Chondrogenesis and cartilage tissue engineering: The longer road to technology development

Trends in Biotechnology

Volumn 30, Issue 3, 2012, Pages 166-176

  Mahmoudifar, Nastaran ^a   Doran, Pauline M ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BODY OF KNOWLEDGE; CARTILAGE TISSUE ENGINEERING; CHONDROGENESIS; CURRENT LIMITATION; IN-VITRO; JOINT INJURIES; KEY ELEMENTS; STEM CELL RESEARCH; TECHNOLOGY DEVELOPMENT; TISSUE ENGINEERED CARTILAGE; TISSUE ENGINEERS;

JOINTS (ANATOMY); STEM CELLS; TISSUE; TISSUE ENGINEERING;

CARTILAGE;

ALKALINE PHOSPHATASE; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; COLLAGENASE 3; GLYCOSAMINOGLYCAN; TISSUE SCAFFOLD; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9;

ADIPOSE TISSUE; ARTICULAR CARTILAGE; BIOREACTOR; CARTILAGE CELL; CARTILAGE TISSUE ENGINEERING; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL HETEROGENEITY; CHEMICAL ENVIRONMENT; CHONDROCYTE IMPLANTATION; CHONDROGENESIS; COMPRESSION; GRAFT REJECTION; HUMAN; HYPERTROPHY; MEDICAL TECHNOLOGY; MESENCHYMAL STEM CELL; NONHUMAN; PAIN; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STEM CELL RESEARCH; STIMULATION; SWELLING; SYNTHESIS; TENSION; TISSUE DIFFERENTIATION; TISSUE ENGINEERING; TREATMENT FAILURE;

CARTILAGE; CHONDROGENESIS; HUMANS; STEM CELL RESEARCH; TISSUE ENGINEERING;

EID: 84857444112     PISSN: 01677799     EISSN: 18793096     Source Type: Journal    
DOI: 10.1016/j.tibtech.2011.09.002     Document Type: Review

References (84)

