Tumor necrosis factor-α enhances the transcription of smad ubiquitination regulatory factor 1 in an activating protein-1- and runx2-dependent manner

Journal of Cellular Physiology

Volumn 228, Issue 5, 2013, Pages 1076-1086

  Lee, Hye Lim ^a   Yi, Tacghee ^b   Baek, Kyunghwa ^c   Kwon, Arang ^a   Hwang, Hyo Rin ^a   Qadir, Abdul S ^a   Park, Hyun Jung ^a   Woo, Kyung Mi ^a   Ryoo, Hyun Mo ^a   Kim, Gwan Shik ^a   Baek, Jeong Hwa ^a  

^a Seoul National University   (South Korea)

^b Inha University School of Medicine   (South Korea)

^c Gangneung Wonju National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C JUN; SMAD UBIQUITINATION REGULATORY FACTOR 1; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALVARIA; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; GENE ACTIVITY; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; REPORTER GENE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSACTIVATION; UBIQUITINATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION REGULATION; MAP KINASE KINASE 4; MAP KINASE SIGNALING SYSTEM; MICE; NF-KAPPA B; OSTEOBLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKULL; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84873812484     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24256     Document Type: Article

References (47)

1. Angel P, Karin M. 1991. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta 1072:129-157.
2. Blair HC, Sun L, Kohanski RA. 2007. Balanced regulation of proliferation, growth, differentiation, and degradation in skeletal cells. Ann N Y Acad Sci 1116:165-173.
3. Boyce BF, Li P, Yao Z, Zhang Q, Badell IR, Schwarz EM, O'Keefe RJ, Xing L. 2005. TNF-alpha and pathologic bone resorption. Keio J Med 54:127-131.
4. Chen G, Goeddel DV. 2002. TNF-R1 signaling: A beautiful pathway. Science 296:1634-1635.
5. Cheng PL, Lu H, Shelly M, Gao H, Poo MM. 2011. Phosphorylation of E3 ligase Smurf1 switches its substrate preference in support of axon development. Neuron 69:231-243.
6. Chinenov Y, Kerppola TK. 2001. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 20:2438-2452.
7. Chung KY, Agarwal A, Uitto J, Mauviel A. 1996. An AP-1 binding sequence is essential for regulation of the human alpha2(I) collagen (COL1A2) promoter activity by transforming growth factor-beta. J Biol Chem 271:3272-3278.
8. Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T, Miyazono K. 2001. Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem 276:12477-12480.
9. Feldmann M, Brennan FM, Maini RN. 1996. Rheumatoid arthritis. Cell 85:307-310.
10. Franceschi RT, Xiao G. 2003. Regulation of the osteoblast-specific transcription factor, Runx2: Responsiveness to multiple signal transduction pathways. J Cell Biochem 88:446-454.
11. Gilbert L, He X, Farmer P, Boden S, Kozlowski M, Rubin J, Nanes MS. 2000. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 141:3956-3964.
12. Gilbert L, He X, Farmer P, Rubin J, Drissi H, van Wijnen AJ, Lian JB, Stein GS, Nanes MS. 2002. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277:2695-2701.
13. Guo R, Yamashita M, Zhang Q, Zhou Q, Chen D, Reynolds DG, Awad HA, Yanoso L, Zhao L, Schwarz EM, Zhang YE, Boyce BF, Xing L. 2008. Ubiquitin ligase Smurf1 mediates tumor necrosis factor-induced systemic bone loss by promoting proteasomal degradation of bone morphogenetic signaling proteins. J Biol Chem 283:23084-23092.
14. Han H, Du B, Pan X, Liu J, Zhao Q, Lian X, Qian M, Liu M. 2010. CADPE inhibits PMA-stimulated gastric carcinoma cell invasion and matrix metalloproteinase-9 expression by FAK/MEK/ERK-mediated AP-1 activation. Mol Cancer Res 8:1477-1488.
15. Huang C, Rajfur Z, Yousefi N, Chen Z, Jacobson K, Ginsberg MH. 2009. Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration. Nat Cell Biol 11:624-630.
16. Jack GD, Zhang L, Friedman AD. 2009. M-CSF elevates c-Fos and phospho-C/EBPalpha(S21) via ERK whereas G-CSF stimulates SHP2 phosphorylation in marrow progenitors to contribute to myeloid lineage specification. Blood 114:2172-2180.
17. Jeon EJ, Lee KY, Choi NS, Lee MH, Kim HN, Jin YH, Ryoo HM, Choi JY, Yoshida M, Nishino N, Oh BC, Lee KS, Lee YH, Bae SC. 2006. Bone morphogenetic protein-2 stimulates Runx2 acetylation. J Biol Chem 281:16502-16511.
18. Jun JH, Yoon WJ, Seo SB, Woo KM, Kim GS, Ryoo HM, Baek JH. 2010. BMP2-activated Erk/MAP kinase stabilizes Runx2 by increasing p300 levels and histone acetyltransferase activity. J Biol Chem 285:36410-36419.
19. Kaneki H, Guo R, Chen D, Yao Z, Schwarz EM, Zhang YE, Boyce BF, Xing L. 2006. Tumor necrosis factor promotes Runx2 degradation through up-regulation of Smurf1 and Smurf2 in osteoblasts. J Biol Chem 281:4326-4333.
20. Kataoka H, Ochi M, Enomoto K, Yamaguchi A. 2000. Cloning and embryonic expression patterns of the zebrafish Runt domain genes, runxa and runxb. Mech Dev 98:139-143.
