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Tissue engineering. Part A2015; 21(7-8); 1195-1206; doi: 10.1089/ten.TEA.2014.0362

Crosslinkable hydrogels derived from cartilage, meniscus, and tendon tissue.

Abstract: Decellularized tissues have proven to be versatile matrices for the engineering of tissues and organs. These matrices usually consist of collagens, matrix-specific proteins, and a set of largely undefined growth factors and signaling molecules. Although several decellularized tissues have found their way to clinical applications, their use in the engineering of cartilage tissue has only been explored to a limited extent. We set out to generate hydrogels from several tissue-derived matrices, as hydrogels are the current preferred cell carriers for cartilage repair. Equine cartilage, meniscus, and tendon tissue was harvested, decellularized, enzymatically digested, and functionalized with methacrylamide groups. After photo-cross-linking, these tissue digests were mechanically characterized. Next, gelatin methacrylamide (GelMA) hydrogel was functionalized with these methacrylated tissue digests. Equine chondrocytes and mesenchymal stromal cells (MSCs) (both from three donors) were encapsulated and cultured in vitro up to 6 weeks. Gene expression (COL1A1, COL2A1, ACAN, MMP-3, MMP-13, and MMP-14), cartilage-specific matrix formation, and hydrogel stiffness were analyzed after culture. The cartilage, meniscus, and tendon digests were successfully photo-cross-linked into hydrogels. The addition of the tissue-derived matrices to GelMA affected chondrogenic differentiation of MSCs, although no consequent improvement was demonstrated. For chondrocytes, the tissue-derived matrix gels performed worse compared to GelMA alone. This work demonstrates for the first time that native tissues can be processed into crosslinkable hydrogels for the engineering of tissues. Moreover, the differentiation of encapsulated cells can be influenced in these stable, decellularized matrix hydrogels.
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Publication Date: 2015-02-09 PubMed ID: 25557049PubMed Central: PMC4394887DOI: 10.1089/ten.TEA.2014.0362Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article describes the process of transforming cartilage, meniscus, and tendon tissues (harvested from horses) into crosslinkable hydrogels, to explore their potential use in tissue engineering. The study also investigates how these tissue-derived hydrogels affect the differentiation of certain cells, particularly chondrocytes and Mesenchymal Stromal Cells (MSCs).

Processing of Native Tissues into Hydrogels

  • The study aimed to create hydrogels from native tissues, as these hydrogels could potentially facilitate cartilage repair.
  • The native tissues used for the study were cartilage, meniscus, and tendons, sourced from horses.
  • These tissues were decellularized, a process that removes all the cells from a tissue, leaving behind a matrix of collagen, growth factors, and several other elements. This provides a structure for new cells to grow in, and is an important step in many tissue engineering processes.
  • Once decellularized, the tissues were digested enzymatically to get tissue digests. They were then functionalized with methacrylamide groups. The tissues allowing them to create structural crossover points, or ‘crosslinks’, forming hydrogels.
  • After being photo-crosslinked, these tissue hydrogels underwent mechanical characterization, a process that identifies their mechanical properties.

Addition of Tissue-derived Matrices to GelMA

  • GelMA, or Gelatin Methacrylamide, is another type of hydrogel and was also tested in conjunction with the tissue-derived matrices.
  • This hydrogel’s base is made from gelatin, which is desirable for tissue engineering due to its non-toxic, biocompatible properties.
  • By integrating the tissue-derived matrices to GelMA, the researchers aimed to investigate if these combined hydrogels could influence the chondrogenic differentiation of MSCs. Meaning, if they could influence the process by which these stem cells develop into chondrocytes—essential for cartilage formation.

Chondrocytes and MSCs Culture and Analysis

  • Chondrocytes and MSCs were encapsulated into the hydrogels and cultured in vitro for up to 6 weeks.
  • After this culture period, the gene expression of specific markers, including COL1A1, COL2A1, ACAN, MMP-3, MMP-13, and MMP-14, was analyzed. These genes are associated with cartilage formation and degradation.
  • Furthermore, the creation of cartilage-specific matrix and hydrogel stiffness was also observed.
  • While the researchers noticed that the addition of tissue-derived matrices to GelMA influenced the chondrogenic differentiation of MSCs, no significant improvement was observed.
  • For chondrocytes, the tissue-derived matrix gels performed worse compared to the GelMA hydrogel alone.

Conclusion

  • This research successfully demonstrated that native tissues could be processed into crosslinkable hydrogels, opening new possibilities for tissue engineering.
  • Nonetheless, the performance of these hydrogels, with respect to cell differentiation and properties, will require further study to prove their clinical value.

