Synovium-derived stem cells: A tissue-specific stem cell for cartilage engineering and regeneration

Tissue Engineering - Part B: Reviews

Volumn 18, Issue 4, 2012, Pages 301-311

  Jones, Brendan A ^a   Pei, Ming ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMICAL LOCATIONS; ARTICULAR CARTILAGES; AUTOLOGOUS CHONDROCYTE TRANSPLANTATIONS; BIOLOGICAL TREATMENT; CARTILAGE ENGINEERING; CARTILAGE REGENERATION; CELL SOURCES; CHONDROGENESIS; CHONDROGENIC; CHONDROGENIC POTENTIAL; FUNCTIONAL STRUCTURE; GROWTH CHARACTERIZATION; HIGH QUALITY; HYALINE CARTILAGE; MESENCHYMAL STEM CELL; REGENERATIVE MEDICINE; SYNOVIUM;

CARTILAGE; DIAGNOSIS; FLOWCHARTING; STEM CELLS; TISSUE; TISSUE ENGINEERING;

CELL CULTURE;

ADULT STEM CELL; ARTICULAR CARTILAGE; CARTILAGE CELL; CELL DIFFERENTIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYALINE CARTILAGE; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; REVIEW; STEM CELL; SYNOVIUM; TISSUE ENGINEERING; TISSUE REGENERATION; TISSUE SPECIFICITY;

ADULT STEM CELLS; ANIMALS; CARTILAGE; CELL DIFFERENTIATION; HUMANS; ORGAN SPECIFICITY; REGENERATION; SYNOVIAL MEMBRANE; TISSUE ENGINEERING;

EID: 84864194390     PISSN: 19373368     EISSN: 19373376     Source Type: Journal    
DOI: 10.1089/ten.teb.2012.0002     Document Type: Review

References (127)

1. Simon, T.M., and Jackson, D.W. Articular cartilage: injury pathways and treatment options. Sports Med Arthrosc 14, 146, 2006.
2. Chan, W.C., Sze, K.L., Samartzis, D., Leung, V.Y., and Chan, D. Structure and biology of the intervertebral disk in health and disease. Orthop Clin North Am 42, 447, 2011.
3. Becerra, J., Andrades, J.A., Guerado, E., Zamora-Navas, P., López-Puertas, J.M., and Reddi, A.H. Articular cartilage: structure and regeneration. Tissue Eng Part B Rev 16, 617, 2010.
4. Caplan, A.I. Mesenchymal stem cells. J Orthop Res 9, 641, 1991.
5. O'Driscoll, S.W., Recklies, A.D., and Poole, A.R. Chondrogenesis in periosteal explants: an organ culture model for in vitro study. J Bone Joint Surg Am 76, 1042, 1994.
6. Baroffio, A., Hamann, M., Bernheim, L., Bochaton-Piallat, M.L., Gabbiani, G., and Bader, C.R. Identification of selfrenewing myoblasts in the progeny of single human muscle satellite cells. Differentiation 60, 47, 1996.
7. Klein-Nulend, J., Louwerse, R.T., Heyligers, I.C., Wuisman, P.I., Semeins, C.M., Goei, S.W., and Burger, E.H. Osteogenic protein (OP-1, BMP-7) stimulates cartilage differentiation of human and goat perichondrium tissue in vitro. J Biomed Mater Res 40, 614, 1998.
8. Nishimura, K., Solchaga, L.A., Caplan, A.I., Yoo, J.U., Goldberg, V.M., and Johnstone, B. Chondroprogenitor cells of synovial tissue. Arthritis Rheum 42, 2631, 1999.
9. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S., and Marshak, D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143, 1999.
10. De Bari, C., Dell'Accio, F., and Luyten, F.P. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum 44, 85, 2001.
11. De Bari, C., Dell'Accio, F., Tylzanowski, P., and Luyten, F. Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44, 1928, 2001.
