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The effects of crosslinking of scaffolds engineered from cartilage ECM on the chondrogenic differentiation of MSCs
Open accessAbstract
Scaffolds fabricated from cartilage extracellular matrix provide a chondroinductive environment that stimulates cartilaginous matrix synthesis in a variety of cell types. A limitation of these cartilage-derived matrix (CDM) scaffolds is that they contract during in vitro culture, which unpredictably alters their shape. The current study examined the hypothesis that collagen crosslinking techniques could inhibit cell-mediated contraction of CDM scaffolds. We analyzed the effects of dehydrothermal (DHT) treatment, ultraviolet light irradiation (UV), and the chemical crosslinker carbodiimide (CAR) on scaffold contraction and chondrogenic differentiation of adult human bone marrow-derived stem cells (MSCs). Both physical and chemical crosslinking treatments retained the original scaffold dimensions. DHT and UV treatments produced significantly higher glycosaminoglycan and collagen contents than CAR crosslinked and non-crosslinked constructs. Crosslinking treatments influenced the composition of newly synthesized matrix, and DHT treatment best matched the composition of native cartilage. DHT, UV, and non-crosslinked CDM films supported cell attachment, while CAR crosslinking inhibited cell adhesion. These results affirm that collagen crosslinking treatments can prevent cell-mediated contraction of CDM scaffolds. Interestingly, crosslinking treatments influence chondrogenic differentiation. These effects seem to be mediated by modifications to cell-matrix interactions between MSCs and the CDM; however, further work is necessary to elucidate the specific mechanisms involved in this process.
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“Cross-linking agents have been successfully employed to enhance enzymatic resistance, matrix decomposition, and ultimately improve biomechanical strength in various tissues and organs [[171], [172], [173]].”
From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [171]
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Cites
Woessner, J. F. (1961) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(61)90291-0 · Cited by 3,849
Farndale, R. W., Buttle, D. J., & Barrett, A. J. (1986) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/0304-4165(86)90306-5 · Cited by 3,309
Alginate hydrogels as synthetic extracellular matrix materials
Rowley, J. A., Madlambayan, G., & Mooney, D. J. (1999) · Biomaterials · doi:10.1016/s0142-9612(98)00107-0 · Cited by 2,342
The extracellular matrix as a biologic scaffold material
Badylak, S. F. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.04.043 · Cited by 1,022
Pelttari, K., Winter, A., Steck, E., Goetzke, K., Hennig, T., Ochs, B. G., Aigner, T. G., & Richter, W. (2006) · Arthritis & Rheumatism · doi:10.1002/art.22136 · Cited by 824
Intrinsic extracellular matrix properties regulate stem cell differentiation
Reilly, G. C., & Engler, A. J. (2009) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2009.09.009 · Cited by 782
Collagen of articular cartilage.
Eyre, D. R. (2002) · Arthritis Research · doi:10.1186/ar380 · Cited by 721
Functional Tissue Engineering: The Role of Biomechanics
Butler, D. L., Goldstein, S. A., & Guilak, F. (2000) · Journal of Biomechanical Engineering · doi:10.1115/1.1318906 · Cited by 629
Self-citationKnudson, C. B., & Knudson, W. (2001) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0243 · Cited by 601
Rowlands, A., George, P. A., & Cooper-White, J. J. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.67.2008 · Cited by 535
Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells
Mueller, M. B., & Tuan, R. S. (2008) · Arthritis & Rheumatism · doi:10.1002/art.23370 · Cited by 490
Pieper, J. (1999) · Biomaterials · doi:10.1016/s0142-9612(98)00240-3 · Cited by 419
Mechanical characterization of collagen–glycosaminoglycan scaffolds
