Engineering cartilage or endochondral bone: A comparison of different naturally derived hydrogels

Acta Biomaterialia

Volumn 13, Issue , 2015, Pages 245-253

  Sheehy, Eamon J ^a   Mesallati, Tariq ^a   Vinardell, Tatiana ^b   Kelly, Daniel J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Alginate; Chitosan; Endochondral ossification; Fibrin; Mesenchymal stem cell

Indexed keywords

ALGINATE; BONE; CARTILAGE; CELL ENGINEERING; CHITOSAN; FLOWCHARTING; HISTOLOGY; HYDROGELS; STEM CELLS; TISSUE REGENERATION;

ARTICULAR CARTILAGES; BONE FORMATION; CARTILAGINOUS TISSUES; ENDOCHONDRAL OSSIFICATION; FIBRIN; IN-VITRO; IN-VIVO; MESENCHYMAL STEM CELL; SULFATED GLYCOSAMINOGLYCANS; VASCULARIZATION;

CELL CULTURE;

ALGINIC ACID; CALCIUM; CHITOSAN; COLLAGEN; FIBRIN; GLYCOSAMINOGLYCAN POLYSULFATE; HYDROGEL;

ANIMAL EXPERIMENT; ARTICLE; ARTICULAR CARTILAGE; BONE MARROW; CHONDROGENESIS; ENCHONDRAL OSSIFICATION; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; INTERMETHOD COMPARISON; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TISSUE ENGINEERING; VASCULARIZATION; ANIMAL; BAGG ALBINO MOUSE; BONE DEVELOPMENT; CHEMISTRY; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; NUDE MOUSE; PIG; PROCEDURES;

ANIMALS; CARTILAGE, ARTICULAR; CHONDROGENESIS; HYDROGELS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, NUDE; OSTEOGENESIS; SWINE; TISSUE ENGINEERING;

EID: 84920715952     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.11.031     Document Type: Article

References (54)