12. Erickson, G.R., Gimble, J.M., Franklin, D.M., Rice, H.E., Awad, H., and Guilak, F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290, 763, 2002.
13. Jiang, Y., Jahagirdar, B.N., Reinhardt, R.L., Schwartz, R.E., Keene, C.D., Ortiz-Gonzalez, X.R., Reyes, M., Lenvik, T., Lund, T., Blackstad, M., Du, J., Aldrich, S., Lisberg, A., Low, W.C., Largaespada, D.A., and Verfaillie, C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418, 41, 2002.
14. Kurth, T., Dell'Accio, F., Crouch, V., Augello, A., Sharpe, P., and De Bari, C. Functional mesenchymal stem cell niches in adult mouse knee joint synovium in vivo. Arthritis Rheum 63, 1289, 2011.
15. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D.J., and Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315, 2006.
16. Horie, M., Sekiya, I., Muneta, T., Ichinose, S., Matsumoto, K., Saito, H., Murakami, T., and Kobayashi, E. Intraarticular injected synovial stem cells differentiate into meniscal cells directly and promote meniscal regeneration without mobilization to distant organs in rat massive meniscal defect. Stem Cells 27, 878, 2009.
17. Archer, C.W., Morrison, H., and Pitsillides, A.A. Cellular aspects of the development of diarthrodial joints and articular cartilage. J Anat 184, 447, 1994.
18. Nalin, A.M., Greenlee, T.K.J., and Sandell, L.J. Collagen gene expression during development of avian synovial joints: transient expression of types II and XI collagen genes in the joint capsule. Dev Dyn 203, 352, 1995.
19. Archer, C.W., Morrison, E.H., Bayliss, M.T., and Ferguson, M.W.J. The development of articular cartilage. 2. The spatial and temporal patterns of glycosaminoglycans and small leucine-rich proteoglycans. J Anat 189, 23, 1996.
20. Merida-Velasco, J.A., Sanchez-Montesinos, I., Espin-Ferra, J., Rodriguez-Vazquez, J.F., Merida-Velasco, J.R., and Jimenez-Collado, J. Development of the human knee joint. Anat Rec 248, 269, 1997.
21. Edwards, J. The nature and origins of synovium: experimental approaches to the study of synoviocyte differentiation. J Anat 184, 493, 1994.
22. Vandenabeele, F., De Bari, C., Moreels, M., Lambrichts, I., Dell'Accio, F., Lippens, P.L., and Luyten, F.P. Morphological and immunocytochemical characterization of cultured fibroblast-like cells derived from adult human synovial membrane. Arch Histol Cytol 66, 145, 2003.
23. Edwards, J.C. Fibroblast biology: development and differentiation of synovial fibroblasts in arthritis [review]. Arthritis Res 2, 344, 2000.
24. McKee, C.M., Penno, M.B., Cowman, M., Burdick, M.D., Strieter, R.M., Bao, C., and Noble, P.W. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 98, 2403, 1996.
25. Ishida, O., Tanaka, Y., Morimoto, I., Takigawa, M., and Eto, S. Chondrocytes are regulated by cellular adhesion through CD44 and hyaluronic acid pathway. J Bone Miner Res 12, 1657, 1997.
26. Evanko, S.P., Angello, J.C., and Wight, T.N. Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19, 1004, 1999.
27. Lesley, J., Hascall, V.C., Tammi, M., and Hyman, R. Hyaluronan binding by cell surface CD44. J Biol Chem 275, 26967, 2000.
28. Grogan, S.P., Barbero, A., Diaz-Romero, J., Cleton-Jansen, A.M., Soeder, S., Whiteside, R., Hogendoorn, P.C., Farhadi, J., Aigner, T., Martin, I., and Mainil-Varlet, P. Identification of markers to characterize and sort human articular chondrocytes with enhanced in vitro chondrogenic capacity. Arthritis Rheum 56, 586, 2007.
