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Research Article

GRHL2 Enhances Phosphorylated Estrogen Receptor (ER) Chromatin Binding and Regulates ER-Mediated Transcriptional Activation and Repression

ORCID Icon, , , , &
Article: e00191-22 | Received 20 May 2022, Accepted 14 Aug 2022, Published online: 24 Feb 2023

REFERENCES

  • Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, Chambon P. 1986. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320:134–139. https://doi.org/10.1038/320134a0.
  • Sleightholm R, Neilsen BK, Elkhatib S, Flores L, Dukkipati S, Zhao R, Choudhury S, Gardner B, Carmichael J, Smith L, Bennion N, Wahl A, Baine M. 2021. Percentage of hormone receptor positivity in breast cancer provides prognostic value: a single-institute study. J Clin Med Res 13:9–19. https://doi.org/10.14740/jocmr4398.
  • Harvey JM, Clark GM, Osborne CK, Allred DC. 1999. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 17:1474–1481. https://doi.org/10.1200/JCO.1999.17.5.1474.
  • Tora L, White J, Brou C, Tasset D, Webster N, Scheer E, Chambon P. 1989. The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell 59:477–487. https://doi.org/10.1016/0092-8674(89)90031-7.
  • Webster NJ, Green S, Jin JR, Chambon P. 1988. The hormone-binding domains of the estrogen and glucocorticoid receptors contain an inducible transcription activation function. Cell 54:199–207. https://doi.org/10.1016/0092-8674(88)90552-1.
  • Kumar V, Chambon P. 1988. The estrogen receptor binds tightly to its responsive element as a ligand-induced homodimer. Cell 55:145–156. https://doi.org/10.1016/0092-8674(88)90017-7.
  • Klein-Hitpass L, Ryffel GU, Heitlinger E, Cato AC. 1988. A 13 bp palindrome is a functional estrogen responsive element and interacts specifically with estrogen receptor. Nucleic Acids Res 16:647–663. https://doi.org/10.1093/nar/16.2.647.
  • Shiau AK, Barstad D, Loria PM, Cheng L, Kushner PJ, Agard DA, Greene GL. 1998. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95:927–937. https://doi.org/10.1016/s0092-8674(00)81717-1.
  • Beato M, Sanchez-Pacheco A. 1996. Interaction of steroid hormone receptors with the transcription initiation complex. Endocr Rev 17:587–609. https://doi.org/10.1210/edrv-17-6-587.
  • Heery DM, Kalkhoven E, Hoare S, Parker MG. 1997. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736. https://doi.org/10.1038/42750.
  • Le Romancer M, Poulard C, Cohen P, Sentis S, Renoir JM, Corbo L. 2011. Cracking the estrogen receptor’s posttranslational code in breast tumors. Endocr Rev 32:597–622. https://doi.org/10.1210/er.2010-0016.
  • Ali S, Metzger D, Bornert JM, Chambon P. 1993. Modulation of transcriptional activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region. EMBO J 12:1153–1160. https://doi.org/10.1002/j.1460-2075.1993.tb05756.x.
  • Bunone G, Briand PA, Miksicek RJ, Picard D. 1996. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 15:2174–2183. https://doi.org/10.1002/j.1460-2075.1996.tb00571.x.
  • Sarwar N, Kim JS, Jiang J, Peston D, Sinnett HD, Madden P, Gee JM, Nicholson RI, Lykkesfeldt AE, Shousha S, Coombes RC, Ali S. 2006. Phosphorylation of ERalpha at serine 118 in primary breast cancer and in tamoxifen-resistant tumours is indicative of a complex role for ERalpha phosphorylation in breast cancer progression. Endocr Relat Cancer 13:851–861. https://doi.org/10.1677/erc.1.01123.
  • Murphy L, Cherlet T, Adeyinka A, Niu Y, Snell L, Watson P. 2004. Phospho-serine-118 estrogen receptor-alpha detection in human breast tumors in vivo. Clin Cancer Res 10:1354–1359. https://doi.org/10.1158/1078-0432.CCR-03-0112.
  • Cheng J, Zhang C, Shapiro DJ. 2007. A functional serine 118 phosphorylation site in estrogen receptor-alpha is required for down-regulation of gene expression by 17beta-estradiol and 4-hydroxytamoxifen. Endocrinology 148:4634–4641. https://doi.org/10.1210/en.2007-0148.