1. C.J. Koh, and A. Atala Tissue engineering, stem cells, and cloning: opportunities for regenerative medicine J Am Soc Nephrol 15 2004 1113 1125
2. R. Langer Tissue engineering Mol Ther 1 2000 12 15
3. G.J. Meijer, J.D. De Bruijn, R. Koole, and C.A. Van Blitterswijk Cell-based bone tissue engineering PLoS Med 4 2007 0260 264
4. M.I. Santos, and R.L. Reis Vascularization in bone tissue engineering: physiology, current strategies, major hurdles and future challenges Macromol Biosci 10 2010 12 27
5. F.G. Lyons, A.A. Al-Munajjed, S.M. Kieran, M.E. Toner, C.M. Murphy, and G.P. Duffy The healing of bony defects by cell-free collagen-based scaffolds compared to stem cell-seeded tissue engineered constructs Biomaterials 31 2010 9232 9243
6. P. Lenas, M. Moos, and F.P. Luyten Developmental engineering: a new paradigm for the design and manufacturing of cell-based products. Part I: from three-dimensional cell growth to biomimetics of in vivo development Tissue Eng - Part B: Rev 15 2009 381 394
7. H.M. Kronenberg Developmental regulation of the growth plate Nature 423 2003 332 336
8. E. Farrell In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells BMC Musculoskelet Disord 12 2011 31
9. E. Farrell Chondrogenic priming of human bone marrow stromal cells: a better route to bone repair? Tissue Eng Part C Methods 15 2009 285 295
10. J.I. Huang, M.M. Durbhakula, P. Angele, B. Johnstone, and J.U. Yoo Lunate arthroplasty with autologous mesenchymal stem cells in a rabbit model J Bone Joint Surg 88 2006 744 752
11. C. Scotti Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering Proc Natl Acad Sci USA 107 2010 7251 7256
12. P. Janicki, P. Kasten, K. Kleinschmidt, R. Luginbuehl, and W. Richter Chondrogenic pre-induction of human mesenchymal stem cells on β-TCP: enhanced bone quality by endochondral heterotopic bone formation Acta Biomater 6 2010 3292 3301
13. C. Scotti Engineering of a functional bone organ through endochondral ossification Proc Natl Acad Sci USA 110 2013 3997 4002
14. N. Harada Bone regeneration in a massive rat femur defect through endochondral ossification achieved with chondrogenically differentiated MSCs in a degradable scaffold Biomaterials 35 2014 7800 7810
15. J. van der Stok, M.K. Koolen, H. Jahr, N. Kops, J.H. Waarsing, and H. Weinans Chondrogenically differentiated mesenchymal stromal cell pellets stimulate endochondral bone regeneration in critical-sized bone defects Eur Cell Mater 27 2014 137 148 [discussion 48]
16. S.L. Riley, S. Dutt, R. De La Torre, A.C. Chen, R.L. Sah, and A. Ratcliffe Formulation of PEG-based hydrogels affects tissue-engineered cartilage construct characteristics J Mater Sci Mater Med 12 2001 983 990
17. J.L. Drury, and D.J. Mooney Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 24 2003 4337 4351
18. I.E. Erickson, A.H. Huang, C. Chung, R.T. Li, J.A. Burdick, and R.L. Mauck Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels Tissue Eng Part A 15 2009 1041 1052
19. R.L. Mauck, X. Yuan, and R.S. Tuan Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture Osteoarthritis Cartilage 14 2006 179 189
20. E.J. Sheehy, C.T. Buckley, and D.J. Kelly Chondrocytes and bone marrow-derived mesenchymal stem cells undergoing chondrogenesis in agarose hydrogels of solid and channelled architectures respond differentially to dynamic culture conditions J Tissue Eng Regen Med 5 2011 747 758
21. K. Ma, A.L. Titan, M. Stafford, C. Zheng, and M.E. Levenston Variations in chondrogenesis of human bone marrow-derived mesenchymal stem cells in fibrin/alginate blended hydrogels Acta Biomater 8 2012 3754 3764
22. I.E. Erickson, S.R. Kestle, K.H. Zellars, M.J. Farrell, M. Kim, and J.A. Burdick High mesenchymal stem cell seeding densities in hyaluronic acid hydrogels produce engineered cartilage with native tissue properties Acta Biomater 8 2012 3027 3034
23. H.A. Awad, M.Q. Wickham, H.A. Leddy, J.M. Gimble, and F. Guilak Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds Biomaterials 25 2004 3211 3222
24. D. Bosnakovski, M. Mizuno, G. Kim, S. Takagi, M. Okumura, and T. Fujinaga 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 2006 1152 1163
25. R.M. Coleman, N.D. Case, and R.E. Guldberg Hydrogel effects on bone marrow stromal cell response to chondrogenic growth factors Biomaterials 28 2007 2077 2086
26. I.L. Kim, R.L. Mauck, and J.A. Burdick Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid Biomaterials 32 2011 8771 8782
27. A. Dickhut, E. Gottwald, E. Steck, C. Heisel, and W. Richter Chondrogenesis of mesenchymal stem cells in gel-like biomaterials in vitro and in vivo Front Biosci 13 2008 4517 4528
28. Melle M.L. de Vries-van Chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in a simulated osteochondral environment is hydrogel dependent Eur Cell Mater 27 2014 112 123 discussion 23
