Chemokine oligomerization and interactions with receptors and glycosaminoglycans: The role of structural dynamics in function

Experimental Cell Research

Volumn 317, Issue 5, 2011, Pages 590-601

  Salanga, C L ^a   Handel, T M ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Chemokine structure; Glycosaminoglycans; Oligomerization; Receptor structure; Structural plasticity

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; GLYCOSAMINOGLYCAN; INTERLEUKIN 8; MONOMER; OLIGOMER; STROMAL CELL DERIVED FACTOR 1;

AMINO TERMINAL SEQUENCE; COMPLEX FORMATION; HUMAN; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

EID: 79952105330     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.01.004     Document Type: Review

References (86)

1. Baggiolini M. Chemokines and leukocyte traffic. Nature 1998, 392:565-568.
2. Sallusto F., Baggiolini M. Chemokines and leukocyte traffic. Nat. Immunol. 2008, 9:949-952.
3. Webb L.M., Ehrengruber M.U., Clark-Lewis I., Baggiolini M., Rot A. Binding to heparan sulfate or heparin enhances neutrophil responses to interleukin 8. Proc. Natl Acad. Sci. USA 1993, 90:7158-7162.
4. Luster A.D., Greenberg S.M., Leder P. The Ip-10 chemokine binds to a specific cell-surface heparan-sulfate site shared with platelet factor-4 and inhibits endothelial-cell proliferation. J. Exp. Med. 1995, 182:219-231.
5. Middleton J., Neil S., Wintle J., Clark-Lewis I., Moore H., Lam C., Auer M., Hub E., Rot A. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 1997, 91:385-395.
6. Middleton J., Patterson A.M., Gardner L., Schmutz C., Ashton B.A. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 2002, 100:3853-3860.
7. Wang L., Fuster M., Sriramarao P., Esko J.D. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 2005, 6:902-910.
8. Bishop J.R., Schuksz M., Esko J.D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007, 446:1030-1037.
9. Alon R., Grabovsky V., Feigelson S. Chemokine induction of integrin adhesiveness on rolling and arrested leukocytes local signaling events or global stepwise activation?. Microcirculation 2003, 10:297-311.
10. Campbell J.J., Hedrick J., Zlotnik A., Siani M.A., Thompson D.A., Butcher E.C. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 1998, 279:381-384.
11. Rajarathnam K., Sykes B.D., Kay C.M., Dewald B., Geiser T., Baggiolini M., Clark-Lewis I. Neutrophil activation by monomeric interleukin-8. Science 1994, 264:90-92.
12. Appay V., Brown A., Cribbes S., Randle E., Czaplewski L.G. Aggregation of RANTES is responsible for its inflammatory properties. Characterization of nonaggregating, noninflammatory RANTES mutants. J. Biol. Chem. 1999, 274:27505-27512.
13. Appay V., Dunbar P.R., Cerundolo V., McMichael A., Czaplewski L., Rowland-Jones S. RANTES activates antigen-specific cytotoxic T lymphocytes in a mitogen-like manner through cell surface aggregation. Int. Immunol. 2000, 12:1173-1182.
14. Kim K.S., Rajarathnam K., Clark-Lewis I., Sykes B.D. Structural characterization of a monomeric chemokine: monocyte chemoattractant protein-3. FEBS Lett. 1996, 395:277-282.
15. Mizoue L.S., Bazan J.F., Johnson E.C., Handel T.M. Solution structure and dynamics of the CX3C chemokine domain of fractalkine and its interaction with an N-terminal fragment of CX3CR1. Biochemistry 1999, 38:1402-1414.
16. Lodi P.J., Garrett D.S., Kuszewski J., Tsang M.L., Weatherbee J.A., Leonard W.J., Gronenborn A.M., Clore G.M. High-resolution solution structure of the beta chemokine hMIP-1 beta by multidimensional NMR. Science 1994, 263:1762-1767.
17. Kuloglu E.S., McCaslin D.R., Kitabwalla M., Pauza C.D., Markley J.L., Volkman B.F. Monomeric solution structure of the prototypical 'C' chemokine lymphotactin. Biochemistry 2001, 40:12486-12496.
18. Handel T.M., Domaille P.J. Heteronuclear (1H, 13C, 15N) NMR assignments and solution structure of the monocyte chemoattractant protein-1 (MCP-1) dimer. Biochemistry 1996, 35:6569-6584.
19. Booth V., Clark-Lewis I., Sykes B.D. NMR structure of CXCR3 binding chemokine CXCL11. Protein Sci. 2004, 13:2022-2028.
