Exploring the binding mechanisms of MIF to CXCR2 using theoretical approaches

Physical Chemistry Chemical Physics

Volumn 17, Issue 5, 2015, Pages 3370-3382

  Xu, Lei ^a   Li, Youyong ^b   Li, Dan ^a   Xu, Peng ^c   Tian, Sheng ^b   Sun, Huiyong ^b   Liu, Hui ^a   Hou, Tingjun ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; ISOMERASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MIF PROTEIN, HUMAN; PROTEIN BINDING;

AMINO ACID SUBSTITUTION; BINDING SITE; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; THERMODYNAMICS;

AMINO ACID SUBSTITUTION; BINDING SITES; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-8B; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84921822481     PISSN: 14639076     EISSN: None     Source Type: Journal    
DOI: 10.1039/c4cp05095a     Document Type: Article

References (56)

1. T. Calandra and T. Roger, Macrophage migration inhibitory factor: A regulator of innate immunity, Nat. Rev. Immunol., 2003, 3, 791-800.
2. E. F. Morand, M. Leech and B. Jurgen, MIF: a new cytokine link between rheumatoid arthritis and atherosclerosis, Nat. Rev. Drug Discovery, 2006, 5, 399-410.
3. T. Hagemann, S. C. Robinson, R. G. Thompson, K. Charles, H. Kulbe and F. R. Balkwill, Ovarian cancer cell-derived migration inhibitory factor enhances tumor growth, progression, and angiogenesis, Mol. Cancer Ther., 2007, 6, 1993-2002.
4. H. Sugimoto, M. Taniguchi, A. Nakagawa, I. Tanaka, M. Suzuki and J. Nishihira, Crystal structure of human D-dopachrome tautomerase, a homologue of macrophage migration inhibitory factor, at 1.54 angstrom resolution, Biochemistry, 1999, 38, 3268-3279.
5. E. Rosengren, P. Aman, S. Thelin, C. Hansson, S. Ahlfors, P. Bjork, L. Jacobsson and H. Rorsman, The macrophage migration inhibitory factor MIF is a phenylpyruvate tautomerase, FEBS Lett., 1997, 417, 85-88.
6. R. Kleemann, A. Kapurniotu, R. W. Frank, A. Gessner, R. Mischke, O. Flieger, S. Juttner, H. Brunner and J. Bernhagen, Disulfide analysis reveals a role for macrophage migration inhibitory factor (MIF) as thiol-protein oxidoreductase, J. Mol. Biol., 1998, 280, 85-102.
7. L. Leng, C. N. Metz, Y. Fang, J. Xu, S. Donnelly, J. Baugh, T. Delohery, Y. B. Chen, R. A. Mitchell and R. Bucala, MIF signal transduction initiated by binding to CD74, J. Exp. Med., 2003, 197, 1467-1476.
8. X. R. Shi, L. Leng, T. Wang, W. K. Wang, X. Du, J. Li, C. McDonald, Z. Chen, J. W. Murphy, E. Lolis, P. Noble, W. Knudson and R. Bucala, CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex, Immunity, 2006, 25, 595-606.
9. J. Bernhagen, R. Krohn, H. Lue, J. L. Gregory, A. Zernecke, R. R. Koenen, M. Dewor, I. Georgiev, A. Schober, L. Leng, T. Kooistra, G. Fingerle-Rowson, P. Ghezzi, R. Kleemann, S. R. McColl, R. Bucala, M. J. Hickey and C. Weber, MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment, Nat. Med., 2007, 13, 587-596.
10. S. P. Fricker and M. Metz, Chemokine receptor modeling: an interdisciplinary approach to drug design, Future Med. Chem., 2014, 6, 91-114.
11. M. Veenstra and R. M. Ransohoff, Chemokine receptor CXCR2: Physiology regulator and neuroinflammation controller?, J. Neuroimmunol., 2012, 246, 1-9.
