Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix

Tissue Engineering - Part A

Volumn 16, Issue 9, 2010, Pages 2871-2881

  Merritt, Edward K ^a   Cannon, Megan V ^a   Hammers, David W ^a   Le, Long N ^a   Gokhale, Rohit ^a   Sarathy, Apurva ^a   Song, Tae J ^a   Tierney, Matthew T ^a   Suggs, Laura J ^b   Walters, Thomas J ^c   Farrar, Roger P ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b The University of Texas at Austin   (United States)

^c US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; BONE; CELL CULTURE; DEFECTS; FLOWCHARTING; RECOVERY; REPAIR; STEM CELLS;

BONE-MARROW-DERIVED MESENCHYMAL STEM CELLS; EXTRACELLULAR MATRICES; FUNCTIONAL RECOVERY; GASTROCNEMIUS; MYOFIBERS; RECOVERY TIME; SKELETAL MUSCLE; SURGICAL REPAIR; TISSUE LOSS;

MUSCLE;

RATTUS;

DESMIN; MYOGENIN;

ANIMAL; ARTICLE; BONE MARROW CELL; CHEMISTRY; CYTOLOGY; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; INJURY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; METHODOLOGY; RAT; SKELETAL MUSCLE; TISSUE ENGINEERING;

ANIMALS; BONE MARROW CELLS; DESMIN; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MUSCLE, SKELETAL; MYOGENIN; RATS; TISSUE ENGINEERING;

EID: 77955617823     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0826     Document Type: Article

References (71)