Cite This Article

APA
Visser J, Levett PA, te Moller NC, Besems J, Boere KW, van Rijen MH, de Grauw JC, Dhert WJ, van Weeren PR, Malda J. (2015). Crosslinkable hydrogels derived from cartilage, meniscus, and tendon tissue. Tissue Eng Part A, 21(7-8), 1195-1206. https://doi.org/10.1089/ten.TEA.2014.0362

Publication

Tissue engineering. Part A
ISSN: 1937-335X
NlmUniqueID: 101466659
Country: United States
Language: English
Volume: 21
Issue: 7-8
Pages: 1195-1206

Researcher Affiliations

Visser, Jetze
  • 1 Department of Orthopaedics, University Medical Center Utrecht , Utrecht, The Netherlands .
Levett, Peter A
    te Moller, Nikae C R
      Besems, Jeremy
        Boere, Kristel W M
          van Rijen, Mattie H P
            de Grauw, Janny C
              Dhert, Wouter J A
                van Weeren, P René
                  Malda, Jos

                    MeSH Terms

                    • Animals
                    • Cartilage / cytology
                    • Cell Differentiation / drug effects
                    • Cell Survival / drug effects
                    • Chondrocytes / cytology
                    • Chondrocytes / drug effects
                    • Compressive Strength / drug effects
                    • Cross-Linking Reagents / pharmacology
                    • DNA / metabolism
                    • Elastic Modulus / drug effects
                    • Extracellular Matrix / drug effects
                    • Extracellular Matrix / metabolism
                    • Gene Expression Regulation / drug effects
                    • Glycosaminoglycans / metabolism
                    • Horses
                    • Hydrogels / pharmacology
                    • Menisci, Tibial / cytology
                    • Mesenchymal Stem Cells / cytology
                    • Tendons / cytology

