Publications

Faculty in the Department of Epigenetics and Molecular Carcinogenesis have authored more than 350 peer-reviewed publications over the past five years. A selection of our publications is highlighted below.

2018

Franco HL, Nagari A, Malladi V, Li W, Xi Y, Richardson D, Allton KL, Tanaka K, Li J, Murakami S, Keyomarsi K, Bedford MT, Shi X, Li W, Barton MC, Dent SYR, Kraus WL. (2018) Enhancer transcription reveals subtype-specific gene expression programs controlling breast cancer pathogenesis. Genome Res. 28(2):159-170.    

Wang L, Koutelou E, Hirsch C, McCarthy R, Schibler A, Lin K, Lu Y, Jeter C, Shen J, Barton MC, Dent SYR. (2018) GCN5 Regulates FGF Signaling and Activates Selective MYC Target Genes during Early Embryoid Body Differentiation. Stem Cell Reports. 10(1):287-299   

Appikonda S, Thakkar KN, Shah PK, Dent SYR, Andersen JN, Barton MC. (2018) Cross-talk between chromatin acetylation and SUMOylation of tripartite motif-containing protein 24 (TRIM24) impacts cell adhesion. J Biol Chem. 293(19):7476-7485.  

Jain AK, Barton MC. (2018) p53: emerging roles in stem cells, development and beyond. Development. 145(8)   

Bao J, Rousseaux S, Shen J, Lin K, Lu Y, Bedford MT. The arginine methyltransferase CARM1 represses p300•ACT•CREMτ activity and is required for spermiogenesis. (2018) Nucleic Acids Res. 46(9):4327-4343. 

Wible DJ, Bratton SB. (2018)  Reciprocity in ROS and autophagic signaling. Curr Opin Toxicol. 7:28-36. 

Kang R, Zelazowski MJ, Cole F. (2018)  Missing the Mark: PRDM9-Dependent Methylation Is Required for Meiotic DSB Targeting. Mol Cell. 69(5):725-727. 

2017

Mu Y, Zelazowska MA, McBride KM. (2017) Phosphorylation promotes activation-induced cytidine deaminase activity at the Myc oncogene. J Exp Med. 214(12):3543-3552. 

Wan L*, Wen H*, Li Y, Lyu J, Xi Y, Hoshii T, Joseph JK, Wang X, Loh YE, Erb MA, Souza AL, Bradner JE, Shen L, Li W, Allis CD, Armstrong SA, Shi X. (2017) ENL links histone acetylation to oncogeneic gene expression in acute myeloid leukaemia. Nature. 543(7644):265-269 (*equal contribution)

Zelazowski MJ, Sandoval M, Paniker L, Hamilton HM, Han J, Gribbell MA, Kang R, Cole F. (2017)  Age-Dependent Alterations in Meiotic Recombination Cause Chromosome Segregation Errors in Spermatocytes. Cell. 171(3):601-614.e13.

Veland N, Hardikar S, Zhong Y, Gayatri S, Dan J, Strahl BD, Rothbart SB, Bedford MT, Chen T. (2017) The Arginine Methyltransferase PRMT6 Regulates DNA Methylation and Contributes to Global DNA Hypomethylation in Cancer. Cell Rep. 21(12):3390-3397

Mi W, Guan H, Lyu J, Zhao D, Xi Y, Jiang S, Andrews FH, Wang X, Gagea M, Wen H, Tora L, Dent SYR, Kutateladze TG, Li W, Li H, Shi X. (2017) YEATS2 links histone acetylation to tumorigenesis of non-small cell lung cancer. Nat Commun. 8(1):1088

Mu Y, Zelazowska MA, McBride KM. (2017) Phosphorylation promotes activation-induced cytidine deaminase activity at the Myc oncogene. J Exp Med. 214(12):3543-3552.

Bae N, Viviano M, Su X, Lv J, Cheng D, Sagum C, Castellano S, Bai X, Johnson C, Khalil MI, Shen J, Chen K, Li H, Sbardella G, Bedford MT. (2017) Developing Spindlin1 small-molecule inhibitors by using protein microarrays. Nat Chem Biol. 13(7):750-756.

Brahma S, Udugama MI, Kim J, Hada A, Bhardwaj SK, Hailu SG, Lee TH, Bartholomew B. (2017) INO80 exchanges H2A.Z for H2A by translocating on DNA proximal to histone dimers. Nat Commun. 8:15616. 

