Differential effect of hypoxia on human mesenchymal stem cell chondrogenesis and hypertrophy in hyaluronic acid hydrogels

Acta Biomaterialia

Volumn 10, Issue 3, 2014, Pages 1333-1340

  Zhu, Meiling ^a   Feng, Qian ^a   Bian, Liming ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cartilage tissue engineering; Chondrogenesis; Hyaluronic acid; Hydrogel; Mesenchymal stem cells

Indexed keywords

BIOMINERALIZATION; BONE; CARTILAGE; CELL ENGINEERING; CROSSLINKING; HYALURONIC ACID; HYDROGELS; ORGANIC ACIDS; PATHOLOGY; STEM CELLS; TISSUE ENGINEERING;

ACID CONCENTRATIONS; CARTILAGE TISSUE ENGINEERING; CHONDROGENESIS; CROSS-LINKING DENSITY; DIFFERENTIAL EFFECT; HUMAN MESENCHYMAL STEM CELLS; HYALURONIC ACID HYDROGELS; HYDROGEL CROSSLINKING; MACROMERS; MESENCHYMAL STEM CELL;

CELL CULTURE;

HYALURONIC ACID; BIOLOGICAL MARKER; COLLAGEN; GLYCOSAMINOGLYCAN; HYDROGEL;

ARTICLE; CALCIFICATION; CARTILAGE CELL; CELL REGENERATION; CELL VIABILITY; CHONDROGENESIS; CONTROLLED STUDY; CROSS LINKING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROGEL; HYPERTROPHY; HYPOXIA; LIGHT EXPOSURE; MESENCHYMAL STEM CELL; PRIORITY JOURNAL; SYNTHESIS; TISSUE ENGINEERING; BONE MINERALIZATION; CELL HYPOXIA; CELL SURVIVAL; DRUG EFFECTS; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; IMMOBILIZED CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHARMACOLOGY;

BIOLOGICAL MARKERS; CALCIFICATION, PHYSIOLOGIC; CELL HYPOXIA; CELL SURVIVAL; CELLS, IMMOBILIZED; CHONDROGENESIS; COLLAGEN; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HUMANS; HYALURONIC ACID; HYDROGELS; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STROMAL CELLS;

EID: 84895068968     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.12.015     Document Type: Article

References (38)

