Direct and indirect co-culture of chondrocytes and mesenchymal stem cells for the generation of polymer/extracellular matrix hybrid constructs

Acta Biomaterialia

Volumn 10, Issue 5, 2014, Pages 1824-1835

  Levorson, Erica J ^a   Santoro, Marco ^a   Kurtis Kasper, F ^a   Mikos, Antonios G ^a  

^a Rice University   (United States)

Author keywords

Cartilage tissue engineering; Chondrocyte; Co culture; Extracellular matrix; Mesenchymal stem cell

Indexed keywords

BIOREACTORS; BODY FLUIDS; CARTILAGE; CELL ENGINEERING; CELL PROLIFERATION; CELL SIGNALING; FLOWCHARTING; SCAFFOLDS (BIOLOGY); STEM CELLS; WEAVING;

CARTILAGE TISSUE ENGINEERING; CELL TYPES; CELL-CELL CONTACT; CHONDROCYTES; CO-CULTURES; EXTRACELLULAR MATRICES; HYBRID CONSTRUCTS; MATRIX HYBRIDS; MESENCHYMAL STEM CELL; STATIC CULTURE;

CELL CULTURE;

COLLAGEN; GLYCOSAMINOGLYCAN; POLYCAPROLACTONE; TISSUE SCAFFOLD; DNA; POLYESTER;

ANIMAL CELL; ARTICLE; BIOREACTOR; CARTILAGE CELL; CELL CONTACT; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHONDROGENESIS; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EXTRACELLULAR MATRIX; HISTOLOGY; MALE; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; ANIMAL; BIOSYNTHESIS; BOVINAE; CELL COUNT; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; PROCEDURES; RABBIT; STAINING; SURFACE PROPERTY; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ANIMALS; BIOREACTORS; CATTLE; CELL COUNT; CHONDROCYTES; COCULTURE TECHNIQUES; COLLAGEN; DNA; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCANS; MESENCHYMAL STROMAL CELLS; POLYESTERS; RABBITS; STAINING AND LABELING; SURFACE PROPERTIES; TISSUE SCAFFOLDS;

EID: 84898058927     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.12.026     Document Type: Article

References (58)

