Effects of biomimetic surfaces and oxygen tension on redifferentiation of passaged human fibrochondrocytes in 2D and 3D cultures

Biomaterials

Volumn 32, Issue 24, 2011, Pages 5600-5614

  Tan, Guak Kim ^a   Dinnes, Donna Lee M ^b   Myers, Peter T ^c   Cooper White, Justin J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c Specialist Centre   (Australia)

Author keywords

Biomimetic; Chondroitin sulfate; Collagen; Hypoxia; Meniscal tissue engineering; Redifferentiation

Indexed keywords

3D CULTURE; AVASCULAR REGION; BIOMIMETIC SURFACES; CELL POPULATIONS; CHONDROITIN SULFATES; CLINICAL USE; COATED GLASS; COLLAGEN I; COLLAGEN II; DNA QUANTIFICATION; DOWN-REGULATION; EXTRACELLULAR MATRICES; FIBROCHONDROCYTES; HYPOXIA; HYPOXIA-INDUCIBLE FACTORS; IMMUNOHISTOCHEMISTRY; INNER REGION; MATRIX SYNTHESIS; MENISCAL REPAIR; MENISCAL TISSUE ENGINEERING; MONOLAYER EXPANSION; ORTHOPAEDIC SURGERY; OXYGEN TENSION; PHENOTYPIC CHANGES; POLYMERIC SCAFFOLD; REDIFFERENTIATION; REVERSE TRANSCRIPTASE- POLYMERASE CHAIN REACTION; SURFACE-MODIFIED; TAILORED SURFACES; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL ACTIVITY;

ADHESION; BIOMIMETICS; BOTTLES; CELL ADHESION; CELL PROLIFERATION; COLLAGEN; GENE EXPRESSION; MONOLAYERS; POLYMERASE CHAIN REACTION; POLYMERIC GLASS; REPAIR; SCAFFOLDS (BIOLOGY); SYNTHESIS (CHEMICAL); THREE DIMENSIONAL; TISSUE; TISSUE CULTURE;

TWO DIMENSIONAL;

AGGRECAN; BIOMIMETIC MATERIAL; CHONDROITIN 6 SULFATE; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGEN TYPE 3; CYCLOPHILIN A; GLYCOSAMINOGLYCAN POLYSULFATE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; PROTEOGLYCAN; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3;

ARTICLE; BIOMIMETICS; CARTILAGE CELL; CELL ADHESION; CELL CULTURE; CELL DEDIFFERENTIATION; CELL EXPANSION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FIBROCHONDROCYTE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KNEE MENISCUS; MARKER GENE; MENISCAL REPAIR; NUCLEOTIDE SEQUENCE; OXYGEN TENSION; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURFACE PROPERTY; THREE DIMENSIONAL IMAGING; TISSUE CULTURE; TRANSCRIPTION INITIATION;

AGED; CELL ADHESION; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; CHONDROCYTES; CHONDROITIN SULFATES; COLLAGEN; GLYCOSAMINOGLYCANS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, SCANNING; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TISSUE ENGINEERING;

RATTUS;

EID: 79957895021     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.04.033     Document Type: Article

References (71)

