Collagen type XII and versican are present in the early stages of cartilage tissue formation by both redifferentating passaged and primary chondrocytes

Tissue Engineering - Part A

Volumn 21, Issue 3-4, 2015, Pages 683-693

  Taylor, Drew W ^a,b,c   Ahmed, Nazish ^a,b   Parreno, Justin ^b   Lunstrum, Gregory P ^d   Gross, Allan E ^b,c   Diamandis, Eleftherios P ^b   Kandel, Rita A ^a,b,c  

^a CANADIAN INSTITUTES OF HEALTH RESEARCH   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; COLLAGEN; CYTOLOGY; GLYCOPROTEINS; MAMMALS; MASS SPECTROMETRY; MATRIX ALGEBRA; MOLECULES; TISSUE; TISSUE ENGINEERING;

BOVINE CHONDROCYTES; CARTILAGE TISSUE ENGINEERING; COLLAGEN SYNTHESIS; CULTURE CONDITIONS; DIFFERENTIAL EFFECT; EXTRACELLULAR MATRICES; PERICELLULAR MATRIX; PRIMARY CHONDROCYTES;

CARTILAGE;

AGGRECAN; CARTILAGE OLIGOMERIC MATRIX PROTEIN; COLLAGEN TYPE 1; COLLAGEN TYPE 12; COLLAGEN TYPE 2; COLLAGEN TYPE 3; DECORIN; PROTEOGLYCAN; TRANSCRIPTION FACTOR SOX9; VERSICAN; SCLEROPROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BOVINAE; CARTILAGE CELL; CELL CULTURE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CULTURE TECHNIQUE; EXTRACELLULAR MATRIX; GENE EXPRESSION; HYALINE CARTILAGE; IN VITRO STUDY; INFANT; MACROMOLECULE; METACARPOPHALANGEAL JOINT; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; TISSUE DIFFERENTIATION; TISSUE ENGINEERING; ANIMAL; BATCH CELL CULTURE; BOVINE; CARTILAGE; CELL DIFFERENTIATION; CHONDROGENESIS; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROCEDURES;

BOVINAE;

ANIMALS; BATCH CELL CULTURE TECHNIQUES; CARTILAGE; CATTLE; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE XII; EXTRACELLULAR MATRIX PROTEINS; TISSUE ENGINEERING; VERSICANS;

EID: 84923289820     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0103     Document Type: Article

References (47)