                    References

                    This article includes 51 references
                    1. DeForest CA, Anseth KS. Advances in bioactive hydrogels to probe and direct cell fate.. Annu Rev Chem Biomol Eng 2012;3:421-44.
                      pubmed: 22524507doi: 10.1146/annurev-chembioeng-062011-080945google scholar: lookup
                    2. Badylak SF, Weiss DJ, Caplan A, Macchiarini P. Engineered whole organs and complex tissues.. Lancet 2012 Mar 10;379(9819):943-952.
                      pubmed: 22405797doi: 10.1016/s0140-6736(12)60073-7google scholar: lookup
                    3. Badylak SF, Freytes DO, Gilbert TW. Extracellular matrix as a biological scaffold material: Structure and function.. Acta Biomater 2009 Jan;5(1):1-13.
                      pubmed: 18938117doi: 10.1016/j.actbio.2008.09.013google scholar: lookup
                    4. Badylak SF, Brown BN, Gilbert TW, Daly KA, Huber A, Turner NJ. Biologic scaffolds for constructive tissue remodeling.. Biomaterials 2011 Jan;32(1):316-9.
                      pubmed: 21125721doi: 10.1016/j.biomaterials.2010.09.018google scholar: lookup
                    5. Benders KE, van Weeren PR, Badylak SF, Saris DB, Dhert WJ, Malda J. Extracellular matrix scaffolds for cartilage and bone regeneration.. Trends Biotechnol 2013 Mar;31(3):169-76.
                      pubmed: 23298610doi: 10.1016/j.tibtech.2012.12.004google scholar: lookup
                    6. Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes.. Biomaterials 2011 Apr;32(12):3233-43.
                      pmc: PMC3084613pubmed: 21296410doi: 10.1016/j.biomaterials.2011.01.057google scholar: lookup
                    7. Spiller KL, Maher SA, Lowman AM. Hydrogels for the repair of articular cartilage defects.. Tissue Eng Part B Rev 2011 Aug;17(4):281-99.
                      pmc: PMC3171151pubmed: 21510824doi: 10.1089/ten.teb.2011.0077google scholar: lookup
                    8. Huey DJ, Hu JC, Athanasiou KA. Unlike bone, cartilage regeneration remains elusive.. Science 2012 Nov 16;338(6109):917-21.
                      pmc: PMC4327988pubmed: 23161992doi: 10.1126/science.1222454google scholar: lookup
                    9. Malda J, Visser J, Melchels FP, Jüngst T, Hennink WE, Dhert WJ, Groll J, Hutmacher DW. 25th anniversary article: Engineering hydrogels for biofabrication.. Adv Mater 2013 Sep 25;25(36):5011-28.
                      pubmed: 24038336doi: 10.1002/adma.201302042google scholar: lookup
                    10. Mastbergen SC, Saris DB, Lafeber FP. Functional articular cartilage repair: here, near, or is the best approach not yet clear?. Nat Rev Rheumatol 2013 May;9(5):277-90.
                      pubmed: 23507899doi: 10.1038/nrrheum.2013.29google scholar: lookup
                    11. Deponti D, Di Giancamillo A, Mangiavini L, Pozzi A, Fraschini G, Sosio C, Domeneghini C, Peretti GM. Fibrin-based model for cartilage regeneration: tissue maturation from in vitro to in vivo.. Tissue Eng Part A 2012 Jun;18(11-12):1109-22.
                      pubmed: 22316220doi: 10.1089/ten.tea.2011.0272google scholar: lookup
                    12. Homminga GN, Buma P, Koot HW, van der Kraan PM, van den Berg WB. Chondrocyte behavior in fibrin glue in vitro.. Acta Orthop Scand 1993 Aug;64(4):441-5.
                      pubmed: 8213124doi: 10.3109/17453679308993663google scholar: lookup
                    13. Moreira Teixeira LS, Leijten JC, Wennink JW, Chatterjea AG, Feijen J, van Blitterswijk CA, Dijkstra PJ, Karperien M. The effect of platelet lysate supplementation of a dextran-based hydrogel on cartilage formation.. Biomaterials 2012 May;33(14):3651-61.
                      pubmed: 22349290doi: 10.1016/j.biomaterials.2012.01.051google scholar: lookup
                    14. Nguyen LH, Kudva AK, Guckert NL, Linse KD, Roy K. Unique biomaterial compositions direct bone marrow stem cells into specific chondrocytic phenotypes corresponding to the various zones of articular cartilage.. Biomaterials 2011 Feb;32(5):1327-38.
                      pubmed: 21067807doi: 10.1016/j.biomaterials.2010.10.009google scholar: lookup
                    15. Freytes DO, Martin J, Velankar SS, Lee AS, Badylak SF. Preparation and rheological characterization of a gel form of the porcine urinary bladder matrix.. Biomaterials 2008 Apr;29(11):1630-7.
                      pubmed: 18201760doi: 10.1016/j.biomaterials.2007.12.014google scholar: lookup
                    16. Wolf MT, Daly KA, Brennan-Pierce EP, Johnson SA, Carruthers CA, D'Amore A, Nagarkar SP, Velankar SS, Badylak SF. A hydrogel derived from decellularized dermal extracellular matrix.. Biomaterials 2012 Oct;33(29):7028-38.
                      pmc: PMC3408574pubmed: 22789723doi: 10.1016/j.biomaterials.2012.06.051google scholar: lookup
                    17. Medberry CJ, Crapo PM, Siu BF, Carruthers CA, Wolf MT, Nagarkar SP, Agrawal V, Jones KE, Kelly J, Johnson SA, Velankar SS, Watkins SC, Modo M, Badylak SF. Hydrogels derived from central nervous system extracellular matrix.. Biomaterials 2013 Jan;34(4):1033-40.
                      pmc: PMC3512573pubmed: 23158935doi: 10.1016/j.biomaterials.2012.10.062google scholar: lookup
                    18. Pati F, Jang J, Ha DH, Won Kim S, Rhie JW, Shim JH, Kim DH, Cho DW. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink.. Nat Commun 2014 Jun 2;5:3935.
