Stem cell homing in musculoskeletal injury

Biomaterials

Volumn 32, Issue 2, 2011, Pages 395-409

  Fong, Eliza L S ^a   Chan, Casey K ^a,b   Goodman, Stuart B ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Bone; Cartilage; Homing; Mesenchymal stromal cell; Tissue engineering; Trafficking

Indexed keywords

BONE MARROW; DIRECT USE; HOMING; IN-VITRO; MESENCHYMAL STROMAL CELLS; MUSCULOSKELETAL INJURIES; REGENERATIVE PROCESS; STEM CELL; STEM-CELL THERAPIES; TISSUE REPAIR; TRAFFICKING;

BONE; CARTILAGE; CYTOLOGY; HISTOLOGY; LAKES; LIGAMENTS; TISSUE ENGINEERING;

STEM CELLS;

BONE MORPHOGENETIC PROTEIN; CHEMOKINE RECEPTOR CXCR4; FIBROBLAST GROWTH FACTOR; GELATINASE A; INTERSTITIAL COLLAGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; PLATELET DERIVED GROWTH FACTOR; SOMATOMEDIN C; TRANSFORMING GROWTH FACTOR BETA;

ARTICULAR CARTILAGE; AUTOLOGOUS BONE MARROW TRANSPLANTATION; AUTOLOGOUS STEM CELL TRANSPLANTATION; BONE REGENERATION; CELL HOMING; CELL PROLIFERATION; CELL REGENERATION; CHEMOTAXIS; FIBULA FRACTURE; FRACTURE HEALING; FRACTURE REDUCTION; HEMATOPOIETIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; MUSCULAR DYSTROPHY; MUSCULOSKELETAL INJURY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; STEM CELL MOBILIZATION; STROMA CELL; TIBIA FRACTURE; TREATMENT OUTCOME;

ANIMALS; BONE AND BONES; CARTILAGE; HUMANS; MESENCHYMAL STEM CELLS; STROMAL CELLS; TISSUE ENGINEERING; WOUND HEALING;

EID: 78449248193     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.08.101     Document Type: Review

References (150)