Carr SM, Munro S, Sagum CA, Fedorov O, Bedford MT, La Thangue NB. (2017) Tudor-domain protein PHF20L1 reads lysine methylated retinoblastoma tumour suppressor protein. Cell Death Differ. 24(12):2139-2149.

Dan J, Rousseau P, Hardikar S, Veland N, Wong J, Autexier C, Chen T. (2017)  Zscan4 Inhibits Maintenance DNA Methylation to Facilitate Telomere Elongation in Mouse Embryonic Stem Cells.Cell Rep. 20(8):1936-1949.

Espejo AB, Gao G, Black K, Gayatri S, Veland N, Kim J, Chen T, Sudol M, Walker C, Bedford MT. (2017) PRMT5 C-terminal Phosphorylation Modulates a 14-3-3/PDZ Interaction Switch. J Biol Chem. 292(6):2255-2265.

Li J, Xi Y, Li W, McCarthy RL, Stratton SA, Zou W, Li W, Dent SY, Jain AK, Barton MC. (2017) TRIM28 interacts with EZH2 and SWI/SNF to activate genes that promote mammosphere formation. Oncogene. 36(21):2991-3001.

Manandhar M, Lowery MG, Boulware KS, Lin KH, Lu Y, Wood RD. (2017) Transcriptional consequences of XPA disruption in human cell lines. DNA Repair (Amst). 57:76-90.

Ortiz GJ, Li Y, Post SM, Pant V, Xiong S, Larsson CA, El-Naggar AK, Johnson DG, Lozano G. (2017) Contrasting effects of an Mdm2 functional polymorphism on tumor phenotypes. Oncogene.  Sep 18. doi: 10.1038/onc.2017.344. [Epub ahead of print]

Takata KI, Reh S, Yousefzadeh MJ, Zelazowski MJ, Bhetawal S, Trono D, Lowery MG, Sandoval M, Takata Y, Lu Y, Lin K, Shen J, Kusewitt DF, McBride KM, Cole F, Wood RD. (2017) Analysis of DNA polymerase ν function in meiotic recombination, immunoglobulin class-switching, and DNA damage tolerance.  PLoS Genet. 13(6):e1006818.

Schrock MS, Batar B, Lee J, Druck T, Ferguson B, Cho JH, Akakpo K, Hagrass H, Heerema NA, Xia F, Parvin JD, Aldaz CM, Huebner K. (2017) Wwox-Brca1 interaction: role in DNA repair pathway choice. Oncogene. 2017 Apr 20;36(16):2215-2227.

Zhu F, Willette-Brown J, Song NY, Lomada D, Song Y, Xue L, Gray Z, Zhao Z, Davis SR, Sun Z, Zhang P, Wu X, Zhan Q, Richie ER, Hu Y. (2017) Autoreactive T Cells and Chronic Fungal Infection Drive Esophageal Carcinogenesis. Cell Host Microbe. 21(4):478-493.

2016

Atanassov BS, Mohan RD, Lan X, Kuang X, Lu Y, Lin K, McIvor E, Li W, Zhang Y, Florens L, Byrum SD, Mackintosh SG, Calhoun-Davis T, Koutelou E, Wang L, Tang DG, Tackett AJ, Washburn MP, Workman JL, Dent SY. (2016) ATXN7L3 and ENY2 Coordinate Activity of Multiple H2B Deubiquitinases Important for Cellular Proliferation and Tumor Growth. Mol Cell. 62(4):558-71.

Bain VE, Gordon J, O’Neil JD, Ramos I, Richie ER, Manley NR. (2016) Tissue-specific roles for sonic hedgehog signaling in establishing thymus and parathyroid organ fate. Development. 143(21):4027-4037.

Jain AK, Xi Y, McCarthy R, Allton K, Akdemir KC, Patel LR, Aronow B, Lin C, Li W, Yang L, Barton MC. (2016) LncPRESS1 Is a p53-Regulated LncRNA that Safeguards Pluripotency by Disrupting SIRT6-Mediated De-acetylation of Histone H3K56. Mol Cell. 64(5):967-981

Lange SS, Tomida J, Boulware KS, Bhetawal S, Wood RD. (2016) The Polymerase Activity of Mammalian DNA Pol ζ Is Specifically Required for Cell and Embryonic Viability.  PLoS Genet. 12(1):e1005759. 

Li Y, Sabari BR, Panchenko T, Wen H, Zhao D, Guan H, Wan L, Huang H, Tang Z, Zhao Y, Roeder RG, Shi X, Allis CD, Li H. (2016) Molecular Coupling of Histone Crotonylation and Active Transcription by AF9 YEATS Domain. Mol Cell. 62(2):181-93. 