1. Chen, C., Tambe, D.T., Deng, L., and Yang, L. Biomechanical properties and mechanobiology of the articular chondrocyte. Am J Physiol Cell Physiol 305, C1202, 2013.
2. McGann, M.E., Bonitsky, C.M., Ovaert, T.C., and Wagner, D.R. The effect of collagen crosslinking on the biphasic poroviscoelastic cartilage properties determined from a semi-Automated microindentation protocol for stress relaxation. J Mech Behav Biomed Mater 34, 264, 2014.
3. Halper, J. Proteoglycans and diseases of soft tissues. Adv Exp Med Biol 802, 49, 2014.
4. Nikitovic, D., Aggelidakis, J., Young, M.F., Iozzo, R.V., Karamanos, N.K., and Tzanakakis, G.N. The biology of small leucine-rich proteoglycans in bone pathophysiology. J Biol Chem 287, 33926, 2012.
5. Budde, B., Blumbach, K., Ylostalo, J., Zaucke, F., Ehlen, H.W., Wagener, R., et al. Altered integration of matrilin-3 into cartilage extracellular matrix in the absence of collagen IX. Mol Cell Biol 25, 10465, 2005.
6. Wagener, R., Ehlen, H.W., Ko, Y.P., Kobbe, B., Mann, H.H., Sengle, G., et al. The matrilins-Adaptor proteins in the extracellular matrix. FEBS Lett 579, 3323, 2005.
7. Halasz, K., Kassner, A., Morgelin, M., and Heinegard, D. COMP acts as a catalyst in collagen fibrillogenesis. J Biol Chem 282, 31166, 2007.
8. Matsuura, K., Utoh, R., Nagase, K., and Okano, T. Cell sheet approach for tissue engineering and regenerative medicine. J Control Release 190, 228, 2014.
9. Musumeci, G., Castrogiovanni, P., Leonardi, R., Trovato, F.M., Szychlinska, M.A., Di Giunta, A., et al. New perspectives for articular cartilage repair treatment through tissue engineering: a contemporary review.World J Orthop 5, 80, 2014.
10. Bhumiratana, S., Eton, R.E., Oungoulian, S.R., Wan, L.Q., Ateshian, G.A., Vunjak-And Novakovic, G. Large, stratified, and mechanically functional human cartilage grown in vitro by mesenchymal condensation. Proc Natl Acad Sci U S A 111, 6940, 2014.
11. Mollon, B., Kandel, R., Chahal, J., and Theodoropoulos, J. The clinical status of cartilage tissue regeneration in humans. Osteoarthritis Cartilage 21, 1824, 2013.
12. Hui, J.H., Goyal, D., Nakamura, N., Ochi, M., and Asian Cartilage Society. Cartilage repair: 2013 Asian update. Arthroscopy 29, 1992, 2013.
13. Johnstone, B., Alini, M., Cucchiarini, M., Dodge, G.R., Eglin, D., Guilak, F., et al. Tissue engineering for articular cartilage repair-The state of the art. Eur Cell Mater 25, 248, 2013.
14. Tuan, R.S., Chen, A.F., and Klatt, B.A. Cartilage regeneration. J Am Acad Orthop Surg 21, 303, 2013.
15. Gopal, K., Amirhamed, H.A., and Kamarul, T. Advances of human bone marrow-derived mesenchymal stem cells in the treatment of cartilage defects: a systematic review. Exp Biol Med (Maywood) 239, 663, 2014.
16. Darling, E.M., and Athanasiou, K.A. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 23, 425, 2005.
17. Goldberg, A.J., Lee, D.A., Bader, D.L., and Bentley, G. Autologous chondrocyte implantation. Culture in a TGFbeta-containing medium enhances the re-expression of a chondrocytic phenotype in passaged human chondrocytes in pellet culture. J Bone Joint Surg Br 87, 128, 2005.
18. Lim, E.H., Sardinha, J.P., Myers, S., and Stevens, M. Latent transforming growth factor-beta1 functionalised electrospun scaffolds promote human cartilage differentiation: towards an engineered cartilage construct. Arch Plastic Surg 40, 676, 2013.
19. Munirah, S., Samsudin, O.C., Aminuddin, B.S., and Ruszymah, B.H. Expansion of human articular chondrocytes and formation of tissue-engineered cartilage: a step towards exploring a potential use of matrix-induced cell therapy. Tissue Cell 42, 282, 2010.
20. Hsieh-Bonassera, N.D., Wu, I., Lin, J.K., Schumacher, B.L., Chen, A.C., Masuda, K., et al. Expansion and redifferentiation of chondrocytes from osteoarthritic cartilage: cells for human cartilage tissue engineering. Tissue Eng Part A 15, 3513, 2009.
21. Liu, G., Kawaguchi, H., Ogasawara, T., Asawa, Y., Kishimoto, J., Takahashi, T., et al. Optimal combination of soluble factors for tissue engineering of permanent cartilage from cultured human chondrocytes. J Biol Chem282, 20407, 2007.
22. Jakob, M., Demarteau, O., Schafer, D., Hintermann, B., Dick, W., Heberer, M., et al. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 81, 368, 2001.
23. Ahmed, N., Iu, J., Brown, C.E., Taylor, D.W., and Kandel, R.A. Serum- And growth-factor-free three-dimensional culture system supports cartilage tissue formation by promoting collagen synthesis via Sox9-Col2a1 interaction. Tissue Eng Part A 20, 2224, 2014.
24. Taylor, D.W., Ahmed, N., Gan, L., Gross, A.E., and Kandel, R.A. Proteoglycan and collagen accumulation by passaged chondrocytes can be enhanced through side-byside culture with primary chondrocytes. Tissue Eng Part A 16, 643, 2010.
