Generation of osteochondral tissue constructs with chondrogenically and osteogenically predifferentiated mesenchymal stem cells encapsulated in bilayered hydrogels

Acta Biomaterialia

Volumn 10, Issue 3, 2014, Pages 1112-1123

  Lam, Johnny ^a   Lu, Steven ^a   Meretoja, Ville V ^a   Tabata, Yasuhiko ^b   Mikos, Antonios G ^a   Kasper, F Kurtis ^a  

^a Rice University   (United States)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Bilayered hydrogel; Chondrogenic predifferentiation; Co culture; Mesenchymal stem cells; Osteogenic predifferentiation

Indexed keywords

CARTILAGE; CELL ENGINEERING; CELL PROLIFERATION; COLLAGEN; FLOWCHARTING; GENE EXPRESSION; GLYCOPROTEINS; HYDROGELS; HYDROXYPROLINE; POLYETHYLENE GLYCOLS; STEM CELLS; TISSUE ENGINEERING;

BILAYERED; BILAYERED HYDROGEL; CHONDROGENIC; CHONDROGENIC PREDIFFERENTIATION; CO-CULTURES; MESENCHYMAL STEM CELL; OSTEOCHONDRAL TISSUES; OSTEOGENIC; OSTEOGENIC CELLS; OSTEOGENIC PREDIFFERENTIATION;

CELL CULTURE;

AGGRECAN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA3; ALKALINE PHOSPHATASE; CALCIUM; DNA; FUMARIC ACID DERIVATIVE; HYDROGEL; MACROGOL DERIVATIVE; POLY(ETHYLENE GLYCOL FUMARATE);

ARTICLE; BONE ATROPHY; BONE MINERALIZATION; CARTILAGE CELL; CARTILAGE DEGENERATION; CELL ENCAPSULATION; CELL POPULATION; CELL PROLIFERATION; CHONDROGENESIS; CHONDROGENIC PREDIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; HYALINE CARTILAGE; HYDROGEL; MESENCHYMAL STEM CELL; OSTEOBLAST; OSTEOGENICALLY PREDIFFERENTIATED; PHENOTYPE; PRIORITY JOURNAL; TISSUE DIFFERENTIATION; ANIMAL; BONE DEVELOPMENT; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMOBILIZED CELL; MESENCHYMAL STROMA CELL; METABOLISM; PHARMACOLOGY; PROCEDURES; RABBIT; TISSUE ENGINEERING; TISSUE SCAFFOLD;

ALKALINE PHOSPHATASE; ANIMALS; CALCIUM; CELL DIFFERENTIATION; CELLS, IMMOBILIZED; CHONDROGENESIS; DNA; FUMARATES; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HYDROGELS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; POLYETHYLENE GLYCOLS; RABBITS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84893166739     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.11.020     Document Type: Article

References (61)

