Conformation of a bactericidal domain of puroindoline a: Structure and mechanism of action of a 13-residue antimicrobial peptide

Journal of Bacteriology

Volumn 185, Issue 16, 2003, Pages 4938-4947

  Jing, Weiguo ^a   Demcoe, Alistair R ^a   Vogel, Hans J ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DYE; INDOLE; PEPTIDE; PUROINDOLINE; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERICIDAL ACTIVITY; BILAYER MEMBRANE; CONTROLLED STUDY; ENERGY TRANSFER; EUKARYOTE; FLUORESCENCE SPECTROSCOPY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; MICELLE; MICROCALORIMETRY; MOLECULAR INTERACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SURFACE CHARGE; WHEAT;

AMINO ACID SEQUENCE; ANTIMICROBIAL CATIONIC PEPTIDES; CALORIMETRY; CELL MEMBRANE; CIRCULAR DICHROISM; ESCHERICHIA COLI; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; PLANT PROTEINS; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; STAPHYLOCOCCUS AUREUS; STRUCTURE-ACTIVITY RELATIONSHIP;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; POSIBACTERIA; TRITICUM AESTIVUM;

EID: 0042060932     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.16.4938-4947.2003     Document Type: Article

References (67)

1. Ames, B. N. 1966. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 8:115-118.
2. Blocher, J. E., C. Chevalier, and D. Marion. 1993. Complete amino acid sequence of puroindoline, a new basic and cystine-rich protein with a unique tryptophan-rich domain, isolated from wheat endosperm by Triton X-114 phase partitioning. FEBS Lett. 3:336-340.
3. Blondelle, S. E., and R. A. Houghten. 1992. Design of model amphipathic peptides having potent antimicrobial activities. Biochemistry 31:12688-12694.
4. Boman, H. G. 1995. Peptide antibiotics and their role in innate immunity. Annu. Rev. Immunol. 13:61-92.
5. Boman, H. G., B. Agerberth, and A. Boman. 1993. Mechanisms of action on Escherichia coli of cecropin PI and PR-39, two antibacterial peptides from pig intestine. Infect. Immun. 61:2978-2984.
6. Braunschweiller, L., and R. R. Ernst. 1983. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53:521-528.
7. Brunger, A. T., P. D. Adams, G. M. Clore, W. L. Delano, P. Gros, R. W. Grosse Kunstleve, J. S. Jiang, J. Kuszwski, 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 54:905-921.
8. Cammue, B. P., K. Thevissen, M. Hendriks, K. Eggermont, I. J. Goderis, P. Proost, J. Van Damme, R. W. Osborn, F. Guerbette, and J. C. Kader. 1995. A potent antimicrobial protein from onion seeds showing sequence homology to plant lipid transfer proteins. Plant Physiol. 109:445-455.
9. 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.
10. Dougherty, D. A. 1996. Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271:163-168.
11. Eftink, M. R., and C. A. Ghiron. 1976. Fluorescence quenching of indole and model micelles system. J. Phys. Chem. 80:486-493.
12. El Jastimi, R., K. Edwards, and M. Lafleur. 1999. Characterization of permeability and morphological perturbations induced by nisin on phosphatidylcholine membranes. Biophys. J. 77:842-852.
13. Epand, R. M., and H. J. Vogel. 1999. Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462:11-28.
14. Fimland, G., V. G. Eijsink, and J. Nissen-Meyer. 2002. Mutational analysis of the role of tryptophan residues in an antimicrobial peptide. Biochemistry 41:9508-9515.
15. Friedrich, C. L., A. Rozek, A. Patrzykat, and R. E. W. Hancock. 2001. Structure and mechanism of action of an indolicidin peptide derivative with improved activity against gram-positive bacteria. J. Biol. Chem. 276:24015-24022.
16. Gallivan, J. P., and D. A. Dougherty. 1999. Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. USA 96:9459-9464.
17. Gazit, E., and Y. Shai. 1993. Structural and functional characterization of the alpha 5 segment of Bacillus thuringiensis delta-endotoxin. Biochemistry 32:3429-3436.
18. Guerneve, C. L., M. Seigneuret, and D. Marion. 1998. Interaction of the wheat endosperm lipid-binding protein puroindoline-a with phospholipids. Arch. Biochem. Biophys. 360:179-186.
