Chemokine signaling specificity: Essential role for the N-terminal domain of chemokine receptor

Biochemistry

Volumn 46, Issue 31, 2007, Pages 8961-8968

  Prado, Gregory N ^a   Suetomi, Katsutoshi ^a   Shumate, David ^a   Maxwell, Carrie ^a   Ravindran, Aishwarya ^a   Rajarathnam, Krishna ^a   Navarro, Javier ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMEDICAL ENGINEERING; NEUROLOGY; TUMORS;

CHEMOKINE RECEPTOR; CHEMOKINE SIGNALING; SIGNAL SPECIFICITY;

SIGNAL TRANSDUCTION;

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL SURVIVAL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INFLAMMATION; INTERNALIZATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WOUND HEALING;

AMINO ACID SUBSTITUTION; ANIMALS; CERCOPITHECUS AETHIOPS; CHEMOKINES, CXC; COS CELLS; ENDOCYTOSIS; HUMANS; INTERLEUKIN-8; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, MOLECULAR; MUTANT CHIMERIC PROTEINS; PHOSPHORYLATION; RABBITS; RECEPTORS, INTERLEUKIN-8; RECEPTORS, INTERLEUKIN-8A; RECEPTORS, INTERLEUKIN-8B; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 34547776727     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7004043     Document Type: Article

References (52)