29. Jones, E.A., Crawford, A., English, A., Henshaw, K., Mundy, J., Corscadden, D., Chapman, T., Emery, P., Hatton, P., and McGonagle, D. Synovial fluid mesenchymal stem cells in health and early osteoarthritis: detection and functional evaluation at the single-cell level. Arthritis Rheum 58, 1731, 2008.
30. Jones, E., Churchman, S.M., English, A., Buch, M.H., Horner, E.A., Burgoyne, C.H., Reece, R., Kinsey, S., Emery, P., McGonagle, D., and Ponchel, F. Mesenchymal stem cells in rheumatoid synovium: enumeration and functional assessment in relation to synovial inflammation level. Ann Rheum Dis 69, 450, 2010.
31. Sakaguchi, Y., Sekiya, I., Yagashita, K., and Muneta, T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 52, 2521, 2005.
32. Bilgen, B., Ren, Y., Pei, M., Aaron, R., and Ciombor, D. CD14-negative isolation enhances chondrogenesis in synovial fibroblasts. Tissue Eng Part A 15, 3261, 2009.
33. Pei, M., He, F., and Vunjack-Novakovic, G. Synoviumderived stem cell-based chondrogenesis. Differentiation 76, 1044, 2008.
34. Gwynn, I., Wade, S., Ito, K., and Richards, R.G. Novel aspects to the structure of rabbit articular cartilage. Eur Cell Mater 4, 18, 2002.
35. Rieppo, J., Hallikainen, J., Jurvelin, J.S., Kiviranta, I., Helminen, H.J., and Hyttinen, M.M. Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage. Microsc Res Tech 71, 279, 2008.
36. Pei, M., Chen, D., Li, J., and Wei, L. Histone deacetylase 4 promotes TGF-b1 induced synovium-derived stem cell chondrogenesis but inhibits chondrogenically differentiated stem cell hypertrophy. Differentiation 78, 260, 2009.
37. Huh, Y.H., Ryu, J.H., and Chun, J.S. Regulation of type II collagen expression by histone deacetylase in articular chondrocytes. J Biol Chem 282, 17123, 2007.
38. Young, A.A., McLennan, S., Smith, M.M., Smith, S.M., Cake, M.A., Read, R.A., Melrose, J., Sonnabend, D.H., Flannery, C.R., and Little, C.B. Proteoglycan 4 downregulation in a sheep meniscectomy model of early osteoarthritis. Arthritis Res Ther 8, R41, 2006.
39. Rhee, D.K., Marcelino, J., Baker, M., Gong, Y., Smits, P., Lefebvre, V., Jay, G.D., Stewart, M., Wang, H., Warman, M.L., and Carpten, J.D. The secreted glycoprotein Lubricin protects cartilage surfaces and inhibits synovial cell overgrowth. J Clin Invest 115, 622, 2005.
40. Klein, T., Malada, J., Sah, R., and Hutmacher, D. Tissue engineering of articular cartilage with biomimetric zones. Tissue Eng Part A 15, 143, 2009.
41. Schumacher, B.L., Hughes, C.E., Kuettner, K.E., Caterson, B., and Aydelotte, M.B. Immunodetection and partial cDNA sequence of the proteoglycan, superficial zone protein, synthesized by cells lining synovial joints. J Orthop Res 17, 110, 1999.
42. Pei, M., He, F., Kish, V., and Vunjak-Novakovic, G. Engineering of functional cartilage tissue using stem cells from synovial lining: a preliminary study. Clin Orthop Relat Res 466, 1880, 2008.
43. Pacifici, M., Koyama, E., Iwamoto, M., and Gentili, C. Development of articular cartilage: what do we know about it and how may it occur? Connect Tissue Res 41, 175, 2000.
44. Archer, C.W., Dowthwaite, G.P., and Francis-West, P. Development of synovial joints [review]. Birth Defects Res C Embryo Today 69, 144, 2003.