  • Valley CC, Metivier R, Solodin NM, Fowler AM, Mashek MT, Hill L, Alarid ET. 2005. Differential regulation of estrogen-inducible proteolysis and transcription by the estrogen receptor alpha N terminus. Mol Cell Biol 25:5417–5428. https://doi.org/10.1128/MCB.25.13.5417-5428.2005.
  • Dutertre M, Smith CL. 2003. Ligand-independent interactions of p160/steroid receptor coactivators and CREB-binding protein (CBP) with estrogen receptor-alpha: regulation by phosphorylation sites in the A/B region depends on other receptor domains. Mol Endocrinol 17:1296–1314. https://doi.org/10.1210/me.2001-0316.
  • Helzer KT, Szatkowski Ozers M, Meyer MB, Benkusky NA, Solodin N, Reese RM, Warren CL, Pike JW, Alarid ET. 2019. The phosphorylated estrogen receptor alpha (ER) cistrome identifies a subset of active enhancers enriched for direct ER-DNA binding and the transcription factor GRHL2. Mol Cell Biol 39:e00417-18. https://doi.org/10.1128/MCB.00417-18.
  • Dynlacht BD, Attardi LD, Admon A, Freeman M, Tjian R. 1989. Functional analysis of NTF-1, a developmentally regulated Drosophila transcription factor that binds neuronal cis elements. Genes Dev 3:1677–1688. https://doi.org/10.1101/gad.3.11.1677.
  • Wilanowski T, Tuckfield A, Cerruti L, O'Connell S, Saint R, Parekh V, Tao J, Cunningham JM, Jane SM. 2002. A highly conserved novel family of mammalian developmental transcription factors related to Drosophila grainyhead. Mech Dev 114:37–50. https://doi.org/10.1016/S0925-4773(02)00046-1.
  • Ming Q, Roske Y, Schuetz A, Walentin K, Ibraimi I, Schmidt-Ott KM, Heinemann U. 2018. Structural basis of gene regulation by the Grainyhead/CP2 transcription factor family. Nucleic Acids Res 46:2082–2095. https://doi.org/10.1093/nar/gkx1299.
  • Ting SB, Caddy J, Hislop N, Wilanowski T, Auden A, Zhao LL, Ellis S, Kaur P, Uchida Y, Holleran WM, Elias PM, Cunningham JM, Jane SM. 2005. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 308:411–413. https://doi.org/10.1126/science.1107511.
  • Boglev Y, Wilanowski T, Caddy J, Parekh V, Auden A, Darido C, Hislop NR, Cangkrama M, Ting SB, Jane SM. 2011. The unique and cooperative roles of the Grainy head-like transcription factors in epidermal development reflect unexpected target gene specificity. Dev Biol 349:512–522. https://doi.org/10.1016/j.ydbio.2010.11.011.
  • Rifat Y, Parekh V, Wilanowski T, Hislop NR, Auden A, Ting SB, Cunningham JM, Jane SM. 2010. Regional neural tube closure defined by the Grainy head-like transcription factors. Dev Biol 345:237–245. https://doi.org/10.1016/j.ydbio.2010.07.017.
  • Auden A, Caddy J, Wilanowski T, Ting SB, Cunningham JM, Jane SM. 2006. Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development. Gene Expr Patterns 6:964–970. https://doi.org/10.1016/j.modgep.2006.03.011.
  • Ting SB, Wilanowski T, Auden A, Hall M, Voss AK, Thomas T, Parekh V, Cunningham JM, Jane SM. 2003. Inositol- and folate-resistant neural tube defects in mice lacking the epithelial-specific factor Grhl-3. Nat Med 9:1513–1519. https://doi.org/10.1038/nm961.
  • Werth M, Walentin K, Aue A, Schonheit J, Wuebken A, Pode-Shakked N, Vilianovitch L, Erdmann B, Dekel B, Bader M, Barasch J, Rosenbauer F, Luft FC, Schmidt-Ott KM. 2010. The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137:3835–3845. https://doi.org/10.1242/dev.055483.
