Engineering cartilage-like tissue using human mesenchymal stem cells and silk protein scaffolds

Biotechnology and Bioengineering

Volumn 88, Issue 3, 2004, Pages 379-391

  Meinel, Lorenz ^a,b,c   Hofmann, Sandra ^c,d   Karageorgiou, Vassilis ^c   Zichner, Ludwig ^b   Langer, Robert ^a   Kaplan, David ^c   Vunjak Novakovic, Gordana ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b U H Orthoped Surg Friedrichsheim   (Germany)

^c Tufts University   (United States)

^d ETH ZURICH   (Switzerland)

Author keywords

Cartilage scaffold; In vitro; Mesenchymal stem cells; Silk; Tissue engineering

Indexed keywords

BIODEGRADATION; CELLS; DISEASES; IMMUNOLOGY; METABOLISM; PROTEINS;

DISEASE TRANSMISSION; HUMAN MESENCHYMAL STEM CELLS (HMSC); IMMUNOREJECTION;

CARTILAGE;

COLLAGEN; COLLAGEN TYPE 2; CROSS LINKED COLLAGEN; LYMPHOCYTE SURFACE MARKER; PROTEIN; SILK PROTEIN; UNCLASSIFIED DRUG;

ALLOGRAFT; ARTICLE; BIODEGRADATION; BONE DEVELOPMENT; BONE MARROW BIOPSY; CARTILAGE; CELL ADHESION; CELL CULTURE; CELL DIFFERENTIATION; CELL ISOLATION; CELL METABOLISM; CELL PROLIFERATION; CELL STRUCTURE; CHONDROGENESIS; COLLAGEN TYPE 2 GENE; CONTROLLED STUDY; CULTURE MEDIUM; DISEASE TRANSMISSION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYMAL STEM CELL; MESENCHYME CELL; POROSITY; SILK; TISSUE CULTURE; TISSUE ENGINEERING; TISSUE GRAFT;

ABSORBABLE IMPLANTS; BIOARTIFICIAL ORGANS; CARTILAGE, ARTICULAR; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; HUMANS; MATERIALS TESTING; MESENCHYMAL STEM CELLS; SILK; TISSUE ENGINEERING;

BOVINAE;

EID: 8744301723     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20252     Document Type: Article

References (52)

