Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine

Yang, Jie; Horton, John R.; Li, Jia; Huang, Yun; Zhang, Xing; Blumenthal, Robert M.; Cheng, Xiaodong

doi:10.1093/nar/gkz381

Title: Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine

Journal Article · Mon May 13 00:00:00 EDT 2019 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkz381· OSTI ID:1577156

Yang, Jie ^[1]; Horton, John R. ^[1]; Li, Jia ^[2];

^[2]; Zhang, Xing ^[1]; Blumenthal, Robert M. ^[3];

^[1]

Univ. of Texas, Houston, TX (United States)
Texas A & M Univ., Houston, TX (United States)
Univ. of Toledo, OH (United States)

The psychiatric risk-associated transcription factor 4 (TCF4) is linked to schizophrenia. Rare TCF4 coding variants are found in individuals with Pitt-Hopkins syndrome—an intellectual disability and autism spectrum disorder. TCF4 contains a C-terminal basic-helix-loop-helix (bHLH) DNA binding domain which recognizes the enhancer-box (E-box) element 5'-CANNTG-3' (where N = any nucleotide). A subset of the TCF4-occupancy sites have the expanded consensus binding specificity 5'-C(A/G)-CANNTG-3', with an added outer Cp(A/G) dinucleotide; for example in the promoter for CNIH3, a gene involved in opioid dependence. In mammalian genomes, particularly brain, the CpG and CpA dinucleotides can be methylated at the 5-position of cytosine (5mC), and then may undergo successive oxidations to the 5-hydroxymethyl (5hmC), 5-formyl (5fC), and 5-carboxyl (5caC) forms. We find that, in the context of 5'-⁰CG-¹CA-²CG-³TG-3'(where the numbers indicate successive dinucleotides), modification of the central E-box ²CG has very little effect on TCF4 binding, E-box ¹CA modification has a negative influence on binding, while modification of the flanking ⁰CG, particularly carboxylation, has a strong positive impact on TCF4 binding to DNA. Crystallization of TCF4 in complex with unmodified or 5caC-modified oligonucleotides revealed that the basic region of bHLH domain adopts multiple conformations, including an extended loop going through the DNA minor groove, or the N-terminal portion of a long helix binding in the DNA major groove. The different protein conformations enable arginine 576 (R576) to interact, respectively, with a thymine in the minor groove, a phosphate group of DNA backbone, or 5caC in the major groove. The Pitt-Hopkins syndrome mutations affect five arginine residues in the basic region, two of them (R569 and R576) involved in 5caC recognition. Our analyses indicate, and suggest a structural basis for, the preferential recognition of 5caC by a transcription factor centrally important in brain development.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH); Cancer Prevention and Research Institute of Texas; American Cancer Society

Grant/Contract Number:: GM049245-24; HL134780; RR160029; RSG-18-043-01-LIB

OSTI ID:: 1577156

Journal Information:: Nucleic Acids Research, Vol. 47, Issue 16; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 13 works

Citation information provided by
Web of Science

References (78)

