Chondrogenesis of mesenchymal stem cells for cartilage tissue engineering

Histology and Histopathology

Volumn 28, Issue 1, 2013, Pages 23-42

  Gardner, Oliver F W ^a,b   Archer, Charles W ^b   Alini, Mauro ^a   Stoddart, Martin J ^a  

^a AO RESEARCH INSTITUTE   (Switzerland)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Cartilage repair; Chondrogenesis; Mesenchymal stem cells; Tissue engineering

Indexed keywords

ANIMAL; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; CYTOLOGY; HUMAN; MESENCHYMAL STROMA CELL; METHODOLOGY; PHYSIOLOGY; REVIEW; TISSUE ENGINEERING;

ANIMALS; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CHONDROCYTES; CHONDROGENESIS; HUMANS; MESENCHYMAL STROMAL CELLS; TISSUE ENGINEERING;

EID: 84872182728     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (119)

1. Abdallah B.M. and Kassem M. (2008). Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther. 15, 109-116.
2. Amiel D., Coutts R.D., Abel M., Stewart W., Harwood F. and Akeson W.H. (1985). Rib perichondrial grafts for the repair of full-thickness articular-cartilage defects. A morphological and biochemical study in rabbits. J. Bone Joint Surg. Am. 67, 911-920.
3. Baksh D., Davies J.E. and Zandstra P.W. (2003). Adult human bone marrow-derived mesenchymal progenitor cells are capable of adhesion-independent survival and expansion. Exp. Hematol. 31, 723-732.
4. Banfi A., Muraglia A., Dozin B., Mastrogiacomo M., Cancedda R. and Quarto R. (2000). Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp. Hematol. 28, 707-715.
5. Barry F., Boynton R.E., Liu B. and Murphy J.M. (2001). Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp. Cell Res. 268, 189-200.
6. Battula V.L., Treml S., Bareiss P.M., Gieseke F., Roelofs H., de Zwart P., Muller I., Schewe B., Skutella T., Fibbe W.E., Kanz L. and Buhring H.J. (2009). Isolation of functionally distinct mesenchymal stem cell subsets using antibodies against CD56, CD271, and mesenchymal stem cell antigen-1. Haematologica 94, 173-184.
7. Becerra J., Andrades J.A., Guerado E., Zamora-Navas P., Lopez-Puertas J.M. and Reddi A.H. (2010). Articular cartilage: structure and regeneration. Tissue Eng. Part B Rev. 16, 617-627.
8. Benya P.D. and Shaffer J.D. (1982). Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30, 215-224.
9. Bernardo M.E., Emons J.A., Karperien M., Nauta A.J., Willemze R., Roelofs H., Romeo S., Marchini A., Rappold G.A., Vukicevic S., Locatelli F. and Fibbe W.E. (2007). Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources. Connect. Tissue Res. 48, 132-140.
10. Bernstein P., Sticht C., Jacobi A., Liebers C., Manthey S. and Stiehler M. (2010). Expression pattern differences between osteoarthritic chondrocytes and mesenchymal stem cells during chondrogenic differentiation. Osteoarthritis Cartilage 18, 1596-1607.
11. Bianco P. and Robey P.G. (2001). Stem cells in tissue engineering. Nature 414, 118-121.
12. Bird H.A. and Ring E.F. (1978). Therapeutic value of arthroscopy. Ann. Rheum. Dis. 37, 78-79.
13. Bosetti M., Boccafoschi F., Leigheb M., Bianchi A.E. and Cannas M. (2012). Chondrogenic induction of human mesenchymal stem cells using combined growth factors for cartilage tissue engineering. J. Tissue Eng. Regen. Med. 6, 205-213.
14. Bosnakovski D., Mizuno M., Kim G., Takagi S., Okumura M. and Fujinaga T. (2006). Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells (MSCs) in different hydrogels: influence of collagen type II extracellular matrix on MSC chondrogenesis. Biotechnol. Bioeng. 93, 1152-1163.
15. Brittberg M. (2010). Cell carriers as the next generation of cell therapy for cartilage repair: a review of the matrix-induced autologous chondrocyte implantation procedure. Am. J. Sports Med. 38, 1259-1271.
16. Brittberg M., Lindahl A., Nilsson A., Ohlsson C., Isaksson O. and Peterson L. (1994). Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N. Engl. J. Med. 331, 889-895.