1. Bartlett, C.S., et al. Ballistics and gunshot wounds: effects on musculoskeletal tissues. J Am Acad Orthop Surg 8, 21, 2000.
2. Zouris, J.M., et al. Wounding patterns for U.S. marines and sailors during Operation Iraqi Freedom, major combat phase. Mil Med 171, 246, 2006.
3. Charge, S.B., and Rudnicki, M.A. Cellular and molecular regulation of muscle regeneration. Physiol Rev 84, 209, 2004.
4. Jarvinen, T.A., et al. Muscle injuries: biology and treatment. Am J Sports Med 33, 745, 2005.
5. Hill, M., Wernig, A., and Goldspink, G. Muscle satellite (stem) cell activation during local tissue injury and repair. J Anat 203, 89, 2003.
6. Mauro, A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9, 493, 1961.
7. Bach, A.D., et al. Skeletal muscle tissue engineering. J Cell Mol Med 8, 413, 2004.
8. Kin, S., et al. Regeneration of skeletal muscle using in situ tissue engineering on an acellular collagen sponge scaffold in a rabbit model. ASAIO J 53, 506, 2007.
9. Terada, N., et al. Muscle repair after a transsection injury with development of a gap: an experimental study in rats. Scand J Plast Reconstr Surg Hand Surg 35, 233, 2001.
10. Fan, C., et al. Functional reconstruction of traumatic loss of flexors in forearm with gastrocnemius myocutaneous flap transfer. Microsurgery 28, 71, 2008.
11. Vekris, M.D., et al. Restoration of elbow function in severe brachial plexus paralysis via muscle transfers. Injury 39 Suppl 3, S15, 2008.
12. Osses, N., and Brandan, E. ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am J Physiol Cell Physiol 282, C383, 2002.
13. Borschel, G.H., Dennis, R.G., and Kuzon, W.M., Jr. Contractile skeletal muscle tissue-engineered on an acellular scaffold. Plast Reconstr Surg 113, 595; discussion 603, 2004.
14. Badylak, S.F. The extracellular matrix as a biologic scaffold material. Biomaterials 28, 3587, 2007.
15. Engler, A.J., et al. Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166, 877, 2004.
16. Engler, A.J., et al. Matrix elasticity directs stem cell lineage specification. Cell 126, 677, 2006.
17. Fansa, H., et al. Acellular muscle with Schwann-cell implantation: an alternative biologic nerve conduit. J Reconstr Microsurg 15, 531, 1999.
18. Ott, H.C., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 14, 213, 2008.
19. Merritt, E., et al. Functional assessment of skeletal muscle regeneration utilizing homologous extracellular matrix as scaffolding. Tissue Eng Part A 16, 1395, 2010.
20. Kochupura, P.V., et al. Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112(9 Suppl), I144, 2005.
21. Robinson, K.A., et al. Extracellular matrix scaffold for cardiac repair. Circulation 112(9 Suppl), I135, 2005.
22. Dufrane, D., et al. Regeneration of abdominal wall muscu-lofascial defects by a human acellular collagen matrix. Bio-materials 29, 2237, 2008.
23. Vindigni, V., et al. Reconstruction of ablated rat rectus ab-dominis by muscle regeneration. Plast Reconstr Surg 114, 1509; discussion 1516, 2004.
24. Conconi, M.T., et al. Homologous muscle acellular matrix seeded with autologous myoblasts as a tissue-engineering approach to abdominal wall-defect repair. Biomaterials 26, 2567, 2005.
25. De Coppi, P., et al. Myoblast-acellular skeletal muscle matrix constructs guarantee a long-term repair of experimental full-thickness abdominal wall defects. Tissue Eng 12, 1929, 2006.
26. Marzaro, M., et al. Autologous satellite cell seeding improves in vivo biocompatibility of homologous muscle acellular matrix implants. Int J Mol Med 10, 177, 2002.
27. Ayele, T., et al. Tissue engineering approach to repair abdominal wall defects using cell-seeded bovine tunica va-ginalis in a rabbit model. J Mater Sci Mater Med 21, 1721, 2010.
28. Friedenstein, A.J., et al. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17, 331, 1974.
29. Wakitani, S., Saito, T., and Caplan, A.I. Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5-azacytidine. Muscle Nerve 18, 1417, 1995.
30. Dezawa, M., et al. Bone marrow stromal cells generate muscle cells and repair muscle degeneration. Science 309, 314, 2005.
31. Prockop, D.J. Marrow stromal cells as stem cells for non-hematopoietic tissues. Science 276, 71, 1997.
32. Jiang, Y., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41, 2002.
33. LaBarge, M.A., and Blau, H.M. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111, 589, 2002.
34. Palermo, A.T., et al. Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev Biol 279, 336, 2005.
35. Fukada, S., et al. Muscle regeneration by reconstitution with bone marrow or fetal liver cells from green fluorescent protein-gene transgenic mice. J Cell Sci 115(Pt 6), 1285, 2002.
36. Matziolis, G., et al. Autologous bone marrow-derived cells enhance muscle strength following skeletal muscle crush injury in rats. Tissue Eng 12, 361, 2006.
37. Natsu, K., et al. Allogeneic bone marrow-derived mesen-chymal stromal cells promote the regeneration of injured skeletal muscle without differentiation into myofibers. Tissue Eng 10, 1093, 2004.
38. Chang, Y., et al. Tissue regeneration observed in a basic fi-broblast growth factor-loaded porous acellular bovine pericardium populated with mesenchymal stem cells. J Thorac Cardiovasc Surg 134, 65, 73.e1, 2007.
