Published July 13, 2022 | Version v1
Journal article Open

Structures of atypical chemokine receptor 3 reveal the basis for its promiscuity and signaling bias

  • 1. Purdue University
  • 2. University of California, San Diego
  • 3. University of Copenhagen
  • 4. University of Chicago
  • 5. ChemoCentryx Inc.

Description

Both CXC chemokine receptor 4 (CXCR4) and atypical chemokine receptor 3 (ACKR3) are activated by the chemokine CXCL12 yet evoke distinct cellular responses. CXCR4 is a canonical G protein–coupled receptor (GPCR), whereas ACKR3 is intrinsically biased for arrestin. The molecular basis for this difference is not understood. Here, we describe cryo-EM structures of ACKR3 in complex with CXCL12, a more potent CXCL12 variant, and a small-molecule agonist. The bound chemokines adopt an unexpected pose relative to those established for CXCR4 and observed in other receptor-chemokine complexes. Along with functional studies, these structures provide insight into the ligand-binding promiscuity of ACKR3, why it fails to couple to G proteins, and its bias toward β-arrestin. The results lay the groundwork for understanding the physiological interplay of ACKR3 with other GPCRs.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. The structures of the seven ACKR3 complexes and the associated data have been deposited into the Protein Data Bank under accession codes 7SK3, 7SK4, 7SK5, 7SK6, 7SK7, 7SK8, and 7SK9, and the Electron Microscopy Data Bank under accession codes EMDB-25171, 25172, 25173, 25174, 25175, 25176, and 25177, respectively. The plasmids and other reagents can be provided pending scientific review and a completed material transfer agreement. Requests for the plasmids and other reagents should be submitted to the corresponding authors T.M.H. and J.J.G.T.

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Additional details

Identifiers

DOI
10.1126/sciadv.abn8063
Other
oai:uchicago.tind.io:10962

Funding

National Institutes of Health
AI161880
National Institutes of Health
CA254402
National Institutes of Health
CA221289
National Institutes of Health
HL071818
National Institutes of Health
P30CA023168
National Institutes of Health
GM117372
National Institutes of Health
GM137505
Canadian Thoracic Society
F32 GM137505
Robertson Research International Limited
Miyuki Giken
00025326
Kanazawa University
Kræftfonden
F32 GM137505
Villum Fonden
Walther Cancer Foundation
National Institutes of Health
CA023168
Robertson Foundation

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Biochemistry and Molecular Biology