Parallel Evolution of Chemokine Binding by Structurally Related Herpesvirus Decoy Receptors

Lubman, Olga Y.; Fremont, Daved H.

doi:10.1016/j.str.2015.10.018

Parallel Evolution of Chemokine Binding by Structurally Related Herpesvirus Decoy Receptors

Journal Article · Thu Dec 03 00:00:00 EST 2015 · Structure

DOI:https://doi.org/10.1016/j.str.2015.10.018· OSTI ID:1237760

Lubman, Olga Y. ^[1]; Fremont, Daved H. ^[1]

Washington Univ. School of Medicine, St. Louis, MO (United States)

A wide variety of pathogens targets chemokine signaling networks in order to disrupt host immune surveillance and defense. Here, we report a structural and mutational analysis of rodent herpesvirus Peru encoded R17, a potent chemokine inhibitor that sequesters CC and C chemokines with high affinity. R17 consists of a pair of β-sandwich domains linked together by a bridging sheet, which form an acidic binding cleft for the chemokine CCL3 on the opposite face of a basic surface cluster that binds glycosaminoglycans. R17 promiscuously engages chemokines primarily through the same N-loop determinants used for host receptor recognition while residues located in the chemokine 40s loop drive kinetically stable complex formation. Here, the core fold adopted by R17 is unexpectedly similar to that of the M3 chemokine decoy receptor encoded by MHV-68, although, strikingly, neither the location of ligand engagement nor the stoichiometry of binding is conserved, suggesting that their functions evolved independently.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: NIAID

OSTI ID:: 1237760

Journal Information:: Structure, Journal Name: Structure Journal Issue: 1 Vol. 24; ISSN 0969-2126

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (71)

