GSK-3α and GSK-3β proteins are involved in early stages of chondrocyte differentiation with functional redundancy through RelA protein phosphorylation

Journal of Biological Chemistry

Volumn 287, Issue 35, 2012, Pages 29227-29236

  Itoh, Shozo ^a   Saito, Taku ^a   Hirata, Makoto ^a,b   Ushita, Masahiro ^a   Ikeda, Toshiyuki ^a   Woodgett, James R ^c,d   Algül, Hana ^e   Schmid, Roland M ^e   Chung, Ung Il ^b   Kawaguchi, Hiroshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TORONTO   (Canada)

^d MOUNT SINAI HOSPITAL   (Canada)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHONDROCYTE DIFFERENTIATION; CHONDROCYTES; COMPUTATIONAL PREDICTIONS; FUNCTIONAL REDUNDANCY; GLYCOGEN SYNTHASE KINASE-3; ISOFORMS; KNOCK OUTS; PHOSPHORYLATION SITES; PROTEIN PHOSPHORYLATION; SKELETAL DEVELOPMENT; TYPE II COLLAGENS;

DNA SEQUENCES; GENES; REDUNDANCY;

PHOSPHORYLATION;

BETA CATENIN; COLLAGEN TYPE 2; GLYCOGEN SYNTHASE KINASE 3ALPHA; GLYCOGEN SYNTHASE KINASE 3BETA; ISOPROTEIN; THREONINE; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SOX9; WNT PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; CARTILAGE CELL; CELL DIFFERENTIATION; COL2A1 GENE; CONTROLLED STUDY; DWARFISM; EMBRYO; ENZYME ACTIVITY; ENZYME REGULATION; GENE; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REDUNDANCY ANALYSIS; SOX9 GENE;

ANIMALS; BETA CATENIN; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL LINE; CHONDROCYTES; COLLAGEN TYPE II; DWARFISM; GLYCOGEN SYNTHASE KINASE 3; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; SOX9 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RELA; WNT PROTEINS; WNT SIGNALING PATHWAY;

MUS;

EID: 84865519156     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.372086     Document Type: Article

References (45)

