Human macrophage inflammatory protein 3α: Protein and peptide nuclear magnetic resonance solution structures, dimerization, dynamics, and anti-infective properties

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 3, 2008, Pages 883-894

  Chan, David I ^a   Hunter, Howard N ^a,c   Tack, Brian F ^b   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF IOWA   (United States)

^c YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; HISTIDINE DERIVATIVE; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOMER;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANTIBACTERIAL ACTIVITY; ANTIFUNGAL ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DIFFUSION; DIMERIZATION; ESCHERICHIA COLI; HYDROGEN BOND; HYDROPHOBICITY; MICROBIAL ACTIVITY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; RECEPTOR BINDING; STAPHYLOCOCCUS AUREUS;

CHEMOKINE CCL20; CRYSTALLIZATION; DIMERIZATION; ESCHERICHIA COLI; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTONS; SOLUTIONS; STAPHYLOCOCCUS AUREUS;

EID: 40549102762     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00805-07     Document Type: Article

References (78)

1. Allen, S. J., S. E. Crown, and T. M. Handel. 2007. Chemokine: receptor structure, interactions, and antagonism. Annu. Rev. Immunol. 25:787-820.
2. Anderson, R. C., and P. L. Yu. 2005. Factors affecting the antimicrobial activity of ovine-derived cathelicidins against E. coli O157:H7. Int. J. Antimicrob. Agents 25:205-210.
3. Baryshnikova, O. K., and B. D. Sykes. 2006. Backbone dynamics of SDF-1alpha determined by NMR: interpretation in the presence of monomer-dimer equilibrium. Protein Sci. 15:2568-2578.
4. Berendsen, H. J. C., J. P. M. Postma, W. F. van Gunsteren, A. Dinola, and J. R. Haak. 1984. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
5. Berendsen, H. J. C., D. van der Spoel, and R. van Drunen. 1995. Gromacs - a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 91:43-56.
6. Björstad, Å., H. M. Fu, A. Karlsson, C. Dahlgren, and J. Bylund. 2005. Interleukin-8-derived peptide has antibacterial activity. Antimicrob. Agents Chemother. 49:3889-3895.
7. Blanpain, C., B. J. Doranz, A. Bondue, C. Govaerts, A. De Leener, G. Vassart, R. W. Doms, A. Proudfoot, and M. Parmentier. 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.
8. Brünger, A. T., P. D. Adams, G. M. Clore, W. L. Delano, P. Gros, R. W. Grosse-Kunstleve, J. S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54:905-921.
9. Cole, A. M., T. Ganz, A. M. Liese, M. D. Burdick, L. Liu, and R. M. Strieter. 2001. Cutting edge: IFN-inducible ELR-CXC chemokines display defensin-like antimicrobial activity. J. Immunol. 167:623-627.
10. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald - an N·log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
11. Delaglio, F., S. Grzesiek, G. W. Vuister, G. Zhu, J. Pfeifer, and A. Bax. 1995. NMRPipe - a multidimensional spectral processing system based on Unix pipes. J. Biomol. NMR 6:277-293.
12. Dieu, M. C., B. Vanbervliet, A. Vicari, J. M. Bridon, E. Oldham, S. Aït-Yahia, F. Brière, A. Zlotnik, S. Lebecque, and C. Caux. 1998. Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites. J. Exp. Med. 188:373-386.
13. Duma, L., D. Häussinger, M. Rogowski, P. Lusso, and S. Grzesiek. 2007. Recognition of RANTES by extracellular parts of the CCR5 receptor. J. Mol. Biol. 365:1063-1075.
14. Epand, R. M., and H. J. Vogel. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462:11-28.
15. Esche, C., C. Stellato, and L. A. Beck. 2005. Chemokines: key players in innate and adaptive immunity. J. Investig. Dermatol. 125:615-628.
16. Feenstra, K. A., B. Hess, and H. J. C. Berendsen. 1999. Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J. Comput. Chem. 20:786-798.
17. Fernando, H., C. Chin, J. Rosgen, and K. Rajarathnam. 2004. Dimer dissociation is essential for interleukin-8 (IL-8) binding to CXCR1 receptor. J. Biol. Chem. 279:36175-36178.