Transient Accumulation of 5-Carboxylcytosine Indicates Involvement of Active Demethylation in Lineage Specification of Neural Stem Cells Wheldon, Lee M.; Abakir, Abdulkadir; Ferjentsik, Zoltan Cell Reports, Vol. 7, Issue 5 https://doi.org/10.1016/j.celrep.2014.05.003	journal	June 2014
Model-based Analysis of ChIP-Seq (MACS) Zhang, Yong; Liu, Tao; Meyer, Clifford A. Genome Biology, Vol. 9, Issue 9 https://doi.org/10.1186/gb-2008-9-9-r137	journal	January 2008
Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Ellenberger, T.; Fass, D.; Arnaud, M. Genes & Development, Vol. 8, Issue 8 https://doi.org/10.1101/gad.8.8.970	journal	April 1994
Common variants conferring risk of schizophrenia Stefansson, Hreinn; Ophoff, Roel A.; Steinberg, Stacy Nature, Vol. 460, Issue 7256 https://doi.org/10.1038/nature08186	journal	July 2009
The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain Kriaucionis, S.; Heintz, N. Science, Vol. 324, Issue 5929 https://doi.org/10.1126/science.1169786	journal	April 2009
Global Epigenomic Reconfiguration During Mammalian Brain Development Lister, R.; Mukamel, E. A.; Nery, J. R. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.1237905	journal	July 2013
Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc Blackwood, E.; Eisenman, R. Science, Vol. 251, Issue 4998 https://doi.org/10.1126/science.2006410	journal	March 1991
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Functional Diversity of Human Basic Helix-Loop-Helix Transcription Factor TCF4 Isoforms Generated by Alternative 5′ Exon Usage and Splicing Sepp, Mari; Kannike, Kaja; Eesmaa, Ave PLoS ONE, Vol. 6, Issue 7 https://doi.org/10.1371/journal.pone.0022138	journal	July 2011
The Phyre2 web portal for protein modeling, prediction and analysis Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M. Nature Protocols, Vol. 10, Issue 6 https://doi.org/10.1038/nprot.2015.053	journal	May 2015
Lmx1a drives Cux2 expression in the cortical hem through activation of a conserved intronic enhancer Fregoso, Santiago P.; Dwyer, Brett E.; Franco, Santos J. Development, Vol. 146, Issue 5 https://doi.org/10.1242/dev.170068	journal	February 2019
Functional analysis of TCF4 missense mutations that cause Pitt-Hopkins syndrome Forrest, Marc; Chapman, Ria M.; Doyle, A. Michelle Human Mutation, Vol. 33, Issue 12 https://doi.org/10.1002/humu.22160	journal	July 2012
Introducing Pitt-Hopkins syndrome-associated mutations of TCF4 to Drosophila daughterless Tamberg, L.; Sepp, M.; Timmusk, T. Biology Open, Vol. 4, Issue 12 https://doi.org/10.1242/bio.014696	journal	November 2015
The Psychiatric Risk Gene Transcription Factor 4 (TCF4) Regulates Neurodevelopmental Pathways Associated With Schizophrenia, Autism, and Intellectual Disability Forrest, Marc P.; Hill, Matthew J.; Kavanagh, David H. Schizophrenia Bulletin, Vol. 44, Issue 5 https://doi.org/10.1093/schbul/sbx164	journal	December 2017
MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma Wang, Dongxue; Hashimoto, Hideharu; Zhang, Xing Nucleic Acids Research, Vol. 45, Issue 5 https://doi.org/10.1093/nar/gkw1184	journal	November 2016
Genome-wide Analysis Reveals TET- and TDG-Dependent 5-Methylcytosine Oxidation Dynamics Shen, Li; Wu, Hao; Diep, Dinh Cell, Vol. 153, Issue 3 https://doi.org/10.1016/j.cell.2013.04.002	journal	April 2013
Helix-Loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms Massari, M. E.; Murre, C. Molecular and Cellular Biology, Vol. 20, Issue 2 https://doi.org/10.1128/MCB.20.2.429-440.2000	journal	January 2000
Genome-wide Profiling of 5-Formylcytosine Reveals Its Roles in Epigenetic Priming Song, Chun-Xiao; Szulwach, Keith E.; Dai, Qing Cell, Vol. 153, Issue 3 https://doi.org/10.1016/j.cell.2013.04.001	journal	April 2013
Crystal Structure of a Complex of DNA with One AT-Hook of HMGA1 Fonfría-Subirós, Elsa; Acosta-Reyes, Francisco; Saperas, Núria PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0037120	journal	May 2012
The emerging roles of TCF4 in disease and development Forrest, Marc P.; Hill, Matthew J.; Quantock, Andrew J. Trends in Molecular Medicine, Vol. 20, Issue 6 https://doi.org/10.1016/j.molmed.2014.01.010	journal	June 2014
