The effect of dexamethasone and triiodothyronine on terminal differentiation of primary bovine chondrocytes and chondrogenically differentiated mesenchymal stem cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Randau, Thomas M ^a,c   Schildberg, Frank A ^b   Alini, Mauro ^c   Wimmer, Matthias D ^a   Haddouti, El Mustapha ^a   Gravius, Sascha ^a   Ito, Keita ^c,d   Stoddart, Martin J ^c  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c AO RESEARCH INSTITUTE   (Switzerland)

^d EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; ALKALINE PHOSPHATASE; COLLAGEN; COLLAGEN TYPE 10; DEXAMETHASONE; GLYCOSAMINOGLYCAN; LIOTHYRONINE; MESSENGER RNA; BIOLOGICAL MARKER; CALCIUM; DNA; HYDROXYPROLINE; MICROSPHERE; PROTEOGLYCAN;

ANIMAL CELL; ARTICLE; BONE TISSUE; BOVINE; CARTILAGE CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROGENESIS; CONTROLLED STUDY; DRUG EFFECT; ENCHONDRAL OSSIFICATION; EXTRACELLULAR MATRIX; GLYCOSAMINOGLYCAN METABOLISM; MESENCHYMAL STEM CELL; NONHUMAN; OSSIFICATION; OSTEOARTHRITIS; OSTEOLYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGENERATIVE MEDICINE; TISSUE ENGINEERING; ANIMAL; BOVINAE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HYPERTROPHY; MESENCHYMAL STROMA CELL; METABOLISM; STAINING; TIME; ULTRAMICROTOMY;

BOVINAE;

ALGINATES; ANIMALS; BIOLOGICAL MARKERS; CALCIUM; CATTLE; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN; CRYOULTRAMICROTOMY; DEXAMETHASONE; DNA; GENE EXPRESSION REGULATION; GLYCOSAMINOGLYCANS; HYDROXYPROLINE; HYPERTROPHY; MESENCHYMAL STROMAL CELLS; MICROSPHERES; PROTEOGLYCANS; RNA, MESSENGER; STAINING AND LABELING; TIME FACTORS; TRIIODOTHYRONINE;

EID: 84898478393     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072973     Document Type: Article

References (78)

1. Lidgren L (2003) The Bone and Joint Decade and the global economic and healthcare burden of musculoskeletal disease. J Rheumatol Suppl 67: 4-5. PubMed: 12926643.
2. Sun H, Liu W, Zhou G, Zhang W, Cui L et al. (2011) Tissue engineering of cartilage, tendon and bone. Front Med 5: 61-69. doi:10.1007/s11684-011-0122-1. PubMed: 21681676.
3. Zomorodian E, Baghaban Eslaminejad M (2012) Mesenchymal stem cells as a potent cell source for bone regeneration. Stem Cells Int, 2012: 2012: 980353. PubMed: 22448175
4. Kuo TK, Ho JH, Lee OK (2009) Mesenchymal stem cell therapy for nonmusculoskeletal diseases: emerging applications. Cell Transplant 18: 1013-1028. doi:10.3727/096368909X471206. PubMed: 19523328.
5. Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O et al. (1994) Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331: 889-895. doi:10.1056/NEJM199410063311401. PubMed: 8078550.
6. Lim HC, Bae JH, Song SH, Park YE, Kim SJ (2012) Current treatments of isolated articular cartilage lesions of the knee achieve similar outcomes. Clin Orthop Relat Res 470: 2261-2267. doi:10.1007/s11999-012-2304-9. PubMed: 22422593.
7. Dhinsa BS, Adesida AB (2012) Current clinical therapies for cartilage repair, their limitation and the role of stem cells. Curr Stem Cell Res Ther 7: 143-148. doi:10.2174/157488812799219009. PubMed: 22023635.
