Interaction of human β-defensin 2 (HBD2) with glycosaminoglycans

Biochemistry

Volumn 49, Issue 49, 2010, Pages 10486-10495

  Seo, Emily S ^a   Blaum, Bärbel S ^a   Vargues, Thomas ^a   De Cecco, Martin ^a   Deakin, Jon A ^b   Lyon, Malcolm ^b   Barran, Perdita E ^a   Campopiano, Dominic J ^a   Uhrín, Dušan ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNE SYSTEMS; ANTIMICROBIAL PEPTIDE; BACTERICIDAL ACTION; CHONDROITIN SULFATES; COOPERATIVE BINDING; DEFENSINS; DERMATAN SULFATE; DIFFUSION COEFFICIENTS; DISSOCIATION CONSTANT; GEL MOBILITY SHIFT ASSAY; GLYCOSAMINOGLYCANS; HEXASACCHARIDES; LIGAND-BINDING SITES; MODEL COMPOUND; NMR CHEMICAL SHIFTS; NMR SPECTROSCOPY; PENTASACCHARIDES; TOLL-LIKE RECEPTORS;

AMINO ACIDS; ANIMALS; BIOCHEMISTRY; COMPLEXATION; DIMERS; DISSOCIATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SODIUM;

BINDING SITES;

BETA DEFENSIN 2; CHONDROITIN SULFATE; DERMATAN SULFATE; FONDAPARINUX; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN;

ARTICLE; COMPLEX FORMATION; DIFFUSION COEFFICIENT; DRUG BINDING; DRUG BINDING SITE; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN INTERACTION; TITRIMETRY;

BETA-DEFENSINS; BINDING SITES; CHEMOTAXIS, LEUKOCYTE; GLYCOSAMINOGLYCANS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; OLIGOSACCHARIDES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; STATIC ELECTRICITY; SULFATES;

INVERTEBRATA; VERTEBRATA;

EID: 78650129716     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1011749     Document Type: Article

References (59)