45. Bandara, G., Georgescu, H.I., Lin, C.W., and Evans, C.H. Synovial activation of chondrocytes: evidence for complex cytokine interactions. Agents Actions 34, 285, 1991.
46. Hamerman, D., Smith, C., Keiser, H.D., and Craig, R. Glycosaminoglycans produced by human synovial cell cultures. Coll Relat Res 2, 313, 1982.
47. Fife, R.S., Caterson, B., and Myers, S.L. Identification of link proteins in canine synovial cell cultures and canine articular cartilage. J Cell Biol 100, 1050, 1985.
48. Di Cesare, P.E., Carlson, C.S., Stollerman, E.S., Chen, F.S., Leslie, M., and Perris, R. Expression of cartilage oligomeric matrix protein by human synovium. FEBS Lett 412, 249, 1997.
49. Dodge, G.R., Hawkins, D., Boesler, E., Sakai, L., and Jimenez, S.A. Production of cartilage oligomeric matrix protein (COMP) by cultured human dermal and synovial fibroblasts. Osteoarthritis Cartilage 6, 435, 1998.
50. Recklies, A.D., Baillargeon, L., and White, C. Regulation of cartilage oligomeric matrix protein synthesis in human synovial cells and articular chondrocytes. Arthritis Rheum 41, 997, 1998.
51. Allard, S.A., Maini, R.N., and Muirden, K.D. Cells and matrix expressing cartilage components in fibroblastic tissue in rheumatoid pannus. Scand J Rheumatol Suppl 76, 125, 1988.
52. Xue, C., Takahashi, M., Hasunuma, T., Aono, H., Yamamoto, K., Yoshino, S., Sumida, T., and Nishioka, K. Characterisation of fibroblast like cells in pannus lesions of patients with rheumatoid arthritis sharing properties of fibroblasts and chondrocytes. Ann Rheum Dis 56, 262, 1997.
53. Shirasawa, S., Sekiya, I., Sakaguchi, Y., Yagishita, K., Ichinose, S., and Muneta, T. In vitro chondrogenesis of human synovium-derived mesenchymal stem cells: optimal condition and comparison with bone marrow-derived cells. J Cell Biochem 97, 84, 2006.
54. Jo, C.H., Ahn, H.J., Kim, H.J., Seong, S.C., and Lee, M.C. Surface characterization and chondrogenic differentiation of mesenchymal stromal cells derived from synovium. Cytotherapy 9, 316, 2007.
55. Hunziker, E.B., and Rosenberg, L.C. Repair of partialthickness defects in articular cartilage: cell recruitment from the synovial membrane. J Bone Joint Surg Am 78, 721, 1996.
56. Fickert, S., Fiedler, J., and Brenner, R.E. Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarthritis Cartilage 11, 790, 2003.
57. Moore, K., and Lemischka, I. Stem cells and their niches. Science 311, 1880, 2006.
58. Fuchs, E., Tumbar, T., and Guasch, G. Socializing with the neighbors: stem cells and their niche. Cell 116, 769, 2004.
59. Wakitani, S., Takaoka, K., Hattori, T., Miyazawa, N., Iwanaga, T., Takeda, S., Watanabe, T.K., and Tanigami, A. Embryonic stem cells injected into the mouse knee joint form teratomas and subsequently destroy the joint. Rheumatology (Oxford) 42, 162, 2003.
60. He, F., Chen, X.D., and Pei, M. Reconstruction of an in vitro tissue-specific microenvironment to rejuvenate synoviumderived stem cells for cartilage tissue engineering. Tissue Eng Part A 15, 3809, 2009.
61. He. F, and Pei, M. Extracellular matrix enhances differentiation of adipose stem cells from infrapatellar fat pad toward chondrogenesis. J Tissue Eng Regen Med [Epub ahead of print]; DOI: 10.1002/term.505, 2011.
62. He, F., and Pei, M. Rejuvenation of nucleus pulposus cells using extracellular matrix deposited by synovium-derived stem cells. Spine 37, 459, 2012.