                      pmc: PMC4059935pubmed: 24887553doi: 10.1038/ncomms4935google scholar: lookup
                    19. Mescher A.L.Junqueira's Basic Histology: Text and Atlas, 12th edition. New York, NY: The McGraw-Hill Companies, 2010
                    20. Benders KE, Boot W, Cokelaere SM, Van Weeren PR, Gawlitta D, Bergman HJ, Saris DB, Dhert WJ, Malda J. Multipotent Stromal Cells Outperform Chondrocytes on Cartilage-Derived Matrix Scaffolds.. Cartilage 2014 Oct;5(4):221-30.
                      pmc: PMC4335771pubmed: 26069701doi: 10.1177/1947603514535245google scholar: lookup
                    21. Klatt AR, Paul-Klausch B, Klinger G, Kühn G, Renno JH, Banerjee M, Malchau G, Wielckens K. A critical role for collagen II in cartilage matrix degradation: collagen II induces pro-inflammatory cytokines and MMPs in primary human chondrocytes.. J Orthop Res 2009 Jan;27(1):65-70.
                      pubmed: 18655132doi: 10.1002/jor.20716google scholar: lookup
                    22. Fichter M, Körner U, Schömburg J, Jennings L, Cole AA, Mollenhauer J. Collagen degradation products modulate matrix metalloproteinase expression in cultured articular chondrocytes.. J Orthop Res 2006 Jan;24(1):63-70.
                      pubmed: 16419970doi: 10.1002/jor.20001google scholar: lookup
                    23. Delcogliano M, de Caro F, Scaravella E, Ziveri G, De Biase CF, Marotta D, Marenghi P, Delcogliano A. Use of innovative biomimetic scaffold in the treatment for large osteochondral lesions of the knee.. Knee Surg Sports Traumatol Arthrosc 2014 Jun;22(6):1260-9.
                      pubmed: 24146051doi: 10.1007/s00167-013-2717-3google scholar: lookup
                    24. Zheng MH, Willers C, Kirilak L, Yates P, Xu J, Wood D, Shimmin A. Matrix-induced autologous chondrocyte implantation (MACI): biological and histological assessment.. Tissue Eng 2007 Apr;13(4):737-46.
                      pubmed: 17371156doi: 10.1089/ten.2006.0246google scholar: lookup
                    25. Boere KW, Visser J, Seyednejad H, Rahimian S, Gawlitta D, van Steenbergen MJ, Dhert WJ, Hennink WE, Vermonden T, Malda J. Covalent attachment of a three-dimensionally printed thermoplast to a gelatin hydrogel for mechanically enhanced cartilage constructs.. Acta Biomater 2014 Jun;10(6):2602-11.
                      pubmed: 24590160doi: 10.1016/j.actbio.2014.02.041google scholar: lookup
                    26. Nikkhah M, Eshak N, Zorlutuna P, Annabi N, Castello M, Kim K, Dolatshahi-Pirouz A, Edalat F, Bae H, Yang Y, Khademhosseini A. Directed endothelial cell morphogenesis in micropatterned gelatin methacrylate hydrogels.. Biomaterials 2012 Dec;33(35):9009-18.
                      pmc: PMC3643201pubmed: 23018132doi: 10.1016/j.biomaterials.2012.08.068google scholar: lookup
                    27. Nichol JW, Koshy ST, Bae H, Hwang CM, Yamanlar S, Khademhosseini A. Cell-laden microengineered gelatin methacrylate hydrogels.. Biomaterials 2010 Jul;31(21):5536-44.
                      pmc: PMC2878615pubmed: 20417964doi: 10.1016/j.biomaterials.2010.03.064google scholar: lookup
                    28. Levett PA, Melchels FP, Schrobback K, Hutmacher DW, Malda J, Klein TJ. A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate.. Acta Biomater 2014 Jan;10(1):214-23.
                      pubmed: 24140603doi: 10.1016/j.actbio.2013.10.005google scholar: lookup
                    29. Piper DW, Fenton BH. pH stability and activity curves of pepsin with special reference to their clinical importance.. Gut 1965 Oct;6(5):506-8.
                      pmc: PMC1552331pubmed: 4158734doi: 10.1136/gut.6.5.506google scholar: lookup
                    30. Van Den Bulcke AI, Bogdanov B, De Rooze N, Schacht EH, Cornelissen M, Berghmans H. Structural and rheological properties of methacrylamide modified gelatin hydrogels.. Biomacromolecules 2000 Spring;1(1):31-8.
                      pubmed: 11709840doi: 10.1021/bm990017dgoogle scholar: lookup
                    31. Schuurman W, Levett PA, Pot MW, van Weeren PR, Dhert WJ, Hutmacher DW, Melchels FP, Klein TJ, Malda J. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs.. Macromol Biosci 2013 May;13(5):551-61.
                      pubmed: 23420700doi: 10.1002/mabi.201200471google scholar: lookup
                    32. Gawlitta D, Farrell E, Malda J, Creemers LB, Alblas J, Dhert WJ. Modulating endochondral ossification of multipotent stromal cells for bone regeneration.. Tissue Eng Part B Rev 2010 Aug;16(4):385-95.
                      pubmed: 20131956doi: 10.1089/ten.teb.2009.0712google scholar: lookup
                    33. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells.. Science 1999 Apr 2;284(5411):143-7.
                      pubmed: 10102814doi: 10.1126/science.284.5411.143google scholar: lookup
                    34. Chomczynski P, Mackey K. Substitution of chloroform by bromo-chloropropane in the single-step method of RNA isolation.. Anal Biochem 1995 Feb 10;225(1):163-4.
                      pubmed: 7539982doi: 10.1006/abio.1995.1126google scholar: lookup
                    35. Fujiwara T, Kubo T, Kanazawa S, Shingaki K, Taniguchi M, Matsuzaki S, Gurtner GC, Tohyama M, Hosokawa K. Direct contact of fibroblasts with neuronal processes promotes differentiation to myofibroblasts and induces contraction of collagen matrix in vitro.. Wound Repair Regen 2013 Jul-Aug;21(4):588-94.
