A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella

Insect Biochemistry and Molecular Biology

Volumn 39, Issue 11, 2009, Pages 792-800

  Brown, Susan E ^a   Howard, Antoinette ^a   Kasprzak, Annette B ^a   Gordon, Karl H ^a   East, Peter D ^a  

^a CSIRO   (Australia)

Author keywords

Antifungal; Antimicrobial peptide; Galleria mellonella; Immune response; Peptidomics; Proline rich peptide

Indexed keywords

ANTIINFECTIVE AGENT; PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; GENETICS; HEMOLYMPH; METABOLISM; MOLECULAR GENETICS; MOTH; NUCLEOTIDE SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; BASE SEQUENCE; HEMOLYMPH; MOLECULAR SEQUENCE DATA; MOTHS; PEPTIDES;

GALLERIA MELLONELLA; LEPIDOPTERA;

EID: 70449658824     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2009.09.004     Document Type: Article

References (55)

1. Altamirano M.M., Garcia C., Possani L.D., and Fersht A.R. Oxidative refolding chromatography: folding of the scorpion toxin Cn5. Nat. Biotechnol. 17 (1999) 187-191
2. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215 (1990) 403-410
3. Baggerman G., Verleyen P., Clynen E., Huybrechts J., De Loof A., and Schoofs L. Peptidomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 803 (2004) 3-16
4. Bao Y., Yamano Y., and Morishima I. A novel lebocin-like gene from eri-silkworm, Samia cynthia ricini, that does not encode the antibacterial peptide lebocin. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 140 (2005) 127-131
5. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: signalP 3.0. J. Mol. Biol. 340 (2004) 783-795
6. Bergin D., Murphy L., Keenan J., Clynes M., and Kavanagh K. Pre-exposure to yeast protects larvae of Galleria mellonella from a subsequent lethal infection by Candida albicans and is mediated by the increased expression of antimicrobial peptides. Microbes Infect. 8 (2006) 2105-2112
7. Boman H.C., Boman I.A., Andreu D., Li Z.-Q., Merrifield R.B., Schlenstedt G., and Zimmermann R. Chemical synthesis and enzymic processing of precursor forms of cecropins A and B. J. Biol. Chem. 264 (1989) 5852-5860
8. Brahmachary M., Krishnan S.P., Koh J.L., Khan A.M., Seah S.H., Tan T.W., Brusic V., and Bajic V.B. ANTIMIC: a database of antimicrobial sequences. Nucleic Acids Res. 32 (2004) D586-D589
9. Brown S.E., Howard A., Kasprzak A.B., Gordon K.H., and East P.D. The discovery and analysis of a diverged family of novel antifungal moricin-like peptides in the wax moth Galleria mellonella. Insect Biochem. Mol. Biol. 38 (2008) 201-212
10. Bulet P., Charlet M., and Hetru C. Antimicrobial peptides in insect immunity. In: Ezekowitz R.A.B., and Hoffmann J.A. (Eds). Innate Immunity (2003), Humana Press, Totowa, NJ 89-107
11. Casteels-Josson K., Capaci T., Casteels P., and Tempst P. Apidaecin multipeptide precursor structure: a putative mechanism for amplification of the insect antibacterial response. EMBO J. 12 (1993) 1569-1578
12. Casteels P., Ampe C., Jacobs F., Vaeck M., and Tempst P. Apidaecins: antibacterial peptides from honeybees. EMBO J. 8 (1989) 2387-2391
13. Cheng T., Zhao P., Liu C., Xu P., Gao Z., Xia Q., and Xiang Z. Structures, regulatory regions, and inductive expression patterns of antimicrobial peptide genes in the silkworm Bombyx mori. Genomics 87 (2006) 356-365
14. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P.T., Collins F.H., Danielli A., Dimopoulos G., Hetru C., Hoa N.T., Hoffmann J.A., Kanzok S.M., Letunic I., Levashina E.A., Loukeris T.G., Lycett G., Meister S., Michel K., Moita L.F., Müller H.-M., Osta M.A., Paskewitz S.M., Reichhart J.-M., Rzhetsky A., Troxler L., Vernick K.D., Vlachou D., Volz J., von Mering C., Xu J., Zheng L., Bork P., and Kafatos F.C. Immunity-related genes and gene families in Anopheles gambiae. Science 298 (2002) 159-165