1. Granero-Molto F., Weis J.A., Longobardi L., Spagnoli A. Role of mesenchymal stem cells in regenerative medicine: application to bone and cartilage repair. Expert Opin Biol Ther 2008, 8(3):255-268.
2. Prockop D.J., Gregory C.A., Spees J.L. One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc Natl Acad Sci U S A 2003, 100(Suppl. 1):11917-11923.
3. Roberts S.J., Howard D., Buttery L.D., Shakesheff K.M. Clinical applications of musculoskeletal tissue engineering. Br Med Bull 2008, 86:7-22.
4. da Silva Meirelles L., Caplan A.I., Nardi N.B. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008, 26(9):2287-2299.
5. Liu Z.J., Zhuge Y., Velazquez O.C. Trafficking and differentiation of mesenchymal stem cells. J Cell Biochem 2009, 106(6):984-991.
6. Zannettino A.C.W., Paton S., Arthur A., Khor F., Itescu S., Gimble J.M., et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008, 214(2):413-421.
7. Shi S., Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003, 18(4):696-704.
8. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008, 3(3):301-313.
9. Schipani E., Kronenberg H.M. Adult mesenchymal stem cells. StemBook 2009, http://www.stembook.org, 10.3824/stembook.1.38.1.
10. Pountos I., Jones E., Tzioupis C., McGonagle D., Giannoudis P.V. Growing bone and cartilage. The role of mesenchymal stem cells. J Bone Jt Surg Br 2006, 88(4):421-426.
11. Mansilla E., Marín G.H., Drago H., Sturla F., Salas E., Gardiner C., et al. Bloodstream cells phenotypically identical to human mesenchymal bone marrow stem cells circulate in large amounts under the influence of acute large skin damage: new evidence for their use in regenerative medicine. Transpl Proc 2006, 38(3):967-969.
12. Wang Y., Johnsen H.E., Mortensen S., Bindslev L., Ripa R.S., Haack-Sørensen M., et al. Changes in circulating mesenchymal stem cells, stem cell homing factor, and vascular growth factors in patients with acute ST elevation myocardial infarction treated with primary percutaneous coronary intervention. Heart 2006, 92(6):768-774.
13. Granero-Moltó F., Weis J.A., Miga M.I., Landis B., Myers T.J., O'Rear L., et al. Regenerative effects of transplanted mesenchymal stem cells in fracture healing. Stem Cells 2009, 27(8):1887-1898.
14. Ortiz L.A., Gambelli F., McBride C., Gaupp D., Baddoo M., Kaminski N., et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci U S A 2003, 100(14):8407-8411.
15. Chen J., Li Y., Wang L., Lu M., Zhang X., Chopp M. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001, 189(1-2):49-57.
16. Wu G.D., Nolta J.A., Jin Y.S., Barr M.L., Yu H., Starnes V.A., et al. Migration of mesenchymal stem cells to heart allografts during chronic rejection. Transplantation 2003, 75(5):679-685.
17. Fox J.M., Chamberlain G., Ashton B.A., Middleton J. Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 2007, 137(6):491-502.
18. Lee S.W., Padmanabhan P., Ray P., Gambhir S.S., Doyle T., Contag C., et al. Stem cell-mediated accelerated bone healing observed with in vivo molecular and small animal imaging technologies in a model of skeletal injury. J Orthop Res 2009, 27(3):295-302.
19. Caplan A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007, 213(2):341-347.
20. Cancedda R., Giannoni P., Mastrogiacomo M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials 2007, 28(29):4240-4250.
21. Csaki C., Schneider P.R.A., Shakibaei M. Mesenchymal stem cells as a potential pool for cartilage tissue engineering. Ann Anat 2008, 190(5):395-412.
22. Kuroda R., Ishida K., Matsumoto T., Akisue T., Fujioka H., Mizuno K., et al. Treatment of a full-thickness articular cartilage defect in the femoral condyle of an athlete with autologous bone-marrow stromal cells. Osteoarthritis Cartilage 2007, 15(2):226-231.
23. Wakitani S., Goto T., Pineda S.J., Young R.G., Mansour J.M., Caplan A.I., et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Jt Surg Am 1994, 76(4):579-592.
24. Wakitani S., Imoto K., Yamamoto T., Saito M., Murata N., Yoneda M. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 2002, 10(3):199-206.
25. Lee K.B.L., Hui J.H.P., Song I.C., Ardany L., Lee E.H. Injectable mesenchymal stem cell therapy for large cartilage defects - a porcine model. Stem Cells 2007, 25(11):2964-2971.
