Mesenchymal stem cells downregulate articular chondrocyte differentiation in noncontact coculture systems: Implications in cartilage tissue regeneration

Stem Cells and Development

Volumn 22, Issue 11, 2013, Pages 1657-1669

  Xu, Lei ^a   Wang, Qi ^a   Xu, Feiyue ^a   Ye, Zhaoyang ^a   Zhou, Yan ^a   Tan, Wen Song ^a  

^a EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN;

ANIMAL CELL; ARTICLE; CARTILAGE CELL; CELL AGGREGATION; CELL CONTACT; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL TRANSFORMATION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; ENCAPSULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDROGEL; MESENCHYMAL STEM CELL; MONOLAYER CULTURE; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; SPINDLE CELL; TISSUE REGENERATION;

ALGINATES; ANIMALS; CARTILAGE, ARTICULAR; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COCULTURE TECHNIQUES; COLLAGEN TYPE II; EXTRACELLULAR MATRIX; GLUCURONIC ACID; GLYCOSAMINOGLYCANS; GUIDED TISSUE REGENERATION; HEXURONIC ACIDS; HUMANS; HYDROGELS; MESENCHYMAL STROMAL CELLS; RABBITS;

EID: 84878101584     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0605     Document Type: Article

References (54)

1. Redman SN, SF Oldfield and CW Archer. (2005). Current strategies for articular cartilage repair. Eur Cell Mater 9:23-32; discussion 23-32.
2. Brittberg M, A Lindahl, A Nilsson, C Ohlsson, O Isaksson and L Peterson. (1994). Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331:889-895.
3. Hunziker EB. (2009). The elusive path to cartilage regeneration. Adv Mater 21:3419-3424.
4. Goepfert C, A Slobodianski, AF Schilling, P Adamietz and R Portner. (2010). Cartilage engineering from mesenchymal stem cells. Adv Biochem Eng Biotechnol 123:163-200.
5. Bulman SE, V Barron, CM Coleman and F Barry. (2012). Enhancing the mesenchymal stem cell therapeutic response: cell localization and support for cartilage repair. Tissue Eng Part B Rev 19:58-68.
6. Tew SR, AD Murdoch, RP Rauchenberg and TE Hardingham. (2008). Cellular methods in cartilage research: primary human chondrocytes in culture and chondrogenesis in human bone marrow stem cells. Methods 45:2-9.
7. Erickson IE, AH Huang, C Chung, RT Li, JA Burdick and RL Mauck. (2009). Differential maturation and structure-function relationships in mesenchymal stem cell-and chondrocyteseeded hydrogels. Tissue Eng Part A 15:1041-1052.
8. Scotti C, B Tonnarelli, A Papadimitropoulos, A Scherberich, S Schaeren, A Schauerte, J Lopez-Rios, R Zeller, A Barbero and I Martin. (2010). Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci USA 107:7251-7256.
9. Hellingman CA, W Koevoet and GJ van Osch. (2012). Can one generate stable hyaline cartilage from adult mesenchymal stem cells? A developmental approach. J Tissue Eng Regen Med 6:e1-e11.
10. Dickhut A, K Pelttari, P Janicki, W Wagner, V Eckstein, M Egermann and W Richter. (2009). Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage. J Cell Physiol 219:219-226.
11. Pelttari K, A Winter, E Steck, K Goetzke, T Hennig, BG Ochs, T Aigner and W Richter. (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.
12. Hillel AT, JM Taube, TC Cornish, B Sharma, M Halushka, EF McCarthy, GM Hutchins and JH Elisseeff. (2010). Characterization of human mesenchymal stem cell-engineered cartilage: analysis of its ultrastructure, cell density and chondrocyte phenotype compared to native adult and fetal cartilage. Cells Tissues Organs 191:12-20.
13. Muraglia A, A Corsi, M Riminucci, M Mastrogiacomo, R Cancedda, P Bianco and R Quarto. (2003). Formation of a chondro-osseous rudiment in micromass cultures of human bone-marrow stromal cells. J Cell Sci 116:2949-2955.
14. Leijten J, N Georgi, L Wu, C van Blitterswijk and M Karperien. (2012). Cell sources for articular cartilage repair strategies: shifting from mono-cultures to co-cultures. Tissue Eng Part B Rev 19:31-40.
15. Hendriks J, J Riesle and CA van Blitterswijk. (2007). Coculture in cartilage tissue engineering. J Tissue Eng Regen Med 1:170-178.
