Engineering endostatin-expressing cartilaginous constructs using injectable biopolymer hydrogels

Acta Biomaterialia

Volumn 8, Issue 6, 2012, Pages 2203-2212

  Jeng, Lily ^a,b   Olsen, Bjorn R ^c   Spector, Myron ^a,d  

^a VA BOSTON HEALTHCARE SYSTEM   (United States)

^b Massachusetts Institute of Technology   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cartilage tissue engineering; Gene therapy; Mesenchymal stem cell; Scaffold

Indexed keywords

CARTILAGE; CELL CULTURE; CELL ENGINEERING; CROSSLINKING; GENE THERAPY; HYDROGELS; MOLECULAR BIOLOGY; MOLECULES; REPAIR; SCAFFOLDS (BIOLOGY); STEM CELLS; SULFUR COMPOUNDS;

ARTICULAR CARTILAGES; BASEMENT MEMBRANE; CARTILAGE TISSUE ENGINEERING; ENDOSTATINS; GENIPIN; IN-VIVO; INJECTABLES; MESENCHYMAL STEM CELL; MICROBIAL TRANSGLUTAMINASE; TRANSGLUTAMINASE 2;

COLLAGEN;

BIOPOLYMER; CHONDROITIN SULFATE; COLLAGEN; COLLAGEN GEL; COLLAGEN TYPE 18; COLLAGEN TYPE 4; ENDOSTATIN; GENIPIN; HEPARAN SULFATE; HEPARIN; LAMININ; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2;

ANIMAL CELL; ARTICLE; ARTICULAR CARTILAGE; BASEMENT MEMBRANE; CARTILAGE; CHONDROGENESIS; CONTROLLED STUDY; COVALENT BOND; CROSS LINKING; GOAT; HYDROGEL; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE ENGINEERING;

EID: 84860539245     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.02.015     Document Type: Article

References (45)