1. Lee J., Fu F. The meniscus: basic science and clinical applications. Oper Tech Orthop 2000, 10:162-168.
2. Kurosawa H., Fukubayashi T., Nakajima H. Load-bearing mode of the knee joint: physical behavior of the knee joint with or without menisci. Clin Orthop Relat Res 1980, 149:283-290.
3. Fithian D.C., Kelly M.A., Mow V.C. Material properties and structure-function relationships in the menisci. Clin Orthop Relat Res 1990, 252:19-31.
4. Englund M., Roos E.M., Lohmander L.S. Impact of type of meniscal tear on radiographic and symptomatic knee osteoarthritis: a sixteen-year followup of meniscectomy with matched controls. Arthritis Rheum 2003, 48:2178-2187.
5. Berthiaume M.J., Raynauld J.P., Martel-Pelletier J., Labonte F., Beaudoin G., Bloch D.A., et al. Meniscal tear and extrusion are strongly associated with progression of symptomatic knee osteoarthritis as assessed by quantitative magnetic resonance imaging. Ann Rheum Dis 2005, 64:556-563.
6. Jakob R.P., Staubli H.U., Zuber K., Esser M. The arthroscopic meniscal repair. Techniques and clinical experience. Am J Sports Med 1988, 16:137-142.
7. Klompmaker J., Veth R.P., Jansen H.W., Nielsen H.K., de Groot J.H., Pennings A.J., et al. Meniscal repair by fibrocartilage in the dog: characterization of the repair tissue and the role of vascularity. Biomaterials 1996, 17:1685-1691.
8. Rubman M.H., Noyes F.R., Barber-Westin S.D. Arthroscopic repair of meniscal tears that extend into the avascular zone. A review of 198 single and complex tears. Am J Sports Med 1998, 26:87-95.
9. Eyre D.R., Wu J.J. Collagen of fibrocartilage: a distinctive molecular phenotype in bovine meniscus. FEBS Lett 1983, 158:265-270.
10. Chevrier A., Nelea M., Hurtig M.B., Hoemann C.D., Buschmann M.D. Meniscus structure in human, sheep, and rabbit for animal models of meniscus repair. J Orthop Res 2009, 27:1197-1203.
11. Hellio Le Graverand M.P., Ou Y., Schield-Yee T., Barclay L., Hart D., Natsume T., et al. The cells of the rabbit meniscus: their arrangement, interrelationship, morphological variations and cytoarchitecture. J Anat 2001, 198:525-535.
12. Ghadially F.N., Thomas I., Yong N., Lalonde J.M. Ultrastructure of rabbit semilunar cartilages. J Anat 1978, 125:499-517.
13. Webber R.J., Harris M.G., Hough A.J. Cell culture of rabbit meniscal fibrochondrocytes: proliferative and synthetic response to growth factors and ascorbate. J Orthop Res 1985, 3:36-42.
14. Cheung H.S. Distribution of type I, II, III and V in the pepsin solubilized collagens in bovine menisci. Connect Tissue Res 1987, 16:343-356.
15. McNicol D., Roughley P.J. Extraction and characterization of proteoglycan from human meniscus. Biochem J 1980, 185:705-713.
16. McDevitt C.A., Webber R.J. The ultrastructure and biochemistry of meniscal cartilage. Clin Orthop Relat Res 1990, 8-18.
17. Webber R.J., York J.L., Vanderschilden J.L., Hough A.J. An organ culture model for assaying wound repair of the fibrocartilaginous knee joint meniscus. Am J Sports Med 1989, 17:393-400.
18. Stone K.R., Rodkey W.G., Webber R.J., McKinney L., Steadman J.R. Future directions. Collagen-based prostheses for meniscal regeneration. Clin Orthop Relat Res 1990, 252:129-135.
19. Mueller S.M., Shortkroff S., Schneider T.O., Breinan H.A., Yannas I.V., Spector M. Meniscus cells seeded in type I and type II collagen-GAG matrices in vitro. Biomaterials 1999, 20:701-709.
20. Chiari C., Koller U., Kapeller B., Dorotka R., Bindreiter U., Nehrer S. Different behavior of meniscal cells in collagen II/I, III and Hyaff-11 scaffolds in vitro. Tissue Eng Part A 2008, 14:1295-1304.
21. Verdonk P.C., Forsyth R.G., Wang J., Almqvist K.F., Verdonk R., Veys E.M., et al. Characterisation of human knee meniscus cell phenotype. Osteoarthritis Cartilage 2005, 13:548-560.
22. Nakata K., Shino K., Hamada M., Mae T., Miyama T., Shinjo H., et al. Human meniscus cell: characterization of the primary culture and use for tissue engineering. Clin Orthop Relat Res 2001, 391:S208-S218. Suppl.
23. Gunja N.J., Athanasiou K.A. Passage and reversal effects on gene expression of bovine meniscal fibrochondrocytes. Arthritis Res Ther 2007, 9:R93.
