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Structural basis of chemokine sequestration by a herpesvirus decoy receptor.

Abstract

The M3 protein encoded by murine gamma herpesvirus68 (gamma HV68) functions as an immune system saboteur by the engagement of chemoattractant cytokines, thereby altering host antiviral inflammatory responses. Here we report the crystal structures of M3 both alone and in complex with the CC chemokine MCP-1. M3 is a two-domain beta sandwich protein with a unique sequence and topology, forming a tightly packed anti-parallel dimer. The stoichiometry of the MCP-1:M3 complex is 2:2, with two monomeric chemokines embedded at distal ends of the preassociated M3 dimer. Conformational flexibility and electrostatic complementation are both used by M3 to achieve high-affinity and broad-spectrum chemokine engagement. M3 also employs structural mimicry to promiscuously sequester chemokines, engaging conservative structural elements associated with both chemokine homodimerization and binding to G protein-coupled receptors.

Reviews - 1ml0 mentioned but not cited (1)

  1. Sequence, structure, function, immunity: structural genomics of costimulation. Chattopadhyay K, Lazar-Molnar E, Yan Q, Rubinstein R, Zhan C, Vigdorovich V, Ramagopal UA, Bonanno J, Nathenson SG, Almo SC. Immunol Rev 229 356-386 (2009)

Articles - 1ml0 mentioned but not cited (22)

  1. Protein-protein docking benchmark version 3.0. Hwang H, Pierce B, Mintseris J, Janin J, Weng Z. Proteins 73 705-709 (2008)
  2. Benchmarking and analysis of protein docking performance in Rosetta v3.2. Chaudhury S, Berrondo M, Weitzner BD, Muthu P, Bergman H, Gray JJ. PLoS One 6 e22477 (2011)
  3. Accelerating and focusing protein-protein docking correlations using multi-dimensional rotational FFT generating functions. Ritchie DW, Kozakov D, Vajda S. Bioinformatics 24 1865-1873 (2008)
  4. Protein-protein docking using region-based 3D Zernike descriptors. Venkatraman V, Yang YD, Sael L, Kihara D. BMC Bioinformatics 10 407 (2009)
  5. A web interface for easy flexible protein-protein docking with ATTRACT. de Vries SJ, Schindler CE, Chauvot de Beauchêne I, Zacharias M. Biophys J 108 462-465 (2015)
  6. Dual GPCR and GAG mimicry by the M3 chemokine decoy receptor. Alexander-Brett JM, Fremont DH. J Exp Med 204 3157-3172 (2007)
  7. Prediction of protein-protein interaction sites using electrostatic desolvation profiles. Fiorucci S, Zacharias M. Biophys J 98 1921-1930 (2010)
  8. Designing coarse grained-and atom based-potentials for protein-protein docking. Tobi D. BMC Struct Biol 10 40 (2010)
  9. Consensus scoring for enriching near-native structures from protein-protein docking decoys. Liang S, Meroueh SO, Wang G, Qiu C, Zhou Y. Proteins 75 397-403 (2009)
  10. Protein-protein binding site identification by enumerating the configurations. Guo F, Li SC, Wang L, Zhu D. BMC Bioinformatics 13 158 (2012)
  11. Identification of hot regions in protein-protein interactions by sequential pattern mining. Hsu CM, Chen CY, Liu BJ, Huang CC, Laio MH, Lin CC, Wu TL. BMC Bioinformatics 8 Suppl 5 S8 (2007)
  12. DockRank: ranking docked conformations using partner-specific sequence homology-based protein interface prediction. Xue LC, Jordan RA, El-Manzalawy Y, Dobbs D, Honavar V. Proteins 82 250-267 (2014)
  13. Structural deformation upon protein-protein interaction: a structural alphabet approach. Martin J, Regad L, Lecornet H, Camproux AC. BMC Struct Biol 8 12 (2008)
  14. Refining near-native protein-protein docking decoys by local resampling and energy minimization. Liang S, Wang G, Zhou Y. Proteins 76 309-316 (2009)
  15. How to use not-always-reliable binding site information in protein-protein docking prediction. Li L, Huang Y, Xiao Y. PLoS One 8 e75936 (2013)
  16. Protein docking by Rotation-Based Uniform Sampling (RotBUS) with fast computing of intermolecular contact distance and residue desolvation. Solernou A, Fernandez-Recio J. BMC Bioinformatics 11 352 (2010)
  17. Focused grid-based resampling for protein docking and mapping. Mamonov AB, Moghadasi M, Mirzaei H, Zarbafian S, Grove LE, Bohnuud T, Vakili P, Ch Paschalidis I, Vajda S, Kozakov D. J Comput Chem 37 961-970 (2016)
  18. Applying Side-chain Flexibility in Motifs for Protein Docking. Liu H, Lin F, Yang JL, Wang HR, Liu XL. Genomics Insights 8 1-10 (2015)
  19. Residue Mutations in Murine Herpesvirus 68 Immunomodulatory Protein M3 Reveal Specific Modulation of Chemokine Binding. Šebová R, Bauerová-Hlinková V, Beck K, Nemčovičová I, Bauer J, Kúdelová M. Front Cell Infect Microbiol 9 210 (2019)
  20. Sampling the conformation of protein surface residues for flexible protein docking. Francis-Lyon P, Gu S, Hass J, Amenta N, Koehl P. BMC Bioinformatics 11 575 (2010)
  21. Virtual screening of m3 protein antagonists for finding a model to study the gammaherpesvirus damaged immune system and chemokine related diseases. Torktaz I, Behjati M, Arjmand S. Bioimpacts 3 177-183 (2013)
  22. Residue-Residue Interaction Prediction via Stacked Meta-Learning. Chen KH, Hu YJ. Int J Mol Sci 22 6393 (2021)


