okumura K, et al. Beta-blocker therapy for cardiac dysfunction in patients with muscular dystrophy. Circ J. 2006;70:991–994
  18. Tidball JG, Wehling-Henricks M. The role of free radicals in the pathophysiology of muscular dystrophy. J Appl Physiol. 2007;102:1677–1686
  19. Brunelli S, Sciorati C, D'Antona G, et al. Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc Natl Acad Sci U S A. 2007;104:264–269
  20. Zhou GQ, Xie HQ, Zhang SZ, Yang ZM. Current understanding of dystrophin-related muscular dystrophy and therapeutic challenges ahead. Chin Med J (Engl). 2006;119:1381–1391
  21. Sampaolesi M, Blot S, D'Antona G, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature. 2006;444:574–579
  22. Duan D. Challenges and opportunities in dystrophin-deficient cardiomyopathy gene therapy. Hum Mol Genet. 2006;15:R253–R261Spec No 2.
  23. Rodino-Klapac LR, Janssen PM, Montgomery CL, et al. A translational approach for limb vascular delivery of the micro-dystrophin gene without high volume or high pressure for treatment of Duchenne muscular dystrophy. J Transl Med. 2007;5:45
  24. van Deutekom JC, Janson AA, Ginjaar IB, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med. 2007;357:2677–2686
  25. Mattei E, Corbi N, Di Certo MG, et al. Utrophin up-regulation by an artificial transcription factor in transgenic mice. PLoS ONE. 2007;2:e774
  26. Bostick B, Yue Y, Long C, Duan D. Prevention of dystrophin-deficient cardiomyopathy in twenty-one-month-old carrier mice by mosaic dystrophin expression or complementary dystrophin/utrophin expression. Circ Res. 2008;102:121–130
  27. Cerletti M, Negri T, Cozzi F, et al. Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther. 2003;10:750–757
  28. Gillis JM. An attempt of gene therapy in Duchenne muscular dystrophy: overexpression of utrophin in transgenic mdx mice. Acta Neurol Belg. 2000;100:146–150
  29. Hirst RC, McCullagh KJ, Davies KE. Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol. 2005;24:209–216
  30. Odom GL, Gregorevic P, Chamberlain JS. Viral-mediated gene therapy for the muscular dystrophies: successes, limitations and recent advances. Biochim Biophys Acta. 2007;1772:243–262
  31. Laird DJ, von Andrian UH, Wagers AJ. Stem cell trafficking in tissue development, growth, and disease. Cell. 2008;132:612–630
  32. Price FD, Kuroda K, Rudnicki MA. Stem cell based therapies to treat muscular dystrophy. Biochim Biophys Acta. 2007;1772:272–283
  33. Huard J, Cao B, Qu-Petersen Z. Muscle-derived stem cells: potential for muscle regeneration. Birth Defects Res C Embryo Today. 2003;69:230–237
  34. Borycki AG, Brunk B, Tajbakhsh S, Buckingham M, Chiang C, Emerson CP. Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development. 1999;126:4053–4063
  35. Cossu G. Fusion of bone marrow-derived stem cells with striated muscle may not be sufficient to activate muscle genes. J Clin Invest. 2004;114:1540–1543
  36. Maltin CA, Delday MI, Sinclair KD, Steven J, Sneddon AA. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction. 2001;122:359–374
  37. Christ B, Brand-Saberi B. Limb muscle development. Int J Dev Biol. 2002;46:905–914
  38. Relaix F. Skeletal muscle progenitor cells: from embryo to adult. Cell Mol Life Sci. 2006;63:1221–1225
  39. Haberland M, Arnold MA, McAnally J, Phan D, Kim Y, Olson EN. Regulation of HDAC9 gene expression by MEF2 establishes a negative-feedback loop in the transcriptional circuitry of muscle differentiation. Mol Cell Biol. 2007;27:518–525
  40. Buckingham M. Muscle differentiation (Which myogenic factors make muscle?). Curr Biol. 1994;4:61–63
  41. Buckingham M, Bajard L, Chang T, et al. The formation of skeletal muscle: from somite to limb. J Anat. 2003;202:59–68
  42. Shi X, Garry DJ. Muscle stem cells in development, regeneration, and disease. Genes Dev. 2006;20:1692–1708
  43. Cossu G, Borello U. Wnt signaling and the activation of myogenesis in mammals. EMBO J. 1999;18:6867–6872
  44. Yen BL, Huang HI, Chien CC, et al. Isolation of multipotent cells from human term placenta. Stem Cells. 2005;23:3–9
  45. Wagers AJ, Christensen JL, Weissman IL. Cell fate determination from stem cells. Gene Ther. 2002;9:606–612
  46. Kuang S, Gillespie MA, Rudnicki MA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell. 2008;2:22–31
  47. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341–347
