Effect of three-dimensional expansion and cell seeding density on the cartilage-forming capacity of human articular chondrocytes in type II collagen sponges

Journal of Biomedical Materials Research - Part A

Volumn 95, Issue 3 A, 2010, Pages 924-931

  Francioli, Silvia E ^a   Candrian, Christian ^a,b   Martin, Katja ^c   Heberer, Michael ^a   Martin, Ivan ^a   Barbero, Andrea ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b REGIONAL HOSPITAL OF LUGANO   (Switzerland)

^c Geistlich Pharma AG   (Switzerland)

Author keywords

Chondrocyte proliferation; Chondrogenic differentiation; Human articular chondrocytes; Tissue engineering; Type II collagen sponges

Indexed keywords

3D SCAFFOLDS; CARTILAGINOUS TISSUES; CELL DEDIFFERENTIATION; CELL DENSITY; CELL DIFFERENTIATION; CELL NUMBER; CELL SEEDING DENSITY; CHONDROCYTE PROLIFERATION; CHONDROCYTES; CHONDROCYTIC; CHONDROGENESIS; CHONDROGENIC; CHONDROGENIC DIFFERENTIATION; DIMENSIONAL EXPANSION; DIRECT EXPANSION; DOUBLINGS; GLYCOSAMINOGLYCANS; HUMAN ARTICULAR CHONDROCYTES; IN-VITRO; SEEDED CELLS; SEEDING DENSITY; TYPE II COLLAGENS;

BODY FLUIDS; CARTILAGE; COLLAGEN; EXPANSION; FLOW MEASUREMENT; MONOLAYERS; SCAFFOLDS; SEED; THREE DIMENSIONAL; TISSUE ENGINEERING;

CELL CULTURE;

COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; MESSENGER RNA; TISSUE SCAFFOLD;

ARTICLE; CARTILAGE CELL; CARTILAGINOUS TISSUE; CELL COUNT; CELL DEDIFFERENTIATION; CELL DENSITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL SEEDING DENSITY; CHONDROGENESIS; HUMAN; HUMAN CELL; PHENOTYPE;

ADULT; AGED; ANIMALS; BIOCOMPATIBLE MATERIALS; CARTILAGE, ARTICULAR; CELL COUNT; CELL CULTURE TECHNIQUES; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; GLYCOSAMINOGLYCANS; HUMANS; MATERIALS TESTING; MIDDLE AGED; SWINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 78249286486     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.32917     Document Type: Article

References (45)