1. Karsenty, G. (2008) Transcriptional control of skeletogenesis. Annu. Rev. Genomics Hum. Genet. 9, 183-196
2. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
3. Doble, B. W., and Woodgett, J. R. (2003) GSK-3: tricks of the trade for a multitasking kinase. J. Cell Sci. 116, 1175-1186
4. Patel, S., Doble, B., and Woodgett, J. R. (2004) Glycogen synthase kinase-3 in insulin and Wnt signaling: a double-edged sword? Biochem. Soc. Trans. 32, 803-808
5. Kita, K., Kimura, T., Nakamura, N., Yoshikawa, H., and Nakano, T. (2008) PI3K/Akt signaling as a key regulatory pathway for chondrocyte terminal differentiation. Genes Cells 13, 839-850
6. Li, T. F., Zuscik, M. J., Ionescu, A. M., Zhang, X., Rosier, R. N., Schwarz, E. M., Drissi, H., and O'Keefe, R. J. (2004) PGE2 inhibits chondrocyte differentiation through PKA and PKC signaling. Exp. Cell Res. 300, 159-169
7. Day, T. F., Guo, X., Garrett-Beal, L., and Yang, Y. (2005) Wnt/β-Catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 8, 739-750
8. MacAulay, K., Doble, B. W., Patel, S., Hansotia, T., Sinclair, E. M., Drucker, D. J., Nagy, A., and Woodgett, J. R. (2007) Glycogen synthase kinase 3α-specific regulation of murine hepatic glycogen metabolism. Cell Metab. 6, 329-337
9. Kawasaki, Y., Kugimiya, F., Chikuda, H., Kamekura, S., Ikeda, T., Kawamura, N., Saito, T., Shinoda, Y., Higashikawa, A., Yano, F., Ogasawara, T., Ogata, N., Hoshi, K., Hofmann, F., Woodgett, J. R., Nakamura, K., Chung, U. I., and Kawaguchi, H. (2008) Phosphorylation of GSK-3β by cGMP-dependent protein kinase II promotes hypertrophic differentiation of murine chondrocytes. J. Clin. Invest. 118, 2506-2515
10. Hoeflich, K. P., Luo, J., Rubie, E. A., Tsao, M. S., Jin, O., and Woodgett, J. R. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature 406, 86-90
11. Gillespie, J. R., Ulici, V., Dupuis, H., Higgs, A., Dimattia, A., Patel, S., Woodgett, J. R., and Beier, F. (2011) Deletion of glycogen synthase kinase-3β in cartilage results in up-regulation of glycogen synthase kinase-3α protein expression. Endocrinology 152, 1755-1766
12. Zhou, Z., Xie, J., Lee, D., Liu, Y., Jung, J., Zhou, L., Xiong, S., Mei, L., and Xiong, W. C. (2010) Neogenin regulation of BMP-induced canonical Smad signaling and endochondral bone formation. Dev. Cell 19, 90-102
13. Kitamura, T. (1998)Newexperimental approaches in retrovirus-mediated expression screening. Int. J. Hematol. 67, 351-359
14. Linding, R., Jensen, L. J., Ostheimer, G. J., van Vugt, M. A., Jørgensen, C., Miron, I. M., Diella, F., Colwill, K., Taylor, L., Elder, K., Metalnikov, P., Nguyen, V., Pasculescu, A., Jin, J., Park, J. G., Samson, L. D., Woodgett, J. R., Russell, R. B., Bork, P., Yaffe, M. B., and Pawson, T. (2007) Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426
15. James, C. G., Stanton, L. A., Agoston, H., Ulici, V., Underhill, T. M., and Beier, F. (2010) Genome-wide analyses of gene expression during mouse endochondral ossification. PLoS One 5, e8693
16. Huang, B., Yang, X. D., Lamb, A., and Chen, L. F. (2010) Posttranslational modifications of NF-κB: another layer of regulation for NF-κB signaling pathway. Cell. Signal. 22, 1282-1290
17. Chen, L. F., and Greene, W. C. (2004) Shaping the nuclear action of NF-κB. Nat. Rev. Mol. Cell Biol. 5, 392-401
18. Hayden, M. S., and Ghosh, S. (2008) Shared principles in NF-κB signaling. Cell 132, 344-362
19. Algül, H., Treiber, M., Lesina, M., Nakhai, H., Saur, D., Geisler, F., Pfeifer, A., Paxian, S., and Schmid, R. M. (2007) Pancreas-specific RelA/p65 truncation increases susceptibility of acini to inflammation-associated cell death following cerulein pancreatitis. J. Clin. Invest. 117, 1490-1501
20. Doble, B. W., Patel, S., Wood, G. A., Kockeritz, L. K., and Woodgett, J. R. (2007) Functional redundancy of GSK-3α and GSK-3β in Wnt/β-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev. Cell 12, 957-971
21. Matsuda, T., Zhai, P., Maejima, Y., Hong, C., Gao, S., Tian, B., Goto, K., Takagi, H., Tamamori-Adachi, M., Kitajima, S., and Sadoshima, J. (2008) Distinct roles of GSK-3α and GSK-3β phosphorylation in the heart under pressure overload. Proc. Natl. Acad. Sci. U.S.A. 105, 20900-20905
22. Cho, J., Rameshwar, P., and Sadoshima, J. (2009) Distinct roles of glycogen synthase kinase (GSK)-3α and GSK-3β in mediating cardiomyocyte differentiation in murine bone marrow-derived mesenchymal stem cells. J. Biol. Chem. 284, 36647-36658
23. Kugimiya, F., Kawaguchi, H., Ohba, S., Kawamura, N., Hirata, M., Chikuda, H., Azuma, Y., Woodgett, J. R., Nakamura, K., and Chung, U. I. (2007) GSK-3β controls osteogenesis through regulating Runx2 activity. PLoS One 2, e837
24. McManus, E. J., Sakamoto, K., Armit, L. J., Ronaldson, L., Shpiro, N., Marquez, R., and Alessi, D. R. (2005) Role that phosphorylation of GSK-3 plays in insulin and Wnt signaling defined by knock-in analysis. EMBO J. 24, 1571-1583