16. Fischer J, A Dickhut, M Rickert and W Richter. (2010). Human articular chondrocytes secrete parathyroid hormonerelated protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 62:2696-2706.
17. Chen WH, MT Lai, AT Wu, CC Wu, JG Gelovani, CT Lin, SC Hung, WT Chiu and WP Deng. (2009). In vitro stage-specific chondrogenesis of mesenchymal stem cells committed to chondrocytes. Arthritis Rheum 60:450-459.
18. Liu X, H Sun, D Yan, L Zhang, X Lv, T Liu,WZhang,WLiu, Y Cao and G Zhou. (2010). In vivo ectopic chondrogenesis of BMSCs directed by mature chondrocytes. Biomaterials 31:9406-9414.
19. Aung A, G Gupta, G Majid and S Varghese. (2011). Osteoarthritic chondrocyte-secreted morphogens induce chondrogenic differentiation of human mesenchymal stem cells. Arthritis Rheum 63:148-158.
20. Acharya C, A Adesida, P Zajac, M Mumme, J Riesle, I Martin and A Barbero. (2012). Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation. J Cell Physiol 227:88-97.
21. Meretoja VV, RL Dahlin, FK Kasper and AG Mikos. (2012). Enhanced chondrogenesis in co-cultures with articular chondrocytes and mesenchymal stem cells. Biomaterials 33:6362-6369.
22. Wu L, JC Leijten, N Georgi, JN Post, CA van Blitterswijk and M Karperien. (2011). Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation. Tissue Eng Part A 17:1425-1436.
23. Giovannini S, J Diaz-Romero, T Aigner, P Heini, P Mainil-Varlet and D Nesic. (2010). Micromass co-culture of human articular chondrocytes and human bone marrow mesenchymal stem cells to investigate stable neocartilage tissue formation in vitro. Eur Cell Mater 20:245-259.
24. Caplan AI and JE Dennis. (2006). Mesenchymal stem cells as trophic mediators. J Cell Biochem 98:1076-1084.
25. Gnecchi M, H He, OD Liang, LG Melo, F Morello, H Mu, N Noiseux, L Zhang, RE Pratt, JS Ingwall and VJ Dzau. (2005). Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11:367-368.
26. Tsuchiya K, G Chen, T Ushida, T Matsuno and T Tateishi. (2004). The effect of coculture of chondrocytes with mesenchymalstemcells on their cartilaginous phenotype in vitro. Mater Sci Eng C 24:391-396.
27. Watanabe T, D Sakai, Y Yamamoto, T Iwashina, K Serigano, F Tamura and J Mochida. (2010). Human nucleus pulposus cells significantly enhanced biological properties in a coculture system with direct cell-to-cell contact with autologous mesenchymal stem cells. J Orthop Res 28:623-630.
28. Ma D, C Zhong, H Yao, Y Liu, F Chen, J Li, J Zhao, T Mao and L Ren. (2011). Engineering injectable bone using bone marrow stromal cell aggregates. Stem Cells Dev 20:989-999.
29. Lapi S, F Nocchi, R Lamanna, S Passeri, M Iorio, A Paolicchi, P Urciuoli, A Coli, F Abramo, et al. (2008). Different media and supplements modulate the clonogenic and expansion properties of rabbit bone marrow mesenchymal stem cells. BMC Res Notes 1:53.
30. Chen M, X Wang, Z Ye, Y Zhang, Y Zhou and WS Tan. (2011). A modular approach to the engineering of a centimeter-sized bone tissue construct with human amniotic mesenchymal stem cells-laden microcarriers. Biomaterials 32:7532-7542.
31. Hass R, C Kasper, S Bohm and R Jacobs. (2011). Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal 9:12.
32. Kim YJ, RL Sah, JY Doong and AJ Grodzinsky. (1988). Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174:168-176.
33. Farndale RW, DJ Buttle and AJ Barrett. (1986). Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173-177.
34. Enobakhare BO, DL Bader and DA Lee. (1996). Quantification of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue. Anal Biochem 243:189-191.
35. Mahmoudifar N and PM Doran. (2012). Chondrogenesis and cartilage tissue engineering: the longer road to technology development. Trends Biotechnol 30:166-176.
36. Xu J, W Wang, M Ludeman, K Cheng, T Hayami, JC Lotz and S Kapila. (2008). Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels. Tissue Eng Part A 14:667-680.