  • Nieto MA. 2013. Epithelial plasticity: a common theme in embryonic and cancer cells. Science 342:1234850. https://doi.org/10.1126/science.1234850.
  • Werner S, Frey S, Riethdorf S, Schulze C, Alawi M, Kling L, Vafaizadeh V, Sauter G, Terracciano L, Schumacher U, Pantel K, Assmann V. 2013. Dual roles of the transcription factor grainyhead-like 2 (GRHL2) in breast cancer. J Biol Chem 288:22993–23008. https://doi.org/10.1074/jbc.M113.456293.
  • Yang Z, Wu D, Chen Y, Min Z, Quan Y. 2019. GRHL2 inhibits colorectal cancer progression and metastasis via oppressing epithelial-mesenchymal transition. Cancer Biol Ther 20:1195–1205. https://doi.org/10.1080/15384047.2019.1599664.
  • Hao Y, Li Y, Wu J, Hao N, Qin Y, Zhang H, Zhao W, Kang S. 2022. Hypermethylation of the GRHL2 promoter region is associated with ovarian endometriosis. Reproduction 163:379–386. https://doi.org/10.1530/REP-21-0383.
  • Xiang J, Fu X, Ran W, Wang Z. 2017. Grhl2 reduces invasion and migration through inhibition of TGFbeta-induced EMT in gastric cancer. Oncogenesis 6:e284. https://doi.org/10.1038/oncsis.2016.83.
  • Cieply B, Riley P, Pifer PM, Widmeyer J, Addison JB, Ivanov AV, Denvir J, Frisch SM. 2012. Suppression of the epithelial-mesenchymal transition by Grainyhead-like-2. Cancer Res 72:2440–2453. https://doi.org/10.1158/0008-5472.CAN-11-4038.
  • Pan X, Zhang R, Xie C, Gan M, Yao S, Yao Y, Jin J, Han T, Huang Y, Gong Y, Wang J, Yu B. 2017. GRHL2 suppresses tumor metastasis via regulation of transcriptional activity of RhoG in non-small cell lung cancer. Am J Transl Res 9:4217–4226.
  • Chen W, Yi JK, Shimane T, Mehrazarin S, Lin YL, Shin KH, Kim RH, Park NH, Kang MK. 2016. Grainyhead-like 2 regulates epithelial plasticity and stemness in oral cancer cells. Carcinogenesis 37:500–510. https://doi.org/10.1093/carcin/bgw027.
  • Chung VY, Tan TZ, Tan M, Wong MK, Kuay KT, Yang Z, Ye J, Muller J, Koh CM, Guccione E, Thiery JP, Huang RY. 2016. GRHL2-miR-200-ZEB1 maintains the epithelial status of ovarian cancer through transcriptional regulation and histone modification. Sci Rep 6:19943. https://doi.org/10.1038/srep19943.
  • Paltoglou S, Das R, Townley SL, Hickey T, Tarulli G, Coutinho I, Fernandes RC, Hanson A, Denis I, Carroll J, Dehm SM, Raj GV, Plymate S, Tilley WD, Selth LA. 2017. Novel androgen receptor co-regulator GRHL2 exerts both oncogenic and anti-metastatic functions in prostate cancer. Cancer Res 77:3417–3430. https://doi.org/10.1158/0008-5472.CAN-16-1616.
  • Shen J, Lv X, Zhang L. 2020. GRHL2 acts as an anti-oncogene in bladder cancer by regulating ZEB1 in epithelial-mesenchymal transition (EMT) process. Onco Targets Ther 13:2511–2522. https://doi.org/10.2147/OTT.S239120.
  • Pyrgaki C, Liu A, Niswander L. 2011. Grainyhead-like 2 regulates neural tube closure and adhesion molecule expression during neural fold fusion. Dev Biol 353:38–49. https://doi.org/10.1016/j.ydbio.2011.02.027.
  • Gao X, Bali AS, Randell SH, Hogan BL. 2015. GRHL2 coordinates regeneration of a polarized mucociliary epithelium from basal stem cells. J Cell Biol 211:669–682. https://doi.org/10.1083/jcb.201506014.
