The effect of hypoxia on the chondrogenic differentiation of co-cultured articular chondrocytes and mesenchymal stem cells in scaffolds

Biomaterials

Volumn 34, Issue 17, 2013, Pages 4266-4273

  Meretoja, Ville V ^a   Dahlin, Rebecca L ^a   Wright, Sarah ^a   Kasper, F Kurtis ^a   Mikos, Antonios G ^a  

^a Rice University   (United States)

Author keywords

Cartilage tissue engineering; Chondrocyte; Co culture; Gene expression; Mesenchymal stem cell

Indexed keywords

ARTICULAR CHONDROCYTES; CARTILAGE ENGINEERING; CARTILAGE TISSUE ENGINEERING; CHONDROCYTES; CHONDROGENIC DIFFERENTIATION; CHONDROGENIC PHENOTYPES; COCULTURE; MESENCHYMAL STEM CELL;

BIOMINERALIZATION; BODY FLUIDS; CARTILAGE; CELL ENGINEERING; COLLAGEN; FLOWCHARTING; GENE EXPRESSION; HYDROXYPROLINE; OXYGEN; PATHOLOGY; SCAFFOLDS (BIOLOGY);

CELL CULTURE;

CALCIUM; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; HYDROXYPROLINE; TISSUE SCAFFOLD;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIFICATION; CARTILAGE CELL; CELL DIFFERENTIATION; CHONDROGENESIS; COCULTURE; CONTROLLED STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OXYGEN TENSION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; CALCIUM; CARTILAGE, ARTICULAR; CATTLE; CELL DIFFERENTIATION; CELL HYPOXIA; CHONDROCYTES; CHONDROGENESIS; COCULTURE TECHNIQUES; COLLAGEN; DNA; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HYDROXYPROLINE; MESENCHYMAL STROMAL CELLS; OXYGEN; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE SCAFFOLDS;

EID: 84875539112     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.02.064     Document Type: Article

References (54)

