Design and receptor interactions of obligate dimeric mutant of chemokine monocyte chemoattractant protein-1 (MCP-1)

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14692-14702

  Tan, Joshua H Y ^a   Canals, Meritxell ^b   Ludeman, Justin P ^a   Wedderburn, Jamie ^a   Boston, Christopher ^c   Butler, Stephen J ^d   Carrick, Ann Marie ^c   Parody, Todd R ^c   Taleski, Deni ^d   Christopoulos, Arthur ^b   Payne, Richard J ^d   Stone, Martin J ^a  

^a MONASH UNIVERSITY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c INDIANA UNIVERSITY   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL ANALYSIS; CELL-BASED ASSAYS; CHEMOATTRACTANTS; CHEMOKINE RECEPTORS; CHEMOKINES; DIMER INTERFACE; IN-VIVO; ORDERS OF MAGNITUDE; RECEPTOR INTERACTION; WILD TYPES;

BODY FLUIDS; PEPTIDES;

DIMERS;

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR2; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOMER; THREONINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; DIMERIZATION; GEL PERMEATION CHROMATOGRAPHY; MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE;

AMINO ACID SUBSTITUTION; CELL LINE; CHEMOKINE CCL2; HUMANS; MUTATION, MISSENSE; PROTEIN MULTIMERIZATION; RECEPTORS, CCR2;

EID: 84860356196     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.334201     Document Type: Article

References (33)

