Operative Techniques in Orthopaedics
Volume 20, Issue 2 , Pages 119-126 , June 2010

Regenerative Medicine Based on Muscle-Derived Stem Cells

  • Johnny Huard, PhD

      Affiliations

    • Corresponding Author InformationAddress reprint requests to Johnny Huard, PhD, Stem Cell Research Center, Bridgeside Point II, 450 Technology Dr, Suite 206, Pittsburgh, PA 15219
    • ,
  • Burhan Gharaibeh, PhD
    • ,
  • Arvydas Usas, MD

References 

  1. Phillippi JA, Miller E, Weiss L, et al. Microenvironments engineered by inkjet bioprinting spatially direct adult stem cells toward muscle- and bone-like subpopulations. Stem Cells. 2008;26:127–134
  2. O'Driscoll SW. The healing and regeneration of articular cartilage. J Bone Joint Surg Am. 1998;80:1795–1812
  3. Koval KJ. Orthopaedic Update 7. Dallas, TX: American Academy of Orthopaedic Surgeons; 2002;
  4. Hangody L, Kish G, Karpati Z, et al. Arthroscopic autogenous osteochondral mosaicplasty for the treatment of femoral condylar articular defects (A preliminary report). Knee Surg Sports Traumatol Arthrosc. 1997;5:262–267
  5. Easton BT. Evaluation and treatment of the patient with osteoarthritis. J Fam Pract. 2001;50:791–797
  6. LaPrade RF, Swiontkowski MF. New horizons in the treatment of osteoarthritis of the knee. JAMA. 1999;281:876–878
  7. Gossec L, Dougados M. Intra-articular treatments in osteoarthritis: From the symptomatic to the structure modifying. Ann Rheum Dis. 2004;63:478–482
  8. Archibeck MJ, White RE. What's new in adult reconstructive knee surgery. J Bone Joint Surg Am. 2003;85-A:1404–1411
  9. Giannoni P, Pagano A, Maggi E, et al. Autologous chondrocyte implantation (ACI) for aged patients: Development of the proper cell expansion conditions for possible therapeutic applications. Osteoarthritis Cartilage. 2005;13:589–600
  10. NIH Consensus Panel. Consensus statement on total knee replacement December 8-10, 2003. J Bone Joint Surg Am. 2004;86-A:1328–1335
  11. Brittberg M, Lindahl A, Nilsson A, et al. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med. 1994;331:889–895
  12. Peterson L, Minas T, Brittberg M, et al. : Treatment of osteochondritis dissecans of the knee with autologous chondrocyte transplantation: Results at two to ten years. J Bone Joint Surg Am. 2003;85-A(suppl 2):17–24
  13. Adachi N, Sato K, Usas A, et al. Muscle derived, cell based ex vivo gene therapy for treatment of full thickness articular cartilage defects. J Rheumatol. 2002;29:1920–1930
  14. 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
  15. Kuroda R, Usas A, Kubo S, et al. Cartilage repair using bone morphogenetic protein 4 and muscle-derived stem cells. Arthritis Rheum. 2006;54:433–442
  16. Tavian M, Zheng B, Oberlin E, et al. The vascular wall as a source of stem cells. Ann N Y Acad Sci. 2005;1044:41–50
  17. Zheng B, Cao B, Crisan M, et al. Prospective identification of myogenic endothelial cells in human skeletal muscle. Nat Biotechnol. 2007;25:1025–1034
  18. O'Connor WJ, Botti T, Khan SN, et al. The use of growth factors in cartilage repair. Orthop Clin North Am. 2000;31:399–410
  19. Semba I, Nonaka K, Takahashi I, et al. Positionally-dependent chondrogenesis induced by BMP4 is co-regulated by Sox9 and Msx2. Dev Dyn. 2000;217:401–414
  20. Kramer J, Hegert C, Guan K, et al. Embryonic stem cell-derived chondrogenic differentiation in vitro: Activation by BMP-2 and BMP-4. Mech Dev. 2000;92:193–205
  21. van der Kraan PM, Buma P, van Kuppevelt T, et al. Interaction of chondrocytes, extracellular matrix and growth factors: Relevance for articular cartilage tissue engineering. Osteoarthritis Cartilage. 2002;10:631–637