29. M.M. Pleumeekers, L. Nimeskern, W.L. Koevoet, N. Kops, R.M. Poublon, and K.S. Stok The in vitro and in vivo capacity of culture-expanded human cells from several sources encapsulated in alginate to form cartilage Eur Cell Mater 27 2014 264 280 discussion 78-80
30. E.J. Sheehy, C.T. Buckley, and D.J. Kelly Oxygen tension regulates the osteogenic, chondrogenic and endochondral phenotype of bone marrow derived mesenchymal stem cells Biochem Biophys Res Commun 417 2012 305 310
31. V. Vacanti, E. Kong, G. Suzuki, K. Sato, J.M. Canty, and T. Lee Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture J Cell Physiol 205 2005 194 201
32. T. Vinardell, S.D. Thorpe, C.T. Buckley, and D.J. Kelly Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model Ann Biomed Eng 37 2009 2556 2565
33. S.D. Thorpe, C.T. Buckley, A.J. Steward, and D.J. Kelly European Society of Biomechanics S.M. Perren Award 2012: The external mechanical environment can override the influence of local substrate in determining stem cell fate J Biomech 45 15 2012 2483 2492
34. T. Vinardell, E.J. Sheehy, C.T. Buckley, and D.J. Kelly A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cells sources Tissue Eng Part A 18 2012 1161 1170
35. E.J. Sheehy, T. Vinardell, C.T. Buckley, and D.J. Kelly Engineering osteochondral constructs through spatial regulation of endochondral ossification Acta Biomater 9 2013 5484 5492
36. D.A. Cheresh, S.A. Berliner, V. Vicente, and Z.M. Ruggeri Recognition of distinct adhesive sites on fibrinogen by related integrins on platelets and endothelial cells Cell 58 1989 945 953
37. R. McBeath, D.M. Pirone, C.M. Nelson, K. Bhadriraju, and C.S. Chen Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment Dev Cell 6 2004 483 495
38. D.P. Lennon, J.M. Edmison, and A.I. Caplan Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis J Cell Physiol 187 2001 345 355
39. 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
40. Y. Yang, I. Wimpenny, and M. Ahearne Portable nanofiber meshes dictate cell orientation throughout three-dimensional hydrogels Nanomed: Nanotechnol, Biol, Med 7 2011 131 136
41. C.D. Hoemann, J. Sun, A. Legare, M.D. McKee, and M.D. Buschmann Tissue engineering of cartilage using an injectable and adhesive chitosan-based cell-delivery vehicle Osteoarthritis Cartilage 13 2005 318 329
42. P. Roughley, C. Hoemann, E. DesRosiers, F. Mwale, J. Antoniou, and M. Alini The potential of chitosan-based gels containing intervertebral disc cells for nucleus pulposus supplementation Biomaterials 27 2006 388 396
43. S.M. Richardson, N. Hughes, J.A. Hunt, A.J. Freemont, and J.A. Hoyland Human mesenchymal stem cell differentiation to NP-like cells in chitosan-glycerophosphate hydrogels Biomaterials 29 2008 85 93
44. H. Park, B. Choi, J. Hu, and M. Lee Injectable chitosan hyaluronic acid hydrogels for cartilage tissue engineering Acta Biomater 9 2013 4779 4786
45. T. Hao The support of matrix accumulation and the promotion of sheep articular cartilage defects repair in vivo by chitosan hydrogels Osteoarthritis Cartilage 18 2010 257 265
46. J.K. Suh, and H.W. Matthew Application of chitosan-based polysaccharide biomaterials in cartilage tissue engineering: a review Biomaterials 21 2000 2589 2598
47. Y. Wen, L. Grøndahl, M.R. Gallego, L. Jorgensen, E.H. Møller, and H.M. Nielsen Delivery of dermatan sulfate from polyelectrolyte complex-containing alginate composite microspheres for tissue regeneration Biomacromolecules 13 2012 905 917
48. D. Gawlitta, M.H.P. Van Rijen, E.J.M. Schrijver, J. Alblas, and W.J.A. Dhert Hypoxia impedes hypertrophic chondrogenesis of human multipotent stromal cells Tissue Eng Part A 18 2012 1957 1966
49. 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
50. E. Alsberg, H.J. Kong, Y. Hirano, M.K. Smith, A. Albeiruti, and D.J. Mooney Regulating bone formation via controlled scaffold degradation J Dent Res 82 2003 903 908
51. O. Jeon, K.H. Bouhadir, J.M. Mansour, and E. Alsberg Photocrosslinked alginate hydrogels with tunable biodegradation rates and mechanical properties Biomaterials 30 2009 2724 2734
52. O. Jeon, C. Powell, L.D. Solorio, M.D. Krebs, and E. Alsberg Affinity-based growth factor delivery using biodegradable, photocrosslinked heparin-alginate hydrogels J Control Release 154 2011 258 266
53. M. Mumme Interleukin-1β modulates endochondral ossification by human adult bone marrow stromal cells Eur Cells Mater 24 2012 224 236
54. E.J. Sheehy, T. Vinardell, M.E. Toner, C.T. Buckley, and D.J. Kelly Altering the architecture of tissue engineered hypertrophic cartilaginous grafts facilitates vascularisation and accelerates mineralisation PLoS ONE 9 3 2014 e90716