18. Formaneck, M. S., L. Ma, and Q. Cui. 2006. Effects of temperature and salt concentration on the structural stability of human lymphotactin: insights from molecular simulations. J. Am. Chem. Soc. 128:9506-9517.
19. Gill, S. C., and P. H. von Hippel. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:319-326.
20. Guijarro, J. I., M. Sunde, J. A. Jones, I. D. Campbell, and C. M. Dobson. 1998. Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. USA 95:4224-4228.
21. Haney, E. F., F. Lau, and H. J. Vogel. 2007. Solution structures and model membrane interactions of lactoferrampin, an antimicrobial peptide derived from bovine lactoferrin. Biochim. Biophys. Acta 1768:2355-2364.
22. Harrison, J. K., A. M. Fong, P. A. W. Swain, S. Z. Chen, Y. R. A. Yu, M. N. Salafranca, W. B. Greenleaf, T. Imai, and D. D. Patel. 2001. Mutational analysis of the fractalkine chemokine domain - basic amino acid residues differentially contribute to CX3CR1 binding, signaling, and cell adhesion. J. Biol. Chem. 276:21632-21641.
23. Hasan, L., L. Mazzucchelli, M. Liebi, M. Lis, R. E. Hunger, A. Tester, C. M. Overall, and M. Wolf. 2006. Function of liver activation-regulated chemokine/CC chemokine ligand 20 is differently affected by cathepsin B and cathepsin D processing. J. Immunol. 176:6512-6522.
24. Hess, B., H. Bekker, H. J. C. Berendsen, and J. G. E. M. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
25. Homey, B., M. C. Dieu-Nosjean, A. Wiesenborn, C. Massacrier, J. J. Pin, E. Oldham, D. Catron, M. E. Buchanan, A. Muller, R. D. Malefyt, G. Deng, R. Orozco, T. Ruzicka, P. Lehmann, S. Lebecque, C. Caux, and A. Zlotnik. 2000. Up-regulation of macrophage inflammatory protein-3 alpha/CCL20 and CC chemokine receptor 6 in psoriasis. J. Immunol. 164:6621-6632.
26. Hoogewerf, A. J., G. S. V. Kuschert, A. E. I. Proudfoot, F. Borlat, I. Clark-Lewis, C. A. Power, and T. N. C. Wells. 1997. Glycosaminoglycans mediate cell surface oligomerization of chemokines. Biochemistry 36:13570-13578.
27. Hoover, D. M., C. Boulègue, D. Yang, J. J. Oppenheim, K. Tucker, W. Y. Lu, and J. Lubkowski. 2002. The structure of human macrophage inflammatory protein-3 alpha/CCL20 - linking antimicrobial and CC chemokine receptor-6-binding activities with human beta-defensins. J. Biol. Chem. 277:37647-37654.
28. Horcher, M., A. Rot, H. Aschauer, and J. Besemer. 1998. IL-8 derivatives with a reduced potential to form homodimers are fully active in vitro and in vivo. Cytokine 10:1-12.
29. + T-cell accumulation in periodontal diseased tissue. Clin. Exp. Immunol. 128:548-554.
30. Humphrey, W., A. Dalke, and K. Schulten. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38.
31. Hunter, H. N., D. B. Fulton, T. Ganz, and H. J. Vogel. 2002. The solution structure of human hepcidin, a peptide hormone with antimicrobial activity that is involved in iron uptake and hereditary hemochromatosis. J. Biol. Chem. 277:37597-37603.
32. Hwang, T. L., and A. J. Shaka. 1995. Water suppression that works - excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson. A 112:275-279.
33. Jarnagin, K., D. Grunberger, M. Mulkins, B. Wong, S. Hemmerich, C. Paavola, A. Bloom, S. Bhakta, F. Diehl, R. Freedman, D. McCarley, I. Polsky, A. Ping-Tsou, A. Kosaka, and T. M. Handel. 1999. Identification of surface residues of the monocyte chemotactic protein 1 that affect signaling through the receptor CCR2. Biochemistry 38:16167-16177.
34. Johnson, B. A., and R. A. Blevins. 1994. NMRView - a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4:603-614.
35. Jones, J. A., D. K. Wilkins, L. J. Smith, and C. M. Dobson. 1997. Characterisation of protein unfolding by NMR diffusion measurements. J. Biomol. NMR 10:199-203.
36. Keizer, D. W., M. P. Crump, T. W. Lee, C. M. Slupsky, I. Clark-Lewis, and B. D. Sykes. 2000. Human CC chemokine I-309, structural consequences of the additional disulfide bond. Biochemistry 39:6053-6059.
37. Kim, B. E., D. Y. M. Leung, J. E. Streib, M. Boguniewicz, Q. A. Hamid, and M. D. Howell. 2007. Macrophage inflammatory protein 3alpha deficiency in atopic dermatitis skin and role in innate immune response to vaccinia virus. J. Allergy Clin. Immunol. 119:457-463.