  • Senga K, Mostov KE, Mitaka T, Miyajima A, Tanimizu N. 2012. Grainyhead-like 2 regulates epithelial morphogenesis by establishing functional tight junctions through the organization of a molecular network among claudin3, claudin4, and Rab25. Mol Biol Cell 23:2845–2855. https://doi.org/10.1091/mbc.E12-02-0097.
  • Varma S, Mahavadi P, Sasikumar S, Cushing L, Hyland T, Rosser AE, Riccardi D, Lu J, Kalin TV, Kalinichenko VV, Guenther A, Ramirez MI, Pardo A, Selman M, Warburton D. 2014. Grainyhead-like 2 (GRHL2) distribution reveals novel pathophysiological differences between human idiopathic pulmonary fibrosis and mouse models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 306:L405–L419. https://doi.org/10.1152/ajplung.00143.2013.
  • Gao X, Vockley CM, Pauli F, Newberry KM, Xue Y, Randell SH, Reddy TE, Hogan BL. 2013. Evidence for multiple roles for grainyhead-like 2 in the establishment and maintenance of human mucociliary airway epithelium. Proc Natl Acad Sci USA 110:9356–9361. https://doi.org/10.1073/pnas.1307589110.
  • Aue A, Hinze C, Walentin K, Ruffert J, Yurtdas Y, Werth M, Chen W, Rabien A, Kilic E, Schulzke JD, Schumann M, Schmidt-Ott KM. 2015. A Grainyhead-like 2/Ovo-like 2 pathway regulates renal epithelial barrier function and lumen expansion. J Am Soc Nephrol 26:2704–2715. https://doi.org/10.1681/ASN.2014080759.
  • MacFawn I, Wilson H, Selth LA, Leighton I, Serebriiskii I, Bleackley RC, Elzamzamy O, Farris J, Pifer PM, Richer J, Frisch SM. 2019. Grainyhead-like-2 confers NK-sensitivity through interactions with epigenetic modifiers. Mol Immunol 105:137–149. https://doi.org/10.1016/j.molimm.2018.11.006.
  • Sundararajan V, Tan M, Zea Tan T, Pang QY, Ye J, Chung VY, Huang RY. 2020. SNAI1-driven sequential EMT changes attributed by selective chromatin enrichment of RAD21 and GRHL2. Cancers (Basel) 12:1140. https://doi.org/10.3390/cancers12051140.
  • Ray HJ, Niswander LA. 2016. Grainyhead-like 2 downstream targets act to suppress epithelial-to-mesenchymal transition during neural tube closure. Development 143:1192–1204. https://doi.org/10.1242/dev.129825.
  • Walentin K, Hinze C, Werth M, Haase N, Varma S, Morell R, Aue A, Potschke E, Warburton D, Qiu A, Barasch J, Purfurst B, Dieterich C, Popova E, Bader M, Dechend R, Staff AC, Yurtdas ZY, Kilic E, Schmidt-Ott KM. 2015. A Grhl2-dependent gene network controls trophoblast branching morphogenesis. Development 142:1125–1136. https://doi.org/10.1242/dev.113829.
  • Chen AF, Liu AJ, Krishnakumar R, Freimer JW, DeVeale B, Blelloch R. 2018. GRHL2-dependent enhancer switching maintains a pluripotent stem cell transcriptional subnetwork after exit from naive pluripotency. Cell Stem Cell 23:226–238.e4. https://doi.org/10.1016/j.stem.2018.06.005.
  • Xiang X, Deng Z, Zhuang X, Ju S, Mu J, Jiang H, Zhang L, Yan J, Miller D, Zhang HG. 2012. Grhl2 determines the epithelial phenotype of breast cancers and promotes tumor progression. PLoS One 7:e50781. https://doi.org/10.1371/journal.pone.0050781.
  • Cieply B, Farris J, Denvir J, Ford HL, Frisch SM. 2013. Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res 73:6299–6309. https://doi.org/10.1158/0008-5472.CAN-12-4082.