  48. Thomas ED, Lochte HL, Lu WC, Ferrebee JW. Intravenous infusion of bone marrow in patients receiving radiation and chemotherapy. N Engl J Med. 1957;257:491–496
  49. Ema H, Morita Y, Yamazaki S, et al. Adult mouse hematopoietic stem cells: purification and single-cell assays. Nat Protoc. 2006;1:2979–2987
  50. Cao YA, Wagers AJ, Beilhack A, et al. Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc Natl Acad Sci U S A. 2004;101:221–226
  51. Bryder D, Rossi DJ, Weissman IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol. 2006;169:338–346
  52. Schoemans H, Theunissen K, Maertens J, Boogaerts M, Verfaillie C, Wagner J. Adult umbilical cord blood transplantation: a comprehensive review. Bone Marrow Transplant. 2006;38:83–93
  53. Broxmeyer HE, Douglas GW, Hangoc G, et al. Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc Natl Acad Sci U S A. 1989;86:3828–3832
  54. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties (Lessons for and from the crypt). Development. 1990;110:1001–1020
  55. Giannakis M, Stappenbeck TS, Mills JC, et al. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem. 2006;281:11292–11300
  56. Dekaney CM, Rodriguez JM, Graul MC, Henning SJ. Isolation and characterization of a putative intestinal stem cell fraction from mouse jejunum. Gastroenterology. 2005;129:1567–1580
  57. Blanpain C, Fuchs E. Epidermal stem cells of the skin. Annu Rev Cell Dev Biol. 2006;22:339–373
  58. Weissman IL, Anderson DJ, Gage F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol. 2001;17:387–403
  59. Metcalf D. Concise review: hematopoietic stem cells and tissue stem cells: current concepts and unanswered questions. Stem Cells. 2007;25:2390–2395
  60. Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol. 2002;30:896–904
  61. Presnell SC, Petersen B, Heidaran M. Stem cells in adult tissues. Semin Cell Dev Biol. 2002;13:369–376
  62. Gage FH. Mammalian neural stem cells. Science. 2000;287:1433–1438
  63. Anversa P, Kajstura J, Leri A, Bolli R. Life and death of cardiac stem cells: a paradigm shift in cardiac biology. Circulation. 2006;113:1451–1463
  64. Crisan M, Yap S, Casteilla L, et al. A Perivascular Origin for Mesenchymal Stem Cells in Multiple Human Organs. Cell Stem Cell. 2008;3:301–313
  65. Gimble J, Guilak F. Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy. 2003;5:362–369
  66. Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9:641–650
  67. Caplan AI. The mesengenic process. Clin Plast Surg. 1994;21:429–435
  68. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–74
  69. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol. 1976;4:267–274
  70. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284:143–147
  71. Pittenger M, Vanguri P, Simonetti D, Young R. Adult mesenchymal stem cells: potential for muscle and tendon regeneration and use in gene therapy. J Musculoskelet Neuronal Interact. 2002;2:309–320
  72. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105:1815–1822
  73. Alviano F, Fossati V, Marchionni C, et al. Term Amniotic membrane is a high throughput source for multipotent Mesenchymal Stem Cells with the ability to differentiate into endothelial cells in vitro. BMC Dev Biol. 2007;7:11
  74. Fox JM, Chamberlain G, Ashton BA, Middleton J. Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol. 2007;137:491–502
  75. Gawronska-Kozak B, Manuel JA, Prpic V. Ear mesenchymal stem cells (EMSC) can differentiate into spontaneously contracting muscle cells. J Cell Biochem. 2007;102:122–135
  76. Jackson L, Jones DR, Scotting P, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med. 2007;53:121–127
  77. Rodriguez AM, Pisani D, Dechesne CA, et al. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med. 2005;201:1397–1405
  78. Schrepfer S, Deuse T, Lange C, et al. Simplified protocol to isolate, purify, and culture expand mesenchymal stem cells. Stem Cells Dev. 2007;16:105–107
  79. Soncini M, Vertua E, Gibelli L, et al. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med. 2007;1:296–305
  80. Tavian M, Peault B. Embryonic development of the human hematopoietic system. Int J Dev Biol. 2005;49:243–250
  81. Parolini O, Alviano F, Bagnara GP, et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells. 2008;26:300–311