Tcf4 Regulates Synaptic Plasticity, DNA Methylation, and Memory Function Kennedy, Andrew J.; Rahn, Elizabeth J.; Paulukaitis, Brynna S. Cell Reports, Vol. 16, Issue 10 https://doi.org/10.1016/j.celrep.2016.08.004	journal	September 2016
Detecting and interpreting DNA methylation marks Ren, Ren; Horton, John R.; Zhang, Xing Current Opinion in Structural Biology, Vol. 53 https://doi.org/10.1016/j.sbi.2018.06.004	journal	December 2018
Mutational, functional, and expression studies of the TCF4 gene in Pitt-Hopkins syndrome de Pontual, Lo��c; Mathieu, Yves; Golzio, Christelle Human Mutation, Vol. 30, Issue 4 https://doi.org/10.1002/humu.20935	journal	April 2009
Carboxylation of cytosine (5caC) in the CG dinucleotide in the E-box motif (CGCAG\|GTG) increases binding of the Tcf3\|Ascl1 helix-loop-helix heterodimer 10-fold Golla, Jaya Prakash; Zhao, Jianfei; Mann, Ishminder K. Biochemical and Biophysical Research Communications, Vol. 449, Issue 2 https://doi.org/10.1016/j.bbrc.2014.05.018	journal	June 2014
Cistrome Data Browser: expanded datasets and new tools for gene regulatory analysis Zheng, Rongbin; Wan, Changxin; Mei, Shenglin Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky1094	journal	November 2018
A Druggable TCF4- and BRD4-Dependent Transcriptional Network Sustains Malignancy in Blastic Plasmacytoid Dendritic Cell Neoplasm Ceribelli, Michele; Hou, Zhiying Esther; Kelly, Priscilla N. Cancer Cell, Vol. 30, Issue 5 https://doi.org/10.1016/j.ccell.2016.10.002	journal	November 2016
Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine Ito, S.; Shen, L.; Dai, Q. Science, Vol. 333, Issue 6047 https://doi.org/10.1126/science.1210597	journal	July 2011
Simultaneous mapping of active DNA demethylation and sister chromatid exchange in single cells Wu, Xiaoji; Inoue, Azusa; Suzuki, Tsukasa Genes & Development, Vol. 31, Issue 5 https://doi.org/10.1101/gad.294843.116	journal	March 2017
Investigation of the role of TCF4 rare sequence variants in schizophrenia Basmanav, F. Buket; Forstner, Andreas J.; Fier, Heide American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, Vol. 168, Issue 5 https://doi.org/10.1002/ajmg.b.32318	journal	May 2015
Evidence of CNIH3 involvement in opioid dependence Nelson, E. C.; Agrawal, A.; Heath, A. C. Molecular Psychiatry, Vol. 21, Issue 5 https://doi.org/10.1038/mp.2015.102	journal	August 2015
daughterless, a Drosophila gene essential for both neurogenesis and sex determination, has sequence similarities to myc and the achaete-scute complex Caudy, Michael; Vässin, Harald; Brand, Michael Cell, Vol. 55, Issue 6 https://doi.org/10.1016/0092-8674(88)90250-4	journal	December 1988
Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1 Tahiliani, M.; Koh, K. P.; Shen, Y. Science, Vol. 324, Issue 5929 https://doi.org/10.1126/science.1170116	journal	April 2009
Crystal Structure of E47−NeuroD1/Beta2 bHLH Domain−DNA Complex: Heterodimer Selectivity and DNA Recognition ^† ^, ^‡ Longo, Antonella; Guanga, Gerald P.; Rose, Robert B. Biochemistry, Vol. 47, Issue 1 https://doi.org/10.1021/bi701527r	journal	January 2008
Base-resolution maps of 5-formylcytosine and 5-carboxylcytosine reveal genome-wide DNA demethylation dynamics Lu, Xingyu; Han, Dali; Zhao, Boxuan Simen Cell Research, Vol. 25, Issue 3 https://doi.org/10.1038/cr.2015.5	journal	January 2015
Single-base resolution analysis of active DNA demethylation using methylase-assisted bisulfite sequencing Wu, Hao; Wu, Xiaoji; Shen, Li Nature Biotechnology, Vol. 32, Issue 12 https://doi.org/10.1038/nbt.3073	journal	November 2014
5-formylcytosine and 5-carboxylcytosine reduce the rate and substrate specificity of RNA polymerase II transcription Kellinger, Matthew W.; Song, Chun-Xiao; Chong, Jenny Nature Structural & Molecular Biology, Vol. 19, Issue 8 https://doi.org/10.1038/nsmb.2346	journal	July 2012
Building a schizophrenia genetic network: transcription factor 4 regulates genes involved in neuronal development and schizophrenia risk Xia, Hanzhang; Jahr, Fay M.; Kim, Nak-Kyeong Human Molecular Genetics, Vol. 27, Issue 18 https://doi.org/10.1093/hmg/ddy222	journal	June 2018
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Tet3 CXXC Domain and Dioxygenase Activity Cooperatively Regulate Key Genes for Xenopus Eye and Neural Development Xu, Yufei; Xu, Chao; Kato, Akiko Cell, Vol. 151, Issue 6 https://doi.org/10.1016/j.cell.2012.11.014	journal	December 2012