15. Clermont A., Wedde M., Seitz V., Podsiadlowski L., Lenze D., Hummel M., and Vilcinskas A. Cloning and expression of an inhibitor of microbial metalloproteinases from insects contributing to innate immunity. Biochem. J. 382 (2004) 315-322
16. Cytrynska M., Mak P., Zdybicka-Barabas A., Suder P., and Jakubowicz T. Purification and characterization of eight peptides from Galleria mellonella immune hemolymph. Peptides 28 (2007) 533-546
17. Evans J.D., Aronstein K., Chen Y.P., Hetru C., Imler J.-L., Jiang H., Kanost M., Thompson G.J., Zou Z., and Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15 (2006) 645-656
18. Gennaro R., Zanetti M., Benincasa M., Podda E., and Miani M. Pro-rich antimicrobial peptides from animals: structure, biological functions and mechanism of action. Curr. Pharm. Des 8 (2002) 763-778
19. Hara S., and Yamakawa M. Cooperative antibacterial relationship between lebocin and cecropin D, antibacterial peptides isolated from the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Appl. Entomol. Zool. 30 (1995) 606-608 (Jpn)
20. Kay B.K., Williamson M.P., and Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 14 (2000) 231-241
21. Kim C.H., Lee J.H., Kim I., Seo S.J., Son S.M., Lee K.Y., and Lee I.H. Purification and cDNA cloning of a cecropin-like peptide from the great wax moth, Galleria mellonella. Mol. Cells 17 (2004) 262-266
22. Lavine M.D., Chen G., and Strand M.R. Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochem. Mol. Biol. 35 (2005) 1335-1346
23. Lee Y.S., Yun E.K., Jang W.S., Kim I., Lee J.H., Park S.Y., Ryu K.S., Seo S.J., Kim C.H., and Lee I.H. Purification, cDNA cloning and expression of an insect defensin from the great wax moth, Galleria mellonella. Insect Mol. Biol. 13 (2004) 65-72
24. Lemaitre B., and Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25 (2007) 697-743
25. Levy F., Rabel D., Charlet M., Bulet P., Hoffmann J.A., and Ehret-Sabatier L. Peptidomic and proteomic analyses of the systemic immune response of Drosophila. Biochimie 86 (2004) 607-616
26. Li W.F., Ma G.X., and Zhou X.X. Apidaecin-type peptides: biodiversity, structure-function relationships and mode of action. Peptides 27 (2006) 2350-2359
27. Liu G., Kang D.W., and Steiner H. Trichoplusia ni lebocin, an inducible immune gene with a downstream insertion element. Biochem. Biophys. Res. Commun. 269 (2000) 803-807
28. Lüders T., Birkemo G.A., Nissen-Meyer J., Andersen O., and Nes I.F. Proline conformation-dependent antimicrobial activity of a proline-rich histone H1 N-terminal peptide fragment isolated from the skin mucus of Atlantic salmon. Antimicrob. Agents Chemother. 49 (2005) 2399-2406
29. Mackintosh J.A., Gooley A.A., Karuso P.H., Beattie A.J., Jardine D.R., and Veal D.A. A gloverin-like antibacterial protein is synthesized in Helicoverpa armigera following bacterial challenge. Dev. Comp. Immunol. 22 (1998) 387-399
30. Mak P., Chmiel D., and Gacek G.J. Antibacterial peptides of the moth Galleria mellonella. Acta Biochim. Pol. 48 (2001) 1191-1195
31. Mcguffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
32. O'Keefe M.P., Nedelkov D., Bieber A.L., and Nieman R.A. Evidence for isomerization in myotoxin A from the prairie rattlesnake (Crotalus viridis viridis). Toxicon 34 (1996) 417-434
33. Otvos Jr. L. Antibacterial peptides isolated from insects. J. Pept. Sci. 6 (2000) 497-511
34. Perkins, P.D., Miller, C.A., Kuhlmann, F.E., 2005. Comparison of different approaches for the label-free relative quantitation of proteins. Agilent Technologies Application Note.
35. Rabel D., Charlet M., Ehret-Sabatier L., Cavicchioli L., Cudic M., Otvos L., and Bu P. Primary structure and in vitro antibacterial properties of the Drosophila melanogaster attacin C pro-domain. J. Biol. Chem. 279 (2004) 14853-14859
