High-resolution solution structure of a designed peptide bound to lipopolysaccharide: Transferred nuclear overhauser effects, micelle selectivity, and anti-endotoxic activity

Biochemistry

Volumn 46, Issue 20, 2007, Pages 5864-5874

  Bhattacharjya, Surajit ^a   Domadia, Prerna N ^a   Bhunia, Anirban ^a   Malladi, Subbalakshmi ^b   David, Sunil A ^b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC STRUCTURE; ANTI-ENDOTOXIC ACTIVITY; LIPOPOLYSACCHARIDE;

AMINO ACIDS; HYDROPHOBICITY; LIPIDS; MICELLES; SOLUTIONS; SPECTROSCOPIC ANALYSIS;

PEPTIDES;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; AROMATIC AMINO ACID; DODECYL SULFATE SODIUM; DODECYLPHOSPHORYLCHOLINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; PEPTIDE; PROTEIN YW12; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; BETA CHAIN; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; FLUORESCENCE; HUMAN; HUMAN CELL; HYDROPHOBICITY; MICELLE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN STRUCTURE; SEPSIS; ULTRAVIOLET SPECTROSCOPY;

ANTI-BACTERIAL AGENTS; CRYSTALLOGRAPHY, X-RAY; DRUG DESIGN; ENDOTOXINS; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; OLIGOPEPTIDES; PROTEIN BINDING; PROTEIN CONFORMATION; SOLUTIONS;

EID: 34248995513     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi6025159     Document Type: Article

References (54)

