In vitro cartilage tissue engineering with 3D porous aqueous-derived silk scaffolds and mesenchymal stem cells

Biomaterials

Volumn 26, Issue 34, 2005, Pages 7082-7094

  Wang, Yongzhong ^a   Kim, Ung Jin ^b   Blasioli, Dominick J ^a   Kim, Hyeon Joo ^a   Kaplan, David L ^a  

^a Tufts University   (United States)

^b Samsung Fine Chemicals Co   (South Korea)

Author keywords

Aqueous derived silk scaffold; Cartilage tissue engineering; Mesenchymal stem cell; MSC

Indexed keywords

BIOCOMPATIBILITY; BONE; CARTILAGE; CELLS; COLLAGEN; DEGRADATION; SCAFFOLDS;

CARTILAGE TISSUE ENGINEERING; MESENCHYMAL STEM CELLS (MSC); OSTEOARTHRITIS; SILK SCAFFOLD;

TISSUE;

DEXAMETHASONE; SILK FIBROIN; TRANSFORMING GROWTH FACTOR BETA3;

ADULT; ARTICLE; CARTILAGE; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHONDROGENESIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FILM; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; POROSITY; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; TISSUE ENGINEERING;

ADULT; BIOCOMPATIBLE MATERIALS; CARTILAGE; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; HUMANS; MATERIALS TESTING; MEMBRANES, ARTIFICIAL; MESENCHYMAL STEM CELLS; POROSITY; SILK; SURFACE PROPERTIES; TISSUE ENGINEERING;

EID: 23244455905     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2005.05.022     Document Type: Article

References (68)