1. Felson D.T., Lawrence R.C., Dieppe P.A., Hirsch R., Helmick C.G., Jordan J.M., et al. Osteoarthritis: new insights-part 1: the disease and its risk factors. Ann Intern Med 2000, 133:635-646.
2. Cohen N.P., Foster R.J., Mow V.C. Composition and dynamics of articular cartilage: structure, function, and maintaining healthy state. J Orthop Sports Phys Ther 1998, 28:203-215.
3. Farr J., Cole B., Dhawan A., Kercher J., Sherman S. Clinical cartilage restoration evolution and overview. Clin Orthop 2011, 469:2696-2705.
4. Kock L., van Donkelaar C.C., Ito K. Tissue engineering of functional articular cartilage: the current status. Cell Tissue Res 2012, 347:613-627.
5. Brittberg M., Peterson L., Sjogren-Jansson E., Tallheden T., Lindahl A. Articular cartilage engineering with autologous chondrocyte transplantation-a review of recent developments. J Bone Joint Surg Am 2003, 85A:109-115.
6. Matricali G.A., Dereymaeker G.P.E., Luyten F.P. Donor site morbidity after articular cartilage repair procedures: a review. Acta Orthop Belg 2010, 76:669-674.
7. Dell'Accio F., De Bari C., Luyten F.P. Microenvironment and phenotypic stability specify tissue formation by human articular cartilage-derived cells in vivo. Exp Cell Res 2003, 287:16-27.
8. Freyria A.M., Mallein-Gerin F. Chondrocytes or adult stem cells for cartilage repair: the indisputable role of growth factors. Injury-Int J Care Inj 2012, 43:259-265.
9. Dickhut A., Pelttari K., Janicki P., Wagner W., Eckstein V., Egermann M., et al. Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage. J Cell Physiol 2009, 219:219-226.
10. Tang Q.O., Carasco C.F., Gamie Z., Korres N., Mantalaris A., Tsiridis E. Preclinical and clinical data for the use of mesenchymal stem cells in articular cartilage tissue engineering. Expert Opin Biol Ther 2012, 12:1361-1382.
11. Leijten J.C.H., Georgi N., Wu L., Van Blitterswijk C.A., Karperien M. Cell sources for articular cartilage repair strategies: shifting from monocultures to cocultures. Tissue Eng Part B: Rev 2013, 19:31-40.
12. Fermor B., Christensen S.E., Youn I., Cernanec J.M., Davies C.M., Weinberg B. Oxygen, nitric oxide and articular cartilage. Eur Cell Mater 2007, 13:56-65.
13. Araldi E., Schipani E. Hypoxia, hifs and bone development. Bone 2010, 47:190-196.
14. Schrobback K., Klein T.J., Crawford R., Upton Z., Malda J., Leavesley D.I. Effects of oxygen and culture system on in vitro propagation and redifferentiation of osteoarthritic human articular chondrocytes. Cell Tissue Res 2012, 347:649-663.
15. Markway B.D., Tan G.K., Brooke G., Hudson J.E., Cooper-White J.J., Doran M.R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant 2010, 19:29-42.
16. Coyle C.H., Izzo N.J., Chu C.R. Sustained hypoxia enhances chondrocyte matrix synthesis. J Orthop Res 2009, 27:793-799.
17. Robins J.C., Akeno N., Mukherjee A., Dalal R.R., Aronow B.J., Koopman P., et al. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of sox9. Bone 2005, 37:313-322.
18. Dahlin R.L., Meretoja V.V., Ni M., Kasper F.K., Mikos A.G. Hypoxia and flow perfusion modulate proliferation and gene expression of articular chondrocytes on porous scaffolds. AIChE J 2013, Available from URL. http://onlinelibrary.wiley.com/doi/10.1002/aic.13958/pdf, 10.1002/aic.13958.
19. Meretoja V.V., Dahlin R.L., Kasper F.K., Mikos A.G. Enhanced chondrogenesis in co-cultures with articular chondrocytes and mesenchymal stem cells. Biomaterials 2012, 33:6362-6369.
20. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative pcr and the 2̂(-delta delta ct) method. Methods 2001, 25:402-408.
21. Farndale R.W., Buttle D.J., Barrett A.J. Improved quantitation and discrimination of sulfated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986, 883:173-177.
22. Stegeman H., Stalder K. Determination of hydroxyproline. Clin Chim Acta 1967, 18:267-273.
23. Wei W., Yu X.D. Hypoxia-inducible factors: crosstalk between their protein stability and protein degradation. Cancer Lett 2007, 257:145-156.
24. Duval E., Bauge C., Andriamanalijaona R., Benateau H., Leclercq S., Dutoit S., et al. Molecular mechanism of hypoxia-induced chondrogenesis and its application in in vivo cartilage tissue engineering. Biomaterials 2012, 33:6042-6051.
25. Lafont J.E., Talma S., Hopfgarten C., Murphy C.L. Hypoxia promotes the differentiated human articular chondrocyte phenotype through sox9-dependent and -independent pathways. J Biol Chem 2008, 283:4778-4786.
26. Malda J., Martens D.E., Tramper J., van Blitterswijk C.A., Riesle J. Cartilage tissue engineering: controversy in the effect of oxygen. Crit Rev Biotechnol 2003, 23:175-194.
27. Egli R.J., Bastian J.D., Ganz R., Hofstetter W., Leunig M. Hypoxic expansion promotes the chondrogenic potential of articular chondrocytes. J Orthop Res 2008, 26:977-985.
28. Foldager C.B., Nielsen A.B., Munir S., Ulrich-Vinther M., Soballe K., Bunger C., et al. Combined 3d and hypoxic culture improves cartilage-specific gene expression in human chondrocytes. Acta Orthop 2011, 82:234-240.