Harley, B. A. C., LEUNG, J., Silva, E. C. C. M., & Gibson, L. J. (2007) · Acta Biomaterialia · doi:10.1016/j.actbio.2006.12.009 · Cited by 397
Weadock, K. S., Miller, E. J., Bellincampi, L. D., Zawadsky, J. P., & Dunn, M. G. (1995) · Journal of Biomedical Materials Research · doi:10.1002/jbm.820291108 · Cited by 387
Lee, C. R., Grodzinsky, A. J., & Spector, M. (2001) · Biomaterials · doi:10.1016/s0142-9612(01)00067-9 · Cited by 385
Yang, Q., Peng, J. C., Guo, Q., Huang, J., Zhang, L., Yao, J., Yang, F., Wang, S., Xu, W., Wang, Y., et al. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2008.01.037 · Cited by 355
Yan, L., Wang, Y., Ren, L., Wu, G., Caridade, S. G., Fan, J., Wang, L., Ji, P., Oliveira, J. M., Oliveira, J. T., et al. (2010) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32869 · Cited by 352
Tissue engineering of functional articular cartilage: the current status
Kock, L. M., van Donkelaar, C. C., & Ito, K. (2011) · Cell and Tissue Research · doi:10.1007/s00441-011-1243-1 · Cited by 339
Pieper, J., Hafmans, T. G. M., Veerkamp, J. H., & Kuppevelt, T. H. V. (2000) · Biomaterials · doi:10.1016/s0142-9612(99)00222-7 · Cited by 323
Tissue Engineering of Articular Cartilage with Biomimetic Zones
Klein, T. J., Malda, J., Sah, R. L., & Hutmacher, D. W. (2009) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2008.0563 · Cited by 314
Anatomy, Biochemistry, and Physiology of Articular Cartilage
Huber, M., Trattnig, S., & Lintner, F. (2000) · Investigative Radiology · doi:10.1097/00004424-200010000-00003 · Cited by 304
Cheng, N., Estes, B. T., Awad, H. A., & Guilak, F. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0253 · Cited by 290
Self-citationLennon, D. P., Haynesworth, S. E., Bruder, S. P., Jaiswal, N., & Caplan, A. I. (1996) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/bf02724045 · Cited by 284
Self-citationHaugh, M. G., Jaasma, M. J., & O’Brien, F. J. (2008) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.31955 · Cited by 282
Diekman, B. O., Rowland, C. R., Lennon, D. P., Caplan, A. I., & Guilak, F. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2009.0398 · Cited by 267
Self-citationDecellularized Cartilage Matrix as a Novel Biomatrix for Cartilage Tissue-Engineering Applications
Schwarz, S., Körber, L., Elsaesser, A. F., Goldberg‐Bockhorn, E., Seitz, A. M., Dürselen, L., Ignatius, A. A., Walther, P., Breiter, R., & Rotter, N. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2011.0705 · Cited by 243
Liang, H., Chang, W., Liang, H., Lee, M., & Sung, H. (2004) · Journal of Applied Polymer Science · doi:10.1002/app.13563 · Cited by 228
Scaffolds for Articular Cartilage Repair
Frenkel, S. R., & Cesare, P. E. D. (2003) · Annals of Biomedical Engineering · doi:10.1023/b:abme.0000007788.41804.0d · Cited by 226
Extracellular Matrix Biomaterials for Soft Tissue Repair
Cornwell, K. G., Landsman, A. S., & James, K. S. (2009) · Clinics in Podiatric Medicine and Surgery · doi:10.1016/j.cpm.2009.08.001 · Cited by 219
Hu, X., Park, S., Gil, E. S., Xia, X., Weiss, A. S., & Kaplan, D. L. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.08.037 · Cited by 210
Extraction techniques for the decellularization of tissue engineered articular cartilage constructs
Elder, B. D., Eleswarapu, S. V., & Athanasiou, K. A. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.03.050 · Cited by 209
Koide, M., Osaki, K., Konishi, J., Oyamada, K., Katakura, T., Takahashi, A., & Yoshizato, K. (1993) · Journal of Biomedical Materials Research · doi:10.1002/jbm.820270111 · Cited by 202
A sandwich model for engineering cartilage with acellular cartilage sheets and chondrocytes
Gong, Y., Xue, J. X., Zhang, W. J., Zhou, G. D., Liu, W., & Cao, Y. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.11.078 · Cited by 169
Cornwell, K. G., Lei, P., Andreadis, S. T., & Pins, G. D. (2006) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.30893 · Cited by 153
