Structural basis of ligand interaction with atypical chemokine receptor 3

Gustavsson, Martin; Wang, Liwen; van Gils, Noortje; Stephens, Bryan S.; Zhang, Penglie; Schall, Thomas J.; Yang, Sichun; Abagyan, Ruben; Chance, Mark R.; Kufareva, Irina; Handel, Tracy M.

doi:10.1038/ncomms14135

Title: Structural basis of ligand interaction with atypical chemokine receptor 3

Abstract

Chemokines drive cell migration through their interactions with seven-transmembrane (7TM) chemokine receptors on cell surfaces. The atypical chemokine receptor 3 (ACKR3) binds chemokines CXCL11 and CXCL12 and signals exclusively through β-arrestin-mediated pathways, without activating canonical G-protein signalling. This receptor is upregulated in numerous cancers making it a potential drug target. Here we collected over 100 distinct structural probes from radiolytic footprinting, disulfide trapping, and mutagenesis to map the structures of ACKR3:CXCL12 and ACKR3:small-molecule complexes, including dynamic regions that proved unresolvable by X-ray crystallography in homologous receptors. The data are integrated with molecular modelling to produce complete and cohesive experimentally driven models that confirm and expand on the existing knowledge of the architecture of receptor:chemokine and receptor:small-molecule complexes. Additionally, we detected and characterized ligand-induced conformational changes in the transmembrane and intracellular regions of ACKR3 that elucidate fundamental structural elements of agonism in this atypical receptor.

Authors:

Gustavsson, Martin; Wang, Liwen; van Gils, Noortje; Stephens, Bryan S.; Zhang, Penglie; Schall, Thomas J.;

; Abagyan, Ruben; Chance, Mark R.;

; Handel, Tracy M.

Publication Date:: Wed Jan 18 00:00:00 EST 2017

Research Org.:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1409609

Report Number(s):: BNL-114661-2017-JA¿¿¿
Journal ID: ISSN 2041-1723

DOE Contract Number:: SC0012704

Resource Type:: Journal Article

Journal Name:: Nature Communications

Additional Journal Information:: Journal Volume: 8; Journal ID: ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Gustavsson, Martin, Wang, Liwen, van Gils, Noortje, Stephens, Bryan S., Zhang, Penglie, Schall, Thomas J., Yang, Sichun, Abagyan, Ruben, Chance, Mark R., Kufareva, Irina, and Handel, Tracy M. Structural basis of ligand interaction with atypical chemokine receptor 3.  United States: N. p., 2017. 
        Web.  doi:10.1038/ncomms14135.

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                    Gustavsson, Martin, Wang, Liwen, van Gils, Noortje, Stephens, Bryan S., Zhang, Penglie, Schall, Thomas J., Yang, Sichun, Abagyan, Ruben, Chance, Mark R., Kufareva, Irina, & Handel, Tracy M. Structural basis of ligand interaction with atypical chemokine receptor 3.  United States.  https://doi.org/10.1038/ncomms14135

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                    Gustavsson, Martin, Wang, Liwen, van Gils, Noortje, Stephens, Bryan S., Zhang, Penglie, Schall, Thomas J., Yang, Sichun, Abagyan, Ruben, Chance, Mark R., Kufareva, Irina, and Handel, Tracy M. 2017.  
        "Structural basis of ligand interaction with atypical chemokine receptor 3".  United States.  https://doi.org/10.1038/ncomms14135.

