PRISMA: Protein Interaction Screen on Peptide Matrix Reveals Interaction Footprints and Modifications- Dependent Interactome of Intrinsically Disordered C/EBPβ
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Abstract
CCAAT enhancer-binding protein beta (C/EBPβ) is a pioneer transcription factor that specifies cell differentiation. C/EBPβ is intrinsically unstructured, a molecular feature common to many proteins involved in signal processing and epigenetics. The structure of C/EBPβ differs depending on alternative translation initiation and multiple post-translational modifications (PTM). Mutation of distinct PTM sites in C/EBPβ alters protein interactions and cell differentiation, suggesting that a C/EBPβ PTM indexing code determines epigenetic outcomes. Herein, we systematically explored the interactome of C/EBPβ using an array technique based on spot-synthesized C/EBPβ-derived linear tiling peptides with and without PTM, combined with mass spectrometric proteomic analysis of protein interactions. We identified interaction footprints of ∼1,300 proteins in nuclear extracts, many with chromatin modifying, chromatin remodeling, and RNA processing functions. The results suggest that C/EBPβ acts as a multi-tasking molecular switchboard, integrating signal-dependent modifications and structural plasticity to orchestrate interactions with numerous protein complexes directing cell fate and function.
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Cites
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855 · see citing works
ggplot2: Elegant Graphics for Data Analysis
Wickham, H. (2009) · doi:10.1007/978-0-387-98141-3 · Cited by 14,447 · see citing works
STRING v10: protein–protein interaction networks, integrated over the tree of life
Szklarczyk, D., Franceschini, A., Wyder, S., Forslund, K., Heller, D., Huerta-Cepas, J., Simonovic, M., Roth, A., Santos, A., Tsafou, K. P., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1003 · Cited by 10,436 · see citing works
The Perseus computational platform for comprehensive analysis of (prote)omics data
Tyanova, S., Temu, T., Sinitcyn, P. G., Carlson, A., Hein, M. Y., Geiger, T., Mann, M., & Cox, J. (2016) · Nature Methods · doi:10.1038/nmeth.3901 · Cited by 7,977 · see citing works
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · see citing works
Self-citationThe Pfam protein families database: towards a more sustainable future
Finn, R. D., Coggill, P., Eberhardt, R. Y., Eddy, S. R., Mistry, J., Mitchell, A. L., Potter, S. C., Punta, M., Qureshi, M., Sangrador-Vegas, A., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1344 · Cited by 5,975 · see citing works
Andromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., & Mann, M. (2011) · Journal of Proteome Research · doi:10.1021/pr101065j · Cited by 5,349 · see citing works
Rappsilber, J., Mann, M., & Ishihama, Y. (2007) · Nature Protocols · doi:10.1038/nprot.2007.261 · Cited by 4,641 · see citing works
Gene Ontology Consortium: going forward
The Gene Ontology Consortium (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1179 · Cited by 3,492 · see citing works
Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm
Wright, P. E., & Dyson, H. J. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.3110 · Cited by 2,968 · see citing works
Intrinsically disordered proteins in cellular signalling and regulation
Wright, P. E., & Dyson, H. J. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3920 · Cited by 2,371 · see citing works
Classification of Intrinsically Disordered Regions and Proteins
van der Lee, R., Buljan, M., Lang, B., Weatheritt, R. J., Daughdrill, G. W., Dunker, A. K., Fuxreiter, M., Gough, J., Gsponer, J., Jones, D. T., et al. (2014) · Chemical Reviews · doi:10.1021/cr400525m · Cited by 2,155 · see citing works
Four faces of cellular senescence
Rodier, F., & Campisi, J. (2011) · Journal of Cell Biology · doi:10.1083/jcb.201009094 · Cited by 2,016 · see citing works
Gregoretti, I., Lee, Y.-M., & Goodson, H. V. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.02.006 · Cited by 1,456 · see citing works
InterPro in 2017—beyond protein family and domain annotations
Finn, R. D., Attwood, T. K., Babbitt, P. C., Bateman, A. G., Peer Bork, B., Bridge, A. J., Chang, H.-Y., Dosztányi, Z., El-Gebali, S., Fraser, M., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1107 · Cited by 1,455 · see citing works
CORUM: the comprehensive resource of mammalian protein complexes—2009
Ruepp, A., Wägele, B., Lechner, M., Brauner, B., Dunger-Kaltenbach, I., Fobo, G., Frishman, G., Montrone, C., & Mewes, H. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp914 · Cited by 1,320 · see citing works
MLL translocations, histone modifications and leukaemia stem-cell development
Krivtsov, A., & Armstrong, S. (2007) · Nature Reviews. Cancer · doi:10.1038/nrc2253 · Cited by 1,294 · see citing works
g:Profiler—a web server for functional interpretation of gene lists (2016 update)
Reimand, J., Arak, T., Adler, P., Kolberg, L., Reisberg, S., Peterson, H., & Vilo, J. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw199 · Cited by 1,229 · see citing works
Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark
Ruthenburg, A. J., Allis, C. D., & Wysocka, J. (2007) · Molecular Cell · doi:10.1016/j.molcel.2006.12.014 · Cited by 1,147 · see citing works
Controlling the elongation phase of transcription with P-TEFb
Peterlin, B. M., & Price, D. H. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.06.014 · Cited by 1,144 · see citing works
Shilatifard, A. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-051710-134100 · Cited by 1,091 · see citing works
Stepwise reprogramming of B cells into macrophages.