1. Altman GH, Horan RL, Lu HH, Moreau J, Martin I, Richmond JC, Kaplan DL. 2002. Silk matrix for tissue engineered anterior cruciate ligaments. Biomaterials 23:4131-4141.
2. Altman GH, Diaz F, Jakuba C, Calabro T, Horan R, Chen J, Lu H, Richmond J, Kaplan DL. 2003. Silk-based biomaterials. Biomaterials 24:401-416.
3. Athanasiou KA, Niederauer GG, Agrawal CM. 1996. Sterilization, toxicity, biocompatibility and clinical applications of polylactic acid/polyglycolic acid copolymers. Biomaterials 17:93-102.
4. Barry FP, Boynton RE, Haynesworth S, Murphy JM, Zaia J. 1999. The monoclonal antibody SH-2, raised against human mesenchymal stem cells, recognizes an epitope on endoglin (CD105). Biochem Biophys Res Commun 265:134-139.
5. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L. 1994. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331:889-895.
6. Caplan AI. 1994. The mesengenic process. Clin Plast Surg 21:429-435.
7. Caplan AI. 2003. Embryonic development and the principles of tissue engineering. Novartis Found Symp 249:17-25.
8. Caplan AI, Fink DJ, Bruder SP, Young RG. 1997. The regeneration of skeletal tissues using mesenchymal stem cells. In: Patrick CW Jr, Mikos AG, McIntire LV, editors. Frontiers in tissue engineering. New York: Elsevier Science.
9. Caterson EJ, Nesti LJ, Li WJ, Danielson KG, Albert TJ, Vaccaro AR, Tuan RS. 2001. Three-dimensional cartilage formation by bone marrow-derived cells seeded in polylactide/alginate amalgam. J Biomed Mater Res 57:394-403.
10. Chen J, Altman GH, Karageorgiou V, Horan R, Collette A, Volloch V, Colabro T, Kaplan DL. 2003. Human bone marrow stromal cells and ligament fibroblast responses on RGD-modified silk fibers. J Biomed Mater Res 67A:559-570.
11. DeLisser HM, Newman PJ, Albelda SM. 1993. Platelet endothelial cell adhesion molecule (CD31). Curr Top Microbiol Immunol 184:37-45.
12. Dennis JE, Merriam A, Awadallah A, Yoo JU, Johnstone B, Caplan AI. 1999. A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse. J Bone Miner Res 14:700-709.
13. Farndale RW, Buttler DJ, Barrett AJ. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by the use of dimethylmethylene blue. Biochim Biophys Acta 883:173-177.
14. Freed LE, Vunjak-Novakovic G. 2000. Tissue engineering bioreactors. In: Lanza RP, Langer R, Vacanti J, editors. Principles of tissue engineering, 2nd ed. San Diego: Academic Press, p 143-156.
15. Freed LE, Marquis JC, Nohria A, Emmanual J, Mikos AG, Langer R. 1993. Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J Biomed Mater Res 27:11-23.
16. Friedenstein AJ. 1976. Precursor cells of mechanocytes. Int Rev Cytol 47:327-359.
17. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. 1987. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 20:263-272.
18. Gatherer D, Ten Dijke P, Baird DT, Akhurst RJ. 1990. Expression of TGF-beta isoforms during first trimester human embryogenesis. Development 110:445-460.
19. Harris LD, Kim BS, Mooney DJ. 1998. Open pore biodegradable matrices formed with gas foaming. J Biomed Mater Res 42:396-402.
20. Hollinger JO, Brekke J, Gruskin E, Lee D. 1996. Role of bone substitutes. Clin Orthop Rel Res 324:55-65.
21. Jin H-J, Kaplan DL. 2003. Mechanism of silk processing in insects and spiders. Nature 424:1057-1061.
22. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. 1998. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238:265-272.
23. Judd W, Poodry CA, Strominger JL. 1980. Novel surface antigen expressed on dividing cells but absent from nondividing cells. J Exp Med 152:1430-1435.
24. Kaplan DL. 2002. Spiderless spider webs. Nat Biotechnol 20:239-240.
25. Kuhn LC, McClelland A, Ruddle FH. 1984. Gene transfer, expression, and molecular cloning of the human transferrin receptor gene. Cell 37:95-103.
26. Kulyk WM, Rodgers BJ, Greer K, Kosher RA. 1989. Promotion of embryonic chick limb cartilage differentiation by transforming growth factor b. Dev Biol 135:424-430.
27. Lange F. 1903. Über die Sehenplastik. Verb Dtsch Orthop Ges 2:10-12.
28. Lange F. 1907. Künstliche Bänder aus Seide. Münch Med Wochenschr 17:834-836.
