The carboxyl terminus of the chemokine receptor CCR3 contains distinct domains which regulate chemotactic signaling and receptor down-regulation in a ligand-dependent manner

European Journal of Immunology

Volumn 35, Issue 4, 2005, Pages 1301-1310

  Sabroe, Ian ^a   Jorritsma, Annelies ^a   Stubbs, Victoria E L ^a   Xanthou, Georgina ^a   Jopling, Louise A ^a   Ponath, Paul D ^b,d   Williams, Timothy J ^a   Murphy, Philip M ^c   Pease, James E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MILLENNIUM PHARMACEUTICALS INC   (United States)

^c NATIONAL INSTRUMENTS   (United States)

^d TolerRx Inc   (United States)

Author keywords

Chemokine receptors; Chemokines; Chemotaxis; Eosinophils

Indexed keywords

AMINO ACID DERIVATIVE; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CCR3; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR;

ALLERGIC DISEASE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL SHAPE; CHEMOTAXIS; CONTROLLED STUDY; EOSINOPHIL; GENE CONSTRUCT; GENE REPLICATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKOCYTE; LYMPHOCYTE ACTIVATION; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; WILD TYPE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CHEMOKINES, CC; CHEMOTAXIS; DOWN-REGULATION; HUMANS; LIGANDS; MAP KINASE KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MONOCYTE CHEMOATTRACTANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CHEMOKINE; UP-REGULATION;

EID: 17444366208     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425171     Document Type: Article

References (28)

