Tissue engineering of human cartilage in bioreactors using single and composite cell-seeded Scaffolds

Biotechnology and Bioengineering

Volumn 91, Issue 3, 2005, Pages 338-355

  Mahmoudifar, Nastaran ^a   Doran, Pauline M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Bioreactor; Cartilage; Chondrocyte; Polyglycolic acid; Scaffold; Tissue engineering

Indexed keywords

BIOREACTORS; BIOTECHNOLOGY; CELLS; HISTOLOGY; PROTEINS;

CHONDROCYTES; COLUMN BIOREACTORS; GLYCOSAMINOGLYCAN (CAG); HUMAN CARTILAGE; POLYGLYCOLIC ACID (PGA);

TISSUE CULTURE;

COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; POLYGLYCOLIC ACID;

ARTICLE; ARTICULAR CARTILAGE; BIOREACTOR; CARTILAGE; CARTILAGE CELL; CELL DENSITY; EXTRACELLULAR MATRIX; HISTOLOGY; HUMAN; HUMAN TISSUE; HYDRODYNAMICS; IMMUNOHISTOCHEMISTRY; QUALITY CONTROL; TISSUE ENGINEERING;

BIOREACTORS; BIOTECHNOLOGY; CARTILAGE; CHONDROCYTES; COLLAGEN TYPE II; EMBRYO; GLYCOSAMINOGLYCANS; HUMANS; POLYGLYCOLIC ACID; TISSUE ENGINEERING;

EID: 23044495960     PISSN: 00063592     EISSN: None     Source Type: Journal    
DOI: 10.1002/bit.20490     Document Type: Article

References (61)