63. Li, J.T., He, F., and Pei, M. Creation of an in vitro microenvironment to enhance human fetal synovium-derived stem cell chondrogenesis. Cell Tissue Res 345, 357, 2011.
64. Li, J.T., and Pei, M. Optimization of an in vitro threedimensional microenvironment to reprogram synoviumderived stem cells for cartilage tissue engineering. Tissue Eng Part A 17, 703, 2011.
65. Pei, M., He, F., and Wei, L. Three dimensional cell expansion substrate for cartilage tissue engineering and regeneration: a comparision in decellularized matrix deposited by synovium-derived stem cells and chondrocytes. J Tissue Sci Eng 2, 104, 2011.
66. Pei, M., and He, F. Extracellular matrix deposited by synovium-derived stem cells delays chondrocyte dedifferentiation and enhances redifferentiation. J Cell Physiol 227, 2163, 2012.
67. Rider, C.C. Heparin/heparin sulphate binding in the TGFbeta cytokine superfamily. Biochem Soc Trans 34, 458, 2006.
68. Kresse, H., and Schönherr, E. Proteoglycans of the extracellular matrix and growth control. J Cell Physiol 189, 266, 2001.
69. Pei, M., He, F., and Kish, V.L. Expansion on extracellular matrix deposited by human bone marrow stromal cells facilitates stem cell proliferation and tissue-specific lineage potential. Tissue Eng Part A 17, 3067, 2011.
70. Ando, W., Tateishi, K., Katakai, D., Hart, D., Higuchi, C., Nakata, K., Hashimoto, J., Fujie, H., Shino, K., Yoshikawa, H., and Nakamura, N. In vitro generation of a scaffold-free tissue-engineered construct (TEC) derived from human synovial mesenchymal stem cells: biological and mechanical properties and further chondrogenic potential. Tissue Eng Part A 14, 2041, 2008.
71. Yoshimura, H., Muneta, T., Nimura, A., Yokoyama, A., Koga, H., and Sekiya, I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 327, 449, 2007.
72. Colter, D.C., Class, R., DiGirolamo, C.M., and Prockop, D.J. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci U S A 97, 3213, 2000.
73. Colter, D.C., Sekiya, I., and Prockop, D.J. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proc Natl Acad Sci U S A 98, 7841, 2001.
74. Sekiya, I., Larson, B.L., Smith, J.R., Pochampally, R., Cui, J.G., and Prockop, D.J. Expansion of human adult stem cells from bone marrow stroma: conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20, 530, 2002.
75. Prockop, D.J., Gregory, C.A., and 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 100, 11917, 2003.
76. Mueller, S.M., and Glowacki, J. Age-related decline in the osteogenic potential of human bone marrow cells cultured in three-dimensional collagen sponges. J Cell Biochem 82, 583, 2001.
77. Segawa, Y., Muneta, T., Makino, H., Nimura, A., Mochizuki, T., Ju, Y.J., Ezura, Y., Umezawa, A., and Sekiya, I. Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. J Orthop Res 27, 435, 2009.
78. Djouad, F., Bony, C., Haupl, T., Uze, G., Lahlou, N., Louis- Plence, P., Apparailly, F., Canovas, F., Reme, T., Sany, J., Jorgensen, C., and Noel, D. Transcriptional profiles discriminate bone marrow-derived and synovium-derived mesenchymal stem cells. Arthritis Res Ther 7, R304, 2005.
79. Roche, S., Delorme, B., Oostendorp, R., Barbet, R., Caton, D., Noel, D., Boumediene, K., Papadaki, H., Cousin, B., Crozet, C., Milhavet, O., Casteilla, L., Hatzfeld, J., Jorgensen, C., Charbord, P., and Lehmann, S. Comparative proteomic analysis of human mesenchymal and embryonic stem cells: towards the definition of a mesenchymal stem cell proteomic signature. Proteomics 9, 223, 2009.