Stuckey JI, Dickson BM, Cheng N, Liu Y, Norris JL, Cholensky SH, Tempel W, Qin S, Huber KG, Sagum C, Black K, Li F, Huang XP, Roth BL, Baughman BM, Senisterra G, Pattenden SG, Vedadi M, Brown PJ, Bedford MT, Min J, Arrowsmith CH, James LI, Frye SV. (2016) A cellular chemical probe targeting the chromodomains of Polycomb repressive complex 1.  Nat Chem Biol. 12(3):180-7. 

Vélez-Cruz R, Manickavinayaham S, Biswas AK, Clary RW, Premkumar T, Cole F, Johnson DG. (2016) RB localizes to DNA double-strand breaks and promotes DNA end resection and homologous recombination through the recruitment of BRG1. Genes Dev. 2016 Nov 15;30(22):2500-2512.

Wu CC, Lee S, Malladi S, Chen MD, Mastrandrea NJ, Zhang Z, Bratton SB. (2016) The Apaf-1 apoptosome induces
formation of caspase-9 homo- and heterodimers with distinct activities. Nat Commun. 2016 Nov 24;7:13565

Zhang D, Park D, Zhong Y, Lu Y, Rycaj K, Gong S, Chen X, Liu X, Chao HP, Whitney P, Calhoun-Davis T, Takata Y, Shen J, Iyer VR, Tang DG. (2016) Stem cell and neurogenic gene-expression profiles link prostate basal cells to aggressive prostate cancer. Nat Commun. 7:10798. 

Zhang X, Peng D, Xi Y, Yuan C, Sagum CA, Klein BJ, Tanaka K, Wen H, Kutateladze TG, Li W, Bedford MT, Shi X. (2016) G9a-mediated methylation of ERα links the PHF20/MOF histone acetyltransferase complex to hormonal gene expression.  Nat Commun. 7:10810. 

2015

Hirsch CL, Coban Akdemir Z, Wang L, Jayakumaran G, Trcka D, Weiss A, Hernandez JJ, Pan Q, Han H, Xu X, Xia Z, Salinger AP, Wilson M, Vizeacoumar F, Datti A, Li W, Cooney AJ, Barton MC, Blencowe BJ, Wrana JL, Dent SY. (2015) Myc and SAGA rewire an alternative splicing network during early somatic cell reprogramming.  Genes Dev.29(8):803-16. 

Hu SB, Xiang JF, Li X, Xu Y, Xue W, Huang M, Wong CC, Sagum CA, Bedford MT, Yang L, Cheng D, Chen LL. (2015) Protein arginine methyltransferase CARM1 attenuates the paraspeckle-mediated nuclear retention of mRNAs containing inverted repeat Alus.  Genes Dev. 29(6):630-45.

Kapoor P, Bao Y, Xiao J, Espejo A, Yang L, Bedford MT, Peng G, Shen X. (2015) Phosphorylation-Dependent Enhancement of Rad53 Kinase Activity through the INO80 Chromatin Remodeling Complex. Mol Cell. 58(5):863-9.

Kapoor P, Bao Y, Xiao J, Luo J, Shen J, Persinger J, Peng G, Ranish J, Bartholomew B, Shen X. (2015) Regulation of Mec1 kinase activity by the SWI/SNF chromatin remodeling complex.  Genes Dev. 29(6):591-602. 

Li M, Hada A, Sen P, Olufemi L, Hall MA, Smith BY, Forth S, McKnight JN, Patel A, Bowman GD, Bartholomew B, Wang MD. (2015) Dynamic regulation of transcription factors by nucleosome remodeling. Elife. 4. doi: 10.7554/eLife.06249.

Pathiraja TN, Thakkar KN, Jiang S, Stratton S, Liu Z, Gagea M, Shi X, Shah PK, Phan L, Lee MH, Andersen J, Stampfer M, Barton MC. (2015) TRIM24 links glucose metabolism with transformation of human mammary epithelial cells. Oncogene. 34(22):2836-45.

Yang Y, Hadjikyriacou A, Xia Z, Gayatri S, Kim D, Zurita-Lopez C, Kelly R, Guo A, Li W, Clarke SG, Bedford MT. (2015)  PRMT9 is a type II methyltransferase that methylates the splicing factor SAP145.  Nat Commun. 6:6428.

2014

Biswas AK, Mitchell DL, Johnson DG (2014) E2F1 responds to ultraviolet radiation by directly stimulating DNA repair and suppressing carcinogenesis. Cancer Res. 74(12):3369-77.

