Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors

Ke, Jiyuan; Ma, Honglei; Gu, Xin; Thelen, Adam; Brunzelle, Joseph S.; Li, Jiayang; Xu, H. Eric; Melcher, Karsten

doi:10.1126/sciadv.1500107

Title: Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors

Journal Article · Fri Jul 03 00:00:00 EDT 2015 · Science Advances

DOI:https://doi.org/10.1126/sciadv.1500107· OSTI ID:1203740

Ke, Jiyuan ^[1]; Ma, Honglei ^[1]; Gu, Xin ^[2]; Thelen, Adam ^[2]; Brunzelle, Joseph S. ^[3]; Li, Jiayang ^[4]; Xu, H. Eric ^[1]; Melcher, Karsten ^[1]

Key Laboratory of Receptor Research, VARI-SIMM Center, Center for Structure and Function of Drug Targets, Shanghai Institute of Materia Medica, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201203, People’s Republic of China.;Laboratory of Structural Sciences and Laboratory of Structural Biology and Biochemistry, Van Andel Research Institute, 333 Bostwick Avenue Northeast, Grand Rapids, MI 49503, USA.
Laboratory of Structural Sciences and Laboratory of Structural Biology and Biochemistry, Van Andel Research Institute, 333 Bostwick Avenue Northeast, Grand Rapids, MI 49503, USA.
Department of Molecular Pharmacology and Biological Chemistry, Life Sciences Collaborative Access Team, Synchrotron Research Center, Northwestern University, Argonne, IL 60439, USA.
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, People’s Republic of China.

Groucho-related corepressors in plants bind a peptide motif found in numerous repressors through a novel peptide recognition fold.

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

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Health (NIH); National Science Foundation (NSF)

DOE Contract Number:: AC02-06CH11357; 2012ZX09301001; 2012CB910403; 2013CB910600; XDB08020303; 2013ZX09507001; NSF 9121731; NIH DK071662; GM102545; GM104212; 085P1000817

OSTI ID:: 1203740

Journal Information:: Science Advances, Vol. 1, Issue 6; ISSN 2375-2548

Publisher:: AAAS

Country of Publication:: United States

Language:: ENGLISH

References (59)