26. Liu Y., Shu X.Z., Prestwich G.D. Osteochondral defect repair with autologous bone marrow-derived mesenchymal stem cells in an injectable, in situ, cross-linked synthetic extracellular matrix. Tissue Eng 2006, 12(12):3405-3416.
27. Guo X., Wang C., Zhang Y., Xia R., Hu M., Duan C., et al. Repair of large articular cartilage defects with implants of autologous mesenchymal stem cells seeded into beta-tricalcium phosphate in a sheep model. Tissue Eng 2004, 10(11-12):1818-1829.
28. Murphy J.M., Fink D.J., Hunziker E.B., Barry F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 2003, 48(12):3464-3474.
29. Im G.I., Kim D.Y., Shin J.H., Hyun C.W., Cho W.H. Repair of cartilage defect in the rabbit with cultured mesenchymal stem cells from bone marrow. J Bone Jt Surg Br 2001, 83(2):289-294.
30. Yan H., Yu C. Repair of full-thickness cartilage defects with cells of different origin in a rabbit model. Arthroscopy 2007, 23(2):178-187.
31. Bruder S.P., Kraus K.H., Goldberg V.M., Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Jt Surg Am 1998, 80(7):985-996.
32. Bensaïd W., Oudina K., Viateau V., Potier E., Bousson V., Blanchat C., et al. De novo reconstruction of functional bone by tissue engineering in the metatarsal sheep model. Tissue Eng 2005, 11(5-6):814-824.
33. Marcacci M., Kon E., Moukhachev V., Lavroukov A., Kutepov S., Quarto R., et al. Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. Tissue Eng 2007, 13(5):947-955.
34. Quarto R., Mastrogiacomo M., Cancedda R., Kutepov S.M., Mukhachev V., Lavroukov A., et al. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 2001, 344(5):385-386.
35. Winkler T., von Roth P., Matziolis G., Mehta M., Perka C., Duda G.N. Dose-response relationship of mesenchymal stem cell transplantation and functional regeneration after severe skeletal muscle injury in rats. Tissue Engineering Part A 2009, 15(3):487-492.
36. Matziolis G., Winkler T., Schaser K., Wiemann M., Krocker D., Tuischer J., et al. Autologous bone marrow-derived cells enhance muscle strength following skeletal muscle crush injury in rats. Tissue Eng 2006, 12(2):361-367.
37. Winkler T., von Roth P., Schuman M.R., Sieland K., Stoltenburg-Didinger G., Taupitz M., et al. In vivo visualization of locally transplanted mesenchymal stem cells in the severely injured muscle in rats. Tissue Engineering Part A 2008, 14(7):1149-1160.
38. Krampera M., Pizzolo G., Aprili G., Franchini M. Mesenchymal stem cells for bone, cartilage, tendon and skeletal muscle repair. Bone 2006, 39(4):678-683.
39. Papathanasopoulos A., Giannoudis P.V. Biological considerations of mesenchymal stem cells and endothelial progenitor cells. Injury 2008, 39(Suppl. 2):S21-S32.
40. Devine S.M. Mesenchymal stem cells: will they have a role in the clinic?. J Cell Biochem Suppl 2002, 38:73-79.
41. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8(4):315-317.
42. Karp J.M., Leng Teo G.S. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009, 4(3):206-216.
43. Sordi V. Mesenchymal stem cell homing capacity. Transplantation 2009, 87(9 Suppl.):S42-S45.
44. 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(3):697-702. discussion 702.
45. Mouiseddine M., François S., Semont A., Sache A., Allenet B., Mathieu N., et al. Human mesenchymal stem cells home specifically to radiation-injured tissues in a non-obese diabetes/severe combined immunodeficiency mouse model. Br J Radiol 2007, 80(Spec No. 1):S49-S55.
46. Chapel A., Bertho J.M., Bensidhoum M., Fouillard L., Young R.G., Frick J., et al. Mesenchymal stem cells home to injured tissues when co-infused with hematopoietic cells to treat a radiation-induced multi-organ failure syndrome. J Gene Med 2003, 5(12):1028-1038.
47. Chen Y., Xiang L.X., Shao J.Z., Pan R.L., Wang Y.X., Dong X.J., et al. Recruitment of endogenous bone marrow mesenchymal stem cells towards injured liver. J Cell Mol Med 2009.
48. Morigi M., Imberti B., Zoja C., Corna D., Tomasoni S., Abbate M., et al. Mesenchymal stem cells are renotropic, helping to repair the kidney and improve function in acute renal failure. J Am Soc Nephrol 2004, 15(7):1794-1804.
49. Schenk S., Mal N., Finan A., Zhang M., Kiedrowski M., Popovic Z., et al. Monocyte chemotactic protein-3 is a myocardial mesenchymal stem cell homing factor. Stem Cells 2007, 25(1):245-251.
