Molecular basis of promiscuous chemokine binding and structural mimicry at the C-X-C chemokine receptor, CXCR2

Shirsha Saha, Fumiya K. Sano, Saloni Sharma, Manisankar Ganguly, Sudha Mishra, Annu Dalal, Hiroaki Akasaka, Takaaki A. Kobayashi, Nashrah Zaidi, Divyanshu Tiwari, Nabarun Roy, Manish K. Yadav, Nilanjana Banerjee, Sayantan Saha, Samanwita Mohapatra, Yuzuru Itoh, Andy Chevigné, Ramanuj Banerjee*, Wataru Shihoya*, Osamu Nureki*Arun K. Shukla*

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

1 Citation (Scopus)

Abstract

Selectivity of natural agonists for their cognate receptors is a hallmark of G-protein-coupled receptors (GPCRs); however, this selectivity often breaks down at the chemokine receptors. Chemokines often display promiscuous binding to chemokine receptors, but the underlying molecular determinants remain mostly elusive. Here, we perform a comprehensive transducer-coupling analysis, testing all known C-X-C chemokines on every C-X-C type chemokine receptor to generate a global fingerprint of the selectivity and promiscuity encoded within this system. Taking lead from this, we determine cryoelectron microscopy (cryo-EM) structures of the most promiscuous receptor, C-X-C chemokine receptor 2 (CXCR2), in complex with several chemokines. These structural snapshots elucidate the details of ligand-receptor interactions, including structural motifs, which are validated using mutagenesis and functional experiments. We also observe that most chemokines position themselves on CXCR2 as a dimer while CXCL6 exhibits a monomeric binding pose. Taken together, our findings provide the molecular basis of chemokine promiscuity at CXCR2 with potential implications for developing therapeutic molecules.

Original languageEnglish
Pages (from-to)976-988.e9
Number of pages23
JournalMolecular Cell
Volume85
Issue number5
DOIs
Publication statusPublished - 6 Mar 2025

Keywords

  • biased signaling
  • chemokine receptors
  • cryo-EM
  • dimerization
  • drug discovery
  • GPCRs
  • ligand promiscuity
  • signal transduction
  • structural mimicry
  • β-arrestin

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