20. Allen S.J., Crown S.E., Handel T.M. Chemokine: receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 2007, 25:787-820.
21. Fernandez E.J., Lolis E. Structure, function, and inhibition of chemokines. Annu. Rev. Pharmacol. Toxicol. 2002, 42:469-499.
22. Bacon K., Baggiolini M., Broxmeyer H., Horuk R., Lindley I., Mantovani A., Maysushima K., Murphy P., Nomiyama H., Oppenheim J., Rot A., Schall T., Tsang M., Thorpe R., Van Damme J., Wadhwa M., Yoshie O., Zlotnik A., Zoon K. Chemokine/chemokine receptor nomenclature. J. Interferon Cytokine Res. 2002, 22:1067-1068.
23. Tuinstra R.L., Peterson F.C., Kutlesa S., Elgin E.S., Kron M.A., Volkman B.F. Interconversion between two unrelated protein folds in the lymphotactin native state. Proc. Natl Acad. Sci. USA 2008, 105:5057-5062.
24. Hoogewerf A.J., Kuschert G.S., Proudfoot A.E., Borlat F., Clark-Lewis I., Power C.A., Wells T.N. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 1997, 36:13570-13578.
25. Lau E.K., Paavola C.D., Johnson Z., Gaudry J.P., Geretti E., Borlat F., Kungl A.J., Proudfoot A.E., Handel T.M. Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1: implications for structure and function in vivo. J. Biol. Chem. 2004, 279:22294-22305.
26. Zhang X., Chen L., Bancroft D.P., Lai C.K., Maione T.E. Crystal structure of recombinant human platelet factor 4. Biochemistry 1994, 33:8361-8366.
27. Skelton N.J., Aspiras F., Ogez J., Schall T.J. Proton NMR assignments and solution conformation of RANTES, a chemokine of the C-C type. Biochemistry 1995, 34:5329-5342.
28. Ren M., Guo Q., Guo L., Lenz M., Qian F., Koenen R.R., Xu H., Schilling A.B., Weber C., Ye R.D., Dinner A.R., Tang W.J. Polymerization of MIP-1 chemokine (CCL3 and CCL4) and clearance of MIP-1 by insulin-degrading enzyme. EMBO J. 2010, 29:3952-3966.
29. Veldkamp C.T., Peterson F.C., Pelzek A.J., Volkman B.F. The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 2005, 14:1071-1081.
30. Paavola C., Hemmerich S., Grunberger D., Polsky I., Bloom A., Freedman R., Mulkins M., Bhakta S., McCarley D., Wiesent L., Wong B., Jarnagin K., Handel T.M. Monomeric monocyte chemoattractant protein-1 (MCP-1) binds and activates the MCP-1 receptor CCR2B. J. Biol. Chem. 1998, 273:33157-33165.
31. Jansma A.L., Kirkpatrick J.P., Hsu A.R., Handel T.M., Nietlispach D. NMR analysis of the structure, dynamics, and unique oligomerization properties of the chemokine CCL27. J. Biol. Chem. 2010, 285:14424-14437.
32. Proudfoot A.E.I., Handel T.M., Johnson Z., Lau E.K., LiWang P., Clark-Lewis I., Borlat F., Wells T.N.C., Kosco-Vilbois M.H. Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines. Proc. Natl Acad. Sci. USA 2003, 100:1885-1890.
33. Laurence J.S., Blanpain C., Burgner J.W., Parmentier M., LiWang P.J. CC chemokine MIP-1 beta can function as a monomer and depends on Phe13 for receptor binding. Biochemistry 2000, 39:3401-3409.
34. Handel T.M., Johnson Z., Rodrigues D.H., Dos Santos A.C., Cirillo R., Muzio V., Riva S., Mack M., Deruaz M., Borlat F., Vitte P.A., Wells T.N., Teixeira M.M., Proudfoot A.E. An engineered monomer of CCL2 has anti-inflammatory properties emphasizing the importance of oligomerization for chemokine activity in vivo. J. Leukoc. Biol. 2008, 84:1101-1108.
35. Campanella G.S., Grimm J., Manice L.A., Colvin R.A., Medoff B.D., Wojtkiewicz G.R., Weissleder R., Luster A.D. Oligomerization of CXCL10 is necessary for endothelial cell presentation and in vivo activity. J. Immunol. 2006, 177:6991-6998.
36. Veldkamp C.T., Seibert C., Peterson F.C., De la Cruz N.B., Haugner J.C., Basnet H., Sakmar T.P., Volkman B.F. Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12. Sci. Signal. 2008, 1:ra4.
