Perspectives of stem cell therapy in Duchenne muscular dystrophy

FEBS Journal

Volumn 280, Issue 17, 2013, Pages 4251-4262

  Meregalli, Mirella ^a   Farini, Andrea ^a   Belicchi, Marzia ^a   Parolini, Daniele ^a   Cassinelli, Letizia ^a   Razini, Paola ^a   Sitzia, Clementina ^a   Torrente, Yvan ^a  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

Author keywords

Duchenne muscular dystrophy; stem cells; therapy

Indexed keywords

CADHERIN; CD133 ANTIGEN; CD34 ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; DESMIN; MICRORNA 31; MYOGENIC FACTOR; MYOGENIC FACTOR 5; VIMENTIN; VON WILLEBRAND FACTOR;

AUTOTRANSPLANTATION; BASEMENT MEMBRANE; CYTOSKELETON; DUCHENNE MUSCULAR DYSTROPHY; GENE MUTATION; HUMAN; MESODERM; MONONUCLEAR CELL; MOUSE; MUSCLE ATROPHY; MUSCLE REGENERATION; MUSCLE WEAKNESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; STEM CELL TRANSPLANTATION;

DUCHENNE MUSCULAR DYSTROPHY; STEM CELLS; THERAPY;

ANIMALS; HUMANS; MUSCULAR DYSTROPHY, DUCHENNE; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE THERAPY;

EID: 84882725695     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12083     Document Type: Review

References (107)

