Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters
Abstract
The MuvB complex recruits transcription factors to activate or repress genes with cell cycle-dependent expression patterns. MuvB contains the DNA-binding protein LIN54, which directs the complex to promoter cell cycle genes homology region (CHR) elements. Here we characterize the DNA-binding properties of LIN54 and describe the structural basis for recognition of a CHR sequence. We biochemically define the CHR consensus as TTYRAA and determine that two tandem cysteine rich regions are required for high-affinity DNA association. A crystal structure of the LIN54 DNA-binding domain in complex with a CHR sequence reveals that sequence specificity is conferred by two tyrosine residues, which insert into the minor groove of the DNA duplex. We demonstrate that this unique tyrosine-mediated DNA binding is necessary for MuvB recruitment to target promoters. Our results suggest a model in which MuvB binds near transcription start sites and plays a role in positioning downstream nucleosomes.
- Authors:
-
- Univ. of California, Santa Cruz, CA (United States)
- Virginia Commonwealth Univ., Richmond, VA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC); UC Office of the President, Multicampus Research Programs and Initiatives Grant; Sandler Foundation; National Institutes of Health (NIH)
- OSTI Identifier:
- 1357644
- Grant/Contract Number:
- AC02-06CH11357; MR-15-328599; R01CA188571; R01GM34059; R01CA132685
- Resource Type:
- Journal Article: Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Cell division; Transcription; X-ray crystallography
Citation Formats
Marceau, Aimee H., Felthousen, Jessica G., Goetsch, Paul D., Iness, Audra N., Lee, Hsiau-Wei, Tripathi, Sarvind M., Strome, Susan, Litovchick, Larisa, and Rubin, Seth M. Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters. United States: N. p., 2016.
Web. doi:10.1038/ncomms12301.
Marceau, Aimee H., Felthousen, Jessica G., Goetsch, Paul D., Iness, Audra N., Lee, Hsiau-Wei, Tripathi, Sarvind M., Strome, Susan, Litovchick, Larisa, & Rubin, Seth M. Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters. United States. https://doi.org/10.1038/ncomms12301
Marceau, Aimee H., Felthousen, Jessica G., Goetsch, Paul D., Iness, Audra N., Lee, Hsiau-Wei, Tripathi, Sarvind M., Strome, Susan, Litovchick, Larisa, and Rubin, Seth M. 2016.
"Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters". United States. https://doi.org/10.1038/ncomms12301. https://www.osti.gov/servlets/purl/1357644.
@article{osti_1357644,
title = {Structural basis for LIN54 recognition of CHR elements in cell cycle-regulated promoters},
author = {Marceau, Aimee H. and Felthousen, Jessica G. and Goetsch, Paul D. and Iness, Audra N. and Lee, Hsiau-Wei and Tripathi, Sarvind M. and Strome, Susan and Litovchick, Larisa and Rubin, Seth M.},
abstractNote = {The MuvB complex recruits transcription factors to activate or repress genes with cell cycle-dependent expression patterns. MuvB contains the DNA-binding protein LIN54, which directs the complex to promoter cell cycle genes homology region (CHR) elements. Here we characterize the DNA-binding properties of LIN54 and describe the structural basis for recognition of a CHR sequence. We biochemically define the CHR consensus as TTYRAA and determine that two tandem cysteine rich regions are required for high-affinity DNA association. A crystal structure of the LIN54 DNA-binding domain in complex with a CHR sequence reveals that sequence specificity is conferred by two tyrosine residues, which insert into the minor groove of the DNA duplex. We demonstrate that this unique tyrosine-mediated DNA binding is necessary for MuvB recruitment to target promoters. Our results suggest a model in which MuvB binds near transcription start sites and plays a role in positioning downstream nucleosomes.},
doi = {10.1038/ncomms12301},
url = {https://www.osti.gov/biblio/1357644},
journal = {Nature Communications},
issn = {2041-1723},
number = 1,
volume = 7,
place = {United States},
year = {Thu Jul 28 00:00:00 EDT 2016},
month = {Thu Jul 28 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
Human housekeeping genes, revisited
journal, October 2013
- Eisenberg, Eli; Levanon, Erez Y.
