The candidate tumor suppressor BTG3 is a transcriptional target of p53 that inhibits E2F1

Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage‐inducible, CHK1‐modulated genes, we have identified BTG3 ( B ‐cell t ranslocation g ene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in...

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Published in	The EMBO journal Vol. 26; no. 17; pp. 3968 - 3980
Main Authors	Ou, Yi-Hung, Chung, Pei-Han, Hsu, Fu-Fei, Sun, Te-Ping, Chang, Wen-Ying, Shieh, Sheau-Yann
Format	Journal Article
Language	English
Published	Chichester, UK John Wiley & Sons, Ltd 05.09.2007 Nature Publishing Group UK Springer Nature B.V Nature Publishing Group
Subjects	BTG Cell cycle Cell Line, Tumor Cellular biology Deoxyribonucleic acid DNA DNA Damage E2F1 E2F1 Transcription Factor - antagonists & inhibitors E2F1 Transcription Factor - metabolism Genomics Humans Inhibitor drugs Introns Molecular biology Oligonucleotide Array Sequence Analysis p53 Protein Binding Proteins - genetics Proteins - metabolism Transcriptional Activation Translocation Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism Tumors BTG E2F1 p53
Online Access	Get full text
ISSN	0261-4189 1460-2075 1460-2075
DOI	10.1038/sj.emboj.7601825

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Abstract	Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage‐inducible, CHK1‐modulated genes, we have identified BTG3 ( B ‐cell t ranslocation g ene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in intron 2 of the gene both in vitro and in vivo , and depletion of p53 by small interfering RNA (siRNA) abolishes DNA damage‐induced expression of the gene. Furthermore, ablation of BTG3 by siRNA in cancer cells results in accelerated exit from the DNA damage‐induced G2/M block. In vitro , BTG3 binds to and inhibits E2F1 through an N‐terminal domain including the conserved box A. Deletion of the interaction domain in BTG3 abrogates not only its growth suppression activity, but also its repression on E2F1‐mediated transactivation. We also present evidence that by disrupting the DNA binding activity of E2F1, BTG3 participates in the regulation of E2F1 target gene expression. Therefore, our studies have revealed a previously unidentified pathway through which the activity of E2F1 may be guarded by activated p53.
AbstractList	Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage-inducible, CHK1-modulated genes, we have identified BTG3 (B-cell translocation gene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in intron 2 of the gene both in vitro and in vivo, and depletion of p53 by small interfering RNA (siRNA) abolishes DNA damage-induced expression of the gene. Furthermore, ablation of BTG3 by siRNA in cancer cells results in accelerated exit from the DNA damage-induced G2/M block. In vitro, BTG3 binds to and inhibits E2F1 through an N-terminal domain including the conserved box A. Deletion of the interaction domain in BTG3 abrogates not only its growth suppression activity, but also its repression on E2F1- mediated transactivation. We also present evidence that by disrupting the DNA binding activity of E2F1, BTG3 participates in the regulation of E2F1 target gene expression. Therefore, our studies have revealed a previously unidentified pathway through which the activity of E2F1 may be guarded by activated p53. Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage‐inducible, CHK1‐modulated genes, we have identified BTG3 ( B ‐cell t ranslocation g ene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in intron 2 of the gene both in vitro and in vivo , and depletion of p53 by small interfering RNA (siRNA) abolishes DNA damage‐induced expression of the gene. Furthermore, ablation of BTG3 by siRNA in cancer cells results in accelerated exit from the DNA damage‐induced G2/M block. In vitro , BTG3 binds to and inhibits E2F1 through an N‐terminal domain including the conserved box A. Deletion of the interaction domain in BTG3 abrogates not only its growth suppression activity, but also its repression on E2F1‐mediated transactivation. We also present evidence that by disrupting the DNA binding activity of E2F1, BTG3 participates in the regulation of E2F1 target gene expression. Therefore, our studies have revealed a previously unidentified pathway through which the activity of E2F1 may be guarded by activated p53. Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage-inducible, CHK1-modulated genes, we have identified BTG3 (B-cell translocation gene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in intron 2 of the gene both in vitro and in vivo, and depletion of p53 by small interfering RNA (siRNA) abolishes DNA damage-induced expression of the gene. Furthermore, ablation of BTG3 by siRNA in cancer cells results in accelerated exit from the DNA damage-induced G2/M block. In vitro, BTG3 binds to and inhibits E2F1 through an N-terminal domain including the conserved box A. Deletion of the interaction domain in BTG3 abrogates not only its growth suppression activity, but also its repression on E2F1-mediated transactivation. We also present evidence that by disrupting the DNA binding activity of E2F1, BTG3 participates in the regulation of E2F1 target gene expression. Therefore, our studies have revealed a previously unidentified pathway through which the activity of E2F1 may be guarded by activated p53.Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage-inducible, CHK1-modulated genes, we have identified BTG3 (B-cell translocation gene 3) as a direct p53 target. The p53 transcription factor binds to a consensus sequence located in intron 2 of the gene both in vitro and in vivo, and depletion of p53 by small interfering RNA (siRNA) abolishes DNA damage-induced expression of the gene. Furthermore, ablation of BTG3 by siRNA in cancer cells results in accelerated exit from the DNA damage-induced G2/M block. In vitro, BTG3 binds to and inhibits E2F1 through an N-terminal domain including the conserved box A. Deletion of the interaction domain in BTG3 abrogates not only its growth suppression activity, but also its repression on E2F1-mediated transactivation. We also present evidence that by disrupting the DNA binding activity of E2F1, BTG3 participates in the regulation of E2F1 target gene expression. Therefore, our studies have revealed a previously unidentified pathway through which the activity of E2F1 may be guarded by activated p53.
Author	Sun, Te‐Ping Ou, Yi‐Hung Chung, Pei‐Han Chang, Wen‐Ying Hsu, Fu‐Fei Shieh, Sheau‐Yann
Author_xml	– sequence: 1 givenname: Yi-Hung surname: Ou fullname: Ou, Yi-Hung organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan – sequence: 2 givenname: Pei-Han surname: Chung fullname: Chung, Pei-Han organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan – sequence: 3 givenname: Fu-Fei surname: Hsu fullname: Hsu, Fu-Fei organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan – sequence: 4 givenname: Te-Ping surname: Sun fullname: Sun, Te-Ping organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan – sequence: 5 givenname: Wen-Ying surname: Chang fullname: Chang, Wen-Ying organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan – sequence: 6 givenname: Sheau-Yann surname: Shieh fullname: Shieh, Sheau-Yann email: sy88@ibms.sinica.edu.tw organization: Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/17690688$$D View this record in MEDLINE/PubMed