1. Wood J.J., et al. Autologous cultured chondrocytes: adverse events reported to the United States Food and Drug Administration. J. Bone Joint Surg. 2006, 88A:503-507.
2. Revell C.M., Athanasiou K.A. Success rates and immunologic responses of autogenic, allogenic, and xenogenic treatments to repair articular cartilage defects. Tissue Eng. B 2009, 15:1-15.
3. Freed L.E., et al. Composition of cell-polymer cartilage implants. Biotechnol. Bioeng. 1994, 43:605-614.
4. Dunkelman N.S., et al. Cartilage production by rabbit articular chondrocytes on polyglycolic acid scaffolds in a closed bioreactor system. Biotechnol. Bioeng. 1995, 46:299-305.
5. Lima E.G., et al. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with TGF-β3. Osteoarthr. Cartilage 2007, 15:1025-1033.
6. Byers B.A., et al. Transient exposure to transforming growth factor beta 3 under serum-free conditions enhances the biomechanical and biochemical maturation of tissue-engineered cartilage. Tissue Eng. A 2008, 14:1821-1834.
7. Duda G.N., et al. Mechanical quality of tissue engineered cartilage: results after 6 and 12 weeks in vivo. J. Biomed. Mater. Res. B Appl. Biomater. 2000, 53:673-677.
8. Mauck R.L., et al. The role of cell seeding density and nutrient supply for articular cartilage tissue engineering with deformational loading. Osteoarthr. Cartilage 2003, 11:879-890.
9. Ingber D.E., et al. Tissue engineering and developmental biology: going biomimetic. Tissue Eng. 2006, 12:3265-3283.
10. Lenas P., et al. Developmental engineering: a new paradigm for the design and manufacturing of cell-based products. Part I: from three-dimensional cell growth to biomimetics of in vivo development. Tissue Eng. B 2009, 15:381-394.
11. Scotti C., et al. Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7251-7256.
12. Hanley J., et al. An introduction to induced pluripotent stem cells. Br. J. Haematol. 2010, 151:16-24.
13. Kingham P.J., et al. Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp. Neurol. 2007, 207:267-274.
14. Mauck R.L., et al. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthr. Cartilage 2006, 14:179-189.
15. Connelly J.T., et al. Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs. Osteoarthr. Cartilage 2008, 16:1092-1100.
16. Erickson I.E., et al. Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng. A 2009, 15:1041-1052.
17. Huang A.H., et al. Evaluation of the complex transcriptional topography of mesenchymal stem cell chondrogenesis for cartilage tissue engineering. Tissue Eng. A 2010, 16:2699-2708.
18. Mahmoudifar N., Doran P.M. Extent of cell differentiation and capacity for cartilage synthesis in human adult adipose-derived stem cells: comparison with fetal chondrocytes. Biotechnol. Bioeng. 2010, 107:393-401.
19. Boeuf S., et al. Subtractive gene expression profiling of articular cartilage and mesenchymal stem cells: serpins as cartilage-relevant differentiation markers. Osteoarthr. Cartilage 2008, 16:48-60.
20. Ji Y., et al. Quantitative proteomics analysis of chondrogenic differentiation of C3H10T1/2 mesenchymal stem cells by iTRAQ labeling coupled with on-line two-dimensional LC/MS/MS. Mol. Cell. Proteomics 2010, 9:550-564.
21. Sekiya I., et al. In vitro cartilage formation by human adult stem cells from bone marrow stroma defines the sequence of cellular and molecular events during chondrogenesis. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:4397-4402.
22. Pelttari K., et al. Premature induction of hypertrophy during in vitro chondrogenesis of human mesenchymal stem cells correlates with calcification and vascular invasion after ectopic transplantation in SCID mice. Arthritis Rheum. 2006, 54:3254-3266.
23. Xu J., et al. Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels. Tissue Eng. A 2008, 14:667-680.
24. Estes B.T., et al. Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J. Cell. Physiol. 2006, 209:987-995.
25. Kim H.-J., Im G.-I. Chondrogenic differentiation of adipose tissue-derived mesenchymal stem cells: greater doses of growth factor are necessary. J. Orthop. Res. 2009, 27:612-619.
26. Mueller M.B., Tuan R.S. Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum. 2008, 58:1377-1388.
27. Awad H.A., et al. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 2004, 25:3211-3222.
28. Chen S., et al. Coculture of synovium-derived stem cells and nucleus pulposus cells in serum-free defined medium with supplementation of transforming growth factor-β1. Spine 2009, 34:1272-1280.
29. Fischer J., et al. Human articular chondrocytes secrete parathyroid hormone-related protein and inhibit hypertrophy of mesenchymal stem cells in coculture during chondrogenesis. Arthritis Rheum. 2010, 62:2696-2706.
30. Nelea V., et al. Selective inhibition of type X collagen expression in human mesenchymal stem cell differentiation on polymer substrates surface-modified by glow discharge plasma. J. Biomed. Mater. Res. A 2005, 75:216-223.
31. Mahmoudifar N., Doran P.M. Chondrogenic differentiation of human adipose-derived stem cells in polyglycolic acid mesh scaffolds under dynamic culture conditions. Biomaterials 2010, 31:3858-3867.
32. Engler A.J., et al. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
33. Tew S.R., Hardingham T.E. Regulation of SOX9 mRNA in human articular chondrocytes involving p38 MAPK activation and mRNA stabilization. J. Biol. Chem. 2006, 281:39471-39479.
34. Mammoto A., Ingber D.E. Cytoskeletal control of growth and cell fate switching. Curr. Opin. Cell Biol. 2009, 21:864-870.
35. Guilak F., et al. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
36. Lutolf M.P., et al. Designing materials to direct stem-cell fate. Nature 2009, 462:433-441.
37. Huebsch N., et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 2010, 9:518-526.
38. Mammoto T., Ingber D.E. Mechanical control of tissue and organ development. Development 2010, 137:1407-1420.
39. Huang A.H., et al. Mechanics and mechanobiology of mesenchymal stem cell-based engineered cartilage. J. Biomech. 2010, 43:128-136.
40. Kelly D.J., Jacobs C.R. The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defects Res. C 2010, 90:75-85.
41. Kupcsik L., et al. Improving chondrogenesis: potential and limitations of SOX9 gene transfer and mechanical stimulation for cartilage tissue engineering. Tissue Eng. A 2010, 16:1845-1855.
42. Mouw J.K., et al. Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells. Stem Cells 2007, 25:655-663.
