Yin Yang 1 (YY1) synergizes with Smad7 to inhibit TGF-β signaling in the nucleus

Science China Life Sciences

Volumn 57, Issue 1, 2014, Pages 128-136

  Yan, XiaoHua ^a   Pan, Jun ^a   Xiong, WanWan ^a   Cheng, MinZhang ^a   Sun, YingYuan ^a   Zhang, SuPing ^a   Chen, YeGuang ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

HDAC1; signaling regulation; Smad7; TGF ; transcriptional co repressor; YY1

Indexed keywords

PRIMER DNA; SMAD7 PROTEIN; SMAD7 PROTEIN, HUMAN; TRANSCRIPTION FACTOR YY1; TRANSFORMING GROWTH FACTOR BETA; YY1 PROTEIN, HUMAN;

ARTICLE; HEK293 CELL LINE; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BASE SEQUENCE; DNA PRIMERS; HEK293 CELLS; HUMANS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; YY1 TRANSCRIPTION FACTOR;

EID: 84891901026     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-013-4581-2     Document Type: Article

References (47)

1. Massague J. The transforming growth factor-beta family. Annu Rev Cell Biol, 1990, 6: 597-641.
2. Xu P, Liu J, Derynck R. Post-translational regulation of TGF-beta receptor and Smad signaling. FEBS Lett, 2012, 586: 1871-1884.
3. Moustakas A, Heldin CH. The regulation of TGFbeta signal transduction. Development, 2009, 136: 3699-3714.
4. Massague J, Chen YG. Controlling TGF-beta signaling. Genes Dev, 2000, 14: 627-644.
5. Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol, 2012, 13: 616-630.
6. Ikushima H, Miyazono K. Cellular context-dependent "colors" of transforming growth factor-beta signaling. Cancer Sci, 2010, 101: 306-312.
7. Heldin CH, Landstrom M, Moustakas A. Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol, 2009, 21: 166-176.
8. Massague J. TGFbeta in cancer. Cell, 2008, 134: 215-230.
9. Wu MY, Hill CS. TGF-beta superfamily signaling in embryonic development and homeostasis. Dev Cell, 2009, 16: 329-343.
10. Wrighton KH, Feng XH. To (TGF)beta or not to (TGF)beta: fine-tuning of Smad signaling via post-translational modifications. Cell Signal, 2008, 20: 1579-1591.
11. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature, 1997, 390: 465-471.
12. Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res, 2009, 19: 128-139.
13. Feng XH, Derynck R. Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol, 2005, 21: 659-693.
14. Yan X, Chen YG. Smad7: Not only a regulator, but also a cross-talk mediator of TGF-beta signalling. Biochem J, 2011, 434: 1-10.
15. Zhu L, Chen S, Chen Y. Unraveling the biological functions of Smad7 with mouse models. Cell Biosci, 2011, 1: 44.
16. Li R, Rosendahl A, Brodin G, Cheng AM, Ahgren A, Sundquist C, Kulkarni S, Pawson T, Heldin CH, Heuchel RL. Deletion of exon I of SMAD7 in mice results in altered B cell responses. J Immunol, 2006, 176: 6777-6784.
17. Chen Q, Chen H, Zheng D, Kuang C, Fang H, Zou B, Zhu W, Bu G, Jin T, Wang Z, Zhang X, Chen J, Field LJ, Rubart M, Shou W, Chen Y. Smad7 is required for the development and function of the heart. J Biol Chem, 2009, 284: 292-300.
18. Tojo M, Takebe A, Takahashi S, Tanaka K, Imamura T, Miyazono K, Chiba T. Smad7-deficient mice show growth retardation with reduced viability. J Biochem, 2012, 151: 621-631.
19. Shi W, Sun C, He B, Xiong W, Shi X, Yao D, Cao X. GADD34-PP1c recruited by Smad7 dephosphorylates TGFbeta type I receptor. J Cell Biol, 2004, 164: 291-300.
20. Zhang S, Fei T, Zhang L, Zhang R, Chen F, Ning Y, Han Y, Feng XH, Meng A, Chen YG. Smad7 antagonizes transforming growth factor beta signaling in the nucleus by interfering with functional Smad-DNA complex formation. Mol Cell Biol, 2007, 27: 4488-4499.
21. Shi X, Chen F, Yu J, Xu Y, Zhang S, Chen YG, Fang X. Study of interaction between Smad7 and DNA by single-molecule force spectroscopy. Biochem Biophys Res Commun, 2008, 377: 1284-1287.
22. Simonsson M, Heldin CH, Ericsson J, Gronroos E. The balance between acetylation and deacetylation controls Smad7 stability. J Biol Chem, 2005, 280: 21797-21803.
23. Kume S, Haneda M, Kanasaki K, Sugimoto T, Araki S, Isshiki K, Isono M, Uzu T, Guarente L, Kashiwagi A, Koya D. SIRT1 inhibits transforming growth factor beta-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J Biol Chem, 2007, 282: 151-158.
24. Emori T, Kitamura K, Okazaki K. Nuclear Smad7 overexpressed in mesenchymal cells acts as a transcriptional corepressor by interacting with HDAC-1 and E2F to regulate cell cycle. Biol Open, 2012, 1: 247-260.