Structure-activity relationships of chemokines Clark-Lewis, Ian; Kim, Key-Sun; Rajarathnam, Krishnakumar Journal of Leukocyte Biology, Vol. 57, Issue 5 https://doi.org/10.1002/jlb.57.5.703	journal	May 1995
Dissection of the energetic coupling across the src SH2 domain-tyrosyl phosphopeptide interface Lubman, Olga Y.; Waksman, Gabriel Journal of Molecular Biology, Vol. 316, Issue 2 https://doi.org/10.1006/jmbi.2001.5362	journal	February 2002
The T1/35kDa Family of Poxvirus-Secreted Proteins Bind Chemokines and Modulate Leukocyte Influx into Virus-Infected Tissues Graham, Kathryn A.; Lalani, Alshad S.; Macen, Joanne L. Virology, Vol. 229, Issue 1 https://doi.org/10.1006/viro.1996.8423	journal	March 1997
Poxvirus Genomes Encode a Secreted, Soluble Protein That Preferentially Inhibits β Chemokine Activity yet Lacks Sequence Homology to Known Chemokine Receptors Smith, Craig A.; Smith, Terri Davis; Smolak, Pamela J. Virology, Vol. 236, Issue 2 https://doi.org/10.1006/viro.1997.8730	journal	September 1997
Modulation of chemokine activity by viruses Alcami, Antonio; Lira, Sergio A. Current Opinion in Immunology, Vol. 22, Issue 4 https://doi.org/10.1016/j.coi.2010.06.004	journal	August 2010
Targeting chemokines: Pathogens can, why can’t we? Proudfoot, Amanda E. I.; Bonvin, Pauline; Power, Christine A. Cytokine, Vol. 74, Issue 2 https://doi.org/10.1016/j.cyto.2015.02.011	journal	August 2015
Glycoprotein Structural Genomics: Solving the Glycosylation Problem Chang, Veronica T.; Crispin, Max; Aricescu, A. Radu Structure, Vol. 15, Issue 3 https://doi.org/10.1016/j.str.2007.01.011	journal	March 2007
Immune modulation by virus-encoded secreted chemokine binding proteins Heidarieh, Haleh; Hernáez, Bruno; Alcamí, Antonio Virus Research, Vol. 209 https://doi.org/10.1016/j.virusres.2015.02.028	journal	November 2015
Structural Basis of Chemokine Sequestration by a Herpesvirus Decoy Receptor Alexander, Jennifer M.; Nelson, Christopher A.; van Berkel, Victor Cell, Vol. 111, Issue 3 https://doi.org/10.1016/s0092-8674(02)01007-3	journal	November 2002
Direct Interaction of the Mouse Cytomegalovirus m152/gp40 Immunoevasin with RAE-1 Isoforms Zhi, Li; Mans, Janet; Paskow, Michael J. Biochemistry, Vol. 49, Issue 11 https://doi.org/10.1021/bi902130j	journal	March 2010
Structure of the Epstein-Barr virus major envelope glycoprotein Szakonyi, Gerda; Klein, Michael G.; Hannan, Jonathan P. Nature Structural & Molecular Biology, Vol. 13, Issue 11 https://doi.org/10.1038/nsmb1161	journal	October 2006
Human cytomegalovirus encodes a highly specific RANTES decoy receptor Wang, D.; Bresnahan, W.; Shenk, T. Proceedings of the National Academy of Sciences, Vol. 101, Issue 47 https://doi.org/10.1073/pnas.0407233101	journal	November 2004
Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2. Molina, H.; Holers, V. M.; Li, B. Proceedings of the National Academy of Sciences, Vol. 93, Issue 8 https://doi.org/10.1073/pnas.93.8.3357	journal	April 1996
Molecular Cloning and Characterization of a Highly Selective Chemokine-binding Protein from the Tick Rhipicephalus sanguineus Frauenschuh, Achim; Power, Christine A.; Déruaz, Maud Journal of Biological Chemistry, Vol. 282, Issue 37 https://doi.org/10.1074/jbc.m704706200	journal	September 2007
NK cell activation through the NKG2D ligand MULT-1 is selectively prevented by the glycoprotein encoded by mouse cytomegalovirus gene m145 Krmpotic, Astrid; Hasan, Milena; Loewendorf, Andrea Journal of Experimental Medicine, Vol. 201, Issue 2 https://doi.org/10.1084/jem.20041617	journal	January 2005
Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity Smith, Philip; Fallon, Rosie E.; Mangan, Niamh E. Journal of Experimental Medicine, Vol. 202, Issue 10 https://doi.org/10.1084/jem.20050955	journal	November 2005
Dual GPCR and GAG mimicry by the M3 chemokine decoy receptor Alexander-Brett, Jennifer M.; Fremont, Daved H. Journal of Experimental Medicine, Vol. 204, Issue 13 https://doi.org/10.1084/jem.20071677	journal	December 2007