  82. Peault B, Rudnicki M, Torrente Y, et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther. 2007;15:867–877
  83. Hughes SM, Blau HM. Migration of myoblasts across basal lamina during skeletal muscle development. Nature. 1990;345:350–353
  84. Yokota T, Lu QL, Morgan JE, et al. Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J Cell Sci. 2006;119:2679–2687
  85. Christov C, Chretien F, bou-Khalil R, et al. Muscle satellite cells and endothelial cells: close neighbors and privileged partners. Mol Biol Cell. 2007;18:1397–1409
  86. De Angelis L, Berghella L, Coletta M, et al. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol. 1999;147:869–878
  87. Dellavalle A, Sampaolesi M, Tonlorenzi R, et al. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9:255–267
  88. Ramirez M, Lucia A, Gomez-Gallego F, et al. Mobilisation of mesenchymal cells into blood in response to skeletal muscle injury. Br J Sports Med. 2006;40:719–722
  89. Sampaolesi M, Torrente Y, Innocenzi A, et al. Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science. 2003;301:487–492
  90. Traktuev DO, Merfeld-Clauss S, Li J, et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res. 2008;102:77–85
  91. Kardon G, Campbell JK, Tabin CJ. Local extrinsic signals determine muscle and endothelial cell fate and patterning in the vertebrate limb. Dev Cell. 2002;3:533–545
  92. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25:2739–2749
  93. Montarras D, Morgan J, Collins C, et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science. 2005;309:2064–2067
  94. Parenteau NL, Nolte CM, Bilbo P, et al. Epidermis generated in vitro: practical considerations and applications. J Cell Biochem. 1991;45:245–251
  95. Oberpenning F, Meng J, Yoo JJ, Atala A. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat Biotechnol. 1999;17:149–155
  96. Uchida N, Buck DW, He D, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A. 2000;97:14720–14725
  97. Gage FH. Mammalian neural stem cells. Science. 2000;287:1433–1438
  98. Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, van der Kooy D. Is there a neural stem cell in the mammalian forebrain?. Trends Neurosci. 1996;19:387–393
  99. Schmelzer E, Zhang L, Bruce A, et al. Human hepatic stem cells from fetal and postnatal donors. J Exp Med. 2007;204:1973–1987
  100. Wauthier E, Schmelzer E, Turner W, et al. Hepatic stem cells and hepatoblasts: identification, isolation, and ex vivo maintenance. Methods Cell Biol. 2008;86:137–225
  101. Turner WS, Seagle C, Galanko JA, et al. Nuclear magnetic resonance metabolomic footprinting of human hepatic stem cells and hepatoblasts cultured in hyaluronan-matrix hydrogels. Stem Cells. 2008;26:1547–1555
  102. Kubota H, Avarbock MR, Brinster RL. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci U S A. 2004;101:16489–16494
  103. Pittenger M, Vanguri P, Simonetti D, Young R. Adult mesenchymal stem cells: potential for muscle and tendon regeneration and use in gene therapy. J Musculoskelet Neuronal Interact. 2002;2:309–320
  104. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997;276:71–74
  105. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD. Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation. 2002;105:93–98
  106. Sampaolesi M, Blot S, D'Antona G, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature. 2006;444:574–579
  107. Jackson L, Jones DR, Scotting P, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med. 2007;53:121–127
  108. Mizuno H, Hyakusoku H. Mesengenic potential and future clinical perspective of human processed lipoaspirate cells. J Nippon Med Sch. 2003;70:300–306
  109. Barberi T, Willis LM, Socci ND, Studer L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med. 2005;2:e161
  110. Wise CJ, Watt DJ, Jones GE. Conversion of dermal fibroblasts to a myogenic lineage is induced by a soluble factor derived from myoblasts. J Cell Biochem. 1996;61:363–374
  111. Chan J, O'Donoghue K, de la Fuente J, et al. Human fetal mesenchymal stem cells as vehicles for gene delivery. Stem Cells. 2005;23:93–102
  112. Mizuno H, Hyakusoku H. Mesengenic potential and future clinical perspective of human processed lipoaspirate cells. J Nippon Med Sch. 2003;70:300–306
  113. Li Y, Zhang C, Xiong F, et al. Comparative study of mesenchymal stem cells from C57BL/10 and mdx mice. BMC Cell Biol. 2008;9:24