25. Miyake T, Alli NS, McDermott JC. Nuclear function of Smad7 promotes myogenesis. Mol Cell Biol, 2010, 30: 722-735.
26. Hong S, Kim HY, Kim J, Ha HT, Kim YM, Bae E, Kim TH, Lee KC, Kim SJ. Smad7 protein induces interferon regulatory factor 1-dependent transcriptional activation of caspase 8 to restore tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis. J Biol Chem, 2013, 288: 3560-3570.
27. Lin X, Liang YY, Sun B, Liang M, Shi Y, Brunicardi FC, Shi Y, Feng XH. Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol Cell Biol, 2003, 23: 9081-9093.
28. Bai S, Shi X, Yang X, Cao X. Smad6 as a transcriptional corepressor. J Biol Chem, 2000, 275: 8267-8270.
29. Bai S, Cao X. A nuclear antagonistic mechanism of inhibitory Smads in transforming growth factor-beta signaling. J Biol Chem, 2002, 277: 4176-4182.
30. Atchison M, Basu A, Zaprazna K, Papasani M. Mechanisms of Yin Yang 1 in oncogenesis: the importance of indirect effects. Crit Rev Oncog, 2011, 16: 143-161.
31. Gordon S, Akopyan G, Garban H, Bonavida B. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene, 2006, 25: 1125-1142.
32. Zhang Q, Stovall DB, Inoue K, Sui G. The oncogenic role of Yin Yang 1. Crit Rev Oncog, 2011, 16: 163-197.
33. Deng Z, Wan M, Cao P, Rao A, Cramer SD, Sui G. Yin Yang 1 regulates the transcriptional activity of androgen receptor. Oncogene, 2009, 28: 3746-3757.
34. Xu J, De Zhu J, Ni M, Wan F, Gu JR. The ATF/CREB site is the key element for transcription of the human RNA methyltransferase like 1(RNMTL1) gene, a newly discovered 17p13. 3 gene. Cell Res, 2002, 12: 177-197.
35. Luke MP, Sui G, Liu H, Shi Y. Yin Yang 1 physically interacts with Hoxa11 and represses Hoxa11-dependent transcription. J Biol Chem, 2006, 281: 33226-33232.
36. Lu P, Hankel IL, Hostager BS, Swartzendruber JA, Friedman AD, Brenton JL, Rothman PB, Colgan JD. The developmental regulator protein Gon4l associates with protein YY1, co-repressor Sin3a, and histone deacetylase 1 and mediates transcriptional repression. J Biol Chem, 2011, 286: 18311-18319.
37. Kurisaki K, Kurisaki A, Valcourt U, Terentiev AA, Pardali K, Ten Dijke P, Heldin CH, Ericsson J, Moustakas A. Nuclear factor YY1 inhibits transforming growth factor beta- and bone morphogenetic protein-induced cell differentiation. Mol Cell Biol, 2003, 23: 4494-4510.
38. Lee KH, Evans S, Ruan TY, Lassar AB. SMAD-mediated modulation of YY1 activity regulates the BMP response and cardiac-specific expression of a GATA4/5/6-dependent chick Nkx2. 5 enhancer. Development, 2004, 131: 4709v4723.
39. Yan X, Lin Z, Chen F, Zhao X, Chen H, Ning Y, Chen YG. Human BAMBI cooperates with Smad7 to inhibit transforming growth factor-beta signaling. J Biol Chem, 2009, 284: 30097-30104.
40. Yan X, Zhang J, Sun Q, Tuazon PT, Wu X, Traugh JA, Chen YG. p21-Activated kinase 2 (PAK2) inhibits TGF-beta signaling in Madin-Darby canine kidney (MDCK) epithelial cells by interfering with the receptor-Smad interaction. J Biol Chem, 2012, 287: 13705-13712.
41. Yan X, Zhang J, Pan L, Wang P, Xue H, Zhang L, Gao X, Zhao X, Ning Y, Chen YG. TSC-22 promotes transforming growth factor beta-mediated cardiac myofibroblast differentiation by antagonizing Smad7 activity. Mol Cell Biol, 2011, 31: 3700-3709.
42. Kee K, Angeles VT, Flores M, Nguyen HN, Reijo Pera RA. Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature, 2009, 462: 222-225.
43. Chen YG, Liu F, Massague J. Mechanism of TGFbeta receptor inhibition by FKBP12. Embo J, 1997, 16: 3866-3876.
44. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J, 1998, 17: 3091-3100.
45. Pulaski L, Landstrom M, Heldin CH, Souchelnytskyi S. Phosphorylation of Smad7 at Ser-249 does not interfere with its inhibitory role in transforming growth factor-beta-dependent signaling but affects Smad7-dependent transcriptional activation. J Biol Chem, 2001, 276: 14344-14349.
46. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature, 1997, 389: 631-635.
47. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone MA Jr., Wrana JL, Falb D. The MAD-related protein Smad7 associates with the TGF? receptor and functions as an antagonist of TGF? signaling. Cell, 1997, 89: 1165-1173.