12. C. A. Hebert, R. V. Vitangcol and J. B. Baker, Scanning Mutagenesis of Interleukin-8 Identifies a Cluster of Residues Required for Receptor-Binding, J. Biol. Chem., 1991, 266, 18989-18994.
13. B. Degryse and M. de Virgilio, The nuclear protein HMGB1, a new kind of chemokine?, FEBS Lett., 2003, 553, 11-17.
14. D. Yang, O. Chertov, N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schroder, J. M. Wang, O. M. Z. Howard and J. J. Oppenheim, beta-defensins: Linking innate and adaptive immunity through dendritic and T cell CCR6, Science, 1999, 286, 525-528.
15. H. Noels, J. Bernhagen and C. Weber, Macrophage Migration Inhibitory Factor: A Noncanonical Chemokine Important in Atherosclerosis, Trends Cardiovasc. Med., 2009, 19, 76-86.
16. C. Weber, S. Kraemer, M. Drechsler, H. Q. Lue, R. R. Koenen, A. Kapurniotu, A. Zernecke and J. Bernhagen, Structural determinants of MIF functions in CXCR2- mediated inflammatory and atherogenic leukocyte recruitment, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 16278-16283.
17. S. Kraemer, H. Q. Lue, A. Zernecke, A. Kapurniotu, E. Andreetto, R. Frank, B. Lennartz, C. Weber and J. Bernhagen, MIF-chemokine receptor interactions in atherogenesis are dependent on an N-loop-based 2-site binding mechanism, FASEB J., 2011, 25, 894-906.
18. B. L. Wu, E. Y. T. Chien, C. D. Mol, G. Fenalti, W. Liu, V. Katritch, R. Abagyan, A. Brooun, P. Wells, F. C. Bi, D. J. Hamel, P. Kuhn, T.M. Handel, V. Cherezov and R. C. Stevens, Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists, Science, 2010, 330, 1066-1071.
19. A. Sali, L. Potterton, F. Yuan, H. Vanvlijmen and M. Karplus, Evaluation of Comparative Protein Modeling by Modeler, Proteins, 1995, 23, 318-326.
20. T. Ichiye and M. Karplus, Collective Motions in Proteins - a Covariance Analysis of Atomic Fluctuations in Molecular-Dynamics and Normal Mode Simulations, Proteins: Struct., Funct., Genet., 1991, 11, 205-217.
21. C. T. Veldkamp, C. Seibert, F. C. Peterson, N. B. De la Cruz, J. C. Haugner, H. Basnet, T. P. Sakmar and B. F. Volkman, Structural Basis of CXCR4 Sulfotyrosine Recognition by the Chemokine SDF-1/CXCL12, Sci. Signaling., 2008, 1, ra4.
22. L. Xu, Y. Y. Li, H. Y. Sun, D. Li and T. J. Hou, Structural basis of the interactions between CXCR4 and CXCL12/SDF-1 revealed by theoretical approaches, Mol. BioSyst., 2013, 9, 2107-2117.
23. D. Rajasekaran, C. Keeler, M. A. Syed, M. C. Jones, J. K. Harrison, D. Q. Wu, V. Bhandari, M. E. Hodsdon and E. J. Lolis, A Model of GAG/MIP-2/CXCR2 Interfaces and Its Functional Effects, Biochemistry, 2012, 51, 5642-5654.
24. P. de Kruijf, H. D. Lim, L. Roumen, V. A. Renjaan, J. Q. Zhao, M. L. Webb, D. S. Auld, J. Wijkmans, G. J. R. Zaman, M. J. Smit, C. de Graaf and R. Leurs, Identification of a Novel Allosteric Binding Site in the CXCR2 Chemokine Receptor, Mol. Pharmacol., 2011, 80, 1108-1118.
25. Q. Tan, Y. Zhu, J. Li, Z. Chen, G. W. Han, I. Kufareva, T. Li, L. Ma, G. Fenalti, J. Li, W. Zhang, X. Xie, H. Yang, H. Jiang, V. Cherezov, H. Liu, R. C. Stevens, Q. Zhao and B. Wu, Structure of the CCR5 Chemokine Receptor-HIV Entry Inhibitor Maraviroc Complex, Science, 2013, 341, 1387-1390.