8. Pelttari K, Steck E, Richter W (2008) The use of mesenchymal stem cells for chondrogenesis. Injury 39 Suppl 1: S58-S65. doi:10.1016/j.injury.2008.01.038. PubMed: 18313473.
9. Pneumaticos SG, Triantafyllopoulos GK, Basdra EK, Papavassiliou AG (2010) Segmental bone defects: from cellular and molecular pathways to the development of novel biological treatments. J Cell Mol Med, 14: 2561-9. PubMed: 20345845.
10. Mistry AS, Mikos AG (2005) Tissue engineering strategies for bone regeneration. Adv Biochem Eng/Biotechnol 94: 1-22. doi:10.1007/b99997. PubMed: 15915866.
11. Cancedda R, Giannoni P, Mastrogiacomo M (2007) A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials 28: 4240-4250. doi:10.1016/j.biomaterials.2007.06.023. PubMed: 17644173.
12. Archer CW, Francis-West P (2003) The chondrocyte. Int J Biochem Cell Biol 35: 401-404. doi:10.1016/S1357-2725(02)00301-1. PubMed: 12565700.
13. Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423: 332-336. doi:10.1038/nature01657. PubMed: 12748651.
14. Fuerst M, Bertrand J, Lammers L, Dreier R, Echtermeyer F et al. (2009) Calcification of articular cartilage in human osteoarthritis. Arthritis Rheum 60: 2694-2703. doi:10.1002/art.24774. PubMed: 19714647.
15. Rutges JP, Duit RA, Kummer JA, Oner FC, van Rijen MH et al. (2010) Hypertrophic differentiation and calcification during intervertebral disc degeneration. Osteoarthritis Cartilage 18: 1487-1495. doi:10.1016/j.joca.2010.08.006. PubMed: 20723612.
16. Kawaguchi H (2008) Endochondral ossification signals in cartilage degradation during osteoarthritis progression in experimental mouse models. Mol Cells 25: 1-6. PubMed: 18319608.
17. Siebler T, Robson H, Shalet SM, Williams GR (2001) Glucocorticoids, thyroid hormone and growth hormone interactions: implications for the growth plate. Horm Res 56 Suppl 1: 7-12. doi:10.1159/000048127. PubMed: 11786678.
18. Yudt MR, Cidlowski JA (2002) The glucocorticoid receptor: coding a diversity of proteins and responses through a single gene. Mol Endocrinol 16: 1719-1726. doi:10.1210/me.2002-0106. PubMed: 12145329.
19. Eyigor S, Hepguler S, Sezak M, Oztop F, Capaci K (2006) Effects of intra-articular hyaluronic acid and corticosteroid therapies on articular cartilage in experimental severe osteoarthritis. Clin Exp Rheumatol 24: 724. PubMed: 17207396.
20. Derfoul A, Perkins GL, Hall DJ, Tuan RS (2006) Glucocorticoids promote chondrogenic differentiation of adult human mesenchymal stem cells by enhancing expression of cartilage extracellular matrix genes. Stem Cells 24: 1487-1495. doi:10.1634/stemcells.2005-0415. PubMed: 16469821.
21. Chrysis D, Ritzen EM, Sävendahl L (2003) Growth retardation induced by dexamethasone is associated with increased apoptosis of the growth plate chondrocytes. J Endocrinol 176: 331-337. doi:10.1677/joe.0.1760331. PubMed: 12630918.
22. Hossain MA, Park J, Choi SH, Kim G (2008) Dexamethasone induces apoptosis in proliferative canine tendon cells and chondrocytes. Vet Comp Orthop Traumatol 21: 337-342. PubMed: 18704240.
23. Zhang J, Lazar MA (2000) The mechanism of action of thyroid hormones. Annu Rev Physiol 62: 439-466. doi:10.1146/annurev.physiol.62.1.439. PubMed: 10845098.