Cole F, Baudat F, Grey C, Keeney S, de Massy B, Jasin M (2014) Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet. 46(10):1072-80

Jin M, Zhang T, Liu C, Badeaux MA, Liu B, Liu R, Jeter C, Chen X, Vlassov AV, Tang DG (2014) miRNA-128 suppresses prostate cancer by inhibiting BMI-1 to inhibit tumor-initiating cells. Cancer Res. 74(15):4183-95.

Li Y, Wen H, Xi Y, Tanaka K, Wang H, Peng D, Ren Y, Jin Q, Dent SYR., Li W, Li H, Shi X (2014) AF9 YEATS Domain Links Histone Acetylation to DOT1L-Mediated H3K79 Methylation. Cell.159(3):558-71.

Reeh KA, Cardenas KT, Bain VE, Liu Z, Laurent M, Manley NR, Richie, ER  (2014) Ectopic TBX1 suppresses thymic epithelial cell differentiation and proliferation during thymus organogenesis. Development. 141(15):2950-8.

Wen H, Li Y, Xi Y, Jiang S, Stratton S, Peng D, Tanaka K, Ren Y, Xia Z, Wu J, Li B, Barton MC, Li W, Li H, Shi X (2014) ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature. 508(7495):263-8.

Yang Y, McBride KM, Hensley S, Lu Y, Chedin F, Bedford MT (2014) Arginine methylation facilitates the recruitment of TOP3B to chromatin to prevent R loop accumulation. Mol Cell. 53(3):484-97.

Yousefzadeh MJ, Wyatt DW, Takata K, Mu Y, Hensley SC, Tomida J, Bylund, GO, Doublie S, Johansson E, Ramsden DA, McBride KM and Wood, RD (2014) Mechanism of Suppression of Chromosomal Instability by DNA Polymerase POLQ. PLoS Genet. 10(10):e1004654.

2013

Chen K, Wilson MA, Hirsch C, Watson A, Liang S, Lu Y, Li W, Dent SY (2013) Stabilization of the promoter nucleosomes in nucleosome-free regions by the yeast Cyc8-Tup1 corepressor. Genome Res. 23:312-22.

Johnson DG, Dent SY (2013) Chromatin: receiver and quarterback for cellular signals. Cell. 152(4):685-9.

Kapoor P, Chen M, Winkler DD, Luger K, Shen X (2013) Evidence for monomeric actin function in INO80 chromatin remodeling. Nat Struct Mol Biol. 20(4):426-32.

Lange SS, Bedford E, Reh S, Wittschieben JP, Carbajal S, Kusewitt DF, DiGiovanni J, Wood RD (2013) Dual role for mammalian DNA polymerase zeta in maintaining genome stability and proliferative responses. Proc Natl Acad Sci U S A. 110(8):E687-96.

Li J, Zhao Z, Carter C, Ehrlich LI, Bedford MT, Richie ER (2013) Coactivator-Associated Arginine Methyltransferase 1 Regulates Fetal Hematopoiesis and Thymocyte Development. J Immunol. 190(2):597-604.

Yeh TC, Bratton SB (2013) Caspase-dependent regulation of the ubiquitin-proteasome system through direct substrate targeting. Proc Natl Acad Sci U S A. 110(35):14284-9.

2012

Badeaux AI, Yang Y, Cardenas K, Vemulapalli V, Chen K, Kusewitt D, Richie E, Li W, Bedford MT (2012). Loss of the methyl lysine effector protein PHF20 impacts the expression of genes regulated by the lysine acetyltransferase MOF. J Biol Chem. 287(1):429-37. 

Biswas AK, Johnson DG. (2012) Transcriptional and nontranscriptional functions of E2F1 in response to DNA damage. Cancer Res. 72(1):13-7.

Chen YC, Gatchel JR, Lewis RW, Mao CA, Grant PA, Zoghbi HY, Dent SY (2012) Gcn5 loss-of-function accelerates cerebellar and retinal degeneration in a SCA7 mouse model. Hum Mol Genet. 21(2):394-405.

Ferguson BW, Gao X, Kil H, Lee J, Benavides F, Abba MC, Aldaz CM (2012) Conditional Wwox deletion in mouse mammary gland by means of two Cre recombinase approaches. PLoS One. 7(5):e36618.

Lange SS, Wittschieben JP, Wood RD (2012) DNA polymerase zeta is required for proliferation of normal mammalian cells. Nucleic Acids Res. 40 (10):4473-82.