50. Chavakis E., Urbich C., Dimmeler S. Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 2008, 45(4):514-522.
51. Lapidot T., Dar A., Kollet O. How do stem cells find their way home?. Blood 2005, 106(6):1901-1910.
52. Rüster B., Göttig S., Ludwig R.J., Bistrian R., Müller S., Seifried E., et al. Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 2006, 108(12):3938-3944.
53. Butcher E.C. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 1991, 67(6):1033-1036.
54. Laird D.J., von Andrian U.H., Wagers A.J. Stem cell trafficking in tissue development, growth, and disease. Cell 2008, 132(4):612-630.
55. Honczarenko M., Le Y., Swierkowski M., Ghiran I., Glodek A.M., Silberstein L.E. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 2006, 24(4):1030-1041.
56. Sordi V., Malosio M.L., Marchesi F., Mercalli A., Melzi R., Giordano T., et al. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005, 106(2):419-427.
57. Ringe J., Strassburg S., Neumann K., Endres M., Notter M., Burmester G.R., et al. Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1, CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem 2007, 101(1):135-146.
58. Lapidot T., Kollet O. The essential roles of the chemokine SDF-1 and its receptor CXCR4 in human stem cell homing and repopulation of transplanted immune-deficient NOD/SCID and NOD/SCID/B2m(null) mice. Leukemia 2002, 16(10):1992-2003.
59. Peled A., Petit I., Kollet O., Magid M., Ponomaryov T., Byk T., et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999, 283(5403):845-848.
60. Müller A., Homey B., Soto H., Ge N., Catron D., Buchanan M.E., et al. Involvement of chemokine receptors in breast cancer metastasis. Nature 2001, 410(6824):50-56.
61. Wynn R.F., Hart C.A., Corradi-Perini C., O'Neill L., Evans C.A., Wraith J.E., et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 2004, 104(9):2643-2645.
62. Kitaori T., Ito H., Schwarz E.M., Tsutsumi R., Yoshitomi H., Oishi S., et al. 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 2009, 60(3):813-823.
63. Cheng Z., Ou L., Zhou X., Li F., Jia X., Zhang Y., et al. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol Ther 2008, 16(3):571-579.
64. Ji J.F., He B.P., Dheen S.T., Tay S.S.W. Interactions of chemokines and chemokine receptors mediate the migration of mesenchymal stem cells to the impaired site in the brain after hypoglossal nerve injury. Stem Cells 2004, 22(3):415-427.
65. Ozaki Y., Nishimura M., Sekiya K., Suehiro F., Kanawa M., Nikawa H., et al. Comprehensive analysis of chemotactic factors for bone marrow mesenchymal stem cells. Stem Cells Dev 2007, 16(1):119-129.
66. Li Y., Yu X., Lin S., Li X., Zhang S., Song Y.H. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun 2007, 356(3):780-784.
67. Ries C., Egea V., Karow M., Kolb H., Jochum M., Neth P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: differential regulation by inflammatory cytokines. Blood 2007, 109(9):4055-4063.
68. Louridas M., Letourneau S., Lautatzis M.E., Vrontakis M. Galanin is highly expressed in bone marrow mesenchymal stem cells and facilitates migration of cells both in vitro and in vivo. Biochem Biophys Res Commun 2009, 390(3):867-871.
69. Dwyer R.M., Potter-Beirne S.M., Harrington K.A., Lowery A.J., Hennessy E., Murphy J.M., et al. Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 2007, 13(17):5020-5027.
70. Wang L., Li Y., Chen J., Gautam S.C., Zhang Z., Lu M., et al. Ischemic cerebral tissue and MCP-1 enhance rat bone marrow stromal cell migration in interface culture. Exp Hematol 2002, 30(7):831-836.
71. Schmidt A., Ladage D., Steingen C., Brixius K., Schinköthe T., Klinz F.J., et al. Mesenchymal stem cells transmigrate over the endothelial barrier. Eur J Cell Biol 2006, 85(11):1179-1188.
72. Einhorn T.A. The cell and molecular biology of fracture healing. Clin Orthop Relat Res 1998, 355(Suppl.):S7-S21.
73. Phillips A.M. Overview of the fracture healing cascade. Injury 2005, 36(Suppl. 3):S5-S7.
74. Tsiridis E., Upadhyay N., Giannoudis P. Molecular aspects of fracture healing: which are the important molecules?. Injury 2007, 38(Suppl. 1):S11-S25.
75. Bielby R., Jones E., McGonagle D. The role of mesenchymal stem cells in maintenance and repair of bone. Injury 2007, 38(Suppl. 1):S26-S32.