1. J.A. Jansen, J.W.M. Vehof, P.Q. Ruhé, H. Kroeze-Deutman, Y. Kuboki, and H. Takita et al. Growth factor-loaded scaffolds for bone engineering J Control Release 101 2005 127
2. H. Park, J.S. Temenoff, T.A. Holland, Y. Tabata, and A.G. Mikos Delivery of TGF-[beta]1 and chondrocytes via injectable, biodegradable hydrogels for cartilage tissue engineering applications Biomaterials 26 2005 7095 7103
3. B.S. Harrison, D. Eberli, S.J. Lee, A. Atala, and J.J. Yoo Oxygen producing biomaterials for tissue regeneration Biomaterials 28 2007 4628
4. C.V.C. Bouten, P.Y.W. Dankers, A. Driessen-Mol, S. Pedron, A.M.A. Brizard, and F.P.T. Baaijens Substrates for cardiovascular tissue engineering Adv Drug Deliv Rev 63 2011 221 241
5. L.A. Solchaga, J. Gao, J.E. Dennis, A. Awadallah, M. Lundberg, and A.I. Caplan et al. Treatment of osteochondral defects with autologous bone marrow in a hyaluronan-based delivery vehicle Tissue Eng 8 2002 333 347
6. R.A. Calandruccio, and W.S. Gilmer Jr. Proliferation, regeneration, and repair of articular cartilage of immature animals J Bone Joint Surg Am 44 1962 431 455
7. J. Weisser, B. Rahfoth, A. Timmermann, T. Aigner, R. Bräuer, and K. von der Mark Role of growth factors in rabbit articular cartilage repair by chondrocytes in agarose Osteoarthr Cartil 9 2001 S48 S54
8. K.E.M. Benders, P.R.v. Weeren, S.F. Badylak, D.B.F. Saris, W.J.A. Dhert, and J. Malda Extracellular matrix scaffolds for cartilage and bone regeneration Trends Biotechnol 31 2013 169 176
9. J.A. Matthews, E.D. Boland, G.E. Wnek, D.G. Simpson, and G.L. Bowlin Electrospinning of collagen type II: a feasibility study J Bioact Compat Polym 18 2003 125 134
10. A.M. Bhosale, and J.B. Richardson Articular cartilage: structure, injuries and review of management Br Med Bull 87 2008 77 95
11. W.-C. Chen, C.-L. Yao, Y.-H. Wei, and I.M. Chu Evaluating osteochondral defect repair potential of autologous rabbit bone marrow cells on type II collagen scaffold Cytotechnology 63 2011 13 23
12. M. Wollenweber, H. Domaschke, T. Hanke, S. Boxberger, G. Schmack, and K. Gliesche et al. Mimicked bioartificial matrix containing chondroitin sulphate on a textile scaffold of poly(3-hydroxybutyrate) alters the differentiation of adult human mesenchymal stem cells Tissue Eng 12 2006 345 359
13. S.-h. Hsu, H.-J. Yen, C.-S. Tseng, C.-S. Cheng, and C.-L. Tsai Evaluation of the growth of chondrocytes and osteoblasts seeded into precision scaffolds fabricated by fused deposition manufacturing J Biomed Mater Res B Appl Biomater 80B 2007 519 527
14. J. Liao, X. Guo, K.J. Grande-Allen, F.K. Kasper, and A.G. Mikos Bioactive polymer/extracellular matrix scaffolds fabricated with a flow perfusion bioreactor for cartilage tissue engineering Biomaterials 31 2010 8911 8920
15. Levorson EJ, Mountziaris PM, Hu O, Kasper FK, Mikos AG. Cell derived polymer/extracellular matrix composite scaffolds for cartilage regeneration. Part 1. Investigation of co-cultures and seeding densities for improved extracellular matrix deposition. Tissue Eng Part C Methods 2013. http://dx.doi.org/10.1089/ten.TEC.2013.0286 [Epub ahead of print].
16. V.V. Meretoja, R.L. Dahlin, F.K. Kasper, and A.G. Mikos Enhanced chondrogenesis in co-cultures with articular chondrocytes and mesenchymal stem cells Biomaterials 33 2012 6362 6369
17. W.-H. Chen, M.-T. Lai, A.T.H. Wu, C.-C. Wu, J.G. Gelovani, and C.-T. Lin et al. In vitro stage-specific chondrogenesis of mesenchymal stem cells committed to chondrocytes Arthritis Rheum 60 2009 450 459
18. J. Hendriks, J. Riesle, and C.A. van Blitterswijk Co-culture in cartilage tissue engineering J Tissue Eng Regen Med 1 2007 170 178
19. N.S. Hwang, S. Varghese, C. Puleo, Z. Zhang, and J. Elisseeff Morphogenetic signals from chondrocytes promote chondrogenic and osteogenic differentiation of mesenchymal stem cells J Cell Physiol 212 2007 281 284