- Trends in Genetics, Vol. 29, Issue 10
Native E2F/RBF Complexes Contain Myb-Interacting Proteins and Repress Transcription of Developmentally Controlled E2F Target Genes
journal, October 2004
- Korenjak, Michael; Taylor-Harding, Barbie; Binné, Ulrich K.
- Cell, Vol. 119, Issue 2
Disruption of pocket protein dream complexes by E7 proteins of different types of human papillomaviruses
journal, January 2013
- Rashid, N. Nor; Yusof, R.; Watson, R. J.
- Acta virologica, Vol. 57, Issue 04
Mapping and analysis of chromatin state dynamics in nine human cell types
journal, March 2011
- Ernst, Jason; Kheradpour, Pouya; Mikkelsen, Tarjei S.
- Nature, Vol. 473, Issue 7345
Solving structures of protein complexes by molecular replacement with Phaser
journal, December 2006
- McCoy, Airlie J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1
The CHR site: definition and genome-wide identification of a cell cycle transcriptional element
journal, August 2014
- Müller, Gerd A.; Wintsche, Axel; Stangner, Konstanze
- Nucleic Acids Research, Vol. 42, Issue 16
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome
journal, January 2009
- Langmead, Ben; Trapnell, Cole; Pop, Mihai
- Genome Biology, Vol. 10, Issue 3
Structural and Energetic Basis of Carbohydrate–Aromatic Packing Interactions in Proteins
journal, June 2013
- Chen, Wentao; Enck, Sebastian; Price, Joshua L.
- Journal of the American Chemical Society, Vol. 135, Issue 26
A Structural Basis for Recognition of A·T and T·A Base Pairs in the Minor Groove of B-DNA
journal, October 1998
- Kielkopf, C. L.
- Science, Vol. 282, Issue 5386
Structure of the even-skipped homeodomain complexed to AT-rich DNA: new perspectives on homeodomain specificity.
journal, December 1995
- Hirsch, J. A.; Aggarwal, A. K.
- The EMBO Journal, Vol. 14, Issue 24
LINC, a Human Complex That is Related to pRB-Containing Complexes in Invertebrates Regulates the Expression of G 2 /M Genes
journal, August 2007
- Schmit, Fabienne; Korenjak, Michael; Mannefeld, Mirijam
- Cell Cycle, Vol. 6, Issue 15
Chromosome-Biased Binding and Gene Regulation by the Caenorhabditis elegans DRM Complex
journal, May 2011
- Tabuchi, Tomoko M.; Deplancke, Bart; Osato, Naoki
- PLoS Genetics, Vol. 7, Issue 5
Structure of the Rb C-Terminal Domain Bound to E2F1-DP1: A Mechanism for Phosphorylation-Induced E2F Release
journal, December 2005
- Rubin, Seth M.; Gall, Anne-Laure; Zheng, Ning
- Cell, Vol. 123, Issue 6
The conserved cysteine-rich domain of a tesmin/TSO1-like protein binds zinc in vitro and TSO1 is required for both male and female fertility in Arabidopsis thaliana
journal, October 2007
- Andersen, Stig Uggerhøj; Algreen-Petersen, Randi Groslier; Hoedl, Martina
- Journal of Experimental Botany, Vol. 58, Issue 13
Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation
journal, December 2014
- Zheng, Sanduo; Villa, Raffaella; Wang, Jia
- Genes & Development, Vol. 28, Issue 23
The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression
journal, March 2012
- Sadasivam, S.; Duan, S.; DeCaprio, J. A.
- Genes & Development, Vol. 26, Issue 5
Two distinct modes of protein-induced bending in DNA 1 1Edited by J. Karn
journal, September 1998
- El Hassan, M. A.; Calladine, C. R.
- Journal of Molecular Biology, Vol. 282, Issue 2
The CCP4 suite programs for protein crystallography
journal, September 1994
- ,
- Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763
A Novel Testis-Specific Metallothionein-like Protein,Tesmin,Is an Early Marker of Male Germ Cell Differentiation
journal, April 1999
- Sugihara, Takashi; Wadhwa, Renu; Kaul, Sunil C.
