Structural basis for differential binding of the interleukin-8 monomer and dimer to the CXCR1 N-domain: Role of coupled interactions and dynamics

Biochemistry

Volumn 48, Issue 37, 2009, Pages 8795-8805

  Ravindran, Aishwarya ^a   Joseph, Prem Raj B ^a   Rajarathnam, Krishna ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITIES; BINDING PROCESS; CONFORMATIONAL CHANGE; CONFORMATIONAL FLEXIBILITY; COUPLED INTERACTION; DIFFERENTIAL BINDING; DIMER INTERFACE; HIGH AFFINITY LIGANDS; IMMUNE RESPONSE; INTERFACE INTERACTION; INTERLEUKIN-8; LOCALIZED EVENTS; NMR CHEMICAL SHIFTS; NMR DATA; NONSEQUENTIAL; PEAK INTENSITY; RECEPTOR COMPLEX; STRUCTURAL BASIS;

BINDING ENERGY; DISSOCIATION; LIGANDS; MONOMERS; NUCLEAR MAGNETIC RESONANCE; OLIGOMERS;

CONFORMATIONS;

CHEMOKINE RECEPTOR CXCR1; DIMER; INTERLEUKIN 8; MONOMER;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISSOCIATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN VARIANT; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; HUMANS; INTERLEUKIN-8; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-8A; SURFACE PROPERTIES; THERMODYNAMICS;

EID: 70349146698     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901194p     Document Type: Article

References (53)