25. Ahmed, N., Taylor, D.W., Wunder, J., Nagy, A., Gross, A.E., and Kandel, R.A. Passaged human chondrocytes accumulate extracellular matrix when induced by bovine chondrocytes. J Tissue Eng Regen Med 4, 233, 2010.
26. Brittberg, M. Autologous chondrocyte transplantation. Clin Orthop Relat Res S147-S155, 1999.
27. Ahmed, N., Gan, L., Nagy, A., Zheng, J., Wang, C., and Kandel, R.A. Cartilage tissue formation using redifferentiated passaged chondrocytes in vitro. Tissue Eng Part A 15, 665, 2009.
28. Shinomura, T., Jensen, K.L., Yamagata, M., Kimata, K., and Solursh, M. The distribution of mesenchyme proteoglycan (PG-M) during wing bud outgrowth. Anat Embryol (Berl) 181, 227, 1990.
29. Kimata, K., Oike, Y., Tani, K., Shinomura, T., Yamagata, M., Uritani, M., et al. A large chondroitin sulfate proteoglycan (PG-M) synthesized before chondrogenesis in the limb bud of chick embryo. J Biol Chem 261, 13517, 1986.
30. Shepard, J.B., Gliga, D.A., Morrow, A.P., Hoffman, S., and Capehart, A.A. Versican knock-down compromises chondrogenesis in the embryonic chick limb. Anat Rec (Hoboken) 291, 19, 2008.
31. Hudson, D.M., Weis, M., and Eyre, D.R. Insights on the evolution of prolyl 3-hydroxylation sites from comparative analysis of chicken and Xenopus fibrillar collagens. PLoS One 6, e19336, 2010.
32. Matsumoto, K., Kamiya, N., Suwan, K., Atsumi, F., Shimizu, K., Shinomura, T., et al. Identification and characterization of versican/PG-M aggregates in cartilage. J Biol Chem 281, 18257, 2006.
33. Gregory, K.E., Keene, D.R., Tufa, S.F., Lunstrum, G.P., and Morris, N.P. Developmental distribution of collagen type XII in cartilage: association with articular cartilage and the growth plate. J Bone Miner Res 16, 2005, 2001.
34. Watt, S.L., Lunstrum, G.P., McDonough, A.M., Keene, D.R., Burgeson, R.E., and Morris, N.P. Characterization of collagen types XII and XIV from fetal bovine cartilage. J Biol Chem 267, 20093, 1992.
35. Hudson, K.S., Andrews, K., Early, J., Mjaatvedt, C.H., and Capehart, A.A. Versican G1 domain and V3 isoform overexpression results in increased chondrogenesis in the developing chick limb in ovo. Anat Rec (Hoboken) 293, 1669, 2010.
36. Choocheep, K., Hatano, S., Takagi, H., Watanabe, H., Kimata, K., and Kongtawelert, P. Versican facilitates chondrocyte differentiation and regulates joint morphogenesis. J Biol Chem 285, 21114, 2010.
37. Gerecke, D.R., Foley, J.W., Castagnola, P., Gennari, M., Dublet, B., Cancedda, R., et al. Type XIV collagen is encoded by alternative transcripts with distinct 5¢ regions and is a multidomain protein with homologies to von Willebrand's factor, fibronectin, and other matrix proteins. J Biol Chem 268, 12177, 1993.
38. Shaw, L.M., and Olsen, B.R. FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16, 191, 1991.
39. Mazzorana, M., Cogne, S., Goldschmidt, D., Aubert-Foucher E. Collagenous sequence governs the trimeric assembly of collagen XII. J Biol Chem 276, 27989, 2001.
40. Wei, Y., Yang, E.V., Klatt, K.P., and Tassava, R.A. Monoclonal antibody MT2 identifies the urodele alpha 1 chain of type XII collagen, a developmentally regulated extracellular matrix protein in regenerating newt limbs. Dev Biol 168, 503, 1995.
41. Agarwal, P., Zwolanek, D., Keene, D.R., Schulz, J.N., Blumbach, K., Heinegard, D., et al. Collagen XII and XIV, new partners of cartilage oligomeric matrix protein in the skin extracellular matrix suprastructure. J Biol Chem 287, 22549, 2012.
42. Hemmavanh, C., Koch, M., Birk, D.E., and Espana, E.M. Abnormal corneal endothelial maturation in collagen XII and XIV null mice. Invest Ophthalmol Vis Sci 54, 3297, 2013.
43. Polacek, M., Bruun, J.A., Elvenes, J., Figenschau, Y., and Martinez, I. The secretory profiles of cultured human articular chondrocytes and mesenchymal stem cells: implications for autologous cell transplantation strategies. Cell Transplant 20, 1381, 2011.
44. Lee, W.D., Hurtig, M.B., Kandel, R.A., and Stanford, W.L. Membrane culture of bone marrow stromal cells yields better tissue than pellet culture for engineering cartilage-bone substitute biphasic constructs in a two-step process. Tissue Eng Part C Methods 17, 939, 2011.
45. Lee, J., Abdeen, A.A., Zhang, D., and Kilian, K.A. Directing stem cell fate on hydrogel substrates by controlling cell geometry, matrix mechanics and adhesion ligand composition. Biomaterials 34, 8140, 2013.
46. Zhu, J., Cai, Q., Zhang, X., Hu, X., Li, L., Wang, W., et al. Biological characteristics of mesenchymal stem cells grown on different topographical nanofibrous poly-Llactide meshes. J Biomed Nanotechnol 9, 1757, 2013.
47. Takahashi, T., Ogasawara, T., Asawa, Y., Mori, Y., Uchinuma, E., Takato, T., et al. Three-dimensional microenvironments retain chondrocyte phenotypes during proliferation culture. Tissue Eng 13, 1583, 2007.