1. T. Aigner, and J. Stove Collagens - major component of the physiological cartilage matrix, major target of cartilage degeneration, major tool in cartilage repair Adv Drug Deliv Rev 55 2003 1569 1593
2. R.S. Tuan, G. Boland, and R. Tuli Adult mesenchymal stem cells and cell-based tissue engineering Arthritis Res Ther 5 2003 32 45
3. M. Brittberg, A. Lindahl, A. Nilsson, C. Ohlsson, O. Isaksson, and L. Peterson Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation N Engl J Med 331 1994 889 895
4. A. Lindahl, M. Brittberg, and L. Peterson Cartilage repair with chondrocytes: clinical and cellular aspects Novartis Found Symp 249 2003 175 186 (discussion 186-9, 234-8, 239-41)
5. S. Wakitani, T. Goto, S.J. Pineda, R.G. Young, J.M. Mansour, A.I. Caplan, and V.M. Goldberg Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage J Bone J Surg Am 76 1994 579 592
6. S. Wakitani, K. Imoto, T. Yamamoto, M. Saito, N. Murata, and M. Yoneda Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees Osteoarthritis Cartilage 10 2002 199 206
7. B. Johnstone, T.M. Hering, A.I. Caplan, V.M. Goldberg, and J.U. Yoo In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells Exp Cell Res 238 1998 265 272
8. A.M. DeLise, L. Fischer, and R.S. Tuan Cellular interactions and signaling in cartilage development Osteoarthritis Cartilage 8 2000 309 334
9. A.M. DeLise, E. Stringa, W.A. Woodward, M.A. Mello, and R.S. Tuan Embryonic limb mesenchyme micromass culture as an in vitro model for chondrogenesis and cartilage maturation Methods Mol Biol 137 2000 359 375
10. B. de Crombrugghe, V. Lefebvre, R.R. Behringer, W. Bi, S. Murakami, and W. Huang Transcriptional mechanisms of chondrocyte differentiation Matrix Biol 19 2000 389 394
11. M. Radice, P. Brun, R. Cortivo, R. Scapinelli, C. Battaliard, and G. Abatangelo Hyaluronan-based biopolymers as delivery vehicles for bone-marrow-derived mesenchymal progenitors J Biomed Mater Res 50 2000 101 109
12. W.J. Li, R. Tuli, C. Okafor, A. Derfoul, K.G. Danielson, D.J. Hall, and R.S. Tuan A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells Biomaterials 26 2005 599 609
13. C.Y. Huang, P.M. Reuben, G. D'Ippolito, P.C. Schiller, and H.S. Cheung Chondrogenesis of human bone marrow-derived mesenchymal stem cells in agarose culture Anat Rec 278A 2004 428 436
14. G. Vunjak-Novakovic, B. Obradovic, I. Martin, P.M. Bursac, R. Langer, and L.E. Freed Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering Biotechnol Prog 14 1998 193 202
15. P. Angele, R. Kujat, M. Nerlich, J. Yoo, V. Goldberg, and B. Johnstone Engineering of osteochondral tissue with bone marrow mesenchymal progenitor cells in a derivatized hyaluronan-gelatin composite sponge Tissue Eng 5 1999 545 554
16. E.J. Caterson, L.J. Nesti, W.J. Li, K.G. Danielson, T.J. Albert, A.R. Vaccaro, and R.S. Tuan Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam J Biomed Mater Res 57 2001 394 403
17. M.S. Ponticiello, R.M. Schinagl, S. Kadiyala, and F.P. Barry Gelatin-based resorbable sponge as a carrier matrix for human mesenchymal stem cells in cartilage regeneration therapy J Biomed Mater Res 52 2000 246 255
18. C.G. Williams, T.K. Kim, A. Taboas, A. Malik, P. Manson, and J. Elisseeff In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel Tissue Eng 9 2003 679 688
19. D.R. Diduch, L.C. Jordan, C.M. Mierisch, and G. Balian Marrow stromal cells embedded in alginate for repair of osteochondral defects Arthroscopy 16 2000 571 577
20. L.A. Solchaga, J.E. Dennis, V.M. Goldberg, and A.I. Caplan Hyaluronic acid-based polymers as cell carriers for tissue-engineered repair of bone and cartilage J Orthop Res 17 1999 205 213
21. U. Noth, R. Tuli, A.M. Osyczka, K.G. Danielson, and R.S. Tuan In vitro engineered cartilage constructs produced by press-coating biodegradable polymer with human mesenchymal stem cells Tissue Eng 8 2002 131 144
22. C. Wong Po Foo, and D.L. Kaplan Genetic engineering of fibrous proteins: spider dragline silk and collagen Adv Drug Deliv Rev 54 2002 1131 1143
23. G.H. Altman, F. Diaz, C. Jakuba, T. Calabro, R.L. Horan, J. Chen, H. Lu, J. Richmond, and D.L. Kaplan Silk-based biomaterials Biomaterials 24 2003 401 416