Ticks produce highly selective chemokine binding proteins with antiinflammatory activity Déruaz, Maud; Frauenschuh, Achim; Alessandri, Ana L. Journal of Experimental Medicine, Vol. 205, Issue 9 https://doi.org/10.1084/jem.20072689	journal	August 2008
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/s0907444906019949	journal	July 2006
Iodide-SAD, SIR and SIRAS phasing for structure solution of a nucleosome assembly protein Yogavel, Manickam; Gill, Jasmita; Sharma, Amit Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/s0907444909013171	journal	May 2009
Recent developments in classical density modification Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s090744490903947x	journal	March 2010
Chemokines: Key Players in Innate and Adaptive Immunity Esche, Clemens; Stellato, Cristiana; Beck, Lisa A. Journal of Investigative Dermatology, Vol. 125, Issue 4 https://doi.org/10.1111/j.0022-202x.2005.23841.x	journal	October 2005
Structural basis for chemokine recognition and activation of a viral G protein-coupled receptor Burg, J. S.; Ingram, J. R.; Venkatakrishnan, A. J. Science, Vol. 347, Issue 6226 https://doi.org/10.1126/science.aaa5026	journal	March 2015
Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d Nemerow, G. R.; Mold, C.; Schwend, V. K. Journal of Virology, Vol. 61, Issue 5 https://doi.org/10.1128/jvi.61.5.1416-1420.1987	journal	May 1987
Identification of a Gammaherpesvirus Selective Chemokine Binding Protein That Inhibits Chemokine Action van Berkel, Victor; Barrett, John; Tiffany, H. Lee Journal of Virology, Vol. 74, Issue 15 https://doi.org/10.1128/jvi.74.15.6741-6747.2000	journal	August 2000
Chemokine:Receptor Structure, Interactions, and Antagonism Allen, Samantha J.; Crown, Susan E.; Handel, Tracy M. Annual Review of Immunology, Vol. 25, Issue 1 https://doi.org/10.1146/annurev.immunol.24.021605.090529	journal	April 2007
S TRUCTURE , F UNCTION , AND I NHIBITION OF C HEMOKINES Fernandez, Elias J.; Lolis, Elias Annual Review of Pharmacology and Toxicology, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.pharmtox.42.091901.115838	journal	April 2002
Structure and Function of the Glycosaminoglycan Binding Site of Chemokine Macrophage-Inflammatory Protein-1β Koopmann, Witte; Ediriwickrema, Chandrika; Krangel, Michael S. The Journal of Immunology, Vol. 163, Issue 4 https://doi.org/10.4049/jimmunol.163.4.2120	journal	August 1999
Shape Complementarity at Protein/Protein Interfaces Lawrence, Michael C.; Colman, Peter M. Journal of Molecular Biology, Vol. 234, Issue 4 https://doi.org/10.1006/jmbi.1993.1648	journal	December 1993
Kifunensine inhibits glycoprotein processing and the function of the modified LDL receptor in endothelial cells Elbein, Alan D.; Kerbacher, James K.; Schwartz, Colin J. Archives of Biochemistry and Biophysics, Vol. 288, Issue 1 https://doi.org/10.1016/0003-9861(91)90181-H	journal	July 1991
Structural Basis of Chemokine Sequestration by a Herpesvirus Decoy Receptor Alexander, Jennifer M.; Nelson, Christopher A.; van Berkel, Victor Cell, Vol. 111, Issue 3 https://doi.org/10.1016/S0092-8674(02)01007-3	journal	November 2002
Dali: a network tool for protein structure comparison Holm, Liisa; Sander, Chris Trends in Biochemical Sciences, Vol. 20, Issue 11 https://doi.org/10.1016/S0968-0004(00)89105-7	journal	November 1995
The M4 gene of γHV68 encodes a secreted glycoprotein and is required for the efficient establishment of splenic latency Evans, Andrew G.; Moorman, Nathaniel J.; Willer, David O. Virology, Vol. 344, Issue 2 https://doi.org/10.1016/j.virol.2005.08.020	journal	January 2006
Multi-step regulation of innate immune signaling by Kaposi's sarcoma-associated herpesvirus Lee, Hye-Ra; Amatya, Rina; Jung, Jae U. Virus Research, Vol. 209 https://doi.org/10.1016/j.virusres.2015.03.004	journal	November 2015
The Phenix software for automated determination of macromolecular structures Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Methods, Vol. 55, Issue 1 https://doi.org/10.1016/j.ymeth.2011.07.005	journal	September 2011