Xie, H.-F., Ye, M., Feng, R., & Graf, T. (2004) · Cell · doi:10.1016/s0092-8674(04)00419-2 · Cited by 1,030 · see citing works
Analysis of Molecular Recognition Features (MoRFs)
Mohan, A., Oldfield, C. J., Predrag Radivojac, A., Vacic, V., Cortese, M. S., Dunker, A. K., & Uversky, V. N. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.07.087 · Cited by 746 · see citing works
Initiation of myoblast to brown fat switch by a PRDM16–C/EBP-β transcriptional complex
Kajimura, S., Seale, P., Kubota, K., Lunsford, E., Frangioni, J. V., Gygi, S. P., & Spiegelman, B. M. (2009) · Nature · doi:10.1038/nature08262 · Cited by 703 · see citing works
FACT, a Factor that Facilitates Transcript Elongation through Nucleosomes
Orphanides, G., LeRoy, G., Chang, C.-H., Luse, D. S., & Reinberg, D. (1998) · Cell · doi:10.1016/s0092-8674(00)80903-4 · Cited by 657 · see citing works
Prediction of Protein Binding Regions in Disordered Proteins
Mészáros, B., Simon, I., & Dosztányi, Z. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000376 · Cited by 621 · see citing works
Histone chaperone networks shaping chromatin function
Hammond, C. M., Strømme, C. B., Huang, H., Patel, D. J., & Groth, A. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.159 · Cited by 528 · see citing works
A Million Peptide Motifs for the Molecular Biologist
Tompa, P., Davey, N. E., Gibson, T. J., & Babu, M. M. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.032 · Cited by 515 · see citing works
How cells get the message: dynamic assembly and function of mRNA–protein complexes
Müller-McNicoll, M., & Neugebauer, K. M. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3434 · Cited by 397 · see citing works
An essential role for C/EBPβ in female reproductionPreprint
Sterneck, E., Tessarollo, L., & Johnson, P. F. (1997) · Genes & Development · doi:10.1101/gad.11.17.2153 · Cited by 389 · see citing works
Protein disorder and the evolution of molecular recognition: theory, predictions and observations.
