Endochondral bone formation in gelatin methacrylamide hydrogel with embedded cartilage-derived matrix particles

Biomaterials

Volumn 37, Issue , 2015, Pages 174-182

  Visser, Jetze ^a   Gawlitta, Debby ^a   Benders, Kim E M ^a   Toma, Selynda M H ^a   Pouran, Behdad ^a,b   van Weeren, P René ^c   Dhert, Wouter J A ^a,c   Malda, Jos ^a,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Decellularized matrix; GelMA; Rat; Regeneration; Tissue engineering

Indexed keywords

BIOMINERALIZATION; CARTILAGE; CELL CULTURE; FLOWCHARTING; HYDROGELS; RATING; RATS; TISSUE; TISSUE ENGINEERING; TISSUE REGENERATION;

BONE TISSUE ENGINEERING; DECELLULARIZED MATRICES; DEGRADABLE HYDROGEL; GELMA; MATRIX FORMATION; MINERALIZED BONE; REGENERATION; STANDARD DEVIATION;

BONE;

GELATIN METHACRYLAMIDE HYDROGEL; POLYACRYLAMIDE GEL; UNCLASSIFIED DRUG; ACRYLAMIDE DERIVATIVE; GELATIN; HYDROGEL; METHACRYLAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; ENCHONDRAL OSSIFICATION; HISTOLOGY; HYDROGEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; RAT; STROMA CELL; TISSUE ENGINEERING; ANIMAL; BONE DEVELOPMENT; CARTILAGE; CELL DIFFERENTIATION; CELL SURVIVAL; CHONDROGENESIS; CYTOLOGY; DRUG EFFECTS; EXTRACELLULAR MATRIX; HORSE; MALE; MESENCHYMAL STROMA CELL; METABOLISM; MICRO-COMPUTED TOMOGRAPHY; NUDE RAT; PHARMACOLOGY; PIG;

RATTUS;

ACRYLAMIDES; ANIMALS; CARTILAGE; CELL DIFFERENTIATION; CELL SURVIVAL; CHONDROCYTES; CHONDROGENESIS; EXTRACELLULAR MATRIX; GELATIN; HORSES; HYDROGEL; MALE; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; RATS; RATS, NUDE; SUS SCROFA; X-RAY MICROTOMOGRAPHY;

EID: 84922219247     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.10.020     Document Type: Article

References (48)