1. Ferrari G, Cusella-De Angelis G, Coletta M, Paolucci E, Stornaiuolo A, Cossu G, &, Mavilio F, (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528-1530.
2. Blau HM, Dhawan J, &, Pavlath GK, (1993) Myoblasts in pattern formation and gene therapy. Trends Genet 9, 269-274.
3. Sabourin LA, &, Rudnicki MA, (2000) The molecular regulation of myogenesis. Clin Genet 57, 16-25.
4. Crist CG, Montarras D, &, Buckingham M, (2012) Muscle satellite cells are primed for myogenesis but maintain quiescence with sequestration of Myf5 mRNA targeted by microRNA-31 in mRNP granules. Cell Stem Cell 11, 118-126.
5. Cooper RN, Tajbakhsh S, Mouly V, Cossu G, Buckingham M, &, Butler-Browne GS, (1999) In vivo satellite cell activation via Myf5 and MyoD in regenerating mouse skeletal muscle. J Cell Sci 112 (Pt 17), 2895-2901.
6. Cornelison DD, &, Wold BJ, (1997) Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev Biol 191, 270-283.
7. Knothe C, Boldt J, Zickmann B, Ballesteros M, Haufler G, Bruns F, &, Hempelmann G, (1993) Cardiac protection in heart surgery interventions by preventive drug administration before extracorporeal circulation. Studies with troponin T as a parameter for perioperative myocardial damage. Herz 18, 379-386.
8. Yablonka-Reuveni Z, &, Rivera AJ, (1994) Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 164, 588-603.
9. Emery AE, (2002) The muscular dystrophies. Lancet 359, 687-695.
10. Ray PN, Belfall B, Duff C, Logan C, Kean V, Thompson MW, Sylvester JE, Gorski JL, Schmickel RD, &, Worton RG, (1985) Cloning of the breakpoint of an X;21 translocation associated with Duchenne muscular 9 dystrophy. Nature 318, 672-675.
11. Emery AE, (1998) The muscular dystrophies. BMJ 317, 991-995.
12. Bertoni C, (2008) Clinical approaches in the treatment of Duchenne muscular dystrophy (DMD) using oligonucleotides. Front Biosci 13, 517-527.
13. 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, 1441-1444.
14. Biggar WD, Harris VA, Eliasoph L, &, Alman B, (2006) Long-term benefits of deflazacort treatment for boys with Duchenne muscular dystrophy in their second decade. Neuromuscul Disord 16, 249-255.
15. McClorey G, Fall AM, Moulton HM, Iversen PL, Rasko JE, Ryan M, Fletcher S, &, Wilton SD, (2006) Induced dystrophin exon skipping in human muscle explants. Neuromuscul Disord 16, 583-590.
16. Hamed SA, (2006) Drug evaluation: PTC-124-a potential treatment of cystic fibrosis and Duchenne muscular dystrophy. IDrugs 9, 783-789.
17. Hyser CL, &, Mendell JR, (1988) Recent advances in Duchenne and Becker muscular dystrophy. Neurol Clin 6, 429-453.
18. Owonikoko T, Agha M, Balassanian R, Smith R, &, Raptis A, (2007) Gemtuzumab therapy for isolated extramedullary AML relapse following allogeneic stem-cell transplant. Nat Clin Pract Oncol 4, 491-495.
19. Singh N, Pillay V, &, Choonara YE, (2007) Advances in the treatment of Parkinson's disease. Prog Neurobiol 81, 29-44.
20. Grounds MD, Garrett KL, Lai MC, Wright WE, &, Beilharz MW, (1992) Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes. Cell Tissue Res 267, 99-104.
21. Cossu G, (1997) Unorthodox myogenesis: possible developmental significance and implications for tissue histogenesis and regeneration. Histol Histopathol 12, 755-760.
22. Sarig R, Baruchi Z, Fuchs O, Nudel U, &, Yaffe D, (2006) Regeneration and transdifferentiation potential of muscle-derived stem cells propagated as myospheres. Stem Cells 24, 1769-1778.
23. Tamaki T, Okada Y, Uchiyama Y, Tono K, Masuda M, Wada M, Hoshi A, Ishikawa T, &, Akatsuka A, (2007) Clonal multipotency of skeletal muscle-derived stem cells between mesodermal and ectodermal lineage. Stem Cells 25, 2283-2290.
24. Cossu G, &, Bianco P, (2003) Mesoangioblasts-vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev 13, 537-542.
25. Benchaouir R, Meregalli M, Farini A, D'Antona G, Belicchi M, Goyenvalle A, Battistelli M, Bresolin N, Bottinelli R, Garcia L, et al,. (2007) Restoration of human dystrophin following transplantation of exon-skipping-engineered DMD patient stem cells into dystrophic mice. Cell Stem Cell 1, 646-657.
26. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, &, Marshak DR, (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147.
27. Prockop DJ, (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276, 71-74.
28. 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, 257-266.
29. Sambasivan R, &, Tajbakhsh S, (2007) Skeletal muscle stem cell birth and properties. Semin Cell Dev Biol 18, 870-882.
30. Shi X, &, Garry DJ, (2006) Muscle stem cells in development, regeneration, and disease. Genes Dev 20, 1692-1708.
31. Whalen RG, Harris JB, Butler-Browne GS, &, Sesodia S, (1990) Expression of myosin isoforms during notexin-induced regeneration of rat soleus muscles. Dev Biol 141, 24-40.