- Genomics, Vol. 57, Issue 1
Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex
journal, December 2004
- Lewis, P. W.
- Genes & Development, Vol. 18, Issue 23
Structural plasticity of histones H3–H4 facilitates their allosteric exchange between RbAp48 and ASF1
journal, November 2012
- Zhang, Wei; Tyl, Marek; Ward, Richard
- Nature Structural & Molecular Biology, Vol. 20, Issue 1
NCBI GEO: archive for functional genomics data sets—update
journal, November 2012
- Barrett, Tanya; Wilhite, Stephen E.; Ledoux, Pierre
- Nucleic Acids Research, Vol. 41, Issue D1
Tombola, a tesmin/TSO1-family protein, regulates transcriptional activation in the Drosophila male germline and physically interacts with Always early
journal, March 2007
- Jiang, J.; Benson, E.; Bausek, N.
- Development, Vol. 134, Issue 8
Localizing the NADP+ binding site on the MurB enzyme by NMR
journal, December 1996
- Farmer, Bennett T.; Constantine, Keith L.; Goldfarb, Valentina
- Nature Structural Biology, Vol. 3, Issue 12
Localizing the NADP+ binding site on the MurB enzyme by NMR
journal, December 1996
- Farmer, Bennett T.; Constantine, Keith L.; Goldfarb, Valentina
- Nature Structural Biology, Vol. 3, Issue 12
Cell cycle regulation of the cyclin A, cdc25C and cdc2 genes is based on a common mechanism of transcriptional repression.
journal, September 1995
- Zwicker, J.; Lucibello, F. C.; Wolfraim, L. A.
- The EMBO Journal, Vol. 14, Issue 18
An integrated encyclopedia of DNA elements in the human genome
journal, September 2012
- ,
- Nature, Vol. 489, Issue 7414, p. 57-74
The DREAM complex: master coordinator of cell cycle-dependent gene expression
journal, July 2013
- Sadasivam, Subhashini; DeCaprio, James A.
- Nature Reviews Cancer, Vol. 13, Issue 8
Tombola, a tesmin/TSO1-family protein, regulates transcriptional activation in the Drosophila male germline and physically interacts with Always early
journal, March 2007
- Jiang, J.; Benson, E.; Bausek, N.
- Development, Vol. 134, Issue 8
NMR View: A computer program for the visualization and analysis of NMR data
journal, September 1994
- Johnson, Bruce A.; Blevins, Richard A.
- Journal of Biomolecular NMR, Vol. 4, Issue 5
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
The CHR promoter element controls cell cycle-dependent gene transcription and binds the DREAM and MMB complexes
journal, November 2011
- Müller, Gerd A.; Quaas, Marianne; Schümann, Michael
- Nucleic Acids Research, Vol. 40, Issue 4
ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases
journal, January 2014
- Shen, Li; Shao, Ningyi; Liu, Xiaochuan
- BMC Genomics, Vol. 15, Issue 1
Structural mechanisms of DREAM complex assembly and regulation
journal, April 2015
- Guiley, Keelan Z.; Liban, Tyler J.; Felthousen, Jessica G.
- Genes & Development, Vol. 29, Issue 9
DNA–protein π-interactions in nature: abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar
journal, April 2014
- Wilson, Katie A.; Kellie, Jennifer L.; Wetmore, Stacey D.
- Nucleic Acids Research, Vol. 42, Issue 10
Solution Structure of MSL2 CXC Domain Reveals an Unusual Zn3Cys9 Cluster and Similarity to Pre-SET Domains of Histone Lysine Methyltransferases
journal, September 2012
- Zheng, Sanduo; Wang, Jia; Feng, Yingang
- PLoS ONE, Vol. 7, Issue 9
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly
journal, April 2011
- Litovchick, L.; Florens, L. A.; Swanson, S. K.