1. Raetz, C. R. H., and Whitfield, C. (2002) Lipopolysaccharide endotoxins, Annu. Rev. Biochem. 71, 635-700.
2. Rietschel, E. T., Kirikae, T., Schade, F. U., Mamat, U., Schmidt, G., Loppnow, H., Ulmer. A. J., Zahringer, U., Seydel, U., Di Padova, F., Schreier, M., and Brade, H. (1994) Bacterial endotoxin: molecular relationships of structure to activity and function, FASEB J. 8, 217-225.
3. Hancock, R. E., and Scott, M. G. (2000) The vole of antimicrobial peptides in animal defenses, Proc. Natl. Acad. Sci. U.S.A. 97, 8856-8861.
4. Dinarello, C. A. (1996) Cytokines as mediators in the pathogenesis of septic shock, Curr. Top. Microbiol. Immunol. 216, 133-165.
5. Cohen, J. (2002) The immunopathogenesis of sepsis, Nature 420, 885-891.
6. Zhang, F. X., Krisching, C. J., Mancinelli, R., Xu, X. P., Jin, Y., Faure, E., Mantovani, A., Rothe, M., Muzio, M., and Arditi, M. (1999) Bacterial lipopolysaccharide activates nuclear factorkappaB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes, J. Biol. Chem. 274, 7611-7614.
7. Fink, P. F. (1990) In Sepsis Syndrome. Handbook of Critical Care (Berk, J. L., and Sampliner, J. E., Eds.), Little Brown and Co.: Boston.
8. Hardaway, R. M. (2000) Traumatic shock alias post-trauma critical illness, Am. Surg. 66, 22-29.
9. Schumann, R. R., Leong, S. R., Flaggs, G. W., Gray, P. W., Wright, S. D., Mathison, J. C., Tobias, P. S., and Ulevitch, R. J. (1990) Structure and function of lipopolysaccharide binding protein, Science 249, 1429-1431.
10. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., and Mathison, J. C. (1990) CD14, a receptor for complexes of lipopolvsaccharide (LPS) and LPS binding protein. Science 249, 1431-1433.
11. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffet, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene, Science 282, 2085-2088.
12. Lee, H. K., Dunzendorfer, S., and Tobias, P. S. (2004) Cytoplasmic domain-mediated dimerizations of toll-like receptor 4 observed by beta-lactamase enzyme fragment complementation, J. Biol. Chem. 279, 10564-10574.
13. Martin, G. S., Mannino, D. M., Eaton, S., and Moss, M. (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348, 1546-1554.
14. David, S. A. (2001) Towards a rational development of anti-ednotoxin agents: novel approaches to sequestration of bacterial endotoxins with small molecules, J. Mol. Recognit. 14, 370-387.
15. Boman, H. G. (1995) Peptide antibiotics and their role in innate immunity, Annu. Rev. Immunol. 13, 61-92.
16. Scott, M. G., Yan, H., and Hancock, R. E. (1999) Biological properties of structurally related alpha-helical cationic antimicrobial peptides, Infect. Immun. 67, 2005-2009.
17. David, S. A., Awasthi, S. K., and Balaram, P. (2000) The role of polar and facial amphipathic character in determining lipopolysaccharide-binding properties in synthetic cationic peptides, J. Endotoxin Res. 6, 249-256.
18. Muhle, S. A., and Tarn, J. P. (2001) Design of Gram-negative selective antimicrobial peptides, Biochemistry 40, 5777-5785.
19. Scott, M. G., Vreugdenhil, A. C., Buurman, W. A., Hancock, R. E., and Gold, M. R. (2000) Cutting edge: cationic antimicrobial peptides block the binding of lipopolysaccharide (LPS) to LPS binding protein, J. Immunol. 164, 549-553.
20. Jerala, R., and Porro, M. (2004) Endotoxin neutralizing peptides. Curr. Top. Med. Chem. 4, 1173-1184.
21. Tan, N. G., NG. M., Yau, Y., Chong, P. K., Ho. B., and Ding, J. L. (2000) Definition of endotoxin binding sites in horseshoe crab factor C recombinant sushi proteins and neutralization of endotoxin by sushi peptides, FASEB, J. 14, 1801-1813.
22. Rustici, A., Velucchi, M., Faggioni, R., Sironi, M., Ghezzi, P., Quataert, S., Green, B., and Porro, M. (1993) Molecular mapping and detoxification of the lipid A binding site by synthetic peptides, Science 259, 361-365.
23. Pristovsek, P., and Kidric, J. (2004) The search for molecular determinants of LPS inhibition by proteins and peptides, Curr. Top. Med. Chem. 4, 1185-1201.
24. Clore. G. M., and Gronenborn, A. M. (1982) Theory of the time dependent transferred nuclear Overhauser effect: applications to ligand protein complexes in solution. J. Magn. Reson. 48, 402-417.
25. Post, C. B. (2003) Exchange-transferred NOE spectroscopy and bound ligand structure determination, Curr. Opin. Struct. Biol. 13, 581-588.
26. Guntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA, J. Mol. Biol. 273, 283-298.
27. 1H NMR, Biochemistry 31, 11973-11977.
28. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function, J. Comput. Chem. 19, 1639-1662.
29. Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K, and Weite, W. (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide, Science 282, 2215-2220.
30. Rietschel, E. T., Brade, H., Brade, L., Brandenburg, K., Schade, U. F., Seydel, U., Zahringer, U., Galanos, C., Luderitz, O., Westphal, O., Labischinski, H., Kusumoto, S., and Shiba, T. (1987) Lipid A, the endotoxic center of bacterial lipopolysaccharides: relation of chemical structure to biological activity, Prog. Clin. Biol. Res. 231, 25-53.
31. Ferguson, A. D., Welte, W., Hofmann, E., Linder, B., Holst, O., Coulton, J. W., and Diederichs, K. (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins, Structure 8, 585-592.
32. Schibli, D. J., Epand, R. F., Vogel, H. J., and Epand, R. M. (2002) Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions, Biochem. Cell Biol. 80, 667-677.
33. Bishop, C. M., Walkenhorst, W. F., and Wimley, W. C. (2001) Folding of β-sheets in membranes: specificity and promiscuity in peptide model systems, J. Mol. Biol. 309, 975-988.
34. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, John Wiley & Sons, New York.
35. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms, Nature 415, 389-395.
36. Santos, N. C., Silva, A. C., Castanho, M. A., Martins-Silva, J., and Saldanha, C. (2003) Evaluation of lipopolysaccharide aggregation by light scattering spectroscopy, ChemBioChem 4, 96-100.
37. Bhattacharjya, S., David, S. A., Madian, V. I., and Balaram, P. (1997) Polymyxin B nonapeptide: conformations in water and in lipopolysaccharide-bound state determined by two-dimensional NMR and molecular dynamics. Biopolymers 41, 251-265.
38. Pristovsek, P., and Kidric, J. (1999) Solution structure of polymyxins B and E and effect of binding to lipopolysaccharide: an NMR and molecular modeling study, J. Med. Chem. 42, 4604-4613.
39. Japelj, B., Pristovsek, P., Majerle, A., and Jerala, R. (2005) Structural origin of endotoxin neutralization and antimicrobial activity of a lactoferrin-based peptide. J. Biol. Chem. 280, 16955-16961.
40. Lakowicz, J. R. (1983) Principles of Fluorescence Spectroscopy, Plenum press, New York.
41. Adler, A. J., Greenfield, N. J., and Fasman, G. D. (1973) Circular dichroism and optical rotatory dispersion of proteins and polypeptide, Methods Enzymol. 27, 675-735.
42. Woody, R. W. (1994) Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins, Eur. Biophys. J. 23, 253-262.
43. Chan, D. I., Premier, E. J., and Vogel, H. J. (2006) Tryptophanand arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta 1758, 1184-1202.
44. Pristovsek, P., Feher, K., Szilagyi, L., and Kidric, J. (2005) Structure of a synthetic fragment of the LALF protein when bound to lipopolysaccharide. J. Med. Chem. 48, 1666-1670.
45. Pristovsek, P., Simcic, S., Wraber, B., and Urleb, U. (2005) Structure of a synthetic fragment of the lipopolysaccharide (LPS) binding protein when bound to LPS and design of a peptidic LPS inhibitor, J. Med. Chem. 48, 7911-7914.
46. Schibli, D. J., Hwang, P. M., and Vogel, H. J. (1999) Structure of the antimicrobial peptide tritrpticin bound to micelles: a distinct membrane-bound peptide fold. Biochemistry 38, 16794-16755.
47. Rozek, A., Friedrich, C. L., and Hancock, R. E. (2000) Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 39, 15765-15774.
48. Inagaki, F., Shimada, L. Kawaguchi, K., Hirano, M., Terasawa, I., Ikura, T., and Go, N. (1989) Structure of melittin bound to perdeuterated dodecylphosphocholine micelles as studied by twodimensional NMR and distance geometry calculations, Biochemistry 28, 5985-5991.
49. Wang, G., Li, Y., and Li, X. (2005) Correlation of three-dimensional structures with the antibacterial activity of a group of peptides designed based on a nontoxic bacterial membrane anchor. J. Biol. Chem. 280, 5803-5811.
50. Powers, J. P., Tan, A., Ramaoorthy, A., and Hancock, R. E. (2005) Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes. Biochemistry 44, 15504-15513.
51. Jing, W., Demcoe, A. R., and Vogel, H. J. (2003) Conformation of a bactericidal domain of puroindoline a: structure and mechanism of action of a 13-residue antimicrobial peptide. J. Bacterial. 185, 4938-4947.
52. Brogden, K. A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria. Nature 3, 238-250.
53. Hwang, P. M., and Vogel, H. J. (1998) Structure-function relationships of antimicrobial peptides. Biochem. Cell Biol. 76, 235-246.
54. Matsuzaki, K. (1999) Why and how are peptides-lipid interactions utilized for self-defense? magainins and tachyplesins as archetypes, Biochim. Biophys. Acta 1462, 1-10.