  • Cocce KJ, Jasper JS, Desautels TK, Everett L, Wardell S, Westerling T, Baldi R, Wright TM, Tavares K, Yllanes A, Bae Y, Blitzer JT, Logsdon C, Rakiec DP, Ruddy DA, Jiang T, Broadwater G, Hyslop T, Hall A, Laine M, Phung L, Greene GL, Martin LA, Pancholi S, Dowsett M, Detre S, Marks JR, Crawford GE, Brown M, Norris JD, Chang CY, McDonnell DP. 2019. The lineage determining factor GRHL2 collaborates with FOXA1 to establish a targetable pathway in endocrine therapy-resistant breast cancer. Cell Rep 29:889–903.e10. https://doi.org/10.1016/j.celrep.2019.09.032.
  • Chi D, Singhal H, Li L, Xiao T, Liu W, Pun M, Jeselsohn R, He H, Lim E, Vadhi R, Rao P, Long H, Garber J, Brown M. 2019. Estrogen receptor signaling is reprogrammed during breast tumorigenesis. Proc Natl Acad Sci USA 116:11437–11443. https://doi.org/10.1073/pnas.1819155116.
  • Yuan M, Wang J, Fang F. 2020. Grainyhead-like genes family may act as novel biomarkers in colon cancer. Onco Targets Ther 13:3237–3245. https://doi.org/10.2147/OTT.S242763.
  • Hu F, He Z, Sun C, Rong D. 2019. Knockdown of GRHL2 inhibited proliferation and induced apoptosis of colorectal cancer by suppressing the PI3K/Akt pathway. Gene 700:96–104. https://doi.org/10.1016/j.gene.2019.03.051.
  • Quan Y, Jin R, Huang A, Zhao H, Feng B, Zang L, Zheng M. 2014. Downregulation of GRHL2 inhibits the proliferation of colorectal cancer cells by targeting ZEB1. Cancer Biol Ther 15:878–887. https://doi.org/10.4161/cbt.28877.
  • Quan Y, Xu M, Cui P, Ye M, Zhuang B, Min Z. 2015. Expression and clinical significance of GRHL2 in colorectal cancer. Zhonghua Zhong Liu Za Zhi 37:764–768.
  • Tanaka Y, Kanai F, Tada M, Tateishi R, Sanada M, Nannya Y, Ohta M, Asaoka Y, Seto M, Shiina S, Yoshida H, Kawabe T, Yokosuka O, Ogawa S, Omata M. 2008. Gain of GRHL2 is associated with early recurrence of hepatocellular carcinoma. J Hepatol 49:746–757. https://doi.org/10.1016/j.jhep.2008.06.019.
  • Kang X, Chen W, Kim RH, Kang MK, Park NH. 2009. Regulation of the hTERT promoter activity by MSH2, the hnRNPs K and D, and GRHL2 in human oral squamous cell carcinoma cells. Oncogene 28:565–574. https://doi.org/10.1038/onc.2008.404.
  • Faddaoui A, Sheta R, Bachvarova M, Plante M, Gregoire J, Renaud MC, Sebastianelli A, Gobeil S, Morin C, Ghani K, Bachvarov D. 2017. Suppression of the grainyhead transcription factor 2 gene (GRHL2) inhibits the proliferation, migration, invasion and mediates cell cycle arrest of ovarian cancer cells. Cell Cycle 16:693–706. https://doi.org/10.1080/15384101.2017.1295181.
  • Nie Y, Ding Y, Yang M. 2020. GRHL2 upregulation predicts a poor prognosis and promotes the resistance of serous ovarian cancer to cisplatin. Onco Targets Ther 13:6303–6314. https://doi.org/10.2147/OTT.S250412.
  • Nishino H, Takano S, Yoshitomi H, Suzuki K, Kagawa S, Shimazaki R, Shimizu H, Furukawa K, Miyazaki M, Ohtsuka M. 2017. Grainyhead-like 2 (GRHL2) regulates epithelial plasticity in pancreatic cancer progression. Cancer Med 6:2686–2696. https://doi.org/10.1002/cam4.1212.
  • Butz H, Szabo PM, Nofech-Mozes R, Rotondo F, Kovacs K, Mirham L, Girgis H, Boles D, Patocs A, Yousef GM. 2014. Integrative bioinformatics analysis reveals new prognostic biomarkers of clear cell renal cell carcinoma. Clin Chem 60:1314–1326. https://doi.org/10.1373/clinchem.2014.225854.