- Genes & Development, Vol. 25, Issue 8
Structure of the Rb C-Terminal Domain Bound to E2F1-DP1: A Mechanism for Phosphorylation-Induced E2F Release
journal, December 2005
- Rubin, Seth M.; Gall, Anne-Laure; Zheng, Ning
- Cell, Vol. 123, Issue 6
Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression
journal, April 2000
- Takahashi, Yasuhiko; Rayman, Joseph B.; Dynlacht, Brian David
- Genes & Development, Vol. 14, Issue 7
NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995
- Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
- Journal of Biomolecular NMR, Vol. 6, Issue 3
LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner: LIN54 is an essential core subunit of the DREAM/LINC complex
journal, September 2009
- Schmit, Fabienne; Cremer, Sarah; Gaubatz, Stefan
- FEBS Journal, Vol. 276, Issue 19
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities
journal, May 2010
- Heinz, Sven; Benner, Christopher; Spann, Nathanael
- Molecular Cell, Vol. 38, Issue 4
Conserved functions of the pRB and E2F families
journal, September 2008
- van den Heuvel, Sander; Dyson, Nicholas J.
- Nature Reviews Molecular Cell Biology, Vol. 9, Issue 9
Conformational characteristics of DNA: empirical classifications and a hypothesis for the conformational behaviour of dinucleotide steps
journal, January 1997
- El Hassan, M. A.; Calladine, C. R.
- Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences, Vol. 355, Issue 1722
C-h⋯π-interactions in proteins
journal, March 2001
- Brandl, Maria; Weiss, Manfred S.; Jabs, Andreas
- Journal of Molecular Biology, Vol. 307, Issue 1
Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter
journal, October 2011
- Rubio-Cosials, Anna; Sydow, Jasmin F.; Jiménez-Menéndez, Nereida
- Nature Structural & Molecular Biology, Vol. 18, Issue 11
Human housekeeping genes, revisited
journal, October 2013
- Eisenberg, Eli; Levanon, Erez Y.
- Trends in Genetics, Vol. 29, Issue 10
Native E2F/RBF Complexes Contain Myb-Interacting Proteins and Repress Transcription of Developmentally Controlled E2F Target Genes
journal, October 2004
- Korenjak, Michael; Taylor-Harding, Barbie; Binné, Ulrich K.
- Cell, Vol. 119, Issue 2
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
Web 3DNA--a web server for the analysis, reconstruction, and visualization of three-dimensional nucleic-acid structures
journal, May 2009
- Zheng, G.; Lu, X. -J.; Olson, W. K.
- Nucleic Acids Research, Vol. 37, Issue Web Server
Structural plasticity of histones H3–H4 facilitates their allosteric exchange between RbAp48 and ASF1
journal, November 2012
- Zhang, Wei; Tyl, Marek; Ward, Richard
- Nature Structural & Molecular Biology, Vol. 20, Issue 1
Disruption of pocket protein dream complexes by E7 proteins of different types of human papillomaviruses
journal, January 2013
- Rashid, N. Nor; Yusof, R.; Watson, R. J.
- Acta virologica, Vol. 57, Issue 04
A Novel Testis-Specific Metallothionein-like Protein,Tesmin,Is an Early Marker of Male Germ Cell Differentiation
journal, April 1999
- Sugihara, Takashi; Wadhwa, Renu; Kaul, Sunil C.