Dunker, A. K., Garner, E. C., Guilliot, S., Romero, P. R., Albrecht, K., Hart, J., Zoran Obradovic, A., Kissinger, C. R., & Villafranca, J. E. (1998) · PubMed · Cited by 378 · see citing works
The super elongation complex (SEC) family in transcriptional control
Luo, Z., Lin, C., & Shilatifard, A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3417 · Cited by 374 · see citing works
bioDBnet: the biological database network
Mudunuri, U. S., Che, A., Yi, M., & Stephens, R. M. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btn654 · Cited by 366 · see citing works
Disfani, F. M., Hsu, W.-L., Mizianty, M. J., Oldfield, C. J., Xue, B., Dunker, A. K., Uversky, V. N., & Kurgan, L. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts209 · Cited by 366 · see citing works
The super elongation complex (SEC) and MLL in development and diseasePreprint
Smith, E. R., Lin, C., & Shilatifard, A. (2011) · Genes & Development · doi:10.1101/gad.2015411 · Cited by 362 · see citing works
Siersbæk, R., Nielsen, R., John, S., Sung, M., Baek, S., Loft, A., Hager, G. L., & Mandrup, S. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.65 · Cited by 350 · see citing works
MBD2/NuRD and MBD3/NuRD, Two Distinct Complexes with Different Biochemical and Functional Properties
Le Guezennec, X., Vermeulen, M., Brinkman, A. B., Hoeijmakers, W. A. M., Cohen, A., Lasonder, E., & Stunnenberg, H. G. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.3.843-851.2006 · Cited by 340 · see citing works
Elongin (SIII): A Multisubunit Regulator of Elongation by RNA Polymerase II
Aso, T., Lane, W. S., Conaway, J. W., & Conaway, R. C. (1995) · Science · doi:10.1126/science.7660129 · Cited by 327 · see citing works
The molecular biology of mixed lineage leukemia
Slany, R. K. (2009) · Haematologica · doi:10.3324/haematol.2008.002436 · Cited by 321 · see citing works
Tsukada, J., Yoshida, Y., Kominato, Y., & Auron, P. E. (2011) · Cytokine · doi:10.1016/j.cyto.2010.12.019 · Cited by 316 · see citing works
A C/EBPβ Isoform Recruits the SWI/SNF Complex to Activate Myeloid Genes
Kowenz‐Leutz, E., & Leutz, A. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80384-6 · Cited by 301 · see citing works
Self-citationMyb and NF-M: combinatorial activators of myeloid genes in heterologous cell types.Preprint
Ness, S. A., Kowenz‐Leutz, E., Casini, T., Graf, T., & Leutz, A. (1993) · Genes & Development · doi:10.1101/gad.7.5.749 · Cited by 262 · see citing works
Self-citationSmits, A. H., Jansen, P. W. T. C., Poser, I., Hyman, A. A., & Vermeulen, M. (2013) · Nucleic Acids Research · doi:10.1093/nar/gks941 · Cited by 258 · see citing works
Transcription Factor Cooperativity in Early Adipogenic Hotspots and Super-Enhancers
Siersbæk, R., Rabiee, A., Nielsen, R., Sidoli, S., Traynor, S., Loft, A., Poulsen, L. L. C., Rogowska-Wrzesinska, A., Jensen, O. N., & Mandrup, S. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.042 · Cited by 234 · see citing works
Novel mechanism of C/EBP beta (NF-M) transcriptional control: activation through derepression.Preprint
Kowenz‐Leutz, E., Twamley, G. M., Ansieau, S., & Leutz, A. (1994) · Genes & Development · doi:10.1101/gad.8.22.2781 · Cited by 233 · see citing works
Self-citationControl of mammalian gene expression by selective mRNA export
Wickramasinghe, V. O., & Laskey, R. A. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm4010 · Cited by 230 · see citing works
Williams, S. C., Baer, M., Dillner, A., & Johnson, P. F. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07319.x · Cited by 222 · see citing works
He, N., Chan, C. K., Sobhian, B., Chou, S., Xue, Y., Liu, M., Alber, T., Benkirane, M., & Zhou, Q. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107107108 · Cited by 194 · see citing works
Upstream open reading frames: Molecular switches in (patho)physiology
Wethmar, K., Smink, J. J., & Leutz, A. (2010) · Bioessays · doi:10.1002/bies.201000037 · Cited by 192 · see citing works
Self-citationThe Mediator Complex: At the Nexus of RNA Polymerase II Transcription
Jerónimo, C., & Robert, F. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.07.001 · Cited by 189 · see citing works
RUNX1 reshapes the epigenetic landscape at the onset of haematopoiesis
Lichtinger, M., Ingram, R., Hannah, R., Müller, D., Clarke, D., Assi, S. A., Lie‐A‐Ling, M., Noailles, L., Vijayabaskar, M. S., Wu, M., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.275 · Cited by 180 · see citing works