24. Robson H, Siebler T, Stevens DA, Shalet SM, Williams GR (2000) Thyroid hormone acts directly on growth plate chondrocytes to promote hypertrophic differentiation and inhibit clonal expansion and cell proliferation. Endocrinology 141: 3887-3897. doi:10.1210/en.141.10.3887. PubMed: 11014246.
25. Grüters A, Krude H (2007) Update on the management of congenital hypothyroidism. Horm Res 68 Suppl 5: 107-111. doi: 10.1159/000110591. PubMed: 18174723.
26. Quarto R, Campanile G, Cancedda R, Dozin B (1992) Thyroid hormone, insulin, and glucocorticoids are sufficient to support chondrocyte differentiation to hypertrophy: a serum-free analysis. J Cell Biol 119: 989-995. doi:10.1083/jcb.119.4.989. PubMed: 1429844.
27. Ishikawa Y, Genge BR, Wuthier RE, Wu LN (1998) Thyroid hormone inhibits growth and stimulates terminal differentiation of epiphyseal growth plate chondrocytes. J Bone Miner Res 13: 1398-1411. doi: 10.1359/jbmr.1998.13.9.1398. PubMed: 9738512.
28. Alini M, Kofsky Y, Wu W, Pidoux I, Poole AR (1996) In serum-free culture thyroid hormones can induce full expression of chondrocyte hypertrophy leading to matrix calcification. J Bone Miner Res 11: 105-113. PubMed: 8770703.
29. Rosenthal AK, Heinkel D, Gohr CM (2003) Thyroxine stimulates transglutaminase activity in articular chondrocytes. Osteoarthritis Cartilage 11: 463-470. doi:10.1016/S1063-4584(03)00074-8. PubMed: 12801486.
30. Grad S, Zhou L, Gogolewski S, Alini M (2003) Chondrocytes seeded onto poly (L/DL-lactide) 80%/20% porous scaffolds: a biochemical evaluation. J Biomed Mater Res A 66: 571-579. PubMed: 12918040.
31. Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M et al. (2005) Isolation and multilineage differentiation of bovine bone marrow mesenchymal stem cells. Cell Tissue Res 319: 243-253. doi:10.1007/s00441-004-1012-5. PubMed: 15654654.
32. Stoddart MJ, Ettinger L, Häuselmann HJ (2006) Generation of a scaffold free cartilage-like implant from a small amount of starting material. J Cell Mol Med 10: 480-492. doi:10.1111/j.1582-4934.2006.tb00413.x. PubMed: 16796813.
33. Häuselmann HJ, Fernandes RJ, Mok SS, Schmid TM, Block JA et al. (1994) Phenotypic stability of bovine articular chondrocytes after longterm culture in alginate beads. J Cell Sci 107(1): 17-27. PubMed: 8175906.
34. Caron MM, Emans PJ, Coolsen MM, Voss L, Surtel DA et al. (2012) Redifferentiation of dedifferentiated human articular chondrocytes: comparison of 2D and 3D cultures. Osteoarthritis Cartilage 20: 1170-1178. doi:10.1016/j.joca.2012.06.016. PubMed: 22796508.
35. Häuselmann HJ, Aydelotte MB, Schumacher BL, Kuettner KE, Gitelis SH et al. (1992) Synthesis and turnover of proteoglycans by human and bovine adult articular chondrocytes cultured in alginate beads. Matrix 12: 116-129. doi:10.1016/S0934-8832(11)80053-3. PubMed: 1603034.
36. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU (1998) In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 238: 265-272. doi:10.1006/excr.1997.3858. PubMed: 9457080.
37. Bosnakovski D, Mizuno M, Kim G, Ishiguro T, Okumura M et al. (2004) Chondrogenic differentiation of bovine bone marrow mesenchymal stem cells in pellet cultural system. Exp Hematol 32: 502-509. doi: 10.1016/j.exphem.2004.02.009. PubMed: 15145219.