  114. Barberi T, Bradbury M, Dincer Z, Panagiotakos G, Socci ND, Studer L. Derivation of engraftable skeletal myoblasts from human embryonic stem cells. Nat Med. 2007;13:642–648
  115. Chan J, O'Donoghue K, Gavina M, et al. Galectin-1 induces skeletal muscle differentiation in human fetal mesenchymal stem cells and increases muscle regeneration. Stem Cells. 2006;24:1879–1891
  116. Di Rocco G, Iachininoto MG, Tritarelli A, et al. Myogenic potential of adipose-tissue-derived cells. J Cell Sci. 2006;119:2945–2952
  117. Gang EJ, Jeong JA, Hong SH, et al. Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells. 2004;22:617–624
  118. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–228
  119. Invernici G, Emanueli C, Madeddu P, et al. Human fetal aorta contains vascular progenitor cells capable of inducing vasculogenesis, angiogenesis, and myogenesis in vitro and in a murine model of peripheral ischemia. Am J Pathol. 2007;170:1879–1892
  120. Shang YC, Wang SH, Xiong F, et al. Wnt3a signaling promotes proliferation, myogenic differentiation, and migration of rat bone marrow mesenchymal stem cells. Acta Pharmacol Sin. 2007;28:1761–1774
  121. Singh R, Artaza JN, Taylor WE, Gonzalez-Cadavid NF, Bhasin S. Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptor-mediated pathway. Endocrinology. 2003;144:5081–5088
  122. Shefer G, Wleklinski-Lee M, Yablonka-Reuveni Z. Skeletal muscle satellite cells can spontaneously enter an alternative mesenchymal pathway. J Cell Sci. 2004;117:5393–5404
  123. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;126:677–689
  124. Engler AJ, Sweeney HL, Discher DE, Schwarzbauer JE. Extracellular matrix elasticity directs stem cell differentiation. J Musculoskelet Neuronal Interact. 2007;7:335
  125. Liu Y, Yan X, Sun Z, et al. Flk-1+ adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx mice. Stem Cells Dev. 2007;16:695–706
  126. Bossolasco P, Corti S, Strazzer S, et al. Skeletal muscle differentiation potential of human adult bone marrow cells. Exp Cell Res. 2004;295:66–78
  127. Dezawa M, Ishikawa H, Itokazu Y, et al. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science. 2005;309:314–317
  128. Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279:1528–1530
  129. Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve. 1995;18:1417–1426
  130. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001;7:211–228
  131. Liu Y, Yan X, Sun Z, et al. Flk-1+ adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx mice. Stem Cells Dev. 2007;16:695–706
  132. De Coppi P, Bartsch G, Siddiqui MM, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25:100–106
  133. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, et al. Amniotic fluid as a novel source of mesenchymal stem cells for therapeutic transplantation. Blood. 2003;102:1548–1549
  134. Kaviani A, Perry TE, Dzakovic A, Jennings RW, Ziegler MM, Fauza DO. The amniotic fluid as a source of cells for fetal tissue engineering. J Pediatr Surg. 2001;36:1662–1665
  135. Kunisaki SM, Armant M, Kao GS, Stevenson K, Kim H, Fauza DO. Tissue engineering from human mesenchymal amniocytes: a prelude to clinical trials. J Pediatr Surg. 2007;42:974–979
  136. Trelford JD, Trelford-Sauder M. The amnion in surgery, past and present. Am J Obstet Gynecol. 1979;134:833–845
  137. Bili C, Divane A, Apessos A, et al. Prenatal diagnosis of common aneuploidies using quantitative fluorescent PCR. Prenat Diagn. 2002;22:360–365
  138. Torricelli F, Brizzi L, Bernabei PA, et al. Identification of hematopoietic progenitor cells in human amniotic fluid before the 12th week of gestation. Ital J Anat Embryol. 1993;98:119–126
  139. Wakitani S, Saito T, Caplan AI. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve. 1995;18:1417–1426
  140. Muguruma Y, Reyes M, Nakamura Y, et al. In vivo and in vitro differentiation of myocytes from human bone marrow-derived multipotent progenitor cells. Exp Hematol. 2003;31:1323–1330
  141. Bianco P, Gehron RP. Marrow stromal stem cells. J Clin Invest. 2000;105:1663–1668
  142. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2:313–319
  143. Gawronska-Kozak B, Manuel JA, Prpic V. Ear mesenchymal stem cells (EMSC) can differentiate into spontaneously contracting muscle cells. J Cell Biochem. 2007;102:122–135