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Proc Natl Acad Sci USA 92: 12146-12150 Yamamoto N, Uzawa K, Yakushij T, Shibahara T, Noma H, Tanzawa H (2001) Analysis of the ANA gene as a candidate for the chromosome 21q oral cancer susceptibility locus. Br J Cancer 84: 754-759 Guardavaccaro K, Corrente G, Covone F, Micheli L, Dagnano I, Starace G, Caruso M, Tirone F (2000) Arrest of G1-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of Cyclin D1 transcription. Mol Cell Biol 20: 1797-1815 Dimova DK, Dyson NJ (2005) The E2F transcriptional network: old acquaintances with new faces. Oncogene 24: 2810-2826 Rahmani Z (2006) APRO4 negatively regulates Src tyrosine kinase activity in PC12 cells. J Cell Sci 119: 646-658 Wei J-H, Chou Y-F, Ou Y-H, Yeh Y-H, Tyan S-W, Sun T-P, Shen C-Y, Shieh S-Y (2005) TTK/hMps1 participates in the regulation of DNA damage checkpoint response by phosphorylating CHK2 on Threonine 68. J Biol Chem 280: 7748-7757 Ou Y-H, Chung P-H, Sun T-P, Shieh S-Y (2005) P53 C-terminal phosphorylation by CHK1 and CHK2 participates in the regulation of DNA-damage-induced C-terminal acetylation. Mol Biol Cell 16: 1684-1695 Wu Z-H, Shi Y, Tibbetts RS, Miyamoto S (2006) Molecular linkage between the kinase ATM and NF-κB signaling in response to genotoxic stimuli. Science 311: 1141-1146 Guehenneux F, Duret L, Callanan MB, Bouhas R, Hayette S, Berthet C, Samarut C, Rimokh R, Birot AM, Wang Q, Magaud JP, Rouault JP (1997) Cloning of the mouse BTG3 gene and definition of a new gene family (the BTG family) involved in the negative control of the cell cycle. Leukemia 11: 370-375 Field SJ, Tsai F-Y, Kuo F, Zubiaga AM, Kaelin Jr WG, Livingston DM, Orkin SH, Greenberg ME (1996) E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85: 549-561 Burri N, Shaw P, Bouzourene H, Sordat I, Sordat B, Gillet M, Schorderet D, Bosman FT, Chaubert P (2001) Methylation silencing and mutations of the p14ARF and p16ink4a genes in colon cancer. Lab Invest 81: 217-229 Bradbury A, Possenti R, Shooter EM, Tirone F (1991) Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Proc Natl Acad Sci USA 88: 3353-3357 Matsuda S, Rouault R-P, Magaud J-P, Berthet C (2001) In search of a function for the TES21/PC3/BTG1/TOB family. FEBS Lett 497: 67-72 Montagnoli A, Guardavaccaro D, Starace G, Tirone F (1996) Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ 7: 1327-1336 Harris SL, Levine AJ (2005) The p53 pathway: positive and negative feedback loops. Oncogene 24: 2899-2908 Rouault J-P, Falette N, Guehenneux F, Guillot C, Rimokh R, Wang Q, Berthet C, Moyret-Lalle C, Savatier P, Pain B, Shaw P, Berger R, Samarut J, Magaud J-P, Ozturk M, Samarut C, Puisieux A (1996) Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat Genet 14: 482-486 Rodier A, Marchal-Victorion S, Rochard P, Casas F, Cassar-Malek I, Rouault J-P, Magaud J-P, Mason DY, Wrutniak C, Cabello G (1999) BTG1: a triiodothyronine target involved in the myogenic influence of the hormone. Exp Cell Res 249: 337-348 Yoshida Y, Matsuda S, Ikematsu N, Kawamura-Tsuzuku J, Inazawa J, Umenori H, Yamamoto T (1998) ANA, a novel member of Tob/BTG1 family, is expressed in the ventricular zone of the developing central nervous system. Oncogene 16: 2687-2693 Delavaine L, La Thangue NB (1999) Control of E2F activity by p21Waf1/Cip1. Oncogene 18: 5381-5392 Martinez-Balbás MA, Bauer U-M, Nielsen SJ, Brehm A, Kouzarides T (2000) Regulation of E2F1 activity by acetylation. EMBO J 19: 662-671 Lin W-C, Lin F-T, Nevins JR (2001) Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev 15: 1833-1844 Muller H, Bracken AP, Vernell R, Moroni MC, Christians F, Grassilli E, Prosperimi E, Vigo E, Oliner Jd, Helin K (2001) E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev 15: 267-285 Lavin MF, Gueven N (2006) The complexity of p53 stabilization and activation. Cell Death Differ 13: 941-950 Watanabe G, Albanese C, Lee RJ, Reutens A, Vairo G, Henglein B, Pestell RG (1998) Inhibition of Cyclin D1 kinase activity is associated with E2F-mediated inhibition os