37. Das S.T., Rajagopalan L., Guerrero-Plata A., Sai J., Richmond A., Garofalo R.P., Rajarathnam K. Monomeric and dimeric CXCL8 are both essential for in vivo neutrophil recruitment. PLoS One 2010, 5:e11754.
38. Baltus T., Weber K.S., Johnson Z., Proudfoot A.E., Weber C. Oligomerization of RANTES is required for CCR1-mediated arrest but not CCR5-mediated transmigration of leukocytes on inflamed endothelium. Blood 2003, 102:1985-1988.
39. von Hundelshausen P., Koenen R.R., Sack M., Mause S.F., Adriaens W., Proudfoot A.E., Hackeng T.M., Weber C. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005, 105:924-930.
40. Clark-Lewis I., Dewald B., Loetscher M., Moser B., Baggiolini M. Structural requirements for interleukin-8 function identified by design of analogs and CXC chemokine hybrids. J. Biol. Chem. 1994, 269:16075-16081.
41. Clark-Lewis I., Kim K.S., Rajarathnam K., Gong J.H., Dewald B., Moser B., Baggiolini M., Sykes B.D. Structure-activity relationships of chemokines. J. Leukoc. Biol. 1995, 57:703-711.
42. Loetscher P., Clark-Lewis I. Agonistic and antagonistic activities of chemokines. J. Leukoc. Biol. 2001, 69:881-884.
43. Mizoue L.S., Sullivan S.K., King D.S., Kledal T.N., Schwartz T.W., Bacon K.B., Handel T.M. Molecular determinants of receptor binding and signaling by the CX3C chemokine fractalkine. J. Biol. Chem. 2001, 276:33906-33914.
44. Clark-Lewis I., Schumacher C., Baggiolini M., Moser B. 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. 1991, 266:23128-23134.
45. 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., Handel T.M. Identification of surface residues of the monocyte chemotactic protein 1 that affect signaling through the receptor CCR2. Biochemistry 1999, 38:16167-16177.
46. Detheux M., Standker L., Vakili J., Munch J., Forssmann U., Adermann K., Pohlmann S., Vassart G., Kirchhoff F., Parmentier M., Forssmann W.G. Natural proteolytic processing of hemofiltrate CC chemokine 1 generates a potent CC chemokine receptor (CCR)1 and CCR5 agonist with anti-HIV properties. J. Exp. Med. 2000, 192:1501-1508.
47. Proost P., Struyf S., Van Damme J. Natural post-translational modifications of chemokines. Biochem. Soc. Trans. 2006, 34:997-1001.
48. Hemmerich S., Paavola C., Bloom A., Bhakta S., Freedman R., Grunberger D., Krstenansky J., Lee S., McCarley D., Mulkins M., Wong B., Pease J., Mizoue L., Mirzadegan T., Polsky I., Thompson K., Handel T.M., Jarnagin K. Identification of residues in the monocyte chemotactic protein-1 that contact the MCP-1 receptor, CCR2. Biochemistry 1999, 38:13013-13025.
49. Proudfoot A.E., Power C.A., Hoogewerf A.J., Montjovent M.O., Borlat F., Offord R.E., Wells T.N. Extension of recombinant human RANTES by the retention of the initiating methionine produces a potent antagonist. J. Biol. Chem. 1996, 271:2599-2603.
50. Gaertner H., Cerini F., Escola J.M., Kuenzi G., Melotti A., Offord R., Rossitto-Borlat I., Nedellec R., Salkowitz J., Gorochov G., Mosier D., Hartley O. Highly potent, fully recombinant anti-HIV chemokines: reengineering a low-cost microbicide. Proc. Natl Acad. Sci. USA 2008, 105:17706-17711.
51. Hartley O., Offord R.E. Engineering chemokines to develop optimized HIV inhibitors. Curr. Protein Pept. Sci. 2005, 6:207-219.
52. Pastore C., Picchio G.R., Galimi F., Fish R., Hartley O., Offord R.E., Mosier D.E. Two mechanisms for human immunodeficiency virus type 1 inhibition by N-terminal modifications of RANTES. Antimicrob. Agents Chemother. 2003, 47:509-517.
53. Blanpain C., Doranz B.J., Bondue A., Govaerts C., De Leener A., Vassart G., Doms R.W., Proudfoot A., Parmentier M. The core domain of chemokines binds CCR5 extracellular domains while their amino terminus interacts with the transmembrane helix bundle. J. Biol. Chem. 2003, 278:5179-5187.
