Hydrogen peroxide inhibits formation of cartilage in chicken micromass cultures and decreases the activity of calcineurin: Implication of ERK1/2 and Sox9 pathways

Experimental Cell Research

Volumn 305, Issue 1, 2005, Pages 190-199

  Zákány, Róza ^a   Szíjgyártó, Zsolt ^a   Matta, Csaba ^a   Juhász, Tamás ^a   Csortos, Csilla ^a   Szucs, Kornélia ^a   Czifra, Gabriella ^a   Bíró, Tamás ^a   Módis, László ^a   Gergely, Pál ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Calcineurin; Chondrogenesis; Cyclosporine A; ERK1 2; Oxidative stress; PD098059; Protein phosphatases; Protein phosphorylation; Sox9

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; AGGRECAN; CALCINEURIN; CYCLOSPORIN A; HYDROGEN PEROXIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CARTILAGE; CELL COUNT; CELL VIABILITY; CHICKEN; CHONDROGENESIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 20144375217     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.12.016     Document Type: Article

References (56)

1. B. de Crombrugghe, V. Lefebvre, R.R. Behringer, W. Bi, S. Murakami, and W. Huang Transcriptional mechanisms of chondrocyte differentiation Matrix Biol. 19 2000 389 394
2. H. Akiyama, M.C. Chaboissier, J.F. Martin, A. Schedl, and B. de Crombrugghe The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 Genes Dev. 16 2002 2813 2828
3. W.M. Kulyk, J.L. Franklin, and L.M. Hoffman Sox9 expression during chondrogenesis in micromass cultures of embryonic limb mesenchyme Exp. Cell Res. 255 2000 327 332
4. V. Lefebvre, W. Huang, V.R. Harley, P.N. Goodfellow, and B. de Crombrugghe SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene Mol. Cell. Biol. 17 1997 2336 2346
5. W. Huang, X. Zhou, V. Lefebvre, and B. de Crombrugghe Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer Mol. Cell. Biol. 20 2000 4149 4158
6. D. Macias, Y. Ganan, J. Rodriguez-Leon, R. Merino, and J.M. Hurle Regulation by members of the transforming growth factor beta superfamily of the digital and interdigital fates of the autopodial limb mesoderm Cell Tissue Res. 296 1999 95 102
7. Y.S. Lee, and C.M. Chuong Activation of protein kinase A is a pivotal step involved in both BMP-2- and cyclic AMP-induced chondrogenesis J. Cell. Physiol. 170 1997 153 165
8. C.D. Oh, and J.S. Chun Signaling mechanisms leading to the regulation of differentiation and apoptosis of articular chondrocytes by insulin-like growth factor-1 J. Biol. Chem. 278 2003 36563 36571
9. S.H. Chang, C.D. Oh, M.S. Yang, S.S. Kang, Y.S. Lee, J.K. Sonn, and J.S. Chun Protein kinase C regulates chondrogenesis of mesenchymes via mitogen-activated protein kinase signaling J. Biol. Chem. 273 1998 19213 19219
10. R. Zakany, K. Szucs, E. Bako, S. Felszeghy, G. Czifra, T. Biro, L. Modis, and P. Gergely Protein phosphatase 2A is involved in the regulation of protein kinase A signaling pathway during in vitro chondrogenesis Exp. Cell Res. 275 2002 1 8
11. M. Tomita, M.I. Reinhold, J.D. Molkentin, and M.C. Naski Calcineurin and NFAT4 induce chondrogenesis J. Biol. Chem. 277 2002 42214 42218
12. F. Rusnak, and P. Mertz Calcineurin: form and function Physiol. Rev. 80 2000 1483 1521
13. S. Matsuda, and S. Koyasu Regulation of MAPK signaling pathways through immunophilin-ligand complex Curr. Top. Med. Chem. 3 2003 1358 1367
14. S. Matsuda, F. Shibasaki, K. Takehana, H. Mori, E. Nishida, and S. Koyasu Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T-cell activation EMBO Rep. 1 2000 428 434
15. Z. Chen, T.B. Gibson, F. Robinson, L. Silvestro, G. Pearson, B. Xu, A. Wright, C. Vanderbilt, and M.H. Cobb MAP kinases Chem. Rev. 101 2001 2449 2476
16. C. Hagemann, and J.L. Blank The ups and downs of MEK kinase interactions Cell Signalling 13 2001 863 875
17. M. Haneda, T. Sugimoto, and R. Kikkawa Mitogen-activated protein kinase phosphatase: a negative regulator of the mitogen-activated protein kinase cascade Eur. J. Pharmacol. 365 1999 1 7