38. Kim YJ, Sah RL, Doong JY, Grodzinsky AJ (1988) Fluorometric assay of DNA in cartilage explants using Hoechst 33258. Anal Biochem 174: 168-176. doi:10.1016/0003-2697(88)90532-5. PubMed: 2464289.
39. Stegemann H, Stalder K (1967) Determination of hydroxyproline. Clin Chim Acta 18: 267-273. doi:10.1016/0009-8981(67)90167-2. PubMed: 4864804.
40. Masuda K, Sah RL, Hejna MJ, Thonar EJ (2003) A novel two-step method for the formation of tissue-engineered cartilage by mature bovine chondrocytes: the alginate-recovered-chondrocyte (ARC) method. J Orthop Res 21: 139-148. doi:10.1016/S0736-0266(02)00109-2. PubMed: 12507591.
41. Alini M, Matsui Y, Dodge GR, Poole AR (1992) The extracellular matrix of cartilage in the growth plate before and during calcification: changes in composition and degradation of type II collagen. Calcif Tissue Int 50: 327-335. doi:10.1007/BF00301630. PubMed: 1571844.
42. Randle WL, Cha JM, Hwang YS, Chan KL, Kazarian SG et al. (2007) Integrated 3-dimensional expansion and osteogenic differentiation of murine embryonic stem cells. Tissue Eng 13: 2957-2970. doi:10.1089/ten.2007.0072. PubMed: 17988191.
43. Ichinose S, Yamagata K, Sekiya I, Muneta T, Tagami M (2005) Detailed examination of cartilage formation and endochondral ossification using human mesenchymal stem cells. Clin Exp Pharmacol Physiol 32: 561-570. doi:10.1111/j.1440-1681.2005.04231.x. PubMed: 16026516.
44. Carson FL (1990) Histotechnology: a self-instructional text. Chicago: ASCP Press. 294pp.
45. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi:10.1006/meth.2001.1262. PubMed: 11846609.
46. Yuan JS, Reed A, Chen F, Stewart CN Jr. (2006) Statistical analysis of real-time PCR data. BMC Bioinformatics 7: 85. doi: 10.1186/1471-2105-7-85. PubMed: 16504059.
47. Quinn TM, Hunziker EB, Häuselmann HJ (2005) Variation of cell and matrix morphologies in articular cartilage among locations in the adult human knee. Osteoarthritis Cartilage 13: 672-678. doi:10.1016/j.joca.2005.04.011. PubMed: 15970445.
48. Hering TM, Kollar J, Huynh TD, Varelas JB, Sandell LJ (1994) Modulation of extracellular matrix gene expression in bovine highdensity chondrocyte cultures by ascorbic acid and enzymatic resuspension. Arch Biochem Biophys 314: 90-98. doi:10.1006/abbi.1994.1415. PubMed: 7944410.
49. Weisser J, Riemer S, Schmidl M, Suva LJ, Pöschl E et al. (2002) Four distinct chondrocyte populations in the fetal bovine growth plate: highest expression levels of PTH/PTHrP receptor, Indian hedgehog, and MMP-13 in hypertrophic chondrocytes and their suppression by PTH (1-34) and PTHrP (1-40). Exp Cell Res 279: 1-13. doi:10.1006/excr.2002.5580. PubMed: 12213208.
50. Benya PD, Shaffer JD (1982) Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30: 215-224. doi:10.1016/0092-8674(82)90027-7. PubMed: 7127471.
51. Bian L, Lima EG, Angione SL, Ng KW, Williams DY et al. (2008) Mechanical and biochemical characterization of cartilage explants in serum-free culture. J Biomech 41: 1153-1159. doi:10.1016/j.jbiomech.2008.01.026. PubMed: 18374344.
52. Katayama R, Wakitani S, Tsumaki N, Morita Y, Matsushita I et al. (2004) Repair of articular cartilage defects in rabbits using CDMP1 gene-transfected autologous mesenchymal cells derived from bone marrow. Rheumatology (Oxf) 43: 980-985. doi:10.1093/rheumatology/keh240. PubMed: 15187242.