80. Nagase, T., Muneta, T., Ju, Y.J., Hara, K., Morito, T., Koga, H., Nimura, A., Mochizuki, T., and Sekiya, I. Analysis of the chondrogenic potential of human synovial stem cells according to harvest site and culture parameters in knees with medial compartment osteoarthritis. Arthritis Rheum 58, 1389, 2008.
81. Chen, F., and Tuan, R. Mesenchymal stem cells in arthritis diseases. Arthritis Res Ther 10, 223, 2008.
82. Koga, H., Shimaya, M., Muneta, T., Nimura, A., Morito, T., Hayashi, M., Suzuki, S., Ju, Y.J., Mochizuki, T., and Sekiya, I. Local adherent technique for transplanting mesenchymal stem cells as a potential treatment of cartilage defect. Arthritis Res Ther 10, R84, 2008.
83. Wakitani, S., Mitsuoka, T., Nakamura, N., Toritsuka, Y., Nakamura, Y., and Horibe, S. Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports. Cell Transplant 13, 595, 2004.
84. Kamekura, S., Kawasaki, Y., Hoshi, K., Shimoaka, T., Chikuda, H., Maruyama, Z., Komori, T., Sato, S., Takeda, S., Karsenty, G., Nakamura, K., Chung, U.I., and Kawaguchi, H. Contribution of runt-related transcription factor 2 to the pathogenesis of osteoarthritis in mice after induction of knee joint instability. Arthritis Rheum 54, 2462, 2006.
85. Koga, H., Muneta, T., Ju, Y.J., Nagase, T., Nimura, A., Mochizuki, T., Ichinose, S., von der Mark, K., and Sekiya, I. Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration. Stem Cells 25, 689, 2007.
86. Muraglia, A., Cancedda, R., and Quarto, R. Clonal mesenchymalprogenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 113, 1161, 2000.
87. Pelttari, K., Winter, A., Steck, E., Goetzke, K., Hennig, T., Ochs, B.G., Aigner, T., and Richter, W. 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, 2006.
88. De Bari, C., Dell'Accio, F., Karystinou, A., Guillot, P.V., Fisk, N.M., Jones, E.A., McGonagle, D., Khan, I.M., Archer, C.W., Mitsiadis, T.A., Donaldson, A.N., Luyten, F.P., and Pitzalis, C. A biomarker-based mathematical model to predict bone forming potency of human synovial and periosteal mesenchymal stem cells. Arthritis Rheum 58, 240, 2008.
89. Dickhut, A., Pelttari, K., Janicki, P., Wagner, W., Eckstein, V., Egermann, M., and Richter, W. Calcification or dedifferentiation: requirment to lock mesenchymal stem cells in a desired differentiation stage. J Cell Physiol 219, 219, 2009.
90. Mochizuki, T., Muneta, T., Sakaguchi, Y., Nimura, A., Yokoyama, A., Koga, H., and Sekiya, I. Higher chondrogenic potential of fibrous synovium- and adipose synoviumderived cells compared with subcutaneous fat-derived cells. Arthritis Rheum 54, 843, 2006.
91. Lee, S., Nakagawa, T., and Reddi, A. Mesenchymal progenitor cells derived from synovium and infrapatellar fat pad as a source for superficial zone cartilage tissue engineering: analysis of superficial zone protein/lubricin expression. Tissue Eng Part A 16, 317, 2010.
92. Mobasheri, A., Csaki, C., Clutterbuck, A.L., Rahmanzadeh, M., and Shakibael, M. Mesenchymal stem cells in connective tissue engineering and regenerative medicine: applications in cartilage repair and osteoarthritis therapy. Histol Histopathol 24, 347, 2009.
93. Zheng, H., Martin, J.A., Duwayri, Y., Falcon, G., and Buckwalter, J.A. Impact of aging on rat bone marrowderived stem cell chondrogenesis. J Gerontol A Biol Sci Med Sci 62, 136, 2007.