1. Hunziker EB, Quinn TM, Hauselmann HJ,. Quantitative structural organization of normal adult human articular cartilage. Osteoarthritis Cartilage 2002; 10: 564 -572.
2. Mankin HJ,. The response of articular cartilage to mechanical injury. J Bone Joint Surg Am 1982; 64: 126 -145.
3. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L,. Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 1994; 331: 58 -69.
4. Hunziker EB,. Articular cartilage repair: Basic science and clinical progress. A review of the current status and prospects. Osteoarthritis Cartilage 2002; 10: 432 -463.
5. Brittberg M, Winalski CS,. Evaluation of cartilage injuries and repair. J Bone Joint Surg Am 2003; 85A (Suppl 2): 58 -69.
6. Brittberg M,. Autologous chondrocyte implantation-technique and long-term follow-up. Injury 2008; 39 (Suppl 1): S40 -S49.
7. Gikas PD, Bayliss L, Bentley G, Briggs TW,. An overview of autologous chondrocyte implantation. J Bone Joint Surg Br 2009; 91: 997 -1006.
8. Peterson L, Minas T, Brittberg M, Nilsson A, Sjogren-Jansson E, Lindahl A,. Two-to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res 2000; 374: 212 -234.
9. Bartlett W, Skinner JA, Gooding CR, Carrington RW, Flanagan AM, Briggs TW, Bentley G,. Autologous chondrocyte implantation versus matrix-induced autologous chondrocyte implantation for osteochondral defects of the knee: A prospective, randomised study. J Bone Joint Surg Br 2005; 87: 640 -645.
10. Marcacci M, Berruto M, Brocchetta D, Delcogliano A, Ghinelli D, Gobbi A, Kon E, Pederzini L, Rosa D, Sacchetti GL, Stefani G, Zanasi S,. Articular cartilage engineering with Hyalograft C: 3-year clinical results. Clin Orthop Relat Res 2005; 435: 96 -105.
11. Nehrer S, Domayer S, Dorotka R, Schatz K, Bindreiter U, Kotz R,. Three-year clinical outcome after chondrocyte transplantation using a hyaluronan matrix for cartilage repair. Eur J Radiol 2006; 57: 3 -8.
12. Pelttari K, Wixmerten A, Martin I,. Do we really need cartilage tissue engineering? Swiss Med Wkly 2009; 139: 602 -609.
13. Benya PD, Shaffer JD,. Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 1982; 30: 215 -224.
14. Benya PD, Padilla SR, Nimni ME,. Independent regulation of collagen types by chondrocytes during the loss of differentiated function in culture. Cell 1978; 15: 1313 -1321.
15. Binette F, McQuaid DP, Haudenschild DR, Yaeger PC, McPherson JM, Tubo R,. Expression of a stable articular cartilage phenotype without evidence of hypertrophy by adult human articular chondrocytes in vitro. J Orthop Res 1998; 16: 207 -216.
16. Freed LE, Marquis JC, Nohria A, Emmanual J, Mikos AG, Langer R,. Neocartilage formation in vitro and in vivo using cells cultured on synthetic biodegradable polymers. J Biomed Mater Res 1993; 27: 11 -23.
17. Stokes DG, Liu G, Dharmavaram R, Hawkins D, Piera-Velazquez S, Jimene SA,. Regulation of type-II collagen gene expression during human chondrocyte de-differentiation and recovery of chondrocyte-specific phenotype in culture involves Sry-type high-mobility-group box (SOX) transcription factors. Biochem J 2001; 360: 461 -470.
18. Bonaventure J, Kadhom N, Cohen-Solal, Ng KH, Bourguignon J, Lasselin C, Freisinger P,. Reexpression of cartilage-specific genes by dedifferentiated human articular chondrocytes cultured in alginate beads. Exp Cell Res 1994; 212: 97 -104.
19. Concaro S, Nicklasson E, Ellowsson L, Lindahl A, Brittberg M, Gatenholm P,. Effect of cell seeding concentration on the quality of tissue engineered constructs loaded with adult human articular chondrocytes. J Tissue Eng Regen 2008; 2: 14 -21.
20. Moretti M, Wendt D, Dickinson SC, Sims TJ, Hollander AP, Kelly D, Prendergast PJ, Heberer M, Martin I,. Effects of in vitro preculture on in vivo development of human engineered cartilage in an ectopic model. Tissue Eng 2005; 11: 1421 -1428.
21. Barbero A, Grogan S, Schafer D, Heberer M, Mainil-Varlet P, Martin I,. Age related changes in human articular chondrocyte yield, proliferation and post-expansion chondrogenic capacity. Osteoarthritis Cartilage 2004; 12: 476 -484.
22. Jakob M, Demarteau O, Schafer D, Hintermann B, Dick W, Heberer M, Martin I,. Specific growth factors during the expansion and redifferentiation of adult human articular chondrocytes enhance chondrogenesis and cartilaginous tissue formation in vitro. J Cell Biochem 2001; 81: 368 -377.