18. C.D. Oh, S.H. Chang, Y.M. Yoon, S.J. Lee, Y.S. Lee, S.S. Kang, and J.S. Chun Opposing role of mitogen-activated protein kinase subtypes, erk-1/2 and p38, in the regulation of chondrogenesis of mesenchymes J. Biol. Chem. 275 2000 5613 5619
19. H.W. Lim, L. New, J. Han, and J.D. Molkentin Calcineurin enhances MAPK phosphatase-1 expression and p38 MAPK inactivation in cardiac myocytes J. Biol. Chem. 276 2001 15913 15919
20. L.J. De Windt, H.W. Lim, S. Haq, T. Force, and J.D. Molkentin Calcineurin promotes protein kinase C and c-Jun NH2-terminal kinase activation in the heart. Cross-talk between cardiac hypertrophic signaling pathways J. Biol. Chem. 275 2000 13571 13579
21. d.A. Gomez, S. Martinez-Martinez, J.L. Maldonado, I. Ortega-Perez, and J.M. Redondo A role for the p38 MAP kinase pathway in the nuclear shuttling of NFATp J. Biol. Chem. 275 2000 13872 13878
22. X. Wang, V.C. Culotta, and C.B. Klee Superoxide dismutase protects calcineurin from inactivation Nature 383 1996 434 437
23. T.A. Reiter, R.T. Abraham, M. Choi, and F. Rusnak Redox regulation of calcineurin in T-lymphocytes J. Biol. Inorg. Chem. 4 1999 632 644
24. K. Furuke, M. Shiraishi, H.S. Mostowski, and E.T. Bloom Fas ligand induction in human NK cells is regulated by redox through a calcineurin-nuclear factors of activated T cell-dependent pathway J. Immunol. 162 1999 1988 1993
25. R.T. Waldron, and E. Rozengurt Oxidative stress induces protein kinase D activation in intact cells. Involvement of Src and dependence on protein kinase C J. Biol. Chem. 275 2000 17114 17121
26. J.A. Rosado, P.C. Redondo, G.M. Salido, E. Gomez-Arteta, S.O. Sage, and J.A. Pariente Hydrogen peroxide generation induces pp60src activation in human platelets: evidence for the involvement of this pathway in store-mediated calcium entry J. Biol. Chem. 279 2004 1665 1675
27. A. Salmeen, J.N. Andersen, M.P. Myers, T.C. Meng, J.A. Hinks, N.K. Tonks, and D. Barford Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate Nature 423 2003 769 773
28. R. Bogumil, D. Namgaladze, D. Schaarschmidt, T. Schmachtel, S. Hellstern, R. Mutzel, and V. Ullrich Inactivation of calcineurin by hydrogen peroxide and phenylarsine oxide. Evidence for a dithiol-disulfide equilibrium and implications for redox regulation Eur. J. Biochem. 267 2000 1407 1415
29. T.A. Reiter, and F. Rusnak Is calcineurin a peroxide-specific sensor in T-lymphocytes? J. Biol. Inorg. Chem. 7 2002 823 834
30. Y.E. Henrotin, P. Bruckner, and J.P. Pujol The role of reactive oxygen species in homeostasis and degradation of cartilage Osteoarthr. Cartilage 11 2003 747 755
31. Y. Henrotin, G. by-Dupont, C. Deby, B.M. De, M. Lamy, and P. Franchimont Production of active oxygen species by isolated human chondrocytes Br. J. Rheumatol. 32 1993 562 567
32. E.J. Bates, C.C. Johnson, and D.A. Lowther Inhibition of proteoglycan synthesis by hydrogen peroxide in cultured bovine articular cartilage Biochim. Biophys. Acta 838 1985 221 228
33. R.E. Allen, D.R. Blake, N.B. Nazhat, and P. Jones Superoxide radical generation by inflamed human synovium after hypoxia Lancet 2 1989 282 283
34. P.I. Mapp, M.C. Grootveld, and D.R. Blake Hypoxia, oxidative stress and rheumatoid arthritis Br. Med. Bull. 51 1995 419 436
35. B. Borsiczky, Z. Szabo, M.T. Jaberansari, P.P. Mack, and E. Roth Activated PMNs lead to oxidative stress on chondrocytes: a study of swine knees Acta Orthop. Scand. 74 2003 190 195
36. I. Mazzetti, B. Grigolo, L. Pulsatelli, P. Dolzani, T. Silvestri, L. Roseti, R. Meliconi, and A. Facchini Differential roles of nitric oxide and oxygen radicals in chondrocytes affected by osteoarthritis and rheumatoid arthritis Clin. Sci. (Lond.) 101 2001 593 599
