1eih › Citations

NMR solution structure and receptor peptide binding of the CC chemokine eotaxin-2.

Mayer KL, Stone MJ
Biochemistry 39 8382-95 (2000)
Cited: 36 times
EuropePMC logo PMID: 10913244

Abstract

The human CC chemokine eotaxin-2 is a specific agonist for the chemokine receptor CCR3 and may play a role in the recruitment of eosinophils in allergic diseases and parasitic infections. We report the solution structure of eotaxin-2 determined using heteronuclear and triple resonance NMR methods. A family of 20 structures was calculated by hybrid distance geometry-simulated annealing from 854 NOE distance restraints, 48 dihedral angle restraints, and 12 hydrogen bond restraints. The structure of eotaxin-2 (73 amino acid residues) consists of a helical turn (residues 17-20) followed by a 3-stranded antiparallel beta-sheet (residues 22-26, 37-41, and 44-49) and an alpha-helix (residues 54-66). The N-loop (residues 9-16) is packed against both the sheet and the helix with the two conserved disulfide bonds tethering the N-terminal/N-loop region to the beta-sheet. The average backbone and heavy atom rmsd values of the 20 structures (residues 7-66) are 0.52 and 1.13 A, respectively. A linear peptide corresponding to the N-terminal region of CCR3 binds to eotaxin-2, inducing concentration-dependent chemical shift changes or line broadening of many residues. The distribution of these residues suggests that the peptide binds into an extended groove located at the interface between the N-loop and the beta2-beta3 hairpin. The receptor peptide may also interact with the N-terminus of the chemokine and part of the alpha-helix. Comparison of the eotaxin-2 structure with those of related chemokines indicates several structural features that may contribute to receptor specificity.

Articles - 1eih mentioned but not cited (4)

  1. Search for allosteric disulfide bonds in NMR structures. Schmidt B, Hogg PJ. BMC Struct Biol 7 49 (2007)
  2. Retrovirus-induced spongiform neurodegeneration is mediated by unique central nervous system viral targeting and expression of env alone. Li Y, Cardona SM, Traister RS, Lynch WP. J Virol 85 2060-2078 (2011)
  3. Protein folding, misfolding and aggregation: The importance of two-electron stabilizing interactions. Cieplak AS. PLoS One 12 e0180905 (2017)
  4. The chemokine X-factor: Structure-function analysis of the CXC motif at CXCR4 and ACKR3. Wedemeyer MJ, Wedemeyer MJ, Mahn SA, Getschman AE, Crawford KS, Peterson FC, Marchese A, McCorvy JD, Volkman BF. J Biol Chem 295 13927-13939 (2020)


Reviews citing this publication (9)

  1. Chemokine: receptor structure, interactions, and antagonism. Allen SJ, Crown SE, Handel TM. Annu Rev Immunol 25 787-820 (2007)
  2. Structure, function, and inhibition of chemokines. Fernandez EJ, Lolis E. Annu Rev Pharmacol Toxicol 42 469-499 (2002)
  3. Structural basis of chemokine receptor function--a model for binding affinity and ligand selectivity. Rajagopalan L, Rajarathnam K. Biosci Rep 26 325-339 (2006)
  4. The structural role of receptor tyrosine sulfation in chemokine recognition. Ludeman JP, Stone MJ. Br J Pharmacol 171 1167-1179 (2014)
  5. New paradigms in chemokine receptor signal transduction: Moving beyond the two-site model. Kleist AB, Getschman AE, Ziarek JJ, Nevins AM, Gauthier PA, Chevigné A, Szpakowska M, Volkman BF. Biochem Pharmacol 114 53-68 (2016)
  6. Chemokine oligomerization in cell signaling and migration. Wang X, Sharp JS, Handel TM, Prestegard JH. Prog Mol Biol Transl Sci 117 531-578 (2013)
  7. 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)
  8. Structural basis of chemokine and receptor interactions: Key regulators of leukocyte recruitment in inflammatory responses. Bhusal RP, Foster SR, Stone MJ. Protein Sci 29 420-432 (2020)
  9. Disorder and cysteines in proteins: A design for orchestration of conformational see-saw and modulatory functions. Bhopatkar AA, Uversky VN, Rangachari V. Prog Mol Biol Transl Sci 174 331-373 (2020)

Articles citing this publication (23)