1. 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
2. K. Pelttari, A. Winter, E. Steck, K. Goetzke, T. Hennig, and B.G. Ochs et al. 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 2006 3254 3266
3. C. Chung, M. Beecham, R.L. Mauck, and J.A. Burdick The influence of degradation characteristics of hyaluronic acid hydrogels on in vitro neocartilage formation by mesenchymal stem cells Biomaterials 30 2009 4287 4296
4. L. Bian, M. Guvendiren, R.L. Mauck, and J.A. Burdick Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis Proc Natl Acad Sci USA 110 2013 10117 10122
5. L. Bian, D.Y. Zhai, E. Tous, R. Rai, R.L. Mauck, and J.A. Burdick Enhanced MSC chondrogenesis following delivery of TGF-beta3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo Biomaterials 32 2011 6425 6434
6. A.L. Boskey The role of extracellular matrix components in dentin mineralization Crit Rev Oral Biol Med 2 1991 369 387
7. H.C. Anderson Molecular biology of matrix vesicles Clin Orthop Relat Res 1995 266 280
8. B. Jubeck, C. Gohr, M. Fahey, E. Muth, M. Matthews, and E. Mattson et al. Promotion of articular cartilage matrix vesicle mineralization by type I collagen Arthritis Rheum 58 2008 2809 2817
9. N. Ortega, D.J. Behonick, and Z. Werb Matrix remodeling during endochondral ossification Trends Cell Biol 14 2004 86 93
10. C. Chung, J. Mesa, M.A. Randolph, M. Yaremchuk, and J.A. Burdick Influence of gel properties on neocartilage formation by auricular chondrocytes photoencapsulated in hyaluronic acid networks J Biomed Mater Res A 77 2006 518 525
11. I.E. Erickson, A.H. Huang, S. Sengupta, S. Kestle, J.A. Burdick, and R.L. Mauck Macromer density influences mesenchymal stem cell chondrogenesis and maturation in photocrosslinked hyaluronic acid hydrogels Osteoarthritis Cartilage 17 2009 1639 1648
12. L. Bian, C. Hou, E. Tous, R. Rai, R.L. Mauck, and J.A. Burdick The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy Biomaterials 34 2012 413 421
13. E. Duval, C. Bauge, R. Andriamanalijaona, H. Benateau, S. Leclercq, and S. Dutoit et al. Molecular mechanism of hypoxia-induced chondrogenesis and its application in in vivo cartilage tissue engineering Biomaterials 33 2012 6042 6051
14. K. Schrobback, T.J. Klein, R. Crawford, Z. Upton, J. Malda, and D.I. Leavesley Effects of oxygen and culture system on in vitro propagation and redifferentiation of osteoarthritic human articular chondrocytes Cell Tissue Res 347 2011 649 663
15. D. Gawlitta, M.H. van Rijen, E.J. Schrijver, J. Alblas, and W.J. Dhert Hypoxia impedes hypertrophic chondrogenesis of human multipotent stromal cells Tissue Eng Part A 18 2012 1957 1966
16. R. Amarilio, S.V. Viukov, A. Sharir, I. Eshkar-Oren, R.S. Johnson, and E. Zelzer HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis Development 134 2007 3917 3928
17. S. Provot, D. Zinyk, Y. Gunes, R. Kathri, Q. Le, and H.M. Kronenberg et al. Hif-1alpha regulates differentiation of limb bud mesenchyme and joint development J Cell Biol 177 2007 451 464
18. M. Hirao, N. Tamai, N. Tsumaki, H. Yoshikawa, and A. Myoui Oxygen tension regulates chondrocyte differentiation and function during endochondral ossification J Biol Chem 281 2006 31079 31092
19. J.C. Leijten, L.S. Moreira Teixeira, E.B. Landman, C.A. van Blitterswijk, and M. Karperien Hypoxia inhibits hypertrophic differentiation and endochondral ossification in explanted tibiae PLoS One 7 2012 e49896
20. 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 17 2011 1137 1145
21. L. Bian, D.Y. Zhai, E.C. Zhang, R.L. Mauck, and J.A. Burdick Dynamic compressive loading enhances cartilage matrix synthesis and distribution and suppresses hypertrophy in hMSC-laden hyaluronic acid hydrogels Tissue Eng Part A 18 2012 715 724
22. M.B. Mueller, and R.S. Tuan Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells Arthritis Rheum 58 2008 1377 1388
23. K.A. Smeds, A. Pfister-Serres, D. Miki, K. Dastgheib, M. Inoue, and D.L. Hatchell et al. Photocrosslinkable polysaccharides for in situ hydrogel formation J Biomed Mater Res 54 2001 115 121
24. B.A. Byers, R.L. Mauck, I.E. Chiang, and R.S. Tuan Transient exposure to transforming growth factor beta 3 under serum-free conditions enhances the biomechanical and biochemical maturation of tissue-engineered cartilage Tissue Eng Part A 14 2008 1821 1834
25. K.B. McGowan, M.S. Kurtis, L.M. Lottman, D. Watson, and R.L. Sah Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258 Osteoarthritis Cartilage 10 2002 580 587
26. 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
27. A.P. Hollander, T.F. Heathfield, C. Webber, Y. Iwata, R. Bourne, and C. Rorabeck et al. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay J Clin Invest 93 1994 1722 1732
28. C. Scotti, B. Tonnarelli, A. Papadimitropoulos, A. Scherberich, S. Schaeren, and A. Schauerte et al. 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
29. 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
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. N.V. Ghone, and W.L. Grayson Recapitulation of mesenchymal condensation enhances in vitro chondrogenesis of human mesenchymal stem cells J Cell Physiol 227 2012 3701 3708
32. B.A. Derfus, S.M. Kurtin, N.P. Camacho, I. Kurup, and L.M. Ryan Comparison of matrix vesicles derived from normal and osteoarthritic human articular cartilage Connect Tissue Res 35 1996 337 342
33. C.C. Chen, A.L. Boskey, and L.C. Rosenberg The inhibitory effect of cartilage proteoglycans on hydroxyapatite growth Calcif Tissue Int 36 1984 285 290
34. B. Jubeck, E. Muth, C.M. Gohr, and A.K. Rosenthal Type II collagen levels correlate with mineralization by articular cartilage vesicles Arthritis Rheum 60 2009 2741 2746
35. J.A. Hubbell Materials as morphogenetic guides in tissue engineering Curr Opin Biotechnol 14 2003 551 558
36. R.O. Hynes The extracellular matrix: not just pretty fibrils Science 326 2009 1216 1219
37. M.A. Mello, and R.S. Tuan Effects of TGF-beta1 and triiodothyronine on cartilage maturation: in vitro analysis using long-term high-density micromass cultures of chick embryonic limb mesenchymal cells J Orthop Res 24 2006 2095 2105
38. M. Hirsila, P. Koivunen, V. Gunzler, K.I. Kivirikko, and J. Myllyharju Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor J Biol Chem 278 2003 30772 30780