MIF-chemokine receptor interactions in atherogenesis are dependent on an N-loop-based 2-site binding mechanism

FASEB Journal

Volumn 25, Issue 3, 2011, Pages 894-906

  Kraemer, Sandra ^a   Lue, Hongqi ^a   Zernecke, Alma ^b   Kapurniotu, Aphrodite ^c   Andreetto, Erika ^c   Frank, Ronald ^d   Lennartz, Birgitt ^a   Weber, Christian ^e   Bernhagen, Jürgen ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^e LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

CLF chemokine; Cytokine; Domain analysis; G protein coupled receptor; Structure activity analysis

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR2; MACROPHAGE MIGRATION INHIBITION FACTOR;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BINDING SITE; CELL ADHESION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LEUKOCYTE; MONOCYTE; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS;

EID: 79954573511     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-168559     Document Type: Article

References (75)

1. Thelen, M. (2001) Dancing to the tune of chemokines. Nat. Immunol. 2, 129-134 (Pubitemid 33707930)
2. Moser, B., Wolf, M., Walz, A., and Loetscher, P. (2004) Chemokines: multiple levels of leukocyte migration control. Trends Immunol. 25, 75-84 (Pubitemid 38167488)
3. Charo, I. F., and Ransohoff, R. M. (2006) The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354, 610-621 (Pubitemid 43209108)
4. Moser, B., and Loetscher, P. (2001) Lymphocyte traffic control by chemokines. Nat. Immunol. 2, 123-128 (Pubitemid 33707929)
5. Sallusto, F., and Baggiolini, M. (2008) Chemokines and leukocyte traffic. Nat. Immunol. 9, 949-952
6. Baggiolini, M. (2001) Chemokines in pathology and medicine. J. Intern. Med. 250, 91-104 (Pubitemid 32868689)
7. Libby, P. (2002) Inflammation in atherosclerosis. Nature 420, 868-874 (Pubitemid 36019640)
8. Lusis, A. J. (2000) Insight review article: atherosclerosis. Nature 407, 233-241
9. Balkwill, F. (2004) Cancer and the chemokine network. Nat. Rev. Cancer 4, 540-550 (Pubitemid 38868623)
10. Murphy, P. M., Baggiolini, M., Charo, I. F., Hebert, C. A., Horuk, R., Matsushima, K., Miller, L. H., Oppenheim, J. J., and Power, C. A. (2000) International union of pharmacology. XXII. Nomenclature for chemokine receptors. Pharmacol. Rev. 52, 145-176 (Pubitemid 30127598)
11. Mantovani, A. (1999) The chemokine system: redundancy for robust outputs. Immunol. Today 20, 254-257 (Pubitemid 29258161)
12. Fernandez, E. J., and Lolis, E. (2002) Structure, function, and inhibition of chemokines. Annu. Rev. Pharmacol. Toxicol. 42, 469-499 (Pubitemid 34160533)
13. Luster, A. D. (1998) Chemokines-chemotactic cytokines that mediate inflammation. N. Engl. J. Med. 338, 436-445 (Pubitemid 28135672)
14. Handel, T. M., and Domaille, P. J. (1996) Heteronuclear (1H, 13C, 15N) NMR assignments and solution structure of the monocyte chemoattractant protein-1 (MCP-1) dimer. Biochemistry 35, 6569-6584
15. 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)
16. Skelton, N. J., Aspiras, F., Ogez, J., and Schall, T. J. (1995) Proton NMR assignments and solution conformation of RANTES, a chemokine of the C-C type. Biochemistry 34, 5329-5342
17. 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)
18. Qian, Y. Q., Johanson, K. O., and McDevitt, P. (1999) Nuclear magnetic resonance solution structure of truncated human GRObeta [5-73] and its structural comparison with CXC chemokine family members GROalpha and IL-8. J. Mol. Biol. 294, 1065-1072 (Pubitemid 30008781)
19. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739-745 (Pubitemid 30650186)