- Genomics, Vol. 57, Issue 1
NCBI GEO: archive for functional genomics data sets—update
journal, November 2012
- Barrett, Tanya; Wilhite, Stephen E.; Ledoux, Pierre
- Nucleic Acids Research, Vol. 41, Issue D1
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities
journal, May 2010
- Heinz, Sven; Benner, Christopher; Spann, Nathanael
- Molecular Cell, Vol. 38, Issue 4
Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex
journal, October 2006
- Harrison, M. M.; Ceol, C. J.; Lu, X.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 45
Structural basis of X chromosome DNA recognition by the MSL2 CXC domain during Drosophila dosage compensation
journal, December 2014
- Zheng, Sanduo; Villa, Raffaella; Wang, Jia
- Genes & Development, Vol. 28, Issue 23
Evolutionarily Conserved Multisubunit RBL2/p130 and E2F4 Protein Complex Represses Human Cell Cycle-Dependent Genes in Quiescence
journal, May 2007
- Litovchick, Larisa; Sadasivam, Subhashini; Florens, Laurence
- Molecular Cell, Vol. 26, Issue 4
Molecular basis for recognition of methylated and specific DNA sequences by the zinc finger protein Kaiso
journal, September 2012
- Buck-Koehntop, B. A.; Stanfield, R. L.; Ekiert, D. C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 38
CPP1, a DNA-binding protein involved in the expression of a soybean leghemoglobin c3 gene
journal, June 2000
- Cvitanich, C.; Pallisgaard, N.; Nielsen, K. A.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 14
LINC, a Human Complex That is Related to pRB-Containing Complexes in Invertebrates Regulates the Expression of G 2 /M Genes
journal, August 2007
- Schmit, Fabienne; Korenjak, Michael; Mannefeld, Mirijam
- Cell Cycle, Vol. 6, Issue 15
Structural and Energetic Basis of Carbohydrate–Aromatic Packing Interactions in Proteins
journal, June 2013
- Chen, Wentao; Enck, Sebastian; Price, Joshua L.
- Journal of the American Chemical Society, Vol. 135, Issue 26
The role of DNA shape in protein–DNA recognition
journal, October 2009
- Rohs, Remo; West, Sean M.; Sosinsky, Alona
- Nature, Vol. 461, Issue 7268
A Structural Basis for Recognition of A·T and T·A Base Pairs in the Minor Groove of B-DNA
journal, October 1998
- Kielkopf, C. L.
- Science, Vol. 282, Issue 5386
Structural basis of DNA recognition by the heterodimeric cell cycle transcription factor E2F-DP
journal, March 1999
- Zheng, N.; Fraenkel, E.; Pabo, C. O.
- Genes & Development, Vol. 13, Issue 6
Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex
journal, June 2007
- Pilkinton, M.; Sandoval, R.; Colamonici, O. R.
- Oncogene, Vol. 26, Issue 54
DNA base-stacking interactions: a comparison of theoretical calculations with oligonucleotide X-ray crystal structures
journal, January 1997
- Hunter, Christopher A.; Lu, Xiang-Jun
- Journal of Molecular Biology, Vol. 265, Issue 5
DNA base-stacking interactions: a comparison of theoretical calculations with oligonucleotide X-ray crystal structures
journal, January 1997
- Hunter, Christopher A.; Lu, Xiang-Jun
- Journal of Molecular Biology, Vol. 265, Issue 5
The central role of CDE/CHR promoter elements in the regulation of cell cycle-dependent gene transcription: CDE/CHR-dependent cell cycle-gene transcription
journal, December 2009
- Müller, Gerd A.; Engeland, Kurt
- FEBS Journal, Vol. 277, Issue 4
Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex
journal, December 2004
- Lewis, P. W.
- Genes & Development, Vol. 18, Issue 23
Solution Structure of MSL2 CXC Domain Reveals an Unusual Zn3Cys9 Cluster and Similarity to Pre-SET Domains of Histone Lysine Methyltransferases
journal, September 2012
- Zheng, Sanduo; Wang, Jia; Feng, Yingang
- PLoS ONE, Vol. 7, Issue 9
Conserved functions of the pRB and E2F families
journal, September 2008
- van den Heuvel, Sander; Dyson, Nicholas J.
- Nature Reviews Molecular Cell Biology, Vol. 9, Issue 9
The DREAM complex: master coordinator of cell cycle-dependent gene expression
journal, July 2013
- Sadasivam, Subhashini; DeCaprio, James A.
- Nature Reviews Cancer, Vol. 13, Issue 8
The CHR promoter element controls cell cycle-dependent gene transcription and binds the DREAM and MMB complexes
journal, November 2011
- Müller, Gerd A.; Quaas, Marianne; Schümann, Michael
- Nucleic Acids Research, Vol. 40, Issue 4
Disruption of repressive p130–DREAM complexes by human papillomavirus 16 E6/E7 oncoproteins is required for cell-cycle progression in cervical cancer cells
journal, November 2011
- Nor Rashid, Nurshamimi; Yusof, Rohana; Watson, Roger J.