24. Tan G.K., Dinnes D.L., Butler L.N., Cooper-White J.J. Interactions between meniscal cells and a self assembled biomimetic surface composed of hyaluronic acid, chitosan and meniscal extracellular matrix molecules. Biomaterials 2010, 31:6104-6118.
25. Kino-Oka M., Yashiki S., Ota Y., Mushiaki Y., Sugawara K., Yamamoto T., et al. Subculture of chondrocytes on a collagen type I-coated substrate with suppressed cellular dedifferentiation. Tissue Eng 2005, 11:597-608.
26. Brodkin K.R., Garcia A.J., Levenston M.E. Chondrocyte phenotypes on different extracellular matrix monolayers. Biomaterials 2004, 25:5929-5938.
27. Domm C., Schunke M., Christesen K., Kurz B. Redifferentiation of dedifferentiated bovine articular chondrocytes in alginate culture under low oxygen tension. Osteoarthritis Cartilage 2002, 10:13-22.
28. Yaeger P.C., Masi T.L., de Ortiz J.L., Binette F., Tubo R., McPherson J.M. Synergistic action of transforming growth factor-beta and insulin-like growth factor-I induces expression of type II collagen and aggrecan genes in adult human articular chondrocytes. Exp Cell Res 1997, 237:318-325.
29. Malda J., van Blitterswijk C.A., van Geffen M., Martens D.E., Tramper J., Riesle J. Low oxygen tension stimulates the redifferentiation of dedifferentiated adult human nasal chondrocytes. Osteoarthritis Cartilage 2004, 12:306-313.
30. Allen K.D., Erickson K., Athanasiou K.A. The effects of protein-coated surfaces on passaged porcine TMJ disc cells. Arch Oral Biol 2008, 53:53-59.
31. Allen K.D., Athanasiou K.A. Growth factor effects on passaged TMJ disk cells in monolayer and pellet cultures. Orthod Craniofac Res 2006, 9:143-152.
32. Adesida A.B., Grady L.M., Khan W.S., Hardingham T.E. The matrix-forming phenotype of cultured human meniscus cells is enhanced after culture with fibroblast growth factor 2 and is further stimulated by hypoxia. Arthritis Res Ther 2006, 8:R61.
33. Adesida A.B., Grady L.M., Khan W.S., Millward-Sadler S.J., Salter D.M., Hardingham T.E. Human meniscus cells express hypoxia inducible factor-1alpha and increased SOX9 in response to low oxygen tension in cell aggregate culture. Arthritis Res Ther 2007, 9:R69.
34. Semenza G.L. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 1998, 8:588-594.
35. Weidemann A., Johnson R.S. Biology of HIF-1alpha. Cell Death Differ 2008, 15:621-627.
36. Wenger R.H. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J 2002, 16:1151-1162.
37. Duval E., Leclercq S., Elissalde J.M., Demoor M., Galera P., Boumediene K. Hypoxia-inducible factor 1alpha inhibits the fibroblast-like markers type I and type III collagen during hypoxia-induced chondrocyte redifferentiation: hypoxia not only induces type II collagen and aggrecan, but it also inhibits type I and type III collagen in the hypoxia-inducible factor 1alpha-dependent redifferentiation of chondrocytes. Arthritis Rheum 2009, 60:3038-3048.
38. Lafont J.E., Talma S., Hopfgarten C., Murphy C.L. Hypoxia promotes the differentiated human articular chondrocyte phenotype through SOX9-dependent and -independent pathways. J Biol Chem 2008, 283:4778-4786.
39. Kang S.W., Son S.M., Lee J.S., Lee E.S., Lee K.Y., Park S.G., et al. Regeneration of whole meniscus using meniscal cells and polymer scaffolds in a rabbit total meniscectomy model. J Biomed Mater Res A 2006, 78:659-671.
40. Uematsu K., Hattori K., Ishimoto Y., Yamauchi J., Habata T., Takakura Y., et al. Cartilage regeneration using mesenchymal stem cells and a three-dimensional poly-lactic-glycolic acid (PLGA) scaffold. Biomaterials 2005, 26:4273-4279.
41. D'Ippolito G., Diabira S., Howard G.A., Roos B.A., Schiller P.C. Low oxygen tension inhibits osteogenic differentiation and enhances stemness of human MIAMI cells. Bone 2006, 39:513-522.
42. Khan W.S., Adesida A.B., Hardingham T.E. Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther 2007, 9:R55.
43. Lund-Olesen K. Oxygen tension in synovial fluids. Arthritis Rheum 1970, 13:769-776.
44. Tan GK, Dinnes DL, Cooper-White JJ. Modulation of collagen ll fiber formation in 3D porous scaffold environments. 2011 March 23, (Epub ahead of print). doi:10.1016/j.actbio.2011.03.022.
45. Ho S.T., Hutmacher D.W. A comparison of micro CT with other techniques used in the characterization of scaffolds. Biomaterials 2006, 27:1362-1376.