Tendon cell contraction of collagen–GAG matrices in vitro: effect of cross-linking
Torres, D. S., Freyman, T. M., Yannas, I. V., & Spector, M. (2000) · Biomaterials · doi:10.1016/s0142-9612(00)00051-x · Cited by 149
Vickers, S. M., Squitieri, L. S., & Spector, M. (2006) · Tissue Engineering · doi:10.1089/ten.2006.12.1345 · Cited by 146
Stem cell-based therapies for osteoarthritis
Diekman, B. O., & Guilak, F. (2012) · Current Opinion in Rheumatology · doi:10.1097/bor.0b013e32835aa28d · Cited by 143
Self-citationPanseri, S., Russo, A., Cunha, C., Bondi, A., Martino, A. D., Patella, S., & Kon, E. (2011) · Knee Surgery Sports Traumatology Arthroscopy · doi:10.1007/s00167-011-1655-1 · Cited by 137
Fabrication and Repair of Cartilage Defects with a Novel Acellular Cartilage Matrix Scaffold
Yang, Z., Shi, Y., Wei, X., He, J., Yang, S., Dickson, G. R., Tang, J., Xiang, J., Song, C., & Li, G. (2009) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2009.0444 · Cited by 136
Articular Cartilage Tissue Engineering
Athanasiou, K. A., Darling, E. M., & Hu, J. C. Y. (2010) · Synthesis lectures on tissue engineering · doi:10.1007/978-3-031-02578-5 · Cited by 128
Wess, T. J., & Orgel, J. P. R. O. (2000) · Thermochimica Acta · doi:10.1016/s0040-6031(00)00619-5 · Cited by 123
Cheng, N., Estes, B. T., Young, T., & Guilak, F. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0384 · Cited by 106
Self-citationIrradiation-Induced Crosslinking of Collagen
Bailey, A. J., Rhodes, D. N., & Cater, C. W. (1964) · Radiation Research · doi:10.2307/3571543 · Cited by 105
Multifunctional Hybrid Three‐dimensionally Woven Scaffolds for Cartilage Tissue Engineering
Moutos, F. T., Estes, B. T., & Guilak, F. (2010) · Macromolecular Bioscience · doi:10.1002/mabi.201000124 · Cited by 104
Self-citationLee, J. E., Park, J., Hwang, Y. S., Kim, J. K., Kim, J. G., & Suh, H. (2001) · Yonsei Medical Journal · doi:10.3349/ymj.2001.42.2.172 · Cited by 101
Miles, C. A., Sionkowska, A., Hulin-Curtis, S. L., Sims, T. J., Avery, N. C., & Bailey, A. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002346200 · Cited by 100
Wang, C., Gong, Y., Zhong, Y., Yao, Y., Su, K. C., & Wang, D. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.12.072 · Cited by 95
Articular Cartilage Tissue Engineering
Athanasiou, K. A., Darling, E. M., & Hu, J. C. Y. (2009) · Synthesis lectures on tissue engineering · doi:10.2200/s00212ed1v01y200910tis003 · Cited by 88
Synergistic effects of glucose and ultraviolet irradiation on the physical properties of collagen
Ohan, M. P., Weadock, K. S., & Dunn, M. G. (2002) · Journal of Biomedical Materials Research · doi:10.1002/jbm.10111 · Cited by 87
Engineered Cartilage Using Primary Chondrocytes Cultured in a Porous Cartilage-Derived Matrix
Cheng, N., Estes, B. T., Young, T., & Guilak, F. (2010) · Regenerative Medicine · doi:10.2217/rme.10.87 · Cited by 82
Self-citationCrosslinking and modification of dermal sheep collagen using 1,4-butanediol diglycidyl ether
Zeeman, R., Dijkstra, P. J., van Wachem, P. B., van Luyn, M. J. A., Hendriks, M., Cahalan, P. T., & Feijen, J. (1999) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(19990905)46:3 · Cited by 80
Vickers, S. M., Gotterbarm, T., & Spector, M. (2010) · Journal of Orthopaedic Research® · doi:10.1002/jor.21113 · Cited by 77
Pfeiffer, E. R., Vickers, S. M., Frank, E. H., Grodzinsky, A. J., & Spector, M. (2008) · Osteoarthritis and Cartilage · doi:10.1016/j.joca.2008.02.014 · Cited by 69
Osborne, C. S., Barbenel, J. C., Smith, D. W., Savakis, M., & Grant, M. H. (1998) · Medical & Biological Engineering & Computing · doi:10.1007/bf02522870 · Cited by 69
Control of cell adhesion, migration, and orientation on photochemically microprocessed surfaces
Matsuda, T., & Sugawara, T. (1996) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(199610)32:2 · Cited by 68
Yang, I. H., Kim, S. H., Kim, Y. H., Sun, H. J., Kim, S., & Lee, J. W. (2004) · Yonsei Medical Journal · doi:10.3349/ymj.2004.45.5.891 · Cited by 68
