Interactions of the Chemokine CCL5/RANTES with Medium-Sized Chondroitin Sulfate Ligands

Structure

Volumn 23, Issue 6, 2015, Pages 1066-1077

  Deshauer, Courtney ^a   Morgan, Ashli M ^a   Ryan, Eathen O ^a   Handel, Tracy M ^b   Prestegard, James H ^c   Wang, Xu ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE DERIVATIVE; CHONDROITIN SULFATE; N ACETYLGALACTOSAMINE; RANTES; 2,2,6,6-TETRAMETHYLPIPERIDIDE; LIGAND; OLIGOSACCHARIDE; PIPERIDINE DERIVATIVE; POLYSACCHARIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOHYDRATE ANALYSIS; DIMERIZATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE; SULFATION; TITRIMETRY; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

CHEMOKINE CCL5; CHONDROITIN SULFATES; DIMERIZATION; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; OLIGOSACCHARIDES; PIPERIDINES; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 84930384439     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.03.024     Document Type: Article

References (42)

1. V. Appay, A. Brown, S. Cribbes, E. Randle, and L.G. Czaplewski Aggregation of RANTES is responsible for its inflammatory properties-characterization of nonaggregating, noninflammatory RANTES mutants J. Biol. Chem. 274 1999 27505 27512
2. J.R. Bishop, M. Schuksz, and J.D. Esko Heparan sulphate proteoglycans fine-tune mammalian physiology Nature 446 2007 1030 1037
3. W.J. Carter, E. Cama, and J.A. Huntington Crystal structure of thrombin bound to heparin J. Biol. Chem. 280 2005 2745 2749
4. G.M. Clore, C. Tang, and J. Iwahara Elucidating transient macromolecular interactions using paramagnetic relaxation enhancement Curr. Opin. Struct. Biol. 17 2007 603 616
5. L.G. Czaplewski, J. McKeating, C.J. Craven, L.D. Higgins, V. Appay, A. Brown, T. Dudgeon, L.A. Howard, T. Meyers, and J. Owen Identification of amino acid residues critical for aggregation of human CC chemokines macrophage inflammatory protein (MIP)-1 alpha, MIP-1 beta, and RANTES-characterization of active disaggregated chemokine variants J. Biol. Chem. 274 1999 16077 16084
6. L. Duma, D. Haussinger, M. Rogowski, P. Lusso, and S. Grzesiek Recognition of RANTES by extracellular parts of the CCR5 receptor J. Mol. Biol. 365 2007 1063 1075
7. J.Y. Guan, J.M. Foerster, J.W. Drijfhout, M. Timmer, A. Blok, G.M. Ullmann, and M. Ubbink An ensemble of rapidly interconverting orientations in electrostatic protein-peptide complexes characterized by NMR spectroscopy Chembiochem 15 2014 556 566
8. A.J. Hoogewerf, G.S.V. Kuschert, A.E.I. Proudfoot, F. Borlat, I. ClarkLewis, C.A. Power, and T.N.C. Wells Glycosaminoglycans mediate cell surface oligomerization of chemokines Biochemistry 36 1997 13570 13578
9. C.J.M. Huige, and C. Altona Force field parameters for sulfates and sulfamates based on ab initio calculations-extensions of AMBER and CHARMm fields J. Comput. Chem. 16 1995 56 79
10. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-38
11. J. Iwahara, C. Tang, and G. Marius Clore Practical aspects of (1)H transverse paramagnetic relaxation enhancement measurements on macromolecules J. Magn. Reson. 184 2007 185 195
12. C.H. Jen, and J.A. Leary A competitive binding study of chemokine, sulfated receptor, and glycosaminoglycan interactions by nano-electrospray ionization mass spectrometry Anal. Biochem. 407 2010 134 140