46. Liebman J., Goldberg R.L. Unit 12.2 Chondrocyte culture and assay. Curr Protoc Pharmacol 2001, 12:S1-S18.
47. Markway B.D., Tan G.K., Brooke G., Hudson J.E., Cooper-White J.J., Doran M.R. Enhanced chondrogenic differentiation of human bone marrow-derived mesenchymal stem cells in low oxygen environment micropellet cultures. Cell Transplant 2010, 19:29-42.
48. Dayan D., Hiss Y., Hirshberg A., Bubis J.J., Wolman M. Are the polarization colors of picrosirius red-stained collagen determined only by the diameter of the fibers?. Histochemistry 1989, 93:27-29.
49. Ginzinger D.G. Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp Hematol 2002, 30:503-512.
50. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25:402-408.
51. Dery M.A., Michaud M.D., Richard D.E. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 2005, 37:535-540.
52. Zagorska A., Dulak J. HIF-1: the knowns and unknowns of hypoxia sensing. Acta Biochim Pol 2004, 51:563-585.
53. Marlovits S., Hombauer M., Truppe M., Vecsei V., Schlegel W. Changes in the ratio of type-I and type-II collagen expression during monolayer culture of human chondrocytes. J Bone Jt Surg Br 2004, 86:286-295.
54. Herwig J., Egner E., Buddecke E. Chemical changes of human knee joint menisci in various stages of degeneration. Ann Rheum Dis 1984, 43:635-640.
55. Katsuragawa Y., Saitoh K., Tanaka N., Wake M., Ikeda Y., Furukawa H., et al. Changes of human menisci in osteoarthritic knee joints. Osteoarthritis Cartilage 2010, 18:1133-1143.
56. Tanaka T., Fujii K., Kumagae Y. Comparison of biochemical characteristics of cultured fibrochondrocytes isolated from the inner and outer regions of human meniscus. Knee Surg Sports Traumatol Arthrosc 1999, 7:75-80.
57. Darling E.M., Athanasiou K.A. Retaining zonal chondrocyte phenotype by means of novel growth environments. Tissue Eng 2005, 11:395-403.
58. Glowacki J., Trepman E., Folkman J. Cell shape and phenotypic expression in chondrocytes. Proc Soc Exp Biol Med 1983, 172:93-98.
59. Pangborn C.A., Athanasiou K.A. Growth factors and fibrochondrocytes in scaffolds. J Orthop Res 2005, 23:1184-1190.
60. Kurz B., Domm C., Jin M., Sellckau R., Schunke M. Tissue engineering of articular cartilage under the influence of collagen I/III membranes and low oxygen tension. Tissue Eng 2004, 10:1277-1286.
61. Grigolo B., Lisignoli G., Piacentini A., Fiorini M., Gobbi P., Mazzotti G., et al. Evidence for redifferentiation of human chondrocytes grown on a hyaluronan-based biomaterial (HYAff 11): molecular, immunohistochemical and ultrastructural analysis. Biomaterials 2002, 23:1187-1195.
62. Kambic H.E., McDevitt C.A. Spatial organization of types I and II collagen in the canine meniscus. J Orthop Res 2005, 23:142-149.
63. Lafont J.E., Talma S., Murphy C.L. Hypoxia-inducible factor 2alpha is essential for hypoxic induction of the human articular chondrocyte phenotype. Arthritis Rheum 2007, 56:3297-3306.
64. Robins J.C., Akeno N., Mukherjee A., Dalal R.R., Aronow B.J., Koopman P., et al. Hypoxia induces chondrocyte-specific gene expression in mesenchymal cells in association with transcriptional activation of Sox9. Bone 2005, 37:313-322.
65. Lefebvre V., Huang W., Harley V.R., Goodfellow P.N., de Crombrugghe B. SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 1997, 17:2336-2346.
66. Bell D.M., Leung K.K., Wheatley S.C., Ng L.J., Zhou S., Ling K.W., et al. SOX9 directly regulates the type-II collagen gene. Nat Genet 1997, 16:174-178.
67. Stokes D.G., Liu G., Dharmavaram R., Hawkins D., Piera-Velazquez S., Jimenez S.A. 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.
68. Wenger R.H., Kvietikova I., Rolfs A., Gassmann M., Marti H.H. Hypoxia-inducible factor-1 alpha is regulated at the post-mRNA level. Kidney Int 1997, 51:560-563.
69. Hellio Le Graverand M.P., Reno C., Hart D.A. Gene expression in menisci from the knees of skeletally immature and mature female rabbits. J Orthop Res 1999, 17:738-744.
70. Cannon W.D., Vittori J.M. The incidence of healing in arthroscopic meniscal repairs in anterior cruciate ligament-reconstructed knees versus stable knees. Am J Sports Med 1992, 20:176-181.
71. Darling E.M., Athanasiou K.A. Rapid phenotypic changes in passaged articular chondrocyte subpopulations. J Orthop Res 2005, 23:425-432.