1. Gerard, C. and Rollins, B. J., Chemokines and disease. Nat. Immunol. 2001. 2: 108-115.
2. Jose, P. J., Griffiths-Johnson, D. A., Collins, P. D., Walsh, D. T., Moqbel, R., Totty, N. F., Truong, O., Hsuan, J. J. and Williams, T. J., Eotaxin: A potent eosinophil chemoattractant cytokine detected in a guinea-pig model of allergic airways inflammation. J. Exp. Med. 1994. 179: 881-887.
3. Heath, H., Qin, S., Wu, L., LaRosa, G., Kassam, N., Ponath, P. D. and Mackay, C. R., Chemokine receptor usage by human eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J. Clin. Invest. 1997. 99: 178-184.
4. Uguccioni, M., Mackay, C. R., Ochensberger, B., Loetscher, P., Rhis, S., LaRosa, G. J., Rao, P., Ponath, P. D., Baggiolini, M. and Dahinden, C. A., High expression of the chemokine receptor CCR3 in human blood basophils. Role in activation by eotaxin, MCP-4, and other chemokines. J. Clin. Invest. 1997. 100: 1137-1143.
5. Sallusto, F., Mackay, C. R. and Lanzavecchia, A., Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 1997. 277: 2005-2007.
6. Stellato, C., Collins, P., Li, H., White, J., Ponath, P. D., Newman, W., Soler, D., LaRosa, G., Schwiebert, L. M., Bickel, C., Liu, M, Bochner, B., Williams, T. J. and Schleimer, R., Production of the novel CC chemokine MCP-4 by airway cells and comparison of its biological activity to other CC chemokines. J. Clin. Invest. 1997. 99: 926-936.
7. Mueller, S. G., White, J. R., Schraw, W. P., Lam, V. and Richmond, A., Ligand-induced desensitization of the human CXC chemokine receptor-2 is modulated by multiple serine residues in the carboxyl-terminal domain of the receptor. J. Biol. Chem. 1997. 272: 8207-8214.
8. Haribabu, B., Richardson, R. M., Fisher, I., Sozzani, S., Peiper, S. C., Horuk, R., Ali, H. and Snyderman, R., Regulation of human chemokine receptors CXCR4. Role of phosphorylation in desensitization and internalization. J. Biol. Chem. 1997. 272: 28726-28731.
9. Oppermann, M., Mack, M., Proudfoot, A. E. and Olbrich, H., Differential effects of CC chemokines on CC chemokine receptor 5 (CCRS) phosphorylation and identification of phosphorylation sites on the CCR5 carboxyl terminus. J. Biol. Chem. 1999. 274: 8875-8885.
10. Auger, G. A., Pease, J. E., Shen, X., Xanthou, G. and Barker, M. D., Alanine scanning mutagenesis of CCR3 reveals that the three intracellular loops are essential for functional receptor expression. Eur. J. Immunol. 2002. 32: 1052-1058.
11. Mack, M., Luckow, B., Nelson, P. J., Cihak, J., Simmons, G., Clapham, P. R., Signoret, N., Marsh, M., Stangassinger, M., Borlat, F., Wells, T. N., Schlondorff, D. and Proudfoot, A. E., Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: a novel inhibitory mechanism of HIV infectivity. J. Exp. Med. 1998. 187: 1215-1224.
12. Zimmermann, N., Conkright, J. J. and Rothenberg, M. E., CC chemokine receptor-3 undergoes prolonged ligand-induced internalization. J. Biol. Chem. 1999. 274: 12611-12618.
13. Ponath, P. D., Qin, S., Ringler, D. J., Clark-Lewis, I., Wang, J., Kassam, N., Smith, H., Shi, X., Gonzalo, J.-A., Newman, W., Gutierrez-Ramos, J.-C. and Mackay, C. R., Cloning of the human eosinophil chemoattractant, eotaxin. Expression, receptor binding and functional properties suggest a mechanism for the selective recruitment of eosinophils. J. Clin. Invest. 1996. 97: 604-612.
14. Venkatesan, S., Rose, J. J., Lodge, R., Murphy, P. M. and Foley, J. F., Distinct mechanisms of agonist-induced endocytosis for human chemokine receptors CCR5 and CXCR4. Mol. Biol. Cell 2003. 14: 3305-3324.
15. Daugherty, B. L., Siciliano, S. J., DeMartino, J., Malkowitz, L., Sirontino, A. and Springer, M. S., Cloning, expression and characterization of the human eosinophil eotaxin receptor. J. Exp. Med. 1996. 183: 2349-2354.
16. Sabroe, I., Hartnell, A., Jopling, L. A., Bel, S., Ponath, P. D., Pease, J. E., Collins, P. D. and Williams, T. J., Differential regulation of eosinophil chemokine signaling via CCR3 and non-CCR3 pathways. J. Immunol. 1999. 162: 2946-2955.
17. Vila-Coro, A. J., Mellado, M., Martin, d. A., Martinez, A. and Rodriguez-Frade, J. M., Characterization of RANTES- and aminooxypentane-RANTES-triggered desensitization signals reveals differences in recruitment of the G protein-coupled receptor complex. J. Immunol. 1999. 163: 3037-3044.
18. Richardson, R. M., Marjoram, R. J., Barak, L. S. and Snyderman, R., Role of the cytoplasmic tails of CXCR1 and CXCR2 in mediating leukocyte migration, activation, and regulation. J. Immunol. 2003. 170: 2904-2911.
19. Stubbs, V. E., Schratl, P., Hartnell, A., Williams, T. J., Peskar, B. A., Heinemann, A. and Sabroe, I., Indomethacin causes PGD2-like and eotaxin-like selective responses in eosinophils and basophils. J. Biol. Chem. 2002. 277: 26012-26020.
20. Boehme, S. A., Sullivan, S. K., Crowe, P. D., Santos, M., Conlon, P. J., Sriramarao, P. and Bacon, K. B., Activation of mitogen-activated protein kinase regulates eotaxin-induced eosinophil migration. J. Immunol. 1999. 163: 1611-1618.
21. Kampen, G. T., Stafford, S., Adachi, T., Jinquan, T., Quan, S., Grant, J. A., Skov, P. S., Poulsen, L. K. and Alam R., Eotaxin induces degranulation and chemotaxis of eosinophils through the activation of ERK2 and p38 mitogen-activated protein kinases. Blood 2000. 95: 1911-1917.
22. Heinemann, A., Hartnell, A., Stubbs, V. E. L., Murakami, K., Soler, D., LaRosa, G., Askenase, P. W., Williams, T. J. and Sabroe, I., Basophil responses to chemokines are regulated by both sequential and cooperative receptor signaling. J. Immunol. 2000. 165: 7224-7233.
23. Mellado, M., Rodriguez-Frade, J. M., Aragay, A., del Real, G., Martin, A. M., Vila-Coro, A. J., Serrano, A., Mayor, F., Jr and Martinez, A., The chemokine monocyte chemotactic protein 1 triggers Janus kinase 2 activation and tyrosine phosphorylation of the CCR2B receptor. J. Immunol. 1998. 161: 805-813.
24. Huttenrauch, F., Nitzki, A., Lin, F. T., Honing, S. and Oppermann, M., Beta-arrestin binding to CC chemokine receptor 5 requires multiple C-terminal receptor phosphorylation sites and involves a conserved Asp-Arg-Tyr sequence motif. J. Biol. Chem. 2002. 277: 30769-30777.
25. Alkhatib, G., Locati, M., Kennedy, P. E., Murphy, P. M. and Berger, E. A., HIV-1 coreceptor activity of CCR5 and its inhibition by chemokines: Independence from G protein signaling and importance of coreceptor downmodulation. Virology 1997. 234: 340-348.
26. Kraft, K., Olbrich, H., Majoul, I., Mack, M., Proudfoot, A. and Oppermann, M., Characterization of sequence determinants within the carboxyl-terminal domain of chemokine receptor CCR5 that regulate signaling and receptor internalization. J. Biol. Chem. 2001. 276: 34408-34418.
27. Fan, G. H., Yang, W., Wang, X. J., Qian, Q. and Richmond, A., Identification of a motif in the carboxyl terminus of CXCR2 that is involved in adaptin 2 binding and receptor internalization. Biochemistry 2001. 40: 791-800.
28. Sabroe, I., Peck, M. J., Jan Van Keulen, B., Jorritsma, A., Simmons, G., Clapham, P. R., Williams, T. J. and Pease, J. E., A small molecule antagonist of the chemokine receptors CCR1 and CCR3: Potent inhibition of eosinophil function and CCR3-mediated HIV-1 entry. J. Biol. Chem. 2000. 275: 25985-25992.