Cyclin D1 promoter activity through E2F and Sp1. Mol Cell Biol 18: 3212-3222 Boiko AD, Porteous S, Razorenova OV, Krivokrysenko VI, Williams BR, Gudkov AV (2006) A systematic search for downstream mediators of tumor suppressor function of p53 reveals a major role of BTG2 in suppression of Ras-induced transformation. Genes Dev 20: 236-252 Wang X, Zou L, Lu T, Bao S, Hurov KE, Hittelman WN, Elledge SJ, Li L (2006) Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell 23: 331-341 Komori H, Enomoto M, Nakamura M, Iwanaga R, Ohtani K (2005) Distinct E2F-mediated transcriptional program regulates p14ARF gene expression. EMBO J 24: 3724-3736 Laptenko O, Prives C (2006) The transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 13: 951-961 Rouault J-P, Rimokh R, Tessa C, Paranhos G, Ffrench M, Duret L, Garoccio M, Germain D, Samarut J, Magaud J-P (1992) BTG1, a member of a new family of antiproliferative genes. EMBO J 11: 1663-1670 Altin JG, Kujubu DA, Raffion S, Eveleth DD, Herschman HR, Bradshaw RA (1991) Differntial induction of primary-response (TIS) genes in PC12 pheochromocytoma cells and the unresponsive variant PC12nnr5. J Biol Chem 266: 5401-5406 Yamasaki L, Jacks T, Bronson R, Goillot E, Harlow E, Dyson NJ (1996) Tumor induction and tissue atrophy in mice lacking E2F1. Cell 85: 537-548 Fletcher BS, Lim RW, Varnum BC, Kujubu DA, Koski RA, Herschman HR (1991) Structure and expression of TIS21, a primary response gene induced by growth factors and tumor promoters. J Biol Chem 266: 14511-14518 Pediconi N, Ianari A, Costanzo A, Belloni L, Gallo R, Cimino L, Porcellini A, Screpanti I, Balsano C, Alesse E, Gulino A, Levrero M (2003) Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nat Cell Biol 5: 552-558 Bracken AP, Ciro M, Cocito A, Helin K (2004) E2F target genes: unraveling the biology. 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Hum Mutat 19: 607-614 – reference: Wang X, Zou L, Lu T, Bao S, Hurov KE, Hittelman WN, Elledge SJ, Li L (2006) Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell 23: 331-341 – reference: Montagnoli A, Guardavaccaro D, Starace G, Tirone F (1996) Overexpression of the nerve growth factor-inducible PC3 immediate early gene is associated with growth inhibition. Cell Growth Differ 7: 1327-1336 – reference: Rodier A, Marchal-Victorion S, Rochard P, Casas F, Cassar-Malek I, Rouault J-P, Magaud J-P, Mason DY, Wrutniak C, Cabello G (1999) BTG1: a triiodothyronine target involved in the myogenic influence of the hormone. Exp Cell Res 249: 337-348 – reference: Bradbury A, Possenti R, Shooter EM, Tirone F (1991) Molecular cloning of PC3, a putatively secreted protein whose mRNA is induced by nerve growth factor and depolarization. Proc Natl Acad Sci USA 88: 3353-3357 – reference: Guardavaccaro K, Corrente G, Covone F, Micheli L, Dagnano I, Starace G, Caruso M, Tirone F (2000) Arrest of G1-S progression by the p53-inducible gene PC3 is Rb dependent and relies on the inhibition of Cyclin D1 transcription. Mol Cell Biol 20: 1797-1815 – reference: Laptenko O, Prives C (2006) The transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ 13: 951-961 – reference: Guehenneux F, Duret L, Callanan MB, Bouhas R, Hayette S, Berthet C, Samarut C, Rimokh R, Birot AM, Wang Q, Magaud JP, Rouault JP (1997) Cloning of the mouse BTG3 gene and definition of a new gene family (the BTG family) involved in the negative control of the cell cycle. Leukemia 11: 370-375 – reference: Wu Z-H, Shi Y, Tibbetts RS, Miyamoto S (2006) Molecular linkage between the kinase ATM and NF-κB signaling in response to genotoxic stimuli. 