32. 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, 2064-2067.
33. Cerletti M, Jurga S, Witczak CA, Hirshman MF, Shadrach JL, Goodyear LJ, &, Wagers AJ, (2008) Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134, 37-47.
34. Sacco A, Doyonnas R, Kraft P, Vitorovic S, &, Blau HM, (2008) Self-renewal and expansion of single transplanted muscle stem cells. Nature 456, 502-506.
35. Tanaka KK, Hall JK, Troy AA, Cornelison DD, Majka SM, &, Olwin BB, (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4, 217-225.
36. Price FD, Kuroda K, &, Rudnicki MA, (2007) Stem cell based therapies to treat muscular dystrophy. Biochim Biophys Acta 1772, 272-283.
37. Gussoni E, Blau HM, &, Kunkel LM, (1997) The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med 3, 970-977.
38. Mendell JR, Kissel JT, Amato AA, King W, Prior TW, Sahenk Z, Benson S, McAndrew PE, Rice R, et al,. (1995) Myoblast transfer in the treatment of Duchenne's muscular dystrophy. N Engl J Med 333, 832-838.
39. Tremblay JP, Malouin F, Roy R, Huard J, Bouchard JP, Satoh A, &, Richards CL, (1993) Results of a triple blind clinical study of myoblast transplantations without immunosuppressive treatment in young boys with Duchenne muscular dystrophy. Cell Transplant 2, 99-112.
40. Qu-Petersen Z, Deasy B, Jankowski R, Ikezawa M, Cummins J, Pruchnic R, Mytinger J, Cao B, Gates C, Wernig A, et al,. (2002) Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. J Cell Biol 157, 851-864.
41. Torrente Y, Tremblay JP, Pisati F, Belicchi M, Rossi B, Sironi M, Fortunato F, El Fahime M, D'Angelo MG, Caron NJ, et al,. (2001) Intraarterial injection of muscle-derived CD34(+)Sca-1(+) stem cells restores dystrophin in mdx mice. J Cell Biol 152, 335-348.
42. Alessandri G, Pagano S, Bez A, Benetti A, Pozzi S, Iannolo G, Baronio M, Invernici G, Caruso A, Muneretto C, et al,. (2004) Isolation and culture of human muscle-derived stem cells able to differentiate into myogenic and neurogenic cell lineages. Lancet 364, 1872-1883.
43. Rouger K, Larcher T, Dubreil L, Deschamps JY, Le Guiner C, Jouvion G, Delorme B, Lieubeau B, Carlus M, Fornasari B, 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, 2501-2518.
44. Deasy BM, Gharaibeh BM, Pollett JB, Jones MM, Lucas MA, Kanda Y, &, Huard J, (2005) Long-term self-renewal of postnatal muscle-derived stem cells. Mol Biol Cell 16, 3323-3333.
45. Deasy BM, Jankowski RJ, &, Huard J, (2001) Muscle-derived stem cells: characterization and potential for cell-mediated therapy. Blood Cells Mol Dis 27, 924-933.
46. Tagliafico E, Brunelli S, Bergamaschi A, De Angelis L, Scardigli R, Galli D, Battini R, Bianco P, Ferrari S, Cossu G, et al,. (2004) TGFbeta/BMP activate the smooth muscle/bone differentiation programs in mesoangioblasts. J Cell Sci 117, 4377-4388.
47. Brunelli S, Tagliafico E, De Angelis FG, Tonlorenzi R, Baesso S, Ferrari S, Niinobe M, Yoshikawa K, Schwartz RJ, Bozzoni I, et al,. (2004) Msx2 and necdin combined activities are required for smooth muscle differentiation in mesoangioblast stem cells. Circ Res 94, 1571-1578.
48. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, et al,. (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9, 255-267.
49. Cossu G, &, Sampaolesi M, (2007) New therapies for Duchenne muscular dystrophy: challenges, prospects and clinical trials. Trends Mol Med 13, 520-526.
50. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, Innocenzi A, Mognol P, Thibaud JL, Galvez BG, Barthelemy, et al,. (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444, 574-579.
51. Galvez BG, Sampaolesi M, Brunelli S, Covarello D, Gavina M, Rossi B, Constantin G, Toorente Y, &, Cossu G, (2006) Complete repair of dystrophic skeletal muscle by mesoangioblasts with enhanced migration ability. J Cell Biol 174, 231-243.
52. Tedesco FS, Hoshiya H, Gerli MF, Messina G, Antonini S, Tonlorenzi R, Benedetti S, Berghella L, Torrente Y, et al,. (2011) Stem cell-mediated transfer of a human artificial chromosome ameliorates muscular dystrophy. Sci Transl Med 3, 96ra78.
53. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi A, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MA, Campbell KP, et al,. (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301, 487-492.
54. Tedesco FS, Gerli MF, Perani L, Benedetti S, Ungaro F, Cassano M, Antonini S, Tagliafico E, Artusi V, Longa E, et al,. (2012) Transplantation of genetically corrected human iPSC-derived progenitors in mice with limb-girdle muscular dystrophy. Sci Transl Med 4, 140ra89.
55. Corbeil D, Roper K, Fargeas CA, Joester A, &, Huttner WB, (2001) Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic 2, 82-91.
56. Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, Bray RA, Waller EK, &, Buck DW, (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90, 5013-5021.
57. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, &, Buck DW, (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90, 5002-5012.
58. Torrente Y, Belicchi M, Sampaolesi M, Pisati F, Meregalli M, D'Antona G, Tonlorenzi R, Porretti L, Gavina M, Mamchaoui K, et al,. (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J Clin Invest 114, 182-195.
59. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, &, Weissman IL, (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97, 14720-14725.
60. Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan JC, Garcia L, &, Danos O, (2004) Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306, 1796-1799.
61. Peault B, Rudnicki M, Torrente Y, Cossu G, Tremblay JP, Partridge T, Gussoni E, Kunkel LM, &, Huard J, (2007) Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 15, 867-877.
62. Graf T, &, Stadtfeld M, (2008) Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 3, 480-483.
63. Negroni E, Riederer I, Chaouch S, Belicchi M, Razini P, Di Santo J, Torrente Y, Butler-Browne GS, &, Mouly V, (2009) In vivo myogenic potential of human CD133+ muscle-derived stem cells: a quantitative study. Mol Ther 17, 1771-1778.
64. Gavina M, Belicchi M, &, Camirand G, (2006) VCAM-1 expression on dystrophic muscle vessels has a critical role in the recruitment of human blood-derived CD133+ stem cells after intra-arterial transplantation. Blood 108, 2857-2866.
65. Alhadlaq A, &, Mao JJ, (2004) Mesenchymal stem cells: isolation and therapeutics. Stem Cells Dev 13, 436-448.
66. Beyer Nardi N, &, da Silva Meirelles L, (2006) Mesenchymal stem cells: isolation, in vitro expansion and characterization. Handb Exp Pharmacol 174, 249-282.
67. Le Blanc K, &, Pittenger M, (2005) Mesenchymal stem cells: progress toward promise. Cytotherapy 7, 36-45.
68. Zheng B, Cao B, Crisan M, Sun B, Li G, Logar A, Yap S, Pollett JB, Drowley L, Cassino T, et al,. (2007) Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol 25, 1025-1034.
69. Nesti LJ, Jackson WM, Shanti RM, Koehler SM, Aragon AB, Bailey JR, Sracic MK, Freedman BA, Giuliani JR, &, Tuan RS, (2008) Differentiation potential of multipotent progenitor cells derived from war-traumatized muscle tissue. J Bone Joint Surg Am 90, 2390-2398.
70. Jackson WM, Nesti LJ, &, Tuan RS, (2010) Potential therapeutic applications of muscle-derived mesenchymal stem and progenitor cells. Expert Opin Biol Ther 10, 505-517.
71. Avniel S, Ariz Z, Maly A, Sagie A, Basst HB, Yahana MD, Weiss ID, Pal B, Wald O, Ad-El D, et al,. (2006) Involvement of the CXCL12/CXCR4 pathway in the recovery of skin following burns. J Invest Dermatol 126, 468-476.
72. Fox A, Smythe J, Fisher N, Tyler MP, McGrouther DA, Watt SM, &, Harris AL, (2008) Mobilization of endothelial progenitor cells into the circulation in burned patients. Br J Surg 95, 244-251.
73. Kitaori T, Ito H, Schwarz EM, Tsutsumi R, Yoshitomi H, Osihi S, Nakano M, Fujii N, Nagasawa T, &, Nakamura T, (2009) Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 60, 813-823.
74. Penn MS, (2009) Importance of the SDF-1:CXCR4 axis in myocardial repair. Circ Res 104, 1133-1135.
75. Schonemeier B, Schulz S, Hoellt V, &, Stumm R, (2008) Enhanced expression of the CXCl12/SDF-1 chemokine receptor CXCR7 after cerebral ischemia in the rat brain. J Neuroimmunol 198, 39-45.
76. Goncalves MA, de Vries AA, Holkers M, van de Watering MJ, van der Velde I, van Nierop GP, Valerio D, &, Knaan-Shanzer S, (2006) Human mesenchymal stem cells ectopically expressing full-length dystrophin can complement Duchenne muscular dystrophy myotubes by cell fusion. Hum Mol Genet 15, 213-221.
77. Gang EJ, Jeong JA, Hong SH, Hwang SH, Kim SW, Yang IH, Ahn C, Han H, &, Kim H, (2004) Skeletal myogenic differentiation of mesenchymal stem cells isolated from human umbilical cord blood. Stem Cells 22, 617-624.
78. Erices A, Conget P, &, Minguell JJ, (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 109, 235-242.
79. Romanov YA, Svintsitskaya VA, &, Smirnov VN, (2003) Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like cells from umbilical cord. Stem Cells 21, 105-110.
80. Riordan NH, Chan K, Marleau AM, &, Ichim TE, (2007) Cord blood in regenerative medicine: do we need immune suppression? J Transl Med 5, 8.
81. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmlee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, et al,. (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15, 42-49.
82. Fiorina P, Jurewicz M, Augello A, Vergani A, Dada S, La Rosa S, Selig, Godwin J, Law K, Placidi C, et al,. (2009) Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol 183, 993-1004.