1. Moser, B., Wolf, M., Walz, A., and Loetscher, P. (2004) Chemokines: multiple levels of leukocyte migration control. Trends Immunol. 25, 75-84. (Pubitemid 38167488)
2. Luster, A. D. (2002) The role of chemokines in linking innate and adaptive immunity. Curr. Opin. Immunol. 14, 129-135. (Pubitemid 34085117)
3. Gerard, C., and Rollins, B. J. (2001) Chemokines and disease. Nat. Immunol. 2, 108-115.
4. Rajarathnam, K. (2002) Designing decoys for chemokine-chemokine receptor interaction. Curr. Pharm. Des. 8, 2159-2169.
5. Luster, A.D. (1998) Chemokines - chemotactic cytokines that mediate inflammation. N. Engl. J.Med. 338, 436-445.
6. Clore, G. M., Appella, E., Yamada, M., Matsushima, K., and Gronenborn, A. M. (1990) Three-dimensional structure of interleukin 8 in solution. Biochemistry 29, 1689-1696.
7. 1H NMR solution structure of an active monomeric interleukin-8. Biochemistry 34, 12983-12990.
8. 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. (Pubitemid 44185505)
9. Clark-Lewis, I., Schumacher, C., Baggiolini, M., and Moser, B. (1991) Structure-activity relationships of interleukin-8 determined using chemically synthesized analogs. Critical role of NH2-terminal residues and evidence for uncoupling of neutrophil chemotaxis, exocytosis, and receptor binding activities. J. Biol. Chem. 266, 23128-23134. (Pubitemid 21908769)
10. 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. (Pubitemid 23111409)
11. 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. (Pubitemid 24209294)
12. 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. (Pubitemid 26190332)
13. 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. (Pubitemid 129518433)
14. 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. (Pubitemid 26137363)
15. 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. (Pubitemid 23105620)
16. Crump, M. P., Gong, J. H., Loetscher, P., Rajarathnam, K., Amara, A., Arenzana-Seisdedos, F., Virelizier, J. L., Baggiolini, M., Sykes, B. D., and Clark-Lewis, I. (1997) Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J. 16, 6996-7007. (Pubitemid 27520800)
17. 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. (Pubitemid 44730316)
18. 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. (Pubitemid 29159701)
19. 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.
20. 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.
21. Burrows, S. D., Doyle, M. L., Murphy, K. P., Franklin, S. G., White, J. R., Brooks, I., McNulty, D. E., Scott, M. O., Knutson, J. R., and Porter, D.; et al. (1994) Determination of the monomer-dimer equilibrium of interleukin-8 reveals it is a monomer at physiological concentrations. Biochemistry 33, 12741-12745. (Pubitemid 24352861)
22. Rajarathnam, K., Kay, C. M., Clark-Lewis, I., and Sykes, B. D. (1997) Characterization of quaternary structure of interleukin-8 and functional implications. Methods Enzymol. 287, 89-105. (Pubitemid 27430235)
23. Lowman, H. B., Fairbrother, W. J., Slagle, P. H., Kabakoff, R., Liu, J., Shire, S., and Hebert, C. A. (1997) Monomeric variants of IL-8: effects of side chain substitutions and solution conditions upon dimer formation. Protein Sci. 6, 598-608. (Pubitemid 27120056)
24. Rajagopalan, L., and Rajarathnam, K. (2004) Ligand selectivity and affinity of chemokine receptor CXCR1. Role of N-terminal domain. J. Biol. Chem. 279, 30000-30008. (Pubitemid 38937920)
25. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140.
26. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
27. Johnson, B. A., and Blevins, R. A. (1994) NMR View: a computer program for the visualization and analysis of NMR data. J. Biol. NMR 4, 603-614.
28. 15N NMR relaxation. Biochemistry 33, 5984-6003.
29. 15N NMR relaxation data. J. Biomol. NMR 36, 215-224.
30. Lian, L., and Roberts, G. C. K. (1993) Effects of chemical exchange on NMR spectra, in NMR of macromolecules. A practical approach (Roberts, G. C. K., Ed.) pp 153-182, Oxford University Press, Oxford, U.K.
31. Qin, J., Vinogradova, O., and Gronenborn, A. M. (2001) Protein-protein interactions probed by nuclear magnetic resonance spectroscopy. Methods Enzymol. 339, 377-389. (Pubitemid 32666570)
32. Reuben, J., and Fiat, D. (1969) Nuclear magnetic resonance studies of solutions of the rare-earth ions and their complexes. IV. Concentration and temperature dependence of the oxygen-17 transverse relaxation in aqueous solutions. J. Chem. Phys. 51, 10.
33. Hammond, M. E., Shyamala, V., Siani, M. A., Gallegos, C. A., Feucht, P. H., Abbott, J., Lapointe, G. R., Moghadam, M., Khoja, H., Zakel, J., and Tekamp-Olson, P. (1996) Receptor recognition and specificity of interleukin-8 is determined by residues that cluster near a surface-accessible hydrophobic pocket. J. Biol. Chem. 271, 8228-8235. (Pubitemid 26108654)
34. Schraufstatter, I. U., Ma, M., Oades, Z. G., Barritt, D. S., and Cochrane, C. G. (1995) The role of Tyr13 and Lys15 of interleukin-8 in the high affinity interaction with the interleukin-8 receptor type A. J. Biol. Chem. 270, 10428-10431.
35. Rajarathnam, K., Sykes, B. D., Dewald, B., Baggiolini, M., and Clark-Lewis, I. (1999) Disulfide bridges in interleukin-8 probed using non-natural disulfide analogues: dissociation of roles in structure from function. Biochemistry 38, 7653-7658. (Pubitemid 129515071)
36. Kuschert, G. S., Hoogewerf, A. J., Proudfoot, A. E., Chung, C. W., Cooke, R. M., Hubbard, R. E., Wells, T. N., and Sanderson, P. N. (1998) Identification of a glycosaminoglycan binding surface on human interleukin-8. Biochemistry 37, 11193-11201. (Pubitemid 28394867)
37. Clubb, R. T., Omichinski, J. G., Clore, G. M., and Gronenborn, A. M. (1994) Mapping the binding surface of interleukin-8 complexes with an N-terminal fragment of the type 1 human interleukin-8 receptor. FEBS Lett. 338, 93-97. (Pubitemid 24047789)
38. 15N relaxation measurements. J. Mol. Biol. 230, 364-372.
39. Fernando, H., Nagle, G. T., and Rajarathnam, K. (2007) Thermodynamic characterization of interleukin-8 monomer binding to CXCR1 receptor N-terminal domain. FEBS J. 274, 241-251. (Pubitemid 44952912)
40. Fernando, H., Chin, C., Rosgen, J., and Rajarathnam, K. (2004) Dimer dissociation is essential for interleukin-8 (IL-8) binding to CXCR1 receptor. J. Biol. Chem. 279, 36175-36178. (Pubitemid 39128951)
41. Shoemaker, B. A., Portman, J. J., and Wolynes, P. G. (2000) Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. U.S.A. 97, 8868-8873.
42. Duma, L., Haussinger, D., Rogowski, M., Lusso, P., and Grzesiek, S. (2007) Recognition of RANTES by extracellular parts of the CCR5 receptor. J. Mol. Biol. 365, 1063-1075. (Pubitemid 46014180)
43. Ye, J., Kohli, L. L., and Stone, M. J. (2000) Characterization of binding between the chemokine eotaxin and peptides derived from the chemokine receptor CCR3. J. Biol. Chem. 275, 27250-27257. (Pubitemid 30688082)
44. Mizoue, L. S., Bazan, J. F., Johnson, E. C., and Handel, T. M. (1999) Solution structure and dynamics of the CX3C chemokine domain of fractalkine and its interaction with an N-terminal fragment of CX3CR1. Biochemistry 38, 1402-1414. (Pubitemid 129502134)
45. Mayer, K. L., and Stone, M. J. (2000) NMR solution structure and receptor peptide binding of the CC chemokine eotaxin-2. Biochemistry 39, 8382-8395. (Pubitemid 30489935)
46. Booth, V., Keizer, D. W., Kamphuis, M. B., Clark-Lewis, I., and Sykes, B. D. (2002) The CXCR3 binding chemokine IP-10/CXCL10: structure and receptor interactions. Biochemistry 41, 10418-10425. (Pubitemid 34898398)
47. Veldkamp, C. T., Seibert, C., Peterson, F. C., Sakmar, T. P., and Volkman, B. F. (2006) Recognition of a CXCR4 sulfotyrosine by the chemokine stromal cell-derived factor-1alpha (SDF-1alpha/CXCL12). J. Mol. Biol. 359, 1400-1409. (Pubitemid 43903502)
48. Chuntharapai, A., and Kim, K. J. (1995) Regulation of the expression of IL-8 receptor A/B by IL-8: possible functions of each receptor. J. Immunol. 155, 2587-2594.
49. Veldkamp, C. T., Seibert, C., Peterson, F. C., De la Cruz, N. B., Haugner, J. C.III, Basnet, H., Sakmar, T. P., and Volkman, B. F. (2008) Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci. Signal. 1, ra4.
50. Jin, H., Shen, X., Baggett, B. R., Kong, X., and LiWang, P. J. (2007) The human CC chemokine MIP-1beta dimer is not competent to bind to the CCR5 receptor. J. Biol. Chem. 282, 27976-27983. (Pubitemid 47529496)
51. Proudfoot, A. E., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N., and Kosco-Vilbois, M. H. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl. Acad. Sci. U.S.A. 100, 1885-1890. (Pubitemid 36254543)
52. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
53. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003) VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 31, 3316-3319. (Pubitemid 37442148)