25. Baryawno, N., Sveinbjörnsson, B., Eksborg, S., Chen, C. S., Kogner, P., and Johnsen, J. I. (2010) Small-molecule inhibitors of phosphatidylinositol 3-kinase/Akt signaling inhibit Wnt/β-catenin pathway cross-talk and suppress medulloblastoma growth. Cancer Res. 70, 266-276
26. Akiyama, H., Lyons, J. P., Mori-Akiyama, Y., Yang, X., Zhang, R., Zhang, Z., Deng, J. M., Taketo, M. M., Nakamura, T., Behringer, R. R., McCrea, P. D., and de Crombrugghe, B. (2004) Interactions between Sox9 and β-catenin control chondrocyte differentiation. Genes Dev. 18, 1072-1087
27. Beg, A. A., Sha, W. C., Bronson, R. T., Ghosh, S., and Baltimore, D. (1995) Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κ B. Nature 376, 167-170
28. Ushita, M., Saito, T., Ikeda, T., Yano, F., Higashikawa, A., Ogata, N., Chung, U., Nakamura, K., and Kawaguchi, H. (2009) Transcriptional induction of SOX9 by NF-κB family member RelA in chondrogenic cells. Osteoarthritis Cartilage 17, 1065-1075
29. Wu, S., Flint, J. K., Rezvani, G., and De Luca, F. (2007) Nuclear factor-κB p65 facilitates longitudinal bone growth by inducing growth plate chondrocyte proliferation and differentiation and by preventing apoptosis. J. Biol. Chem. 282, 33698-33706
30. Kanegae, Y., Tavares, A. T., Izpisúa Belmonte, J. C., and Verma, I. M. (1998) Role of Rel/NF-κB transcription factors during the outgrowth of the vertebrate limb. Nature 392, 611-614
31. Li, Q., Lu, Q., Hwang, J. Y., Büscher, D., Lee, K. F., Izpisua-Belmonte, J. C., and Verma, I. M. (1999) IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 13, 1322-1328
32. Janssen, R., van Wengen, A., Hoeve, M. A., ten Dam, M., van der Burg, M., van Dongen, J., van de Vosse, E., van Tol, M., Bredius, R., Ottenhoff, T. H., Weemaes, C., van Dissel, J. T., and Lankester, A. (2004) The same IκBα mutation in two related individuals leads to completely different clinical syndromes. J. Exp. Med. 200, 559-568
33. Steinbrecher, K. A., Wilson, W., 3rd, Cogswell, P. C., and Baldwin, A. S. (2005) Glycogen synthase kinase 3β functions to specify gene-specific, NF-κB-dependent transcription. Mol. Cell Biol. 25, 8444-8455
34. Ougolkov, A. V., Fernandez-Zapico, M. E., Savoy, D. N., Urrutia, R. A., and Billadeau, D. D. (2005) Glycogen synthase kinase-3β participates in nuclear factor κB-mediated gene transcription and cell survival in pancreatic cancer cells. Cancer Res. 65, 2076-2081
35. Gong, R., Rifai, A., Ge, Y., Chen, S., and Dworkin, L. D. (2008) Hepatocyte growth factor suppresses proinflammatory NF-κB activation through GSK-3β inactivation in renal tubular epithelial cells. J. Biol. Chem. 283, 7401-7410
36. Graham, J. R., Tullai, J. W., and Cooper, G. M. (2010) GSK-3 represses growth factor-inducible genes by inhibiting NF-κB in quiescent cells. J. Biol. Chem. 285, 4472-4480
37. Bachelder, R. E., Yoon, S. O., Franci, C., de Herreros, A. G., and Mercurio, A. M. (2005) Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J. Cell Biol. 168, 29-33
38. Deng, J., Miller, S. A., Wang, H. Y., Xia, W., Wen, Y., Zhou, B. P., Li, Y., Lin, S. Y., and Hung, M. C. (2002) β-Catenin interacts with and inhibits NF-κB in human colon and breast cancer. Cancer Cell 2, 323-334
39. Buss, H., Dörrie, A., Schmitz, M. L., Frank, R., Livingstone, M., Resch, K., and Kracht, M. (2004) Phosphorylation of serine 468 by GSK-3β negatively regulates basal p65 NF-κB activity. J. Biol. Chem. 279, 49571-49574
40. Iwamoto, M., Yagami, K., Lu Valle, P., Olsen, B. R., Petropoulos, C. J., Ewert, D. L., and Pacifici, M. (1993) Expression and role of c-myc in chondrocytes undergoing endochondral ossification. J. Biol. Chem. 268, 9645-9652
41. Ray, A., Bal, B. S., and Ray, B. K. (2005) Transcriptional induction of matrix metalloproteinase-9 in the chondrocyte and synoviocyte cells is regulated via a novel mechanism: evidence for functional cooperation between serum amyloid A-activating factor-1 and AP-1. J. Immunol. 175, 4039-4048
42. Liacini, A., Sylvester, J., Li, W. Q., and Zafarullah, M. (2002) Inhibition of interleukin-1-stimulated MAP kinases, activating protein-1 (AP-1), and nuclear factor κB (NF-κB) transcription factors down-regulates matrix metalloproteinase gene expression in articular chondrocytes. Matrix Biol. 21, 251-262
43. Li, S. W., Prockop, D. J., Helminen, H., Fässler, R., Lapveteläinen, T., Kiraly, K., Peltarri, A., Arokoski, J., Lui, H., and Arita, M. (1995) Transgenic mice with targeted inactivation of the Col2 α1 gene for collagen II develop a skeleton with membranous and periosteal bone but no endochondral bone. Genes Dev. 9, 2821-2830
44. Lefebvre, V., Huang, W., Harley, V. R., Goodfellow, P. N., and de Crombrugghe, B. (1997) SOX9 is a potent activator of the chondrocyte-specific enhancer of the Proα1(II) collagen gene. Mol. Cell Biol. 17, 2336-2346
45. Saito, T., Fukai, A., Mabuchi, A., Ikeda, T., Yano, F., Ohba, S., Nishida, N., Akune, T., Yoshimura, N., Nakagawa, T., Nakamura, K., Tokunaga, K., Chung, U. I., and Kawaguchi, H. (2010) Transcriptional regulation of endochondral ossification by HIF-2α during skeletal growth and osteoarthritis development. Nat. Med. 16, 678-686