Structural Comparison of Monomeric Variants of the Chemokine MIP-1β Having Differing Ability To Bind the Receptor CCR5 ^, Kim, Seho; Jao, Shu-chuan; Laurence, Jennifer S. Biochemistry, Vol. 40, Issue 36 https://doi.org/10.1021/bi011065x	journal	August 2001
CC Chemokine MIP-1β Can Function As a Monomer and Depends on Phe13 for Receptor Binding ^† Laurence, Jennifer S.; Blanpain, Cedric; Burgner, John W. Biochemistry, Vol. 39, Issue 12 https://doi.org/10.1021/bi9923196	journal	March 2000
Chemokines and disease Gerard, Craig; Rollins, Barrett J. Nature Immunology, Vol. 2, Issue 2 https://doi.org/10.1038/84209	journal	February 2001
Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies Kufareva, Irina; Salanga, Catherina L.; Handel, Tracy M. Immunology and Cell Biology, Vol. 93, Issue 4 https://doi.org/10.1038/icb.2015.15	journal	February 2015
Viral mimicry of cytokines, chemokines and their receptors Alcami, Antonio Nature Reviews Immunology, Vol. 3, Issue 1 https://doi.org/10.1038/nri980	journal	January 2003
Chemokines — Chemotactic Cytokines That Mediate Inflammation Luster, Andrew D. New England Journal of Medicine, Vol. 338, Issue 7 https://doi.org/10.1056/NEJM199802123380706	journal	February 1998
Solution structure of the complex between poxvirus-encoded CC chemokine inhibitor vCCI and human MIP-1beta Zhang, L.; DeRider, M.; McCornack, M. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 38 https://doi.org/10.1073/pnas.0602142103	journal	September 2006
Control of feeding behavior in C. elegans by human G protein-coupled receptors permits screening for agonist-expressing bacteria Teng, M. S.; Shadbolt, P.; Fraser, A. G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 39 https://doi.org/10.1073/pnas.0803290105	journal	September 2008
Structural basis of mouse cytomegalovirus m152/gp40 interaction with RAE1 reveals a paradigm for MHC/MHC interaction in immune evasion Wang, R.; Natarajan, K.; Revilleza, M. J. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 51 https://doi.org/10.1073/pnas.1214088109	journal	November 2012
The N-terminal Extracellular Segments of the Chemokine Receptors CCR1 and CCR3 Are Determinants for MIP-1α and Eotaxin Binding, Respectively, but a Second Domain Is Essential for Efficient Receptor Activation Pease, James E.; Wang, Juan; Ponath, Paul D. Journal of Biological Chemistry, Vol. 273, Issue 32 https://doi.org/10.1074/jbc.273.32.19972	journal	August 1998
Identification of Amino Acid Residues Critical for Aggregation of Human CC Chemokines Macrophage Inflammatory Protein (MIP)-1α, MIP-1β, and RANTES: CHARACTERIZATION OF ACTIVE DISAGGREGATED CHEMOKINE VARIANTS Czaplewski, Lloyd G.; McKeating, Jane; Craven, C. Jeremy Journal of Biological Chemistry, Vol. 274, Issue 23 https://doi.org/10.1074/jbc.274.23.16077	journal	June 1999
Molecular Cloning and Characterization of a Highly Selective Chemokine-binding Protein from the Tick Rhipicephalus sanguineus Frauenschuh, Achim; Power, Christine A.; Déruaz, Maud Journal of Biological Chemistry, Vol. 282, Issue 37 https://doi.org/10.1074/jbc.M704706200	journal	September 2007
The Cytomegalovirus m155 Gene Product Subverts Natural Killer Cell Antiviral Protection by Disruption of H60–NKG2D Interactions Lodoen, Melissa B.; Abenes, Gerardo; Umamoto, Sean Journal of Experimental Medicine, Vol. 200, Issue 8 https://doi.org/10.1084/jem.20040583	journal	October 2004
Immune Mechanisms in Murine Gammaherpesvirus-68 Infection Stevenson, Philip G.; Efstathiou, Stacey Viral Immunology, Vol. 18, Issue 3 https://doi.org/10.1089/vim.2005.18.445	journal	September 2005
DNA sequence of the gene encoding a major secreted protein of vaccinia virus, strain Lister Patel, A. H.; Gaffney, D. F.; Subak-Sharpe, J. H. Journal of General Virology, Vol. 71, Issue 9 https://doi.org/10.1099/0022-1317-71-9-2013	journal	September 1990
A short history of SHELX Sheldrick, George M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122 https://doi.org/10.1107/S0108767307043930	journal	December 2007
Substructure solution with SHELXD Schneider, Thomas R.; Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 10 https://doi.org/10.1107/S0907444902011678	journal	September 2002