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@article{osti_1409609,

  title        = {Structural basis of ligand interaction with atypical chemokine receptor 3},

  author       = {Gustavsson, Martin and Wang, Liwen and van Gils, Noortje and Stephens, Bryan S. and Zhang, Penglie and Schall, Thomas J. and Yang, Sichun and Abagyan, Ruben and Chance, Mark R. and Kufareva, Irina and Handel, Tracy M.},

  abstractNote = {Chemokines drive cell migration through their interactions with seven-transmembrane (7TM) chemokine receptors on cell surfaces. The atypical chemokine receptor 3 (ACKR3) binds chemokines CXCL11 and CXCL12 and signals exclusively through β-arrestin-mediated pathways, without activating canonical G-protein signalling. This receptor is upregulated in numerous cancers making it a potential drug target. Here we collected over 100 distinct structural probes from radiolytic footprinting, disulfide trapping, and mutagenesis to map the structures of ACKR3:CXCL12 and ACKR3:small-molecule complexes, including dynamic regions that proved unresolvable by X-ray crystallography in homologous receptors. The data are integrated with molecular modelling to produce complete and cohesive experimentally driven models that confirm and expand on the existing knowledge of the architecture of receptor:chemokine and receptor:small-molecule complexes. Additionally, we detected and characterized ligand-induced conformational changes in the transmembrane and intracellular regions of ACKR3 that elucidate fundamental structural elements of agonism in this atypical receptor.},

  doi          = {10.1038/ncomms14135},

  url          = {https://www.osti.gov/biblio/1409609},
  journal      = {Nature Communications},

  issn         = {2041-1723},

  number       = ,

  volume       = 8,

  place        = {United States},

  year         = {Wed Jan 18 00:00:00 EST 2017},

  month        = {Wed Jan 18 00:00:00 EST 2017}

}

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https://doi.org/10.1038/ncomms14135

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Title: Structural basis of ligand interaction with atypical chemokine receptor 3

Abstract

Citation Formats

Biased Probability Monte Carlo Conformational Searches and Electrostatic Calculations for Peptides and Proteins journal, January 1994

Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine journal, January 2015

Conformational Dynamics of Activation for the Pentameric Complex of Dimeric G Protein-Coupled Receptor and Heterotrimeric G Protein journal, May 2012

Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser journal, July 2015

Conformational states of the full-length glucagon receptor journal, July 2015

The Beamline X28C of the Center for Synchrotron Biosciences: a National Resource for Biomolecular Structure and Dynamics Experiments Using Synchrotron Footprinting journal, April 2007

Structure-Based Identification of Novel Ligands Targeting Multiple Sites within a Chemokine–G-Protein-Coupled-Receptor Interface journal, April 2016

-arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7 journal, December 2009

Activation of G-protein-coupled receptors correlates with the formation of a continuous internal water pathway journal, September 2014

The significance of cancer cell expression of the chemokine receptor CXCR4 journal, June 2004

Biased agonism: An emerging paradigm in GPCR drug discovery journal, January 2016

Sulfopeptide Probes of the CXCR4/CXCL12 Interface Reveal Oligomer-Specific Contacts and Chemokine Allostery journal, June 2013

A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data journal, April 2007

Radiolytic Modification and Reactivity of Amino Acid Residues Serving as Structural Probes for Protein Footprinting journal, June 2005

Microscale Fluorescent Thermal Stability Assay for Membrane Proteins journal, March 2008

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Biased Signaling Pathways in 2-Adrenergic Receptor Characterized by 19F-NMR journal, January 2012

Prediction of the binding energy for small molecules, peptides and proteins journal, May 1999

Methodological advances: the unsung heroes of the GPCR structural revolution journal, January 2015

Structure of the CCR5 Chemokine Receptor-HIV Entry Inhibitor Maraviroc Complex journal, September 2013

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Allosteric sodium in class A GPCR signaling journal, May 2014

Crystal Structure of Rhodopsin: A G Protein-Coupled Receptor journal, August 2000

Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists journal, October 2010

Crystal structure of the β2 adrenergic receptor–Gs protein complex journal, July 2011

Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors journal, May 2009

Effective Application of Bicelles for Conformational Analysis of G Protein-Coupled Receptors by Hydrogen/Deuterium Exchange Mass Spectrometry journal, March 2015

Quantitative Protein Topography Analysis and High-Resolution Structure Prediction Using Hydroxyl Radical Labeling and Tandem-Ion Mass Spectrometry (MS) journal, February 2015