37. Hauselmann HJ, RJ Fernandes, SS Mok, TM Schmid, JA Block, MB Aydelotte, KE Kuettner and EJ Thonar. (1994). Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads. J Cell Sci 107 (Pt 1): 17-27.
38. Schnabel M, S Marlovits, G Eckhoff, I Fichtel, L Gotzen, V Vecsei and J Schlegel. (2002). Dedifferentiation-associated changes in morphology and gene expression in primary human articular chondrocytes in cell culture. Osteoarthritis Cartilage 10:62-70.
39. Bian L, DY Zhai, RL Mauck and JA Burdick. (2011). Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng Part A 17:1137-1145.
40. Grandolfo M, P D'Andrea, S Paoletti, M Martina, G Silvestrini, E Bonucci and F Vittur. (1993). Culture and differentiation of chondrocytes entrapped in alginate gels. Calcif Tissue Int 52:42-48.
41. Varghese S, NS Hwang, AC Canver, P Theprungsirikul, DW Lin and J Elisseeff. (2008). Chondroitin sulfate based niches for chondrogenic differentiation of mesenchymal stem cells. Matrix Biol 27:12-21.
42. Domm C, M Schunke, K Christesen and B Kurz. (2002). Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 10:13-22.
43. Schulze-Tanzil G, P de Souza, H Villegas Castrejon, T John, HJ Merker, A Scheid and M Shakibaei. (2002). Redifferentiation of dedifferentiated human chondrocytes in high-density cultures. Cell Tissue Res 308:371-379.
44. Giovannini S, J Diaz-Romero, T Aigner, P Mainil-Varlet and D Nesic. (2010). Population doublings and percentage of S100-positive cells as predictors of in vitro chondrogenicity of expanded human articular chondrocytes. J Cell Physiol 222:411-420.
45. Diaz-Romero J, D Nesic, SP Grogan, P Heini and P Mainil-Varlet. (2008). Immunophenotypic changes of human articular chondrocytes during monolayer culture reflect bona fide dedifferentiation rather than amplification of progenitor cells. J Cell Physiol 214:75-83.
46. Diaz-Romero J, JP Gaillard, SP Grogan, D Nesic, T Trub and P Mainil-Varlet. (2005). Immunophenotypic analysis of human articular chondrocytes: changes in surface markers associated with cell expansion in monolayer culture. J Cell Physiol 202:731-742.
47. Zeiter S, M der Werf and K Ito. (2009). The fate of bovine bone marrow stromal cells in hydrogels: a comparison to nucleus pulposus cells and articular chondrocytes. J Tissue Eng Regen Med 3:310-320.
48. Murphy JM, DJ Fink, EB Hunziker and FP Barry. (2003). Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48:3464-3474.
49. Weil BR, TA Markel, JL Herrmann, AM Abarbanell and DR Meldrum. (2009). Mesenchymal stem cells enhance the viability and proliferation of human fetal intestinal epithelial cells following hypoxic injury via paracrine mechanisms. Surgery 146:190-197.
50. Poree B, M Kypriotou, C Chadjichristos, G Beauchef, E Renard, F Legendre, M Melin, S Gueret, DJ Hartmann, et al. (2008). Interleukin-6 (IL-6) and/or soluble IL-6 receptor down-regulation of human type II collagen gene expression in articular chondrocytes requires a decrease of Sp1.Sp3 ratio and of the binding activity of both factors to the COL2A1 promoter. J Biol Chem 283:4850-4865.
51. Guerne PA, A Desgeorges, JM Jaspar, B Relic, R Peter, P Hoffmeyer and JM Dayer. (1999). Effects of IL-6 and its soluble receptor on proteoglycan synthesis and NO release by human articular chondrocytes: comparison with IL-1. Modulation by dexamethasone. Matrix Biol 18:253-260.
52. Grassel S, M Rickert, A Opolka, A Bosserhoff, P Angele, J Grifka and S Anders. (2010). Coculture between periosteal explants and articular chondrocytes induces expression of TGF-beta1 and collagen I. Rheumatology (Oxford) 49:218-230.
53. Rothenberg AR, L Ouyang and JH Elisseeff. (2011). Mesenchymal stem cell stimulation of tissue growth depends on differentiation state. Stem Cells Dev 20:405-414.
54. Guo X, H Park, G Liu, W Liu, Y Cao, Y Tabata, FK Kasper and AG Mikos. (2009). In vitro generation of an osteochondral construct using injectable hydrogel composites encapsulating rabbit marrow mesenchymal stem cells. Biomaterials 30:2741-2752.