20. Rasmussen, S. G., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I., and Kobilka, B. K. (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450, 383-387 (Pubitemid 350126755)
21. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265 (Pubitemid 350172884)
22. Jaakola, V. P., Griffith, M. T., Hanson, M. A., Cherezov, V., Chien, E. Y., Lane, J. R., Ijzerman, A. P., and Stevens, R. C. (2008) The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322, 1211-1217
23. Serrano-Vega, M. J., Magnani, F., Shibata, Y., and Tate, C. G. (2008) Conformational thermostabilization of the beta1-adrenergic receptor in a detergent-resistant form. Proc. Natl. Acad. Sci. U. S. A. 105, 877-882 (Pubitemid 351282049)
24. Ahuja, S. K., and Murphy, P. M. (1996) The CXC chemokines growth-regulated oncogene (GRO) alpha, GRObeta, GROgamma, 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 (Pubitemid 26281830)
25. Katancik, J. A., Sharma, A., and de Nardin, E. (2000) Interleukin 8, neutrophil-activating peptide-2 and GRO-alpha bind to and elicit cell activation via specific and different amino acid residues of CXCR2. Cytokine 12, 1480-1488
26. Blanpain, C., Doranz, B. J., Bondue, A., Govaerts, C., De Leener, A., Vassart, G., Doms, R. W., Proudfoot, A., and Parmentier, M. (2003) The core domain of chemokines binds CCR5 extracellular domains while their amino terminus interacts with the transmembrane helix bundle. J. Biol. Chem. 278, 5179-5187 (Pubitemid 36801030)
27. 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
28. 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)
29. Rajagopalan, L. R. K. (2006) Structural basis of chemokine receptor function-a model for binding affinity and ligand selectivity. Biosci. Rep. 26, 325-339
30. 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)
31. 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)
32. 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)
33. 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)
34. Degryse, B., and de Virgilio, M. (2003) The nuclear protein HMGB1, a new kind of chemokine? FEBS Lett. 553, 11-17 (Pubitemid 37206316)
35. Noels, H., Bernhagen, J., and Weber, C. (2009) Macrophage migration inhibitory factor: a noncanonical chemokine important in atherosclerosis. Trends Cardiovasc. Med. 19, 76-86
36. Yang, D., Chertov, O., Bykovskaia, S. N., Chen, Q., Buffo, M. J., Shogan, J., Anderson, M., Schroder, J. M., Wang, J. M., Howard, O. M., and Oppenheim, J. J. (1999) Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286, 525-528
37. David, J. R. (1966) Delayed hypersensitivity in vitro: its mediation by cell-free substances formed by lymphoid cell-antigen interaction. Proc. Natl. Acad. Sci. U. S. A. 56, 72-77
38. Calandra, T., and Roger, T. (2003) Macrophage migration inhibitory factor: A regulator of innate immunity. Nat. Rev. Immunol. 3, 791-800 (Pubitemid 37328657)
39. Morand, E. F., Leech, M., and Bernhagen, J. (2006) MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis. Nat. Rev. Drug Discov. 5, 399-410
40. Zernecke, A., Bernhagen, J., and Weber, C. (2008) Macrophage migration inhibitory factor in cardiovascular disease. Circulation 117, 1594-1602 (Pubitemid 351440647)
41. Burger-Kentischer, A., Goebel, H., Seiler, R., Fraedrich, G., Schaefer, H. E., Dimmeler, S., Kleemann, R., Bernhagen, J., and Ihling, C. (2002) Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation 105, 1561-1566 (Pubitemid 34297633)
42. Bernhagen, J., Krohn, R., Lue, H., Gregory, J. L., Zernecke, A., Koenen, R. R., Dewor, M., Georgiev, I., Schober, A., Leng, L., Kooistra, T., Fingerle-Rowson, G., Ghezzi, P., Kleemann, R., McColl, S. R., Bucala, R., Hickey, M. J., and Weber, C. (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat. Med. 13, 587-596 (Pubitemid 46828480)