- Journal of General Virology, Vol. 92, Issue 11
Structural mechanisms of DREAM complex assembly and regulation
journal, April 2015
- Guiley, Keelan Z.; Liban, Tyler J.; Felthousen, Jessica G.
- Genes & Development, Vol. 29, Issue 9
The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression
journal, March 2012
- Sadasivam, S.; Duan, S.; DeCaprio, J. A.
- Genes & Development, Vol. 26, Issue 5
C-h⋯π-interactions in proteins
journal, March 2001
- Brandl, Maria; Weiss, Manfred S.; Jabs, Andreas
- Journal of Molecular Biology, Vol. 307, Issue 1
The role of DNA shape in protein–DNA recognition
journal, October 2009
- Rohs, Remo; West, Sean M.; Sosinsky, Alona
- Nature, Vol. 461, Issue 7268
Loss of the Mammalian DREAM Complex Deregulates Chondrocyte Proliferation
journal, April 2014
- Forristal, C.; Henley, S. A.; MacDonald, J. I.
- Molecular and Cellular Biology, Vol. 34, Issue 12
DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly
journal, April 2011
- Litovchick, L.; Florens, L. A.; Swanson, S. K.
- Genes & Development, Vol. 25, Issue 8
Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex
journal, June 2007
- Pilkinton, M.; Sandoval, R.; Colamonici, O. R.
- Oncogene, Vol. 26, Issue 54
DNA–protein π-interactions in nature: abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar
journal, April 2014
- Wilson, Katie A.; Kellie, Jennifer L.; Wetmore, Stacey D.
- Nucleic Acids Research, Vol. 42, Issue 10
CPP1, a DNA-binding protein involved in the expression of a soybean leghemoglobin c3 gene
journal, June 2000
- Cvitanich, C.; Pallisgaard, N.; Nielsen, K. A.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 14
Molecular basis for recognition of methylated and specific DNA sequences by the zinc finger protein Kaiso
journal, September 2012
- Buck-Koehntop, B. A.; Stanfield, R. L.; Ekiert, D. C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 38
Evolutionarily Conserved Multisubunit RBL2/p130 and E2F4 Protein Complex Represses Human Cell Cycle-Dependent Genes in Quiescence
journal, May 2007
- Litovchick, Larisa; Sadasivam, Subhashini; Florens, Laurence
- Molecular Cell, Vol. 26, Issue 4
An integrated encyclopedia of DNA elements in the human genome
journal, September 2012
- ,
- Nature, Vol. 489, Issue 7414, p. 57-74
The integration of macromolecular diffraction data
journal, December 2005
- Leslie, Andrew G. W.
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1
ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases
journal, January 2014
- Shen, Li; Shao, Ningyi; Liu, Xiaochuan
- BMC Genomics, Vol. 15, Issue 1
Nucleosome Assembly by a Complex of CAF-1 and Acetylated Histones H3/H4
journal, October 1996
- Verreault, Alain; Kaufman, Paul D.; Kobayashi, Ryuji
- Cell, Vol. 87, Issue 1
Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex
journal, October 2006
- Harrison, M. M.; Ceol, C. J.; Lu, X.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 45
Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression
journal, April 2000
- Takahashi, Yasuhiko; Rayman, Joseph B.; Dynlacht, Brian David
- Genes & Development, Vol. 14, Issue 7
Works referencing / citing this record:
Structural mechanism of Myb–MuvB assembly
journal, September 2018
- Guiley, Keelan Z.; Iness, Audra N.; Saini, Siddharth
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 40
RB, p130 and p107 differentially repress G1/S and G2/M genes after p53 activation
journal, October 2019
- Schade, Amy E.; Fischer, Martin; DeCaprio, James A.