17. Buckwalter J.A., Glimcher M.J., Cooper R.R. and Recker R. (1996). Bone biology. II: Formation, form, modeling, remodeling, and regulation of cell function. Instr. Course Lect. 45, 387-399.
18. Caplan A.I. (2007). Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell Physiol. 213, 341-347.
19. Caplan A.I. (2009a). New era of cell-based orthopedic therapies. Tissue Eng. Part B Rev. 15, 195-200.
20. Caplan A.I. (2009b). Why are MSCs therapeutic? New data: new insight. J. Pathol. 217, 318-324.
21. Chamberlain G., Fox J., Ashton B. and Middleton J. (2007). Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25, 2739-2749.
22. Chang C.H., Lin F.H., Lin C.C., Chou C.H. and Liu H.C. (2004). Cartilage tissue engineering on the surface of a novel gelatincalcium-phosphate biphasic scaffold in a double-chamber bioreactor. J. Biomed. Mater. Res. B Appl. Biomater. 71, 313-321.
23. Crisan M., Yap S., Casteilla L., Chen C.W., Corselli M., Park T.S., Andriolo G., Sun B., Zheng B., Zhang L., Norotte C., Teng P.N., Traas J., Schugar R., Deasy B.M., Badylak S., Buhring H.J., Giacobino J.P., Lazzari L., Huard J. and Peault B. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313.
24. Davies L.C., Blain E.J., Gilbert S.J., Caterson B. and Duance V.C. (2008). The potential of IGF-1 and TGFbeta1 for promoting adult articular cartilage repair: an in vitro study. Tissue Eng. Part A 14, 1251-1261.
25. De Bari C., Dell'Accio F., Tylzanowski P. and Luyten F.P. (2001). Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum. 44, 1928-1942.
26. Deckelbaum R.A., Chan G., Miao D., Goltzman D. and Karaplis A.C. (2002). Ihh enhances differentiation of CFK-2 chondrocytic cells and antagonizes PTHrP-mediated activation of PKA. J. Cell Sci. 115, 3015-3025.
27. Derynck R. and Zhang Y.E. (2003). Smad-dependent and Smadindependent pathways in TGF-beta family signalling. Nature 425, 577-584.
28. Diekman B.O., Rowland C.R., Lennon D.P., Caplan A.I. and Guilak F. (2010). Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage-derived matrix. Tissue Eng. Part A 16, 523-533.
29. Dimitriou R., Tsiridis E. and Giannoudis P.V. (2005). Current concepts of molecular aspects of bone healing. Injury 36, 1392-1404.
30. Djouad F., Delorme B., Maurice M., Bony C., Apparailly F., Louis-Plence P., Canovas F., Charbord P., Noel D. and Jorgensen C. (2007). Microenvironmental changes during differentiation of mesenchymal stem cells towards chondrocytes. Arthritis Res. Ther. 9, R33.
31. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D. and Horwitz E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317.
32. Dowthwaite G.P., Bishop J.C., Redman S.N., Khan I.M., Rooney P., Evans D.J., Haughton L., Bayram Z., Boyer S., Thomson B., Wolfe M.S. and Archer C.W. (2004). The surface of articular cartilage contains a progenitor cell population. J. Cell Sci. 117, 889-897.
33. Eckstein F., Reiser M., Englmeier K.H. and Putz R. (2001). In vivo morphometry and functional analysis of human articular cartilage with quantitative magnetic resonance imaging--from image to data, from data to theory. Anat. Embryol. 203, 147-173.
34. Elder B.D. and Athanasiou K.A. (2009). Hydrostatic pressure in articular cartilage tissue engineering: from chondrocytes to tissue regeneration. Tissue Eng. Part B Rev. 15, 43-53.
35. Fehrer C. and Lepperdinger G. (2005). Mesenchymal stem cell aging. Exp. Gerontol. 40, 926-930.
36. Fischer J., Dickhut A., Rickert M. and Richter W. (2010). Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum. 62, 2696-2706.
37. Fortier L.A., Mohammed H.O., Lust G. and Nixon A.J. (2002). Insulinlike growth factor-I enhances cell-based repair of articular cartilage. J. Bone Joint Surg. Br. 84, 276-288.
38. Freyria A.M. and Mallein-Gerin F. (2012). Chondrocytes or adult stem cells for cartilage repair: The indisputable role of growth factors. Injury 43, 259-65.
39. Friedenstein A.J., Chailakhyan R.K. and Gerasimov U.V. (1987). Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Prolif. 20, 263-272.