13. H. Jin, X. Shen, B.R. Baggett, X. Kong, and P.J. LiWang The human CC chemokine MIP-1beta dimer is not competent to bind to the CCR5 receptor J. Biol. Chem. 282 2007 27976 27983
14. H. Jin, I. Kagiampakis, P. Li, and P.J. Liwang Structural and functional studies of the potent anti-HIV chemokine variant P2-RANTES Proteins 78 2010 295 308
15. K.N. Kirschner, A.B. Yongye, S.M. Tschampel, J. Gonzalez-Outeirino, C.R. Daniels, B.L. Foley, and R.J. Woods GLYCAM06: a generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29 2008 622 655
16. U. Lindahl What else can 'heparin' do? Haemostasis 29 1999 38 47
17. L. Martin, C. Blanpain, P. Garnier, V. Wittamer, M. Parmentier, and C. Vita Structural and functional analysis of the RANTES-glycosaminoglycans interactions Biochemistry 40 2001 6303 6318
18. M.A. McCornack, C.K. Cassidy, and P.J. LiWang The binding surface and affinity of monomeric and dimeric chemokine macrophage inflammatory protein 1 beta for various glycosaminoglycan disaccharides J. Biol. Chem. 278 2003 1946 1956
19. S. Mizumoto, D. Fongmoon, and K. Sugahara Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines Glycoconj. J. 30 2013 619 632
20. B. Mulloy, and R.J. Linhardt Order out of complexity-protein structures that interact with heparin Curr. Opin. Struct. Biol. 11 2001 623 628
21. T.T. Murooka, M.M. Wong, R. Rahbar, B. Majchrzak-Kita, A.E. Proudfoot, and E.N. Fish CCL5-CCR5-mediated apoptosis in T cells: requirement for glycosaminoglycan binding and CCL5 aggregation J. Biol. Chem. 281 2006 25184 25194
22. I. Oynebraten, N. Barois, T. Bergeland, A.M. Kuchler, O. Bakke, and G. Haraldsen Oligomerized, filamentous surface presentation of RANTES/CCL5 on vascular endothelial cells Sci. Rep. 5 2015 9261
23. D.R. Pakianathan, E.G. Kuta, D.R. Artis, N.J. Skelton, and C.A. Hebert Distinct but overlapping epitopes for the interaction of a CC-chemokine with CCR1, CCR3, and CCR5 Biochemistry 36 1997 9642 9648
24. A.E.I. Proudfoot, S. Fritchley, F. Borlat, J.P. Shaw, F. Vilbois, C. Zwahlen, A. Trkola, D. Marchant, P.R. Clapham, and T.N.C. Wells The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity J. Biol. Chem. 276 2001 10620 10626
25. A.E.I. Proudfoot, T.M. Handel, Z. Johnson, E.K. Lau, P. LiWang, I. Clark-Lewis, F. Borlat, T.N.C. Wells, and M.H. Kosco-Vilbois Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines Proc. Natl. Acad. Sci. USA 100 2003 1885 1890
26. L. Qin, I. Kufareva, L.G. Holden, C. Wang, Y. Zheng, C. Zhao, G. Fenalti, H. Wu, G.W. Han, and V. Cherezov Crystal structure of the chemokine receptor CXCR4 in complex with a viral chemokine Science 347 2015 1117 1122
27. A. Ravindran, K.V. Sawant, J. Sarmiento, J. Navarro, and K. Rajarathnam Chemokine CXCL1 dimer is a potent agonist for the CXCR2 receptor J. Biol. Chem. 288 2013 12244 12252
28. A. Rek, B. Brandner, E. Geretti, and A.J. Kungl A biophysical insight into the RANTES-glycosaminoglycan interaction Biochim. Biophys. Acta 1794 2009 577 582
29. M. Sakakura, S. Oo-Puthinan, C. Moriyama, T. Kimura, J. Moriya, T. Irimura, and I. Shimada Carbohydrate binding mechanism of the macrophage galactose-type C-type lectin 1 revealed by saturation transfer experiments J. Biol. Chem. 283 2008 33665 33673