Reviews citing this publication (26)

  1. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Cyster JG. Annu Rev Immunol 23 127-159 (2005)
  2. International Union of Basic and Clinical Pharmacology. [corrected]. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Bachelerie F, Ben-Baruch A, Burkhardt AM, Combadiere C, Farber JM, Graham GJ, Horuk R, Sparre-Ulrich AH, Locati M, Luster AD, Mantovani A, Matsushima K, Murphy PM, Nibbs R, Nomiyama H, Power CA, Proudfoot AE, Rosenkilde MM, Rot A, Sozzani S, Thelen M, Yoshie O, Zlotnik A. Pharmacol Rev 66 1-79 (2014)
  3. Viral mimicry of cytokines, chemokines and their receptors. Alcami A. Nat Rev Immunol 3 36-50 (2003)
  4. Regulation of protein function by glycosaminoglycans--as exemplified by chemokines. Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE. Annu Rev Biochem 74 385-410 (2005)
  5. Tuning inflammation and immunity by chemokine sequestration: decoys and more. Mantovani A, Bonecchi R, Locati M. Nat Rev Immunol 6 907-918 (2006)
  6. Pathogenesis and host control of gammaherpesviruses: lessons from the mouse. Barton E, Mandal P, Speck SH. Annu Rev Immunol 29 351-397 (2011)
  7. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Johnson Z, Proudfoot AE, Handel TM. Cytokine Growth Factor Rev 16 625-636 (2005)
  8. Chemokines: roles in leukocyte development, trafficking, and effector function. Ono SJ, Nakamura T, Miyazaki D, Ohbayashi M, Dawson M, Toda M. J Allergy Clin Immunol 111 1185-99; quiz 1200 (2003)
  9. Mechanisms of Regulation of the Chemokine-Receptor Network. Stone MJ, Hayward JA, Huang C, E Huma Z, Sanchez J. Int J Mol Sci 18 (2017)
  10. Evasion of innate and adaptive immunity by flaviviruses. Diamond MS. Immunol Cell Biol 81 196-206 (2003)
  11. Pathogen-derived immunomodulatory molecules: future immunotherapeutics? Fallon PG, Alcami A. Trends Immunol 27 470-476 (2006)
  12. Immune evasion by gamma-herpesviruses. Stevenson PG. Curr Opin Immunol 16 456-462 (2004)
  13. Platelet-derived chemokines: pathophysiology and therapeutic aspects. Flad HD, Brandt E. Cell Mol Life Sci 67 2363-2386 (2010)
  14. Targeting chemokines: Pathogens can, why can't we? Proudfoot AE, Bonvin P, Power CA. Cytokine 74 259-267 (2015)
  15. Mechanisms of immunomodulation by mammalian and viral decoy receptors: insights from structures. Felix J, Savvides SN. Nat Rev Immunol 17 112-129 (2017)
  16. Modulation of chemokine activity by viruses. Alcami A, Lira SA. Curr Opin Immunol 22 482-487 (2010)
  17. Subversion of cytokine networks by virally encoded decoy receptors. Epperson ML, Lee CA, Fremont DH. Immunol Rev 250 199-215 (2012)
  18. How microorganisms avoid phagocyte attraction. Bestebroer J, De Haas CJ, Van Strijp JA. FEMS Microbiol Rev 34 395-414 (2010)
  19. Neutralizing endogenous chemokines with small molecules. Principles and potential therapeutic applications. Galzi JL, Hachet-Haas M, Bonnet D, Daubeuf F, Lecat S, Hibert M, Haiech J, Frossard N. Pharmacol Ther 126 39-55 (2010)
  20. Immune modulation by virus-encoded secreted chemokine binding proteins. Heidarieh H, Hernáez B, Alcamí A. Virus Res 209 67-75 (2015)
  21. Cytokines and costimulatory molecules in the immune response to murine gammaherpesvirus-68. Sarawar SR, Lee BJ, Giannoni F. Viral Immunol 17 3-11 (2004)
  22. Immune regulation of viral infection and vice versa. Virgin HW. Immunol Res 32 293-315 (2005)
  23. Evasins: Tick Salivary Proteins that Inhibit Mammalian Chemokines. Bhusal RP, Eaton JRO, Chowdhury ST, Power CA, Proudfoot AEI, Stone MJ, Bhattacharya S. Trends Biochem Sci 45 108-122 (2020)
  24. Deriving Immune Modulating Drugs from Viruses-A New Class of Biologics. Yaron JR, Zhang L, Guo Q, Burgin M, Schutz LN, Awo E, Wise L, Krause KL, Ildefonso CJ, Kwiecien JM, Juby M, Rahman MM, Chen H, Moyer RW, Alcami A, McFadden G, Lucas AR. J Clin Med 9 (2020)
  25. Does C-C Motif Chemokine Ligand 2 (CCL2) Link Obesity to a Pro-Inflammatory State? Dommel S, Blüher M. Int J Mol Sci 22 (2021)
  26. The binding and specificity of chemokine binding proteins, through the lens of experiment and computation. Stark LE, Guan W, Colvin ME, LiWang PJ. Biomed J 45 439-453 (2022)