37. M. Solursh, P.B. Ahrens, and R.S. Reiter A tissue culture analysis of the steps in limb chondrogenesis In Vitro 14 1978 51 61
38. R. Zakany, E. Bako, S. Felszeghy, K. Hollo, M. Balazs, H. Bardos, P. Gergely, and L. Modis Okadaic acid-induced inhibition of protein phosphatase 2A enhances chondrogenesis in chicken limb bud micromass cell cultures Anat. Embryol. (Berl.) 203 2001 23 34
39. L. Modis Organization of the Extracellular Matrix: A Polarization Microscopic Approach 1991 CRC Press, Inc. Boca Raton, FL, USA
40. E. Szabo, L. Virag, E. Bakondi, L. Gyure, G. Hasko, P. Bai, J. Hunyadi, P. Gergely, and C. Szabo Peroxynitrite production, DNA breakage, and poly(ADP-ribose) polymerase activation in a mouse model of oxazolone-induced contact hypersensitivity J. Invest. Dermatol. 117 2001 74 80
41. S.D. Yang, E.A. Tallant, and W.Y. Cheung Calcineurin is a calmodulin-dependent protein phosphatase Biochem. Biophys. Res. Commun. 106 1982 1419 1425
42. P. Cohen, J.G. Foulkes, C.F. Holmes, G.A. Nimmo, and N.K. Tonks Protein phosphatase inhibitor-1 and inhibitor-2 from rabbit skeletal muscle Methods Enzymol. 159 1988 427 437
43. B. Kurz, J. Steinhagen, and M. Schunke Articular chondrocytes and synoviocytes in a co-culture system: influence on reactive oxygen species-induced cytotoxicity and lipid peroxidation Cell Tissue Res. 296 1999 555 563
44. S. Asada, K. Fukuda, M. Oh, C. Hamanishi, and S. Tanaka Effect of hydrogen peroxide on the metabolism of articular chondrocytes Inflamm. Res. 48 1999 399 403
45. H.S. Kim, M.C. Song, I.H. Kwak, T.J. Park, and I.K. Lim Constitutive induction of p-Erk1/2 accompanied by reduced activities of protein phosphatases 1 and 2A and MKP3 due to reactive oxygen species during cellular senescence J. Biol. Chem. 278 2003 37497 37510
46. I.A. Graef, F. Chen, L. Chen, A. Kuo, and G.R. Crabtree Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature Cell 105 2001 863 875
47. T. Matsushita, K. Fukuda, K. Yamazaki, N. Yamamoto, S. Asada, K. Yoshida, H. Munakata, and C. Hamanishi Hypoxia-induced nitric oxide protects chondrocytes from damage by hydrogen peroxide Inflamm. Res. 53 2004 344 350
48. S. Baksh, and S.J. Burakoff The role of calcineurin in lymphocyte activation Semin. Immunol. 12 2000 405 415
49. L.J. De Windt, H.W. Lim, T. Taigen, D. Wencker, G. Condorelli, G.W. Dorn, R.N. Kitsis, and J.D. Molkentin Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: an apoptosis-independent model of dilated heart failure Circ. Res. 86 2000 255 263
50. R.A. Schulz, and K.E. Yutzey Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development Dev. Biol. 266 2004 1 16
51. X.C. Bai, D. Lu, J. Bai, H. Zheng, Z.Y. Ke, X.M. Li, and S.Q. Luo Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB Biochem. Biophys. Res. Commun. 314 2004 197 207
52. B.E. Bobick, and W.M. Kulyk The MEK-ERK signaling pathway is a negative regulator of cartilage-specific gene expression in embryonic limb mesenchyme J. Biol. Chem. 279 2004 4588 4595
53. S. Murakami, M. Kan, W.L. McKeehan, and B. de Crombrugghe Up-regulation of the chondrogenic Sox9 gene by fibroblast growth factors is mediated by the mitogen-activated protein kinase pathway Proc. Natl. Acad. Sci. U. S. A. 97 2000 1113 1118
54. V.M. Coghlan, B.A. Perrino, M. Howard, L.K. Langeberg, J.B. Hicks, W.M. Gallatin, and J.D. Scott Association of protein kinase A and protein phosphatase 2B with a common anchoring protein Science 267 1995 108 111
55. R.D. Cauthron, K.B. Carter, S. Liauw, and R.A. Steinberg Physiological phosphorylation of protein kinase A at Thr-197 is by a protein kinase A kinase Mol. Cell. Biol. 18 1998 1416 1423
56. Y. Hashimoto, and T.R. Soderling Regulation of calcineurin by phosphorylation. Identification of the regulatory site phosphorylated by Ca2+/calmodulin-dependent protein kinase II and protein kinase C J. Biol. Chem. 264 1989 16524 16529