Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions

Abstract Phosphorylation is a ubiquitous post‐translation modification that regulates protein function by promoting, inhibiting or modulating protein–protein interactions. Hundreds of thousands of phosphosites have been identified but the vast majority have not been functionally characterised and it...

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Main Authors: Johanna Kliche, Dimitriya Hristoforova Garvanska, Leandro Simonetti, Dilip Badgujar, Doreen Dobritzsch, Jakob Nilsson, Norman E Davey, Ylva Ivarsson
Format: Article
Language:English
Published: Springer Nature 2023-05-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.202211164
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author Johanna Kliche
Dimitriya Hristoforova Garvanska
Leandro Simonetti
Dilip Badgujar
Doreen Dobritzsch
Jakob Nilsson
Norman E Davey
Ylva Ivarsson
author_facet Johanna Kliche
Dimitriya Hristoforova Garvanska
Leandro Simonetti
Dilip Badgujar
Doreen Dobritzsch
Jakob Nilsson
Norman E Davey
Ylva Ivarsson
author_sort Johanna Kliche
collection DOAJ
description Abstract Phosphorylation is a ubiquitous post‐translation modification that regulates protein function by promoting, inhibiting or modulating protein–protein interactions. Hundreds of thousands of phosphosites have been identified but the vast majority have not been functionally characterised and it remains a challenge to decipher phosphorylation events modulating interactions. We generated a phosphomimetic proteomic peptide‐phage display library to screen for phosphosites that modulate short linear motif‐based interactions. The peptidome covers ~13,500 phospho‐serine/threonine sites found in the intrinsically disordered regions of the human proteome. Each phosphosite is represented as wild‐type and phosphomimetic variant. We screened 71 protein domains to identify 248 phosphosites that modulate motif‐mediated interactions. Affinity measurements confirmed the phospho‐modulation of 14 out of 18 tested interactions. We performed a detailed follow‐up on a phospho‐dependent interaction between clathrin and the mitotic spindle protein hepatoma‐upregulated protein (HURP), demonstrating the essentiality of the phospho‐dependency to the mitotic function of HURP. Structural characterisation of the clathrin‐HURP complex elucidated the molecular basis for the phospho‐dependency. Our work showcases the power of phosphomimetic ProP‐PD to discover novel phospho‐modulated interactions required for cellular function.
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spelling doaj-art-48453826b2ae47fd8b34a2bc589dcaef2025-08-20T04:02:45ZengSpringer NatureMolecular Systems Biology1744-42922023-05-0119712110.15252/msb.202211164Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactionsJohanna Kliche0Dimitriya Hristoforova Garvanska1Leandro Simonetti2Dilip Badgujar3Doreen Dobritzsch4Jakob Nilsson5Norman E Davey6Ylva Ivarsson7Department of Chemistry, BMC, Uppsala UniversityFaculty of Health and Medical Sciences, Novo Nordisk Foundation Center for Protein Research, University of CopenhagenDepartment of Chemistry, BMC, Uppsala UniversityDepartment of Chemistry, BMC, Uppsala UniversityDepartment of Chemistry, BMC, Uppsala UniversityFaculty of Health and Medical Sciences, Novo Nordisk Foundation Center for Protein Research, University of CopenhagenDivision of Cancer Biology, The Institute of Cancer ResearchDepartment of Chemistry, BMC, Uppsala UniversityAbstract Phosphorylation is a ubiquitous post‐translation modification that regulates protein function by promoting, inhibiting or modulating protein–protein interactions. Hundreds of thousands of phosphosites have been identified but the vast majority have not been functionally characterised and it remains a challenge to decipher phosphorylation events modulating interactions. We generated a phosphomimetic proteomic peptide‐phage display library to screen for phosphosites that modulate short linear motif‐based interactions. The peptidome covers ~13,500 phospho‐serine/threonine sites found in the intrinsically disordered regions of the human proteome. Each phosphosite is represented as wild‐type and phosphomimetic variant. We screened 71 protein domains to identify 248 phosphosites that modulate motif‐mediated interactions. Affinity measurements confirmed the phospho‐modulation of 14 out of 18 tested interactions. We performed a detailed follow‐up on a phospho‐dependent interaction between clathrin and the mitotic spindle protein hepatoma‐upregulated protein (HURP), demonstrating the essentiality of the phospho‐dependency to the mitotic function of HURP. Structural characterisation of the clathrin‐HURP complex elucidated the molecular basis for the phospho‐dependency. Our work showcases the power of phosphomimetic ProP‐PD to discover novel phospho‐modulated interactions required for cellular function.https://doi.org/10.15252/msb.202211164clathrinphage displayphosphomimetic mutationphosphorylationprotein–protein interactions
spellingShingle Johanna Kliche
Dimitriya Hristoforova Garvanska
Leandro Simonetti
Dilip Badgujar
Doreen Dobritzsch
Jakob Nilsson
Norman E Davey
Ylva Ivarsson
Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
Molecular Systems Biology
clathrin
phage display
phosphomimetic mutation
phosphorylation
protein–protein interactions
title Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
title_full Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
title_fullStr Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
title_full_unstemmed Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
title_short Large‐scale phosphomimetic screening identifies phospho‐modulated motif‐based protein interactions
title_sort large scale phosphomimetic screening identifies phospho modulated motif based protein interactions
topic clathrin
phage display
phosphomimetic mutation
phosphorylation
protein–protein interactions
url https://doi.org/10.15252/msb.202211164
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