40. Gauci S.J., Golub S.B., Tutolo L., Little C.B., Sims N.A., Lee E.R., Mackie E.J. and Fosang A.J. (2008). Modulating chondrocyte hypertrophy in growth plate and osteoarthritic cartilage. J. Musculoskelet. Neuronal. Interact. 8, 308-310.
41. Goldring M.B., Tsuchimochi K. and Ijiri K. (2006). The control of chondrogenesis. J. Cell Biochem. 97, 33-44.
42. Hangody L., Rathonyi G.K., Duska Z., Vasarhelyi G., Fules P. and Modis L. (2004). Autologous osteochondral mosaicplasty. Surgical technique. J. Bone Joint Surg. Am. 86, 65-72.
43. Hodge W.A., Fijan R.S., Carlson K.L., Burgess R.G., Harris W.H. and Mann R.W. (1986). Contact pressures in the human hip joint measured in vivo. Proc. Natl. Acad. Sci. USA 83, 2879-2883.
44. Huang C.Y., Hagar K.L., Frost L.E., Sun Y. and Cheung H.S. (2004). Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 22, 313-323.
45. Huang C.Y., Reuben P.M. and Cheung H.S. (2005). Temporal expression patterns and corresponding protein inductions of early responsive genes in rabbit bone marrow-derived mesenchymal stem cells under cyclic compressive loading. Stem Cells 23, 1113-1121.
46. Hunter W. (1743). reprinted (1995). Of the structure and disease of articulating cartilages. Clin. Orthop. Relat. Res. 317, 3-6.
47. Indrawattana N., Chen G., Tadokoro M., Shann L.H., Ohgushi H., Tateishi T., Tanaka J. and Bunyaratvej A. (2004). Growth factor combination for chondrogenic induction from human mesenchymal stem cell. Biochem. Biophys. Res. Commun. 320, 914-919.
48. Insall J.N. (1967). Intra-articular surgery for degenerative arthritis of the knee. A report of the work of the late K. H. Pridie. J. Bone Joint Surg. Br. 49, 211-228.
49. James C.B. and Uhl T.L. (2001). A review of articular cartilage pathology and the use of glucosamine sulfate. J. Athl. Train. 36, 413-419.
50. Johnson L.L. (1986). Arthroscopic abrasion arthroplasty historical and pathologic perspective: present status. Arthroscopy 2, 54-69.
51. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M. and Yoo J.U. (1998). In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 238, 265-272.
52. Kafienah W., Mistry S., Dickinson S.C., Sims T.J., Learmonth I. and Hollander A.P. (2007). Three-dimensional cartilage tissue engineering using adult stem cells from osteoarthritis patients. Arthritis Rheum. 56, 177-187.
53. Kelly D.J. and Jacobs C.R. (2010). The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defects Res. C. Embryo Today 90, 75-85.
54. Kelly D.J. and Prendergast P.J. (2005). Mechano-regulation of stem cell differentiation and tissue regeneration in osteochondral defects. J. Biomech. 38, 1413-1422.
55. Khan I.M., Bishop J.C., Gilbert S. and Archer C.W. (2009). Clonal chondroprogenitors maintain telomerase activity and Sox9 expression during extended monolayer culture and retain chondrogenic potential. Osteoarthritis Cartilage 17, 518-528.
56. Khan I.M., Evans S.L., Young R.D., Blain E.J., Quantock A.J., Avery N. and Archer C.W. (2011). Fibroblast growth factor 2 and transforming growth factor beta1 induce precocious maturation of articular cartilage. Arthritis Rheum. 63, 3417-3427.
57. Kim H.K., Moran M.E. and Salter R.B. (1991). The potential for regeneration of articular cartilage in defects created by chondral shaving and subchondral abrasion. An experimental investigation in rabbits. J. Bone Joint Surg. Am. 73, 1301-1315.
58. Kim Y.J., Kim H.J. and Im G.I. (2008). PTHrP promotes chondrogenesis and suppresses hypertrophy from both bone marrow-derived and adipose tissue-derived MSCs. Biochem. Biophys. Res. Commun. 373, 104-108.
59. Kisiday J.D., Frisbie D.D., McIlwraith C.W. and Grodzinsky A.J. (2009). Dynamic compression stimulates proteoglycan synthesis by mesenchymal stem cells in the absence of chondrogenic cytokines. Tissue Eng. Part A 15, 2817-2824.