  22. Sekiya I, Vuoristo JT, Larson BL, et al. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc Natl Acad Sci USA. 2002;99:4397–4402
  23. Kubo S, Cooper GM, Matsumoto T, et al. Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells. Arthritis Rheum. 2009;60:155–165
  24. Matsumoto T, Cooper GM, Gharaibeh B, et al. Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1. Arthritis Rheum. 2009;60:1390–1405
  25. Elisseeff J. Injectable cartilage tissue engineering. Expert Opin Biol Ther. 2004;4:1849–1859
  26. Stark Y, Suck K, Kasper C, et al. Application of collagen matrices for cartilage tissue engineering. Exp Toxicol Pathol. 2006;57:305–311
  27. Moretti M, Wendt D, Dickinson SC, et al. Effects of in vitro preculture on in vivo development of human engineered cartilage in an ectopic model. Tissue Eng. 2005;11:1421–1428
  28. Li WJ, Tuli R, Okafor C, et al. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials. 2005;26:599–609
  29. Caterson EJ, Nesti LJ, Li WJ, et al. Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam. J Biomed Mater Res. 2001;57:394–403
  30. Summers BN, Eisenstein SM. Donor site pain from the ilium (A complication of lumbar spine fusion). J Bone Joint Surg Br. 1989;71:677–680
  31. Awad HA, Zhang X, Reynolds DG, et al. Recent advances in gene delivery for structural bone allografts. Tissue Eng. 2007;13:1973–1985
  32. Zhang X, Awad HA, O'Keefe RJ, et al. A perspective: Engineering periosteum for structural bone graft healing. Clin Orthop Relat Res. 2008;466:1777–1787
  33. Urist MR. Bone formation by autoinduction. Science. 1965;150:893–899
  34. Friedlaender GE, Perry CR, Cole JD, et al. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions. J Bone Joint Surg Am. 2001;83-A(suppl 1):S151–S158
  35. Burkus JK, Gornet MF, Dickman CA, et al. Anterior lumbar interbody fusion using rhBMP-2 with tapered interbody cages. J Spinal Disord Tech. 2002;15:337–349
  36. Govender S, Csimma C, Genant HK, et al. : Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: A prospective, controlled, randomized study of four hundred and fifty patients. J Bone Joint Surg Am. 2002;84-A:2123–2134
  37. Mori S, Yoshikawa H, Hashimoto J, et al. Antiangiogenic agent (TNP-470) inhibition of ectopic bone formation induced by bone morphogenetic protein-2. Bone. 1998;22:99–105
  38. Ferguson C, Alpern E, Miclau T, et al. Does adult fracture repair recapitulate embryonic skeletal formation?. Mech Dev. 1999;87:57–66
  39. Nakagawa M, Kaneda T, Arakawa T, et al. Vascular endothelial growth factor (VEGF) directly enhances osteoclastic bone resorption and survival of mature osteoclasts. FEBS Lett. 2000;473:161–164
  40. Leung DW, Cachianes G, Kuang WJ, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–1309
  41. Peng H, Usas A, Olshanski A, et al. VEGF improves, whereas sFlt1 inhibits, BMP2-induced bone formation and bone healing through modulation of angiogenesis. J Bone Miner Res. 2005;20:2017–2027
  42. Peng H, Wright V, Usas A, et al. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110:751–759
  43. Gerber HP, Vu TH, Ryan AM, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5:623–628
  44. Street J, Bao M, deGuzman L, et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA. 2002;99:9656–9661
  45. Pelled G, Ben Arav A, Hock C, et al: Direct gene therapy for bone regeneration: Gene delivery, animal models and outcome measures. Tissue Eng Part A (Epub ahead of print)
  46. Lee JY, Musgrave D, Pelinkovic D, et al. Effect of bone morphogenetic protein-2-expressing muscle-derived cells on healing of critical-sized bone defects in mice. J Bone Joint Surg Am. 2001;83-A:1032–1039