1. M. Yin, and M. Pacifici Vascular regression is required for mesenchymal condensation and chondrogenesis in the developing limb Dev Dyn 222 2001 522 533
2. S.A. Fenwick, P.J. Gregg, and P. Rooney Osteoarthritic cartilage loses its ability to remain avascular Osteoarthritis Cartilage 7 1999 441 452
3. S. Kubo, G.M. Cooper, T. Matsumoto, J.A. Phillippi, K.A. Corsi, and A. Usas Blocking vascular endothelial growth factor with soluble Flt-1 improves the chondrogenic potential of mouse skeletal muscle-derived stem cells Arthritis Rheum 60 2009 155 165
4. T. Matsumoto, G.M. Cooper, B. Gharaibeh, L.B. Meszaros, G. Li, and A. Usas Cartilage repair in a rat model of osteoarthritis through intraarticular transplantation of muscle-derived stem cells expressing bone morphogenetic protein 4 and soluble Flt-1 Arthritis Rheum 60 2009 1390 1405
5. X.-D. Sun, L. Jeng, C. Bolliet, B.R. Olsen, and M. Spector Non-viral endostatin plasmid transfection of mesenchymal stem cells via collagen scaffolds Biomaterials 30 2009 1222 1231
6. L. Jeng, B.R. Olsen, and M. Spector Engineering endostatin-producing cartilaginous constructs for cartilage repair using nonviral transfection of chondrocyte-seeded and mesenchymal-stem-cell-seeded collagen scaffolds Tissue Eng Part A 16 2010 3011 3021
7. M.M. Stevens, R.P. Marini, D. Schaefer, J. Aronson, R. Langer, and V.P. Shastri In vivo engineering of organs: the bone bioreactor Proc Natl Acad Sci USA 102 2005 11450 11455
8. M.S. OReilly, T. Boehm, Y. Shing, N. Fukai, G. Vasios, and W.S. Lane Endostatin: an endogenous inhibitor of angiogenesis and tumor growth Cell 88 1997 277 285
9. J. Stempel, H. Fritsch, K. Pfaller, and M.J. Blumer Development of articular cartilage and the metaphyseal growth plate: the localization of TRAP cells, VEGF, and endostatin J Anat 218 2011 608 618
10. T. Pufe, W.J. Petersen, N. Miosge, M.B. Goldring, R. Mentlein, and D.J. Varoga Endostatin/collagen XVIII - an inhibitor of angiogenesis - is expressed in cartilage and fibrocartilage Matrix Biol 23 2004 267 276
11. Y. Feng, Y.P. Wu, X.D. Zhu, Y.H. Zhang, and Q.J. Ma Endostatin promotes the anabolic program of rabbit chondrocyte Cell Res 15 2005 201 206
12. H.G. Sundararaghavan, G.A. Monteiro, N.A. Lapin, Y.J. Chabal, J.R. Miksan, and D.I. Shreiber Genipin-induced changes in collagen gels: correlation of mechanical properties to fluorescence J Biomed Mater Res Part A 87A 2008 308 320
13. Y.S. Pek, M. Spector, I.V. Yannas, and L.J. Gibson Degradation of a collagen-chondroltin-6-sulfate matrix by collagenase and by chondroitinase Biomaterials 25 2004 473 482
14. C. Faye, A. Inforzato, M. Bignon, D.J. Hartmann, L. Muller, and L. Ballut Transglutaminase-2: a new endostatin partner in the extracellular matrix of endothelial cells Biochem J 427 2010 467 475
15. T. Kashiwagi, K. Yokoyama, K. Ishikawa, K. Ono, D. Ejima, and H. Matsui Crystal structure of microbial transglutaminase from Streptoverticillium mobaraense J Biol Chem 277 2002 44252 44260
16. M.K. McHale, L.A. Setton, and A. Chilkoti Synthesis and in vitro evaluation of enzymatically cross-linked elastin-like polypeptide gels for cartilaginous tissue repair Tissue Eng 11 2005 1768 1779
17. E.G. Lima, A.R. Tan, T. Tai, K.G. Marra, A. DeFail, and G.A. Ateshian Genipin enhances the mechanical properties of tissue-engineered cartilage and protects against inflammatory degradation when used as a medium supplement J Biomed Mater Res Part A 91A 2009 692 700
18. E.V. Dare, M. Griffith, P. Poitras, J.A. Kaupp, S.D. Waldman, and D.J. Carlsson Genipin cross-linked fibrin hydrogels for in vitro human articular cartilage tissue-engineered regeneration Cells Tissues Organs 190 2009 313 325
19. L. Zheng, H.S. Fan, J. Sun, X.N. Chen, G. Wang, and L. Zhang Chondrogenic differentiation of mesenchymal stem cells induced by collagen-based hydrogel: an in vivo study J Biomed Mater Res A 93 2010 783 792
20. H.A. Breinan, S.D. Martin, H.P. Hsu, and M. Spector Healing of canine articular cartilage defects treated with microfracture, a type-II collagen matrix, or cultured autologous chondrocytes J Orthop Res 18 2000 781 789
21. A. Sommer, and D.B. Rifkin Interaction of heparin with human basic fibroblast growth-factor - protection of the angiogenic protein from proteolytic degradation by a glycosaminoglycan J Cell Physiol 138 1989 215 220