60. Klein T.J., Malda J., Sah R.L. and Hutmacher D.W. (2009). Tissue engineering of articular cartilage with biomimetic zones. Tissue Eng. Part B Rev. 15, 143-157.
61. Klein-Nulend J., Roelofsen J., Sterck J.G., Semeins C.M. and Burger E.H. (1995). Mechanical loading stimulates the release of transforming growth factor-beta activity by cultured mouse calvariae and periosteal cells. J. Cell Physiol. 163, 115-119.
62. Knutsen G., Drogset J.O., Engebretsen L., Grontvedt T., Isaksen V., Ludvigsen T.C., Roberts S., Solheim E., Strand T. and Johansen O. (2007). A randomized trial comparing autologous chondrocyte implantation with microfracture. Findings at five years. J. Bone Joint Surg. Am. 89, 2105-2112.
63. Kobayashi T., Chung U.I., Schipani E., Starbuck M., Karsenty G., Katagiri T., Goad D.L., Lanske B. and Kronenberg H.M. (2002). PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 129, 2977-2986.
64. Kobayashi T., Soegiarto D.W., Yang Y., Lanske B., Schipani E., McMahon A.P. and Kronenberg H.M. (2005). Indian hedgehog stimulates periarticular chondrocyte differentiation to regulate growth plate length independently of PTHrP. J. Clin. Invest. 115, 1734-1742.
65. Kronenberg H.M. (2003). Developmental regulation of the growth plate. Nature 423, 332-336.
66. Kupcsik L., Stoddart M.J., Li Z., Benneker L.M. and Alini M. (2010). Improving chondrogenesis: potential and limitations of SOX9 gene transfer and mechanical stimulation for cartilage tissue engineering. Tissue Eng. Part A. 16, 1845-1855.
67. Lai L.P. and Mitchell J. (2005). Indian hedgehog: its roles and regulation in endochondral bone development. J. Cell Biochem. 96, 1163-1173.
68. LaPrade R.F. and Botker J.C. (2004). Donor-site morbidity after osteochondral autograft transfer procedures. Arthroscopy 20, 69-73.
69. Lee D.A., Knight M.M., Campbell J.J. and Bader D.L. (2011). Stem cell mechanobiology. J. Cell Biochem. 112, 1-9.
70. Li Z., Kupcsik L., Yao S.J., Alini M. and Stoddart M.J. (2009). Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites. Tissue Eng. Part A. 15, 1729-1737.
71. Li Z., Kupcsik L., Yao S.J., Alini M. and Stoddart M.J. (2010a). Mechanical load modulates chondrogenesis of human mesenchymal stem cells through the TGF-beta pathway. J. Cell Mol. Med. 14, 1338-1346.
72. Li Z., Yao S.J., Alini M. and Stoddart M.J. (2010b). Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress. Tissue Eng. Part A. 16, 575-584.
73. Liu J.P., Baker J., Perkins A.S., Robertson E.J. and Efstratiadis A. (1993). Mice carrying null mutations of the genes encoding insulinlike growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59-72.
74. Longobardi L., O'Rear L., Aakula S., Johnstone B., Shimer K., Chytil A., Horton W.A., Moses H.L. and Spagnoli A. (2006). Effect of IGF-I in the chondrogenesis of bone marrow mesenchymal stem cells in the presence or absence of TGF-beta signaling. J. Bone Miner. Res. 21, 626-636.
75. Lutzner J., Kasten P., Gunther K.P. and Kirschner S. (2009). Surgical options for patients with osteoarthritis of the knee. Nat. Rev. Rheumatol. 5, 309-316.
76. Mackie E.J., Tatarczuch L. and Mirams M. (2011). The skeleton: a multifunctional complex organ: the growth plate chondrocyte and endochondral ossification. J. Endocrinol. 211, 109-121.
77. Madry H., Orth P., Kaul G., Zurakowski D., Menger M.D., Kohn D. and Cucchiarini M. (2010). Acceleration of articular cartilage repair by combined gene transfer of human insulin-like growth factor I and fibroblast growth factor-2 in vivo. Arch. Orthop. Trauma Surg. 130, 1311-1322.
78. Madry H., Grun U.W. and Knutsen G. (2011). Cartilage repair and joint preservation: medical and surgical treatment options. Dtsch. Arztebl. Int. 108, 669-677.
