Dimerization of plant defensin NaD1 enhances its antifungal activity

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 19961-19972

  Lay, Fung T ^a,b   Mills, Grant D ^a,b   Poon, Ivan K H ^a   Cowieson, Nathan P ^c   Kirby, Nigel ^c   Baxter, Amy A ^a,b   Van Der Weerden, Nicole L ^a,b   Dogovski, Con ^a   Perugini, Matthew A ^a   Anderson, Marilyn A ^a,b   Kvansakul, Marc ^a   Hulett, Mark D ^a,b,c  

^a LA TROBE UNIVERSITY   (Australia)

^b Hexima Limited   (Australia)

^c AUSTRALIAN SYNCHROTRON   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; ANTI-FUNGAL ACTIVITY; CATIONIC PEPTIDES; CROP PROTECTION; CRYSTAL FORMS; DEFENSINS; DIMER FORMATION; FILAMENTOUS FUNGI; FUNGAL PATHOGEN; FUSARIUM OXYSPORUMS; HIGH RESOLUTION; INHIBITORY ACTIVITY; MOLECULAR BASIS; PROTEIN CROSSLINKING; SITE DIRECTED MUTAGENESIS; SMALL ANGLE X-RAY SCATTERING; STRUCTURAL STUDIES;

CENTRIFUGATION; DIMERS; FUNGI;

DIMERIZATION;

DEFENSIN; PROTEIN NAD1; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIFUNGAL ACTIVITY; ARTICLE; BOTRYTIS CINEREA; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTALLIZATION; DIMERIZATION; FUSARIUM OXYSPORUM; MEMBRANE PERMEABILITY; NICOTIANA; NICOTIANA ALATA; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY;

ANTI-INFECTIVE AGENTS; CRYSTALLOGRAPHY, X-RAY; DEFENSINS; FUSARIUM; MUTAGENESIS, SITE-DIRECTED; PLANT DISEASES; PLANT PROTEINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; TOBACCO;

FUNGI; FUSARIUM OXYSPORUM; NICOTIANA ALATA;

EID: 84862017137     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.331009     Document Type: Article

References (91)