19. Hancock, R. E. W., and R. Lehrer. 1998. Cationic peptides: a new source of antibiotics. Trends Biotechnol. 16:82-88.
20. Hancock, R. E. W., T. Falla, and M. Brown. 1995. Cationic bactericidal peptides. Adv. Microb. Physiol. 37:135-175.
21. Hwang, P. M., and H. J. Vogel. 1998. Structure-function relationships of antimicrobial peptides. Biochem. Cell Biol. 76:235-246.
22. Jeener, J., B. H. Meier, P. Bachmann, and R. R. Ernst. 1979. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71:4546-4553.
23. 2 bound to micelles and its interactions with phospholipid bilayers. J. Pept. Res. 61:219-229.
24. 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.
25. Killian, J. A., J. W. Timmermans, S. Keur, and B. De Kruijff. 1985. The tryptophans of gramicidin are essential for the lipid structure modulating effect of the peptide. Biochim. Biophys. Acta 820:154-156.
26. Koradi, R., M. Billeter, and K. Wüthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14:51-55.
27. Krishnamurthy, K., C. Balconi, J. E. Sherwood, and M. J. Giroux. 2001. Wheat puroindolines enhance fungal disease resistance in transgenic rice. Mol. Plant-Microbe Interact. 14:1255-1260.
28. Lakowicz, J. R. 1999. Principles of fluorescence spectroscopy. Plenum Press, New York, N.Y.
29. Latal, A., G. Degovics, R. F. Epand, R. M. Epand, and K. Lohner. 1997. Structural aspects of the interaction of peptidyl-glycylleucine-carboxyamide, a highly potent antimicrobial peptide from frog skin, with lipids. Eur. J. Biochem. 248:938-946.
30. Lawyer, C., S. Pai, M. Watabe, P. Borgia, T. Mashimo, L. Eagleton, and K. Watabe. 1996. Antimicrobial activity of a 13 amino acid tryptophan-rich peptide derived from a putative porcine precursor protein of a novel family of antibacterial peptides. FEBS Lett. 390:95-98.
31. MacKenzie, K. R., J. H. Prestegard, and D. M. Engelman. 1997. A transmembrane helix dimer: structure and implications. Science 276:131-133.
32. Marion, D., M. F. Gautier, P. Joudrier, M. Ptak, M. Pezolet, M. Forest, D. C. Clark, and W. Broekaert. 1994. In Processing of the wheat kernel proteins - molecular and functional aspects, p. 175-180. Universita della Tuscia, Viterbo, Italy.
33. Matsuzaki, K., S. Nakai, T. Handa, Y. Takaishi, T. Fujita, and K. Miyajima. 1989. Hypelcin A, an alpha-aminoisobutyric acid containing antibiotic peptide, induced permeability change of phosphatidylcholine bilayers. Biochemistry 28:9392-9398.
34. Matsuzaki, K., K. Sugishita, N. Ishibe, M. Ueha, S. Nakata, K. Miyajima, and R. M. Epand. 1998. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37:11856-11863.
35. McElhaney, R. N. 1986. Differential scanning calorimetric studies of lipid-protein interactions in model membrane systems. Biochim. Biophys. Acta 864:361-421.
36. McElhaney, R. N. 1982. The use of differential scanning calorimetry and differential thermal analysis in studies of model and biological membranes. Chem. Phys. Lipids 30:229-259.
37. Morris, C. F. 2002. Puroindolines: the molecular genetic basis of wheat grain hardness. Plant Mol. Biol. 48:633-647.
38. Nicolas, P., and A. Mor. 1995. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 49:277-304.
39. Nilges, M. 1995. Calculation of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE crosspeaks and disulphide connectivities. J. Mol. Biol. 245:645-660.
40. Oren, Z., and Y. Shai. 1998. Mode of action of linear amphipathic alpha-helical antimicrobial peptides. Biopolymers 47:451-4613.
41. Park, C.-B., H.-S. Kim, and S.-C. Kim. 1998. Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244:253-257.
42. Perczel, A., and M. Hollosi. 1996. Turns, p. 285-380. In G. D. Fasman (ed.), Circular dichroism and the conformational analysis of biomolecules. Plenum Press, New York, N.Y.
43. Rance, M., O. W. Sorenson, G. Bodenhausen, G. Wagner, R. R. Ernst, and K. Wüthrich. 1983. Improved spectral resolution in COSY 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:479-485.