1. Gawlitta D., Farrell E., Malda J., Creemers L.B., Alblas J., Dhert W.J. Modulating endochondral ossification of multipotent stromal cells for bone regeneration. Tissue Eng Part B Rev 2010, 16:385-395.
2. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
3. Scammell B.E., Roach H.I. Anew role for the chondrocyte in fracture repair: endochondral ossification includes direct bone formation by former chondrocytes. JBone Min Res 1996, 11:737-745.
4. Mackie E.J., Tatarczuch L., Mirams M. The skeleton: a multi-functional complex organ: the growth plate chondrocyte and endochondral ossification. JEndocrinol 2011, 211:109-121.
5. Ma J., Both S.K., Yang F., Cui F.Z., Pan J., Meijer G.J., et al. Concise review: cell-based strategies in bone tissue engineering and regenerative medicine. Stem Cells Transl Med 2014, 3:98-107.
6. Dawson J.I., Kanczler J., Tare R., Kassem M., Oreffo R.C. Bridging the gap: bone regeneration using skeletal stem cell-based strategies - where are we now?. Stem Cells 2013, 32:35-44.
7. Kolesky D.B., Truby R.L., Gladman A.S., Busbee T.A., Homan K.A., Lewis J.A. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 2014, 26:3124-3130.
8. Miller J.S., Stevens K.R., Yang M.T., Baker B.M., Nguyen D.H., Cohen D.M., et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 2012, 11:768-774.
9. Hirao M., Tamai N., Tsumaki N., Yoshikawa H., Myoui A. Oxygen tension regulates chondrocyte differentiation and function during endochondral ossification. JBiol Chem 2006, 281:31079-31092.
10. Grimshaw M.J., Mason R.M. Bovine articular chondrocyte function invitro depends upon oxygen tension. Osteoarthr Cartil 2000, 8:386-392.
11. 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.
12. Pelttari K., Winter A., Steck E., Goetzke K., Hennig T., Ochs B.G., et al. Premature induction of hypertrophy during invitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum 2006, 54:3254-3266.
13. Farrell E., Both S.K., Odorfer K.I., Koevoet W., Kops N., O'Brien F.J., et al. In-vivo generation of bone via endochondral ossification by in-vitro chondrogenic priming of adult human and rat mesenchymal stem cells. BMC Musculoskelet Disord 2011, 12:31.
14. van der Stok J., Koolen M.K., Jahr H., Kops N., Waarsing J.H., Weinans H., et al. Chondrogenically differentiated mesenchymal stromal cell pellets stimulate endochondral bone regeneration in critical-sized bone defects. Eur Cell Mater 2014, 27:137-148.
15. Bahney C.S., Hu D.P., Taylor A.J., Ferro F., Britz H.M., Hallgrimsson B., et al. Stem cell-derived endochondral cartilage stimulates bone healing by tissue transformation. JBone Min Res 2014, 29:1269-1282.
16. Harada N., Watanabe Y., Sato K., Abe S., Yamanaka K., Sakai Y., et al. Bone regeneration in a massive rat femur defect through endochondral ossification achieved with chondrogenically differentiated MSCs in a degradable scaffold. Biomaterials 2014, 35:7800-7810.
17. Janicki P., Kasten P., Kleinschmidt K., Luginbuehl R., Richter W. Chondrogenic pre-induction of human mesenchymal stem cells on beta-TCP: enhanced bone quality by endochondral heterotopic bone formation. Acta Biomater 2010, 6:3292-3301.
18. Benders K.E.M., van Weeren P.R., Badylak S.F., Saris D.B.F., Dhert W.J.A., Malda J. Extracellular matrix scaffolds for cartilage and bone regeneration. Trends Biotechnol 2013, 31:169-176.
19. Benders K.E.M., Boot W., van Weeren P.R., Gawlitta D., Bergman H.J., Saris D.B.F., et al. Multipotent stromal cells outperform chondrocytes on cartilage-derived matrix scaffolds. Cartilage 2014, 10.1177/1947603514535245.
20. DeForest C.A., Anseth K.S. Advances in bioactive hydrogels to probe and direct cell fate. Annu Rev Chem Biomol Eng 2012, 3:421-444.
21. Sheehy E.J., Vinardell T., Buckley C.T., Kelly D.J. Engineering osteochondral constructs through spatial regulation of endochondral ossification. Acta Biomater 2013, 9:5484-5492.
22. Malda J., Visser J., Melchels F.P., Jungst T., Hennink W.E., Dhert W.J., et al. 25th anniversary article: engineering hydrogels for biofabrication. Adv Mater 2013, 25:5011-5028.
23. Levett P.A., Melchels F.P., Schrobback K., Hutmacher D.W., Malda J., Klein T.J. Abiomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate. Acta Biomater 2014, 10:214-223.
24. Schuurman W., Levett P.A., Pot M.W., van Weeren P.R., Dhert W.J., Hutmacher D.W., et al. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol Biosci 2013, 13:551-561.