1. De-Paula, V. S., Razzera, G., Medeiros, L., Miyamoto, C. A., Almeida, M. S., Kurtenbach, E., Almeida, F. C., and Valente, A. P. (2008) Evolutionary relationship between defensins in the Poaceae family strengthened by the characterization of new sugarcane defensins. Plant Mol. Biol. 68, 321-335
2. Graham, M. A., Silverstein, K. A., Cannon, S. B., and VandenBosch, K. A. (2004) Computational identification and characterization of novel genes from legumes. Plant Physiol. 135, 1179-1197 (Pubitemid 39009369)
3. Mergaert, P., Nikovics, K., Kelemen, Z., Maunoury, N., Vaubert, D., Kondorosi, A., and Kondorosi, E. (2003)Anovel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol. 132, 161-173 (Pubitemid 36590408)
4. Silverstein, K. A., Graham, M. A., Paape, T. D., and VandenBosch, K. A. (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol. 138, 600-610 (Pubitemid 43793143)
5. Silverstein, K. A., Moskal, W. A., Jr., Wu, H. C., Underwood, B. A., Graham, M. A., Town, C. D., and VandenBosch, K. A. (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J. 51, 262-280 (Pubitemid 47030121)
6. Broekaert, W. F., Terras, F. R., Cammue, B. P., and Osborn, R. W. (1995) Plant defensins. Novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108, 1353-1358
7. Lay, F. T., and Anderson, M. A. (2005) Defensins-Components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85-101 (Pubitemid 40259804)
8. Janssen, B. J., Schirra, H. J., Lay, F. T., Anderson, M. A., and Craik, D. J. (2003) Structure of Petunia hybrida defensin 1, a novel plant defensin with five disulfide bonds. Biochemistry 42, 8214-8222 (Pubitemid 36858982)
9. Lay, F. T., Brugliera, F., and Anderson, M. A. (2003) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol. 131, 1283-1293 (Pubitemid 36400360)
10. Lay, F. T., Schirra, H. J., Scanlon, M. J., Anderson, M. A., and Craik, D. J. (2003) The three-dimensional solution structure of NaD1, a new floral defensin from Nicotiana alata and its application to a homology model of the crop defense protein alfAFP. J. Mol. Biol. 325, 175-188 (Pubitemid 36153006)
11. Almeida, M. S., Cabral, K. M., Kurtenbach, E., Almeida, F. C., and Valente, A. P. (2002) Solution structure of Pisum sativum defensin 1 by high resolution NMR. Plant defensins, identical backbone with different mechanisms of action. J. Mol. Biol. 315, 749-757 (Pubitemid 34729323)
12. 1H NMR structure of an antifungal γ-thionin protein SIα1. Similarity to scorpion toxins. Proteins 32, 334-349
13. 1H NMR studies on the structure of a new thionin from barley endosperm. Biopolymers 36, 751-763
14. 1H NM. A structural motif common to toxic arthropod proteins. Biochemistry 32, 715-724
15. de Paula, V. S., Razzera, G., Barreto-Bergter, E., Almeida, F. C., and Valente, A. P. (2011) Portrayal of complex dynamic properties of sugarcane defensin 5 by NMR. Multiple motions associated with membrane interaction. Structure 19, 26-36
16. Fant, F., Vranken, W., Broekaert, W., and Borremans, F. (1998) Determination of the three-dimensional solution structure of Raphanus sativus antifungal protein 1 by 1H NMR. J. Mol. Biol. 279, 257-270 (Pubitemid 28252144)
17. Fant, F., Vranken, W. F., and Borremans, F. A. (1999) The three-dimensional solution structure of Aesculus hippocastanum antimicrobial protein 1 determined by 1H nuclear magnetic resonance. Proteins 37, 388-403 (Pubitemid 29519729)
18. Lin, K. F., Lee, T. R., Tsai, P. H., Hsu, M. P., Chen, C. S., and Lyu, P. C. (2007) Structure-based protein engineering for α-amylase inhibitory activity of plant defensin. Proteins 68, 530-540
19. Liu, Y. J., Cheng, C. S., Lai, S. M., Hsu, M. P., Chen, C. S., and Lyu, P. C. (2006) Solution structure of the plant defensin VrD1 from mung bean and its possible role in insecticidal activity against bruchids. Proteins 63, 777-786
20. Song, X., Zhang, M., Zhou, Z., and Gong, W. (2011) Ultra-high resolution crystal structure of a dimeric defensin SPE10. FEBS Lett. 585, 300-306
21. Osborn, R. W., De Samblanx, G. W., Thevissen, K., Goderis, I., Torrekens, S., Van Leuven, F., Attenborough, S., Rees, S. B., and Broekaert, W. F. (1995) Isolation and characterization of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae, and Saxifragaceae. FEBS Lett. 368, 257-262
22. Terras, F. R., Schoofs, H. M., De Bolle, M. F., Van Leuven, F., Rees, S. B., Vanderleyden, J., Cammue, B. P., and Broekaert, W. F. (1992) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267, 15301-15309