29. Langer R, Vacanti JP. 1993. Tissue engineering. Science 260:920-926.
30. Lohmander LS. 2003. Tissue engineering of cartilage: do we need it, can we do it, is it good and can we prove it? Novartis Found Symp 249:2-10.
31. Mackay AM, Beck SC, Murphy JM, Barry FP, Chichester CO, Pittenger MF. 1998. Chondrogenic differentiation of cultured human mesenchymal stem cells from marrow. Tissue Eng 4:415-428.
32. Majumdar MK, Banks V, Peluso DP, Morris EA. 2000. Isolation, characterization, and chondrogenic potential of human bone marrow-derived multipotential stromal cells. J Cell Physiol 185:98-106.
33. Martin I, Shastri V, Padera RF, Langer R, Vunjak-Novakovic G, Freed LE. 1999. Bone marrow stromal cell differentiation on porous polymer scaffolds. Trans Orthop Res Soc 24:57.
34. Martin I, Shastri VP, Padera RF, Yang J, Mackay AJ, Langer R, Vunjak-Novakovic G, Freed LE. 2001. Selective differentiation of mammalian bone marrow stromal cells cultured on three-dimensional polymer foams. J Biomed Mater Res 55:229-235.
35. Meinel L, Karageorgiou V, Fajardo R, Snyder B, Shinde-Patil V, Zichner L, Kaplan D, Langer R, Vunjak-Novakovic G. 2004a. Bone tissue engineering using human mesenchymal stem cells: effects of scaffold material and medium flow. Ann Biomed Eng 32:112-122.
36. Meinel L, Hoffmann S, Karageorgiou V, Kirker-Head C, McCool J, Gronowicz G, Zichner L, Langer R, Vunjak-Novakovic G, Kaplan DL. 2005. The inflammatory responses to silk films in vitro and in vivo. Biomaterials 26:147-155.
37. Nazarov R, Jin HJ, Kaplan DL. 2004. Porous 3-D scaffolds from regenerated silk fibroin. Biomacromolecules 5:718-726.
38. Negrin RS, Atkinson K, Leemhuis T, Hanania E, Juttner C, Tierney K, Hu WW, Johnston LJ, Shizurn JA, Stockerl-Goldstein KE, et al. 2000. Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer. Biol Blood Marrow Transplant 6:262-271.
39. Nimni ME, Cheung D, Strates B, Kodama M, Sheikh K. 1987. Chemically modified collagen: a natural biomaterial for tissue replacement. J Biomed Mater Res 21:741-771.
40. Pelton RW, Dickinson ME, Moses HL, Hogan BL. 1990. In situ hybridization analysis of TGF beta 3 RNA expression during mouse development: comparative studies with TGF beta 1 and beta 2. Development 110:609-620.
41. Perez-Rigueiro J, Viney C, Llorca J, Elices M. 1998. Silkworm silk as an engineering material. J Appl Polym Sci 70:2439-2447.
42. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
43. Radisic M, Euloth M, Yang L, Langer R, Freed LE, Vunjak-Novakovic G. 2003. High density seeding of myocyte cells for tissue engineering. Biotechnol Bioeng 82:403-414.
44. Sofia S, McCarthy MB, Gronowicz G, Kaplan DL. 2001. Functionalized silk-based biomaterials for bone formation. J Biomed Mater Res 54:139-148.
45. Spangrude GJ, Heimfeld S, Weissman IL. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241:58-62.
46. Suh H. 1998. Recent advances in biomaterials. Yonsei Med J 39:87-96.
47. Vunjak-Novakovic G. 2003. Fundamentals of tissue engineering: scaffolds and bioreactors. In: Caplan AI, editor. Tissue engineering of cartilage and bone. New York: John Wiley & Sons, p 34-51.
48. Vunjak-Novakovic G, Goldstein SA. 2004. Biomechanical principles of cartilage and bone tissue engineering. In: Mow VC, Huiskes R, editors. Basic orthopaedic biomechanics and mechanobiology, 3rd ed. New York: Lippincott-Williams and Wilkens (in press).
49. Vunjak-Novakovic G, Radisic M. 2004. Cell seeding of polymer scaffolds. Methods Mol Biol 238:131-146.
50. Vunjak-Novakovic G, Obradovic B, Bursac P, Martin I, Langer R, Freed LE. 1998. Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering. Biotechnol Prog 14:193-202.
51. Wakitani S, Goto T, Pineda SJ, Young RG, Mansour JM, Caplan AI, Goldberg VM. 1994. Mesenchymal cell-based repair of large, full-thickness defects of articular cartilage. J Bone Joint Surg Am 76A: 579-592.
52. Yoo JU, Barthel TS, Nishimura K, Solchaga L, Caplan AI, Goldberg VM, Johnstone B. 1998. The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am 80:1745-1757.