83. Madec AM, Mallone R, Afonso G, Abou Mrad E, Mesnier A, Eljaafari A, &, Thivolet C, (2009) Mesenchymal stem cells protect NOD mice from diabetes by inducing regulatory T cells. Diabetologia 52, 1391-1399.
84. Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, Gini B, Bach SD, Martinello M, Bifari F, et al,. (2009) Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27, 2624-2635.
85. Rafei M, Birman E, Forner K, &, Galipeau J, (2009a) Allogeneic mesenchymal stem cells for treatment of experimental autoimmune encephalomyelitis. Mol Ther 17, 1799-1803.
86. Zhou K, Zhang H, Jin O, Feng X, Yao G, Hou Y, &, Sun L, (2008) Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr mice. Cell Mol Immunol 5, 417-424.
87. Song HY, Lee MJ, Kim MY, Kim KH, Lee IH, Shin SH, Lee JS, &, Kim JH, (2010) Lysophosphatidic acid mediates migration of human mesenchymal stem cells stimulated by synovial fluid of patients with rheumatoid arthritis. Biochim Biophys Acta 1801, 23-30.
88. Rafei M, Campeau PM, Aguilar-Mahecha A, Buchanan M, Williams P, Birman E, Yuan S, Young YK, Boivin MN, Forner K, et al,. (2009b) Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. J Immunol 182, 5994-6002.
89. Ichim TE, Alexandrescu DT, Solano F, Lara F, Campion Rde N, Paris E, Woods EJ, Murphy MP, Dasanu CA, Patel AN, et al,. (2010) Mesenchymal stem cells as anti-inflammatories: implications for treatment of Duchenne muscular dystrophy. Cell Immunol 260, 75-82.
90. Asakura A, &, Rudnicki MA, (2002) Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol 30, 1339-1345.
91. Yao SN, &, Kurachi K, (1993) Implanted myoblasts not only fuse with myofibers but also survive as muscle precursor cells. J Cell Sci 105 (Pt 4), 957-963.
92. De Bari C, Dell'Accio F, Tylzanowski P, &, Luyten FP, (2001) Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44, 1928-1942.
93. De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, &, Luyten FP, (2003) Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 160, 909-918.
94. Battistini L, Piccio L, Rossi B, Bach S, Galgani S, Gasperini C, Ottoboni L, Ciabini D, Caramia MD, Bernardi G, et al,. (2003) CD8+ T cells from patients with acute multiple sclerosis display selective increase of adhesiveness in brain venules: a critical role for P-selectin glycoprotein ligand-1. Blood 101, 4775-4782.
95. Piccio L, Rossi B, Scarpini E, Laudanna C, Giagulli C, Issekutz AC, Vestweber D, Butcher EC, &, Constantin G, (2002) Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors. J Immunol 168, 1940-1949.
96. Charge SB, &, Rudnicki MA, (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84, 209-238.
97. Asakura A, Seale P, Girgis-Gabardo A, &, Rudnicki MA, (2002) Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159, 123-134.
98. Doherty MJ, Ashton BA, Walsh S, Beresford JN, Grant ME, &, Canfield AE, (1998) Vascular pericytes express osteogenic potential in vitro and in vivo. J Bone Miner Res 13, 828-838.
99. Skuk D, Goulet M, Roy B, &, Tremblay JP, (2000) Myoblast transplantation in whole muscle of nonhuman primates. J Neuropathol Exp Neurol 59, 197-206.
100. Skuk D, Goulet M, Roy B, &, Tremblay JP, (2002) Efficacy of myoblast transplantation in nonhuman primates following simple intramuscular cell injections: toward defining strategies applicable to humans. Exp Neurol 175, 112-126.
101. Skuk D, Goulet M, Roy B, Chapdelaine P, Bouchard JP, Roy R, Dugre FJ, Sylvain M, Lachance JG, Deschenes L, et al,. (2006) Dystrophin expression in muscles of duchenne muscular dystrophy patients after high-density injections of normal myogenic cells. J Neuropathol Exp Neurol 65, 371-386.
102. Torrente Y, Belicchi M, Marchesi C, D'Antona G, Cogiamanian F, Pisati F, Gavina M, Giordano R, Tonlorenzi R, Fagiolari G, et al,. (2007) Autologous transplantation of muscle-derived CD133+ stem cells in Duchenne muscle patients. Cell Transplant 16, 563-577.
103. Riviere C, Danos O, &, Douar AM, (2006) Long-term expression and repeated administration of AAV type 1, 2 and 5 vectors in skeletal muscle of immunocompetent adult mice. Gene Ther 13, 1300-1308.
104. van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, den Dunnen JT, Koop K, van der Kooi AJ, Goemans NM, et al,. (2007) Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357, 2677-2686.
105. Dubowitz V, (1992) The muscular dystrophies. Postgrad Med J 68, 500-506.
106. Law PK, Goodwin TG, &, Wang MG, (1988) Normal myoblast injections provide genetic treatment for murine dystrophy. Muscle Nerve 11, 525-533.
107. Partridge T, Lu QL, Morris G, &, Hoffman E, (1998) Is myoblast transplantation effective? Nat Med 4, 1208-1209.