ETS transcription factor ERG cooperates with histone demethylase KDM4A
- Authors:
- Tae-Dong Kim
- Sook Shin
- Ralf Janknecht
-
Affiliations: Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA, Department of Cell Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA - Published online on: April 15, 2016 https://doi.org/10.3892/or.2016.4747
- Pages: 3679-3688
This article is mentioned in:
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|
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin. 65:5–29. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Ryan CJ and Tindall DJ: Androgen receptor rediscovered: The new biology and targeting the androgen receptor therapeutically. J Clin Oncol. 29:3651–3658. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, et al: Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 310:644–648. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Clark JP and Cooper CS: ETS gene fusions in prostate cancer. Nat Rev Urol. 6:429–439. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Klezovitch O, Risk M, Coleman I, Lucas JM, Null M, True LD, Nelson PS and Vasioukhin V: A causal role for ERG in neoplastic transformation of prostate epithelium. Proc Natl Acad Sci USA. 105:2105–2110. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Tomlins SA, Laxman B, Varambally S, Cao X, Yu J, Helgeson BE, Cao Q, Prensner JR, Rubin MA, Shah RB, et al: Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia. 10:177–188. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Nguyen LT, Tretiakova MS, Silvis MR, Lucas J, Klezovitch O, Coleman I, Bolouri H, Kutyavin VI, Morrissey C, True LD, et al: ERG activates the YAP1 transcriptional program and induces the development of age-related prostate tumors. Cancer Cell. 27:797–808. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, Alimonti A, Nardella C, Varmeh S, Scardino PT, et al: Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet. 41:619–624. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH, Taylor BS, Sander C, Cardiff RD, Couto SS, et al: Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet. 41:524–526. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Baena E, Shao Z, Linn DE, Glass K, Hamblen MJ, Fujiwara Y, Kim J, Nguyen M, Zhang X, Godinho FJ, et al: ETV1 directs androgen metabolism and confers aggressive prostate cancer in targeted mice and patients. Genes Dev. 27:683–698. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Y, Chi P, Rockowitz S, Iaquinta PJ, Shamu T, Shukla S, Gao D, Sirota I, Carver BS, Wongvipat J, et al: ETS factors reprogram the androgen receptor cistrome and prime prostate tumorigenesis in response to PTEN loss. Nat Med. 19:1023–1029. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Harvey KF, Zhang X and Thomas DM: The Hippo pathway and human cancer. Nat Rev Cancer. 13:246–257. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Varelas X: The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development. 141:1614–1626. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Dowdy SC, Mariani A and Janknecht R: HER2/Neu- and TAK1-mediated up-regulation of the transforming growth factor beta inhibitor Smad7 via the ETS protein ER81. J Biol Chem. 278:44377–44384. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Mooney SM, Grande JP, Salisbury JL and Janknecht R: Sumoylation of p68 and p72 RNA helicases affects protein stability and transactivation potential. Biochemistry. 49:1–10. 2010. View Article : Google Scholar | |
|
Oh S, Shin S, Lightfoot SA and Janknecht R: 14-3-3 proteins modulate the ETS transcription factor ETV1 in prostate cancer. Cancer Res. 73:5110–5119. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wu J and Janknecht R: Regulation of the ETS transcription factor ER81 by the 90-kDa ribosomal S6 kinase 1 and protein kinase A. J Biol Chem. 277:42669–42679. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Papoutsopoulou S and Janknecht R: Phosphorylation of ETS transcription factor ER81 in a complex with its coactivators CREB-binding protein and p300. Mol Cell Biol. 20:7300–7310. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