Synthesis and Screening of Peptide Libraries on Continuous Cellulose Membrane Supports
Kramer, A., & Schneider‐Mergener, J. (2003) · Humana Press eBooks · doi:10.1385/0-89603-392-9:25 · Cited by 179 · see citing works
Ras Induces Mediator Complex Exchange on C/EBPβ
Mo, X., Kowenz‐Leutz, E., Xu, H., & Leutz, A. (2004) · Molecular Cell · doi:10.1016/s1097-2765(03)00521-5 · Cited by 169 · see citing works
Self-citationVillanueva, C. J., Vergnes, L., Wang, J., Drew, B. G., Hong, C., Tu, Y., Hu, Y., Xu, P., Xu, F., Sáez, E., et al. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.01.016 · Cited by 147 · see citing works
C/EBPβ cooperates with RB:E2F to implement RasV12‐induced cellular senescence
Sebastian, T. B., Malı́k, R., Thomas, S., Sage, J., & Johnson, P. F. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600789 · Cited by 147 · see citing works
Kovács, K. A., Steinmann, M., Magistretti, P. J., Halfon, O., & Cardinaux, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303147200 · Cited by 137 · see citing works
The Mediator complex and transcription elongation
Conaway, R. C., & Conaway, J. W. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.08.017 · Cited by 135 · see citing works
Mutations in Disordered Regions Can Cause Disease by Creating Dileucine Motifs
Meyer, K., Kirchner, M., Uyar, B., Cheng, J.-Y., Russo, G., Hernandez-Miranda, L. R., Szymborska, A., Zauber, H., Rudolph, I.-M., Willnow, T. E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.019 · Cited by 132 · see citing works
Self-citationJundt, F., Raetzel, N., Müller, C., Calkhoven, C. F., Kley, K., Mathas, S., Lietz, A., Leutz, A., & Dörken, B. (2005) · Blood · doi:10.1182/blood-2004-11-4513 · Cited by 131 · see citing works
Self-citationRecruitment of p300 by C/EBPβ triggers phosphorylation of p300 and modulates coactivator activity
Schwartz, C., Schachtrup, K., Mink, S., Schmolke, M., Budde, B., Wenning, D., & Klempnauer, K.-H. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg076 · Cited by 122 · see citing works
G9a-mediated Lysine Methylation Alters the Function of CCAAT/Enhancer-binding Protein-β
Pleß, O., Kowenz‐Leutz, E., Knoblich, M., Lausen, J., Beyermann, M., Walsh, M. J., & Leutz, A. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m802132200 · Cited by 107 · see citing works
Self-citationRegulatory evolution through divergence of a phosphoswitch in the transcription factor CEBPB
Lynch, V. J., May, G. E., & Wagner, G. P. (2011) · Nature · doi:10.1038/nature10595 · Cited by 103 · see citing works
Kowenz‐Leutz, E., Pleß, O., Dittmar, G. A. G., Knoblich, M., & Leutz, A. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.3 · Cited by 103 · see citing works
Self-citationStefano, B. D., Collombet, S., Jakobsen, J. S., Wierer, M., Sardina, J. L., Lackner, A., Stadhouders, R., Segura-Morales, C., Francesconi, M., Limone, F., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3326 · Cited by 103 · see citing works
C/EBPs: recipients of extracellular signals through proteome modulation
Nerlov, C. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.02.002 · Cited by 98 · see citing works
Müller, C., Kowenz‐Leutz, E., Grieser‐Ade, S., Graf, T., & Leutz, A. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00303.x · Cited by 91 · see citing works
Self-citationEaton, E. M., & Sealy, L. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305680200 · Cited by 84 · see citing works
SAGA function in tissue-specific gene expression
Weake, V. M., & Workman, J. L. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.11.005 · Cited by 79 · see citing works
Lee, S., Shuman, J. D., Guszczynski, T., Sakchaisri, K., Sebastian, T. B., Copeland, T. D., Miller, M., Cohen, M. S., Taunton, J., Smart, R. C., et al. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00782-09 · Cited by 77 · see citing works
Anastasov, N., Bonzheim, I., Rudelius, M., Klier, M., Dau, T., Angermeier, D., Duyster, J., Pittaluga, S., Fend, F., Raffeld, M. A., et al. (2009) · Haematologica · doi:10.3324/haematol.2009.014050 · Cited by 61 · see citing works
The Groucho/Transducin‐like enhancer of split protein family in animal development
Agarwal, M., Kumar, P., & Mathew, S. J. (2015) · IUBMB Life · doi:10.1002/iub.1395 · Cited by 55 · see citing works
Estimating and improving protein interaction error rates
D’haeseleer, P., & Church, G. M. (2004) · Proceedings. 2004 IEEE Computational Systems Bioinformatics Conference, 2004. CSB 2004. · doi:10.1109/csb.2004.1332435 · Cited by 44 · see citing works