Single-Base Resolution Analysis of 5-Formyl and 5-Carboxyl Cytosine Reveals Promoter DNA Methylation Dynamics Neri, Francesco; Incarnato, Danny; Krepelova, Anna Cell Reports, Vol. 10, Issue 5 https://doi.org/10.1016/j.celrep.2015.01.008	journal	February 2015
Using a structural and logics systems approach to infer bHLH–DNA binding specificity determinants De Masi, Federico; Grove, Christian A.; Vedenko, Anastasia Nucleic Acids Research, Vol. 39, Issue 11 https://doi.org/10.1093/nar/gkr070	journal	February 2011
Quantitative Analysis of the DNA Methylation Sensitivity of Transcription Factor Complexes Kribelbauer, Judith F.; Laptenko, Oleg; Chen, Siying Cell Reports, Vol. 19, Issue 11 https://doi.org/10.1016/j.celrep.2017.05.069	journal	June 2017
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Severe mental retardation with breathing abnormalities (Pitt–Hopkins syndrome) is caused by haploinsufficiency of the neuronal bHLH transcription factor TCF4 Brockschmidt, Antje; Todt, Unda; Ryu, Soojin Human Molecular Genetics, Vol. 16, Issue 12 https://doi.org/10.1093/hmg/ddm099	journal	May 2007
Medulloblastoma and ependymoma cells display increased levels of 5-carboxylcytosine and elevated TET1 expression Ramsawhook, Ashley; Lewis, Lara; Coyle, Beth Clinical Epigenetics, Vol. 9, Issue 1 https://doi.org/10.1186/s13148-016-0306-2	journal	February 2017
Genomic distribution of 5‐formylcytosine and 5‐carboxylcytosine in human preimplantation embryos Pendina, Anna A.; Efimova, Olga A.; Krapivin, Mikhail I. Molecular Reproduction and Development, Vol. 85, Issue 12 https://doi.org/10.1002/mrd.23074	journal	November 2018
Impact of cytosine methylation on DNA binding specificities of human transcription factors Yin, Yimeng; Morgunova, Ekaterina; Jolma, Arttu Science, Vol. 356, Issue 6337 https://doi.org/10.1126/science.aaj2239	journal	May 2017
Pitt–Hopkins syndrome-associated mutations in TCF4 lead to variable impairment of the transcription factor function ranging from hypomorphic to dominant-negative effects Sepp, Mari; Pruunsild, Priit; Timmusk, Tõnis Human Molecular Genetics, Vol. 21, Issue 13 https://doi.org/10.1093/hmg/dds112	journal	March 2012
Cognitive and Sensorimotor Gating Impairments in Transgenic Mice Overexpressing the Schizophrenia Susceptibility Gene Tcf4 in the Brain Brzózka, Magdalena M.; Radyushkin, Konstantin; Wichert, Sven P. Biological Psychiatry, Vol. 68, Issue 1 https://doi.org/10.1016/j.biopsych.2010.03.015	journal	July 2010
Measurement of protein by spectrophotometry at 205 nm Scopes, R. K. Analytical Biochemistry, Vol. 59, Issue 1 https://doi.org/10.1016/0003-2697(74)90034-7	journal	May 1974
Structure and function of helix-loop-helix proteins Murre, Cornelis; Bain, Gretchen; van Dijk, Marc A. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1218, Issue 2 https://doi.org/10.1016/0167-4781(94)90001-9	journal	June 1994
A Sensitive Approach to Map Genome-wide 5-Hydroxymethylcytosine and 5-Formylcytosine at Single-Base Resolution Sun, Zhiyi; Dai, Nan; Borgaro, Janine G. Molecular Cell, Vol. 57, Issue 4 https://doi.org/10.1016/j.molcel.2014.12.035	journal	February 2015
TRIM8-driven transcriptomic profile of neural stem cells identified glioma-related nodal genes and pathways Venuto, Santina; Castellana, Stefano; Monti, Maria Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1863, Issue 2 https://doi.org/10.1016/j.bbagen.2018.12.001	journal	February 2019
A survey of rare coding variants in candidate genes in schizophrenia by deep sequencing Hu, X.; Zhang, B.; Liu, W. Molecular Psychiatry, Vol. 19, Issue 8 https://doi.org/10.1038/mp.2013.131	journal	October 2013
Sequence-specific recognition of double helical nucleic acids by proteins. Seeman, N. C.; Rosenberg, J. M.; Rich, A. Proceedings of the National Academy of Sciences, Vol. 73, Issue 3 https://doi.org/10.1073/pnas.73.3.804	journal	March 1976
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif Henthorn, P.; Kiledjian, M.; Kadesch, T. Science, Vol. 247, Issue 4941 https://doi.org/10.1126/science.2105528	journal	January 1990
Tcf4 regulates dendritic spine density and morphology in the adult brain Crux, Sophie; Herms, Jochen; Dorostkar, Mario M. PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0199359	journal	June 2018