21. Kim YH, Kim JM, Kim SN, Kim GS, Baek JH. 2003. p44/42 MAPK activation is necessary for receptor activator of nuclear factor-kappaB ligand induction by high extracellular calcium. Biochem Biophys Res Commun 304:729-735.
22. Kim YJ, Lee MH, Wozney JM, Cho JY, Ryoo HM. 2004. Bone morphogenetic protein-2-induced alkaline phosphatase expression is stimulated by Dlx5 and repressed by Msx2. J Biol Chem 279:50773-50780.
23. Kuno H, Kurian SM, Hendy GN, White J, deLuca HF, Evans CO, Nanes MS. 1994. Inhibition of 1, 25-dihydroxyvitamin D3 stimulated osteocalcin gene transcription by tumor necrosis factor-alpha: Structural determinants within the vitamin D response element. Endocrinology 134:2524-2531.
24. Lee KS, Kim HJ, Li QL, Chi XZ, Ueta C, Komori T, Wozney JM, Kim EG, Choi JY, Ryoo HM, Bae SC. 2000. Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol Cell Biol 20:8783-8792.
25. Lee MH, Kim YJ, Kim HJ, Park HD, Kang AR, Kyung HM, Sung JH, Wozney JM, Ryoo HM. 2003. BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. J Biol Chem 278:34387-34394.
26. Lee HL, Yi T, Woo KM, Ryoo HM, Kim GS, Baek JH. 2010. Msx2 mediates the inhibitory action of TNF-alpha on osteoblast differentiation. Exp Mol Med 42:437-445.
27. Lee HL, Bae OY, Baek KH, Kwon A, Hwang HR, Qadir AS, Park HJ, Woo KM, Ryoo HM, Baek JH. 2011. High extracellular calcium-induced NFATc3 regulates the expression of receptor activator of NF-kappaB ligand in osteoblasts. Bone 49:242-249.
28. Levanon D, Bettoun D, Harris-Cerruti C, Woolf E, Negreanu V, Eilam R, Bernstein Y, Goldenberg D, Xiao C, Fliegauf M, Kremer E, Otto F, Brenner O, Lev-Tov A, Groner Y. 2002. The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J 21:3454-3463.
29. Moren A, Imamura T, Miyazono K, Heldin CH, Moustakas A. 2005. Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J Biol Chem 280:22115-22123.
30. Mukai T, Otsuka F, Otani H, Yamashita M, Takasugi K, Inagaki K, Yamamura M, Makino H. 2007. TNF-alpha inhibits BMP-induced osteoblast differentiation through activating SAPK/JNK signaling. Biochem Biophys Res Commun 356:1004-1010.
31. Murakami G, Watabe T, Takaoka K, Miyazono K, Imamura T. 2003. Cooperative inhibition of bone morphogenetic protein signaling by Smurf1 and inhibitory Smads. Mol Biol Cell 14:2809-2817.
32. Nakase T, Takaoka K, Masuhara K, Shimizu K, Yoshikawa H, Ochi T. 1997. Interleukin-1 beta enhances and tumor necrosis factor-alpha inhibits bone morphogenetic protein-2-induced alkaline phosphatase activity in MC3T3-E1 osteoblastic cells. Bone 21:17-21.
33. Narimatsu M, Bose R, Pye M, Zhang L, Miller B, Ching P, Sakuma R, Luga V, Roncari L, Attisano L, Wrana JL. 2009. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137:295-307.
34. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL. 2005. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307:1603-1609.
35. Park OJ, Kim HJ, Woo KM, Baek JH, Ryoo HM. 2010. FGF2-activated ERK mitogen-activated protein kinase enhances Runx2 acetylation and stabilization. J Biol Chem 285:3568-3574.
36. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massague J. 2007. Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25:441-454.
37. Shaulian E, Karin M. 2002. AP-1 as a regulator of cell life and death. Nat Cell Biol 4:E131-E136.
38. Sutherland JA, Cook A, Bannister AJ, Kouzarides T. 1992. Conserved motifs in Fos and Jun define a new class of activation domain. Genes Dev 6:1810-1819.
39. Wajant H, Pfizenmaier K, Scheurich P. 2003. Tumor necrosis factor signaling. Cell Death Differ 10:45-65.
40. Wang HR, Zhang Y, Ozdamar B, Ogunjimi AA, Alexandrova E, Thomsen GH, Wrana JL. 2003. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:1775-1779.
41. Xiao G, Jiang D, Thomas P, Benson MD, Guan K, Karsenty G, Franceschi RT. 2000. MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem 275:4453-4459.
42. Yamashita M, Ying SX, Zhang GM, Li C, Cheng SY, Deng CX, Zhang YE. 2005. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121:101-113.
43. Ying SX, Hussain ZJ, Zhang YE. 2003. Smurf1 facilitates myogenic differentiation and antagonizes the bone morphogenetic protein-2-induced osteoblast conversion by targeting Smad5 for degradation. J Biol Chem 278:39029-39036.
44. Zhao M, Qiao M, Oyajobi BO, Mundy GR, Chen D. 2003. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specific role in osteoblast differentiation. J Biol Chem 278:27939-27944.
45. Zhao M, Qiao M, Harris SE, Oyajobi BO, Mundy GR, Chen D. 2004. Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 279:12854-12859.
46. Zhao L, Huang J, Guo R, Wang Y, Chen D, Xing L. 2010. Smurf1 inhibits mesenchymal stem cell proliferation and differentiation into osteoblasts through JunB degradation. J Bone Miner Res 25:1246-1256.
47. Zhu H, Kavsak P, Abdollah S, Wrana JL, Thomsen GH. 1999. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400:687-693.