30. E. Schnur, N. Kessler, Y. Zherdev, E. Noah, T. Scherf, F.X. Ding, S. Rabinovich, B. Arshava, V. Kurbatska, and A. Leonciks NMR mapping of RANTES surfaces interacting with CCR5 using linked extracellular domains FEBS J. 280 2013 2068 2084
31. J.P. Shaw, Z. Johnson, F. Borlat, C. Zwahlen, A. Kungl, K. Roulin, A. Harrenga, T.N.C. Wells, and A.E.I. Proudfoot The X-ray structure of RANTES: heparin-derived disaccharides allows the rational design of chemokine inhibitors Structure 12 2004 2081 2093
32. G.J. Sheng, Y.I. Oh, S.K. Chang, and L.C. Hsieh-Wilson Tunable heparan sulfate mimetics for modulating chemokine activity J. Am. Chem. Soc. 135 2013 10898 10901
33. A. Sutton, V. Friand, D. Papy-Garcia, M. Dagouassat, L. Martin, R. Vassy, O. Haddad, O. Sainte-Catherine, M. Kraemer, and L. Saffar Glycosaminoglycans and their synthetic mimetics inhibit RANTES-induced migration and invasion of human hepatoma cells Mol. Cancer Ther. 6 2007 2948 2958
34. K. Tan, M. Duquette, J.H. Liu, K. Shanmugasundaram, A. Joachimiak, J.T. Gallagher, A.C. Rigby, J.H. Wang, and J. Lawler Heparin-induced cis- and trans-dimerization modes of the thrombospondin-1 N-terminal domain J. Biol. Chem. 283 2008 3932 3941
35. J.H. Tan, M. Canals, J.P. Ludeman, J. Wedderburn, C. Boston, S.J. Butler, A.M. Carrick, T.R. Parody, D. Taleski, and A. Christopoulos Design and receptor interactions of obligate dimeric mutant of chemokine monocyte chemoattractant protein-1 (MCP-1) J. Biol. Chem. 287 2012 14692 14702
36. C. Tang, J.M. Louis, A. Aniana, J.Y. Suh, and G.M. Clore Visualizing transient events in amino-terminal autoprocessing of HIV-1 protease Nature 455 2008 693 696
37. C.T. Veldkamp, C. Seibert, F.C. Peterson, N.B. De la Cruz, J.C. Haugner 3rd, H. Basnet, T.P. Sakmar, and B.F. Volkman Structural basis of CXCR4 sulfotyrosine recognition by the chemokine SDF-1/CXCL12 Sci. Signal. 1 2008 ra4
38. R.R. Vivès, R. Sadir, A. Imberty, A. Rencurosi, and H. Lortat-Jacob A kinetics and modeling study of RANTES(9-68) binding to heparin reveals a mechanism of cooperative oligomerization Biochemistry 41 2002 14779 14789
39. P. von Hundelshausen, R.R. Koenen, M. Sack, S.F. Mause, W. Adriaens, A.E. Proudfoot, T.M. Hackeng, and C. Weber Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium Blood 105 2005 924 930
40. X. Wang, C. Watson, J.S. Sharp, T.M. Handel, and J.H. Prestegard Oligomeric structure of the chemokine CCL5/RANTES from NMR, MS, and SAXS data Structure 19 2011 1138 1148
41. F. Yu, J.J. Wolff, I.J. Amster, and J.H. Prestegard Conformational preferences of chondroitin sulfate oligomers using partially oriented NMR spectroscopy of 13C-labeled acetyl groups J. Am. Chem. Soc. 129 2007 13288 13297
42. J.J. Ziarek, C.T. Veldkamp, F. Zhang, N.J. Murray, G.A. Kartz, X. Liang, J. Su, J.E. Baker, R.J. Linhardt, and B.F. Volkman Heparin oligosaccharides inhibit chemokine (CXC motif) ligand 12 (CXCL12) cardioprotection by binding orthogonal to the dimerization interface, promoting oligomerization, and competing with the chemokine (CXC motif) receptor 4 (CXCR4) N terminus J. Biol. Chem. 288 2013 737 746