- Nucleic Acids Research, Vol. 47, Issue 21
Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas
journal, December 2019
- Takeuchi, Tomomi; Benning, Christoph
- Biotechnology for Biofuels, Vol. 12, Issue 1
Cyclin D–CDK4 relieves cooperative repression of proliferation and cell cycle gene expression by DREAM and RB
journal, March 2019
- Schade, Amy E.; Oser, Matthew G.; Nicholson, Hilary E.
- Oncogene, Vol. 38, Issue 25
Changes in chromatin accessibility ensure robust cell cycle exit in terminally differentiated cells
journal, September 2019
- Ma, Yiqin; McKay, Daniel J.; Buttitta, Laura
- PLOS Biology, Vol. 17, Issue 9
Cell cycle transcription control: DREAM/MuvB and RB-E2F complexes
journal, August 2017
- Fischer, Martin; Müller, Gerd A.
- Critical Reviews in Biochemistry and Molecular Biology, Vol. 52, Issue 6
Nitrogen-dependent coordination of cell cycle, quiescence and TAG accumulation in Chlamydomonas
journal, December 2019
- Takeuchi, Tomomi; Benning, Christoph
- Biotechnology for Biofuels, Vol. 12, Issue 1
Cross-regulation of viral kinases with cyclin A secures shutoff of host DNA synthesis
posted_content, November 2019
- Bogdanow, Boris; Schmidt, Max; Weisbach, Henry
Changes in chromatin accessibility ensure robust cell cycle exit in terminally differentiated cells
journal, September 2019
- Ma, Yiqin; McKay, Daniel J.; Buttitta, Laura
- PLOS Biology, Vol. 17, Issue 9
Cyclin D–CDK4 relieves cooperative repression of proliferation and cell cycle gene expression by DREAM and RB
journal, March 2019
- Schade, Amy E.; Oser, Matthew G.; Nicholson, Hilary E.
- Oncogene, Vol. 38, Issue 25
Zellzykluskontrolle β-herpesviraler Kinasen
text, January 2021
- Schmidt, Max
- Charité - Universitätsmedizin Berlin
DREAM and RB cooperate to induce gene repression and cell-cycle arrest in response to p53 activation
journal, August 2019
- Uxa, Sigrid; Bernhart, Stephan H.; Mages, Christina F. S.
- Nucleic Acids Research, Vol. 47, Issue 17
A DP-like transcription factor protein interacts with E2fl1 to regulate meiosis in Tetrahymena thermophila
journal, March 2018
- Zhang, Jing; Yan, Guanxiong; Tian, Miao
- Cell Cycle, Vol. 17, Issue 5
RB, p130 and p107 differentially repress G1/S and G2/M genes after p53 activation
journal, October 2019
- Schade, Amy E.; Fischer, Martin; DeCaprio, James A.
- Nucleic Acids Research, Vol. 47, Issue 21
Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM
journal, November 2017
- Engeland, Kurt
- Cell Death & Differentiation, Vol. 25, Issue 1
Human papilloma virus E7 oncoprotein abrogates the p53-p21-DREAM pathway
journal, June 2017
- Fischer, Martin; Uxa, Sigrid; Stanko, Clara
- Scientific Reports, Vol. 7, Issue 1
Loss of the Caenorhabditis elegans pocket protein LIN-35 reveals MuvB's innate function as the repressor of DREAM target genes
journal, November 2017
- Goetsch, Paul D.; Garrigues, Jacob M.; Strome, Susan
- PLOS Genetics, Vol. 13, Issue 11
Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM
journal, November 2017
- Engeland, Kurt
- Cell Death & Differentiation, Vol. 25, Issue 1
Cross-regulation of viral kinases with cyclin A secures shutoff of host DNA synthesis
text, January 2020
- Bogdanow, Boris; Schmidt, Max; Weisbach, Henry
- Charité - Universitätsmedizin Berlin
Combining crystallographic and quantum chemical data to understand DNA-protein π-interactions in nature
journal, April 2017
- Wilson, Katie A.; Wetmore, Stacey D.
- Structural Chemistry, Vol. 28, Issue 5