1. Baggiolini, M. (1998) Chemokines and leukocyte traffic, Nature 392, 565-568.
2. Onuffer, J. J., and Horuk, R. (2002) Chemokines, chemokine receptors and small-molecule antagonists: Recent developments, Trends Pharmacol. Sci. 23, 459-467.
3. Thelen, M. (2001) Dancing to the tune of chemokines, Nat. Immunol. 2, 129-134.
4. Ben-Baruch, A., Bengali, K., Tani, K., Xu, L., Oppenheim, J. J., and Wang, J. M. (1997) IL-8 and NAP-2 differ in their capacities to bind and chemoattract 293 cells transfected with either IL-8 receptor type A or type B, Cytokine 9, 37-45.
5. Ben-Baruch, A., Grimm, M., Bengali, K., Evans, G. A., Chertov, O., Wang, J. M., Howard, O. M., Mukaida, N., Matsushima, K., and Oppenheim, J. J. (1997) The differential ability of IL-8 and neutrophil-activating peptide-2 to induce attenuation of chemotaxis is mediated by their divergent capabilities to phosphorylate CXCR2 (IL-8 receptor B), J. Immunol. 158, 5927-5933.
6. Damaj, B. B., McColl, S. R., Neote, K., Hebert, C. A., and Naccache, P. H. (1996) Diverging signal transduction pathways activated by interleukin 8 (IL-8) and related chemokines in human neutrophils. IL-8 and Gro-α differentially stimulate calcium influx through IL-8 receptors A and B, J. Biol. Chem. 271, 20540-20544.
7. +-CXC chemokines and mechanisms regulating CXCR2 internalization and recycling, Blood 95, 1551-1559.
8. Katancik, J. A., Sharma, A., and de Nardin, E. (2000) Interleukin 8, neutrophil-activating peptide-2 and GRO-α bind to and elicit cell activation via specific and different amino acid residues of CXCR2, Cytokine 12, 1480-1488.
9. Katancik, J. A., Sharma, A., Radel, S. J., and De Nardin, E. (1997) Mapping of the extracellular binding regions of the human interleukin-8 type B receptor, Biochem. Biophys. Res. Commun. 232, 663-668.
10. Devalaraja, R. M., Nanney, L. B., Du, J., Qian, Q., Yu, Y., Devalaraja, M. N., and Richmond, A. (2000) Delayed wound healing in CXCR2 knockout mice, J. Invest. Dermatol. 115, 234-244.
11. Rosenkilde, M. M., and Schwartz, T. W. (2004) The chemokine system: A major regulator of angiogenesis in health and disease, APMIS 112, 481-495.
12. Tran, P. B., and Miller, R. J. (2003) Chemokine receptors: Signposts to brain development and disease, Nat. Rev. Neurosci. 4, 444-455.
13. Ahuja, S. K., and Murphy, P. M. (1996) The CXC chemokines growth-regulated oncogene (GRO) α, GROβ, GROγ, neutrophil-activating peptide-2, and epithelial cell-derived neutrophil-activating peptide-78 are potent agonists for the type B, but not the type A, human interleukin-8 receptor, J. Biol. Chem. 271, 20545-20550.
14. LaRosa, G. J., Thomas, K. M., Kaufmann, M. E., Mark, R., White, M., Taylor, L., Gray, G., Witt, D., and Navarro, J. (1992) Amino terminus of the interleukin-8 receptor is a major determinant of receptor subtype specificity, J. Biol. Chem. 267, 25402-25406.
15. Rajagopalan, L., and Rajarathnam, K. (2006) Structural basis of chemokine receptor function: A model for binding affinity and ligand selectivity Biosci. Rep. 26, 325-339.
16. Clark-Lewis, I., Dewald, B., Geiser, T., Moser, B., and Baggiolini, M. (1993) Platelet factor 4 binds to interleukin 8 receptors and activates neutrophils when its N terminus is modified with Glu-Leu-Arg, Proc. Natl. Acad. Sci. U.S.A. 90, 3574-3577.
17. Clark-Lewis, I., Dewald, B., Loetscher, M., Moser, B., and Baggiolini, M. (1994) Structural requirements for interleukin-8 function identified by design of analogs and CXC chemokine hybrids, J. Biol. Chem. 269, 16075-16081.
18. Leong, S. R., Kabakoff, R. C., and Hebert, C. A. (1994) Complete mutagenesis of the extracellular domain of interleukin-8 (IL-8) type A receptor identifies charged residues mediating IL-8 binding and signal transduction, J. Biol. Chem. 269, 19343-19348.
19. Lowman, H. B., Slagle, P. H., DeForge, L. E., Wirth, C. M., Gillece-Castro, B. L., Bourell, J. H., and Fairbrother, W. J. (1996) Exchanging interleukin-8 and melanoma growth-stimulating activity receptor binding specificities, J. Biol. Chem. 271, 14344-14352.
20. Moser, B., Dewald, B., Barella, L., Schumacher, C., Baggiolini, M., and Clark-Lewis, I. (1993) Interleukin-8 antagonists generated by N-terminal modification, J. Biol. Chem. 268, 7125-7128.
21. Skelton, N. J., Quan, C., Reilly, D., and Lowman, H. (1999) Structure of a CXC chemokine-receptor fragment in complex with interleukin-8, Structure 7, 157-168.
22. Jones, S. A., Wolf, M., Qin, S., Mackay, C. R., and Baggiolini, M. (1996) Different functions for the interleukin 8 receptors (IL-8R) of human neutrophil leukocytes: NADPH oxidase and phospholipase D are activated through IL-8R1 but not IL-8R2, Proc. Natl. Acad. Sci. U.S.A. 93, 6682-6686.
23. Chakrabarti, S., and Patel, K. D. (2005) Regulation of matrix metalloproteinase-9 release from IL-8-stimulated human neutrophils, J. Leukocyte Biol. 78, 279-288.
24. Watson, K., and Fan, G. H. (2005) Macrophage inflammatory protein 2 inhibits β-amyloid peptide (1-42)-mediated hippocampal neuronal apoptosis through activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase signaling pathways, Mol. Pharmacol. 67, 757-765.
25. Prado, G. N., Suzuki, H., Wilkinson, N., Cousins, B., and Navarro, J. (1996) Role of the C terminus of the interleukin 8 receptor in signal transduction and internalization, J. Biol. Chem. 271, 19186-19190.
26. Richardson, R. M., Marjoram, R. J., Barak, L. S., and Snyderman, R. (2003) Role of the cytoplasmic tails of CXCR1 and CXCR2 in mediating leukocyte migration, activation, and regulation, J. Immunol. 170, 2904-2911.
27. Reiter, E., and Lefkowitz, R. J. (2006) GRKs and β-arrestins: Roles in receptor silencing, trafficking and signaling, Trends Endocrinol. Metab. 17, 159-165.