43. Weber, C., Kraemer, S., Drechsler, M., Lue, H., Koenen, R. R., Kapurniotu, A., Zernecke, A., and Bernhagen, J. (2008) Structural determinants of MIF functions in CXCR2-mediated inflammatory and atherogenic leukocyte recruitment. Proc. Natl. Acad. Sci. U. S. A. 105, 16278-16283
44. Weber, C., Aepfelbacher, M., Haag, H., Ziegler-Heitbrock, H. W., and Weber, P. C. (1993) Tumor necrosis factor induces enhanced responses to platelet-activating factor and differentiation in human monocytic Mono Mac 6 cells. Eur. J. Immunol. 23, 852-859 (Pubitemid 23101069)
45. Bernhagen, J., Mitchell, R. A., Calandra, T., Voelter, W., Cerami, A., and Bucala, R. (1994) Purification, bioactivity, and secondary structure analysis of mouse and human macrophage migration Inhibitory factor (MIF). Biochemistry 33, 14144-14155 (Pubitemid 24382359)
46. Frank, R. (1992) Spot-synthesis: an easy technique for the positionally adressable, parallel chemical synthesis on a membrane support. Tetrahedron 48, 9217-9232
47. Frank, R., and Overwin, H. (1996) SPOT synthesis. Epitope analysis with arrays of synthetic peptides prepared on cellulose membranes. Methods Mol. Biol. 66, 149-169
48. Andreetto, E., Yan, L. M., Tatarek-Nossol, M., Velkova, A., Frank, R., and Kapurniotu, A. (2010) Identification of hot regions of the Abeta-IAPP interaction interface as high-affinity binding sites in both cross-and self-association. Angew. Chem. Int. Ed. Engl. 49, 3081-3085
49. Prado, G. N., Suetomi, K., Shumate, D., Maxwell, C., Ravindran, A., Rajarathnam, K., and Navarro, J. (2007) Chemokine signaling specificity: essential role for the N-terminal domain of chemokine receptors. Biochemistry 46, 8961-8968 (Pubitemid 47237371)
50. Sun, H., Bernhagen, J., Bucala, R., and Lolis, E. (1996) Crystal structure at 2.6 Å resolution of human macrophage migration inhibitory factor. Proc. Natl. Acad. Sci. U. S. A. 93, 5191-5196
51. 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 (Pubitemid 21908180)
52. 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 (Pubitemid 24233454)
53. Huang, X., Shen, J., Cui, M., Shen, L., Luo, X., Ling, K., Pei, G., Jiang, H., and Chen, K. (2003) Molecular dynamics simulations on SDF-1alpha: binding with CXCR4 receptor. Biophys. J. 84, 171-184 (Pubitemid 36026388)
54. Huynh, N., Mallik, B., Zhang, L., Martins-Green, M., and Morikis, D. (2008) Computational studies of CXCR1, the receptor of IL-8/CXCL8, using molecular dynamics and electrostatics. Biopolymers 89, 52-61
55. Farzan, M., Mirzabekov, T., Kolchinsky, P., Wyatt, R., Cayabyab, M., Gerard, N. P., Gerard, C., Sodroski, J., and Choe, H. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96, 667-676 (Pubitemid 29122809)
56. Farzan, M., Babcock, G. J., Vasilieva, N., Wright, P. L., Kiprilov, E., Mirzabekov, T., and Choe, H. (2002) The role of posttranslational modifications of the CXCR4 amino terminus in stromal-derived factor 1 alpha association and HIV-1 entry. J. Biol. Chem. 277, 29484-29489 (Pubitemid 41079234)
57. 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
58. 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)
59. Cormier, E. G., Persuh, M., Thompson, D. A., Lin, S. W., Sakmar, T. P., Olson, W. C., and Dragic, T. (2000) Specific interaction of CCR5 amino-terminal domain peptides containing sulfotyrosines with HIV-1 envelope glycoprotein gp120. Proc. Natl. Acad. Sci. U. S. A. 97, 5762-5767 (Pubitemid 30367472)