Articles citing this publication (42)

  1. Assessing the performance of the MM/PBSA and MM/GBSA methods. 6. Capability to predict protein-protein binding free energies and re-rank binding poses generated by protein-protein docking. Chen F, Liu H, Sun H, Pan P, Li Y, Li D, Hou T. Phys Chem Chem Phys 18 22129-22139 (2016)
  2. SCOPPI: a structural classification of protein-protein interfaces. Winter C, Henschel A, Kim WK, Schroeder M. Nucleic Acids Res 34 D310-4 (2006)
  3. Human cytomegalovirus encodes a highly specific RANTES decoy receptor. Wang D, Bresnahan W, Shenk T. Proc Natl Acad Sci U S A 101 16642-16647 (2004)
  4. A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Alejo A, Ruiz-Argüello MB, Ho Y, Smith VP, Saraiva M, Alcami A. Proc Natl Acad Sci U S A 103 5995-6000 (2006)
  5. Molecular cloning and characterization of a highly selective chemokine-binding protein from the tick Rhipicephalus sanguineus. Frauenschuh A, Power CA, Déruaz M, Ferreira BR, Silva JS, Teixeira MM, Dias JM, Martin T, Wells TNC, Proudfoot AEI. J Biol Chem 282 27250-27258 (2007)
  6. Thermodynamic analysis of degenerate recognition by the NKG2D immunoreceptor: not induced fit but rigid adaptation. McFarland BJ, Strong RK. Immunity 19 803-812 (2003)
  7. Analysis of an orf virus chemokine-binding protein: Shifting ligand specificities among a family of poxvirus viroceptors. Seet BT, McCaughan CA, Handel TM, Mercer A, Brunetti C, McFadden G, Fleming SB. Proc Natl Acad Sci U S A 100 15137-15142 (2003)
  8. Structure and function of A41, a vaccinia virus chemokine binding protein. Bahar MW, Kenyon JC, Putz MM, Abrescia NG, Pease JE, Wise EL, Stuart DI, Smith GL, Grimes JM. PLoS Pathog 4 e5 (2008)
  9. Solution structure of the complex between poxvirus-encoded CC chemokine inhibitor vCCI and human MIP-1beta. Zhang L, Derider M, McCornack MA, Jao SC, Isern N, Ness T, Moyer R, LiWang PJ. Proc Natl Acad Sci U S A 103 13985-13990 (2006)
  10. Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. Müller S, Zocher G, Steinle A, Stehle T. PLoS Pathog 6 e1000723 (2010)
  11. Structural basis of chemokine sequestration by a tick chemokine binding protein: the crystal structure of the complex between Evasin-1 and CCL3. Dias JM, Losberger C, Déruaz M, Power CA, Proudfoot AE, Shaw JP. PLoS One 4 e8514 (2009)
  12. Viral chemokine-binding proteins inhibit inflammatory responses and aortic allograft transplant vasculopathy in rat models. Liu L, Dai E, Miller L, Seet B, Lalani A, Macauley C, Li X, Virgin HW, Bunce C, Turner P, Moyer R, McFadden G, Lucas A. Transplantation 77 1652-1660 (2004)
  13. Structural basis of chemokine sequestration by CrmD, a poxvirus-encoded tumor necrosis factor receptor. Xue X, Lu Q, Wei H, Wang D, Chen D, He G, Huang L, Wang H, Wang X. PLoS Pathog 7 e1002162 (2011)
  14. Structural determinants of chemokine binding by an Ectromelia virus-encoded decoy receptor. Arnold PL, Fremont DH. J Virol 80 7439-7449 (2006)