36. Schoofs L., and Baggerman G. Peptidomics in Drosophila melanogaster. Brief. Funct. Genomic Proteomic 2 (2003) 114-120
37. Schuhmann B., Seitz V., Vilcinskas A., and Podsiadlowski L. Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch. Insect Biochem. Physiol. 53 (2003) 125-133
38. Seitz V., Clermont A., Wedde M., Hummel M., Vilcinskas A., Schlatterer K., and Podsiadlowski L. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev. Comp. Immunol. 27 (2003) 207-215
39. Shai Y. Mode of action of membrane active antimicrobial peptides. Biopolymers 66 (2002) 236-248
40. Song J., Burrage K., Yuan Z., and Huber T. Prediction of cis/trans isomerization in proteins using PSI-BLAST profiles and secondary structure information. BMC Bioinform. 7 (2006) 124
41. Song K.H., Jung S.J., Seo Y.R., Kang S.W., and Han S.S. Identification of up-regulated proteins in the hemolymph of immunized Bombyx mori larvae. Comp. Biochem. Physiol. Part D Genomics Proteomics 1 (2006) 260-266
42. Steiner H., Hultmark D., Engstrom A., Bennich H., and Boman H.G. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292 (1981) 246-248
43. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
44. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
45. Veenstra J.A. Mono- and dibasic proteolytic cleavage sites in insect neuroendocrine peptide precursors. Arch. Insect Biochem. Physiol. 43 (2000) 49-63
46. Verleyen P., Baggerman G., D'Hertog W., Vierstraete E., Husson S.J., and Schoofs L. Identification of new immune induced molecules in the haemolymph of Drosophila melanogaster by 2D-nanoLC MS/MS. J. Insect Physiol. 52 (2006) 379-388
47. Vizioli J., Bulet P., Charlet M., Lowenberger C., Blass C., Müller H.-M., Dimopoulos G., Hoffmann J., Kafatos F.C., and Richman A. Cloning and analysis of a cecropin gene from the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 9 (2000) 75-84
48. Vizioli J., Bulet P., Hoffmann J.A., Kafatos F.C., Müller H.-M., and Dimopoulos G. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12630-12635
49. Vizioli J., Richman A.M., Uttenweiler-Joseph S., Blass C., and Bulet P. The defensin peptide of the malaria vector mosquito Anopheles gambiae: antimicrobial activities and expression in adult mosquitoes. Insect Biochem. Mol. Biol. 31 (2001) 241-248
50. Wang Z., and Wang G. APD: the Antimicrobial Peptide Database. Nucleic Acids Res. 32 (2004) D590-D592
51. Wedde M., Weise C., Nuck R., Altincicek B., and Vilcinskas A. The insect metalloproteinase inhibitor gene of the lepidopteran Galleria mellonella encodes two distinct inhibitors. Biol. Chem. 388 (2007) 119-127
52. Xia Q., Zhou Z., Lu C., Cheng D., Dai F., Li B., Zhao P., Zha X., Cheng T., Chai C., Pan G., Xu J., Liu C., Lin Y., Qian J., Hou Y., Wu Z., Li G., Pan M., Li C., Shen Y., Lan X., Yuan L., Li T., Xu H., Yang G., Wan Y., Zhu Y., Yu M., Shen W., Wu D., Xiang Z., Yu J., Wang J., Li R., Shi J., Li H., Li G., Su J., Wang X., Li G., Zhang Z., Wu Q., Li J., Zhang Q., Wei N., Xu J., Sun H., Dong L., Liu D., Zhao S., Zhao X., Meng Q., Lan F., Huang X., Li Y., Fang L., Li C., Li D., Sun Y., Zhang Z., Yang Z., Huang Y., Xi Y., Qi Q., He D., Huang H., Zhang X., Wang Z., Li W., Cao Y., Yu Y., Yu H., Li J., Ye J., Chen H., Zhou Y., Liu B., Wang J., Ye J., Ji H., Li S., Ni P., Zhang J., Zhang Y., Zheng H., Mao B., Wang W., Ye C., Li S., Wang J., Wong G.K., and Yang H. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306 (2004) 1937-1940
53. Xie J.B., and Zhou J.M. Trigger factor assisted folding of green fluorescent protein. Biochemistry 47 (2008) 348-357
54. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 415 (2002) 389-395
55. Zhu Y., Johnson T.J., Myers A.A., and Kanost M.R. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect Biochem. Mol. Biol. 33 (2003) 541-559