  47. Lee JY, Qu-Petersen Z, Cao B, et al. Clonal isolation of muscle-derived cells capable of enhancing muscle regeneration and bone healing. J Cell Biol. 2000;150:1085–1100
  48. Shen HC, Peng H, Usas A, et al. Ex vivo gene therapy-induced endochondral bone formation: Comparison of muscle-derived stem cells and different subpopulations of primary muscle-derived cells. Bone. 2004;34:982–992
  49. Shen HC, Peng H, Usas A, et al. Structural and functional healing of critical-size segmental bone defects by transduced muscle-derived cells expressing BMP4. J Gene Med. 2004;6:984–991
  50. Peng H, Usas A, Gearhart B, et al. Development of a self-inactivating tet-on retroviral vector expressing bone morphogenetic protein 4 to achieve regulated bone formation. Mol Ther. 2004;9:885–894
  51. Lee JY, Peng H, Usas A, et al. Enhancement of bone healing based on ex vivo gene therapy using human muscle-derived cells expressing bone morphogenetic protein 2. Hum Gene Ther. 2002;13:1201–1211
  52. Musgrave DS, Pruchnic R, Bosch P, et al. Human skeletal muscle cells in ex vivo gene therapy to deliver bone morphogenetic protein-2. J Bone Joint Surg Br. 2002;84:120–127
  53. Peng H, Usas A, Gearhart B, et al. Converse relationship between in vitro osteogenic differentiation and in vivo bone healing elicited by different populations of muscle-derived cells genetically engineered to express BMP4. J Bone Miner Res. 2004;19:630–641
  54. Peng H, Usas A, Hannallah D, et al. Noggin improves bone healing elicited by muscle stem cells expressing inducible BMP4. Mol Ther. 2005;12:239–246
  55. Wright V, Peng H, Usas A, et al. BMP4-expressing muscle-derived stem cells differentiate into osteogenic lineage and improve bone healing in immunocompetent mice. Mol Ther. 2002;6:169–178
  56. Corsi KA, Pollett JB, Phillippi JA, et al. Osteogenic potential of postnatal skeletal muscle-derived stem cells is influenced by donor sex. J Bone Miner Res. 2007;22:1592–1602
  57. Li Y, Foster W, Deasy BM, et al. Transforming growth factor-beta1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: A key event in muscle fibrogenesis. Am J Pathol. 2004;164:1007–1019
  58. Li Y, Huard J. Differentiation of muscle-derived cells into myofibroblasts in injured skeletal muscle. Am J Pathol. 2002;161:895–907
  59. Fukushima K, Badlani N, Usas A, et al. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med. 2001;29:394–402
  60. Chan YS, Li Y, Foster W, et al. The use of suramin, an antifibrotic agent, to improve muscle recovery after strain injury. Am J Sports Med. 2005;33:43–51
  61. Chan YS, Li Y, Foster W, et al. Antifibrotic effects of suramin in injured skeletal muscle after laceration. J Appl Physiol. 2003;95:771–780
  62. Sato K, Li Y, Foster W, et al. Improvement of muscle healing through enhancement of muscle regeneration and prevention of fibrosis. Muscle Nerve. 2003;28:365–372
  63. Foster W, Li Y, Usas A, et al. Gamma interferon as an antifibrosis agent in skeletal muscle. J Orthop Res. 2003;21:798–804
  64. Negishi S, Li Y, Usas A, et al. The effect of relaxin treatment on skeletal muscle injuries. Am J Sports Med. 2005;33:1816–1824
  65. Bedair HS, Karthikeyan T, Quintero A, et al. Angiotensin II receptor blockade administered after injury improves muscle regeneration and decreases fibrosis in normal skeletal muscle. Am J Sports Med. 2008;36:1548–1554
  66. Li Y, Li J, Zhu J, et al. Decorin gene transfer promotes muscle cell differentiation and muscle regeneration. Mol Ther. 2007;15:1616–1622
  67. Li ZB, Kollias HD, Wagner KR. Myostatin directly regulates skeletal muscle fibrosis. J Biol Chem. 2008;283:19371–19378