  144. Chan J, Waddington SN, O'Donoghue K, et al. Widespread distribution and muscle differentiation of human fetal mesenchymal stem cells after intrauterine transplantation in dystrophic mdx mouse. Stem Cells. 2007;25:875–884
  145. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 2001;44:1928–1942
  146. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol. 2007;213:341–347
  147. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25:2739–2749
  148. Chang CJ, Yen ML, Chen YC, et al. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells. 2006;24:2466–2477
  149. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood. 2007;110:3499–3506
  150. Wolbank S, Peterbauer A, Fahrner M, et al. Dose-dependent immunomodulatory effect of human stem cells from amniotic membrane: a comparison with human mesenchymal stem cells from adipose tissue. Tissue Eng. 2007;13:1173–1183
  151. Wolf D, Wolf AM. Mesenchymal stem cells as cellular immunosuppressants. Lancet. 2008;371:1553–1554
  152. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31:890–896
  153. Niederkorn JY. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat Immunol. 2006;7:354–359
  154. Mahmood A, Lu D, Lu M, Chopp M. Treatment of traumatic brain injury in adult rats with intravenous administration of human bone marrow stromal cells. Neurosurgery. 2003;53:697–702
  155. Chen J, Li Y, Wang L, et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke. 2001;32:1005–1011
  156. Berry MF, Engler AJ, Woo YJ, et al. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol. 2006;290:H2196–H2203
  157. Iyer SS, Rojas M. Anti-inflammatory effects of mesenchymal stem cells: novel concept for future therapies. Expert Opin Biol Ther. 2008;8:569–581
  158. Uccelli A, Pistoia V, Moretta L. Mesenchymal stem cells: a new strategy for immunosuppression?. Trends Immunol. 2007;28:219–226
  159. Ferrari G, Cusella-De AG, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 1998;279:1528–1530
  160. Gawronska-Kozak B, Manuel JA, Prpic V. Ear mesenchymal stem cells (EMSC) can differentiate into spontaneously contracting muscle cells. J Cell Biochem. 2007;102:122–135
  161. Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U. Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol Reprod. 2007;77:577–588
  162. Jackson L, Jones DR, Scotting P, Sottile V. Adult mesenchymal stem cells: differentiation potential and therapeutic applications. J Postgrad Med. 2007;53:121–127
  163. Kunisaki SM, Armant M, Kao GS, Stevenson K, Kim H, Fauza DO. Tissue engineering from human mesenchymal amniocytes: a prelude to clinical trials. J Pediatr Surg. 2007;42:974–979
  164. Liu Y, Yan X, Sun Z, et al. Flk-1+ adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx mice. Stem Cells Dev. 2007;16:695–706
  165. Qu-Petersen Z, Deasy B, Jankowski R, et al. Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol. 2002;157:851–864
  166. Tamagawa T, Oi S, Ishiwata I, Ishikawa H, Nakamura Y. Differentiation of mesenchymal cells derived from human amniotic membranes into hepatocyte-like cells in vitro. Hum Cell. 2007;20:77–84
  167. Zhao P, Ise H, Hongo M, Ota M, Konishi I, Nikaido T. Human amniotic mesenchymal cells have some characteristics of cardiomyocytes. Transplantation. 2005;79:528–535
  168. Goncalves MA, Swildens J, Holkers M, et al. Genetic complementation of human muscle cells via directed stem cell fusion. Mol Ther. 2008;16:741–748
  169. Laird DJ, von Andrian UH, Wagers AJ. Stem cell trafficking in tissue development, growth, and disease. Cell. 2008;132:612–630
  170. Kobinger GP, Louboutin JP, Barton ER, Sweeney HL, Wilson JM. Correction of the dystrophic phenotype by in vivo targeting of muscle progenitor cells. Hum Gene Ther. 2003;14:1441–1449
  171. Bertoni C, Rando TA. Dystrophin gene repair in mdx muscle precursor cells in vitro and in vivo mediated by RNA-DNA chimeric oligonucleotides. Hum Gene Ther. 2002;13:707–718
  172. Bujold M, Caron N, Camiran G, et al. Autotransplantation in mdx mice of mdx myoblasts genetically corrected by an HSV-1 amplicon vector. Cell Transplant. 2002;11:759–767
  173. Li S, Kimura E, Fall BM, et al. Stable transduction of myogenic cells with lentiviral vectors expressing a minidystrophin. Gene Ther. 2005;12:1099–1108