76. Dimitriou R., Tsiridis E., Giannoudis P.V. Current concepts of molecular aspects of bone healing. Injury 2005, 36(12):1392-1404.
77. Gerstenfeld L.C., Cullinane D.M., Barnes G.L., Graves D.T., Einhorn T.A. Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem 2003, 88(5):873-884.
78. McKibbin B. The biology of fracture healing in long bones. J Bone Jt Surg Br 1978, 60-B(2):150-162.
79. Pereira R.F., Halford K.W., O'Hara M.D., Leeper D.B., Sokolov B.P., Pollard M.D., 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 U S A 1995, 92(11):4857-4861.
80. Gao J., Dennis J.E., Muzic R.F., Lundberg M., Caplan A.I. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 2001, 169(1):12-20.
81. Kumagai K., Vasanji A., Drazba J.A., Butler R.S., Muschler G.F. Circulating cells with osteogenic potential are physiologically mobilized into the fracture healing site in the parabiotic mice model. J Orthop Res 2008, 26(2):165-175.
82. Shirley D., Marsh D., Jordan G., McQuaid S., Li G. Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 2005, 23(5):1013-1021.
83. Devine M.J., Mierisch C.M., Jang E., Anderson P.C., Balian G. Transplanted bone marrow cells localize to fracture callus in a mouse model. J Orthop Res 2002, 20(6):1232-1239.
84. Patterson T.E., Kumagai K., Griffith L., Muschler G.F. Cellular strategies for enhancement of fracture repair. J Bone Jt Surg Am 2008, 90(Suppl. 1):111-119.
85. Einhorn T.A. Enhancement of fracture-healing. J Bone Jt Surg Am 1995, 77(6):940-956.
86. Cuomo A.V., Virk M., Petrigliano F., Morgan E.F., Lieberman J.R. Mesenchymal stem cell concentration and bone repair: potential pitfalls from bench to bedside. J Bone Jt Surg Am 2009, 91(5):1073-1083.
87. Petite H., Viateau V., Bensaïd W., Meunier A., de Pollak C., Bourguignon M., et al. Tissue-engineered bone regeneration. Nat Biotechnol 2000, 18(9):959-963.
88. Rombouts W.J.C., Ploemacher R.E. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003, 17(1):160-170.
89. Muschler G.F., Nakamoto C., Griffith L.G. Engineering principles of clinical cell-based tissue engineering. J Bone Jt Surg Am 2004, 86-A(7):1541-1558.
90. Kasten P., Beyen I., Egermann M., Suda A.J., Moghaddam A.A., Zimmermann G., et al. Instant stem cell therapy: characterization and concentration of human mesenchymal stem cells in vitro. Eur Cell Mater 2008, 16:47-55.
91. Paley D., Young M.C., Wiley A.M., Fornasier V.L., Jackson R.W. Percutaneous bone marrow grafting of fractures and bony defects. An experimental study in rabbits. Clin Orthop Relat Res 1986, 208:300-312.
92. Healey J.H., Zimmerman P.A., McDonnell J.M., Lane J.M. Percutaneous bone marrow grafting of delayed union and nonunion in cancer patients. Clin Orthop Relat Res 1990, 256:280-285.
93. Connolly J.F., Guse R., Tiedeman J., Dehne R. Autologous marrow injection as a substitute for operative grafting of tibial nonunions. Clin Orthop Relat Res 1991, 266:259-270.
94. Garg N.K., Gaur S., Sharma S. Percutaneous autogenous bone marrow grafting in 20 cases of ununited fracture. Acta Orthop Scand 1993, 64(6):671-672.
95. Connolly J.F. Injectable bone marrow preparations to stimulate osteogenic repair. Clin Orthop Relat Res 1995, 313:8-18.
96. Hernigou P., Poignard A., Manicom O., Mathieu G., Rouard H. The use of percutaneous autologous bone marrow transplantation in nonunion and avascular necrosis of bone. J Bone Jt Surg Br 2005, 87(7):896-902.
97. Goel A., Sangwan S.S., Siwach R.C., Ali A.M. Percutaneous bone marrow grafting for the treatment of tibial non-union. Injury 2005, 36(1):203-206.
98. Richter W. Mesenchymal stem cells and cartilage in situ regeneration. J Intern Med 2009, 266(4):390-405.
99. Fuller J.A., Ghadially F.N. Ultrastructural observations on surgically produced partial-thickness defects in articular cartilage. Clin Orthop Relat Res 1972, 86:193-205.
100. Ghadially F.N., Thomas I., Oryschak A.F., Lalonde J.M. Long-term results of superficial defects in articular cartilage: a scanning electron-microscope study. J Pathol 1977, 121(4):213-217.
101. Mankin H.J. The response of articular cartilage to mechanical injury. J Bone Jt Surg Am 1982, 64(3):460-466.
102. Meachim G. The effect of scarification on articular cartilage in the rabbit. J Bone Jt Surg Br 1963, 45(1):150-161.