Why so repressed? Turning off transcription during plant growth and development Krogan, Naden T.; Long, Jeff A. Current Opinion in Plant Biology, Vol. 12, Issue 5 https://doi.org/10.1016/j.pbi.2009.07.011	journal	October 2009
The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis Causier, Barry; Ashworth, Mary; Guo, Wenjia Plant Physiology, Vol. 158, Issue 1 https://doi.org/10.1104/pp.111.186999	journal	November 2011
The ‘Marx’ of Groucho on development and disease Buscarlet, Manuel; Stifani, Stefano Trends in Cell Biology, Vol. 17, Issue 7 https://doi.org/10.1016/j.tcb.2007.07.002	journal	July 2007
Groucho/Tup1 family co-repressors in plant development Liu, Zhongchi; Karmarkar, Vidyadhar Trends in Plant Science, Vol. 13, Issue 3 https://doi.org/10.1016/j.tplants.2007.12.005	journal	March 2008
Genome-Wide Analysis of Ethylene-Responsive Element Binding Factor-Associated Amphiphilic Repression Motif-Containing Transcriptional Regulators in Arabidopsis Kagale, Sateesh; Links, Matthew G.; Rozwadowski, Kevin Plant Physiology, Vol. 152, Issue 3 https://doi.org/10.1104/pp.109.151704	journal	January 2010
EAR motif-mediated transcriptional repression in plants: An underlying mechanism for epigenetic regulation of gene expression Kagale, Sateesh; Rozwadowski, Kevin Epigenetics, Vol. 6, Issue 2 https://doi.org/10.4161/epi.6.2.13627	journal	February 2011
Aux/IAA Proteins Contain a Potent Transcriptional Repression Domain Tiwari, Shiv B.; Hagen, Gretchen; Guilfoyle, Tom J. The Plant Cell, Vol. 16, Issue 2 https://doi.org/10.1105/tpc.017384	journal	January 2004
JAZ8 Lacks a Canonical Degron and Has an EAR Motif That Mediates Transcriptional Repression of Jasmonate Responses in Arabidopsis Shyu, Christine; Figueroa, Pablo; DePew, Cody L. The Plant Cell, Vol. 24, Issue 2 https://doi.org/10.1105/tpc.111.093005	journal	February 2012
NINJA connects the co-repressor TOPLESS to jasmonate signalling Pauwels, Laurens; Barbero, Gemma Fernández; Geerinck, Jan Nature, Vol. 464, Issue 7289 https://doi.org/10.1038/nature08854	journal	April 2010
TOPLESS mediates brassinosteroid-induced transcriptional repression through interaction with BZR1 Oh, Eunkyoo; Zhu, Jia-Ying; Ryu, Hojin Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5140	journal	June 2014
D14–SCFD3-dependent degradation of D53 regulates strigolactone signalling Zhou, Feng; Lin, Qibing; Zhu, Lihong Nature, Vol. 504, Issue 7480 https://doi.org/10.1038/nature12878	journal	December 2013
DWARF 53 acts as a repressor of strigolactone signalling in rice Jiang, Liang; Liu, Xue; Xiong, Guosheng Nature, Vol. 504, Issue 7480 https://doi.org/10.1038/nature12870	journal	December 2013
DELLAs Function as Coactivators of GAI-ASSOCIATED FACTOR1 in Regulation of Gibberellin Homeostasis and Signaling in Arabidopsis Fukazawa, Jutarou; Teramura, Hiroshi; Murakoshi, Satoru The Plant Cell, Vol. 26, Issue 7 https://doi.org/10.1105/tpc.114.125690	journal	July 2014
Evidence for Network Evolution in an Arabidopsis Interactome Map Dreze, M.; Carvunis, A. -R.; Charloteaux, B. Science, Vol. 333, Issue 6042 https://doi.org/10.1126/science.1203877	journal	July 2011
Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis Hiratsu, Keiichiro; Mitsuda, Nobutaka; Matsui, Kyoko Biochemical and Biophysical Research Communications, Vol. 321, Issue 1 https://doi.org/10.1016/j.bbrc.2004.06.115	journal	August 2004
TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis Szemenyei, H.; Hannon, M.; Long, J. A. Science, Vol. 319, Issue 5868 https://doi.org/10.1126/science.1151461	journal	March 2008
From perception to attenuation: auxin signalling and responses Peer, Wendy Ann Current Opinion in Plant Biology, Vol. 16, Issue 5 https://doi.org/10.1016/j.pbi.2013.08.003	journal	October 2013
Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway Wang, Renhou; Estelle, Mark Current Opinion in Plant Biology, Vol. 21 https://doi.org/10.1016/j.pbi.2014.06.006	journal	October 2014
The JAZ family of repressors is the missing link in jasmonate signalling Chini, A.; Fonseca, S.; Fernández, G. Nature, Vol. 448, Issue 7154 https://doi.org/10.1038/nature06006	journal	July 2007
JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling Thines, Bryan; Katsir, Leron; Melotto, Maeli Nature, Vol. 448, Issue 7154 https://doi.org/10.1038/nature05960	journal	July 2007
ABERRANT SPIKELET AND PANICLE1, encoding a TOPLESS-related transcriptional co-repressor, is involved in the regulation of meristem fate in rice Yoshida, Akiko; Ohmori, Yoshihiro; Kitano, Hidemi The Plant Journal, Vol. 70, Issue 2 https://doi.org/10.1111/j.1365-313X.2011.04872.x	journal	January 2012
A new sequence motif linking lissencephaly, Treacher Collins and oral-facial-digital type 1 syndromes, microtubule dynamics and cell migration Emes, R. D. Human Molecular Genetics, Vol. 10, Issue 24 https://doi.org/10.1093/hmg/10.24.2813	journal	November 2001
TOPLESS Regulates Apical Embryonic Fate in Arabidopsis Long, J. A. Science, Vol. 312, Issue 5779 https://doi.org/10.1126/science.1123841	journal	June 2006
The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins Chini, Andrea; Fonseca, Sandra; Chico, Jose M. The Plant Journal, Vol. 59, Issue 1 https://doi.org/10.1111/j.1365-313X.2009.03852.x	journal	July 2009
A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis Chung, Hoo Sun; Howe, Gregg A. The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.064097	journal	January 2009
Protein-protein interactions among the Aux/IAA proteins Kim, J.; Harter, K.; Theologis, A. Proceedings of the National Academy of Sciences, Vol. 94, Issue 22 https://doi.org/10.1073/pnas.94.22.11786	journal	October 1997
Protonation-mediated structural flexibility in the F conjugation regulatory protein, TraM Lu, Jun; Edwards, Ross A.; Wong, Joyce J. W. The EMBO Journal, Vol. 25, Issue 12 https://doi.org/10.1038/sj.emboj.7601151	journal	May 2006
All Tcf HMG box transcription factors interact with Groucho-related co-repressors Brantjes, H. Nucleic Acids Research, Vol. 29, Issue 7 https://doi.org/10.1093/nar/29.7.1410	journal	April 2001
The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors Roose, Jeroen; Molenaar, Miranda; Peterson, Josi Nature, Vol. 395, Issue 6702 https://doi.org/10.1038/26989	journal	October 1998
A Myc Groucho complex integrates EGF and Notch signaling to regulate neural development Orian, A.; Delrow, J. J.; Rosales Nieves, A. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 40 https://doi.org/10.1073/pnas.0707418104	journal	September 2007
Repression by Groucho/TLE/Grg Proteins: Genomic Site Recruitment Generates Compacted Chromatin In Vitro and Impairs Activator Binding In Vivo Sekiya, Takashi; Zaret, Kenneth S. Molecular Cell, Vol. 28, Issue 2 https://doi.org/10.1016/j.molcel.2007.10.002	journal	October 2007
Huckebein repressor activity in Drosophila terminal patterning is mediated by Groucho Goldstein, R. E.; Jimenez, G.; Cook, O. Development, Vol. 126, Issue 17 https://doi.org/10.1242/dev.126.17.3747	journal	September 1999
Groucho acts as a corepressor for a subset of negative regulators, including Hairy and Engrailed Jimenez, G.; Paroush, Z. 'e.; Ish-Horowicz, D. Genes & Development, Vol. 11, Issue 22 https://doi.org/10.1101/gad.11.22.3072	journal	November 1997
Groucho-Mediated Transcriptional Repression Establishes Progenitor Cell Pattern and Neuronal Fate in the Ventral Neural Tube Muhr, Jonas; Andersson, Elisabet; Persson, Madelen Cell, Vol. 104, Issue 6 https://doi.org/10.1016/S0092-8674(01)00283-5	journal	March 2001
Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins Paroush, Z. Cell, Vol. 79, Issue 5 https://doi.org/10.1016/0092-8674(94)90070-1	journal	December 1994
Brinker is a sequence-specific transcriptional repressor in the Drosophila embryo Zhang, H. Genes & Development, Vol. 15, Issue 3 https://doi.org/10.1101/gad.861201	journal	February 2001
Functional dissection of the yeast Cyc8–Tupl transcriptional co-repressor complex Tzamarias, Dimitris; Struhl, Kevin Nature, Vol. 369, Issue 6483 https://doi.org/10.1038/369758a0	journal	June 1994
The WD repeats of Tup1 interact with the homeo domain protein alpha 2. Komachi, K.; Redd, M. J.; Johnson, A. D. Genes & Development, Vol. 8, Issue 23 https://doi.org/10.1101/gad.8.23.2857	journal	December 1994