1. Lau, E. K., Allen, S., Hsu, A. R., and Handel, T. M. (2004) Chemokine receptor interactions. GPCRs, glycosaminoglycans, and viral chemokine-binding proteins. Adv. Protein Chem. 68, 141-153
2. Lodi, P. J., Garrett, D. S., Kuszewski, J., Tsang, M. L., Weatherbee, J. A., Leonard, W. J., Gronenborn, A. M., and Clore, G. M. (1994) High resolution solution structure of the β-chemokine hMIP-1β by multidimensional NMR. Science 263, 1762-1767 (Pubitemid 24131585)
3. 15N) NMR assignments and solution structure of the monocyte chemoattractant protein-1 (MCP-1) dimer. Biochemistry 35, 6569-6584
4. Chung, C. W., Cooke, R. M., Proudfoot, A. E., and Wells, T. N. (1995) The three-dimensional solution structure of RANTES. Biochemistry 34, 9307-9314
5. 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 (Pubitemid 20074708)
6. Laurence, J. S., Blanpain, C., Burgner, J. W., Parmentier, M., and LiWang, P. J. (2000) CC chemokine MIP-1 β can function as a monomer and depends on Phe-13 for receptor binding. Biochemistry 39, 3401-3409 (Pubitemid 30170011)
7. Paavola, C. D., Hemmerich, S., Grunberger, D., Polsky, I., Bloom, A., Freedman, R., Mulkins, M., Bhakta, S., McCarley, D., Wiesent, L., Wong, B., Jarnagin, K., and Handel, T. M. (1998) Monomeric monocyte chemoattractant protein-1 (MCP-1) binds and activates the MCP-1 receptor CCR2B. J. Biol. Chem. 273, 33157-33165 (Pubitemid 29005686)
8. Rajarathnam, K., Sykes, B. D., Kay, C. M., Dewald, B., Geiser, T., Baggiolini, M., and Clark-Lewis, I. (1994) Neutrophil activation by monomeric interleukin-8. Science 264, 90-92 (Pubitemid 24144491)
9. Wells, T. N., Power, C. A., Lusti-Narasimhan, M., Hoogewerf, A. J., Cooke, R. M., Chung, C. W., Peitsch, M. C., and Proudfoot, A. E. (1996) Selectivity and antagonism of chemokine receptors. J. Leukocyte Biol. 59, 53-60 (Pubitemid 26057473)
10. Paolini, J. F., Willard, D., Consler, T., Luther, M., and Krangel, M. S. (1994) The chemokines IL-8, monocyte chemoattractant protein-1, and I-309 are monomers at physiologically relevant concentrations. J. Immunol. 153, 2704-2717 (Pubitemid 24278140)
11. 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)
12. Das, S. T., Rajagopalan, L., Guerrero-Plata, A., Sai, J., Richmond, A., Garofalo, R. P., and Rajarathnam, K. (2010) Monomeric and dimeric CXCL8 are both essential for in vivo neutrophil recruitment. PLoS ONE 5, e11754
13. 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)
14. Nasser, M. W., Raghuwanshi, S. K., Grant, D. J., Jala, V. R., Rajarathnam, K., and Richardson, R. M. (2009) Differential activation and regulation of CXCR1 and CXCR2 by CXCL8 monomer and dimer. J. Immunol. 183, 3425-3432
15. Ravindran, A., Joseph, P. R., and Rajarathnam, K. (2009) Structural basis for differential binding of the interleukin-8 monomer and dimer to the CXCR1 N-domain. Role of coupled interactions and dynamics. Biochemistry 48, 8795-8805
16. Duma, L., Haüssinger, 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)
17. Jin, H., Shen, X., Baggett, B. R., Kong, X., and LiWang, P. J. (2007) The human CC chemokine MIP-1β dimer is not competent to bind to the CCR5 receptor. J. Biol. Chem. 282, 27976-27983 (Pubitemid 47529496)
18. Zhang, Y., and Rollins, B. (1995) A dominant negative inhibitor indicates that monocyte chemoattractant protein 1 functions as a dimer. Mol. Cell. Biol. 15, 4851-4855
19. Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfield, E., Markley, J. L., and Sykes, B. D. (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6, 135-140
20. Taleski, D., Butler, S. J., Stone, M. J., and Payne, R. J. (2011) Divergent and site-selective solid-phase synthesis of sulfopeptides. Chem. Asian J. 6, 1316-1320
21. Mayer, M. R., Parody, T. R., Datta-Mannan, A., and Stone, M. J. (2004) Specificity determinants for chemokine recognition identified using eotaxin-MCP-1 chimeras. FEBS Lett. 571, 166-170 (Pubitemid 38992942)
22. Parody, T. R., and Stone, M. J. (2004) High level expression, activation, and antagonism of CC chemokine receptors CCR2 and CCR3 in Chinese hamster ovary cells. Cytokine 27, 38-46 (Pubitemid 38780935)
23. Hemmerich, S., Paavola, C., Bloom, A., Bhakta, S., Freedman, R., Grun-berger, D., Krstenansky, J., Lee, S., McCarley, D., Mulkins, M., Wong, B., Pease, J., Mizoue, L., Mirzadegan, T., Polsky, I., Thompson, K., Handel, T. M., and Jarnagin, K. (1999) Identification of residues in the monocyte chemotactic protein-1 that contact the MCP-1 receptor, CCR2. Biochemistry 38, 13013-13025
24. Jarnagin, K., Grunberger, D., Mulkins, M., Wong, B., Hemmerich, S., Paavola, C., Bloom, A., Bhakta, S., Diehl, F., Freedman, R., McCarley, D., Polsky, I., Ping-Tsou, A., Kosaka, A., and Handel, T. M. (1999) Identification of surface residues of the monocyte chemotactic protein 1 that affect signaling through the receptor CCR2. Biochemistry 38, 16167-16177 (Pubitemid 129520537)
25. Clubb, R. T., Omichinski, J. G., Clore, G. M., and Gronenborn, A. M. (1994) Mapping the binding surface of interleukin-8 complexed with an N-terminal fragment of the type 1 human interleukin-8 receptor. FEBS Lett. 338, 93-97
26. Monteclaro, F. S., and Charo, I. F. (1997) The amino-terminal domain of CCR2 is both necessary and sufficient for high affinity binding of monocyte chemoattractant protein 1. Receptor activation by a pseudo-tethered ligand. J. Biol. Chem. 272, 23186-23190 (Pubitemid 27392450)
27. 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)
28. Veldkamp, C. T., Seibert, C., Peterson, F. C., De la Cruz, N. B., Haugner, J. C., 3rd, 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
29. 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-1α (SDF-1α/CXCL12). J. Mol. Biol. 359, 1400-1409 (Pubitemid 43903502)
30. Mayer, K. L., and Stone, M. J. (2000)NMRsolution structure and receptor peptide binding of the CC chemokine eotaxin-2. Biochemistry 39, 8382-8395 (Pubitemid 30489935)
31. Simpson, L. S., Zhu, J. Z., Widlanski, T. S., and Stone, M. J. (2009) Regulation of chemokine recognition by site-specific tyrosine sulfation of receptor peptides. Chem. Biol. 16, 153-161
32. 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
33. Zhu, J. Z., Millard, C. J., Ludeman, J. P., Simpson, L. S., Clayton, D. J., Payne, R. J., Widlanski, T. S., and Stone, M. J. (2011) Tyrosine sulfation influences the chemokine binding selectivity of peptides derived from chemokine receptor CCR3. Biochemistry 50, 1524-1534