23. Thomma, B. P., Cammue, B. P., and Thevissen, K. (2002) Plant defensins. Planta 216, 193-202 (Pubitemid 36761777)
24. van der Weerden, N. L., Hancock, R. E., and Anderson, M. A. (2010) Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall-dependent process. J. Biol. Chem. 285, 37513-37520
25. van der Weerden, N. L., Lay, F. T., and Anderson, M. A. (2008) The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J. Biol. Chem. 283, 14445-14452
26. Franco, O. L., Murad, A. M., Leite, J. R., Mendes, P. A., Prates, M. V., and Bloch, C., Jr. (2006) Identification of a cowpea γ-thionin with bactericidal activity. FEBS J. 273, 3489-3497 (Pubitemid 44086949)
27. Segura, A., Moreno, M., Molina, A., and García-Olmedo, F. (1998) Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett. 435, 159-162 (Pubitemid 28434991)
28. Zhang, Y., and Lewis, K. (1997) Fabatins. New antimicrobial plant peptides. FEMS Microbiol. Lett. 149, 59-64 (Pubitemid 27130157)
29. Chen, G. H., Hsu, M. P., Tan, C. H., Sung, H. Y., Kuo, C. G., Fan, M. J., Chen, H. M., Chen, S., and Chen, C. S. (2005) Cloning and characterization of a plant defensin VaD1 from azuki bean. J. Agric. Food Chem. 53, 982-988 (Pubitemid 40270387)
30. Colilla, F. J., Rocher, A., and Mendez, E. (1990) γ-Purothionins. Amino acid sequence of two polypeptides of a new family of thionins from wheat endosperm. FEBS Lett. 270, 191-194 (Pubitemid 20288599)
31. Mendez, E., Moreno, A., Colilla, F., Pelaez, F., Limas, G. G., Mendez, R., Soriano, F., Salinas, M., and de Haro, C. (1990) Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, γ-hordothionin, from barley endosperm. Eur. J. Biochem. 194, 533-539
32. Méndez, E., Rocher, A., Calero, M., Girbés, T., Citores, L., and Soriano, F. (1996) Primary structure of ω-hordothionin, a member of a novel family of thionins from barley endosperm, and its inhibition of protein synthesis in eukaryotic and prokaryotic cell-free systems. Eur. J. Biochem. 239, 67-73 (Pubitemid 26228141)
33. Bloch, C., Jr., and Richardson, M. (1991) A new family of small (5 kDa) protein inhibitors of insect α-amylases from seeds or sorghum (Sorghum bicolar (L) Moench) have sequence homologies with wheat γ-purothionins. FEBS Lett. 279, 101-104
34. Pelegrini, P. B., Lay, F. T., Murad, A. M., Anderson, M. A., and Franco, O. L. (2008) Novel insights on the mechanism of action of α-amylase inhibitors from the plant defensin family. Proteins 73, 719-729 (Pubitemid 352788653)
35. Melo, F. R., Rigden, D. J., Franco, O. L., Mello, L. V., Ary, M. B., Grossi de Sá, M. F., and Bloch, C., Jr. (2002) Inhibition of trypsin by cowpea thionin. Characterization, molecular modeling, and docking. Proteins 48, 311-319 (Pubitemid 34743419)
36. Wijaya, R., Neumann, G. M., Condron, R., Hughes, A. B., and Polya, G. M. (2000) Defense proteins from seed of Cassia fistula include a lipid transfer protein homologue and a protease inhibitory plant defensin. Plant Sci. 159, 243-255
37. Kushmerick, C., de Souza Castro, M., Santos Cruz, J., Bloch, C., Jr., and Beirão, P. S. (1998) Functional and structural features of γ-zeathionins, a new class of sodium channel blockers. FEBS Lett. 440, 302-306 (Pubitemid 29052303)
38. Spelbrink, R. G., Dilmac, N., Allen, A., Smith, T. J., Shah, D. M., and Hockerman, G. H. (2004) Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiol. 135, 2055-2067 (Pubitemid 39182785)
39. Mirouze, M., Sels, J., Richard, O., Czernic, P., Loubet, S., Jacquier, A., François, I. E., Cammue, B. P., Lebrun, M., Berthomieu, P., and Marquès, L. (2006) A putative novel role for plant defensins. A defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J. 47, 329-342 (Pubitemid 44036403)
40. Komori, T., Yamada, S., and Imaseki, H. (1997) cDNA cloning for γ-thionin from Nicotiana paniculata (accession number 005250) (PGR 97-132). Plant Physiol. 115, 314
41. Yamada, S., Komori, T., and Imaseki, H. (1997) cDNA cloning for γ-thionin from Nicotiana paniculata (accession number AB005266) (PGR 97-131). Plant Physiol. 115, 314
42. Koike, M., Okamoto, T., Tsuda, S., and Imai, R. (2002) A novel plant defensin-like gene of winter wheat is specifically induced during cold acclimation. Biochem. Biophys. Res. Commun. 298, 46-53
43. Lay, F. T., Mills, G. D., Hulett, M. D., and Kvansakul, M. (2012) Crystallization and preliminary x-ray crystallographic analysis of the plant defensin NaD1. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 68, 85-88