28. Rajarathnam, K., Prado, G. N., Fernando, H., Clark-Lewis, I., and Navarro, J. (2006) Probing receptor binding activity of interleukin-8 dimer using a disulfide trap, Biochemistry 45, 7882-7888.
29. Suetomi, K., Lu, Z., Heck, T., Wood, T. G., Prusak, D. J., Dunn, K. J., and Navarro, J. (1999) Differential mechanisms of recognition and activation of interleukin-8 receptor subtypes, J. Biol. Chem. 274, 11768-11772.
30. Thomas, K. M., Taylor, L., and Navarro, J. (1991) The interleukin-8 receptor is encoded by a neutrophil-specific cDNA clone, F3R, J. Biol. Chem. 266, 14839-14841.
31. Lu, Z., Murray, K. S., Van Cleave, V., LaVallie, E. R., Stahl, M. L., and McCoy, J. M. (1995) Expression of thioredoxin random peptide libraries on the Escherichia coli cell surface as functional fusions to flagellin: A system designed for exploring protein-protein interactions, Bio/Technology 13, 366-372.
32. Williams, G., Borkakoti, N., Bottomley, G. A., Cowan, I., Fallowfield, A. G., Jones, P. S., Kirtland, S. J., Price, G. J., and Price, L. (1996) Mutagenesis studies of interleukin-8. Identification of a second epitope involved in receptor binding, J. Biol. Chem. 271, 9579-9586.
33. Hebert, C. A., Vitangcol, R. V., and Baker, J. B. (1991) Scanning mutagenesis of interleukin-8 identifies a cluster of residues required for receptor binding, J. Biol. Chem. 266, 18989-18994.
34. Rose, J. J., Foley, J. F., Murphy, P. M., and Venkatesan, S. (2004) On the mechanism and significance of ligand-induced internalization of human neutrophil chemokine receptors CXCR1 and CXCR2, J. Biol. Chem. 279, 24372-24386.
35. Hoeller, D., Volarevic, S., and Dikic, I. (2005) Compartmentalization of growth factor receptor signalling, Curr. Opin. Cell Biol. 17, 107-111.
36. Stork, P. J. (2005) Directing NGF's actions: It's a Rap, Nat. Cell Biol. 7, 338-339.
37. Friedman, A., and Perrimon, N. (2006) A functional RNAi screen for regulators of receptor tyrosine kinase and ERK signalling, Nature 444, 230-234.
38. Kao, S., Jaiswal, R. K., Kolch, W., and Landreth, G. E. (2001) Identification of the mechanisms regulating the differential activation of the mapk cascade by epidermal growth factor and nerve growth factor in PC12 cells, J. Biol. Chem. 276, 18169-18177.
39. York, R. D., Molliver, D. C., Grewal, S. S., Stenberg, P. E., McCleskey, E. W., and Stork, P. J. (2000) Role of phosphoinositide 3-kinase and endocytosis in nerve growth factor-induced extracellular signal-regulated kinase activation via Ras and Rap1, Mol. Cell. Biol. 20, 8069-8083.
40. Ahn, S., Shenoy, S. K., Wei, H., and Lefkowitz, R. J. (2004) Differential kinetic and spatial patterns of β-arrestin and G protein-mediated ERK activation by the angiotensin II receptor, J. Biol. Chem. 279, 35518-35525.
41. Daniels, D., Yee, D. K., Faulconbridge, L. F., and Fluharty, S. J. (2005) Divergent behavioral roles of angiotensin receptor intracellular signaling cascades, Endocrinology 146, 5552-5560.
42. Shyamala, V., and Khoja, H. (1998) Interleukin-8 receptors R1 and R2 activate mitogen-activated protein kinases and induce c-fos, independent of Ras and Raf-1 in Chinese hamster ovary cells, Biochemistry 37, 15918-15924.
43. Fuhler, G. M., Knol, G. J., Drayer, A. L., and Vellenga, E. (2005) Impaired interleukin-8- and GROα-induced phosphorylation of extracellular signal-regulated kinase result in decreased migration of neutrophils from patients with myelodysplasia, J. Leukocyte Biol. 77, 257-266.
44. Knall, C., Young, S., Nick, J. A., Buhl, A. M., Worthen, G. S., and Johnson, G. L. (1996) Interleukin-8 regulation of the Ras/ Raf/mitogen-activated protein kinase pathway in human neutrophils, J. Biol. Chem. 271, 2832-2838.
45. Xia, M., and Hyman, B. T. (2002) GROα/KC, a chemokine receptor CXCR2 ligand, can be a potent trigger for neuronal ERK 1/2 and PI-3 kinase pathways and for tau hyperphosphorylation-a role in Alzheimer's disease? J. Neuroimmunol. 122, 55-64.
46. Zhao, M., Wimmer, A., Trieu, K., Discipio, R. G., and Schraufstatter, I. U. (2004) Arrestin regulates MAPK activation and prevents NADPH oxidase-dependent death of cells expressing CXCR2, J. Biol. Chem. 279, 49259-49267.
47. Lippert, U., Artuc, M., Grutzkau, A., Moller, A., Kenderessy-Szabo, A., Schadendorf, D., Norgauer, J., Hartmann, K., Schweitzer-Stenner, R., Zuberbier, T., Henz, B. M., and Kruger-Krasagakes, S. (1998) Expression and functional activity of the IL-8 receptor type CXCR1 and CXCR2 on human mast cells, J. Immunol. 161, 2600-2608.
48. Gayle, R. B., III, Sleath, P. R., Srinivason, S., Birks, C. W., Weerawarna, K. S., Cerretti, D. P., Kozlosky, C. J., Nelson, N., Vanden Bos, T., and Beckmann, M. P. (1993) Importance of the amino terminus of the interleukin-8 receptor in ligand interactions, J. Biol. Chem. 268, 7283-7289.
49. Nasser, M. W., Raghuwanshi, S. K., Malloy, K. M., Gangavarapu, P., Shim, J. Y., Rajarathnam, K., and Richardson, R. M. (2007) CXCR1 and CXCR2 activation and regulation. Role of aspartate 199 of the second extracellular loop of CXCR2 in CXCL8-mediated rapid receptor internalization, J. Biol. Chem. 282, 6906-6915.
50. Fan, G.-H., Yang, W., Wang, X.-J., Qian, Q., and Richmond, A. (2001) Identification of a motif in the carboxyl terminus of CXCR2 that is involved in adaptin 2 binding and receptor internalization, Biochemistry 40, 791-800.
51. Sai, J., Walker, G., Wikswo, J., and Richmond, A. (2006) The IL sequence in the LLLKIL motif in CXCR2 is required for full ligand-induced activation of Erk, Akt, and chemotaxis in HL-60 cells, J. Biol. Chem. 281, 35931-35941.
52. Wolf, M., Delgado, M. B., Jones, S. A., DeWald, B., Clark-Lewis, I., and Baggiolini, M. (1998) Granulocyte chemotactic protein 2 acts via both IL-8 receptors, CXCR1 and CXCR2, Eur. J. Immunol. 28, 164-170.