53. Barry F, Boynton RE, Liu B, Murphy JM (2001) Chondrogenic differentiation of mesenchymal stem cells from bone marrow: differentiation-dependent gene expression of matrix components. Exp Cell Res 268: 189-200. doi:10.1006/excr.2001.5278. PubMed: 11478845.
54. Garate A, Murua A, Orive G, Hernández RM, Pedraz JL (2012) Stem cells in alginate bioscaffolds. Ther Deliv 3: 761-774. doi:10.4155/tde.12.53. PubMed: 22838071.
55. Malinin TI, Hornicek FJ (1997) Response of human chondrocytes cultured in vitro to human somatotropin, triiodothyronine, and thyroxine. Transplant Proc 29: 2037-2039. doi:10.1016/S0041-1345(97)00220-0. PubMed: 9193515.
56. Jones DG, Smith RL (1990) Stimulation of adult chondrocyte metabolism by a thyroid-derived factor. J Orthop Res 8: 227-233. doi: 10.1002/jor.1100080211. PubMed: 2303955.
57. Yates KE, Allemann F, Glowacki J (2005) Phenotypic analysis of bovine chondrocytes cultured in 3D collagen sponges: effect of serum substitutes 6. Cell Tissue Bank. pp. 45-54.
58. Boos N, Nerlich AG, Wiest I, von der Mark K, Ganz R et al. (1999) Immunohistochemical analysis of type-X-collagen expression in osteoarthritis of the hip joint. J Orthop Res 17: 495-502. doi:10.1002/jor.1100170406. PubMed: 10459754.
59. Adams SL, Cohen AJ, Lassová L (2007) Integration of signaling pathways regulating chondrocyte differentiation during endochondral bone formation. J Cell Physiol 213: 635-641. doi:10.1002/jcp.21262. PubMed: 17886256.
60. Jiang J, Leong NL, Mung JC, Hidaka C, Lu HH (2008) Interaction between zonal populations of articular chondrocytes suppresses chondrocyte mineralization and this process is mediated by PTHrP. Osteoarthritis Cartilage 16: 70-82. doi:10.1016/S1063-4584(08)60179-X. PubMed: 17644010.
61. Liu G, Kawaguchi H, Ogasawara T, Asawa Y, Kishimoto J et al. (2007) Optimal combination of soluble factors for tissue engineering of permanent cartilage from cultured human chondrocytes. J Biol Chem 282: 20407-20415. doi:10.1074/jbc.M608383200. PubMed: 17493933.
62. Rosenthal AK, Henry LA (1999) Thyroid hormones induce features of the hypertrophic phenotype and stimulate correlates of CPPD crystal formation in articular chondrocytes. J Rheumatol 26: 395-401. PubMed: 9972975.
63. Cheung JO, Grant ME, Jones CJ, Hoyland JA, Freemont AJ et al. (2003) Apoptosis of terminal hypertrophic chondrocytes in an in vitro model of endochondral ossification. J Pathol 201: 496-503. doi: 10.1002/path.1462. PubMed: 14595763.
64. Pourmand EP, Binderman I, Doty SB, Kudryashov V, Boskey AL (2007) Chondrocyte apoptosis is not essential for cartilage calcification: evidence from an in vitro avian model. J Cell Biochem 100: 43-57. doi: 10.1002/jcb.20977. PubMed: 16888817.
65. Mueller MB, Tuan RS (2008) Functional characterization of hypertrophy in chondrogenesis of human mesenchymal stem cells. Arthritis Rheum 58: 1377-1388. doi:10.1002/art.23370. PubMed: 18438858.