54. Hanson M.A., Stevens R.C. Discovery of new GPCR biology: one receptor structure at a time. Structure 2009, 17:8-14.
55. Wells T.N., Power C.A., Lusti-Narasimhan M., Hoogewerf A.J., Cooke R.M., Chung C.W., Peitsch M.C., Proudfoot A.E. Selectivity and antagonism of chemokine receptors. J. Leukoc. Biol. 1996, 59:53-60.
56. Elisseeva E.L., Slupsky C.M., Crump M.P., Clark-Lewis I., Sykes B.D. NMR studies of active N-terminal peptides of stromal cell-derived factor-1. Structural basis for receptor binding. J. Biol. Chem. 2000, 275:26799-26805.
57. Booth V., Keizer D.W., Kamphuis M.B., Clark-Lewis I., Sykes B.D. The CXCR3 binding chemokine IP-10/CXCL10: structure and receptor interactions. Biochemistry 2002, 41:10418-10425.
58. Skelton N.J., Quan C., Reilly D., Lowman H. Structure of a CXC chemokine-receptor fragment in complex with interleukin-8. Struct. Fold. Des 1999, 7:157-168.
59. Crump M.P., Gong J.H., Loetscher P., Rajarathnam K., Amara A., Arenzana-Seisdedos F., Virelizier J.L., Baggiolini M., Sykes B.D., Clark-Lewis I. 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. 1997, 16:6996-7007.
60. Kofuku Y., Yoshiura C., Ueda T., Terasawa H., Hirai T., Tominaga S., Hirose M., Maeda Y., Takahashi H., Terashima Y., Matsushima K., Shimada I. Structural basis of the interaction between chemokine stromal cell-derived factor-1/CXCL12 and its G-protein-coupled receptor CXCR4. J. Biol. Chem. 2009, 284:35240-35250.
61. Wu B., Chien E.Y., Mol C.D., Fenalti G., Liu W., Katritch V., Abagyan R., Brooun A., Wells P., Bi F.C., Hamel D.J., Kuhn P., Handel T.M., Cherezov V., Stevens R.C. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 2010, 330:1066-1071.
62. Sohy D., Parmentier M., Springael J.Y. Allosteric transinhibition by specific antagonists in CCR2/CXCR4 heterodimers. J. Biol. Chem. 2007, 282:30062-30069.
63. Sohy D., Yano H., de Nadai P., Urizar E., Guillabert A., Javitch J.A., Parmentier M., Springael J.Y. Hetero-oligomerization of CCR2, CCR5, and CXCR4 and the protean effects of "selective" antagonists. J. Biol. Chem. 2009, 284:31270-31279.
64. Lagane B., Chow K.Y., Balabanian K., Levoye A., Harriague J., Planchenault T., Baleux F., Gunera-Saad N., Arenzana-Seisdedos F., Bachelerie F. CXCR4 dimerization and beta-arrestin-mediated signaling account for the enhanced chemotaxis to CXCL12 in WHIM syndrome. Blood 2008, 112:34-44.
65. Handel T.M., Johnson Z., Crown S.E., Lau E.K., Proudfoot A.E. Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu. Rev. Biochem. 2005, 74:385-410.
66. Johnson Z., Proudfoot A.E., Handel T.M. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 2005, 16:625-636.
67. Witt D.P., Lander A.D. Differential binding of chemokines to glycosaminoglycan subpopulations. Curr. Biol. 1994, 4:394-400.
68. Kuschert G.S.V., Coulin F., Power C.A., Proudfoot A.E.I., Hubbard R.E., Hoogewerf A.J., Wells T.N.C. Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 1999, 38:12959-12968.
69. Proudfoot A.E., Fritchley S., Borlat F., Shaw J.P., Vilbois F., Zwahlen C., Trkola A., Marchant D., Clapham P.R., Wells T.N. The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity. J. Biol. Chem. 2001, 276:10620-10626.
70. Ali S., Robertson H., Wain J.H., Isaacs J.D., Malik G., Kirby J.A. A non-glycosaminoglycan-binding variant of CC chemokine ligand 7 (monocyte chemoattractant protein-3) antagonizes chemokine-mediated inflammation. J. Immunol. 2005, 175:1257-1266.
71. O'Boyle G., Mellor P., Kirby J.A., Ali S. Anti-inflammatory therapy by intravenous delivery of non-heparan sulfate-binding CXCL12. FASEB J. 2009, 23:3906-3916.
72. Severin I.C., Gaudry J.P., Johnson Z., Kungl A., Jansma A., Gesslbauer B., Mulloy B., Power C., Proudfoot A.E., Handel T. Characterization of the chemokine CXCL11-heparin interaction suggests two different affinities for glycosaminoglycans. J. Biol. Chem. 2010, 285:17713-17724.