1. Aigner J, Tegeler J, Hutzler P, Campoccia D, Pavesio A, Hammer C, Kastenbauer E, Naumann A. 1998. Cartilage tissue engineering with novel nonwoven structured biomaterial based on hyaluronic acid benzyl ester. J Biomed Mater Res 42:172-181.
2. Allen RG, Eisenberg SR, Gray ML. 1999. Quantitative measurement of the biological response of cartilage to mechanical deformation. In: Morgan JR, Yarmush ML, editors. Tissue engineering methods and protocols. New Jersey: Humana Press, pp 521-542.
3. Aulthouse AL, Beck M, Griffey E, Sanford J, Arden K, Machado MA, Horton WA. 1989. Expression of the human chondrocyte phenotype in vitro. In Vitro Cell Dev Biol 25:659-668.
4. Benya PD, Shaffer JD. 1982. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30:215-224.
5. Cancedda R, Dozin B, Giannoni P, Quarto R. 2003. Tissue engineering and cell therapy of cartilage and bone. Matrix Biol 22:81-91.
6. Carrier RL, Rupnick M, Langer R, Schoen FJ, Freed LE, Vunjak-Novakovic G. 2002. Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 8:175-188.
7. Carver SE, Heath CA. 1999a. Semi-continuous perfusion system for delivering intermittent physiological pressure to regenerating cartilage. Tissue Eng 5:1-11.
8. Carver SE, Heath CA. 1999b. Influence of intermittent pressure, fluid flow, and mixing on the regenerative properties of articular chondrocytes. Biotechnol Bioeng 65:274-281.
9. Chappard D, Alexandre C, Riffat G. 1986. Uncalcified cartilage resorption in human fetal cartilage canals. Tissue Cell 18:701-707.
10. Croughan MS, Hamel J-F, Wang DIC. 1987. Hydrodynamic effects on animal cells grown in microcarrier cultures. Biotechnol Bioeng 29:130-141.
11. Darling EM, Athanasiou KA. 2003. Articular cartilage bioreactors and bioprocesses. Tissue Eng 9:9-26.
12. Dunkelman NS, Zimber MP, LeBaron RG, Pavelec R, Kwan M, Purchio AF. 1995. Cartilage production by rabbit articular chondrocytes on polyglycolic acid scaffolds in a closed bioreactor system. Biotechnol Bioeng 46:299-305.
13. Farndale RW, Buttle DJ, Barrett AJ. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethyl-methylene blue. Biochim Biophys Acta 883:173-177.
14. Frazza EJ, Schmitt EE. 1971. A new absorbable suture. J Biomed Mater Res Symp 1:43-58.
15. Freed LE, Vunjak-Novakovic G. 1995. Cultivation of cell-polymer tissue constructs in simulated microgravity. Biotechnol Bioeng 46:306-313.
16. Freed LE, Vunjak-Novakovic G. 1997. Microgravity tissue engineering. In Vitro Cell Dev Biol Animal 33:381-385.
17. 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.
18. Freed LE, Marquis JC, Vunjak-Novakovic G, Emmanual J, Langer R. 1994. Composition of cell-polymer cartilage implants. Biotechnol Bioeng 43:605-614.
19. Freed LE, Langer R, Martin I, Pellis NR, Vunjak-Novakovic G. 1997. Tissue engineering of cartilage in space. Proc Natl Acad Sci USA 94:13885-13890.
20. Freed LE, Hollander AP, Martin I, Barry JR, Langer R, Vunjak-Novakovic G. 1998. Chondrogenesis in a cell-polymer-bioreactor system. Exp Cell Res 240:58-65.
21. Freyria A-M, Cortial D, Ronzière M-C, Guerret S, Herbage D. 2004. Influence of medium composition, static and stirred conditions on the proliferation of and matrix protein expression of bovine articular chondrocytes cultured in a 3-D collagen scaffold. Biomaterials 25:687-697.
22. Gooch KJ, Kwon JH, Blunk T, Langer R, Freed LE, Vunjak-Novakovic G. 2001. Effects of mixing intensity on tissue-engineered cartilage. Biotechnol Bioeng 72:402-407.
23. Grande DA, Halberstadt C, Naughton G, Schwartz R, Manji R. 1997. Evaluation of matrix scaffolds for tissue engineering of articular cartilage grafts. J Biomed Mater Res 34:211-220.
24. Gurdon JB. 1988. A community effect in animal development. Nature 336:772-774.
25. Hardingham T, Tew S, Murdoch A. 2002. Tissue engineering: Chondrocytes and cartilage. Arthritis Res 4(Suppl 3):S63-S68.
26. Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, Rorabeck C, Poole AR. 1994. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest 93:1722-1732.
27. Jackson GW, James DF 1986. The permeability of fibrous porous media. Can J Chem Eng 64:364-374.
28. Kim Y-J, Sah RLY, Doong J-YH, Grodzinsky AJ. 1988. Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174:168-176.
29. Kuettner KE, Pauli BU. 1983. Vascularity of cartilage. In: Hall BK, editor. Cartilage, vol 1, New York: Academic Press, pp 281-312.
30. Lee MS, Trindade MCD, Ikenoue T, Schurman DJ, Goodman SB, Smith RL. 2002. Effects of shear stress on nitric oxide and matrix protein gene expression in human osteoarthritic chondrocytes in vitro. J Orthop Res 20:556-561.
31. Lefebvre V, Garofalo S, Zhou G, Metsäranta M, Vuorio E, de Crombrugghe B. 1994. Characterization of primary cultures of chondrocytes from type II collagen/β-galactosidase transgenic mice. Matrix Biol 14:329-335.
32. Levene C. 1964. The patterns of cartilage canals. J Anat Lond 98:515-538.