66. Boeloni JN, Ocarino NM, Melo AB, Silva JF, Castanheira P et al. (2009) Dose-dependent effects of triiodothyronine on the osteogenic differentiation of rat bone marrow mesenchymal stem cells. Horm Res 72: 88-97. doi:10.1159/000232161. PubMed: 19690426.
67. Studer D, Millan C, Öztürk E, Maniura-Weber K, Zenobi-Wong M (2012) Molecular and biophysical mechanisms regulating hypertrophic differentiation in chondrocytes and mesenchymal stem cells. Eur Cells Mater 24: 118-135; discussion 135. PubMed: 22828990
68. Hochberg Z (2002) Mechanisms of steroid impairment of growth. Horm Res 58 Suppl 1: 33-38. doi:10.1159/000064764. PubMed: 12373012.
69. Baron J, Huang Z, Oerter KE, Bacher JD, Cutler GB Jr. (1992) Dexamethasone acts locally to inhibit longitudinal bone growth in rabbits. Am J Physiol 263: E489-E492. PubMed: 1415528.
70. Heino TJ, Chagin AS, Takigawa M, Sävendahl L (2008) Effects of alendronate and pamidronate on cultured rat metatarsal bones: failure to prevent dexamethasone-induced growth retardation. Bone 42: 702-709. doi:10.1016/j.bone.2008.01.001. PubMed: 18276203.
71. D'Lima DD, Hashimoto S, Chen PC, Lotz MK, Colwell CW Jr. (2001) Prevention of chondrocyte apoptosis. J Bone Joint Surg Am 83-A Suppl 2: 25-26. PubMed: 11685840.
72. Richardson DW, Dodge GR (2003) Dose-dependent effects of corticosteroids on the expression of matrix-related genes in normal and cytokine-treated articular chondrocytes. Inflamm Res 52: 39-49. doi: 10.1007/s000110300045. PubMed: 12608648.
73. Busschers E, Holt JP, Richardson DW (2010) Effects of glucocorticoids and interleukin-1 beta on expression and activity of aggrecanases in equine chondrocytes. Am J Vet Res 71: 176-185. doi:10.2460/ajvr.71.2.176. PubMed: 20113225.
74. Na K, Choi SJ, Kim S, Sun BK, Woo DG et al. (2007) Enhancement of cell proliferation and differentiation by combination of ascorbate and dexamethasone in thermo-reversible hydrogel constructs embedded with rabbit chondrocytes. Biotechnol Lett 29: 1453-1457. doi:10.1007/s10529-007-9420-8. PubMed: 17589810.
75. Miyazaki Y, Tsukazaki T, Hirota Y, Yonekura A, Osaki M et al. (2000) Dexamethasone inhibition of TGF beta-induced cell growth and type II collagen mRNA expression through ERK-integrated AP-1 activity in cultured rat articular chondrocytes. Osteoarthritis Cartilage 8: 378-385. doi:10.1053/joca.1999.0313. PubMed: 10966845.
76. Chrysis D, Zaman F, Chagin AS, Takigawa M, Sävendahl L (2005) Dexamethasone induces apoptosis in proliferative chondrocytes through activation of caspases and suppression of the Aktphosphatidylinositol 3'-kinase signaling pathway. Endocrinology 146: 1391-1397. PubMed: 15576458.
77. Mehlhorn AT, Schmal H, Kaiser S, Lepski G, Finkenzeller G et al. (2006) Mesenchymal stem cells maintain TGF-beta-mediated chondrogenic phenotype in alginate bead culture. Tissue Eng 12: 1393-1403. doi:10.1089/ten.2006.12.1393. PubMed: 16846338.
78. Scotti C, Tonnarelli B, Papadimitropoulos A, Scherberich A, Schaeren S et al. (2010) Recapitulation of endochondral bone formation using human adult mesenchymal stem cells as a paradigm for developmental engineering. Proc Natl Acad Sci U S A 107: 7251-7256. doi:10.1073/pnas.1000302107. PubMed: 20406908.