73. Rueda P., Balabanian K., Lagane B., Staropoli I., Chow K., Levoye A., Laguri C., Sadir R., Delaunay T., Izquierdo E., Pablos J.L., Lendinez E., Caruz A., Franco D., Baleux F., Lortat-Jacob H., Arenzana-Seisdedos F. The CXCL12gamma chemokine displays unprecedented structural and functional properties that make it a paradigm of chemoattractant proteins. PLoS ONE 2008, 3:e2543.
74. Laguri C., Sadir R., Rueda P., Baleux F., Gans P., Arenzana-Seisdedos F., Lortat-Jacob H. The novel CXCL12gamma isoform encodes an unstructured cationic domain which regulates bioactivity and interaction with both glycosaminoglycans and CXCR4. PLoS ONE 2007, 2:e1110.
75. Veldkamp C.T., Ziarek J.J., Peterson F.C., Chen Y., Volkman B.F. Targeting SDF-1/CXCL12 with a ligand that prevents activation of CXCR4 through structure-based drug design. J. Am. Chem. Soc. 2010, 132:7242-7243.
76. Johnson Z., Kosco-Vilbois M.H., Herren S., Cirillo R., Muzio V., Zaratin P., Carbonatto M., Mack M., Smailbegovic A., Rose M., Lever R., Page C., Wells T.N., Proudfoot A.E. Interference with heparin binding and oligomerization creates a novel anti-inflammatory strategy targeting the chemokine system. J. Immunol. 2004, 173:5776-5785.
77. Braunersreuther V., Pellieux C., Pelli G., Burger F., Steffens S., Montessuit C., Weber C., Proudfoot A., Mach F., Arnaud C. Chemokine CCL5/RANTES inhibition reduces myocardial reperfusion injury in atherosclerotic mice. J. Mol. Cell. Cardiol. 2010, 48:789-798.
78. Shahrara S., Proudfoot A.E., Park C.C., Volin M.V., Haines G.K., Woods J.M., Aikens C.H., Handel T.M., Pope R.M. Inhibition of monocyte chemoattractant protein-1 ameliorates rat adjuvant-induced arthritis. J. Immunol. 2008, 180:3447-3456.
79. Lubkowski J., Bujacz G., Boque L., Domaille P.J., Handel T.M., Wlodawer A. The structure of MCP-1 in two crystal forms provides a rare example of variable quaternary interactions. Nat. Struct. Biol. 1997, 4:64-69.
80. Clore G.M., Appella E., Yamada M., Matsushima K., Gronenborn A.M. Three-dimensional structure of interleukin 8 in solution. Biochemistry 1990, 29:1689-1696.
81. Kuloglu E.S., McCaslin D.R., Markley J.L., Volkman B.F. Structural rearrangement of human lymphotactin, a C chemokine, under physiological solution conditions. J. Biol. Chem. 2002, 277:17863-17870.
82. Hoover D.M., Mizoue L.S., Handel T.M., Lubkowski J. The crystal structure of the chemokine domain of fractalkine shows a novel quaternary arrangement. J. Biol. Chem. 2000, 275:23187-23193.
83. Swaminathan G.J., Holloway D.E., Colvin R.A., Campanella G.K., Papageorgiou A.C., Luster A.D., Acharya K.R. Crystal structures of oligomeric forms of the IP-10/CXCL10 chemokine. Structure (Camb) 2003, 11:521-532.
84. Jabeen T., Leonard P., Jamaluddin H., Acharya K.R. Structure of mouse IP-10, a chemokine. Acta Crystallogr. D Biol. Crystallogr. 2008, 64:611-619.
85. Zabel B.A., Nakae S., Zuniga L., Kim J.Y., Ohyama T., Alt C., Pan J., Suto H., Soler D., Allen S.J., Handel T.M., Song C.H., Galli S.J., Butcher E.C. Mast cell-expressed orphan receptor CCRL2 binds chemerin and is required for optimal induction of IgE-mediated passive cutaneous anaphylaxis. J. Exp. Med. 2008, 205:2207-2220.
86. Schulte A., Schulz B., Andrzejewski M.G., Hundhausen C., Mletzko S., Achilles J., Reiss K., Paliga K., Weber C., John S.R., Ludwig A. Sequential processing of the transmembrane chemokines CX3CL1 and CXCL16 by alpha- and gamma-secretases. Biochem. Biophys. Res. Commun. 2007, 358:233-240.