Structural Mass Spectrometry of Proteins Using Hydroxyl Radical Based Protein Footprinting journal, October 2011

Crystal structure of chemically synthesized [N33A] stromal cell-derived factor 1 , a potent ligand for the HIV-1 "fusin" coreceptor journal, June 1998

Molecular control of δ-opioid receptor signalling journal, January 2014

Structural Basis of CXCR4 Sulfotyrosine Recognition by the Chemokine SDF-1/CXCL12 journal, September 2008

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Structural insights into µ-opioid receptor activation journal, August 2015

Structural basis for chemokine recognition and activation of a viral G protein-coupled receptor journal, March 2015

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Identification and Characterization of Disulfide Bonds in Proteins and Peptides from Tandem MS Data by Use of the MassMatrix MS/MS Search Engine journal, January 2008

A Hybrid Structural Approach to Analyze Ligand Binding by the Serotonin Type 4 Receptor (5-HT4) journal, February 2013

Chemokines and Chemokine Receptors: Positioning Cells for Host Defense and Immunity journal, March 2014

Biased Probability Monte Carlo Conformational Searches and Electrostatic Calculations for Peptides and Proteins
journal, January 1994

Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine
journal, January 2015

Conformational Dynamics of Activation for the Pentameric Complex of Dimeric G Protein-Coupled Receptor and Heterotrimeric G Protein
journal, May 2012

Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser
journal, July 2015

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journal, July 2015

The Beamline X28C of the Center for Synchrotron Biosciences: a National Resource for Biomolecular Structure and Dynamics Experiments Using Synchrotron Footprinting
journal, April 2007

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journal, April 2016

-arrestin- but not G protein-mediated signaling by the "decoy" receptor CXCR7
journal, December 2009

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journal, September 2014

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journal, June 2004

Biased agonism: An emerging paradigm in GPCR drug discovery
journal, January 2016

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journal, June 2013

A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data
journal, April 2007

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journal, June 2005

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journal, March 2008

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journal, August 2016

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Prediction of the binding energy for small molecules, peptides and proteins
journal, May 1999

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journal, January 2015

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journal, September 2013

Quantitative Mapping of Protein Structure by Hydroxyl Radical Footprinting-Mediated Structural Mass Spectrometry: A Protection Factor Analysis
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journal, December 2014

Allosteric sodium in class A GPCR signaling
journal, May 2014

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journal, August 2000

Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists
journal, October 2010

Crystal structure of the β2 adrenergic receptor–Gs protein complex
journal, July 2011

Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors
journal, May 2009

Effective Application of Bicelles for Conformational Analysis of G Protein-Coupled Receptors by Hydrogen/Deuterium Exchange Mass Spectrometry
journal, March 2015

Quantitative Protein Topography Analysis and High-Resolution Structure Prediction Using Hydroxyl Radical Labeling and Tandem-Ion Mass Spectrometry (MS)
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journal, October 2011

Crystal structure of chemically synthesized [N33A] stromal cell-derived factor 1 , a potent ligand for the HIV-1 "fusin" coreceptor
journal, June 1998

Molecular control of δ-opioid receptor signalling
journal, January 2014

Structural Basis of CXCR4 Sulfotyrosine Recognition by the Chemokine SDF-1/CXCL12
journal, September 2008

Molecular signatures of G-protein-coupled receptors
journal, February 2013

Structural insights into µ-opioid receptor activation
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Structural basis for chemokine recognition and activation of a viral G protein-coupled receptor
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Structural waters define a functional channel mediating activation of the GPCR, rhodopsin
journal, August 2009

Identification and Characterization of Disulfide Bonds in Proteins and Peptides from Tandem MS Data by Use of the MassMatrix MS/MS Search Engine
journal, January 2008

A Hybrid Structural Approach to Analyze Ligand Binding by the Serotonin Type 4 Receptor (5-HT4)
journal, February 2013

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journal, March 2014