Composition-function relations of cartilaginous tissues engineered from chondrocytes and mesenchymal stem cells isolated from bone marrow and infrapatellar fat pad

Journal of Tissue Engineering and Regenerative Medicine

Volumn 5, Issue 9, 2011, Pages 673-683

  Vinardell, T ^a   Buckley, C T ^a   Thorpe, S D ^a   Kelly, D J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cartilage; Chondrocytes; Hydrogel; Infrapatellar fat pad; Mesenchymal stem cells; TGF 3

Indexed keywords

BIOMECHANICS; BODY FLUIDS; BONE; FLOWCHARTING; HISTOLOGY; HYDROGELS; STEM CELLS;

BONE MARROW; CARTILAGINOUS TISSUES; CHONDROCYTES; COMPOSITION FUNCTIONS; FUNCTIONAL PROPERTIES; INFRAPATELLAR FAT PAD; MESENCHYMAL STEM CELL; PROPERTY; TGFΒ3; TISSUE SOURCES;

CELL CULTURE;

AGAROSE; CALCIUM; COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; GLYCOSAMINOGLYCAN; TRANSFORMING GROWTH FACTOR BETA3;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BIOMECHANICS; BONE MARROW; CARTILAGE CELL; CARTILAGINOUS TISSUE; CELL ISOLATION; CELL SWELLING; CHONDROGENESIS; CONTROLLED STUDY; DNA CONTENT; HISTOLOGY; HYDROGEL; INFRAPATELLAR FAT PAD; MESENCHYMAL STEM CELL; NONHUMAN; PATELLOFEMORAL JOINT; PRIORITY JOURNAL; SWINE; TISSUE ENGINEERING;

EID: 80053145900     PISSN: 19326254     EISSN: 19327005     Source Type: Journal    
DOI: 10.1002/term.357     Document Type: Article

References (66)