Lu M, Liu Z, Yu H, Wang LE, Li G, Sturgis EM, Johnson DG, Wei Q (2012) Combined effects of E2F1 and E2F2 polymorphisms on risk and early onset of squamous cell carcinoma of the head and neck. Mol Carcinog. 51 Suppl 1:E132-41. 

Qin J, Liu X, Laffin B, Chen X, Choy G, Jeter CR, Calhoun-Davis T, Li H, Palapattu GS, Pang S, Lin K, Huang J, Ivanov I, Li W, Suraneni MV, Tang DG (2012) The PSA(-/lo) prostate cancer cell population harbors self-renewing long-term tumor-propagating cells that resist castration. Cell Stem Cell. 10(5):556-69.

Regunathan R, Woo J, Pierce MC, Polydorides AD, Raoufi M, Roayaie S, Schwartz M, Labow D, Shin D, Suzuki R, Bhutani MS, Coghlan LG, Richards-Kortum R, Anandasabapathy S, Kim MK. (2012) Feasibility and preliminary accuracy of high-resolution imaging of the liver and pancreas using FNA compatible microendoscopy (with video). Gastrointest Endosc. 76(2):293-300.

2011

Guo R, Chen J, Mitchell DL, Johnson DG (2011) GCN5 and E2F1 stimulate nucleotide excision repair by promoting H3K9 acetylation at sites of damage. Nucleic Acids Res. 39(4):1390-7.

Latham JA, Chosed RJ, Wang S, Dent SY (2011) Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell. 146(5):709-19.

Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 17(2):211-5.

Mitchell D, Paniker L, Godar D (2012) Nucleotide excision repair is reduced in oral epithelial tissues compared with skin. Photochem Photobiol. 88(4):1027-32.

Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JP, Bedford MT (2011) Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Reports. 12(3):238-43.

2010

Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan KL, Shen J, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL (2010) ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci U S A.107:4153-8. 

Guo R, Chen J, Zhu F, Biswas AK, Berton TR, Mitchell DL, Johnson DG (2010) E2F1 localizes to sites of UV-induced DNA damage to enhance nucleotide excision repair. J Biol Chem. 285:19308-15.

Mitchell DL, Fernandez AA, Nairn RS, Garcia R, Paniker L, Trono D, Thames HD, Gimenez-Conti I (2010) Ultraviolet A does not induce melanomas in a Xiphophorus hybrid fish model. Proc Natl Acad Sci U S A. 107(20):9329-34.

Yang Y, Lu Y, Espejo A, Wu J, Xu W, Liang S, Bedford MT (2010) TDRD3 is an effector molecule for arginine-methylated histone marks. Mol Cell. 40(6):1016-23.

Zhu F, Dollé ME, Berton TR, Kuiper RV, Capps C, Espejo A, McArthur MJ, Bedford MT, van Steeg H, de Vries A, Johnson DG (2010) Mouse models for the p53 R72P polymorphism mimic human phenotypes. Cancer Res. 70(14):5851-9.

2009

Atanassov BS, Evrard YA, Multani AS, Zhang Z, Tora L, Devys D, Chang S, Dent SY (2009) Gcn5 and SAGA regulate shelterin protein turnover and telomere maintenance. Mol Cell. 35(3):352-64.

Blando J, Portis M, Benavides F, Alexander A, Mills G, Dave B, Conti CJ, Kim J, Walker CL. (2009) PTEN deficiency is fully penetrant for prostate adenocarcinoma in C57BL/6 mice via mTOR-dependent growth. Am J Pathol. 174(5):1869-79.

Bua DJ, Kuo AJ, Cheung P, Liu CL, Migliori V, Espejo A, Casadio F, Bassi C, Amati B, Bedford MT, Guccione E, Gozani O. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. (2009) PLoS One. 4(8):e6789.

Falbo KB, Alabert C, Katou Y, Wu S, Han J, Wehr T, Xiao J, He X, Zhang Z, Shi Y, Shirahige K, Pasero P, and Shen X (2009) Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nat Struct Mol Biol. 16(11):1167-72.

Griffith AV, Cardenas K, Carter C, Gordon J, Iberg A, Engleka K, Epstein JA, Manley NR, Richie ER (2009) Increased thymus- and decreased parathyroid-fated organ domains in Splotch mutant embryos. Dev Biol. 327(1):216-27.

Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, Liu C, Calhoun-Davis T, Zaehres H, Daley GQ, Tang DG. (2009) Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells. 2009 May;27(5):993-1005.