60. Hoover, D. M., Boulegue, C., Yang, D., Oppenheim, J. J., Tucker, K., Lu, W., and Lubkowski, J. (2002) The structure of human macrophage inflammatory protein-3alpha/CCL20. Linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J. Biol. Chem. 277, 37647-37654
61. Perez-Canadillas, J. M., Zaballos, A., Gutierrez, J., Varona, R., Roncal, F., Albar, J. P., Marquez, G., and Bruix, M. (2001) NMR solution structure of murine CCL20/MIP-3alpha, a chemokine that specifically chemoattracts immature dendritic cells and lymphocytes through its highly specific interaction with the beta-chemokine receptor CCR6. J. Biol. Chem. 276, 28372-28379
62. Yang, D., Chen, Q., Hoover, D. M., Staley, P., Tucker, K. D., Lubkowski, J., and Oppenheim, J. J. (2003) Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J. Leukoc. Biol. 74, 448-455 (Pubitemid 38040406)
63. Taylor, K., Clarke, D. J., McCullough, B., Chin, W., Seo, E., Yang, D., Oppenheim, J., Uhrin, D., Govan, J. R., Campopiano, D. J., MacMillan, D., Barran, P., and Dorin, J. R. (2008) Analysis and separation of residues important for the chemoattractant and antimicrobial activities of beta-defensin 3. J. Biol. Chem. 283, 6631-6639
64. Wakasugi, K., and Schimmel, P. (1999) Two distinct cytokines released from a human aminoacyl-tRNA synthetase. Science 284, 147-151 (Pubitemid 29282068)
65. Howard, O. M., Dong, H. F., Yang, D., Raben, N., Nagaraju, K., Rosen, A., Casciola-Rosen, L., Hartlein, M., Kron, M., Yang, D., Yiadom, K., Dwivedi, S., Plotz, P. H., and Oppenheim, J. J. (2002) Histidyl-tRNA synthetase and asparaginyl-tRNA synthetase, autoantigens in myositis, activate chemokine receptors on T lymphocytes and immature dendritic cells. J. Exp. Med. 196, 781-791
66. Bertini, R., Howard, O. M. Z., Dong, H.-F., Oppenheim, J. J., Bizzarri, C., Caselli, G., Pagliei, S., Romines, B., Wilshire, J. A., Mengozzi, M., Nakamura, H., Yodoi, J., Pekkari, K., Gurunath, R., Holmgren, A., Herzenberg, L. A., Herzenberg, L. A., and Ghezzi, P. (1999) Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells. J. Exp. Med. 189, 1783-1789 (Pubitemid 29272695)
67. Loetscher, P., Gong, J. H., Dewald, B., Baggiolini, M., and Clark-Lewis, I. (1998) N-terminal peptides of stromal cellderived factor-1 with CXC chemokine receptor 4 agonist and antagonist activities. J. Biol. Chem. 273, 22279-22283 (Pubitemid 28399785)
68. Gong, J. H., Uguccioni, M., Dewald, B., Baggiolini, M., and Clark-Lewis, I. (1996) RANTES and MCP-3 antagonists bind multiple chemokine receptors. J. Biol. Chem. 271, 10521-10527 (Pubitemid 26145785)
69. Pakianathan, D. R., Kuta, E. G., Artis, D. R., Skelton, N. J., and Hebert, C. A. (1997) Distinct but overlapping epitopes for the interaction of a CC-chemokine with CCR1, CCR3 and CCR5. Biochemistry 36, 9642-9648 (Pubitemid 27364674)
70. Gayle, R. B., 3rd, 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)
71. 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
72. 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)
73. Schwartz, V., Lue, H., Kraemer, S., Korbiel, J., Krohn, R., Ohl, K., Bucala, R., Weber, C., and Bernhagen, J. (2009) A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett. 583, 2749-2757
74. Heveker, N., Tissot, M., Thuret, A., Schneider-Mergener, J., Alizon, M., Roch, M., and Marullo, S. (2001) Pharmacological properties of peptides derived from stromal cell-derived factor 1: study on human polymorphonuclear cells. Mol. Pharmacol. 59, 1418-1425 (Pubitemid 32510106)
75. Donzella, G. A., Schols, D., Lin, S. W., Este, J. A., Nagashima, K. A., Maddon, P. J., Allaway, G. P., Sakmar, T. P., Henson, G., De Clercq, E., and Moore, J. P. (1998) AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4, 72-77 (Pubitemid 28133082)