1. Afizah H, Yang Z, Hui JHP, et al. 2007; A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adipose-derived stem cells (ADSCs) taken from the same donors. Tissue Eng 13(4): 659-666.
2. Awad HA, Wickham MQ, Leddy HA, et al. 2004; Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 25(16): 3211-3222.
3. Babalola OM, Bonassar LJ. 2010; Effects of seeding density on proteoglycan assembly of passaged mesenchymal stem cells. Cell Mol Bioeng 3(3): 197-206.
4. Bianchi G, Banfi A, Mastrogiacomo M, et al. 2003; Ex vivo enrichment of mesenchymal cell progenitors by fibroblast growth factor 2. Exp Cell Res 287(1): 98-105.
5. Buckley CT, Thorpe SD, Kelly DJ. 2009; Engineering of large cartilaginous tissues through the use of microchanneled hydrogels and rotational culture. Tissue Eng A 15(11): 3213-3220.
6. Buckley CT, Thorpe SD, O'Brien FJ, et al. 2009; The effect of concentration, thermal history and cell seeding density on the initial mechanical properties of agarose hydrogels. J Mech Behav Biomed Mater 2(5): 512-521.
7. Buckley CT, Vinardell T, Thorpe SD, et al. 2010; Functional properties of cartilaginous tissues engineered from infrapatellar fat pad-derived mesenchymal stem cells. J Biomech 43(5): 920-926.
8. Byers BA, Mauck RL, Chiang IE, et al. 2008; Transient exposure to transforming growth factor β3 under serum-free conditions enhances the biomechanical and biochemical maturation of tissue-engineered cartilage. Tissue Eng A 14(11): 1821-1834.
9. Caplan AI. 1991; Mesenchymal stem cells. J Orthop Res 9(5): 641-650.
10. Colter DC, Class R, DiGirolamo CM, et al. 2000; Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 97(7): 3213-3218.
11. Connelly JT, Wilson CG, Levenston ME. 2008; Characterization of proteoglycan production and processing by chondrocytes and BMSCs in tissue engineered constructs. Osteoarthr Cartilage 16(9): 1092-1100.
12. Danišovič L, Varga I, Polák Š, et al. 2009; Comparison of in vitro chondrogenic potential of human mesenchymal stem cells derived from bone marrow and adipose tissue. Gen Physiol Biophys 28(1): 56-62.
13. De Bari C, Dell'Accio F, Tylzanowski P, et al. 2001; Multipotent mesenchymal stem cells from adult human synovial membrane. Arthritis Rheum 44(8): 1928-1942.
14. Diekman BO, Rowland CR, Caplan AI, et al. 2010; Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage derived matrix. Tissue Eng A 16(2): 523-533.
15. Dragoo JL, Samimi B, Zhu M, et al. 2003; Tissue-engineered cartilage and bone using stem cells from human infrapatellar fat pads. J Bone Joint Surg Br 85(5): 740-747.
16. English A, Jones EA, Corscadden D, et al. 2007; A comparative assessment of cartilage and joint fat pad as a potential source of cells for autologous therapy development in knee osteoarthritis. Rheumatology (Oxf) 46(11): 1676-1683.
17. Erickson GR, Gimble JM, Franklin DM, et al. 2002; Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290(2): 763-769.
18. Erickson IE, Huang AH, Chung C, et al. 2009; Differential maturation and structure-function relationships in mesenchymal stem cell- and chondrocyte-seeded hydrogels. Tissue Eng A 15(5): 1041-1052.
19. Estes BT, Diekman BO, Guilak F. 2008; Monolayer cell expansion conditions affect the chondrogenic potential of adipose-derived stem cells. Biotechnol Bioeng 99(4): 986-995.
20. Estes BT, Wu AW, Storms RW, et al. 2006; Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 209(3): 987-995.
21. Fuchs E, Segre JA. 2000; Stem cells: a new lease on life. Cell 100(1): 143-155.
22. Hadjantonakis A, Papaioannou V. 2001; The stem cells of early embryos. Differentiation 68(4-5): 159-166.
23. Hildner F, Peterbauer A, Neussl S, et al. 2009; Minipig derived mesenchymal stem cells from bone marrow and adipose tissue: comparison of adipogenic, osteogenic and chondrogenic differentiation potential. Eur Cells Mater 18(suppl 1): 40.
24. Huang AH, Farrell MJ, Mauck RL. 2010; Mechanics and mechanobiology of mesenchymal stem cell-based engineered cartilage. J Biomech 43(1): 128-136.
25. Huang JI, Kazmi N, Durbhakula MM, et al. 2005; Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison. J Orthop Res 23(6): 1383-1389.
26. Ignat'eva NY, Danilov NA, Averkiev SV, et al. 2007; Determination of hydroxyproline in tissues and the evaluation of the collagen content of the tissues. J Anal Chem 62(1): 51-57.
27. Im GI, Shin YW, Lee KB. 2005; Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthr Cartilage 13(10): 845-853.
28. Jakobsen RB, Shahdadfar A, Reinholt FP, et al. 2009; Chondrogenesis in a hyaluronic acid scaffold: comparison between chondrocytes and MSC from bone marrow and adipose tissue. Knee Surg Sports Traumatol Arthrosc [Epub ahead of print]. DOI: 10.1007/s00167-009-1017-4.
29. Johnstone B, Hering TM, Caplan AI, et al. 1998; In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238(1): 265-272.
30. Kafienah W, Sims TJ. 2004; Biochemical methods for the analysis of tissue-engineered cartilage. Methods Mol Biol 238: 217-230.
31. Kelly DJ, Prendergast PJ. 2004; Effect of a degraded core on the mechanical behaviour of tissue engineered cartilage constructs: a poro-elastic finite element analysis. Med Biol Eng Comput 42(1): 9-13.
32. Kelly TA, Ng KW, Ateshian GA, et al. 2009; Analysis of radial variations in material properties and matrix composition of chondrocyte-seeded agarose hydrogel constructs. Osteoarthr Cartilage 17(1): 73-82.