44. Beck, T., Krasauskas, A., Gruene, T., and Sheldrick, G. M. (2008) A magic triangle for experimental phasing of macromolecules. Acta Crystallogr. D Biol. Crystallogr. 64, 1179-1182
45. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
46. Sheldrick, G. M. (2010) Experimental phasing with SHELXC/D/E. Combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485
47. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
48. Storoni, L. C., McCoy, A. J., and Read, R. J. (2004) Likelihood-enhanced fast rotation functions. Acta Crystallogr. D Biol. Crystallogr. 60, 432-438 (Pubitemid 41087570)
49. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
50. Cabral, K. M., Almeida, M. S., Valente, A. P., Almeida, F. C., and Kurtenbach, E. (2003) Production of the active antifungal Pisum sativum defensin 1 (Psd1) in Pichia pastoris. Overcoming the inefficiency of the STE13 protease. Protein Expr. Purif. 31, 115-122 (Pubitemid 37207649)
51. Chang, T., Schroder, L. A., Thomson, J. M., Klocman, A. S., Tomasini, A. J., Strømhaug, P. E., and Dunn, W. A. (2005) PpATG9 encodes a novel membrane protein that traffics to vacuolar membranes, which sequester peroxisomes during pexophagy in Pichia pastoris. Mol. Biol. Cell 16, 4941-4953 (Pubitemid 41416472)
52. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., eds) pp. 90-125, The Royal Society of Chemistry, Cambridge, UK
53. Perugini, M. A., Schuck, P., and Howlett, G. J. (2000) Self-association of human apolipoprotein E3 and E4 in the presence and absence of phospholipid. J. Biol. Chem. 275, 36758-36765 (Pubitemid 32002083)
54. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
55. Schuck, P., Perugini, M. A., Gonzales, N. R., Howlett, G. J., and Schubert, D. (2002) Size-distribution analysis of proteins by analytical ultracentrifugation. Strategies and application to model systems. Biophys. J. 82, 1096-1111 (Pubitemid 34111246)
56. 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 β-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus. J. Biol. Chem. 277, 8279-8289 (Pubitemid 34968287)
57. Hill, C. P., Yee, J., Selsted, M. E., and Eisenberg, D. (1991) Crystal structure of defensin HNP-3, an amphiphilic dimer. Mechanisms of membrane permeabilization. Science 251, 1481-1485 (Pubitemid 121000438)
58. Hoover, D. M., Chertov, O., and Lubkowski, J. (2001) The structure of human β-defensin-1. New insights into structural properties of β-defensins. J. Biol. Chem. 276, 39021-39026
59. Hoover, D. M., Rajashankar, K. R., Blumenthal, R., Puri, A., Oppenheim, J. J., Chertov, O., and Lubkowski, J. (2000) The structure of human β-defensin-2 shows evidence of higher order oligomerization. J. Biol. Chem. 275, 32911-32918
60. Zhang, Y., Lu, W., and Hong, M. (2010) The membrane-bound structure and topology of a human α-defensin indicate a dimer pore mechanism for membrane disruption. Biochemistry 49, 9770-9782
61. Wei, G., Pazgier, M., de Leeuw, E., Rajabi, M., Li, J., Zou, G., Jung, G., Yuan, W., Lu, W. Y., Lehrer, R. I., and Lu, W. (2010) Trp-26 imparts functional versatility to human α-defensin HNP1. J. Biol. Chem. 285, 16275-16285
62. Song, X., Zhou, Z., Wang, J., Wu, F., and Gong, W. (2004) Purification, characterization, and preliminary crystallographic studies of a novel plant defensin from Pachyrrhizus erosus seeds. Acta Crystallogr. D Biol. Crystallogr. 60, 1121-1124 (Pubitemid 41295455)
63. Song, X., Wang, J., Wu, F., Li, X., Teng, M., and Gong, W. (2005) cDNA cloning, functional expression, and antifungal activities of a dimeric plant defensin SPE10 from Pachyrrhizus erosus seeds. Plant Mol. Biol. 57, 13-20 (Pubitemid 40580439)
64. Bowman, S. M., and Free, S. J. (2006) The structure and synthesis of the fungal cell wall. BioEssays 28, 799-808 (Pubitemid 44433742)
65. Schoffelmeer, E. A., Klis, F. M., Sietsma, J. H., and Cornelissen, B. J. (1999) The cell wall of Fusarium oxysporum. Fungal Genet. Biol. 27, 275-282 (Pubitemid 29412849)
66. Tang, Y. Q., Yuan, J., Osapay, G., Osapay, K., Tran, D., Miller, C. J., Ouellette, A. J., and Selsted, M. E. (1999) A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated α-defensins. Science 286, 498-502
67. Tang, Y. Q., Yuan, J., Miller, C. J., and Selsted, M. E. (1999) Isolation, characterization, cDNA cloning, and antimicrobial properties of two distinct subfamilies of α-defensins from rhesus macaque leukocytes. Infect. Immun. 67, 6139-6144 (Pubitemid 29508147)