Molecular functions of the TLE tetramerization domain in Wnt target gene repression Chodaparambil, J. V.; Pate, K. T.; Hepler, M. R. D. The EMBO Journal, Vol. 33, Issue 7 https://doi.org/10.1002/embj.201387188	journal	March 2014
Crystal Structure of the N-terminal Domain of the Yeast General Corepressor Tup1p and Its Functional Implications Matsumura, Hiroyoshi; Kusaka, Nanoha; Nakamura, Taichi Journal of Biological Chemistry, Vol. 287, Issue 32 https://doi.org/10.1074/jbc.M112.369652	journal	June 2012
Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor Zhu, Z.; Xu, F.; Zhang, Y. Proceedings of the National Academy of Sciences, Vol. 107, Issue 31 https://doi.org/10.1073/pnas.1002828107	journal	July 2010
APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19 Krogan, N. T.; Hogan, K.; Long, J. A. Development, Vol. 139, Issue 22 https://doi.org/10.1242/dev.085407	journal	October 2012
PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis Ogas, J.; Kaufmann, S.; Henderson, J. Proceedings of the National Academy of Sciences, Vol. 96, Issue 24 https://doi.org/10.1073/pnas.96.24.13839	journal	November 1999
The CHD3 Remodeler PICKLE Promotes Trimethylation of Histone H3 Lysine 27 Zhang, Heng; Rider, Stanley Dean; Henderson, James T. Journal of Biological Chemistry, Vol. 283, Issue 33 https://doi.org/10.1074/jbc.M802129200	journal	June 2008
The Groucho/TLE/Grg family of transcriptional co-repressors Jennings, Barbara H.; Ish-Horowicz, David Genome Biology, Vol. 9, Issue 1 https://doi.org/10.1186/gb-2008-9-1-205	journal	January 2008
The Transcription Corepressor LEUNIG Interacts with the Histone Deacetylase HDA19 and Mediator Components MED14 (SWP) and CDK8 (HEN3) To Repress Transcription Gonzalez, Deyarina; Bowen, Adam J.; Carroll, Thomas S. Molecular and Cellular Biology, Vol. 27, Issue 15 https://doi.org/10.1128/MCB.01912-06	journal	August 2007
Structural basis for the auxin-induced transcriptional regulation by Aux/IAA17 Han, Mookyoung; Park, Yangshin; Kim, Iktae Proceedings of the National Academy of Sciences, Vol. 111, Issue 52 https://doi.org/10.1073/pnas.1419525112	journal	December 2014
Structural basis for oligomerization of auxin transcriptional regulators Nanao, Max H.; Vinos-Poyo, Thomas; Brunoud, Géraldine Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4617	journal	April 2014
Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression Korasick, D. A.; Westfall, C. S.; Lee, S. G. Proceedings of the National Academy of Sciences, Vol. 111, Issue 14 https://doi.org/10.1073/pnas.1400074111	journal	March 2014
Groucho Oligomerization Is Required for Repression In Vivo Song, Haiyun; Hasson, Peleg; Paroush, Ze’ev Molecular and Cellular Biology, Vol. 24, Issue 10 https://doi.org/10.1128/MCB.24.10.4341-4350.2004	journal	May 2004
A plasmid expression system for quantitative in vivo biotinylation of thioredoxin fusion proteins in Escherichia coli Smith, P. A.; Tripp, B. C.; DiBlasio-Smith, E. A. Nucleic Acids Research, Vol. 26, Issue 6 https://doi.org/10.1093/nar/26.6.1414	journal	March 1998
Structure and function of Norrin in assembly and activation of a Frizzled 4-Lrp5/6 complex Ke, J.; Harikumar, K. G.; Erice, C. Genes & Development, Vol. 27, Issue 21 https://doi.org/10.1101/gad.228544.113	journal	November 2013
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
The CCP4 suite programs for protein crystallography Acta Crystallographica Section D Biological Crystallography, Vol. 50, Issue 5, p. 760-763 https://doi.org/10.1107/S0907444994003112	journal	September 1994
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909012098	journal	May 2009
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
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
A gate–latch–lock mechanism for hormone signalling by abscisic acid receptors Melcher, Karsten; Ng, Ley-Moy; Zhou, X. Edward Nature, Vol. 462, Issue 7273 https://doi.org/10.1038/nature08613	journal	November 2009

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