79. Mau E., Whetstone H., Yu C., Hopyan S., Wunder J.S. and Alman B.A. (2007). PTHrP regulates growth plate chondrocyte differentiation and proliferation in a Gli3 dependent manner utilizing hedgehog ligand dependent and independent mechanisms. Dev. Biol. 305, 28-39.
80. Mendelson A., Frank E., Allred C., Jones E., Chen M., Zhao W. and Mao J.J. (2011). Chondrogenesis by chemotactic homing of synovium, bone marrow, and adipose stem cells in vitro. FASEB J. 25, 3496-3504.
81. Meyers M.H., Akeson W. and Convery F.R. (1989). Resurfacing of the knee with fresh osteochondral allograft. J. Bone Joint Surg. Am. 71, 704-713.
82. Mezey E., Chandross K.J., Harta G., Maki R.A. and McKercher S.R. (2000). Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290, 1779-1782.
83. Michael J.W., Schluter-Brust K.U. and Eysel P. (2010). The epidemiology, etiology, diagnosis, and treatment of osteoarthritis of the knee. Dtsch. Arztebl. Int. 107, 152-162.
84. Micheli L.J., Browne J.E., Erggelet C., Fu F., Mandelbaum B., Moseley J.B. and Zurakowski D. (2001). Autologous chondrocyte implantation of the knee: multicenter experience and minimum 3- year follow-up. Clin. J. Sport Med. 11, 223-228.
85. Mobasheri A., Csaki C., Clutterbuck A.L., Rahmanzadeh M. and Shakibaei M. (2009). Mesenchymal stem cells in connective tissue engineering and regenerative medicine: applications in cartilage repair and osteoarthritis therapy. Histol. Histopathol. 24, 347-366.
86. Moseley J.B., O'Malley K., Petersen N.J., Menke T.J., Brody B.A., Kuykendall D.H., Hollingsworth J.C., Ashton C.M. and Wray N.P. (2002). A controlled trial of arthroscopic surgery for osteoarthritis of the knee. N. Engl. J. Med. 347, 81-88.
87. Mueller M.B. and Tuan R.S. (2008). Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum. 58, 1377-1388.
88. Mueller M.B., Fischer M., Zellner J., Berner A., Dienstknecht T., Prantl L., Kujat R., Nerlich M., Tuan R.S. and Angele P. (2010). Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning. Cells Tissues Organs 192, 158-166.
89. Muraglia A., Cancedda R. and Quarto R. (2000). Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J. Cell Sci. 113, 1161-1166.
90. Ng K.W., Wang C.C., Mauck R.L., Kelly T.A., Chahine N.O., Costa K.D., Ateshian G.A. and Hung C.T. (2005). A layered agarose approach to fabricate depth-dependent inhomogeneity in chondrocyte-seeded constructs. J. Orthop. Res. 23, 134-141.
91. Ng K.W., Ateshian G.A. and Hung C.T. (2009). Zonal chondrocytes seeded in a layered agarose hydrogel create engineered cartilage with depth-dependent cellular and mechanical inhomogeneity. Tissue Eng. Part A 15, 2315-2324.
92. Orimo H. (2010). The mechanism of mineralization and the role of alkaline phosphatase in health and disease. J. Nihon Med. Sch. 77, 4-12.
93. Panoskaltsis N., Mantalaris A. and Wu J.H. (2005). Engineering a mimicry of bone marrow tissue ex vivo. J. Biosci. Bioeng. 100, 28-35.
94. Pelttari K., Winter A., Steck E., Goetzke K., Hennig T., Ochs B.G., Aigner T. and Richter W. (2006). Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 54, 3254-3266.
95. Pelttari K., Steck E. and Richter W. (2008). The use of mesenchymal stem cells for chondrogenesis. Injury 39 S58-S65.
96. Prockop D.J. (1997). Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276, 71-74.
97. Rabie A.B., Tang G.H., Xiong H. and Hagg U. (2003). PTHrP regulates chondrocyte maturation in condylar cartilage. J. Dent. Res. 82, 627-631.
98. Redman S.N., Oldfield S.F. and Archer C.W. (2005). Current strategies for articular cartilage repair. Eur. Cell Mater. 9, 23-32.
99. Roach H.I. and Clarke N.M. (2000). Physiological cell death of chondrocytes in vivo is not confined to apoptosis. New observations on the mammalian growth plate. J. Bone Joint Surg. Br. 82, 601-613.