  15. Structure of human cytomegalovirus UL141 binding to TRAIL-R2 reveals novel, non-canonical death receptor interactions. Nemčovičová I, Benedict CA, Zajonc DM. PLoS Pathog 9 e1003224 (2013)
  16. Equivalent binding sites reveal convergently evolved interaction motifs. Henschel A, Kim WK, Schroeder M. Bioinformatics 22 550-555 (2006)
  17. Islet expression of M3 uncovers a key role for chemokines in the development and recruitment of diabetogenic cells in NOD mice. Martin AP, Grisotto MG, Canasto-Chibuque C, Kunkel SL, Bromberg JS, Furtado GC, Lira SA. Diabetes 57 387-394 (2008)
  18. Structure activity relationships of monocyte chemoattractant proteins in complex with a blocking antibody. Reid C, Rushe M, Jarpe M, van Vlijmen H, Dolinski B, Qian F, Cachero TG, Cuervo H, Yanachkova M, Nwankwo C, Wang X, Etienne N, Garber E, Bailly V, de Fougerolles A, Boriack-Sjodin PA. Protein Eng Des Sel 19 317-324 (2006)
  19. 4SCOPmap: automated assignment of protein structures to evolutionary superfamilies. Cheek S, Qi Y, Krishna SS, Kinch LN, Grishin NV. BMC Bioinformatics 5 197 (2004)
  20. Expression of the chemokine binding protein M3 promotes marked changes in the accumulation of specific leukocytes subsets within the intestine. Shang L, Thirunarayanan N, Viejo-Borbolla A, Martin AP, Bogunovic M, Marchesi F, Unkeless JC, Ho Y, Furtado GC, Alcami A, Merad M, Mayer L, Lira SA. Gastroenterology 137 1006-18, 1018.e1-3 (2009)
  21. Inhibition of intimal hyperplasia in transgenic mice conditionally expressing the chemokine-binding protein M3. Pyo R, Jensen KK, Wiekowski MT, Manfra D, Alcami A, Taubman MB, Lira SA. Am J Pathol 164 2289-2297 (2004)
  22. Evasins: Therapeutic Potential of a New Family of Chemokine-Binding Proteins from Ticks. Bonvin P, Power CA, Proudfoot AE. Front Immunol 7 208 (2016)
  23. Structures of human CCL18, CCL3, and CCL4 reveal molecular determinants for quaternary structures and sensitivity to insulin-degrading enzyme. Liang WG, Ren M, Zhao F, Tang WJ. J Mol Biol 427 1345-1358 (2015)
  24. Analysis of the herpesvirus chemokine-binding glycoprotein G residues essential for chemokine binding and biological activity. Van de Walle GR, Kaufer BB, Chbab N, Osterrieder N. J Biol Chem 284 5968-5976 (2009)
  25. Identification of the pharmacophore of the CC chemokine-binding proteins Evasin-1 and -4 using phage display. Bonvin P, Dunn SM, Rousseau F, Dyer DP, Shaw J, Power CA, Handel TM, Proudfoot AEI. J Biol Chem 289 31846-31855 (2014)
  26. Structures of Orf Virus Chemokine Binding Protein in Complex with Host Chemokines Reveal Clues to Broad Binding Specificity. Couñago RM, Knapp KM, Nakatani Y, Fleming SB, Corbett M, Wise LM, Mercer AA, Krause KL. Structure 23 1199-1213 (2015)
  27. The gammaherpesvirus chemokine binding protein binds to the N terminus of CXCL8. Webb LM, Clark-Lewis I, Alcami A. J Virol 77 8588-8592 (2003)
  28. Parallel Evolution of Chemokine Binding by Structurally Related Herpesvirus Decoy Receptors. Lubman OY, Fremont DH. Structure 24 57-69 (2016)