20. J. Fischer, A. Dickhut, M. Rickert, and W. Richter Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis Arthritis Rheum 62 2010 2696 2706
21. L. Bian, D.Y. Zhai, R.L. Mauck, and J.A. Burdick Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage Tissue Eng Part A 7 2011 1137 1145
22. L. Wu, J.C.H. Leijten, N. Georgi, J.N. Post, C.A.v. Blitterswijk, and M. Karperien Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation Tissue Eng Part A 17 2011 1425 1436
23. G.M. van Buul, E. Villafuertes, P.K. Bos, J.H. Waarsing, N. Kops, and R. Narcisi et al. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture Osteoarthr Cartil 20 2012 1186 1196
24. L. Wu, H.-J. Prins, M.N. Helder, C.A.v. Blitterswijk, and M. Karperien Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources Tissue Eng Part A 18 2012 1542 1551
25. I. Sekiya, J.T. Vuoristo, B.L. Larson, and D.J. Prockop In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis PNAS 99 2002 4397 4402
26. V. Lettry, K. Hosoya, S. Takagi, and M. Okumura Coculture of equine mesenchymal stem cells and mature equine articular chondrocytes results in improved chondrogenic differentiation of the stem cells Jpn J Vet Res 58 2010 5 15
27. N. Ahmed, R. Dreier, A. Göpferich, J. Grifka, and S. Grässel Soluble signalling factors derived from differentiated cartilage tissue affect chondrogenic differentiation of rat adult marrow stromal cells Cell Physiol Biochem 20 2007 665 678
28. Levorson EJ, Hu O, Mountziaris PM, Kasper FK, Mikos AG. Cell derived polymer/extracellular matrix composite scaffolds for cartilage regeneration. Part 2. Construct Devitalization and Determination of Chondroinductive Capacity. Tissue Eng Part C Methods 2013. http://dx.doi.org/10.1089/ten.tec.2013.0288 [Epub ahead of print].
29. E.J. Levorson, P.R. Sreerekha, K.P. Chennazhi, F.K. Kasper, S.V. Nair, and A.G. Mikos Fabrication and characterization of multiscale electrospun scaffolds for cartilage regeneration Biomed Mater 8 2013 014103
30. V.V. Meretoja, R.L. Dahlin, S. Wright, F.K. Kasper, and A.G. Mikos The effect of hypoxia on the chondrogenic differentiation of co-cultured articular chondrocytes and mesenchymal stem cells in scaffolds Biomaterials 34 2013 4266 4273
31. R.L. Dahlin, V.V. Meretoja, M. Ni, F.K. Kasper, and A.G. Mikos Hypoxia and flow perfusion modulate proliferation and gene expression of articular chondrocytes on porous scaffolds AIChE J 59 2013 3158 3166
32. X. Guo, J. Liao, H. Park, A. Saraf, R.M. Raphael, and Y. Tabata et al. Effects of TGF-beta3 and preculture period of osteogenic cells on the chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in a bilayered hydrogel composite Acta Biomater 6 2010 2920 2931
33. R.L. Dahlin, V.V. Meretoja, M. Ni, F.K. Kasper, and A.G. Mikos Design of a high-throughput flow perfusion bioreactor system for tissue engineering Tissue Eng Part C Methods 18 2012 817 820
34. R.A. Thibault, A.G. Mikos, and F.K. Kasper Osteogenic differentiation of mesenchymal stem cells on demineralized and devitalized biodegradable polymer and extracellular matrix hybrid constructs J Biomed Mater Res A 101A 2013 1225 1236
35. N. Datta, Q.P. Pham, U. Sharma, V.I. Sikavitsas, J.A. Jansen, and A.G. Mikos In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation PNAS 103 2006 2488 2493
36. H. Stegemann, and K. Stalder Determination of hydroxyproline Clin Chim Acta 18 1967 267 273
37. C.P. Barnes, C.W. Pemble, D.D. Brand, D.G. Simpson, and G.L. Bowlin Cross-linking electrospun type II collagen tissue engineering scaffolds with carbodiimide in ethanol Tissue Eng 13 2007 1593 1605
38. B. Rentsch, A. Hofmann, A. Breier, C. Rentsch, and D. Scharnweber Embroidered and surface modified polycaprolactone-co-lactide scaffolds as bone substitute: in vitro characterization Ann Biomed Eng 37 2009 2118 2128