94. Barbero, A., Grogan, S., Schafer, D., Heberer, M., Mainil- Varlet, P., and Martin, I. Age related changes in human articular chondrocyte yield, proliferation and postexpansion chondrogenic capacity. Osteoarthritis Cartilage 12, 476, 2004.
95. D'Ippolito, G., Schiller, P.C., Ricordi, C., Roos, B.A., and Howard, G.A. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 14, 1115, 1999.
96. Muschler, G.F., Nitto, H., Boehm, C.A., and Easley, K.A. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res 19, 117, 2001.
97. Payne, K.A., Didiano, D.M., and Chu, C.R. Donor sex and age influence the chondrogenic potential of human femoral bone marrow stem cells. Osteoarthritis Cartilage 18, 705, 2010.
98. Stolzing, A., Jones, E., McGonagle, D., and Scutt, A. Agerelated changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mech Ageing Dev 129,163, 2008.
99. Campbell, W.G., Jr., and Callahan, B.C. Regeneration of synovium of rabbit knees after total chemical synovectomy by ingrowth of connective tissue-forming elements from adjacent bone. A light and electron microscopic study. Lab Invest 24, 404, 1971.
100. Bentley, G., Kreutner, A., and Ferguson, A.B. Synovial regeneration and articular cartilage changes after synovectomy in normal and steroid-treated rabbits. J Bone Joint Surg Br 57, 454, 1975.
101. Lee, S.Y., Miwa, M., Sakai, Y., Kuroda, R., Matsumoto, T., Iwakura, T., Fujioka, H., Doita, M., and Kurosaka, M. In vitro multipotentiality and characterization of human unfractured traumatic hemarthrosis-derived progenitor cells: a potential cell source for tissue repair. J Cell Physiol 210, 561, 2007.
102. Ochi, T., Yoshikawa, H., Toyosaki-Maeda, T., and Lipsky, P. Nurse-like cells reside in the synovial tissue and bone marrow in rheumatoid arthritis. Arthritis Res Ther 9, 201, 2007.
103. Koga, H., Muneta, T., Nagase, T., Nimura, A., Ju, Y.J., Mochizuki, T., and Sekiya, I. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 333, 207, 2008.
104. Pei, M., He, F., Boyce, B.M., and Kish, V.L. Repair of fullthickness femoral condyle cartilage defects using allogenic synovial cell-engineered tissue constructs. Osteoarthritis Cartilage 17, 714, 2009.
105. Chen, S., Emery, S.E., and Pei, M. Coculture of synoviumderived stem cells and nucleus pulposus cells in serum-free defined medium with supplementation of transforming growth factor-b1. Spine 34, 1272, 2009.
106. Arnoczky, S.P., and Warren, R.F. The microvasculature of the meniscus and its response to injury. An experimental study in the dog. Am J Sports Med 11, 131, 1983.
107. Ghadially, F.N., Wedge, J.H., and Lalonde, J.M. Experimental methods of repairing injured menisci. J Bone Joint Surg Br 68, 106, 1986.
108. Ghosh, P., Sutherland, J., Bellenger, C., Read, R., and Darvodelsky, A. The influence of weight-bearing exercise on articular cartilage of meniscectomized joints. An experimental study in sheep. Clin Orthop Relat Res 252, 101, 1990.
109. Klompmaker, J., Veth, R.P., Jansen, H.W., Nielsen, H.K., deGroot, J.H., Pennings, A.J., and Kuijer, R. Meniscal repair by fibrocartilage in the dog: characterization of the repair tissue and the role of vascularity. Biomaterials 17, 1685, 1996.
110. Fox, D.B., Cook, J.L., Arnoczky, S.P., Tomlinson, J.L., Kuroki, K., Kreeger, J.M., and Malaviya, P. Fibrochondrogenesis of free intraarticular small intestinal submucosa scaffolds. Tissue Eng 10, 129, 2004.