1. Ganz, T. (2003) Defensins: antimicrobial peptides of innate immunity Nat. Rev. Immunol. 3, 710-720 (Pubitemid 41070812)
2. Ganz, T., Selsted, M. E., Szklarek, D., Harwig, S. S., Daher, K., Bainton, D. F., and Lehrer, R. I. (1985) Defensins. Natural peptide antibiotics of human neutrophils J. Clin. Invest. 76, 1427-1435
3. Kluver, E., Adermann, K., and Schulz, A. (2006) Synthesis and structure-activity relationship of beta-defensins, multi-functional peptides of the immune system J. Pept. Sci. 12, 243-257
4. Oppenheim, J. J., Biragyn, A., Kwak, L. W., and Yang, D. (2003) Roles of antimicrobial peptides such as defensins in innate and adaptive immunity Ann. Rheum. Dis. 62, 17-21
5. Pazgier, M., Hoover, D. M., Yang, D., Lu, W., and Lubkowski, J. (2006) Human beta-defensins Cell. Mol. Life Sci. 63, 1294-1313
6. Herr, C., Shaykhiev, R., and Bals, R. (2007) The role of cathelicidin and defensins in pulmonary inflammatory diseases Expert Opin. Biol. Ther. 7, 1449-1461
7. Weichhart, T., Haidinger, M., Horl, W. H., and Saemann, M. D. (2008) Current concepts of molecular defence mechanisms operative during urinary tract infection Eur. J. Clin. Invest. 38 (Suppl. 2) 29-38
8. Wehkamp, J., Schauber, J., and Stange, E. F. (2007) Defensins and cathelicidins in gastrointestinal infections Curr. Opin. Gastroenterol. 23, 32-38
9. Philpott, M. P. (2003) Defensins and acne Mol. Immunol. 40, 457-462
10. Langhorst, J., Wieder, A., Michalsen, A., Musial, F., Dobos, G. J., and Rueffer, A. (2007) Activated innate immune system in irritable bowel syndrome? Gut 56, 1325-1326
11. Varoga, D., Tohidnezhad, M., Paulsen, F., Wruck, C. J., Brandenburg, L., Mentlein, R., Lippross, S., Hassenpflug, J., Besch, L., Muller, M., Jurgens, C., Seekamp, A., Schmitt, L., and Pufe, T. (2008) The role of human beta-defensin-2 in bone J. Anat. 213, 749-757
12. Hoover, D. M., Chertov, O., and Lubkowski, J. (2001) The structure of human beta-defensin-1: new insights into structural properties of beta-defensins J. Biol. Chem. 276, 39021-39026
13. Schibli, D. J., Hunter, H. N., Aseyev, V., Starner, T. D., Wiencek, J. M., McCray, P. B., Jr., Tack, B. F., and Vogel, H. J. (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
14. Hoover, D. M., Rajashankar, K. R., Blumenthal, R., Puri, A., Oppenheim, J. J., Chertov, O., and Lubkowski, J. (2000) The structure of human beta-defensin-2 shows evidence of higher order oligomerization J. Biol. Chem. 275, 32911-32918
15. Sawai, M. V., Jia, H. P., Liu, L., Aseyev, V., Wiencek, J. M., McCray, P. B., Jr., Ganz, T., Kearney, W. R., and Tack, B. F. (2001) The NMR structure of human beta-defensin-2 reveals a novel alpha-helical segment Biochemistry 40, 3810-3816
16. Bauer, F., Schweimer, K., Kluver, E., Conejo-Garcia, J. R., Forssmann, W. G., Rosch, P., Adermann, K., and Sticht, H. (2001) Structure determination of human and murine beta-defensins reveals structural conservation in the absence of significant sequence similarity Protein Sci. 10, 2470-2479
17. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms Nature 415, 389-395
18. Schmidtchen, A., Frick, I. M., and Bjorck, L. (2001) Dermatan sulphate is released by proteinases of common pathogenic bacteria and inactivates antibacterial alpha-defensin Mol. Microbiol. 39, 708-713
19. Kuschert, G. S. V., Coulin, F., Power, C. A., Proudfoot, A. E. I., Hubbard, R. E., Hoogewerf, A. J., and Wells, T. N. C. (1999) Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses Biochemistry 38, 12959-12968
20. Andersson, E., Rydengard, V., Sonesson, A., Morgelin, M., Bjorck, L., and Schmidtchen, A. (2004) Antimicrobial activities of heparin-binding peptides Eur. J. Biochem. 271, 1219-1226