38. Kleeff, J., T. Kusama, D. L. Rossi, T. Ishiwata, H. Maruyama, H. Friess, M. W. Büchler, A. Zlotnik, and M. Korc. 1999. Detection and localization of Mip-3alpha/LARC/Exodus, a macrophage proinflammatory chemokine, and its CCR6 receptor in human pancreatic cancer. Int. J. Cancer 81:650-657.
39. Koradi, R., M. Billeter, and K. Wüthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55.
40. Kuschert, G. S. V., A. J. Hoogewerf, A. E. I. Proudfoot, C. W. Chung, R. M. Cooke, R. E. Hubbard, T. N. C. Wells, and P. N. Sanderson. 1998. Identification of a glycosaminoglycan binding surface on human interleukin-8. Biochemistry 37:11193-11201.
41. Lai, J. R., R. F. Epand, B. Weisblum, R. M. Epand, and S. H. Gellman. 2006 Roles of salt and conformation in the biological and physicochemical behavior of protegrin-1 and designed analogues: correlation of antimicrobial, hemolytic, and lipid bilayer-perturbing activities. Biochemistry 45:15718-15730.
42. Laskowski, R. A., M. W. Macarthur, D. S. Moss, and J. M. Thornton. 1993. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
43. Laurence, J. S., C. Blanpain, J. W. Burgner, M. Parmentier, and P. J. Liwang. 2000. CC chemokine MIP-1 beta can function as a monomer and depends on Phe13 for receptor binding. Biochemistry 39:3401-3409.
44. Lee, H. Y., A. Andalibi, P. Webster, S. K. Moon, K. Teufert, S. H. Kang, J. D. Li, M. Nagura, T. Ganz, and D. J. Lim. 2004. Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect. Dis. 4:12.
45. Lee, I. H., Y. Cho, and R. I. Lehrer. 1997. Effects of pH and salinity on the antimicrobial properties of clavanins. Infect. Immun. 65:2898-2903.
46. Liao, F., R. Alderson, J. Su, S. J. Ullrich, B. L. Kreider, and J. M. Farber. 1997. STRL22 is a receptor for the CC chemokine MIP-3 alpha. Biochem. Biophys. Res. Commun. 236:212-217.
47. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. 7:306-317.
48. Linge, J. P., S. I. O'Donoghue, and M. Nilges. 2001. Automated assignment of ambiguous nuclear Overhauser effects with ARIA. Methods Enzymol. 339:71-90.
49. Ma, L., and Q. Cui. 2006. The temperature dependence of salt-protein association is sequence specific. Biochemistry 45:14466- 14472.
50. Malik, Z. A., and B. F. Tack. 2006. Structure of human MIP-3alpha chemokine. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62:631-634.
51. Malkowski, M. G., J. Y. Wu, J. B. Lazar, P. H. Johnson, and B. F. P. Edwards. 1995. The crystal-structure of recombinant human neutrophil-activating peptide-2 (M6L) at 1.9-angstrom resolution. J. Biol. Chem. 270:7077-7087.
52. Markley, J. L. 1975. Observation of histidine residues in proteins by means of nuclear magnetic resonance spectroscopy. Acc. Chem. Res. 8:70-80.
53. Mason, A. J., C. Gasnier, A. Kichler, G. Prévost, D. Aunis, M. H. Metz-Boutigue, and B. Bechinger. 2006. Enhanced membrane disruption and antibiotic action against pathogenic bacteria by designed histidine-rich peptides at acidic pH. Antimicrob. Agents Chemother. 50:3305-3311.
54. Merrill, M. R. 1993. NMR diffusion measurements using a composite gradient PGSE sequence. J. Magn. Reson. A 103:223-225.
55. Miyakawa, Y., P. Ratnakar, A. G. Rao, M. L. Costello, O. Mathieu-Costello, R. I. Lehrer, and A. Catanzaro. 1996. In vitro activity of the antimicrobial peptides human and rabbit defensins and porcine leukocyte protein against Mycobacterium tuberculosis. Infect. Immun. 64:926-932.
56. Nakayama, T., J. Shirane, K. Hieshima, M. Shibano, M. Watanabe, Z. Jin, D. Nagakubo, T. Saito, Y. Shimomura, and O. Yoshie. 2006. Novel antiviral activity of chemokines. Virology 350:484-492.
57. Nilges, M., and S. I. O'Donoghue. 1998. Ambiguous NOEs and automated NOE assignment. Prog. Nucl. Magn. Reson. Spectrosc. 32:107-139.
58. Paavola, C. D., S. Hemmerich, D. Grunberger, I. Polsky, A. Bloom, R. Freedman, M. Mulkins, S. Bhakta, D. McCarley, L. Wiesent, B. Wong, K. Jarnagin, and T. M. Handel. 1998. Monomeric monocyte chemoattractant protein-1 (MCP-1) binds and activates the MCP-1 receptor CCR2B. J. Biol. Chem. 273:33157-33165.