1. W.W. Curl, J. Krome, E.S. Gordon, J. Rushing, B.P. Smith, and G.G. Poehling Cartilage injuries: a review of 31,516 knee arthroscopies Arthroscopy 13 1997 456 460
2. W. Widuchowski, J. Widuchowski, and T. Trzaska Articular cartilage defects: study of 25,124 knee arthroscopies Knee 14 2007 177 182
3. K.L. Spiller, S.A. Maher, and A.M. Lowman Hydrogels for the repair of articular cartilage defects Tissue Eng Part B Rev 17 2011 281 299
4. K. Mithoefer, T. McAdams, R.J. Williams, P.C. Kreuz, and B.R. Mandelbaum Clinical efficacy of the microfracture technique for articular cartilage repair in the knee: an evidence-based systematic analysis Am J Sports Med 37 2009 2053 2063
5. L. Hangody, G. Vasarhelyi, L.R. Hangody, Z. Sukosd, G. Tibay, and L. Bartha et al. Autologous osteochondral grafting-technique and long-term results Injury 39 Suppl 1 2008 S32 S39
6. C. Tetta, M. Busacca, A. Moio, R. Rinaldi, M. Delcogliano, and E. Kon et al. Knee osteochondral autologous transplantation: long-term MR findings and clinical correlations Eur J Radiol 76 2010 117 123
7. M. Marcacci, G. Filardo, and E. Kon Treatment of cartilage lesions: what works and why? Injury 44 Suppl. 1 2013 S11 S15
8. M. Brittberg Autologous chondrocyte implantation-technique and long-term follow-up Injury 39 Suppl. 1 2008 S40 S49
9. M. Brittberg, A. Lindahl, A. Nilsson, C. Ohlsson, O. Isaksson, and L. Peterson Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation N Engl J Med 331 1994 889 895
10. E. Kon, P. Verdonk, V. Condello, M. Delcogliano, A. Dhollander, and G. Filardo et al. Matrix-assisted autologous chondrocyte transplantation for the repair of cartilage defects of the knee: systematic clinical data review and study quality analysis Am J Sports Med 37 Suppl. 1 2009 156S 166S
11. N.S. Hwang, and J. Elisseeff Application of stem cells for articular cartilage regeneration J Knee Surg 22 2009 60 71
12. E. Kon, G. Filardo, A. Roffi, L. Andriolo, and M. Marcacci New trends for knee cartilage regeneration: from cell-free scaffolds to mesenchymal stem cells Curr Rev Musculoskelet Med 5 2012 236 243
13. S. Wakitani, T. Goto, S.J. Pineda, R.G. Young, J.M. Mansour, and A.I. Caplan et al. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage J Bone Joint Surg Am 76 1994 579 592
14. A.I. Caplan, M. Elyaderani, Y. Mochizuki, S. Wakitani, and V.M. Goldberg Principles of cartilage repair and regeneration Clin Orthop Relat Res 1997 254 269
15. G. Filardo, H. Madry, M. Jelic, A. Roffi, M. Cucchiarini, and E. Kon Mesenchymal stem cells for the treatment of cartilage lesions: from preclinical findings to clinical application in orthopaedics Knee Surg Sports Traumatol Arthrosc 21 2013 1717 1729
16. M. Zscharnack, P. Hepp, R. Richter, T. Aigner, R. Schulz, and J. Somerson et al. Repair of chronic osteochondral defects using predifferentiated mesenchymal stem cells in an ovine model Am J Sports Med 38 2010 1857 1869
17. B. Marquass, R. Schulz, P. Hepp, M. Zscharnack, T. Aigner, and S. Schmidt et al. Matrix-associated implantation of predifferentiated mesenchymal stem cells versus articular chondrocytes: in vivo results of cartilage repair after 1 year Am J Sports Med 39 2011 1401 1412
18. W.L. Grayson, S. Bhumiratana, P.H. Grace Chao, C.T. Hung, and G. Vunjak-Novakovic Spatial regulation of human mesenchymal stem cell differentiation in engineered osteochondral constructs: effects of pre-differentiation, soluble factors and medium perfusion Osteoarthritis Cartilage 18 2010 714 723
19. V. Guarino, A. Gloria, M.G. Raucci, and L. Ambrosio Hydrogel-based platforms for the regeneration of osteochondral tissue and intervertebral disc Polymers 4 2012 1590 1612
20. P. Nooeaid, V. Salih, J.P. Beier, and A.R. Boccaccini Osteochondral tissue engineering: scaffolds, stem cells and applications J Cell Mol Med 16 2012 2247 2270