De Haro L and Janknecht R: Cloning of the murine ER71 gene (Etsrp71) and initial characterization of its promoter. Genomics. 85:493–502. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
DiTacchio L, Bowles J, Shin S, Lim DS, Koopman P and Janknecht R: Transcription factors ER71/ETV2 and SOX9 participate in a positive feedback loop in fetal and adult mouse testis. J Biol Chem. 287:23657–23666. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
De Haro L and Janknecht R: Functional analysis of the transcription factor ER71 and its activation of the matrix metal-loproteinase-1 promoter. Nucleic Acids Res. 30:2972–2979. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Mooney SM, Goel A, D'Assoro AB, Salisbury JL and Janknecht R: Pleiotropic effects of p300-mediated acetylation on p68 and p72 RNA helicase. J Biol Chem. 285:30443–30452. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Knebel J, De Haro L and Janknecht R: Repression of transcription by TSGA/Jmjd1a, a novel interaction partner of the ETS protein ER71. J Cell Biochem. 99:319–329. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S and Janknecht R: Concerted activation of the Mdm2 promoter by p72 RNA helicase and the coactivators p300 and P/CAF. J Cell Biochem. 101:1252–1265. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Goel A and Janknecht R: Acetylation-mediated transcriptional activation of the ETS protein ER81 by p300, P/CAF, and HER2/Neu. Mol Cell Biol. 23:6243–6254. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Goel A and Janknecht R: Concerted activation of ETS protein ER81 by p160 coactivators, the acetyltransferase p300 and the receptor tyrosine kinase HER2/Neu. J Biol Chem. 279:14909–14916. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Berry WL, Kim TD and Janknecht R: Stimulation of β-catenin and colon cancer cell growth by the KDM4B histone demethylase. Int J Oncol. 44:1341–1348. 2014.PubMed/NCBI | |
|
Janknecht R: Regulation of the ER81 transcription factor and its coactivators by mitogen- and stress-activated protein kinase 1 (MSK1). Oncogene. 22:746–755. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S, Bosc DG, Ingle JN, Spelsberg TC and Janknecht R: Rcl is a novel ETV1/ER81 target gene upregulated in breast tumors. J Cell Biochem. 105:866–874. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Goueli BS and Janknecht R: Regulation of telomerase reverse transcriptase gene activity by upstream stimulatory factor. Oncogene. 22:8042–8047. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S, Rossow KL, Grande JP and Janknecht R: Involvement of RNA helicases p68 and p72 in colon cancer. Cancer Res. 67:7572–7578. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S, Oh S, An S and Janknecht R: ETS variant 1 regulates matrix metalloproteinase-7 transcription in LNCaP prostate cancer cells. Oncol Rep. 29:306–314. 2013. | |
|
Goueli BS and Janknecht R: Upregulation of the catalytic telomerase subunit by the transcription factor ER81 and oncogenic HER2/Neu, Ras, or Raf. Mol Cell Biol. 24:25–35. 2004. View Article : Google Scholar : | |
|
Shin S, Kim TD, Jin F, van Deursen JM, Dehm SM, Tindall DJ, Grande JP, Munz JM, Vasmatzis G and Janknecht R: Induction of prostatic intraepithelial neoplasia and modulation of androgen receptor by ETS variant 1/ETS-related protein 81. Cancer Res. 69:8102–8110. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Kim TD, Oh S, Shin S and Janknecht R: Regulation of tumor suppressor p53 and HCT116 cell physiology by histone demethylase JMJD2D/KDM4D. PLoS One. 7:e346182012. View Article : Google Scholar : PubMed/NCBI | |
|
Wu H, Xiao Y, Zhang S, Ji S, Wei L, Fan F, Geng J, Tian J, Sun X, Qin F, et al: The Ets transcription factor GABP is a component of the hippo pathway essential for growth and antioxidant defense. Cell Reports. 3:1663–1677. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Haffner MC, Aryee MJ, Toubaji A, Esopi DM, Albadine R, Gurel B, Isaacs WB, Bova GS, Liu W, Xu J, et al: Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet. 42:668–675. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Hollenhorst PC, McIntosh LP and Graves BJ: Genomic and biochemical insights into the specificity of ETS transcription factors. Annu Rev Biochem. 80:437–471. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Regan MC, Horanyi PS, Pryor EE Jr, Sarver JL, Cafiso DS and Bushweller JH: Structural and dynamic studies of the transcription factor ERG reveal DNA binding is allosterically autoinhibited. Proc Natl Acad Sci USA. 110:13374–13379. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wei GH, Badis G, Berger MF, Kivioja T, Palin K, Enge M, Bonke M, Jolma A, Varjosalo M, Gehrke AR, et al: Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 29:2147–2160. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Bosc DG, Goueli BS and Janknecht R: HER2/Neu-mediated activation of the ETS transcription factor ER81 and its target gene MMP-1. Oncogene. 20:6215–6224. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Janknecht R, Monté D, Baert JL and de Launoit Y: The ETS-related transcription factor ERM is a nuclear target of signaling cascades involving MAPK and PKA. Oncogene. 13:1745–1754. 1996.PubMed/NCBI | |
|
Black JC, Van Rechem C and Whetstine JR: Histone lysine methylation dynamics: Establishment, regulation, and biological impact. Mol Cell. 48:491–507. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Kooistra SM and Helin K: Molecular mechanisms and potential functions of histone demethylases. Nat Rev Mol Cell Biol. 13:297–311. 2012.PubMed/NCBI | |
|
Berry WL and Janknecht R: KDM4/JMJD2 histone demeth-ylases: Epigenetic regulators in cancer cells. Cancer Res. 73:2936–2942. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Whetstine JR, Nottke A, Lan F, Huarte M, Smolikov S, Chen Z, Spooner E, Li E, Zhang G, Colaiacovo M, et al: Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell. 125:467–481. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S and Janknecht R: Diversity within the JMJD2 histone demethylase family. Biochem Biophys Res Commun. 353:973–977. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sun C, Dobi A, Mohamed A, Li H, Thangapazham RL, Furusato B, Shaheduzzaman S, Tan SH, Vaidyanathan G, Whitman E, et al: TMPRSS2-ERG fusion, a common genomic alteration in prostate cancer activates C-MYC and abrogates prostate epithelial differentiation. Oncogene. 27:5348–5353. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Cai Y, Yu W, Ren C, Spencer DM and Ittmann M: Pleiotropic biological activities of alternatively spliced TMPRSS2/ERG fusion gene transcripts. Cancer Res. 68:8516–8524. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Barry ER, Morikawa T, Butler BL, Shrestha K, de la Rosa R, Yan KS, Fuchs CS, Magness ST, Smits R, Ogino S, et al: Restriction of intestinal stem cell expansion and the regenerative response by YAP. Nature. 493:106–110. 2013. View Article : Google Scholar : | |
|
Cottini F, Hideshima T, Xu C, Sattler M, Dori M, Agnelli L, ten Hacken E, Bertilaccio MT, Antonini E, Neri A, et al: Rescue of Hippo coactivator YAP1 triggers DNA damage-induced apoptosis in hematological cancers. Nat Med. 20:599–606. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, et al: Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21:2747–2761. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee SJ, Anders RA, Liu JO and Pan D: Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 26:1300–1305. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Jiao S, Wang H, Shi Z, Dong A, Zhang W, Song X, He F, Wang Y, Zhang Z, Wang W, et al: A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell. 25:166–180. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Labbé RM, Holowatyj A and Yang ZQ: Histone lysine demeth-ylase (KDM) subfamily 4: Structures, functions and therapeutic potential. Am J Transl Res. 6:1–15. 2013. | |
|
Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J and Zhang Y: The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature. 442:312–316. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Trojer P, Zhang J, Yonezawa M, Schmidt A, Zheng H, Jenuwein T and Reinberg D: Dynamic histone H1 isotype 4 methylation and demethylation by histone lysine methyltransferase G9a/KMT1C and the Jumonji domain-containing JMJD2/KDM4 proteins. J Biol Chem. 284:8395–8405. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Crona F, Dahlberg O, Lundberg LE, Larsson J and Mannervik M: Gene regulation by the lysine demethylase KDM4A in Drosophila. Dev Biol. 373:453–463. 2013. View Article : Google Scholar | |