22. J.S. Pieper, T. Hafmans, P.B. van Wachem, M.J.A. van Luyn, L.A. Brouwer, and J.H. Veerkamp Loading of collagen-heparan sulfate matrices with bFGF promotes angiogenesis and tissue generation in rats J Biomed Mater Res 62 2002 185 194
23. S. Ricard-Blum, O. Feraud, H. Lortat-Jacob, A. Rencurosi, N. Fukai, and F. Dkhissi Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling - role of divalent cations J Biol Chem 279 2004 2927 2936
24. T. Sasaki, H. Larsson, J. Kreuger, M. Salmivirta, L. Claesson-Welsh, and U. Lindahl Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin Embo J 18 1999 6240 6248
25. E. Hohenester, T. Sasaki, B.R. Olsen, and R. Timpl Crystal structure of the angiogenesis inhibitor endostatin at 1.5 A resolution Embo J 17 1998 1656 1664
26. C. Faye, E. Chautard, B.R. Olsen, and S. Ricard-Blum The first draft of the endostatin interaction network J Biol Chem 284 2009 22041 22047
27. R.M. Capito, and M. Spector Collagen scaffolds for nonviral IGF-1 gene delivery in articular cartilage tissue engineering Gene Ther 14 2007 721 732
28. S.M. Vickers, L.S. Squitieri, and M. Spector Effects of cross-linking type II collagen-GAG scaffolds on chondrogenesis in vitro: dynamic pore reduction promotes cartilage formation Tissue Eng 12 2006 1345 1355
29. A.J. Kvist, A. Nystrom, K. Hultenby, T. Sasaki, J.F. Talts, and A. Aspberg The major basement membrane components localize to the chondrocyte pericellular matrix - a cartilage basement membrane equivalent? Matrix Biol 27 2008 22 33
30. S.M. Vickers, T. Gotterbarm, and M. Spector Cross-linking affects cellular condensation and chondrogenesis in type II collagen-GAG scaffolds seeded with bone marrow-derived mesenchymal stem cells J Orthop Res 28 2010 1184 1192
31. E. Pfeiffer, S.M. Vickers, E. Frank, A.J. Grodzinsky, and M. Spector The effects of glycosaminoglycan content on the compressive modulus of cartilage engineered in type II collagen scaffolds Osteoarthritis Cartilage 16 2008 1237 1244
32. M.H. Kulke, E.K. Bergsland, D.P. Ryan, P.C. Enzinger, T.J. Lynch, and A.X. Zhu Phase II study of recombinant human endostatin in patients with advanced neuroendocrine tumors J Clin Oncol 24 2006 3555 3561
33. N. Yamaguchi, B. Anand-Apte, M. Lee, T. Sasaki, N. Fukai, and R. Shapiro Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding EMBO J 18 1999 4414 4423
34. J. Melrose, S. Smith, M. Cake, R. Read, and J. Whitelock Perlecan displays variable spatial and temporal immunolocalisation patterns in the articular and growth plate cartilages of the ovine stifle joint Histochem Cell Biol 123 2005 561 571
35. F. Tesche, and N. Miosge Perlecan in late stages of osteoarthritis of the human knee joint Osteoarthritis Cartilage 12 2004 852 862
36. A. Kitano, S. Saika, O. Yamanaka, P.S. Reinach, K. Ikeda, and Y. Okada Genipin suppression of fibrogenic behaviors of the alpha-TN4 lens epithelial cell line J Cataract Refract Surg 32 2006 1727 1735
37. I.V. Yannas, J.F. Burke, P.L. Gordon, C. Huang, and R.H. Rubenstein Design of an artificial skin. 2. Control of chemical-composition J Biomed Mater Res 14 1980 107 132
38. J.C. Salamone Concise polymeric materials encyclopedia 1999 CRC Press Boca Raton, FL
39. D.L. Ellis, and I.V. Yannas Regeneration templates, artifical skin and nerves 1999 CRC Press Boca Raton, FL
40. E.N. Harris, J.A. Weigel, and P.H. Weigel The human hyaluronan receptor for endocytosis (HARE/Stabilin-2) is a systemic clearance receptor for heparin J Biol Chem 283 2008 17341 17350
41. R.E. Vilar, D. Ghael, M. Li, D.D. Bhagat, L.M. Arrigo, and M.K. Cowman Nitric oxide degradation of heparin and heparan sulphate Biochem J 324 1997 473 479
42. S. Raghuvanshi, P. Sharma, S. Singh, L. Van Kaer, and G. Das Mycobacterium tuberculosis evades host immunity by recruiting mesenchymal stem cells Proc Natl Acad Sci USA 107 2010 21653 21658
43. H.J. Kong, J. Liu, K. Riddle, T. Matsumoto, K. Leach, and D.J. Mooney Non-viral gene delivery regulated by stiffness of cell adhesion substrates Nat Mater 4 2005 460 464
44. J.C. Britt, and S.S. Park Autogenous tissue-engineered cartilage - evaluation as an implant material Arch Otolaryngol Head Neck Surg 124 1998 671 677
45. A. Abdollahi, and J. Folkman Evading tumor evasion: current concepts and perspectives of anti-angiogenic cancer therapy Drug Resist Updat 13 2010 16 28