21. S. Jo, H. Shin, A.K. Shung, J.P. Fisher, and A.G. Mikos Synthesis and characterization of oligo(poly(ethylene glycol) fumarate) macromer Macromolecules 34 2001 2839 2844
22. L.A. Kinard, F.K. Kasper, and A.G. Mikos Synthesis of oligo(poly(ethylene glycol) fumarate) Nat Protoc 7 2012 1219 1227
23. H. Park, J.S. Temenoff, T.A. Holland, Y. Tabata, and A.G. Mikos Delivery of TGF-beta1 and chondrocytes via injectable, biodegradable hydrogels for cartilage tissue engineering applications Biomaterials 26 2005 7095 7103
24. H. Park, J.S. Temenoff, Y. Tabata, A.I. Caplan, R.M. Raphael, and J.A. Jansen et al. Effect of dual growth factor delivery on chondrogenic differentiation of rabbit marrow mesenchymal stem cells encapsulated in injectable hydrogel composites J Biomed Mater Res A 88 2009 889 897
25. H. Park, X. Guo, J.S. Temenoff, Y. Tabata, A.I. Caplan, and F.K. Kasper et al. Effect of swelling ratio of injectable hydrogel composites on chondrogenic differentiation of encapsulated rabbit marrow mesenchymal stem cells in vitro Biomacromolecules 10 2009 541 546
26. H. Park, J.S. Temenoff, Y. Tabata, A.I. Caplan, and A.G. Mikos Injectable biodegradable hydrogel composites for rabbit marrow mesenchymal stem cell and growth factor delivery for cartilage tissue engineering Biomaterials 28 2007 3217 3227
27. X. Guo, H. Park, S. Young, J.D. Kretlow, J.J. van den Beucken, and L.S. Baggett et al. Repair of osteochondral defects with biodegradable hydrogel composites encapsulating marrow mesenchymal stem cells in a rabbit model Acta Biomater 6 2010 39 47
28. C.T. Lim, X. Ren, M.H. Afizah, S. Tarigan-Panjaitan, Z. Yang, and Y. Wu et al. Repair of Osteochondral defects with rehydrated freeze-dried oligo[poly(ethylene glycol) fumarate] hydrogels seeded with bone marrow mesenchymal stem cells in a porcine model Tissue Eng Part A 19 2013 1852 1861
29. T.A. Holland, Y. Tabata, and A.G. Mikos In vitro release of transforming growth factor-beta 1 from gelatin microparticles encapsulated in biodegradable, injectable oligo(poly(ethylene glycol) fumarate) hydrogels J Control Release 91 2003 299 313
30. T.A. Holland, J.K. Tessmar, Y. Tabata, and A.G. Mikos Transforming growth factor-beta 1 release from oligo(poly(ethylene glycol) fumarate) hydrogels in conditions that model the cartilage wound healing environment J Control Release 94 2004 101 114
31. 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
32. X. Guo, H. Park, G. Liu, W. Liu, Y. Cao, and Y. Tabata et al. In vitro generation of an osteochondral construct using injectable hydrogel composites encapsulating rabbit marrow mesenchymal stem cells Biomaterials 30 2009 2741 2752
33. K. Kim, J. Lam, S. Lu, P.P. Spicer, A. Lueckgen, and Y. Tabata et al. Osteochondral tissue regeneration using a bilayered composite hydrogel with modulating dual growth factor release kinetics in a rabbit model J Control Release 168 2013 166 178
34. T.D. Schmittgen, and K.J. Livak Analyzing real-time PCR data by the comparative C(T) method Nat Protoc 3 2008 1101 1108
35. R.W. Farndale, D.J. Buttle, and A.J. Barrett Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue Biochim Biophys Acta 883 1986 173 177
36. 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
37. 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
38. E. Lieb, T. Vogel, S. Milz, M. Dauner, and M.B. Schulz Effects of transforming growth factor beta1 on bonelike tissue formation in three-dimensional cell culture. II: Osteoblastic differentiation Tissue Eng 10 2004 1414 1425
39. E.K. Moioli, L. Hong, J. Guardado, P.A. Clark, and J.J. Mao Sustained release of TGFbeta3 from PLGA microspheres and its effect on early osteogenic differentiation of human mesenchymal stem cells Tissue Eng 12 2006 537 546