43. Huang A.H., et al. Long-term dynamic loading improves the mechanical properties of chondrogenic mesenchymal stem cell-laden hydrogels. Eur. Cells Mater. 2010, 19:72-85.
44. Thorpe S.D., et al. The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGF-β3 induced chondrogenic differentiation. Ann. Biomed. Eng. 2010, 38:2896-2909.
45. Buckley C.T., et al. Oxygen tension differentially regulates the functional properties of cartilaginous tissues engineered from infrapatellar fat pad derived MSCs and articular chondrocytes. Osteoarthr. Cartilage 2010, 18:1345-1354.
46. Khan W.S., et al. Bone marrow-derived mesenchymal stem cells express the pericyte marker 3G5 in culture and show enhanced chondrogenesis in hypoxic conditions. J. Orthop. Res. 2010, 28:834-840.
47. Arnsdorf E.J., et al. Mechanically induced osteogenic differentiation - the role of RhoA, ROCKII and cytoskeletal dynamics. J. Cell Sci. 2009, 122:546-553.
48. Wang T.-W., et al. Regulation of adult human mesenchymal stem cells into osteogenic and chondrogenic lineages by different bioreactor systems. J. Biomed. Mater. Res. A 2009, 88:935-946.
49. Terraciano V., et al. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 2007, 25:2730-2738.
50. Haasper C., et al. A system for engineering an osteochondral construct in the shape of an articular surface: preliminary results. Ann. Anat. 2008, 190:351-359.
51. Kisiday J.D., et al. Dynamic compression stimulates proteoglycan synthesis by mesenchymal stem cells in the absence of chondrogenic cytokines. Tissue Eng. A 2009, 15:2817-2824.
52. Li Z., et al. Mechanical load modulates chondrogenesis of human mesenchymal stem cells through the TGF-β pathway. J. Cell. Mol. Med. 2010, 14:1338-1346.
53. Song L., Tuan R.S. Transdifferentiation potential of human mesenchymal stem cells derived from bone marrow. FASEB J. 2004, 18:980-982.
54. Song L., et al. Identification and functional analysis of candidate genes regulating mesenchymal stem cell self-renewal and multipotency. Stem Cells 2006, 24:1707-1718.
55. Jiang Y., et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
56. Russell K.C., et al. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 2010, 28:788-798.
57. Guilak F., et al. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J. Cell. Physiol. 2006, 206:229-237.
58. Karystinou A., et al. Distinct mesenchymal progenitor cell subsets in the adult human synovium. Rheumatology 2009, 48:1057-1064.
59. Chang H.H., et al. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 2008, 453:544-547.
60. Hoffmann M., et al. Noise-driven stem cell and progenitor population dynamics. PLoS ONE 2008, 3:e2922.
61. Pittenger M.F., et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
62. Augst A., et al. Effects of chondrogenic and osteogenic regulatory factors on composite constructs grown using human mesenchymal stem cells, silk scaffolds and bioreactors. J. R. Soc. Interface 2008, 5:929-939.
63. Grayson W.L., et al. Spatial regulation of human mesenchymal stem cell differentiation in engineered osteochondral constructs: effects of pre-differentiation, soluble factors and medium perfusion. Osteoarthr. Cartilage 2010, 18:714-723.
64. De Bari C., et al. Failure of in vitro-differentiated mesenchymal stem cells from the synovial membrane to form ectopic stable cartilage in vivo. Arthritis Rheum. 2004, 50:142-150.
65. Oldershaw R.A., et al. Directed differentiation of human embryonic stem cells toward chondrocytes. Nat. Biotechnol. 2010, 28:1187-1194.
66. Imaizumi M., et al. Potential of induced pluripotent stem cells for the regeneration of the tracheal wall. Ann. Otol. Rhinol. Laryngol. 2010, 119:697-703.
67. Polo J.M., et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 2010, 28:848-855.
68. Mahmoudifar N., Doran P.M. Tissue engineering of human cartilage in bioreactors using single and composite cell-seeded scaffolds. Biotechnol. Bioeng. 2005, 91:338-355.
69. Freed L.E., Vunjak-Novakovic G. Tissue culture bioreactors: chondrogenesis as a model system. Principles of Tissue Engineering 1997, 151-165. Academic Press. R.P. Lanza (Ed.).
70. Shahin K., Doran P.M. Strategies for enhancing the accumulation and retention of extracellular matrix in tissue-engineered cartilage cultured in bioreactors. PLoS ONE 2011, 6:e23119.
71. Shahin K., Doran P.M. Improved seeding of chondrocytes into polyglycolic acid scaffolds using semi-static and alginate loading methods. Biotechnol. Prog. 2011, 27:191-200.
72. Bobick B.E., et al. Regulation of the chondrogenic phenotype in culture. Birth Defects Res. C 2009, 87:351-371.
73. Quintana L., et al. Morphogenetic and regulatory mechanisms during developmental chondrogenesis: new paradigms for cartilage tissue engineering. Tissue Eng. B 2009, 15:29-41.
74. Schulz R.M., Bader A. Cartilage tissue engineering and bioreactor systems for the cultivation and stimulation of chondrocytes. Eur. Biophys. J. 2007, 36:539-568.
75. Athanasiou K.A., et al. Articular Cartilage Tissue Engineering 2010, Morgan and Claypool.
76. Steinert A.F., et al. Concepts in gene therapy for cartilage repair. Injury 2008, 39(S1):S97-S113.
77. Hidaka C., et al. Enhanced matrix synthesis and in vitro formation of cartilage-like tissue by genetically modified chondrocytes expressing BMP-7. J. Orthop. Res. 2001, 19:751-758.
78. Steinert A.F., et al. Hypertrophy is induced during the in vitro chondrogenic differentiation of human mesenchymal stem cells by bone morphogenetic protein-2 and bone morphogenetic protein-4 gene transfer. Arthritis Res. Ther. 2009, 11:R148.
79. Diekman B.O., et al. The effects of BMP6 overexpression on adipose stem cell chondrogenesis: interactions with dexamethasone and exogenous growth factors. J. Biomed. Mater. Res. A 2010, 93:994-1003.
80. Yao Y., et al. Effects of combinatorial adenoviral vector-mediated TGFβ3 transgene and shRNA silencing type I collagen on articular chondrogenesis of synovium-derived mesenchymal stem cells. Biotechnol. Bioeng. 2010, 106:818-828.
81. Evans C.H., et al. Gene transfer to human joints: progress toward a gene therapy of arthritis. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:8698-8703.
82. Kisiday J.D., et al. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J. Orthop. Res. 2008, 26:322-331.
83. Solursh M., Meier S. The requirement for RNA synthesis in the differentiation of cultured chick embryo chondrocytes. J. Exp. Zool. 1972, 181:253-262.
84. Hall B.K. Bones and Cartilage: Developmental Skeletal Biology 2005, Academic Press, pp. 351-357.