44. Rapaport, D., and Y. Shai. 1991. Interaction of fluorescently labeled pardaxin and its analogues with lipid bilayers. J. Biol. Chem. 266:23769-23775.
45. Reithmeier, R. A. 1995. Characterization and modeling of membrane proteins using sequence analysis. Curr. Opin. Struct. Biol. 5:491-500.
46. Rinaldi, A. C., M. L. Mangoni, A. Rufo, C. Luzi, D. Barra, H. Zhao, P. K. Kinnunen, A. Bozzi, A. Di Giulio, and M. Simmaco. 2002. Temporin L: antimicrobial, haemolytic and cytotoxic activities, and effects on membrane permeabilization in lipid vesicles. Biochem. J. 368:91-100.
47. Rozek, A., C. L. Friedrich, and R. E. W. Hancock. 2000. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 39:15765-15774.
48. Schibli, D. J., R. F. Epand, H. J. Vogel, and R. M. Epand. 2002. Tryptophan-rich antimicrobial peptides: comparative properties and membrane interactions. Biochem. Cell Biol. 80:667-677.
49. Schibli, D. J., P. M. Hwang, and H. J. Vogel. 1999. Structure of the antimicrobial peptide tritrpticin bound to micelles: a distinct membrane-bound peptide fold. Biochemistry 38:16749-16755.
50. Schibli, D. J., R. C. Montelaro, and H. J. Vogel. 2001. The membrane-proximal tryptophan-rich region of the HIV glycoprotein, gp41, forms a well-defined helix in dodecylphosphocholine micelles. Biochemistry 40:9570-9578.
51. Schiffer, M., M. H. Chang, and F. J. Stevens. 1992. The functions of tryptophan residues in membrane proteins. Protein Eng. 5:213-214.
52. Selsted, M. E., M. J. Novotny, W. L. Morris, Y. Q. Tang, W. Smith, and J. S. Cullor. 1992. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem. 267:4292-4295.
53. Shai, Y. 1999. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta 1462:55-70.
54. Strom, M. B., O. Rekdal, and J. S. Svendsen. 2002. Antimicrobial activity of short arginine- and tryptophan-rich peptides. J. Pept. Sci. 8:431-437.
55. Tassin, S., W. F. Broekaert, D. Marion, D. Acland, M. Ptak, F. Vovelle, and P. Sodano. 1998. Solution structure of Ace-AMP1, a potent antimicrobial protein extracted from onion seeds. Structural analogies with plant nonspecific lipid transfer proteins. Biochemistry 37:3623-3637.
56. Tinoco, L. W., A. Silva, A. Leite, and A. Valente. 2002. NMR structure of PW2 bound to SDS micelles. A tryptophan-rich anticoccidial peptide selected from phage display libraries. J. Biol. Chem. 277:36351-36356.
57. Vogel, H. J., D. J. Schibli, W. Jing, E. M. Lohmeier-Vogel, R. F. Epand, and R. M. Epand. 2002. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell Biol. 80:49-63.
58. Wenk, M. R., and J. Seelig. 1998. Magainin 2 amide interaction with lipid membranes: calorimetric detection of peptide binding and pore formation. Biochemistry 37:3909-3916.
59. Wieprecht, T., M. Beyermann, and J. Seelig. 1999. Binding of antibacterial magainin peptides to electrically neutral membranes: thermodynamics and structure. Biochemistry 38:10377-10387.
60. Wimley, W. C., and S. H. White. 1996. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:842-848.
61. Woody, R. W. 1994. Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins. Eur. Biophys. J. 23:253-262.
62. Wu, M., E. Maier, R. Benz, and R. E. W. Hancock. 1999. Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38:7235-7242.
63. Wüthrich, K. 1986. NMR of proteins and nucleic acids, p. 130-161. John Wiley and Sons, New York, N.Y.
64. Yang, S.-T., S. Shin, Y.-C. Kim, Y. Kim, K.-S. Hahm, and J. Kim. 2002. Conformation-dependent antibiotic activity of tritrpticin, a cathelicidin-derived antimicrobial peptide. Biochem. Biophys. Res. Commun. 296:1044-1050.
65. Yau, W.-M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry 37:14713-14718.
66. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395.
67. Zhang, Y.-P., R. N. A. H. Lewis, and R. N. McElhaney. 1997. Calorimetric and spectroscopic studies of the thermotropic phase behavior of the n-saturated 1,2 diacylphosphatidylglycerols. Biophys. J. 72:779-793.