                      pubmed: 23758129doi: 10.1111/wrr.12059google scholar: lookup
                    36. Yang G, Rothrauff BB, Lin H, Gottardi R, Alexander PG, Tuan RS. Enhancement of tenogenic differentiation of human adipose stem cells by tendon-derived extracellular matrix.. Biomaterials 2013 Dec;34(37):9295-306.
                      pmc: PMC3951997pubmed: 24044998doi: 10.1016/j.biomaterials.2013.08.054google scholar: lookup
                    37. Williams CG, Kim TK, Taboas A, Malik A, Manson P, Elisseeff J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel.. Tissue Eng 2003 Aug;9(4):679-88.
                      pubmed: 13678446doi: 10.1089/107632703768247377google scholar: lookup
                    38. Erickson IE, Huang AH, Chung C, Li RT, Burdick JA, Mauck RL. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels.. Tissue Eng Part A 2009 May;15(5):1041-52.
                      pmc: PMC2810411pubmed: 19119920doi: 10.1089/ten.tea.2008.0099google scholar: lookup
                    39. Carter-Arnold JL, Neilsen NL, Amelse LL, Odoi A, Dhar MS. In vitro analysis of equine, bone marrow-derived mesenchymal stem cells demonstrates differences within age- and gender-matched horses.. Equine Vet J 2014 Sep;46(5):589-95.
                      pubmed: 23855680doi: 10.1111/evj.12142google scholar: lookup
                    40. de Windt TS, Hendriks JA, Zhao X, Vonk LA, Creemers LB, Dhert WJ, Randolph MA, Saris DB. Concise review: unraveling stem cell cocultures in regenerative medicine: which cell interactions steer cartilage regeneration and how?. Stem Cells Transl Med 2014 Jun;3(6):723-33.
                      pmc: PMC4039458pubmed: 24763684doi: 10.5966/sctm.2013-0207google scholar: lookup
                    41. Xu L, Peng H, Glasson S, Lee PL, Hu K, Ijiri K, Olsen BR, Goldring MB, Li Y. Increased expression of the collagen receptor discoidin domain receptor 2 in articular cartilage as a key event in the pathogenesis of osteoarthritis.. Arthritis Rheum 2007 Aug;56(8):2663-73.
                      pubmed: 17665456doi: 10.1002/art.22761google scholar: lookup
                    42. Zhang Y, Su J, Yu J, Bu X, Ren T, Liu X, Yao L. An essential role of discoidin domain receptor 2 (DDR2) in osteoblast differentiation and chondrocyte maturation via modulation of Runx2 activation.. J Bone Miner Res 2011 Mar;26(3):604-17.
                      pubmed: 20734453doi: 10.1002/jbmr.225google scholar: lookup
                    43. Rutgers M, Saris DB, Vonk LA, van Rijen MH, Akrum V, Langeveld D, van Boxtel A, Dhert WJ, Creemers LB. Effect of collagen type I or type II on chondrogenesis by cultured human articular chondrocytes.. Tissue Eng Part A 2013 Jan;19(1-2):59-65.
                      pubmed: 22861168doi: 10.1089/ten.tea.2011.0416google scholar: lookup
                    44. Schwarz S, Elsaesser AF, Koerber L, Goldberg-Bockhorn E, Seitz AM, Bermueller C, Dürselen L, Ignatius A, Breiter R, Rotter N. Processed xenogenic cartilage as innovative biomatrix for cartilage tissue engineering: effects on chondrocyte differentiation and function.. J Tissue Eng Regen Med 2015 Dec;9(12):E239-51.
                      doi: 10.1002/term.1650pubmed: 23193064google scholar: lookup
                    45. Nehrer S, Breinan HA, Ramappa A, Shortkroff S, Young G, Minas T, Sledge CB, Yannas IV, Spector M. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro.. J Biomed Mater Res 1997 Summer;38(2):95-104.
                      pubmed: 9178736doi: 10.1002/(sici)1097-4636(199722)38:2<95::aid-jbm3>3.0.co;2-bgoogle scholar: lookup
                    46. Nehrer S, Breinan HA, Ramappa A, Young G, Shortkroff S, Louie LK, Sledge CB, Yannas IV, Spector M. Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes.. Biomaterials 1997 Jun;18(11):769-76.
                      pubmed: 9177854doi: 10.1016/s0142-9612(97)00001-xgoogle scholar: lookup
                    47. Chun SY, Lim GJ, Kwon TG, Kwak EK, Kim BW, Atala A, Yoo JJ. Identification and characterization of bioactive factors in bladder submucosa matrix.. Biomaterials 2007 Oct;28(29):4251-6.
                      pubmed: 17617449doi: 10.1016/j.biomaterials.2007.05.020google scholar: lookup
                    48. Voytik-Harbin SL, Brightman AO, Kraine MR, Waisner B, Badylak SF. Identification of extractable growth factors from small intestinal submucosa.. J Cell Biochem 1997 Dec 15;67(4):478-91.
                      pubmed: 9383707
                    49. Chen CC, Liao CH, Wang YH, Hsu YM, Huang SH, Chang CH, Fang HW. Cartilage fragments from osteoarthritic knee promote chondrogenesis of mesenchymal stem cells without exogenous growth factor induction.. J Orthop Res 2012 Mar;30(3):393-400.
                      pubmed: 22267189doi: 10.1002/jor.21541google scholar: lookup
                    50. Xue JX, Gong YY, Zhou GD, Liu W, Cao Y, Zhang WJ. Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells induced by acellular cartilage sheets.. Biomaterials 2012 Aug;33(24):5832-40.
                      pubmed: 22608213doi: 10.1016/j.biomaterials.2012.04.054google scholar: lookup
                    51. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. 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 2006 Apr 20;93(6):1152-63.
                      pubmed: 16470881doi: 10.1002/bit.20828google scholar: lookup