59. Pérez-Cañadillas, J. M., A. Zaballos, J. Gutiérrez, R. Varona, F. Roncal, J. P. Albar, G. Márquez, and M. Bruix. 2001. NMR olution 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.
60. Reference deleted.
61. Power, C. A., D. J. Church, A. Meyer, S. Alouani, A. E. I. Proudfoot, I. Clark-Lewis, S. Sozzani, A. Mantovani, and T. N. C. Wells. 1997. Cloning and characterization of a specific receptor for the novel CC chemokine MIP-3alpha from lung dendritic cells. J. Exp. Med. 186:825-835.
62. Rajarathnam, K., G. N. Prado, H. Fernando, I. Clark-Lewis, and J. Navarro. 2006. Probing receptor binding activity of interleukin-8 dimer using a disulfide trap. Biochemistry 45:7882-7888.
63. Redfield, C., B. A. Schulman, M. A. Milhollen, P. S. Kim, and C. M. Dobson. 1999. Alpha-lactalbumin forms a compact molten globule in the absence of disulfide bonds. Nat. Struct. Biol. 6:948-952.
64. Ruth, J. H., S. Shahrara, C. C. Park, J. C. M. Morel, P. Kumar, S. X. Qin, and A. E. Koch. 2003. Role of macrophage inflammatory protein-3 alpha and its ligand CCR6 in rheumatoid arthritis. Lab. Investig. 83:579-588.
65. Schibli, D. J., H. N. Hunter, V. Aseyev, T. D. Starner, J. M. Wiencek, P. B. McCray, B. F. Tack, and H. J. Vogel. 2002. The solution structures of the human beta-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus. J. Biol. Chem. 277:8279-8289.
66. Schibli, D. J., L. T. Nguyen, S. D. Kernaghan, Ø. Rekdal, and H. J. Vogel. 2006. Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures. Biophys. J. 91:4413-4426.
67. Scott, W. R. P., P. H. Hunenberger, I. G. Tironi, A. E. Mark, S. R. Billeter, J. Fennen, A. E. Torda, T. Huber, P. Krüger, and W. F. van Gunsteren. 1999. The GROMOS biomolecular simulation program package. J. Phys. Chem. A 103:3596-3607.
68. Strøm, M. B., Ø. Rekdal, and J. S. Svendsen. 2002. Antimicrobial activity of short arginine and tryptophan-rich peptides. J. Pept. Sci. 8:431-437.
69. Strøm, M. B., Ø. Rekdal, and J. S. Svendsen. 2002. The effects of charge and lipophilicity on the antibacterial activity of undecapeptides derived from bovine lactoferricin. J. Pept. Sci. 8:36-43.
70. Thomas, C. L., E. McKinnon, B. L. Granger, E. Harms, and R. L. Van Etten. 2002. Kinetic and spectroscopic studies of Tritrichomonas foetus low-molecular weight phosphotyrosyl phosphatase. Hydrogen bond networks and electrostatic effects. Biochemistry 41:15601-15609.
71. Veldkamp, C. T., F. C. Peterson, A. J. Pelzek, and B. F. Volkman. 2005. The monomer-dimer equilibrium of stromal cell-derived factor-1 (CXCL 12) is altered by pH, phosphate, sulfate, and heparin. Protein Sci. 14:1071-1081.
72. Wilkins, D. K., S. B. Grimshaw, V. Receveur, C. M. Dobson, J. A. Jones, and L. J. Smith. 1999. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38:16424-16431.
73. Wishart, D. S., B. D. Sykes, and F. M. Richards. 1992. The chemical-shift index - a fast and simple method for the assignment of protein secondary structure through NMR-spectroscopy. Biochemistry 31:1647-1651.
74. Wu, Z. B., D. M. Hoover, D. Yang, C. Boulègue, F. Santamaria, J. J. Oppenheim, J. Lubkowski, and W. Y. Lu. 2003. Engineering disulfide bridges to dissect antimicrobial and chemotactic activities of human beta-defensin 3. Proc. Natl. Acad. Sci. USA 100:8880-8885.
75. Wüthrich, K. 1986. NMR of proteins and nucleic acids. John Wiley & Sons, Inc., New York, NY.
76. Yang, D., Q. Chen, D. M. Hoover, P. Staley, K. D. Tucker, J. Lubkowski, and J. J. Oppenheim. 2003. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J. Leukoc. Biol. 74:448-455.
77. Yang, D., O. Chertov, N. Bykovskaia, Q. Chen, M. J. Buffo, J. Shogan, M. Anderson, J. M. Schröder, J. M. Wang, O. M. Z. Howard, and J. J. Oppenheim. 1999. Beta-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286:525-528.
78. Zlotnik, A., O. Yoshie, and H. Nomiyama. 2006. The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol. 7:243.