  • Yang X, Vasudevan P, Parekh V, Penev A, Cunningham JM. 2013. Bridging cancer biology with the clinic: relative expression of a GRHL2-mediated gene-set pair predicts breast cancer metastasis. PLoS One 8:e56195. https://doi.org/10.1371/journal.pone.0056195.
  • Pawlak M, Kikulska A, Wrzesinski T, Rausch T, Kwias Z, Wilczynski B, Benes V, Wesoly J, Wilanowski T. 2017. Potential protective role of Grainyhead-like genes in the development of clear cell renal cell carcinoma. Mol Carcinog 56:2414–2423. https://doi.org/10.1002/mc.22682.
  • Zhang Y, Meng W, Yue P, Li X. 2020. M2 macrophage-derived extracellular vesicles promote gastric cancer progression via a microRNA-130b-3p/MLL3/GRHL2 signaling cascade. J Exp Clin Cancer Res 39:134. https://doi.org/10.1186/s13046-020-01626-7.
  • Torres-Reyes LA, Alvarado-Ruiz L, Pina-Sanchez P, Martinez-Silva MG, Ramos-Solano M, Olimon-Andalon V, Ortiz-Lazareno PC, Hernandez-Flores G, Bravo-Cuellar A, Aguilar-Lemarroy A, Jave-Suarez LF. 2014. Expression of transcription factor grainyhead-like 2 is diminished in cervical cancer. Int J Clin Exp Pathol 7:7409–7418.
  • Mohammed H, D’Santos C, Serandour AA, Ali HR, Brown GD, Atkins A, Rueda OM, Holmes KA, Theodorou V, Robinson JL, Zwart W, Saadi A, Ross-Innes CS, Chin SF, Menon S, Stingl J, Palmieri C, Caldas C, Carroll JS. 2013. Endogenous purification reveals GREB1 as a key estrogen receptor regulatory factor. Cell Rep 3:342–349. https://doi.org/10.1016/j.celrep.2013.01.010.
  • Holding AN, Giorgi FM, Donnelly A, Cullen AE, Nagarajan S, Selth LA, Markowetz F. 2019. VULCAN integrates ChIP-seq with patient-derived co-expression networks to identify GRHL2 as a key co-regulator of ERa at enhancers in breast cancer. Genome Biol 20:91. https://doi.org/10.1186/s13059-019-1698-z.
  • Jozwik KM, Chernukhin I, Serandour AA, Nagarajan S, Carroll JS. 2016. FOXA1 directs H3K4 monomethylation at enhancers via recruitment of the methyltransferase MLL3. Cell Rep 17:2715–2723. https://doi.org/10.1016/j.celrep.2016.11.028.
  • Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Weng Z, Green RD, Crawford GE, Ren B. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39:311–318. https://doi.org/10.1038/ng1966.
  • Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS. 2002. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9:279–289. https://doi.org/10.1016/s1097-2765(02)00459-8.
  • Cirillo LA, McPherson CE, Bossard P, Stevens K, Cherian S, Shim EY, Clark KL, Burley SK, Zaret KS. 1998. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J 17:244–254. https://doi.org/10.1093/emboj/17.1.244.
  • Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, Li W, Carroll JS, Liu XS, Brown M. 2008. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132:958–970. https://doi.org/10.1016/j.cell.2008.01.018.
  • Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z. 2017. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res 45:W98–W102. https://doi.org/10.1093/nar/gkx247.
  • Reese RM, Harrison MM, Alarid ET. 2019. Grainyhead-like protein 2: the emerging role in hormone-dependent cancers and epigenetics. Endocrinology 160:1275–1288. https://doi.org/10.1210/en.2019-00213.
  • Kotarba G, Taracha-Wisniewska A, Wilanowski T. 2020. Grainyhead-like transcription factors in cancer—focus on recent developments. Exp Biol Med (Maywood) 245:402–410. https://doi.org/10.1177/1535370220903009.
  • Hoadley KA, Yau C, Hinoue T, Wolf DM, Lazar AJ, Drill E, Shen R, Taylor AM, Cherniack AD, Thorsson V, Akbani R, Bowlby R, Wong CK, Wiznerowicz M, Sanchez-Vega F, Robertson AG, Schneider BG, Lawrence MS, Noushmehr H, Malta TM, Cancer Genome Atlas N, Stuart JM, Benz CC, Laird PW, Cancer Genome Atlas Network. 2018. Cell-of-origin patterns dominate the molecular classification of 10,000 tumors from 33 types of cancer. Cell 173:291–304.e6. https://doi.org/10.1016/j.cell.2018.03.022.
  • Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C, Schultz N. 2012. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:401–404. https://doi.org/10.1158/2159-8290.CD-12-0095.
  • Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N. 2013. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6:pl1. https://doi.org/10.1126/scisignal.2004088.
  • Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS. 2011. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43:27–33. https://doi.org/10.1038/ng.730.
  • Pifer PM, Farris JC, Thomas AL, Stoilov P, Denvir J, Smith DM, Frisch SM. 2016. Grainyhead-like 2 inhibits the coactivator p300, suppressing tubulogenesis and the epithelial-mesenchymal transition. Mol Biol Cell 27:2479–2492. https://doi.org/10.1091/mbc.E16-04-0249.
  • Hanstein B, Eckner R, DiRenzo J, Halachmi S, Liu H, Searcy B, Kurokawa R, Brown M. 1996. p300 is a component of an estrogen receptor coactivator complex. Proc Natl Acad Sci USA 93:11540–11545. https://doi.org/10.1073/pnas.93.21.11540.
  • Franco HL, Nagari A, Kraus WL. 2015. TNFalpha signaling exposes latent estrogen receptor binding sites to alter the breast cancer cell transcriptome. Mol Cell 58:21–34. https://doi.org/10.1016/j.molcel.2015.02.001.
  • Liu Z, Merkurjev D, Yang F, Li W, Oh S, Friedman MJ, Song X, Zhang F, Ma Q, Ohgi KA, Krones A, Rosenfeld MG. 2014. Enhancer activation requires trans-recruitment of a mega transcription factor complex. Cell 159:358–373. https://doi.org/10.1016/j.cell.2014.08.027.
  • Brunelle M, Nordell Markovits A, Rodrigue S, Lupien M, Jacques PE, Gevry N. 2015. The histone variant H2A.Z is an important regulator of enhancer activity. Nucleic Acids Res 43:9742–9756. https://doi.org/10.1093/nar/gkv825.
  • Zhou Y, Gerrard DL, Wang J, Li T, Yang Y, Fritz AJ, Rajendran M, Fu X, Stein G, Schiff R, Lin S, Frietze S, Jin VX. 2019. Temporal dynamic reorganization of 3D chromatin architecture in hormone-induced breast cancer and endocrine resistance. Nat Commun 10:1522. https://doi.org/10.1038/s41467-019-09320-9.
  • Alarid ET, Bakopoulos N, Solodin N. 1999. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 13:1522–1534. https://doi.org/10.1210/mend.13.9.0337.
  • Prall OW, Rogan EM, Sutherland RL. 1998. Estrogen regulation of cell cycle progression in breast cancer cells. J Steroid Biochem Mol Biol 65:169–174. https://doi.org/10.1016/S0960-0760(98)00021-1.
  • Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P. 1995. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270:1491–1494. https://doi.org/10.1126/science.270.5241.1491.
  • Jacobs J, Atkins M, Davie K, Imrichova H, Romanelli L, Christiaens V, Hulselmans G, Potier D, Wouters J, Taskiran II, Paciello G, Gonzalez-Blas CB, Koldere D, Aibar S, Halder G, Aerts S. 2018. The transcription factor Grainy head primes epithelial enhancers for spatiotemporal activation by displacing nucleosomes. Nat Genet 50:1011–1020. https://doi.org/10.1038/s41588-018-0140-x.
  • Nevil M, Bondra ER, Schulz KN, Kaplan T, Harrison MM. 2017. Stable binding of the conserved transcription factor Grainy head to its target genes throughout Drosophila melanogaster development. Genetics 205:605–620. https://doi.org/10.1534/genetics.116.195685.
  • Nevil M, Gibson TJ, Bartolutti C, Iyengar A, Harrison MM. 2020. Establishment of chromatin accessibility by the conserved transcription factor Grainy head is developmentally regulated. Development 147:dev185009. https://doi.org/10.1242/dev.185009.