21. McCullough, B. J., Kalapothakis, J. M., Chin, W., Taylor, K., Clarke, D. J., Eastwood, H., Campopiano, D., MacMillan, D., Dorin, J., and Barran, P. E. (2010) Binding a heparin derived disaccharide to defensin inspired peptides: insights to antimicrobial inhibition from gas-phase measurements Phys. Chem. Chem. Phys. 12, 3589-3596
22. 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
23. Chen, X., Niyonsaba, F., Ushio, H., Hara, M., Yokoi, H., Matsumoto, K., Saito, H., Nagaoka, I., Ikeda, S., Okumura, K., and Ogawa, H. (2007) Antimicrobial peptides human beta-defensin (hBD)-3 and hBD-4 activate mast cells and increase skin vascular permeability Eur. J. Immunol. 37, 434-444
24. 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
25. Vargues, T., Morrison, G. J., Seo, E. S., Clarke, D. J., Fielder, H. L., Bennani, J., Pathania, U., Kilanowski, F., Dorin, J. R., Govan, J. R. W., Mackay, C. L., Uhrin, D., and Campopiano, D. J. (2009) Efficient production of human beta-defensin 2 (HBD2) in Escherichia coli Protein Pept. Lett. 16, 668-676
26. Yang, D., Biragyn, A., Kwak, L. W., and Oppenheim, J. J. (2002) Mammalian defensins in immunity: more than just microbicidal Trends Immunol. 23, 291-296
27. 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-3 alpha, 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
28. Yang, D., Liu, Z. H., Tewary, P., Chen, Q., de la Rosa, G., and Oppenheim, J. J. (2007) Defensin participation in innate and adaptive immunity Curr. Pharm. Des. 13, 3131-3139
29. Yang, D., Chen, Q., Hoover, D. M., Staley, P., Tucker, K. D., Lubkowski, J., and Oppenheim, J. J. (2003) Many chemokines including CCL20/MIP-3 alpha display antimicrobial activity J. Leukocyte Biol. 74, 448-455
30. Proudfoot, A. E. I., Handel, T. M., Johnson, Z., Lau, E. K., LiWang, P., Clark-Lewis, I., Borlat, F., Wells, T. N. C., and Kosco-Vilbois, M. H. (2003) Glycosaminoglycan binding and oligomerization are essential for the in vivo activity of certain chemokines Proc. Natl. Acad. Sci. U.S.A. 100, 1885-1890
31. Hoogewerf, A. J., Kuschert, G. S. V., Proudfoot, A. E. I., Borlat, F., ClarkLewis, I., Power, C. A., and Wells, T. N. C. (1997) Glycosaminoglycans mediate cell surface oligomerization of chemokines Biochemistry 36, 13570-13578
32. Springael, J. Y., Urizar, E., and Parmentier, M. (2005) Dimerization of chemokine receptors and its functional consequences Cytokine Growth Factor Rev. 16, 611-623
33. Lau, E. K., Paavola, C. D., Johnson, Z., Gaudry, J. P., Geretti, E., Borlat, F., Kungl, A. J., Proudfoot, A. E., and Handel, T. M. (2004) Identification of the glycosaminoglycan binding site of the CC chemokine, MCP-1-Implications for structure and function in vivo J. Biol. Chem. 279, 22294-22305
34. Crown, S. E., Yu, Y. H., Sweeney, M. D., Leary, J. A., and Handel, T. M. (2006) Heterodimerization of CCR2 chemokines and regulation by glycosaminoglycan binding J. Biol. Chem. 281, 25438-25446
35. Shaw, J. P., Johnson, Z., Borlat, F., Zwahlen, C., Kungl, A., Roulin, K., Harrenga, A., Wells, T. N. C., and Proudfoot, A. E. I. (2004) The X-ray structure of RANTES: heparin-derived disaccharides allows the rational design of chemokine inhibitors Structure 12, 2081-2093
36. Murphy, J. W., Cho, Y., Sachpatzidis, A., Fan, C. P., Hodsdon, M. E., and Lolis, E. (2007) Structural and functional basis of CXCL12 (strornal cell-derived factor-1 alpha) binding to heparin J. Biol. Chem. 282, 10018-10027
37. Proudfoot, A. E. I., Fritchley, S., Borlat, F., Shaw, J. P., Vilbois, F., Zwahlen, C., Trkola, A., Marchant, D., Clapham, P. R., and Wells, T. N. C. (2001) The BBXB motif of RANTES is the principal site for heparin binding and controls receptor selectivity J. Biol. Chem. 276, 10620-10626
38. McCornack, M. A., Cassidy, C. K., and LiWang, P. J. (2003) The binding surface and affinity of monomeric and dimeric chemokine macrophage inflammatory protein 1 beta for various glycosaminoglycan disaccharides J. Biol. Chem. 278, 1946-1956