26. J. B. Lubetsky, A. Dios, J. L. Han, B. Aljabari, B. Ruzsicska, R. Mitchell, E. Lolis and Y. Al-Abed, The tautomerase active site of macrophage migration inhibitory factor is a potential target for discovery of novel anti-inflammatory agents, J. Biol. Chem., 2002, 277, 24976-24982.
27. K. Wiehe, B. Pierce, J. Mintseris, W. W. Tong, R. Anderson, R. Chen and Z. Weng, ZDOCK and RDOCK performance in CAPRI rounds 3, 4, and 5, Proteins, 2005, 60, 207-213.
28. R. Chen and Z. P. Weng, Docking unbound proteins using shape complementarity, desolvation, and electrostatics, Proteins, 2002, 47, 281-294.
29. R. Chen, L. Li and Z. P. Weng, ZDOCK: An initial-stage protein-docking algorithm, Proteins, 2003, 52, 80-87.
30. B. Pierce and Z. P. Weng, ZRANK: Reranking protein docking predictions with an optimized energy function, Proteins, 2007, 67, 1078-1086.
31. J. Hsin, A. Arkhipov, Y. Yin, J. E. Stone and K. Schulten, Using VMD: an introductory tutorial, Curr. Protocol Bioinform., 2008, ch. 5, unit 5.7.
32. W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey and M. L. Klein, Comparison of Simple Potential Functions for Simulating Liquid Water, J. Chem. Phys., 1983, 79, 926-935.
33. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg and C. Simmerling, Comparison of multiple amber force fields and development of improved protein backbone parameters, Proteins, 2006, 65, 712-725.
34. J. Domanski, P. J. Stansfeld, M. S. P. Sansom and O. Beckstein, Lipidbook: A Public Repository for Force-Field Parameters Used in Membrane Simulations, J. Membr. Biol., 2010, 236, 255-258.
35. J. M. Wang, R. M. Wolf, J. W. Caldwell, P. A. Kollman and D. A. Case, Development and testing of a general amber force field, J. Comput. Chem., 2004, 25, 1157-1174.
36. T. Darden, D. York and L. Pedersen, Particle Mesh Ewald - an N.Log(N) Method for Ewald Sums in Large Systems, J. Chem. Phys., 1993, 98, 10089-10092.
37. J. C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kale and K. Schulten, Scalable molecular dynamics with NAMD, J. Comput. Chem., 2005, 26, 1781-1802.
38. J. P. Ryckaert, G. Ciccotti and H. J. C. Berendsen, Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes, J. Comput. Phys., 1977, 23, 327-341.
39. T. Hou, J. Wang, Y. Li and W. Wang, Assessing the Performance of the MM/PBSA and MM/GBSA Methods. 1. The Accuracy of Binding Free Energy Calculations Based on Molecular Dynamics Simulations, J. Chem. Inf. Model., 2011, 51, 69-82.
40. L. Xu, Y. Li, L. Li, S. Zhou and T. Hou, Understanding microscopic binding of macrophage migration inhibitory factor with phenolic hydrazones by molecular docking, molecular dynamics simulations and free energy calculations, Mol. BioSyst., 2012, 8, 2260-2273.
41. T. Hou and R. Yu, Molecular dynamics and free energy studies on the wild-type and double mutant HIV-1 protease complexed with amprenavir and two amprenavir-related inhibitors: Mechanism for binding and drug resistance, J. Med. Chem., 2007, 50, 1177-1188.
42. L. Xu, H. Sun, Y. Li, J. Wang and T. Hou, Assessing the Performance of MM/PBSA and MM/GBSA Methods. 3. The Impact of Force Fields and Ligand Charge Models, J. Phys. Chem. B, 2013, 117, 8408-8421.