39. M.E. Gomes, C.M. Bossano, C.M. Johnston, R.L. Reis, and A.G. Mikos In vitro localization of bone growth factors in constructs of biodegradable scaffolds seeded with marrow stromal cells and cultured in a flow perfusion bioreactor Tissue Eng 12 2006 177 188
40. J. Liao, X. Guo, D. Nelson, F. Kurtis Kasper, and A.G. Mikos Modulation of osteogenic properties of biodegradable polymer/extracellular matrix scaffolds generated with a flow perfusion bioreactor Acta Biomater 6 2010 2386 2393
41. R.A. Thibault, A.G. Mikos, and F.K. Kasper Protein and mineral composition of osteogenic extracellular matrix constructs generated with a flow perfusion bioreactor Biomacromolecules 12 2011 4204 4212
42. R.A. Thibault Scott Baggett L, Mikos AG, Kasper FK. Osteogenic differentiation of mesenchymal stem cells on pregenerated extracellular matrix scaffolds in the absence of osteogenic cell culture supplements Tissue Eng Part A 16 2010 431 440
43. J.M.M. Martin, M. Smith, and M. Al-Rubeai Cryopreservation and in vitro expansion of chondroprogenitor cells isolated from the superficial zone of articular cartilage Biotechnol Prog 21 2005 168 177
44. Y. Li, T. Ma, D.A. Kniss, L.C. Lasky, and S.-T. Yang Effects of filtration seeding on cell density, spatial distribution, and proliferation in nonwoven fibrous matrices Biotechnol Prog 17 2001 935 944
45. J. Alvarez-Barreto, S. Linehan, R. Shambaugh, and V. Sikavitsas Flow perfusion improves seeding of tissue engineering scaffolds with different architectures Ann Biomed Eng 35 2007 429
46. E.J. Levorson, F.K. Kasper, and A.G. Mikos Scaffolds - flow perfusion bioreactor design P. Ducheyne, K.E. Healy, D.W. Hutmacher, C.J. Kirkpatrick, Comprehensive biomaterials 2011 Elsevier Oxford 1 11
47. G.N. Bancroft, V.I. Sikavitsas, and A.G. Mikos Technical note: design of a flow perfusion bioreactor system for bone tissue-engineering applications Tissue Eng 9 2003 549 554
48. B. Amsden Solute diffusion within hydrogels. mechanisms and models Macromolecules 31 1998 8382 8395
49. D.M. Knapik, J.D. Harris, G. Pangrazzi, M.J. Griesser, R.A. Siston, and S. Agarwal et al. The basic science of continuous passive motion in promoting knee health: a systematic review of studies in a rabbit model Arthroscopy 29 2013 1722 1731
50. P. Edouard, F. Rannou, and E. Coudeyre Animal evidence for hyaluronic acid efficacy in knee trauma injuries. Review of animal-model studies Phys Ther Sport 14 2013 116 123
51. D. Huey, J. Sanchez-Adams, V. Willard, and K. Athanasiou Immunogenicity of bovine and leporine articular chondrocytes and meniscus cells Tissue Eng Part A 18 2012 568 575
52. T.A. Holland, E.W.H. Bodde, L.S. Baggett, Y. Tabata, A.G. Mikos, and J.A. Jansen Osteochondral repair in the rabbit model utilizing bilayered, degradable oligo(poly(ethylene glycol) fumarate) hydrogel scaffolds J Biomed Mater Res Part A 75A 2005 156 167
53. X.-T. Mo, S.-C. Guo, H.-Q. Xie, L. Deng, W. Zhi, and Z. Xiang 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 45 2009 42 51
54. E. Grimaud, D. Heymann, and F. Rédini Recent advances in TGF-β effects on chondrocyte metabolism: potential therapeutic roles of TGF-β in cartilage disorders Cytokine Growth Factor Rev 13 2002 241 257
55. B.D. Elder, and K.A. Athanasiou Systematic assessment of growth factor treatment on biochemical and biomechanical properties of engineered articular cartilage constructs Osteoarthr Cartil 17 2009 114
56. L.Z. Sailor, R.M. Hewick, and E.A. Morris Recombinant human bone morphogenetic protein-2 maintains the articular chondrocyte phenotype in long-term culture J Orthop Res 14 1996 937 945
57. C. Acharya, A. Adesida, P. Zajac, M. Mumme, J. Riesle, and I. Martin et al. Enhanced chondrocyte proliferation and mesenchymal stromal cells chondrogenesis in coculture pellets mediate improved cartilage formation J Cell Physiol 227 2011 88 97
58. X. Liu, H. Sun, D. Yan, L. Zhang, X. Lv, and T. Liu et al. In vivo ectopic chondrogenesis of BMSCs directed by mature chondrocytes Biomaterials 31 2010 9406 9414