39. Murphy, K. J., Merry, C. L. R., Lyon, M., Thompson, J. E., Roberts, I. S., and Gallagher, J. T. (2004) A new model for the domain structure of heparan sulfate based on the novel specificity of K5 lyase J. Biol. Chem. 279, 27239-27245
40. Imberty, A., Lortat-Jacob, H., and Perez, S. (2007) Structural view of glycosaminoglycan-protein interactions Carbohydr. Res. 342, 430-439
41. Hricovini, M. and Torri, G. (1995) Dynamics in aqueous solutions of the pentasaccharide corresponding to the binding site of heparin for antithrombin III studied by NMR relaxation measurements Carbohydr. Res. 268, 159-175
42. Philpott, M. P. (2003) Defensins and acne Mol. Immunol. 40, 457-462
43. Seo, E. S., Vargues, T., Clarke, D. J., Uhrin, D., and Campopiano, D. J. (2009) Preparation of isotopically labelled recombinant beta-defensin for NMR studies Protein Expression Purif. 65, 179-184
44. Lyon, M., Deakin, J. A., Lietha, D., Gherardi, E., and Gallagher, J. T. (2004) The interactions of hepatocyte growth factor/scatter factor and its NK1 and NK2 variants with glycosaminoglycans using a modified gel mobility shift assay. Elucidation of the minimal size of binding and activatory oligosaccharides J. Biol. Chem. 279, 43560-43567
45. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2, 661-665
46. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59, 687-696
47. Masterson, L. R., Mascioni, A., Traaseth, N. J., Taylor, S. S., and Veglia, G. (2008) Allosteric cooperativity in protein kinase A Proc. Natl. Acad. Sci. U.S.A. 105, 506-511
48. Iwahara, J., Jung, Y. S., and Clore, G. M. (2007) Heteronuclear NMR spectroscopy for lysine NH(3) groups in proteins: unique effect of water exchange on (15)N transverse relaxation J. Am. Chem. Soc. 129, 2971-2980
49. Wu, D., Chen, A., and Johnson, C. S., Jr. (1995) An improved diffusion-ordered spectroscopy bipolar-gradient pulses J. Magn. Reson., Ser. A 115, 260-264
50. Kay, L. E., Nicholson, L. K., Delaglio, F., Bax, A., and Torchia, D. A. (1992) Pulse sequences for removal of the effects of cross-correlation between dipolar and chemical shift anisotropy relaxation mechanism on the measurement of heteronuclear T1 and T2 values in proteins J. Magn. Reson. 97, 359-375
51. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques Biochemistry 38, 16424-16431
52. de la Torre, J. G., Huertas, M. L., and Carrasco, B. (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure Biophys. J. 78, 719-730
53. de la Torre, J. G., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147, 138-146
54. Palmer, A. G. (2001) NMR probes of molecular dynamics: overview and comparison with other techniques Annu. Rev. Biophys. Biomol. Struct. 30, 129-155
55. Lee, A. L. and Wand, A. J. (1999) Assessing potential bias in the determination of rotational correlation times of proteins by NMR relaxation J. Biomol. NMR 13, 101-112
56. Johnson, C. S., Jr (1999) Diffusion ordered nuclear magnetic resonance spectroscopy: principles and applications Prog. Nucl. Magn. Reson. Spectrosc. 34, 203-256
57. Jansma, A. L., Kirkpatrick, J. P., Hsu, A. R., Handel, T. M., and Nietlispach, D. (2010) NMR analysis of the structure, dynamics, and unique oligomerization properties of the chemokine CCL27 J. Biol. Chem. 285, 14424-14437
58. Vives, R. R., Sadir, R., Imberty, A., Rencurosi, A., and Lortat-Jacob, H. (2002) A kinetics and modeling study of RANTES(9-68) binding to heparin reveals a mechanism of cooperative oligomerization Biochemistry 41, 14779-14789
59. Silipo, A., Zhang, Z. Q., Canada, F. J., Molinaro, A., Linhardt, R. J., and Jimenez-Barbero, J. (2008) Conformational analysis of a dermatan sulfate-derived tetrasaccharide by NMR, molecular modeling, and residual dipolar couplings ChemBioChem 9, 240-252