43. H. Sun, Y. Li, S. Tian, L. Xu and T. Hou, Assessing the Performance of MM/PBSA and MM/GBSA Methods. 4. Accuracies of MM/PBSA and MM/GBSA Methodologies Evaluated by Various Simulation Protocols using PDBbind Data Set, Phys. Chem. Chem. Phys., 2014, 16, 16719-16729.
44. H. Liu and X. Yao, Molecular Basis of the Interaction for an Essential Subunit PA-PB1 in Influenza Virus RNA Polymerase: Insights from Molecular Dynamics Simulation and Free Energy Calculation, Mol. Pharmaceutics, 2009, 7, 75-85.
45. Q. Xue, J. L. Zhang, Q. C. Zheng, Y. L. Cui, L. Chen, W. T. Chu and H. X. Zhang, Exploring the Molecular Basis of dsRNA Recognition by Mss116p Using Molecular Dynamics Simulations and Free-Energy Calculations, Langmuir, 2013, 29, 11135-11144.
46. P. A. Kollman, I. Massova, C. Reyes, B. Kuhn, S. H. Huo, L. Chong, M. Lee, T. Lee, Y. Duan, W. Wang, O. Donini, P. Cieplak, J. Srinivasan, D. A. Case and T. E. Cheatham, Calculating structures and free energies of complexmolecules: Combining molecular mechanics and continuum models, Acc. Chem. Res., 2000, 33, 889-897.
47. J. Wang, T. Hou and X. Xu, Recent Advances in Free Energy Calculations with a Combination of Molecular Mechanics and Continuum Models, Curr. Comput.-Aided Drug Des., 2006, 2, 287-306.
48. A. Onufriev, D. Bashford and D. A. Case, Exploring protein native states and large-scale conformational changes with a modified generalized bornmodel, Proteins, 2004, 55, 383-394.
49. J. Weiser, P. S. Shenkin and W. C. Still, Approximate atomic surfaces from linear combinations of pairwise overlaps (LCPO), J. Comput. Chem., 1999, 20, 217-230.
50. T. Hou, W. Zhang, D. A. Case and W. Wang, Characterization of domain-peptide interaction interface: A case study on the amphiphysin-1 SH3 domain, J. Mol. Biol., 2008, 376, 1201-1214.
51. T. Hou, Y. Li and W. Wang, Prediction of peptides binding to the PKA RII alpha subunit using a hierarchical strategy, Bioinformatics, 2011, 27, 1814-1821.
52. L. Li, Y. Y. Li, L. L. Zhang and T. J. Hou, Theoretical Studies on the Susceptibility of Oseltamivir against Variants of 2009 A/H1N1 Influenza Neuraminidase, J. Chem. Inf. Model., 2012, 52, 2715-2729.
53. H. Gohlke, C. Kiel and D. A. Case, Insights into proteinprotein binding by binding free energy calculation and free energy decomposition for the Ras-Raf and Ras-RaIGDS complexes, J. Mol. Biol., 2003, 330, 891-913.
54. W. Xue, Y. Yang, X. Wang, H. Liu and X. Yao, Computational Study on the Inhibitor Binding Mode and Allosteric Regulation Mechanism in Hepatitis C Virus NS3/4A Protein, PLoS One, 2014, 9, e87077.
55. F. El-Turk, M. Cascella, H. Ouertatani-Sakouhi, R. L. Narayanan, L. Leng, R. Bucala, M. Zweckstetter, U. Rothlisberger and H. A. Lashuel, The conformational flexibility of the carboxy terminal residues 105-114 is a key modulator of the catalytic activity and stability of macrophage migration inhibitory factor, Biochemistry, 2008, 47, 10740-10756.
56. F. El-Turk, B. Fauvet, A. Ashrafi, H. Ouertatani-Sakouhi, M. K. Cho, M. Neri, M. Cascella, U. Rothlisberger, F. Pojer, M. Zweckstetter and H. Lashuel, Characterization of Molecular Determinants of the Conformational Stability of Macrophage Migration Inhibitory Factor: Leucine 46 Hydrophobic Pocket, PLoS One, 2012, 7, e45024.