Ode, A., Duda, G. N., Glaeser, J. D., Matziolis, G., Frauenschuh, S., Perka, C., Wilson, C. J., & Kasper, G. (2010) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.32909 · Cited by 67
Hafemann, B., Ghofrani, K., Gattner, H. ‐., Stieve, H., & Pallua, N. (2001) · Journal of Materials Science Materials in Medicine · doi:10.1023/a:1011205221972 · Cited by 66
Bigi, A., Cojazzi, G., Roveri, N., & Koch, M. H. J. (1987) · International Journal of Biological Macromolecules · doi:10.1016/0141-8130(87)90010-9 · Cited by 63
Contractile forces generated by articular chondrocytes in collagen-glycosaminoglycan matrices
Zaleskas, J. M., Kinner, B., Freyman, T. M., Yannas, I. V., Gibson, L. J., & Spector, M. (2003) · Biomaterials · doi:10.1016/j.biomaterials.2003.08.005 · Cited by 58
Optimization of UV cross‐linking density for durable and nontoxic collagen GAG dermal substitute
Lew, D., Liu, P. H., & Orgill, D. P. (2006) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.30704 · Cited by 57
Lee, J. W., Qi, W. N., & Scully, S. P. (2002) · Journal of Orthopaedic Research® · doi:10.1016/s0736-0266(01)00073-0 · Cited by 52
Ghone, N. V., & Grayson, W. L. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.24078 · Cited by 49
Effect of UV irradiation on type I collagen fibril formation in neutral collagen solutions
Menter, J. M., Patta, A. M., Sayre, R. M., Dowdy, J. C., & Willis, I. (2001) · Photodermatology Photoimmunology & Photomedicine · doi:10.1034/j.1600-0781.2001.170302.x · Cited by 37
Chiu, L., Yeh, T., Huang, H., Leu, S., Yang, C., & Tsai, Y. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22976 · Cited by 33
Rosenzweig, D. H., Solar-Cafaggi, S., & Quinn, T. M. (2012) · Acta Biomaterialia · doi:10.1016/j.actbio.2012.05.032 · Cited by 30
Ng, K. K., Thatte, H. S., & Spector, M. (2011) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.33163 · Cited by 26
Casas, J., Zhao, Q., Donovan, M. G., Schroeder, P., Stokes, K., & Untereker, D. F. (1999) · Journal of Biomedical Materials Research · doi:10.1002/(sici)1097-4636(19990915)46:4 · Cited by 23
Edwards, G., Coakley, W. T., Ralphs, J. R., & Archer, C. (2010) · European Cells and Materials · doi:10.22203/ecm.v019a01 · Cited by 15
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Metadata
- Authors
- Rowland, C. R., Lennon, D. P., Caplan, A. I., & Guilak, F.
- Affiliations
- Duke Medical Center (US)
- Case Western Reserve University (US)
- Corresponding author
- Guilak, Farshid
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 34
- Issue
- 23
- Pages
- 5802-5812
- ISSN
- 0142-9612 (ISSN-L)
- PMC
- PMC3660461
- OpenAlex
- W2021219047
- Cited by
- 190
- References
- 70
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 10 · 2023: 14 · 2022: 14 · 2021: 18 · 2020: 14 · 2019: 23 · 2018: 18 · 2017: 12 · 2016: 16 · 2015: 22 · 2014: 14 · 2013: 3
- FWCI
- 16.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (AG 15768, R01AG015768)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR 50245, AR48182, AR-48852, P01AR050245, R01AR048852, P01AR053622, AR53622, R01AR048182)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Materials Science › Biomaterials › Hydrogels: synthesis, properties, applications
- Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
- Keywords
- collagen cross-linking, chondrogenic differentiation, mesenchymal stem cells, dehydrothermal treatment, UV irradiation, carbodiimide crosslinking, cell adhesion, cell-matrix interactions, glycosaminoglycans, collagen, cartilage tissue engineering
- MeSH terms
- Adult, Animals, Cartilage, Cell Adhesion, Cell Differentiation, Collagen, Cross-Linking Reagents, DNA, Extracellular Matrix, Female, Glycosaminoglycans, Humans, Immunohistochemistry, Porosity, Chondrogenesis, Tissue Engineering, Sus scrofa, Green Fluorescent Proteins, Transforming Growth Factor beta3, Tissue Scaffolds, Mesenchymal Stem Cells
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