40. E.J. Mackie, and U. Trechsel Stimulation of bone formation in vivo by transforming growth factor-beta: remodeling of woven bone and lack of inhibition by indomethacin Bone 11 1990 295 300
41. M. Noda, and J.J. Camilliere In vivo stimulation of bone formation by transforming growth factor-beta Endocrinology 124 1989 2991 2994
42. C.A. Simmons, E. Alsberg, S. Hsiong, W.J. Kim, and D.J. Mooney Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells Bone 35 2004 562 569
43. B. Hinz Formation and function of the myofibroblast during tissue repair J Invest Dermatol 127 2007 526 537
44. B. Hinz, S.H. Phan, V.J. Thannickal, A. Galli, M.L. Bochaton-Piallat, and G. Gabbiani The myofibroblast: one function, multiple origins Am J Pathol 170 2007 1807 1816
45. W.H. Chen, M.T. Lai, A.T. 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
46. F. Barry, R.E. Boynton, B. Liu, and J.M. Murphy Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components Exp Cell Res 268 2001 189 200
47. A.T. Mehlhorn, H. Schmal, S. Kaiser, G. Lepski, G. Finkenzeller, and G.B. Stark et al. Mesenchymal stem cells maintain TGF-beta-mediated chondrogenic phenotype in alginate bead culture Tissue Eng 12 2006 1393 1403
48. M.B. Mueller, M. Fischer, J. Zellner, A. Berner, T. Dienstknecht, and L. Prantl et al. Hypertrophy in mesenchymal stem cell chondrogenesis: effect of TGF-beta isoforms and chondrogenic conditioning Cells Tissues Organs 192 2010 158 166
49. R. Nakaoka, S.X. Hsiong, and D.J. Mooney Regulation of chondrocyte differentiation level via co-culture with osteoblasts Tissue Eng 12 2006 2425 2433
50. B.R. Weil, T.A. Markel, J.L. Herrmann, A.M. Abarbanell, and D.R. Meldrum Mesenchymal stem cells enhance the viability and proliferation of human fetal intestinal epithelial cells following hypoxic injury via paracrine mechanisms Surgery 146 2009 190 197
51. L. Wu, J.C. Leijten, N. Georgi, J.N. Post, C.A. van Blitterswijk, and M. Karperien Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation Tissue Eng Part A 17 2011 1425 1436
52. 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
53. C.N. Salinas, B.B. Cole, A.M. Kasko, and K.S. Anseth Chondrogenic differentiation potential of human mesenchymal stem cells photoencapsulated within poly(ethylene glycol)-arginine-glycine-aspartic acid-serine thiol-methacrylate mixed-mode networks Tissue Eng 13 2007 1025 1034
54. L.E. Freed, A.P. Hollander, I. Martin, J.R. Barry, R. Langer, and G. Vunjak-Novakovic Chondrogenesis in a cell-polymer-bioreactor system Exp Cell Res 240 1998 58 65
55. A.K. Williamson, A.C. Chen, and R.L. Sah Compressive properties and function-composition relationships of developing bovine articular cartilage J Orthop Res 19 2001 1113 1121
56. A. Asanbaeva, K. Masuda, E.J. Thonar, S.M. Klisch, and R.L. Sah Mechanisms of cartilage growth: modulation of balance between proteoglycan and collagen in vitro using chondroitinase ABC Arthritis Rheum 56 2007 188 198
57. 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
58. Q.P. Pham, F.K. Kasper, L. Scott Baggett, R.M. Raphael, J.A. Jansen, and A.G. Mikos The influence of an in vitro generated bone-like extracellular matrix on osteoblastic gene expression of marrow stromal cells Biomaterials 29 2008 2729 2739
59. J.S. Temenoff, H. Park, E. Jabbari, T.L. Sheffield, R.G. LeBaron, and C.G. Ambrose et al. In vitro osteogenic differentiation of marrow stromal cells encapsulated in biodegradable hydrogels J Biomed Mater Res A 70 2004 235 244
60. J.B. Lian, and G.S. Stein Concepts of osteoblast growth and differentiation: basis for modulation of bone cell development and tissue formation Crit Rev Oral Biol Med 3 1992 269 305
61. H. Castano-Izquierdo, J. Alvarez-Barreto, J. van den Dolder, J.A. Jansen, A.G. Mikos, and V.I. Sikavitsas Pre-culture period of mesenchymal stem cells in osteogenic media influences their in vivo bone forming potential J Biomed Mater Res A 82 2007 129 138