25. Benton J.A., DeForest C.A., Vivekanandan V., Anseth K.S. Photocrosslinking of gelatin macromers to synthesize porous hydrogels that promote valvular interstitial cell function. Tissue Eng Part A 2009, 15:3221-3230.
26. Nichol J.W., Koshy S.T., Bae H., Hwang C.M., Yamanlar S., Khademhosseini A. Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 2010, 31:5536-5544.
27. Chen Y.C., Lin R.Z., Qi H., Yang Y., Bae H., Melero-Martin J.M., et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater 2012, 22:2027-2039.
28. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
29. Gawlitta D., van Rijen M.H., Schrijver E.J., Alblas J., Dhert W.J. Hypoxia impedes hypertrophic chondrogenesis of human multipotent stromal cells. Tissue Eng Part A 2012, 18:1957-1966.
30. Van Den Bulcke A.I., Bogdanov B., De Rooze N., Schacht E.H., Cornelissen M., Berghmans H. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules 2000, 1:31-38.
31. van Gaalen S.M., Kruyt M.C., Geuze R.E., de Bruijn J.D., Alblas J., Dhert W.J. Use of fluorochrome labels in invivo bone tissue engineering research. Tissue Eng Part B Rev 2010, 16:209-217.
32. Hildebrand T., Laib A., Muller R., Dequeker J., Ruegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. JBone Min Res 1999, 14:1167-1174.
33. Kruyt M.C., Dhert W.J., Oner F.C., van Blitterswijk C.A., Verbout A.J., de Bruijn J.D. Analysis of ectopic and orthotopic bone formation in cell-based tissue-engineered constructs in goats. Biomaterials 2007, 28:1798-1805.
34. Kruyt M., De Bruijn J., Rouwkema J., Van Bliterswijk C., Oner C., Verbout A., et al. Analysis of the dynamics of bone formation, effect of cell seeding density, and potential of allogeneic cells in cell-based bone tissue engineering in goats. Tissue Eng Part A 2008, 14:1081-1088.
35. Badylak S.F., Brown B.N., Gilbert T.W., Daly K.A., Huber A., Turner N.J. Biologic scaffolds for constructive tissue remodeling. Biomaterials 2011, 32:316-319.
36. Badylak S.F., Freytes D.O., Gilbert T.W. Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 2009, 5:1-13.
37. Chun S.Y., Lim G.J., Kwon T.G., Kwak E.K., Kim B.W., Atala A., et al. Identification and characterization of bioactive factors in bladder submucosa matrix. Biomaterials 2007, 28:4251-4256.
38. Voytik-Harbin S.L., Brightman A.O., Kraine M.R., Waisner B., Badylak S.F. Identification of extractable growth factors from small intestinal submucosa. JCell Biochem 1997, 67:478-491.
39. Chen C.C., Liao C.H., Wang Y.H., Hsu Y.M., Huang S.H., Chang C.H., et al. Cartilage fragments from osteoarthritic knee promote chondrogenesis of mesenchymal stem cells without exogenous growth factor induction. JOrthop Res 2012, 30:393-400.
40. Xue J.X., Gong Y.Y., Zhou G.D., Liu W., Cao Y., Zhang W.J. Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells induced by acellular cartilage sheets. Biomaterials 2012, 33:5832-5840.
41. Fichter M., Korner U., Schomburg J., Jennings L., Cole A.A., Mollenhauer J. Collagen degradation products modulate matrix metalloproteinase expression in cultured articular chondrocytes. JOrthop Res 2006, 24:63-70.
42. Klatt A.R., Paul-Klausch B., Klinger G., Kuhn G., Renno J.H., Banerjee M., et al. Acritical role for collagen II in cartilage matrix degradation: collagen II induces pro-inflammatory cytokines and MMPs in primary human chondrocytes. JOrthop Res 2009, 27:65-70.
43. Vonk L.A., Doulabi B.Z., Huang C., Helder M.N., Everts V., Bank R.A. Preservation of the chondrocyte's pericellular matrix improves cell-induced cartilage formation. JCell Biochem 2010, 110:260-271.
44. 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.
45. Mastbergen S.C., Saris D.B., Lafeber F.P. Functional articular cartilage repair: here, near, or is the best approach not yet clear?. Nat Rev Rheumatol 2013, 9:277-290.
46. de Windt T.S., Hendriks J.A., Zhao X., Vonk L.A., Creemers L.B., Dhert W.J., et al. Concise review: unraveling stem cell cocultures in regenerative medicine: which cell interactions steer cartilage regeneration and how?. Stem Cells Transl Med 2014, 3:723-733.
47. Billiet T., Gevaert E., De Schryver T., Cornelissen M., Dubruel P. The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials 2014, 35:49-62.
48. Visser J., Peters B., Burger T.J., Boomstra J., Dhert W., Melchels F., et al. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication 2013, 5:035007.