68. Lehrer, R. I., and Ganz, T. (2002) Defensins of vertebrate animals. Curr. Opin. Immunol. 14, 96-102 (Pubitemid 34085112)
69. Selsted, M. E., Tang, Y. Q., Morris, W. L., McGuire, P. A., Novotny, M. J., Smith, W., Henschen, A. H., and Cullor, J. S. (1993) Purification, primary structures, and antibacterial activities of β-defensins, a new family of antimicrobial peptides from bovine neutrophils. J. Biol. Chem. 268, 6641-6648 (Pubitemid 23099368)
70. Hancock, R. E., and Lehrer, R. (1998) Cationic peptides. A new source of antibiotics. Trends Biotechnol. 16, 82-88 (Pubitemid 28055477)
71. Ganz, T. (2003) Defensins. Antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3, 710-720
72. 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 (Pubitemid 16193690)
73. Selsted, M. E., Harwig, S. S., Ganz, T., Schilling, J. W., and Lehrer, R. I. (1985) Primary structures of three human neutrophil defensins. J. Clin. Invest. 76, 1436-1439 (Pubitemid 16193691)
74. Lehrer, R. I., and Ganz, T. (1996) Endogenous vertebrate antibiotics. Defensins, protegrins, and other cysteine-rich antimicrobial peptides. Ann. N.Y. Acad. Sci. 797, 228-239 (Pubitemid 27055594)
75. 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 β-defensin-2 reveals a novel α-helical segment. Biochemistry 40, 3810-3816 (Pubitemid 32280418)
76. Bach, A. C., 2nd, Selsted, M. E., and Pardi, A. (1987) Two-dimensional NMR studies of the antimicrobial peptide NP-5. Biochemistry 26, 4389-4397 (Pubitemid 17137066)
77. Pardi, A., Hare, D. R., Selsted, M. E., Morrison, R. D., Bassolino, D. A., and Bach, A. C., 2nd. (1988) Solution structures of the rabbit neutrophil defensin NP-5. J. Mol. Biol. 201, 625-636
78. Pardi, A., Zhang, X. L., Selsted, M. E., Skalicky, J. J., and Yip, P. F. (1992) NMR studies of defensin antimicrobial peptides. 2. Three-dimensional structures of rabbit NP-2 and human HNP-1. Biochemistry 31, 11357-11364
79. Zhang, X. L., Selsted, M. E., and Pardi, A. (1992) NMR studies of defensin antimicrobial peptides. 1. Resonance assignment and secondary structure determination of rabbit NP-2 and human HNP-1. Biochemistry 31, 11348-11356
80. Zimmermann, G. R., Legault, P., Selsted, M. E., and Pardi, A. (1995) Solution structure of bovine neutrophil β-defensin-12: the peptide fold of the β-defensins is identical to that of the classical defensins. Biochemistry 34, 13663-13671
81. Szyk, A., Wu, Z., Tucker, K., Yang, D., Lu, W., and Lubkowski, J. (2006) Crystal structures of human α-defensins HNP4, HD5, and HD6. Protein Sci. 15, 2749-2760 (Pubitemid 44833756)
82. Pazgier, M., Prahl, A., Hoover, D. M., and Lubkowski, J. (2007) Studies of the biological properties of human β-defensin 1. J. Biol. Chem. 282, 1819-1829 (Pubitemid 47076693)
83. Thomma, B. P., Cammue, B. P., and Thevissen, K. (2003) Mode of action of plant defensins suggests therapeutic potential. Curr. Drug Targets Infect.Disord. 3, 1-8 (Pubitemid 36304942)
84. Thevissen, K., Cammue, B. P., Lemaire, K., Winderickx, J., Dickson, R. C., Lester, R. L., Ferket, K. K., Van Even, F., Parret, A. H., and Broekaert, W. F. (2000) A gene encoding a sphingolipid biosynthesis enzyme determines the sensitivity of Saccharomyces cerevisiae to an antifungal plant defensin from dahlia (Dahlia merckii). Proc. Natl. Acad. Sci. U.S.A. 97, 9531-9536 (Pubitemid 30650810)
85. 2+in the regulation of hyphal extension and branching in Fusarium graminearum A 3/5. Exp. Mycol. 15, 263-272
86. 2+ gradient in the oomycete Saprolegnia ferax. Eur. J. Cell Biol. 60, 358-365
87. Thevissen, K., Ghazi, A., De Samblanx, G. W., Brownlee, C., Osborn, R. W., and Broekaert, W. F. (1996) Fungal membrane responses induced by plant defensins and thionins. J. Biol. Chem. 271, 15018-15025 (Pubitemid 26197577)
88. Possani, L. D., Merino, E., Corona, M., Bolivar, F., and Becerril, B. (2000) Peptides and genes coding for scorpion toxins that affect ion channels. Biochimie 82, 861-868
89. Bontems, F., Gilquin, B., Roumestand, C., Ménez, A., and Toma, F. (1992) Analysis of side-chain organization on a refined model of charybdotoxin. Structural and functional implications. Biochemistry 31, 7756-7764
90. Bontems, F., Roumestand, C., Gilquin, B., Ménez, A., and Toma, F. (1991) Refined structure of charybdotoxin: common motifs in scorpion toxins and insect defensins. Science 254, 1521-1523 (Pubitemid 21917495)
91. Brogden, K. A. (2005) Antimicrobial peptides. Pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250