Mutations in TCF4, Encoding a Class I Basic Helix-Loop-Helix Transcription Factor, Are Responsible for Pitt-Hopkins Syndrome, a Severe Epileptic Encephalopathy Associated with Autonomic Dysfunction Amiel, Jeanne; Rio, Marlène; Pontual, Loïc de The American Journal of Human Genetics, Vol. 80, Issue 5 https://doi.org/10.1086/515582	journal	May 2007
Tet3 Reads 5-Carboxylcytosine through Its CXXC Domain and Is a Potential Guardian against Neurodegeneration Jin, Seung-Gi; Zhang, Zhi-Min; Dunwell, Thomas L. Cell Reports, Vol. 14, Issue 3 https://doi.org/10.1016/j.celrep.2015.12.044	journal	January 2016
Haploinsufficiency of TCF4 Causes Syndromal Mental Retardation with Intermittent Hyperventilation (Pitt-Hopkins Syndrome) Zweier, Christiane; Peippo, Maarit M.; Hoyer, Juliane The American Journal of Human Genetics, Vol. 80, Issue 5 https://doi.org/10.1086/515583	journal	May 2007
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
seqQscorer: automated quality control of next-generation sequencing data using machine learning Albrecht, Steffen; Sprang, Maximilian; Andrade-Navarro, Miguel A. Genome Biology, Vol. 22, Issue 1 https://doi.org/10.1186/s13059-021-02294-2	journal	March 2021
Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine C., Wu, S.; Y., Zhang,; B., Collins, L. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/w7hh-zy88	text	January 2011
Improved crystallographic models through iterated local density-guided model deformation and reciprocal-space refinement. Terwilliger, Thomas C.; Read, Randy; Adams, Paul D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52317	text	January 2012
Quantitative Analysis of the DNA Methylation Sensitivity of Transcription Factor Complexes Kribelbauer, Judith F.; Laptenko, Oleg; Chen, Siying Columbia University https://doi.org/10.7916/d8wd5c2k	text	January 2017
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins Murre, Cornelis; McCaw, Patrick Schonleber; Baltimore, David Cell, Vol. 56, Issue 5 https://doi.org/10.1016/0092-8674(89)90682-x	journal	March 1989
Association of Myn, the murine homolog of Max, with c-Myc stimulates methylation-sensitive DNA binding and ras cotransformation Prendergast, George C.; Lawe, Deirdre; Ziff, Edward B. Cell, Vol. 65, Issue 3 https://doi.org/10.1016/0092-8674(91)90457-a	journal	May 1991
5-Hydroxymethylcytosine in E-box motifs ACAT\|GTG and ACAC\|GTG increases DNA-binding of the B-HLH transcription factor TCF4 Khund-Sayeed, Syed; He, Ximiao; Holzberg, Timothy Integrative Biology, Vol. 8, Issue 9 https://doi.org/10.1039/c6ib00079g	journal	January 2016
Carbon-Oxygen Hydrogen Bonding in Biological Structure and Function Horowitz, Scott; Trievel, Raymond C. Journal of Biological Chemistry, Vol. 287, Issue 50 https://doi.org/10.1074/jbc.r112.418574	journal	October 2012
Multiparametric scaling of diffraction intensities Otwinowski, Zbyszek; Borek, Dominika; Majewski, Wladyslaw Acta Crystallographica Section A Foundations of Crystallography, Vol. 59, Issue 3 https://doi.org/10.1107/s0108767303005488	journal	April 2003
A statistic for local intensity differences: robustness to anisotropy and pseudo-centering and utility for detecting twinning Padilla, Jennifer E.; Yeates, Todd O. Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7 https://doi.org/10.1107/s0907444903007947	journal	June 2003
Improved crystallographic models through iterated local density-guided model deformation and reciprocal-space refinement Terwilliger, Thomas C.; Read, Randy J.; Adams, Paul D. Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 7 https://doi.org/10.1107/s0907444912015636	journal	June 2012
A Syndrome of Mental Retardation, Wide Mouth and Intermittent Overbreathing Pitt, D.; Hopkins, I. Journal of Paediatrics and Child Health, Vol. 14, Issue 3 https://doi.org/10.1111/jpc.1978.14.3.182	journal	September 1978
Transcription factors read epigenetics Hughes, Timothy R.; Lambert, Samuel A. Science, Vol. 356, Issue 6337 https://doi.org/10.1126/science.aan2927	journal	May 2017
Deep C diving: mapping the low-abundance modifications of the DNA demethylation pathway Thomson, John P.; Hunter, Jennifer M.; Meehan, Richard R. Genome Biology, Vol. 14, Issue 5 https://doi.org/10.1186/gb-2013-14-5-118	journal	May 2013