                    Citations

                    This article has been cited 43 times.
                    1. Jin P, Liu L, Chen X, Cheng L, Zhang W, Zhong G. Applications and prospects of different functional hydrogels in meniscus repair. Front Bioeng Biotechnol 2022;10:1082499.
                      doi: 10.3389/fbioe.2022.1082499pubmed: 36568293google scholar: lookup
                    2. Galliger Z, Vogt CD, Helms HR, Panoskaltsis-Mortari A. Extracellular Matrix Microparticles Improve GelMA Bioink Resolution for 3D Bioprinting at Ambient Temperature. Macromol Mater Eng 2022 Oct;307(10).
                      doi: 10.1002/mame.202200196pubmed: 36531127google scholar: lookup
                    3. Hua Y, Huo Y, Bai B, Hao J, Hu G, Ci Z, Wu X, Yu M, Wang X, Chen H, Ren W, Zhang Y, Wang X, Zhou G. Fabrication of biphasic cartilage-bone integrated scaffolds based on tissue-specific photo-crosslinkable acellular matrix hydrogels. Mater Today Bio 2022 Dec 15;17:100489.
                      doi: 10.1016/j.mtbio.2022.100489pubmed: 36388453google scholar: lookup
                    4. Marvin JC, Mochida A, Paredes J, Vaughn B, Andarawis-Puri N. Detergent-Free Decellularization Preserves the Mechanical and Biological Integrity of Murine Tendon. Tissue Eng Part C Methods 2022 Dec;28(12):646-655.
                      doi: 10.1089/ten.TEC.2022.0135pubmed: 36326204google scholar: lookup
                    5. Ma H, Peng Y, Zhang S, Zhang Y, Min P. Effects and Progress of Photo-Crosslinking Hydrogels in Wound Healing Improvement. Gels 2022 Sep 23;8(10).
                      doi: 10.3390/gels8100609pubmed: 36286110google scholar: lookup
                    6. Tan G, Xu J, Yu Q, Zhang J, Hu X, Sun C, Zhang H. Photo-Crosslinkable Hydrogels for 3D Bioprinting in the Repair of Osteochondral Defects: A Review of Present Applications and Future Perspectives. Micromachines (Basel) 2022 Jun 29;13(7).
                      doi: 10.3390/mi13071038pubmed: 35888855google scholar: lookup
                    7. Xu Z, Fang Y, Chen Y, Zhao Y, Wei W, Teng C. Hydrogel Development for Rotator Cuff Repair. Front Bioeng Biotechnol 2022;10:851660.
                      doi: 10.3389/fbioe.2022.851660pubmed: 35782490google scholar: lookup
                    8. Kiyotake EA, Cheng ME, Thomas EE, Detamore MS. The Rheology and Printability of Cartilage Matrix-Only Biomaterials. Biomolecules 2022 Jun 17;12(6).
                      doi: 10.3390/biom12060846pubmed: 35740971google scholar: lookup
                    9. Jeyaraman M, Shivaraj B, Bingi SK, Ranjan R, Muthu S, Khanna M. Does vehicle-based delivery of mesenchymal stromal cells give superior results in knee osteoarthritis? Meta-analysis of randomized controlled trials. J Clin Orthop Trauma 2022 Feb;25:101772.
                      doi: 10.1016/j.jcot.2022.101772pubmed: 35127439google scholar: lookup
                    10. Pouliot RA, Young BM, Link PA, Park HE, Kahn AR, Shankar K, Schneck MB, Weiss DJ, Heise RL. Porcine Lung-Derived Extracellular Matrix Hydrogel Properties Are Dependent on Pepsin Digestion Time. Tissue Eng Part C Methods 2020 Jun;26(6):332-346.
                      doi: 10.1089/ten.TEC.2020.0042pubmed: 32390520google scholar: lookup
                    11. Petrou CL, D'Ovidio TJ, Bölükbas DA, Tas S, Brown RD, Allawzi A, Lindstedt S, Nozik-Grayck E, Stenmark KR, Wagner DE, Magin CM. Clickable decellularized extracellular matrix as a new tool for building hybrid-hydrogels to model chronic fibrotic diseases in vitro. J Mater Chem B 2020 Aug 21;8(31):6814-6826.
                      doi: 10.1039/d0tb00613kpubmed: 32343292google scholar: lookup
                    12. Boere KWM, Blokzijl MM, Visser J, Linssen JEA, Malda J, Hennink WE, Vermonden T. Biofabrication of reinforced 3D-scaffolds using two-component hydrogels. J Mater Chem B 2015 Dec 14;3(46):9067-9078.
                      doi: 10.1039/c5tb01645bpubmed: 32263038google scholar: lookup
                    13. Shridhar A, Amsden BG, Gillies ER, Flynn LE. Investigating the Effects of Tissue-Specific Extracellular Matrix on the Adipogenic and Osteogenic Differentiation of Human Adipose-Derived Stromal Cells Within Composite Hydrogel Scaffolds. Front Bioeng Biotechnol 2019;7:402.
                      doi: 10.3389/fbioe.2019.00402pubmed: 31921807google scholar: lookup
                    14. Lyons LP, Hidalgo Perea S, Weinberg JB, Wittstein JR, McNulty AL. Meniscus-Derived Matrix Bioscaffolds: Effects of Concentration and Cross-Linking on Meniscus Cellular Responses and Tissue Repair. Int J Mol Sci 2019 Dec 19;21(1).
                      doi: 10.3390/ijms21010044pubmed: 31861690google scholar: lookup