23. Lin YJ, Yen CN, Hu YC, Wu YC, Liao CJ, Chu IM,. Chondrocytes culture in three-dimensional porous alginate scaffolds enhanced cell proliferation, matrix synthesis and gene expression. J Biomed Mater Res A 2009; 88: 23 -33.
24. Mukaida T, Urabe K, Naruse K, Aikawa J, Katano M, Hyon SH, Itoman M,. Influence of three-dimensional culture in a type II collagen sponge on primary cultured and dedifferentiated chondrocytes. J Orthop Sci 2005; 10: 521 -528.
25. Yen CN, Lin YR, Chang MD, Tien CW, Wu YC, Liao CJ, Hu YC,. Use of porous alginate sponges for substantial chondrocyte expansion and matrix production: Effects of seeding density. Biotechnol Prog 2008; 24: 452 -457.
26. Dorotka R, Bindreiter U, Vavken P, Nehrer S,. Behavior of human articular chondrocytes derived from nonarthritic and osteoarthritic cartilage in a collagen matrix. Tissue Eng 2005; 11: 877 -886.
27. Dorotka R, Windberger U, Macfelda K, Bindreiter U, Toma C, Nehrer S,. Repair of articular cartilage defects treated by microfracture and a three-dimensional collagen matrix. Biomaterials 2005; 26: 3617 -3629.
28. Lee CR, Breinan HA, Nehrer S, Spector M,. Articular cartilage chondrocytes in type I and type II collagen-GAG matrices exhibit contractile behavior in vitro. Tissue Eng 2000; 6: 555 -565.
29. Nehrer S, Breinan HA, Ramappa A, Shortkroff S, Young G, Minas T, Sledge CB, Yannas IV, Spector M,. Canine chondrocytes seeded in type I and type II collagen implants investigated in vitro. J Biomed Mater Res 1997; 38: 95 -104.
30. Barbero A, Ploegert S, Heberer M, Martin I,. Plasticity of clonal populations of dedifferentiated adult human articular chondrocytes. Arthritis Rheum 2003; 48: 1315 -1325.
31. Jakob M, Démarteau O, Schaefer D, Stumm M, Heberer M, Martin I,. Enzymatic digestion of human articular cartilage yields a small fraction of the total available cells. Connect Tissue Res 2003; 44: 173 -180.
32. Barbero A, Grogan SP, Mainil-Varlet P, Martin I,. Expansion on specific substrates regulates the phenotype and differentiation capacity of human articular chondrocytes. J Cell Biochem 2006; 98: 1140 -1149.
33. Grogan SP, Rieser F, Winkelmann V, Berardi S, Mainil-Varlet P,. A static, closed and scaffold-free bioreactor system that permits chondrogenesis in vitro. Osteoarthritis Cartilage 2003; 11: 403 -411.
34. Farndale RW, Buttle DJ, Barrett AJ,. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986; 883: 173 -177.
35. Handley CJ, Buttle DJ,. Assay of proteoglycan degradation. Methods Enzymol 1995; 248: 47 -58.
36. Candrian C, Bonacina E, Frueh JA, Vonwil D, Dickinson S, Wirz D, Heberer M, Jakob M, Martin I, Barbero A,. Intra-individual comparison of human ankle and knee chondrocytes in vitro: Relevance for talar cartilage repair. Osteoarthritis Cartilage 2009; 17: 489 -496.
37. Wolf F, Candrian C, Wendt D, Farhadi J, Heberer M, Martin I, Barbero A,. Cartilage tissue engineering using pre-aggregated human articular chondrocytes. Eur Cell Mater 2008; 16: 92 -99.
38. Roche S, Ronziere MC, Herbage D, Freyria AM,. Native and DPPA cross-linked collagen sponges seeded with fetal bovine epiphyseal chondrocytes used for cartilage tissue engineering. Biomaterials 2001; 22: 9 -18.
39. Hench LL, Polak JM,. Third-generation biomedical materials. Science 2002; 295: 1014 -1017.
40. Giannoni P, Cancedda R,. Articular chondrocyte culturing for cell-based cartilage repair: Needs and perspectives. Cells Tissues Organs 2006; 184: 1 -15.
41. Stewart MC, Saunders KM, Burton-Wurster N, Macleod JN,. Phenotypic stability of articular chondrocytes in vitro: The effects of culture models, bone morphogenetic protein 2, and serum supplementation. J Bone Miner Res 2000; 15: 166 -174.
42. Delise AM, Tuan RS,. Analysis of N-cadherin function in limb mesenchymal chondrogenesis in vitro. Dev Dyn 2002; 225: 195 -204.
43. Francioli SE, Martin I, Sie CP, Hagg R, Tommasini R, Candrian C, Heberer M, Barbero A,. Growth factors for clinical-scale expansion of human articular chondrocytes: Relevance for automated bioreactor systems. Tissue Eng 2007; 13: 1227 -1234.
44. Kang SW, Yoo SP, Kim BS,. Effect of chondrocyte passage number on histological aspects of tissue-engineered cartilage. Biomed Mater Eng 2007; 17: 269 -276.
45. Candrian C, Vonwil D, Barbero A, Bonacina E, Miot S, Farhadi J, Wirz D, Dickinson S, Hollander A, Jakob M, Li Z, Alini M, Heberer M, Martin I,. Engineered cartilage generated by nasal chondrocytes is responsive to physical forces resembling joint loading. Arthritis Rheum 2008; 58: 197 -208.