High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants

Abstract Many regulatory protein-protein interactions depend on Short Linear Motifs (SLiMs). In the cell cycle, cyclin-CDKs recognize SLiMs to control substrate recruitment and phosphorylation timing. Here, we measure the relative binding strength of ~100,000 peptides to 11 human cyclins from five f...

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Main Authors: Mihkel Örd, Matthew J. Winters, Mythili S. Subbanna, Natàlia de Martín Garrido, Victoria I. Cushing, Johanna Kliche, Caroline Benz, Ylva Ivarsson, Basil J. Greber, Peter M. Pryciak, Norman E. Davey
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-62765-z
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author Mihkel Örd
Matthew J. Winters
Mythili S. Subbanna
Natàlia de Martín Garrido
Victoria I. Cushing
Johanna Kliche
Caroline Benz
Ylva Ivarsson
Basil J. Greber
Peter M. Pryciak
Norman E. Davey
author_facet Mihkel Örd
Matthew J. Winters
Mythili S. Subbanna
Natàlia de Martín Garrido
Victoria I. Cushing
Johanna Kliche
Caroline Benz
Ylva Ivarsson
Basil J. Greber
Peter M. Pryciak
Norman E. Davey
author_sort Mihkel Örd
collection DOAJ
description Abstract Many regulatory protein-protein interactions depend on Short Linear Motifs (SLiMs). In the cell cycle, cyclin-CDKs recognize SLiMs to control substrate recruitment and phosphorylation timing. Here, we measure the relative binding strength of ~100,000 peptides to 11 human cyclins from five families (D, E, A, B, and F). Using a quantitative intracellular binding assay and large-scale tiled peptide screening, we identify multiple non-canonical binders unveiling a broader repertoire of cyclin docking motif types. Cryo-electron microscopy and saturation mutagenesis studies reveal distinct binding modes and sequence features governing motif recognition, binding strength, and cyclin preference. Docking motifs vary from highly selective to pan-cyclin, thereby fine-tuning the timing of CDK phosphorylation during cell cycle. Overall, these findings provide insights into the rules encoding specificity and affinity of SLiM-mediated interactions and offer a framework for understanding motif-driven protein networks across the proteome.
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institution Kabale University
issn 2041-1723
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publishDate 2025-08-01
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series Nature Communications
spelling doaj-art-4d9c871f4c3c407489e814723825c2c22025-08-20T03:46:09ZengNature PortfolioNature Communications2041-17232025-08-0116111910.1038/s41467-025-62765-zHigh-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinantsMihkel Örd0Matthew J. Winters1Mythili S. Subbanna2Natàlia de Martín Garrido3Victoria I. Cushing4Johanna Kliche5Caroline Benz6Ylva Ivarsson7Basil J. Greber8Peter M. Pryciak9Norman E. Davey10University of Cambridge, CRUK Cambridge InstituteDepartment of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical SchoolDepartment of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical SchoolThe Institute of Cancer Research, Chester Beatty LaboratoriesThe Institute of Cancer Research, Chester Beatty LaboratoriesDepartment of Chemistry - BMC, Uppsala University, Husargatan 3Department of Chemistry - BMC, Uppsala University, Husargatan 3Department of Chemistry - BMC, Uppsala University, Husargatan 3The Institute of Cancer Research, Chester Beatty LaboratoriesDepartment of Biochemistry and Molecular Biotechnology, University of Massachusetts Chan Medical SchoolThe Institute of Cancer Research, Chester Beatty LaboratoriesAbstract Many regulatory protein-protein interactions depend on Short Linear Motifs (SLiMs). In the cell cycle, cyclin-CDKs recognize SLiMs to control substrate recruitment and phosphorylation timing. Here, we measure the relative binding strength of ~100,000 peptides to 11 human cyclins from five families (D, E, A, B, and F). Using a quantitative intracellular binding assay and large-scale tiled peptide screening, we identify multiple non-canonical binders unveiling a broader repertoire of cyclin docking motif types. Cryo-electron microscopy and saturation mutagenesis studies reveal distinct binding modes and sequence features governing motif recognition, binding strength, and cyclin preference. Docking motifs vary from highly selective to pan-cyclin, thereby fine-tuning the timing of CDK phosphorylation during cell cycle. Overall, these findings provide insights into the rules encoding specificity and affinity of SLiM-mediated interactions and offer a framework for understanding motif-driven protein networks across the proteome.https://doi.org/10.1038/s41467-025-62765-z
spellingShingle Mihkel Örd
Matthew J. Winters
Mythili S. Subbanna
Natàlia de Martín Garrido
Victoria I. Cushing
Johanna Kliche
Caroline Benz
Ylva Ivarsson
Basil J. Greber
Peter M. Pryciak
Norman E. Davey
High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
Nature Communications
title High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
title_full High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
title_fullStr High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
title_full_unstemmed High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
title_short High-throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
title_sort high throughput investigation of cyclin docking interactions reveals the complexity of motif binding determinants
url https://doi.org/10.1038/s41467-025-62765-z
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