  68. Nozaki M, Li Y, Zhu J, et al. Improved muscle healing after contusion injury by the inhibitory effect of suramin on myostatin, a negative regulator of muscle growth. Am J Sports Med. 2008;36:2354–2362
  69. Hoffman EP, Brown RH, Kunkel LM. Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell. 1987;51:919–928
  70. Watkins SC, Hoffman EP, Slayter HS, et al. Immunoelectron microscopic localization of dystrophin in myofibres. Nature. 1988;333:863–866
  71. Arahata K, Ishiura S, Ishiguro T, et al. Immunostaining of skeletal and cardiac muscle surface membrane with antibody against Duchenne muscular dystrophy peptide. Nature. 1988;333:861–863
  72. Bonilla E, Samitt CE, Miranda AF, et al. Duchenne muscular dystrophy: Deficiency of dystrophin at the muscle cell surface. Cell. 1988;54:447–452
  73. Zubrzycka-Gaarn EE, Bulman DE, Karpati G, et al. The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature. 1988;333:466–469
  74. Ervasti JM, Campbell KP. Membrane organization of the dystrophin-glycoprotein complex. Cell. 1991;66:1121–1131
  75. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, et al. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 1992;355:696–702
  76. Huard J, Roy R, Bouchard JP, et al. Human myoblast transplantation between immunohistocompatible donors and recipients produces immune reactions. Transplant Proc. 1992;24:3049–3051
  77. Huard J, Roy R, Guerette B, et al. Human myoblast transplantation in immunodeficient and immunosuppressed mice: Evidence of rejection. Muscle Nerve. 1994;17:224–234
  78. 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
  79. Beauchamp JR, Morgan JE, Pagel CN, et al. Quantitative studies of efficacy of myoblast transplantation. Muscle Nerve. 1994;18(suppl):261
  80. Fan Y, Maley M, Beilharz M, et al. Rapid death of injected myoblasts in myoblast transfer therapy. Muscle Nerve. 1996;19:853–860
  81. Mendell JR, Kissel JT, Amato AA, et al. Myoblast transfer in the treatment of Duchenne's muscular dystrophy. N Engl J Med. 1995;333:832–838
  82. Gussoni E, Blau HM, Kunkel LM. The fate of individual myoblasts after transplantation into muscles of DMD patients. Nat Med. 1997;3:970–977
  83. Gharaibeh B, Lu A, Tebbets J, et al. Isolation of a slowly adhering cell fraction containing stem cells from murine skeletal muscle by the preplate technique. Nat Protoc. 2008;3:1501–1509
  84. Bischoff R. The satellite cell and muscle regeneration. In:  Engel AG,  Franzini-Armstrong C editor. Myology: Basic and Clinical. New York, NY: McGraw-Hill; 1994;p. 97–118
  85. Asakura A, Komaki M, Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation. 2001;68:245–253
  86. Collins CA, Olsen I, Zammit PS, et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell. 2005;122:289–301
  87. Rando TA. The adult muscle stem cell comes of age. Nat Med. 2005;11:829–831
  88. Zammit P, Beauchamp J. The skeletal muscle satellite cell: Stem cell or son of stem cell?. Differentiation. 2001;68:193–204
  89. Sherwood RI, Christensen JL, Conboy IM, et al. Isolation of adult mouse myogenic progenitors: Functional heterogeneity of cells within and engrafting skeletal muscle. Cell. 2004;119:543–554
  90. Oshima H, Payne TR, Urish KL, et al. Differential myocardial infarct repair with muscle stem cells compared to myoblasts. Mol Ther. 2005;12:1130–1141

 Dr Johnny Huard is receiving consulting fee from Cook MyoSite, Inc. Pittsburgh, PA. Other authors have no conflict of interest to declare.

PII: S1048-6666(09)00166-9

doi: 10.1053/j.oto.2009.10.013

Operative Techniques in Orthopaedics
Volume 20, Issue 2 , Pages 119-126 , June 2010

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