  174. Quenneville SP, Chapdelaine P, Skuk D, et al. Autologous transplantation of muscle precursor cells modified with a lentivirus for muscular dystrophy: human cells and primate models. Mol Ther. 2007;15:431–438
  175. Xiong F, Xiao S, Peng F, et al. Herpes simplex virus VP22 enhances adenovirus-mediated microdystrophin gene transfer to skeletal muscles in dystrophin-deficient (mdx) mice. Hum Gene Ther. 2007;18:490–501
  176. Bailo M, Soncini M, Vertua E, et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation. 2004;78:1439–1448
  177. Koc ON, Gerson SL, Cooper BW, et al. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J Clin Oncol. 2000;18:307–316
  178. Schenk S, Mal N, Finan A, et al. Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor. Stem Cells. 2007;25:245–251
  179. Seeger FH, Zeiher AM, Dimmeler S. Cell-enhancement strategies for the treatment of ischemic heart disease. Nat Clin Pract Cardiovasc Med. 2007;4:S110–S113
  180. Shyu WC, Lee YJ, Liu DD, Lin SZ, Li H. Homing genes, cell therapy and stroke. Front Biosci. 2006;11:899–907
  181. Voermans C, van Hennik PB, van der Schoot CE. Homing of human hematopoietic stem and progenitor cells: new insights, new challenges?. J Hematother Stem Cell Res. 2001;10:725–738
  182. Bachrach E, Perez AL, Choi YH, et al. Muscle engraftment of myogenic progenitor cells following intraarterial transplantation. Muscle Nerve. 2006;34:44–52
  183. Sampaolesi M, Torrente Y, Innocenzi A, et al. Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science. 2003;301:487–492
  184. Sampaolesi M, Blot S, D'Antona G, et al. Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature. 2006;444:574–579
  185. Torrente Y, Tremblay JP, Pisati F, et al. Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol. 2001;152:335–348
  186. Torrente Y, Camirand G, Pisati F, et al. Identification of a putative pathway for the muscle homing of stem cells in a muscular dystrophy model. J Cell Biol. 2003;162:511–520
  187. Urbich C, Dimmeler S. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res. 2004;95:343–353
  188. Hogaboam CM, Carpenter KJ, Schuh JM, Proudfoot AA, Bridger G, Buckland KF. The therapeutic potential in targeting CCR5 and CXCR4 receptors in infectious and allergic pulmonary disease. Pharmacol Ther. 2005;107:314–328
  189. Laird DJ, von Andrian UH, Wagers AJ. Stem cell trafficking in tissue development, growth, and disease. Cell. 2008;132:612–630
  190. Bailo M, Soncini M, Vertua E, et al. Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation. 2004;78:1439–1448
  191. Ueta M, Kweon MN, Sano Y, et al. Immunosuppressive properties of human amniotic membrane for mixed lymphocyte reaction. Clin Exp Immunol. 2002;129:464–470
  192. Kim JC, Tseng SC. Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea. 1995;14:473–484
  193. Trelford JD, Trelford-Sauder M. The amnion in surgery, past and present. Am J Obstet Gynecol. 1979;134:833–845
  194. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103:4619–4621
  195. Munn DH, Zhou M, Attwood JT, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998;281:1191–1193
  196. Galvez BG, Sampaolesi M, Brunelli S, et al. Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J Cell Biol. 2006;174:231–243
  197. Meisel R, Zibert A, Laryea M, Gobel U, Daubener W, Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood. 2004;103:4619–4621
  198. Straino S, Germani A, Di Carlo A, et al. Enhanced arteriogenesis and wound repair in dystrophin-deficient mdx mice. Circulation. 2004;110:3341–3348
  199. Brunelli S, Sciorati C, D'Antona G, et al. Nitric oxide release combined with nonsteroidal antiinflammatory activity prevents muscular dystrophy pathology and enhances stem cell therapy. Proc Natl Acad Sci U S A. 2007;104:264–269
  200. Palermo AT, LaBarge MA, Doyonnas R, Pomerantz J, Blau HM. Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev Biol. 2005;279:336–344
  201. Ambrosio F, Ferrari RJ, Fitzgerald GK, Carvell GE, Boninger ML, Huard J. Functional overloading of dystrophic mice enhances muscle-derived stem cell contribution to muscle contractile capacity. Arch Phys Med Rehab. 2009;90:66–73

 Disclosure Key can be found on the Table of Contents and at www.pmrjournal.org

PII: S1934-1482(09)00223-8

doi: 10.1016/j.pmrj.2009.02.013

PM&R
Volume 1, Issue 6 , Pages 547-559 , June 2009

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