  29. Rodent herpesvirus Peru encodes a secreted chemokine decoy receptor. Lubman OY, Cella M, Wang X, Monte K, Lenschow DJ, Huang YH, Fremont DH. J Virol 88 538-546 (2014)
  30. The M4 gene of gammaHV68 encodes a secreted glycoprotein and is required for the efficient establishment of splenic latency. Evans AG, Moorman NJ, Willer DO, Speck SH. Virology 344 520-531 (2006)
  31. Multipronged attenuation of macrophage-colony stimulating factor signaling by Epstein-Barr virus BARF1. Shim AH, Chang RA, Chen X, Longnecker R, He X. Proc Natl Acad Sci U S A 109 12962-12967 (2012)
  32. Structural basis of GM-CSF and IL-2 sequestration by the viral decoy receptor GIF. Felix J, Kandiah E, De Munck S, Bloch Y, van Zundert GC, Pauwels K, Dansercoer A, Novanska K, Read RJ, Bonvin AM, Vergauwen B, Verstraete K, Gutsche I, Savvides SN. Nat Commun 7 13228 (2016)
  33. Structural basis of the herpesvirus M3-chemokine interaction. Alcami A. Trends Microbiol 11 191-192 (2003)
  34. Structural similarity to bridge sequence space: finding new families on the bridges. Shah PK, Aloy P, Bork P, Russell RB, Russell RB. Protein Sci 14 1305-1314 (2005)
  35. Ancylostoma ceylanicum excretory-secretory protein 2 adopts a netrin-like fold and defines a novel family of nematode proteins. Kucera K, Harrison LM, Cappello M, Modis Y. J Mol Biol 408 9-17 (2011)
  36. Chemokine binding protein 'M3' limits atherosclerosis in apolipoprotein E-/- mice. Ravindran D, Ridiandries A, Vanags LZ, Henriquez R, Cartland S, Tan JT, Tan JT, Bursill CA. PLoS One 12 e0173224 (2017)
  37. A Broad-Spectrum Chemokine-Binding Protein of Bovine Papular Stomatitis Virus Inhibits Neutrophil and Monocyte Infiltration in Inflammatory and Wound Models of Mouse Skin. Sharif S, Nakatani Y, Wise L, Corbett M, Real NC, Stuart GS, Lateef Z, Krause K, Mercer AA, Fleming SB. PLoS One 11 e0168007 (2016)
  38. Structural insights into the interaction between a potent anti-inflammatory protein, viral CC chemokine inhibitor (vCCI), and the human CC chemokine, Eotaxin-1. Kuo NW, Gao YG, Schill MS, Isern N, Dupureur CM, LiWang PJ. J Biol Chem 289 6592-6603 (2014)
  39. Recombinant Myxoma Virus-Derived Immune Modulator M-T7 Accelerates Cutaneous Wound Healing and Improves Tissue Remodeling. Yaron JR, Zhang L, Guo Q, Awo EA, Burgin M, Schutz LN, Zhang N, Kilbourne J, Daggett-Vondras J, Lowe KM, Lucas AR. Pharmaceutics 12 E1003 (2020)
  40. Mechanism of action of the viral chemokine-binding protein E163 from ectromelia virus. Heidarieh H, Alcamí A. J Biol Chem 293 17418-17429 (2018)
  41. Biophysical and Computational Studies of the vCCI:vMIP-II Complex. Nguyen AF, Kuo NW, Showalter LJ, Ramos R, Dupureur CM, Colvin ME, LiWang PJ. Int J Mol Sci 18 (2017)
  42. IL-10 based immunomodulation initiated at birth extends lifespan in a familial mouse model of amyotrophic lateral sclerosis. Strickland MR, Ibanez KR, Yaroshenko M, Diaz CC, Borchelt DR, Chakrabarty P. Sci Rep 10 20862 (2020)