24. G.H. Altman, R.L. Horan, H.H. Lu, J. Moreau, I. Martin, J.C. Richmond, and D.L. Kaplan Silk matrix for tissue engineered anterior cruciate ligaments Biomaterials 23 2002 4131 4141
25. H.J. Jin, and D.L. Kaplan Mechanism of silk processing in insects and spiders Nature 424 2003 1057 1061
26. H.J. Jin, S.V. Fridrikh, G.C. Rutledge, and D.L. Kaplan Electrospinning Bombyx mori silk with poly(ethylene oxide) Biomacromolecules 3 2002 1233 1239
27. G.H. Altman, R.L. Horan, I. Martin, J. Farhadi, P.R. Stark, V. Volloch, J.C. Richmond, G. Vunjak-Novakovic, and D.L. Kaplan Cell differentiation by mechanical stress Faseb J 16 2002 270 272
28. G.H. Altman, H.H. Lu, R.L. Horan, T. Calabro, D. Ryder, D.L. Kaplan, P. Stark, I. Martin, J.C. Richmond, and G. Vunjak-Novakovic Advanced bioreactor with controlled application of multi-dimensional strain for tissue engineering J Biomech Eng 124 2002 742 749
29. J. Chen, G.H. Altman, V. Karageorgiou, R. Horan, A. Collette, V. Volloch, T. Colabro, and D.L. Kaplan Human bone marrow stromal cell and ligament fibroblast responses on RGD-modified silk fibers J Biomed Mater Res 67A 2003 559 570
30. L. Meinel, S. Hofmann, V. Karageorgiou, L. Zichner, R. Langer, D. Kaplan, and G. Vunjak-Novakovic Engineering cartilage-like tissue using human mesenchymal stem cells and silk protein scaffolds Biotechnol Bioeng 88 2004 379 391
31. L. Meinel, V. Karageorgiou, R. Fajardo, B. Snyder, V. Shinde-Patil, L. Zichner, D. Kaplan, R. Langer, and G. Vunjak-Novakovic Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow Ann Biomed Eng 32 2004 112 122
32. L. Meinel, V. Karageorgiou, S. Hofmann, R. Fajardo, B. Snyder, C. Li, L. Zichner, R. Langer, G. Vunjak-Novakovic, and D.L. Kaplan Engineering bone-like tissue in vitro using human bone marrow stem cells and silk scaffolds J Biomed Mater Res 71A 2004 25 34
33. J. Kim U-, J. Park, H.J. Kim, M. Wada, and D.L. Kaplan Three-dimensional aqueous-derived biomaterial scaffolds from silk fibroin Biomaterials 26 2005 4442 4452
34. H.J. Kim, U.J. Kim, G. Vunjak-Novakovic, H. Min B-, and D.L. Kaplan Influence of macroporous protein scaffolds on bone tissue engineering from bone marrow stem cells Biomaterials 26 2005 4442 4452
35. S.A. Ahmed, R.M. Gogal Jr., and J.E. Walsh A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3 H]thymidine incorporation assay J Immunol Methods 170 1994 211 224
36. A.M. Mackay, S.C. Beck, J.M. Murphy, F.P. Barry, C.O. Chichester, and M.F. Pittenger Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow Tissue Eng 4 1998 415 428
37. F. Barry, R.E. Boynton, B. Liu, and J.M. Murphy Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation- dependent gene expression of matrix components Exp Cell Res 268 2001 189 200
38. I. Martin, R.F. Padera, G. Vunjak-Novakovic, and L.E. Freed In vitro differentiation of chick embryo bone marrow stromal cells into cartilaginous and bone-like tissues J Orthop Res 16 1998 181 189
39. D.A. Grande, C. Halberstadt, G. Naughton, R. Schwartz, and R. Manji Evaluation of matrix scaffolds for tissue engineering of articular cartilage grafts J Biomed Mater Res 34 1997 211 220
40. L.E. Freed, J.C. Marquis, A. Nohria, J. Emmanual, A.G. Mikos, and R. Langer Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers J Biomed Mater Res 27 1993 11 23
41. L.E. Freed, G. Vunjak-Novakovic, R.J. Biron, D.B. Eagles, D.C. Lesnoy, S.K. Barlow, and R. Langer Biodegradable polymer scaffolds for tissue engineering Biotechnology (NY) 12 1994 689 693
42. L.E. Freed, G. Vunjak-Novakovic, and R. Langer Cultivation of cell-polymer cartilage implants in bioreactors J Cell Biochem 51 1993 257 264
43. C. Perka, O. Schultz, R.S. Spitzer, and K. Lindenhayn The influence of transforming growth factor beta 1 on mesenchymal cell repair of full-thickness cartilage defects J Biomed Mater Res 52 2000 543 552
44. C. Perka, R.S. Spitzer, K. Lindenhayn, M. Sittinger, and O. Schultz Matrix-mixed culture: new methodology for chondrocyte culture and preparation of cartilage transplants J Biomed Mater Res 49 2000 305 311
45. K.T. Paige, L.G. Cima, M.J. Yaremchuk, B.L. Schloo, J.P. Vacanti, and C.A. Vacanti De novo cartilage generation using calcium alginate-chondrocyte constructs Plast Reconstr Surg 97 1996 168 178 discussion 179-80