|
Mallette FA, Mattiroli F, Cui G, Young LC, Hendzel MJ, Mer G, Sixma TK and Richard S: RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 31:1865–1878. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Hamada S, Kim TD, Suzuki T, Itoh Y, Tsumoto H, Nakagawa H, Janknecht R and Miyata N: Synthesis and activity of N-oxalylglycine and its derivatives as Jumonji C-domain-containing histone lysine demethylase inhibitors. Bioorg Med Chem Lett. 19:2852–2855. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hamada S, Suzuki T, Mino K, Koseki K, Oehme F, Flamme I, Ozasa H, Itoh Y, Ogasawara D, Komaarashi H, et al: Design, synthesis, enzyme-inhibitory activity, and effect on human cancer cells of a novel series of jumonji domain-containing protein 2 histone demethylase inhibitors. J Med Chem. 53:5629–5638. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Rose NR, Woon EC, Kingham GL, King ON, Mecinović J, Clifton IJ, Ng SS, Talib-Hardy J, Oppermann U, McDonough MA, et al: Selective inhibitors of the JMJD2 histone demethylases: Combined nondenaturing mass spectrometric screening and crystallographic approaches. J Med Chem. 53:1810–1818. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
King ON, Li XS, Sakurai M, Kawamura A, Rose NR, Ng SS, Quinn AM, Rai G, Mott BT, Beswick P, et al: Quantitative high-throughput screening identifies 8-hydroxyquinolines as cell-active histone demethylase inhibitors. PLoS One. 5:e155352010. View Article : Google Scholar : PubMed/NCBI | |
|
Luo X, Liu Y, Kubicek S, Myllyharju J, Tumber A, Ng S, Che KH, Podoll J, Heightman TD, Oppermann U, et al: A selective inhibitor and probe of the cellular functions of Jumonji C domain-containing histone demethylases. J Am Chem Soc. 133:9451–9456. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Wang L, Chang J, Varghese D, Dellinger M, Kumar S, Best AM, Ruiz J, Bruick R, Peña-Llopis S, Xu J, et al: A small molecule modulates Jumonji histone demethylase activity and selectively inhibits cancer growth. Nat Commun. 4:20352013.PubMed/NCBI | |
|
Kim TD, Fuchs JR, Schwartz E, Abdelhamid D, Etter J, Berry WL, Li C, Ihnat MA, Li PK and Janknecht R: Pro-growth role of the JMJD2C histone demethylase in HCT-116 colon cancer cells and identification of curcuminoids as JMJD2 inhibitors. Am J Transl Res. 6:236–247. 2014.PubMed/NCBI | |
|
Cloos PA, Christensen J, Agger K, Maiolica A, Rappsilber J, Antal T, Hansen KH and Helin K: The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature. 442:307–311. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Patani N, Jiang WG, Newbold RF and Mokbel K: Histone-modifier gene expression profiles are associated with pathological and clinical outcomes in human breast cancer. Anticancer Res. 31:4115–4125. 2011.PubMed/NCBI | |
|
Berry WL, Shin S, Lightfoot SA and Janknecht R: Oncogenic features of the JMJD2A histone demethylase in breast cancer. Int J Oncol. 41:1701–1706. 2012.PubMed/NCBI | |
|
Slee RB, Steiner CM, Herbert BS, Vance GH, Hickey RJ, Schwarz T, Christan S, Radovich M, Schneider BP, Schindelhauer D, et al: Cancer-associated alteration of pericentromeric heterochromatin may contribute to chromosome instability. Oncogene. 31:3244–3253. 2012. View Article : Google Scholar | |
|
Mallette FA and Richard S: JMJD2A promotes cellular transformation by blocking cellular senescence through transcriptional repression of the tumor suppressor CHD5. Cell Reports. 2:1233–1243. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Shin S and Janknecht R: Activation of androgen receptor by histone demethylases JMJD2A and JMJD2D. Biochem Biophys Res Commun. 359:742–746. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kim TD, Shin S, Berry WL, Oh S and Janknecht R: The JMJD2A demethylase regulates apoptosis and proliferation in colon cancer cells. J Cell Biochem. 113:1368–1376. 2012. View Article : Google Scholar | |
|
Black JC, Manning AL, Van Rechem C, Kim J, Ladd B, Cho J, Pineda CM, Murphy N, Daniels DL, Montagna C, et al: KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumors. Cell. 154:541–555. 2013. View Article : Google Scholar : PubMed/NCBI |