  • Potier D, Davie K, Hulselmans G, Naval Sanchez M, Haagen L, Huynh-Thu VA, Koldere D, Celik A, Geurts P, Christiaens V, Aerts S. 2014. Mapping gene regulatory networks in Drosophila eye development by large-scale transcriptome perturbations and motif inference. Cell Rep 9:2290–2303. https://doi.org/10.1016/j.celrep.2014.11.038.
  • Magnani L, Eeckhoute J, Lupien M. 2011. Pioneer factors: directing transcriptional regulators within the chromatin environment. Trends Genet 27:465–474. https://doi.org/10.1016/j.tig.2011.07.002.
  • Zaret KS, Carroll JS. 2011. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 25:2227–2241. https://doi.org/10.1101/gad.176826.111.
  • Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR, Fox EA, Silver PA, Brown M. 2005. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122:33–43. https://doi.org/10.1016/j.cell.2005.05.008.
  • Kraus WL, Kadonaga JT. 1998. p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes Dev 12:331–342. https://doi.org/10.1101/gad.12.3.331.
  • Martire S, Nguyen J, Sundaresan A, Banaszynski LA. 2020. Differential contribution of p300 and CBP to regulatory element acetylation in mESCs. BMC Mol Cell Biol 21:55. https://doi.org/10.1186/s12860-020-00296-9.
  • Martini M, Gnann A, Scheikl D, Holzmann B, Janssen KP. 2011. The candidate tumor suppressor SASH1 interacts with the actin cytoskeleton and stimulates cell-matrix adhesion. Int J Biochem Cell Biol 43:1630–1640. https://doi.org/10.1016/j.biocel.2011.07.012.
  • Jiang K, Liu P, Xu H, Liang D, Fang K, Du S, Cheng W, Ye L, Liu T, Zhang X, Gong P, Shao S, Wang Y, Meng S. 2020. SASH1 suppresses triple-negative breast cancer cell invasion through YAP-ARHGAP42-actin axis. Oncogene 39:5015–5030. https://doi.org/10.1038/s41388-020-1356-7.
  • FASTQC. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 7 May 2020.
  • Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200.
  • TrimGalore. https://github.com/FelixKrueger/TrimGalore. Accessed 7 May 2020.
  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21. https://doi.org/10.1093/bioinformatics/bts635.
  • Liao Y, Smyth GK, Shi W. 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656.
  • Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8.
  • Stephens M. 2017. False discovery rates: a new deal. Biostatistics 18:275–294. https://doi.org/10.1093/biostatistics/kxw041.
  • pheatmap. https://github.com/raivokolde/pheatmap. Accessed 5 December 2020.
  • Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L, Fu X, Liu S, Bo X, Yu G. 2021. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (Camb) 2:100141. https://doi.org/10.1016/j.xinn.2021.100141.
  • Suarez-Arnedo A, Torres Figueroa F, Clavijo C, Arbelaez P, Cruz JC, Munoz-Camargo C. 2020. An image J plugin for the high throughput image analysis of in vitro scratch wound healing assays. PLoS One 15:e0232565. https://doi.org/10.1371/journal.pone.0232565.
  • Liu N, Hargreaves VV, Zhu Q, Kurland JV, Hong J, Kim W, Sher F, Macias-Trevino C, Rogers JM, Kurita R, Nakamura Y, Yuan GC, Bauer DE, Xu J, Bulyk ML, Orkin SH. 2018. Direct promoter repression by BCL11A controls the fetal to adult hemoglobin switch. Cell 173:430–442.e17. https://doi.org/10.1016/j.cell.2018.03.016.
  • Zhu Q, Liu N, Orkin SH, Yuan GC. 2019. CUT&RUNTools: a flexible pipeline for CUT&RUN processing and footprint analysis. Genome Biol 20:192. https://doi.org/10.1186/s13059-019-1802-4.
  • Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923.
  • Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, Heyne S, Dundar F, Manke T. 2016. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44:W160–W165. https://doi.org/10.1093/nar/gkw257.
  • Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137. https://doi.org/10.1186/gb-2008-9-9-r137.
  • Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38:576–589. https://doi.org/10.1016/j.molcel.2010.05.004.
  • SRA-Toolkit. https://trace.ncbi.nlm.nih.gov/Traces/sra/sra.cgi?view=software. Accessed 21 April 2020.

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