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
SAD phasing of a structure based on cocrystallized iodides using an in-house Cu K α X-ray source: effects of data redundancy and completeness on structure solution Yogavel, Manickam; Gill, Jasmita; Mishra, Prakash Chandra Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 8 https://doi.org/10.1107/S0907444907029174	journal	July 2007
The interdependence of wavelength, redundancy and dose in sulfur SAD experiments Cianci, Michele; Helliwell, John R.; Suzuki, Atsuo Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 12 https://doi.org/10.1107/S0907444908030503	journal	November 2008
Iodide-SAD, SIR and SIRAS phasing for structure solution of a nucleosome assembly protein Yogavel, Manickam; Gill, Jasmita; Sharma, Amit Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909013171	journal	May 2009
Recent developments in classical density modification Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S090744490903947X	journal	March 2010
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
Subversion of cytokine networks by virally encoded decoy receptors Epperson, Megan L.; Lee, Chung A.; Fremont, Daved H. Immunological Reviews, Vol. 250, Issue 1 https://doi.org/10.1111/imr.12009	journal	October 2012
Chemokines: Key Players in Innate and Adaptive Immunity Esche, Clemens; Stellato, Cristiana; Beck, Lisa A. Journal of Investigative Dermatology, Vol. 125, Issue 4 https://doi.org/10.1111/j.0022-202X.2005.23841.x	journal	October 2005
Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine Qin, L.; Kufareva, I.; Holden, L. G. Science, Vol. 347, Issue 6226 https://doi.org/10.1126/science.1261064	journal	January 2015
Identification and Sequencing of a Novel Rodent Gammaherpesvirus That Establishes Acute and Latent Infection in Laboratory Mice Loh, J.; Zhao, G.; Nelson, C. A. Journal of Virology, Vol. 85, Issue 6 https://doi.org/10.1128/JVI.01661-10	journal	January 2011
Rodent Herpesvirus Peru Encodes a Secreted Chemokine Decoy Receptor Lubman, O. Y.; Cella, M.; Wang, X. Journal of Virology, Vol. 88, Issue 1 https://doi.org/10.1128/JVI.02729-13	journal	October 2013
Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d Nemerow, G. R.; Mold, C.; Schwend, V. K. Journal of Virology, Vol. 61, Issue 5 https://doi.org/10.1128/JVI.61.5.1416-1420.1987	journal	May 1987
Identification of a Gammaherpesvirus Selective Chemokine Binding Protein That Inhibits Chemokine Action van Berkel, Victor; Barrett, John; Tiffany, H. Lee Journal of Virology, Vol. 74, Issue 15 https://doi.org/10.1128/JVI.74.15.6741-6747.2000	journal	August 2000
Disruption of the Murine Gammaherpesvirus 68 M1 Open Reading Frame Leads to Enhanced Reactivation from Latency Clambey, Eric T.; Virgin, Herbert W.; Speck, Samuel H. Journal of Virology, Vol. 74, Issue 4 https://doi.org/10.1128/JVI.74.4.1973-1984.2000	journal	February 2000
Regulation of Protein Function by Glycosaminoglycans—As Exemplified by Chemokines Handel, T. M.; Johnson, Z.; Crown, S. E. Annual Review of Biochemistry, Vol. 74, Issue 1 https://doi.org/10.1146/annurev.biochem.72.121801.161747	journal	June 2005
Structural Basis of Chemokine Sequestration by a Tick Chemokine Binding Protein: The Crystal Structure of the Complex between Evasin-1 and CCL3 Dias, João M.; Losberger, Christophe; Déruaz, Maud PLoS ONE, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pone.0008514	journal	December 2009
The Murine Gammaherpesvirus Immediate-Early Rta Synergizes with IRF4, Targeting Expression of the Viral M1 Superantigen to Plasma Cells O'Flaherty, Brigid M.; Soni, Tanushree; Wakeman, Brian S. PLoS Pathogens, Vol. 10, Issue 8 https://doi.org/10.1371/journal.ppat.1004302	journal	August 2014
Impaired Affinity Maturation in Cr2 ^−/− Mice Is Rescued by Adjuvants Without Improvement in Germinal Center Development Wu, Xiaobo; Jiang, Ning; Fang, Yi-Fu The Journal of Immunology, Vol. 165, Issue 6 https://doi.org/10.4049/jimmunol.165.6.3119	journal	September 2000

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