33. Kelly TA, Ng KW, Wang CC, et al. 2006; Spatial and temporal development of chondrocyte-seeded agarose constructs in free-swelling and dynamically loaded cultures. J Biomech 39(8): 1489-1497.
34. Khan WS, Adesida AB, Tew SR, et al. 2009; The epitope characterisation and the osteogenic differentiation potential of human fat pad-derived stem cells is maintained with ageing in later life. Injury 40(2): 150-157.
35. Khan WS, Adesida AB, Hardingham TE. 2007; 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 9(3): R55.
36. Khan WS, Tew SR, Adesida AB, et al. 2008; Human infrapatellar fat pad-derived stem cells express the pericyte marker 3G5 and show enhanced chondrogenesis after expansion in fibroblast growth factor-2. Arthritis Res Ther 10(4): R74.
37. Kisiday JD, Kopesky PW, Evans CH, et al. 2008; Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures. J Orthop Res 26(3): 322-331.
38. Koga H, Muneta T, Nagase T, et al. 2008; Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 333(2): 207-215.
39. Kopesky PW, Lee HY, Vanderploeg EJ, et al. 2010; Adult equine bone marrow stromal cells produce a cartilage-like ECM mechanically superior to animal-matched adult chondrocytes. Matrix Biol (in press).
40. Lennon DP, Caplan AI. 2006; Isolation of human marrow-derived mesenchymal stem cells. Exp Hematol 34(11): 1604-1605.
41. Maniatopoulos C, Sodek J, Melcher AH. 1988; Bone formation in vitro by stromal cells obtained from bone marrow of young adult rats. Cell Tissue Res 254(2): 317-330.
42. Marsano A, Millward-Sadler SJ, Salter DM, et al. 2007; Differential cartilaginous tissue formation by human synovial membrane, fat pad, meniscus cells and articular chondrocytes. Osteoarthr Cartilage 15(1): 48-58.
43. Mauck RL, Byers BA, Yuan X, et al. 2007; Regulation of cartilaginous ECM gene transcription by chondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech Model Mechanobiol 6(1-2): 113-125.
44. Mauck RL, Yuan X, Tuan RS. 2006; Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthr Cartilage 14(2): 179-189.
45. Meneghini RM, Pierson JL, Bagsby D, et al. 2007; The effect of retropatellar fat pad excision on patellar tendon contracture and functional outcomes after total knee arthroplasty. J Arthroplasty 22(6 suppl 2): 47-50.
46. Mochizuki T, Muneta T, Sakaguchi Y, et al. 2006; Higher chondrogenic potential of fibrous synovium- and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans. Arthritis Rheum 54(3): 843-853.
47. Ogilvie-Harris DJ, Giddens J. 1994; Hoffa's disease: arthroscopic resection of the infrapatellar fat pad. Arthroscopy 10(2): 184-187.
48. Pei M, He F, Vunjak-Novakovic G. 2008; Synovium-derived stem cell-based chondrogenesis. Differentiation 76(10): 1044-1056.
49. Pelttari K, Steck E, Richter W. 2008; The use of mesenchymal stem cells for chondrogenesis. Injury 39(suppl 1): S58-65.
50. Peng L, Jia Z, Yin X, et al. 2008; Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue. Stem Cells Dev 17(4): 761-773.
51. Pittenger MF, Mackay AM, Beck SC, et al. 1999; Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143-147.
52. Sakaguchi Y, Sekiya I, Yagishita K, et al. 2005; Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source.Arthritis Rheum 52(8): 2521-2529.
53. Schumann D, Kujat R, Nerlich M, et al. 2006; Mechanobiological conditioning of stem cells for cartilage tissue engineering. Biomed Mater Eng 16(4 suppl): S37-52.
54. Segawa Y, Muneta T, Makino H, et al. 2009; Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. J Orthop Res 27(4): 435-441.
55. Solchaga LA, Penick K, Porter JD, et al. 2005; FGF-2 enhances the mitotic and chondrogenic potentials of human adult bone marrow-derived mesenchymal stem cells. J Cell Physiol 203(2): 398-409.
56. Stewart AA, Byron CR, Pondenis H, et al. 2007; Effect of fibroblast growth factor-2 on equine mesenchymal stem cell monolayer expansion and chondrogenesis. Am J Vet Res 68(9): 941-945.
57. Thorpe SD, Buckley CT, Vinardell T, et al. 2008; Dynamic compression can inhibit chondrogenesis of mesenchymal stem cells. Biochem Biophys Res Commun 377(2): 458-462.
58. Thorpe SD, Buckley CT, Vinardell T, et al. 2010; The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGFβ3 induced chondrogenic differentiation. Ann Biomed Eng 38(9): 2896-2909.
59. Vacanti V, Kong E, Suzuki G, et al. 2005; Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture.J Cell Physiol 205(2): 194-201.
60. Vidal MA, Robinson SO, Lopez MJ, et al. 2008; Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow. Vet Surg 37(8): 713-724.
61. Vinardell T, Thorpe SD, Buckley CT, et al. 2009; Chondrogenesis and integration of mesenchymal stem cells within an in vitro cartilage defect repair model. Ann Biomed Eng 37(12): 2556-2565.
62. Wickham MQ, Erickson GR, Gimble JM, et al. 2003; Multipotent stromal cells derived from the infrapatellar fat pad of the knee. Clin Orthop Relat Res 412: 196-212.
63. Winter A, Breit S, Parsch D, et al. 2003; Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthrit Rheum 48(2): 418-429.
64. Yanada S, Ochi M, Kojima K, et al. 2006; Possibility of selection of chondrogenic progenitor cells by telomere length in FGF-2-expanded mesenchymal stromal cells. Cell Prolif 39(6): 575-584.
65. Zuk PA, Zhu M, Ashjian P, et al. 2002; Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13(12): 4279-4295.
66. Zuk PA, Zhu M, Mizuno H, et al. 2001; Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2): 211-228.