103. Convery F.R., Akeson W.H., Keown G.H. The repair of large osteochondral defects. An experimental study in horses. Clin Orthop Relat Res 1972, 82:253-262.
104. DePalma A.F., McKeever C.D., Subin D.K. Process of repair of articular cartilage demonstrated by histology and autoradiography with tritiated thymidine. Clin Orthop Relat Res 1966, 48:229-242.
105. Mitchell N., Shepard N. The resurfacing of adult rabbit articular cartilage by multiple perforations through the subchondral bone. J Bone Jt Surg Am 1976, 58(2):230-233.
106. Salter R.B., Simmonds D.F., Malcolm B.W., Rumble E.J., MacMichael D., Clements N.D. The biological effect of continuous passive motion on the healing of full-thickness defects in articular cartilage. An experimental investigation in the rabbit. J Bone Jt Surg Am 1980, 62(8):1232-1251.
107. Coletti J.M., Akeson W.H., Woo S.L. A comparison of the physical behavior of normal articular cartilage and the arthroplasty surface. J Bone Jt Surg Am 1972, 54(1):147-160.
108. Furukawa T., Eyre D.R., Koide S., Glimcher M.J. Biochemical studies on repair cartilage resurfacing experimental defects in the rabbit knee. J Bone Jt Surg Am 1980, 62(1):79-89.
109. Gikas P.D., Bayliss L., Bentley G., Briggs T.W.R. An overview of autologous chondrocyte implantation. J Bone Jt Surg Br 2009, 91(8):997-1006.
110. Richardson S.M., Hoyland J.A., Mobasheri R., Csaki C., Shakibaei M., Mobasheri A. Mesenchymal stem cells in regenerative medicine: opportunities and challenges for articular cartilage and intervertebral disc tissue engineering. J Cell Physiol 2010, 222(1):23-32.
111. Brittberg M., Lindahl A., Nilsson A., Ohlsson C., Isaksson O., Peterson L. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994, 331(14):889-895.
112. Peterson L., Brittberg M., Kiviranta I., Akerlund E.L., Lindahl A. Autologous chondrocyte transplantation. Biomechanics and long-term durability. Am J Sports Med 2002, 30(1):2-12.
113. Peterson L., Minas T., Brittberg M., Lindahl A. Treatment of osteochondritis dissecans of the knee with autologous chondrocyte transplantation: results at two to ten years. J Bone Jt Surg Am 2003, 85-A(Suppl. 2):17-24.
114. Peterson L., Minas T., Brittberg M., Nilsson A., Sjögren-Jansson E., Lindahl A. Two- to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res 2000, 374:212-234.
115. Richter W. Cell-based cartilage repair: illusion or solution for osteoarthritis. Curr Opin Rheumatol 2007, 19(5):451-456.
116. Steadman J.R., Rodkey W.G., Briggs K.K., Rodrigo J.J. Orthopade 1999, 28(1):26-32.
117. Steadman J.R., Rodkey W.G., Rodrigo J.J. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res 2001, (391 Suppl.):S362-S369.
118. Mithoefer K., McAdams T., Williams R.J., Kreuz P.C., Mandelbaum B.R. Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis. Am J Sports Med 2009, 37(10):2053-2063.
119. Shapiro F., Koide S., Glimcher M.J. Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Jt Surg Am 1993, 75(4):532-553.
120. Wakitani S., Mitsuoka T., Nakamura N., Toritsuka Y., Nakamura Y., Horibe S. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports. Cell Transpl 2004, 13(5):595-600.
121. Hui J.H.P., Chen F., Thambyah A., Lee E.H. Treatment of chondral lesions in advanced osteochondritis dissecans: a comparative study of the efficacy of chondrocytes, mesenchymal stem cells, periosteal graft, and mosaicplasty (osteochondral autograft) in animal models. J Pediatr Orthop 2004, 24(4):427-433.
122. Kayakabe M., Tsutsumi S., Watanabe H., Kato Y., Takagishi K. Transplantation of autologous rabbit BM-derived mesenchymal stromal cells embedded in hyaluronic acid gel sponge into osteochondral defects of the knee. Cytotherapy 2006, 8(4):343-353.
123. Chen W.H., Lai M.T., Wu A.T.H., Wu C.C., Gelovani J.G., Lin C.T., et al. In vitro stage-specific chondrogenesis of mesenchymal stem cells committed to chondrocytes. Arthritis Rheum 2009, 60(2):450-459.
124. Mo X.T., Guo S.C., Xie H.Q., Deng L., Zhi W., Xiang Z., et al. Variations in the ratios of co-cultured mesenchymal stem cells and chondrocytes regulate the expression of cartilaginous and osseous phenotype in alginate constructs. Bone 2009, 45(1):42-51.
125. Bodine-Fowler S. Skeletal muscle regeneration after injury: an overview. J Voice 1994, 8(1):53-62.