33. Lillie RD. 1965. Histopathologic technic and practical histochemistry. 3rd edition. New York: McGraw-Hill.
34. Malaviya P, Nerem RM. 2002. Fluid-induced shear stress stimulates chondrocyte proliferation partially mediated via TGF-β1. Tissue Eng 8:581-590.
35. Mason JM, Breitbart AS, Barcia M, Porti D, Pergolizzi RG, Grande DA. 2000. Cartilage and bone regeneration using gene-enhanced tissue engineering. Clin Orthop Rel Res 379S:S171-S178.
36. Melrose J, Smith S, Ghosh P, Whitelock J, 2003. Perlecan, the multidomain heparan sulfate proteoglycan of basement membranes, is also a prominent component of the cartilaginous primordia in the developing human fetal spine. J Histochem Cytochem 51:1331-1341.
37. Mow VC, Ratcliffe A, Poole AR. 1992. Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 13:67-97.
38. Obradovic B, Carrier RL, Vunjak-Novakovic G, Freed LE. 1999. Gas exchange is essential for bioreactor cultivation of tissue engineered cartilage. Biotechnol Bioeng 63:197-205.
39. O'Driscoll SW, Fitzsimmons JS, Commisso CN. 1997. Role of oxygen tension during cartilage formation by periosteum. J Orthop Res 15:682-687.
40. Pazzano D, Mercier KA, Moran JM, Fong SS, DiBiasio DD, Rulfs JX, Kohles SS, Bonassar LJ. 2000. Comparison of chondrogenesis in static and perfused bioreactor culture. Biotechnol Prog 16:893-896.
41. Perry SD, Wang DIC. 1989. Fiber bed reactor design for animal cell culture. Biotechnol Bioeng 34:1-9.
42. Poole CA. 1993. The structure and function of articular cartilage matrices. In: Woessner JF, Howell DS, editors. Joint cartilage degradation: Basic and clinical aspects. New York: Marcel Dekker. pp 1-35.
43. Radin EL, Fyhrie D. 1990. Joint physiology and biomechanics. In: Mow VC, Ratcliffe A, Woo S.L-Y, editors. Biomechanics of diarthrodial joints, vol II, New York: Springer-Verlag, pp 369-384.
44. Rajpurohit R, Koch CJ, Tao Z, Teixeira CM, Shapiro IM. 1996. Adaptation of chondrocytes to low oxygen tension: Relationship between hypoxia and cellular metabolism. J Cell Physiol 168:424-432.
45. Reichenberger E, Aigner T, von der Mark K, Stöß H, Bertling W. 1991. In situ hybridization studies on the expression of type X collagen in fetal human cartilage. Dev Biol 148:562-572.
46. Rotter N, Aigner J, Naumann A, Planck H, Hammer C, Burmester G, Sittinger M. 1998. Cartilage reconstruction in head and neck surgery: Comparison of resorbable polymer scaffolds for tissue engineering of human septal cartilage. J Biomed Mater Res 42:347-356.
47. Smith RL, Trindade MCD, Ikenoue T, Mohtai M, Das P, Carter DR, Goodman SB, Schurman DJ. 2000. Effects of shear stress on articular chondrocyte metabolism. Biorheology 37:95-107.
48. Stevens A. 1990. The haematoxylins. In: Bancroft JD, Stevens A, editors. Theory and practice of histological techniques, 3rd edition. Edinburgh: Churchill Livingstone. pp 107-118.
49. Tacchetti C, Tavella S, Dozin B, Quarto R, Robino G, Cancedda R. 1992. Cell condensation in chondrogenic differentiation. Exp Cell Res 200:26-33.
50. Treilleux I, Mallein-Gerin F, Le Guellec D, Herbage D. 1992. Localization of the expression of type I, II, III collagen, and aggrecan core protein genes in developing human articular cartilage. Matrix 12:221-232.
51. Tubo R, Binette F. 1999. Culture and identification of autologous human articular chondrocytes for implantation. In: Morgan JR, Yarmush ML, editors. Tissue engineering methods and protocols. New Jersey: Humana Press, pp 205-215.
52. Vunjak-Novakovic G, Freed LE, Biron RJ, Langer R. 1996. Effects of mixing on the composition and morphology of tissue-engineered cartilage. AIChE J 42:850-860.
53. Vunjak-Novakovic G, Obradovic B, Martin I, Bursac PM, Langer R, Freed LE. 1998. Dynamic cell seeding of polymer scaffolds for cartilage tissue engineering. Biotechnol Prog 14:193-202.
54. Vunjak-Novakovic G, Martin I, Obradovic B, Treppo S, Grodzinsky AJ, Langer R, Freed LE. 1999. Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue-engineered cartilage. J Orthop Res 17:130-138.
55. Wang W-G, Lou S-Q, Ju X-D, Xia K, Xia J-H. 2003. In vitro chondrogenesis of human bone marrow-derived mesenchymal progenitor cells in monolayer culture: Activation by transfection with TGF-β2. Tissue Cell 35:69-77.
56. Wardlaw AC. 1985. Practical statistics for experimental biologists. Chichester: Wiley.
57. Woessner JF. 1961. The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys 93:440-447.
58. Woessner JF. 1977. Determination of hydroxyproline in connective tissues. In: Hall DA, editor. The methodology of connective tissue research. New York: CRC Press, pp 227-233.
59. Ysart GE, Mason RM. 1994. Responses of articular cartilage explant cultures to different oxygen tensions. Biochim Biophys Acta 1221:15-20.
60. Zar JH. 1999. Biostatistical analysis, 4th edition. London: Prentice Hall International.
61. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. 2001. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 7:211-228.