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inhibition of Cyclin D1 transcription publication-title: Mol Cell Biol – volume: 266 start-page: 5401 year: 1991 end-page: 5406 article-title: Differntial induction of primary‐response (TIS) genes in PC12 pheochromocytoma cells and the unresponsive variant PC12nnr5 publication-title: J Biol Chem – volume: 16 start-page: 2687 year: 1998 end-page: 2693 article-title: , a novel member of family, is expressed in the ventricular zone of the developing central nervous system publication-title: Oncogene – volume: 15 start-page: 267 year: 2001 end-page: 285 article-title: E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis publication-title: Genes Dev – volume: 119 start-page: 646 year: 2006 end-page: 658 article-title: APRO4 negatively regulates Src tyrosine kinase activity in PC12 cells publication-title: J Cell Sci – volume: 11 start-page: 1663 year: 1992 end-page: 1670 article-title: , a member of a new family of antiproliferative genes publication-title: EMBO J – volume: 24 start-page: 2810 year: 2005 end-page: 2826 article-title: The E2F transcriptional network: old acquaintances with new faces publication-title: Oncogene – volume: 266 start-page: 14511 year: 1991 end-page: 14518 article-title: Structure and expression of TIS21, a primary response gene induced by growth factors and tumor promoters publication-title: J Biol Chem – volume: 92 start-page: 12146 year: 1995 end-page: 12150 article-title: Regulaition of the cyclin E gene by transcription factor E2F1 publication-title: Proc Natl Acad Sci USA – volume: 15 start-page: 1833 year: 2001 end-page: 1844 article-title: Selective induction of E2F1 in response to DNA damage, mediated by ATM‐dependent phosphorylation publication-title: Genes Dev – volume: 85 start-page: 549 year: 1996 end-page: 561 article-title: E2F‐1 functions in mice to promote apoptosis and suppress proliferation publication-title: Cell – volume: 281 start-page: 3800 year: 2006 end-page: 3809 article-title: Oncogenic RAS induces accelerated transition through G2/M and promotes defects in the G2 DNA damage and mitotic spindle checkpoints publication-title: J Biol Chem – volume: 7 start-page: 1327 year: 1996 end-page: 1336 article-title: Overexpression of the nerve growth factor‐inducible PC3 immediate early gene is associated with growth inhibition publication-title: Cell Growth Differ – volume: 10 start-page: 431 year: 2003 end-page: 442 article-title: Decision making by p53: life, death and cancer publication-title: Cell Death Differ – volume: 13 start-page: 941 year: 2006 end-page: 950 article-title: The complexity of p53 stabilization and activation publication-title: Cell Death Differ – volume: 280 start-page: 7748 year: 2005 end-page: 7757 article-title: TTK/hMps1 participates in the regulation of DNA damage checkpoint response by phosphorylating CHK2 on Threonine 68 publication-title: J Biol Chem – volume: 24 start-page: 2899 year: 2005 end-page: 2908 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Snippet	Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage‐inducible, CHK1‐modulated genes, we have... Proper regulation of cell cycle progression is pivotal for maintaining genome stability. In a search for DNA damage-inducible, CHK1-modulated genes, we have...
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SubjectTerms	BTG Cell cycle Cell Line, Tumor Cellular biology Deoxyribonucleic acid DNA DNA Damage E2F1 E2F1 Transcription Factor - antagonists & inhibitors E2F1 Transcription Factor - metabolism Genomics Humans Inhibitor drugs Introns Molecular biology Oligonucleotide Array Sequence Analysis p53 Protein Binding Proteins - genetics Proteins - metabolism Transcriptional Activation Translocation Tumor Suppressor Protein p53 - genetics Tumor Suppressor Protein p53 - metabolism Tumors
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Title	The candidate tumor suppressor BTG3 is a transcriptional target of p53 that inhibits E2F1
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