                    15. Kim W, Lee H, Lee J, Atala A, Yoo JJ, Lee SJ, Kim GH. Efficient myotube formation in 3D bioprinted tissue construct by biochemical and topographical cues. Biomaterials 2020 Feb;230:119632.
                      doi: 10.1016/j.biomaterials.2019.119632pubmed: 31761486google scholar: lookup
                    16. Cramer MC, Badylak SF.  Extracellular Matrix-Based Biomaterials and Their Influence Upon Cell Behavior. Ann Biomed Eng 2020 Jul;48(7):2132-2153.
                      doi: 10.1007/s10439-019-02408-9pubmed: 31741227google scholar: lookup
                    17. Iannarone VJ, Cruz GE, Hilliard BA, Barbe MF. The answer depends on the question: Optimal conditions for western blot characterization of muscle collagen type 1 depends on desired isoform. J Biol Methods 2019;6(3):e117.
                      doi: 10.14440/jbm.2019.289pubmed: 31583262google scholar: lookup
                    18. Townsend JM, Beck EC, Gehrke SH, Berkland CJ, Detamore MS. Flow Behavior Prior to Crosslinking: The Need for Precursor Rheology for Placement of Hydrogels in Medical Applications and for 3D Bioprinting. Prog Polym Sci 2019 Apr;91:126-140.
                      doi: 10.1016/j.progpolymsci.2019.01.003pubmed: 31571701google scholar: lookup
                    19. Ruprecht JC, Waanders TD, Rowland CR, Nishimuta JF, Glass KA, Stencel J, DeFrate LE, Guilak F, Weinberg JB, McNulty AL. Meniscus-Derived Matrix Scaffolds Promote the Integrative Repair of Meniscal Defects. Sci Rep 2019 Jun 18;9(1):8719.
                      doi: 10.1038/s41598-019-44855-3pubmed: 31213610google scholar: lookup
                    20. Jabbari E. Challenges for Natural Hydrogels in Tissue Engineering. Gels 2019 May 29;5(2).
                      doi: 10.3390/gels5020030pubmed: 31146448google scholar: lookup
                    21. Kim YS, Majid M, Melchiorri AJ, Mikos AG. Applications of decellularized extracellular matrix in bone and cartilage tissue engineering. Bioeng Transl Med 2019 Jan;4(1):83-95.
                      doi: 10.1002/btm2.10110pubmed: 30680321google scholar: lookup
                    22. Visscher DO, Gleadall A, Buskermolen JK, Burla F, Segal J, Koenderink GH, Helder MN, van Zuijlen PPM. Design and fabrication of a hybrid alginate hydrogel/poly(ε-caprolactone) mold for auricular cartilage reconstruction. J Biomed Mater Res B Appl Biomater 2019 Jul;107(5):1711-1721.
                      doi: 10.1002/jbm.b.34264pubmed: 30383916google scholar: lookup
                    23. Roffi A, Nakamura N, Sanchez M, Cucchiarini M, Filardo G. Injectable Systems for Intra-Articular Delivery of Mesenchymal Stromal Cells for Cartilage Treatment: A Systematic Review of Preclinical and Clinical Evidence. Int J Mol Sci 2018 Oct 25;19(11).
                      doi: 10.3390/ijms19113322pubmed: 30366400google scholar: lookup
                    24. Moeinzadeh S, Monavarian M, Kader S, Jabbari E. Sequential Zonal Chondrogenic Differentiation of Mesenchymal Stem Cells in Cartilage Matrices. Tissue Eng Part A 2019 Feb;25(3-4):234-247.
                      doi: 10.1089/ten.TEA.2018.0083pubmed: 30146939google scholar: lookup
                    25. Spang MT, Christman KL. Extracellular matrix hydrogel therapies: In vivo applications and development. Acta Biomater 2018 Mar 1;68:1-14.
                      doi: 10.1016/j.actbio.2017.12.019pubmed: 29274480google scholar: lookup
                    26. Lowe J, Almarza AJ. A review of in-vitro fibrocartilage tissue engineered therapies with a focus on the temporomandibular joint. Arch Oral Biol 2017 Nov;83:193-201.
                      doi: 10.1016/j.archoralbio.2017.07.013pubmed: 28787640google scholar: lookup
                    27. Rothrauff BB, Yang G, Tuan RS. Tissue-specific bioactivity of soluble tendon-derived and cartilage-derived extracellular matrices on adult mesenchymal stem cells. Stem Cell Res Ther 2017 Jun 5;8(1):133.
                      doi: 10.1186/s13287-017-0580-8pubmed: 28583182google scholar: lookup
                    28. Sadeghi AH, Shin SR, Deddens JC, Fratta G, Mandla S, Yazdi IK, Prakash G, Antona S, Demarchi D, Buijsrogge MP, Sluijter JPG, Hjortnaes J, Khademhosseini A. Engineered 3D Cardiac Fibrotic Tissue to Study Fibrotic Remodeling. Adv Healthc Mater 2017 Jun;6(11).
                      doi: 10.1002/adhm.201601434pubmed: 28498548google scholar: lookup
                    29. Rothrauff BB, Coluccino L, Gottardi R, Ceseracciu L, Scaglione S, Goldoni L, Tuan RS. Efficacy of thermoresponsive, photocrosslinkable hydrogels derived from decellularized tendon and cartilage extracellular matrix for cartilage tissue engineering. J Tissue Eng Regen Med 2018 Jan;12(1):e159-e170.