29. Kellner K., Liebsch G., Klimant I., Wolfbeis O.S., Blunk T., Schulz M.B., et al. Determination of oxygen gradients in engineered tissue using a fluorescent sensor. Biotechnol Bioeng 2002, 80:73-83.
30. Ströbel S., Loparic M., Wendt D., Schenk A.D., Candrian C., Lindberg R.L.P., et al. Anabolic and catabolic responses of human articular chondrocytes to varying oxygen percentages. Arthritis Res Ther 2010, 12:R34.
31. Adesida A.B., Mulet-Sierra A., Jomha N.M. Hypoxia mediated isolation and expansion enhances the chondrogenic capacity of bone marrow mesenchymal stromal cells. Stem Cell Res Ther 2012, 3:9.
32. Sheehy E.J., Buckley C.T., Kelly D.J. Oxygen tension regulates the osteogenic, chondrogenic and-endochondral phenotype of bone marrow derived mesenchymal stem cells. Biochem Biophys Res Commun 2012, 417:305-310.
33. Müller J., Benz K., Ahlers M., Gaissmaier C., Mollenhauer J. Hypoxic conditions during expansion culture prime human mesenchymal stromal precursor cells for chondrogenic differentiation in three-dimensional cultures. Cell Transplant 2011, 20:1589-1602.
34. Caron M.M.J., Emans P.J., Coolsen M.M.E., Voss L., Surtel D.A.M., Cremers A., et al. Redifferentiation of dedifferentiated human articular chondrocytes: comparison of 2d and 3d cultures. Osteoarthr Cartilage 2012, 20:1170-1178.
35. Buckley C.T., Vinardell T., Kelly D.J. Oxygen tension differentially regulates the functional properties of cartilaginous tissues engineered from infrapatellar fat pad derived mscs and articular chondrocytes. Osteoarthr Cartilage 2010, 18:1345-1354.
36. Lewis M.C., MacArthur B.D., Malda J., Pettet G., Please C.P. Heterogeneous proliferation within engineered cartilaginous tissue: the role of oxygen tension. Biotechnol Bioeng 2005, 91:607-615.
37. Concaro S., Gustavson F., Gatenholm P. Bioreactors for tissue engineering of cartilage. Bioreactor systems for tissue engineering. Advances in biochemical engineering-biotechnology 2009, 125-143. C. Kasper (Ed.).
38. Le Blanc K., Ringden O. Immunomodulation by mesenchymal stem cells and clinical experience. J Intern Med 2007, 262:509-525.
39. Caplan A. Why are mscs therapeutic? new data: new insight. J Pathol 2009, 217:318-324.
40. Pelttari K., Steck E., Richter W. The use of mesenchymal stem cells for chondrogenesis. Injury-Int J Care Inj 2008, 39:S58-S65.
41. Vinardell T., Sheehy E.J., Buckley C.T., Kelly D.J. A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Eng Part A 2012, 18:1161-1170.
42. Scotti C., Tonnarelli B., Papadimitropoulos A., Scherberich A., Schaeren S., Schauerte A., et al. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 2010, 107:7251-7256.
43. Saito T., Fukai A., Mabuchi A., Ikeda T., Yano F., Ohba S., et al. Transcriptional regulation of endochondral ossification by hif-2 alpha during skeletal growth and osteoarthritis development. Nat Med 2010, 16:678-683.
44. Lin Q., Cong X.Y., Yun Z. Differential hypoxic regulation of hypoxia-inducible factors 1 alpha and 2 alpha. Mol Cancer Res 2011, 9:757-765.
45. Gawlitta D., van Rijen M.H.P., Schrijver E.J.M., Alblas J., Dhert W.J.A. Hypoxia impedes hypertrophic chondrogenesis of human multipotent stromal cells. Tissue Eng Part A 2012, 18:1957-1966.
46. Ghone N.V., Grayson W.L. Recapitulation of mesenchymal condensation enhances in vitro chondrogenesis of human mesenchymal stem cells. J Cell Physiol 2012, 227:3701-3708.
47. Ng K.W., O'Conor C.J., Kugler L.E., Cook J.L., Ateshian G.A., Hung C.T. Transient supplementation of anabolic growth factors rapidly stimulates matrix synthesis in engineered cartilage. Ann Biomed Eng 2011, 39:2491-2500.
48. Huang A.H., Stein A., Tuan R.S., Mauck R.L. Transient exposure to transforming growth factor beta 3 improves the mechanical properties of mesenchymal stem cell-laden cartilage constructs in a density-dependent manner. Tissue Eng Part A 2009, 15:3461-3472.
49. Aung A., Gupta G., Majid G., Varghese S. Osteoarthritic chondrocyte-secreted morphogens induce chondrogenic differentiation of human mesenchymal stem cells. Arthritis Rheum 2011, 63:148-158.
50. Bian L., Zhai D.Y., Mauck R.L., Burdick J.A. Coculture of human mesenchymal stem cells and articular chondrocytes reduces hypertrophy and enhances functional properties of engineered cartilage. Tissue Eng Part A 2011, 17:1137-1145.
51. Wu L., Prins H.J., Helder M.N., van Blitterswijk C.A., Karperien M. Trophic effects of mesenchymal stem cells in chondrocyte co-cultures are independent of culture conditions and cell sources. Tissue Eng Part A 2012, 18:1542-1551.
52. Fischer J., Dickhut A., Rickert M., Richter W. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum 2010, 62:2696-2706.
53. Wu L., Leijten J.C.H., Georgi N., Post J.N., van Blitterswijk C.A., Karperien M. Trophic effects of mesenchymal stem cells increase chondrocyte proliferation and matrix formation. Tissue Eng Part A 2011, 17:1425-1436.
54. Cooke M.E., Allon A.A., Cheng T., Kuo A.C., Kim H.T., Vail T.P., et al. Structured three-dimensional co-culture of mesenchymal stem cells with chondrocytes promotes chondrogenic differentiation without hypertrophy. Osteoarthr Cartilage 2011, 19:1210-1218.