Cited By (2)

bZIP Dimers CREB1, ATF2, Zta, ATF3\|cJun, and cFos\|cJun Prefer to Bind to Some Double-Stranded DNA Sequences Containing 5-Formylcytosine and 5-Carboxylcytosine Ray, Sreejana; Tillo, Desiree; Ufot, Aniekanabasi Biochemistry, Vol. 59, Issue 38 https://doi.org/10.1021/acs.biochem.0c00475	journal	September 2020
Transcription factor 4 and its association with psychiatric disorders Teixeira, José R.; Szeto, Ryan A.; Carvalho, Vinicius M. A. Translational Psychiatry, Vol. 11, Issue 1 https://doi.org/10.1038/s41398-020-01138-0	journal	January 2021

Similar Records

MAX is an epigenetic sensor of 5-carboxylcytosine and is altered in multiple myeloma

Journal Article · Mon Nov 28 00:00:00 EST 2016 · Nucleic Acids Research · OSTI ID:1577156

Wang, Dongxue; Hashimoto, Hideharu; Zhang, Xing; +5 more

Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins

Journal Article · Tue Feb 01 00:00:00 EST 1994 · Molecular and Cellular Biology · OSTI ID:1577156

Hsu, Hai-Ling; Huang, Lan; Tsan, Julia Tsou

Differential Stabilities and Sequence-Dependent Base Pair Opening Dynamics of Watson–Crick Base Pairs with 5-Hydroxymethylcytosine, 5-Formylcytosine, or 5-Carboxylcytosine

Journal Article · Thu Jan 29 00:00:00 EST 2015 · Biochemistry · OSTI ID:1577156

Szulik, Marta W.; Pallan, Pradeep S.; Nocek, Boguslaw; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Structural basis for preferential binding of human TCF4 to DNA containing 5-carboxylcytosine

Citation Formats

References (78)

Cited By (2)

Similar Records

Related Subjects