                      doi: 10.1002/term.2465pubmed: 28486778google scholar: lookup
                    30. Yuan X, Wei Y, Villasante A, Ng JJD, Arkonac DE, Chao PG, Vunjak-Novakovic G. Stem cell delivery in tissue-specific hydrogel enabled meniscal repair in an orthotopic rat model. Biomaterials 2017 Jul;132:59-71.
                      doi: 10.1016/j.biomaterials.2017.04.004pubmed: 28407495google scholar: lookup
                    31. Yang J, Zhang YS, Yue K, Khademhosseini A. Cell-laden hydrogels for osteochondral and cartilage tissue engineering. Acta Biomater 2017 Jul 15;57:1-25.
                      doi: 10.1016/j.actbio.2017.01.036pubmed: 28088667google scholar: lookup
                    32. Rothrauff BB, Shimomura K, Gottardi R, Alexander PG, Tuan RS. Anatomical region-dependent enhancement of 3-dimensional chondrogenic differentiation of human mesenchymal stem cells by soluble meniscus extracellular matrix. Acta Biomater 2017 Feb;49:140-151.
                      doi: 10.1016/j.actbio.2016.11.046pubmed: 27876676google scholar: lookup
                    33. Agmon G, Christman KL. Controlling stem cell behavior with decellularized extracellular matrix scaffolds. Curr Opin Solid State Mater Sci 2016 Aug;20(4):193-201.
                      doi: 10.1016/j.cossms.2016.02.001pubmed: 27524932google scholar: lookup
                    34. Richards D, Jia J, Yost M, Markwald R, Mei Y. 3D Bioprinting for Vascularized Tissue Fabrication. Ann Biomed Eng 2017 Jan;45(1):132-147.
                      doi: 10.1007/s10439-016-1653-zpubmed: 27230253google scholar: lookup
                    35. Abbadessa A, Mouser VHM, Blokzijl MM, Gawlitta D, Dhert WJA, Hennink WE, Malda J, Vermonden T. A Synthetic Thermosensitive Hydrogel for Cartilage Bioprinting and Its Biofunctionalization with Polysaccharides. Biomacromolecules 2016 Jun 13;17(6):2137-2147.
                      doi: 10.1021/acs.biomac.6b00366pubmed: 27171342google scholar: lookup
                    36. Beck EC, Barragan M, Tadros MH, Gehrke SH, Detamore MS. Approaching the compressive modulus of articular cartilage with a decellularized cartilage-based hydrogel. Acta Biomater 2016 Jul 1;38:94-105.
                      doi: 10.1016/j.actbio.2016.04.019pubmed: 27090590google scholar: lookup
                    37. Beck EC, Barragan M, Tadros MH, Kiyotake EA, Acosta FM, Kieweg SL, Detamore MS. Chondroinductive Hydrogel Pastes Composed of Naturally Derived Devitalized Cartilage. Ann Biomed Eng 2016 Jun;44(6):1863-80.
                      doi: 10.1007/s10439-015-1547-5pubmed: 26744243google scholar: lookup
                    38. Song J, Rindone AN, Guan Y, Daswani PS, Elisseeff JH, Gerecht S. Matrix stiffness induces endothelial network senescence. bioRxiv 2025 Oct 6;.
                      doi: 10.1101/2025.10.05.680536pubmed: 41278992google scholar: lookup
                    39. Firoozi S, Ley JC, Chasse DAD, Attarian DE, Wellman SS, Amendola A, McNulty AL. Healthy but not osteoarthritic human meniscus-derived matrix scaffolds promote meniscus repair. Front Bioeng Biotechnol 2024;12:1495015.
                      doi: 10.3389/fbioe.2024.1495015pubmed: 39534671google scholar: lookup
                    40. Lu P, Ruan D, Huang M, Tian M, Zhu K, Gan Z, Xiao Z. Harnessing the potential of hydrogels for advanced therapeutic applications: current achievements and future directions. Signal Transduct Target Ther 2024 Jul 1;9(1):166.
                      doi: 10.1038/s41392-024-01852-xpubmed: 38945949google scholar: lookup
                    41. Gadre M, Kasturi M, Agarwal P, Vasanthan KS. Decellularization and Their Significance for Tissue Regeneration in the Era of 3D Bioprinting. ACS Omega 2024 Feb 20;9(7):7375-7392.
                      doi: 10.1021/acsomega.3c08930pubmed: 38405516google scholar: lookup
                    42. De Castilho T, Rosa GDS, Stievani FC, Apolônio EVP, Pfeifer JPH, Altheman VG, Palialogo V, Santos NJD, Fonseca-Alves CE, Alves ALG. Biocompatibility of hydrogel derived from equine tendon extracellular matrix in horses subcutaneous tissue. Front Bioeng Biotechnol 2023;11:1296743.
                      doi: 10.3389/fbioe.2023.1296743pubmed: 38260745google scholar: lookup
                    43. Elomaa L, Almalla A, Keshi E, Hillebrandt KH, Sauer IM, Weinhart M. Rise of tissue- and species-specific 3D bioprinting based on decellularized extracellular matrix-derived bioinks and bioresins. Biomater Biosyst 2023 Dec;12:100084.
                      doi: 10.1016/j.bbiosy.2023.100084pubmed: 38035034google scholar: lookup
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