111. Mwale, F., Roughley, P., and Antoniou, J. Distinction between the extracellular matrix of the nucleus pulposus and hyaline cartilage: a requisite for tissue engineering of intervertebral disc. Eur Cell Mater 8, 58, 2004.
112. Marinova-Mutafchieva, L., Williams, R.O., Funa, K., Maini, R.N., and Zvaifler, N.J. Inflammation is preceded by tumor necrosis factor dependent infiltration of mesenchymal cells in experimental arthritis. Arthritis Rheum 46, 507, 2002.
113. Murphy, J.M., Dixon, K., Beck, S., Fabian, D., Feldman, A., and Barry, F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum 46, 704, 2002.
114. Loeuille, D., Chary-Valckenaere, I., Champigneulle, J., Rat, A.C., Toussaint, F., Pinzano-Watrin, A., Goebel, J.C., Mainard, D., Blum, A., Pourel, J., Netter, P., and Gillet, P. Macroscopic and microscopic features of synovial membrane inflammation in the osteoarthritic knee: correlating magnetic resonance imaging findings with disease severity. Arthritis Rheum 52, 3492, 2005.
115. Neumann, E., Lefevre, S., Zimmermann, B., Gay, S., and Muller-Ladner, U. Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med 16, 458, 2010.
116. Tyndall, A., and van Laar, J.M. Stem cells in the treatment of inflammatory arthritis. Best Pract Res Clin Rheumatol 24, 565, 2010.
117. Noss, E., and Brenner, M. The role and therapeutic implications of fibroblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunol Rev 223, 252, 2008.
118. Arufe, M.C., De la Fuentes, A., Fuentes-Boquete, I., de Toro, F.J., and Blanco, F.J. Differentiation of synovial CD- 105 + human mesenchymal stem cells into chondrocytelike cells through spheroid formation. J Cell Biochem 108, 145, 2009.
119. Arufe, M.C., De la Fuentes, A., Fuentes, I., de Toro, F.J., and Blanco, F.J. Chondrogenic potential of subpopulations of cells expressing mesenchymal stem cells markers derived from human synovial membranes. J Cell Biochem 111, 834, 2010.
120. Wagner, E.F., and Karsenty, G. Genetic control of skeletal development [review]. Curr Opin Genet Dev 11, 527, 2001.
121. Karsenty, G., and Wagner, E.F. Reaching a genetic and molecular understanding of skeletal development [review]. Dev Cell 2, 389, 2002.
122. Shintani, N., and Hunziker, E. Chondrogenic differentiation of bovine synovium: bone morphogenic proteins 2 and 7 and transforming growth factor b1 induce the formation of different types of cartilaginous tissue. Arthritis Rheum 56, 1869, 2007.
123. Carter, D.R., Beaupre, G.S., Giori, N.J., and Helms, J.A. Mechanobiology of skeletal regeneration. Clin Orthop Relat Res 355(Suppl.), S41, 1998.
124. D'Lima, D.D., Hashimoto, S., Chen, P.C., Lotz, M.K., and Colwell, C.W., Jr. Cartilage injury induces chondrocyte apoptosis. J Bone Joint Surg Am 83A(Suppl. 2), 19, 2001.
125. Rot-Nikcevic, I., Reddy, T., Downing, K.J., Belliveau, A.C., Hallgrimsson, B., Hall, B.K., and Kablar, B. Myf5 -/- :MyoD -/- amyogenic fetuses reveal the importance of early contraction and static loading by striated muscle in mouse skeletogenesis. Dev Genes Evol 216, 1, 2006.
126. Lumpkin, E.A., and Caterina, M.J. Mechanisms of sensory transduction in the skin. Nature 445, 858, 2007.
127. Neu, C.P., Komvopoulos, K., and Reddi, A.H. The interface of functional biotribology and regenerative medicine in synovial joints. Tissue Eng Part B Rev 14, 235, 2008.