Lee, S., Miller, M., Shuman, J. D., & Johnson, P. F. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.128413 · Cited by 37 · see citing works
Crosstalk between phosphorylation and multi-site arginine/lysine methylation in C/EBPs
Leutz, A., Pleß, O., Lappé, M., Dittmar, G. A. G., & Kowenz‐Leutz, E. (2011) · Transcription · doi:10.4161/trns.2.1.13510 · Cited by 32 · see citing works
Self-citationHondele, M., & Ladurner, A. G. (2013) · Nucleus · doi:10.4161/nucl.27235 · Cited by 31 · see citing works
Stoilova, B., Kowenz‐Leutz, E., Scheller, M., & Leutz, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065169 · Cited by 25 · see citing works
Self-citationSteinberg, X. P., Hepp, M. I., Fernández-García, Y., Suganuma, T., Swanson, S. K., Washburn, M. P., Workman, J. L., & Gutiérrez, J. L. (2012) · Biochemistry · doi:10.1021/bi201593q · Cited by 24 · see citing works
Kanashova, T., Popp, O., Orasche, J., Karg, E. W., Harndorf, H., Stengel, B., Sklorz, M., Streibel, T., Zimmermann, R., & Dittmar, G. A. G. (2015) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-015-8595-4 · Cited by 22 · see citing works
Self-citationTime, space, and disorder in the expanding proteome universe
Minde, D., Dunker, A. K., & Lilley, K. S. (2017) · PROTEOMICS · doi:10.1002/pmic.201600399 · Cited by 21 · see citing works
Bhaumik, P., Davis, J. S., Tropea, J. E., Cherry, S., Johnson, P. F., & Miller, M. (2014) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s1399004714009262 · Cited by 20 · see citing works
Pleß, O., Kowenz‐Leutz, E., Dittmar, G. A. G., & Leutz, A. (2011) · Nature Protocols · doi:10.1038/nprot.2011.303 · Cited by 14 · see citing works
Self-citationThe Expanding Mi-2/NuRD Complexes: A Schematic Glance
Zhang, Y., & Li, Y. (2010) · Proteomics Insights · doi:10.4137/pri.s6329 · Cited by 14 · see citing works
Miller, M. (2006) · Cell Cycle · doi:10.4161/cc.5.21.3421 · Cited by 9 · see citing works
Flagged first, then by citations
1 of the 84 references couldn’t be matched to a known paper.
Cited by
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Sandmann, C.-L., Schulz, J. F., Ruiz‐Orera, J., Kirchner, M., Ziehm, M., Adami, E., Marczenke, M., Christ, A., Liebe, N., Greiner, J., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.01.023 · Cited by 164 · see citing works
Self-citationMutations in Disordered Regions Can Cause Disease by Creating Dileucine Motifs
Meyer, K., Kirchner, M., Uyar, B., Cheng, J.-Y., Russo, G., Hernandez-Miranda, L. R., Szymborska, A., Zauber, H., Rudolph, I.-M., Willnow, T. E., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.019 · Cited by 132 · see citing works
Self-citationInteraction modules that impart specificity to disordered protein
Čermáková, K., & Hodges, H. C. (2023) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2023.01.004 · Cited by 92 · see citing works
Martin, E. R., Girardello, R., Dittmar, G., & Ludwig, A. (2021) · FEBS Journal · doi:10.1111/febs.15710 · Cited by 60 · see citing works
Self-citationDavey, N. E., Simonetti, L., & Ivarsson, Y. (2023) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2023.102593 · Cited by 53 · see citing works
Pathogenic mutations of human phosphorylation sites affect protein–protein interactions
Rrustemi, T., Meyer, K., Roske, Y., Uyar, B., Akalin, A., Imami, K., Ishihama, Y., Daumke, O., & Selbach, M. (2024) · Nature Communications · doi:10.1038/s41467-024-46794-8 · Cited by 32 · see citing works
Peptide-based Interaction Proteomics
Meyer, K., & Selbach, M. (2020) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r120.002034 · Cited by 31 · see citing works
The transcription factor code: a beacon for histone methyltransferase docking
Garcia, G. T., & Graf, T. (2021) · Trends in Cell Biology · doi:10.1016/j.tcb.2021.04.001 · Cited by 26 · see citing works
Tamura, I., Fujimura, T., Doi‐Tanaka, Y., Takagi, H., Shirafuta, Y., Kajimura, T., Mihara, Y., Maekawa, R., Taketani, T., Sato, S., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101150 · Cited by 26 · see citing works
Ramberger, E., Sapozhnikova, V., Kowenz‐Leutz, E., Zimmermann, K., Nicot, N., Nazarov, P. V., Pérez-Hernández, D., Reimer, U., Mertins, P., Dittmar, G., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102686 · Cited by 24 · see citing works
Self-citationC/EBPß Isoform Specific Gene Regulation: It’s a Lot more Complicated than you Think!
