Encoding and decoding selectivity and promiscuity in the human chemokine-GPCR interaction network

  • Andrew B. Kleist*
  • , Martyna Szpakowska
  • , Lindsay J. Talbot
  • , Greg Slodkowicz
  • , Duccio Malinverni
  • , Monica A. Thomas
  • , Kyler S. Crawford
  • , Daniel J. McGrail
  • , Acacia F. Dishman
  • , Michael J. Wedemeyer
  • , Madison Sluter
  • , S. Stephen Yi
  • , Nidhi Sahni
  • , Francis C. Peterson
  • , Andy Chevigné
  • , Brian F. Volkman*
  • , M. Madan Babu*
  • *Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

1 Citation (Scopus)

Abstract

In humans, selective and promiscuous interactions between 46 secreted chemokine ligands and 23 cell surface chemokine receptors of the G-protein-coupled receptor (GPCR) family form a complex network to coordinate cell migration. While chemokines and their GPCRs each share common structural scaffolds, the molecular principles driving selectivity and promiscuity remain elusive. Here, we identify conserved, semi-conserved, and variable determinants (i.e., recognition elements) that are encoded and decoded by chemokines and their receptors to mediate interactions. Selectivity and promiscuity emerge from an ensemble of generalized (“public/conserved”) and specific (“private/variable”) determinants distributed among structured and unstructured protein regions, with ligands and receptors recognizing these determinants combinatorially. We employ these principles to engineer a viral chemokine with altered GPCR coupling preferences and provide a web resource to facilitate sequence-structure-function studies and protein design efforts for developing immuno-therapeutics and cell therapies.

Original languageEnglish
Pages (from-to)3603-3622.e27
Number of pages48
JournalCell
Volume188
Issue number13
Early online date21 Apr 2025
DOIs
Publication statusPublished - 26 Jun 2025

Keywords

  • chemokine
  • chemotaxis
  • data science
  • GPCR
  • machine learning
  • polymorphism
  • protein-protein interaction
  • selectivity determinants
  • short linear motif
  • unstructured protein
  • Amino Acid Sequence
  • Humans
  • Models, Molecular
  • Chemokines/metabolism
  • Receptors, Chemokine/metabolism
  • Receptors, G-Protein-Coupled/metabolism
  • Protein Binding
  • Ligands

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