100. Roach H.I., Aigner T. and Kouri J.B. (2004). Chondroptosis: a variant of apoptotic cell death in chondrocytes? Apoptosis 9, 265-277.
101. Rubak J.M. (1982). Reconstruction of articular cartilage defects with free periosteal grafts. An experimental study. Acta Orthop. Scand. 53, 175-180.
102. Saris D.B., Vanlauwe J., Victor J., Haspl M., Bohnsack M., Fortems Y., Vandekerckhove B., Almqvist K.F., Claes T., Handelberg F., Lagae K., van der Bauwhede J., Vandenneucker H., Yang K.G., Jelic M., Verdonk R., Veulemans N., Bellemans J. and Luyten F.P. (2008). Characterized chondrocyte implantation results in better structural repair when treating symptomatic cartilage defects of the knee in a randomized controlled trial versus microfracture. Am. J. Sports Med. 36, 235-246.
103. Scadden D.T. (2006). The stem-cell niche as an entity of action. Nature 441, 1075-1079.
104. Schatti O., Grad S., Goldhahn J., Salzmann G., Li Z., Alini M. and Stoddart M.J. (2011). A combination of shear and dynamic compression leads to mechanically induced chondrogenesis of human mesenchymal stem cells. Eur. Cell Mater. 22, 214-225.
105. Shapiro F., Koide S. and Glimcher M.J. (1993). Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J. Bone Joint Surg. Am. 75, 532-553.
106. Smith J.R., Pochampally R., Perry A., Hsu S.C. and Prockop D.J. (2004). Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem Cells 22, 823-831.
107. Steadman J.R., Rodkey W.G. and Rodrigo J.J. (2001). Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin. Orthop. Relat Res. 391, S362-S369.
108. Steck E., Fischer J., Lorenz H., Gotterbarm T., Jung M. and Richter W. (2009). Mesenchymal stem cell differentiation in an experimental cartilage defect: restriction of hypertrophy to bone-close neocartilage. Stem Cells Dev. 18, 969-978.
109. Steinmeyer J. and Konttinen Y.T. (2006). Oral treatment options for degenerative joint disease--presence and future. Adv. Drug Deliv. Rev. 58, 168-211.
110. Stoddart M.J., Grad S., Eglin D. and Alini M. (2009). Cells and biomaterials in cartilage tissue engineering. Regen. Med. 4, 81-98.
111. Takagi M., Umetsu Y., Fujiwara M. and Wakitani S. (2007). High inoculation cell density could accelerate the differentiation of human bone marrow mesenchymal stem cells to chondrocyte cells. J. Biosci. Bioeng. 103, 98-100.
112. Thorpe S.D., Buckley C.T., Vinardell T., O'Brien F.J., Campbell V.A. and Kelly D.J. (2010). The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGFbeta3 induced chondrogenic differentiation. Ann. Biomed. Eng. 38, 2896-2909.
113. van Osch G.J., van den Berg W.B., Hunziker E.B. and Hauselmann H.J. (1998). Differential effects of IGF-1 and TGF beta-2 on the assembly of proteoglycans in pericellular and territorial matrix by cultured bovine articular chondrocytes. Osteoarthritis Cartilage 6, 187-195.
114. von der Mark K., Gauss V., von der Mark H. and Muller P. (1977). Relationship between cell shape and type of collagen synthesized as chondrocytes lose their cartilage phenotype in culture. Nature 267, 531-532.
115. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M. and Tabin C.J. (1996). Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
116. Wagner W. and Ho A.D. (2007). Mesenchymal stem cell preparations-- comparing apples and oranges. Stem Cell Rev. 3, 239-248.
117. Weiss S., Hennig T., Bock R., Steck E. and Richter W. (2010). Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J. Cell Physiol. 223, 84-93.
118. Williams R., Khan I.M., Richardson K., Nelson L., McCarthy H.E., Analbelsi T., Singhrao S.K., Dowthwaite G.P., Jones R.E., Baird D.M., Lewis H., Roberts S., Shaw H.M., Dudhia J., Fairclough J., Briggs T. and Archer C.W. (2010). Identification and clonal characterisation of a progenitor cell sub-population in normal human articular cartilage. PLoS One 5, e13246.
119. Wright J.M., Crockett H.C., Slawski D.P., Madsen M.W. and Windsor R.E. (2005). High tibial osteotomy. J. Am. Acad. Orthop. Surg. 13, 279-289.