  1. Eotaxin-3/CCL26 is a natural antagonist for CC chemokine receptors 1 and 5. A human chemokine with a regulatory role. Petkovic V, Moghini C, Paoletti S, Uguccioni M, Gerber B. J Biol Chem 279 23357-23363 (2004)
  2. Structural rearrangement of human lymphotactin, a C chemokine, under physiological solution conditions. Kuloğlu ES, McCaslin DR, Markley JL, Volkman BF. J Biol Chem 277 17863-17870 (2002)
  3. Tyrosine sulfation of chemokine receptor CCR2 enhances interactions with both monomeric and dimeric forms of the chemokine monocyte chemoattractant protein-1 (MCP-1). Tan JHY, Ludeman JP, Wedderburn J, Canals M, Hall P, Butler SJ, Taleski D, Christopoulos A, Hickey MJ, Payne RJ, Stone MJ. J Biol Chem 288 10024-10034 (2013)
  4. Regulation of chemokine recognition by site-specific tyrosine sulfation of receptor peptides. Simpson LS, Zhu JZ, Widlanski TS, Stone MJ. Chem Biol 16 153-161 (2009)
  5. 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)
  6. Structural basis for differential binding of the interleukin-8 monomer and dimer to the CXCR1 N-domain: role of coupled interactions and dynamics. Ravindran A, Joseph PR, Rajarathnam K. Biochemistry 48 8795-8805 (2009)
  7. Chemokine CXCL1 dimer is a potent agonist for the CXCR2 receptor. Ravindran A, Sawant KV, Sarmiento J, Navarro J, Rajarathnam K. J Biol Chem 288 12244-12252 (2013)
  8. Monomeric solution structure of the prototypical 'C' chemokine lymphotactin. Kuloglu ES, McCaslin DR, Kitabwalla M, Pauza CD, Markley JL, Volkman BF. Biochemistry 40 12486-12496 (2001)
  9. Molecular determinants for CC-chemokine recognition by a poxvirus CC-chemokine inhibitor. Seet BT, Singh R, Paavola C, Lau EK, Handel TM, McFadden G. Proc Natl Acad Sci U S A 98 9008-9013 (2001)
  10. Thermodynamic characterization of interleukin-8 monomer binding to CXCR1 receptor N-terminal domain. Fernando H, Nagle GT, Rajarathnam K. FEBS J 274 241-251 (2007)
  11. Design and receptor interactions of obligate dimeric mutant of chemokine monocyte chemoattractant protein-1 (MCP-1). Tan JH, Canals M, Ludeman JP, Wedderburn J, Boston C, Butler SJ, Carrick AM, Parody TR, Taleski D, Christopoulos A, Payne RJ, Stone MJ. J Biol Chem 287 14692-14702 (2012)
  12. PDBe: Protein Data Bank in Europe. Velankar S, Alhroub Y, Alili A, Best C, Boutselakis HC, Caboche S, Conroy MJ, Dana JM, van Ginkel G, Golovin A, Gore SP, Gutmanas A, Haslam P, Hirshberg M, John M, Lagerstedt I, Mir S, Newman LE, Oldfield TJ, Penkett CJ, Pineda-Castillo J, Rinaldi L, Sahni G, Sawka G, Sen S, Slowley R, Sousa da Silva AW, Suarez-Uruena A, Swaminathan GJ, Symmons MF, Vranken WF, Wainwright M, Kleywegt GJ. Nucleic Acids Res 39 D402-10 (2011)
  13. Identification of receptor binding and activation determinants in the N-terminal and N-loop regions of the CC chemokine eotaxin. Mayer MR, Stone MJ. J Biol Chem 276 13911-13916 (2001)
  14. Characterization of the interactions of vMIP-II, and a dimeric variant of vMIP-II, with glycosaminoglycans. Zhao B, Liwang PJ. Biochemistry 49 7012-7022 (2010)
  15. Solution structure of CXCL13 and heparan sulfate binding show that GAG binding site and cellular signalling rely on distinct domains. Monneau YR, Luo L, Sankaranarayanan NV, Nagarajan B, Vivès RR, Baleux F, Desai UR, Arenzana-Seidedos F, Lortat-Jacob H. Open Biol 7 (2017)
  16. Alanine scanning mutagenesis of the chemokine receptor CCR3 reveals distinct extracellular residues involved in recognition of the eotaxin family of chemokines. Duchesnes CE, Murphy PM, Williams TJ, Pease JE. Mol Immunol 43 1221-1231 (2006)
  17. High level expression, activation, and antagonism of CC chemokine receptors CCR2 and CCR3 in Chinese hamster ovary cells. Parody TR, Stone MJ. Cytokine 27 38-46 (2004)
  18. Eotaxin and monocyte chemotactic protein-3 use different modes of action. Chung IY, Kim YH, Choi MK, Noh YJ, Park CS, Kwon DY, Lee DY, Lee YS, Chang HS, Kim KS. Biochem Biophys Res Commun 314 646-653 (2004)
  19. Sulfotyrosine recognition as marker for druggable sites in the extracellular space. Ziarek JJ, Heroux MS, Veldkamp CT, Peterson FC, Volkman BF. Int J Mol Sci 12 3740-3756 (2011)
  20. Backbone dynamics of the CC-chemokine eotaxin-2 and comparison among the eotaxin group chemokines. Mayer KL, Stone MJ. Proteins 50 184-191 (2003)
  21. N-terminal domain of eotaxin-3 is important for activation of CC chemokine receptor 3. Shinkai A, Komuta-Kunitomo M, Sato-Nakamura N, Anazawa H. Protein Eng 15 923-929 (2002)
  22. Molecular cloning, characterization and expression analysis of a CC chemokine gene from miiuy croaker (Miichthys miiuy). Cheng Y, Sun Y, Shi G, Wang R, Xu T. Fish Physiol Biochem 38 1697-1708 (2012)
  23. Kinetic and thermodynamic studies reveal chemokine homologues CC11 and CC24 with an almost identical tertiary structure have different folding pathways. Ge B, Jiang X, Chen Y, Sun T, Yang Q, Huang F. BMC Biophys 10 7 (2017)


Quick links