39. Wei, H.J., et al. Porous acellular bovine pericardia seeded with mesenchymal stem cells as a patch to repair a myo-cardial defect in a syngeneic rat model. Biomaterials 27, 5409, 2006.
40. Kragh, J.F., Jr., et al. Epimysium and perimysium in suturing in skeletal muscle lacerations. J Trauma 59, 209, 2005.
41. Lamb, D.W., and Chan, K.M. Surgical reconstruction of the upper limb in traumatic tetraplegia. A review of 41 patients. J Bone Joint Surg Br 65, 291, 1983.
42. Brinchmann, J.E. Expanding autologous multipotent mes-enchymal bone marrow stromal cells. J Neurol Sci 265, 127, 2008.
43. Pereira, R.F., et al. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 92, 4857, 1995.
44. Falanga, V., et al. Autologous bone marrow-derived cultured mesenchymal stem cells delivered in a fibrin spray accelerate healing in murine and human cutaneous wounds. Tissue Eng 13, 1299, 2007.
45. Rose, R.A., et al. Bone marrow-derived mesenchymal stro-mal cells express cardiac-specific markers, retain the stromal phenotype, and do not become functional cardiomyocytes in vitro. Stem Cells 26, 2884, 2008.
46. Rossignol, J., et al. Mesenchymal stem cells induce a weak immune response in the rat striatum after allo or xeno-transplantation. J Cell Mol Med 13, 2547, 2009.
47. Chen, S.L., et al. Effect on left ventricular function of in-tracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol 94, 92, 2004.
48. Dreyfus, P.A., et al. Adult bone marrow-derived stem cells in muscle connective tissue and satellite cell niches. Am J Pa-thol 164, 773, 2004.
49. De Bari, C., et al. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 160, 909, 2003.
50. Corti, S., et al. A subpopulation of murine bone marrow cells fully differentiates along the myogenic pathway and participates in muscle repair in the mdx dystrophic mouse. Exp Cell Res 277, 74, 2002.
51. Goncalves, M.A., et al. Human mesenchymal stem cells ec-topically expressing full-length dystrophin can complement Duchenne muscular dystrophy myotubes by cell fusion. Hum Mol Genet 15, 213, 2006.
52. Pittenger, M.F., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
53. Muguruma, Y., et al. In vivo and in vitro differentiation of myocytes from human bone marrow-derived multipotent progenitor cells. Exp Hematol 31, 1323, 2003.
54. Abedi, M., et al. Robust conversion of marrow cells to skeletal muscle with formation of marrow-derived muscle cell colonies: a multifactorial process. Exp Hematol 32, 426, 2004.
55. Winkler, T., et al. Dose-response relationship of mesenchy-mal stem cell transplantation and functional regeneration after severe skeletal muscle injury in rats. Tissue Eng Part A 15, 487, 2009.
56. Kamihata, H., et al. Implantation of bone marrow mononu-clear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angio-blasts, angiogenic ligands, and cytokines. Circulation 104, 1046, 2001.
57. Kinnaird, T., et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 109, 1543, 2004.
58. Gnecchi, M., et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11, 367, 2005.
59. Shabbir, A., et al. Heart failure therapy mediated by the trophic activities of bone marrow mesenchymal stem cells: a non-invasive therapeutic regimen. Am J Physiol Heart Circ Physiol 296, H1888, 2009.
60. Zisa, D., et al. Vascular endothelial growth factor (VEGF) as a key therapeutic trophic factor in bone marrow mesen-chymal stem cell-mediated cardiac repair. Biochem Biophys Res Commun 390, 834, 2009.
61. Gamba, P.G., et al. Experimental abdominal wall defect repaired with acellular matrix. Pediatr Surg Int 18, 327, 2002.
62. Hwang, J.H., et al. Therapeutic effect of passive mobilization exercise on improvement of muscle regeneration and prevention of fibrosis after laceration injury of rat. Arch Phys Med Rehabil 87, 20, 2006.
63. Reing, J.E., et al. Degradation products of extracellular matrix affect cell migration and proliferation. Tissue Eng Part A 15, 605, 2009.
64. Stern, M.M., et al. The influence of extracellular matrix derived from skeletal muscle tissue on the proliferation and differentiation of myogenic progenitor cells ex vivo. Bioma-terials 30, 2393, 2009.
65. Beattie, A.J., et al. Chemoattraction of Progenitor Cells by Remodeling Extracellular Matrix Scaffolds. Tissue Eng Part A 15, 1119, 2009.
66. Lien, S.C., Cederna, P.S., and Kuzon, W.M., Jr. Optimizing skeletal muscle reinnervation with nerve transfer. Hand Clin 24, 445, vii, 2008.
67. Hobson, M.I., Green, C.J., and Terenghi, G. VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat 197 (Pt 4), 591, 2000.
68. Dhawan, V., et al. Neurotization improves contractile forces of tissue-engineered skeletal muscle. Tissue Eng 13, 2813, 2007.
69. Moon du, G., et al. Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng Part A 14, 473, 2008.
70. Quintero, A.J., et al. Stem cells for the treatment of skeletal muscle injury. Clin Sports Med 28, 1, 2009.
71. Huard, J., Cao, B., and Qu-Petersen, Z. Muscle-derived stem cells: potential for muscle regeneration. Birth Defects Res C Embryo Today 69, 230, 2003.