46. E. Fragonas, M. Valente, M. Pozzi-Mucelli, R. Toffanin, R. Rizzo, F. Silvestri, and F. Vittur Articular cartilage repair in rabbits by using suspensions of allogenic chondrocytes in alginate Biomaterials 21 2000 795 801
47. J.F. Guo, G.W. Jourdian, and D.K. MacCallum Culture and growth characteristics of chondrocytes encapsulated in alginate beads Connect Tissue Res 19 1989 277 297
48. M. Weber, A. Steinert, A. Jork, A. Dimmler, F. Thurmer, N. Schutze, C. Hendrich, and U. Zimmerman Formation of cartilage matrix proteins by BMP-transfected murine mesenchymal stem cells encapsulated in a novel class of alginates Biomaterials 23 2002 2003 2013
49. S.S. Mok, K. Masuda, H.J. Hauselmann, M.B. Aydelotte, and E.J. Thonar Aggrecan synthesized by mature bovine chondrocytes suspended in alginate. Identification of two distinct metabolic matrix pools J Biol Chem 269 1994 33021 33027
50. H.J. Hauselmann, L. Oppliger, B.A. Michel, M. Stefanovic-Racic, and C.H. Evans Nitric oxide and proteoglycan biosynthesis by human articular chondrocytes in alginate culture FEBS Lett 352 1994 361 364
51. H.J. Hauselmann, R.J. Fernandes, S.S. Mok, T.M. Schmid, J.A. Block, M.B. Aydelotte, K.E. Kuettner, and E.J. Thonar Phenotypic stability of bovine articular chondrocytes after long-term culture in alginate beads J Cell Sci 107 Pt 1 1994 17 27
52. W.J. Marijnissen, G.J. van Osch, J. Aigner, S.W. van der Veen, A.P. Hollander, H.L. Verwoerd-Verhoef, and J.A. Verhaar Alginate as a chondrocyte-delivery substance in combination with a non-woven scaffold for cartilage tissue engineering Biomaterials 23 2002 1511 1517
53. H.L. Ma, S.C. Hung, S.Y. Lin, Y.L. Chen, and W.H. Lo Chondrogenesis of human mesenchymal stem cells encapsulated in alginate beads J Biomed Mater Res 64A 2003 273 281
54. R. Cancedda, B. Dozin, P. Giannoni, and R. Quarto Tissue engineering and cell therapy of cartilage and bone Matrix Biol 22 2003 81 91
55. K.A. Athanasiou, G.G. Niederauer, and C.M. Agrawal Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/polyglycolic acid copolymers Biomaterials 17 1996 93 102
56. E.B. Hunziker Articular cartilage repair: basic science and clinical progress A review of the current status and prospects. Osteoarthritis and Cartilage 10 2002 432 463
57. L. Meinel, S. Hofmann, V. Karageorgiou, C. Kirker-Head, J. McCool, G. Gronowicz, L. Zichner, R. Langer, G. Vunjak-Novakovic, and D.L. Kaplan The inflammatory responses to silk films in vitro and in vivo Biomaterials 26 2005 147 155
58. K. von der Mark, V. Gauss, H. von der Mark, and P. Muller Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture Nature 267 1977 531 532
59. P.D. Benya, and J.D. Shaffer Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels Cell 30 1982 215 224
60. J. Bonaventure, N. Kadhom, L. Cohen-Solal, K.H. Ng, J. Bourguignon, C. Lasselin, and P. Freisinger Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads Exp Cell Res 212 1994 97 104
61. L.E. Freed, A.P. Hollander, I. Martin, J.R. Barry, R. Langer, and G. Vunjak-Novakovic Chondrogenesis in a cell-polymer-bioreactor system Exp Cell Res 240 1998 58 65
62. Chen J, Horan R, Bramono D, Moreau JE, Wang Y, Geuss LR, Schilling J, Venjak-Novakovic G, Volloch V, Kaplan DL, Altman GH, in preparation.
63. G.S. Stein, J.B. Lian, and T.A. Owen Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation Faseb J 4 1990 3111 3123
64. G.S. Stein, J.B. Lian, L.G. Gerstenfeld, V. Shalhoub, M. Aronow, T. Owen, and E. Markose The onset and progression of osteoblast differentiation is functionally related to cellular proliferation Connect Tissue Res 20 1989 3 13
65. M. Solursh Formation of cartilage tissue in vitro J Cell Biochem 45 1991 258 260
66. K.R. Brodkin, A.J. Garcia, and M.E. Levenston Chondrocyte phenotypes on different extracellular matrix monolayers Biomaterials 25 2004 5929 5938
67. M.J. Grimshaw, and R.M. Mason Bovine articular chondrocyte function in vitro depends upon oxygen tension Osteoarthritis Cartilage 8 2000 386 392
68. U. Hansen, M. Schunke, C. Domm, N. Ioannidis, J. Hassenpflug, T. Gehrke, and B. Kurz Combination of reduced oxygen tension and intermittent hydrostatic pressure: a useful tool in articular cartilage tissue engineering J Biomech 34 2001 941 949