Spike, A. J., & Rosen, J. M. (2020) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-020-09444-5 · Cited by 23 · see citing works
Jankowski, M. S., Griffith, D., Shastry, D. G., Pelham, J. F., Ginell, G. M., Thomas, J., Karande, P., Holehouse, A. S., & Hurley, J. M. (2024) · Nature Communications · doi:10.1038/s41467-024-47761-z · Cited by 23 · see citing works
Pan-claudin family interactome analysis reveals shared and specific interactions
Suarez-Artiles, L., Breiderhoff, T., Girardello, R., Gonschior, H., Rodius, S., Lesur, A., Reimer, U., Ramberger, E., Pérez-Hernández, D., Müller, D., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111588 · Cited by 18 · see citing works
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Self-citationLukinović, V., & Biggar, K. K. (2021) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2021.110616 · Cited by 1 · see citing works
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Nguyen, L. T., Zimmermann, K., Kowenz‐Leutz, E., Dörr, D., Schütz, A., Schönheit, J., Mildner, A., & Leutz, A. (2024) · iScience · doi:10.1016/j.isci.2024.111199
Self-citationDewani, N., Ruiz‐Orera, J., Popp, O., Liang, N., Sugawara, M., Schulz, J. F., Witte, F., Sandmann, C.-L., Tsuji, T., Blachut, S., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.19.644091
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Pardo, M., Marcozzi, C., Lane, K. A., Sialana, F. J., Shcherbakova, L., Kozik, Z., Wan, M. S. M., Ye, F., Alfieri, C., Downs, J. A., et al. (2026) · Research Square · doi:10.64898/2026.03.15.711656
Dossin, F., Attia, M., Zuniga, F. M., González‐Acosta, D., Brough, R., Song, F., Krastev, D. B., Raghunandan, M., Pettitt, S. J., Bore, A., et al. (2026) · Molecular Cell · doi:10.1016/j.molcel.2026.09.017
- Authors
- Dittmar, G., Hernandez, D. P., Kowenz-Leutz, E., Kirchner, M., Kahlert, G., Wesolowski, R., Baum, K., Knoblich, M., Hofstätter, M., Muller, A., Wolf, J., Reimer, U., & Leutz, A.
- Affiliations
- Max Delbrück Center (DE)
- Luxembourg Institute of Health (LU)
- JPT Peptide Technologies (Germany) (DE)
- Corresponding author
- Dittmar, Gunnar
- Leutz, Achim
- ORCID
- Venue
- iScience
- Publisher
- Elsevier BV
- Published
- 2019-03
- Volume
- 13
- Pages
- 351-370
- ISSN
- 2589-0042 (ISSN-L)
- PMC
- PMC6424098
- OpenAlex
- W2921921533
- Cited by
- 41
- References
- 84
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 6 · 2023: 9 · 2022: 5 · 2021: 9 · 2020: 2 · 2018: 1
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- iScience (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (submittedVersion)
- Funders
- Fonds National de la Recherche Luxembourg
- Deutsche Forschungsgemeinschaft
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- C/EBPβ, intrinsically disordered proteins, post-translational modification, protein-protein interaction network, pioneer transcription factors, chromatin modification, chromatin remodeling, RNA processing, cell differentiation, epigenetics, structural plasticity
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