126. Santa María L., Rojas C.V., Minguell J.J. Signals from damaged but not undamaged skeletal muscle induce myogenic differentiation of rat bone-marrow-derived mesenchymal stem cells. Exp Cell Res 2004, 300(2):418-426.
127. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279(5356):1528-1530.
128. Bittner R.E., Schöfer C., Weipoltshammer K., Ivanova S., Streubel B., Hauser E., et al. Recruitment of bone-marrow-derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice. Anat Embryol (Berl) 1999, 199(5):391-396.
129. LaBarge M.A., Blau H.M. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 2002, 111(4):589-601.
130. Long M.A., Corbel S.Y., Rossi F.M.V. Circulating myogenic progenitors and muscle repair. Semin Cell Dev Biol 2005, 16(4-5):632-640.
131. Shi D., Reinecke H., Murry C.E., Torok-Storb B. Myogenic fusion of human bone marrow stromal cells, but not hematopoietic cells. Blood 2004, 104(1):290-294.
132. Sherwood R.I., Christensen J.L., Conboy I.M., Conboy M.J., Rando T.A., Weissman I.L., et al. Isolation of adult mouse myogenic progenitors: functional heterogeneity of cells within and engrafting skeletal muscle. Cell 2004, 119(4):543-554.
133. Natsu K., Ochi M., Mochizuki Y., Hachisuka H., Yanada S., Yasunaga Y. Allogeneic bone marrow-derived mesenchymal stromal cells promote the regeneration of injured skeletal muscle without differentiation into myofibers. Tissue Eng 2004, 10(7-8):1093-1112.
134. De Bari C., Dell'Accio F., Vandenabeele F., Vermeesch J.R., Raymackers J.M., Luyten F.P. Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 2003, 160(6):909-918.
135. + adipose-derived mesenchymal stem cells differentiate into skeletal muscle satellite cells and ameliorate muscular dystrophy in mdx mice. Stem Cells Dev 2007, 16(5):695-706.
136. Ramírez M., Lucia A., Gómez-Gallego F., Esteve-Lanao J., Pérez-Martínez A., Foster C., et al. Mobilisation of mesenchymal cells into blood in response to skeletal muscle injury. Br J Sports Med 2006, 40(8):719-722.
137. Corbel S.Y., Lee A., Yi L., Duenas J., Brazelton T.R., Blau H.M., et al. Contribution of hematopoietic stem cells to skeletal muscle. Nat Med 2003, 9(12):1528-1532.
138. Camargo F.D., Green R., Capetanaki Y., Jackson K.A., Goodell M.A., Capetenaki Y. Single hematopoietic stem cells generate skeletal muscle through myeloid intermediates. Nat Med 2003, 9(12):1520-1527.
139. Burdzińska A., Gala K., Paczek L. Myogenic stem cells. Folia Histochem Cytobiol 2008, 46(4):401-412.
140. Connolly J., Guse R., Lippiello L., Dehne R. Development of an osteogenic bone-marrow preparation. J Bone Jt Surg Am 1989, 71(5):684-691.
141. Hernigou P., Poignard A., Beaujean F., Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Jt Surg Am 2005, 87(7):1430-1437.
142. Sakai S., Mishima H., Ishii T., Akaogi H., Yoshioka T., Uemura T., et al. Concentration of bone marrow aspirate for osteogenic repair using simple centrifugal methods. Acta Orthop 2008, 79(3):445-448.
143. Muschler G.F., Nitto H., Matsukura Y., Boehm C., Valdevit A., Kambic H., et al. Spine fusion using cell matrix composites enriched in bone marrow-derived cells. Clin Orthop Relat Res 2003, 407:102-118.
144. Muschler George Frederick. Apparatus and methods for preparing an implantable graft. United States 6049026.
145. Au A., Boehm C.A., Mayes A.M., Muschler G.F., Griffith L.G. Formation of osteogenic colonies on well-defined adhesion peptides by freshly isolated human marrow cells. Biomaterials 2007, 28(10):1847-1861.
146. Levi B., James A.W., Nelson E.R., Vistnes D., Wu B., Lee M., et al. Human adipose derived stromal cells heal critical size mouse calvarial defects. PloS One 2010, 5(6):e11177.
147. Xu Y., Malladi P., Wagner D.R., Longaker M.T. Adipose-derived mesenchymal cells as a potential cell source for skeletal regeneration. Curr Opin Mol Ther 2005, 7(4):300-305.
148. Lee R.H., Kim B., Choi I., Kim H., Choi H.S., Suh K., et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 2004, 14(4-6):311-324.
149. Lendeckel S., Jödicke A., Christophis P., Heidinger K., Wolff J., Fraser J.K., et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg 2004, 32(6):370-373.
150. Nathan S., Das De S., Thambyah A., Fen C., Goh J., Lee E.H. Cell-based therapy in the repair of osteochondral defects: a novel use for adipose tissue. Tissue Eng 2003, 9(4):733-744.