Mapping the peptide and protein immune response in the larvae of the fleshfly Sarcophaga bullata

Journal of Peptide Science

Volumn 14, Issue 6, 2008, Pages 670-682

  Ciencialová, Alice ^a   Neubauerová, Tereza ^b   Šanda, Miloslav ^a   Šindelka, Radek ^c   Cvačka, Josef ^a   Voburka, Zdeněk ^a   Budeěšínský, Miloš ^a   Kašicčka, Václav ^a   Sázelová, Petra ^a   Šolínova, Veronika ^a   Macková, Martina ^b   Koutek, Bohumír ^a   Jiráček, Jiří ^a  

^a INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^c INSTITUTE OF MOLECULAR GENETICS   (Czech Republic)

Author keywords

Antimicrobial activity; Fleshfly; Odorant binding protein; Sapecin; Sarcophaga bullata; Transferrin

Indexed keywords

ANTIINFECTIVE AGENT; BETA ALANYLTYROSINAMIDE; BETA ALANYLTYROSINE; BETA ALANYLTYROSINE HYDROXIDE; BINDING PROTEIN; DIPEPTIDE; ENZYME PRECURSOR; FRUCTOPYRANOSE ALANYLTYROSINE HYDROXIDE; N ACETYL BETA ALANYINE HYDROXIDE; N ACETYL BETA ALANYLTYROSINAMIDE; ODORANT BINDING PROTEIN 99B; POLYPEPTIDE ANTIBIOTIC AGENT; PROPHENOL OXIDASE; SAPECIN; TRANSFERRIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG ISOLATION; DRUG SCREENING; DRUG SYNTHESIS; ELECTROPHORESIS; ESCHERICHIA COLI; FEMALE; FLY; GEL ELECTROPHORESIS; HEMOLYMPH; IMMUNE RESPONSE; LARVA; MAGGOT; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; PSEUDOMONAS AERUGINOSA; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SARCOPHAGA BULLATA; STAPHYLOCOCCUS AUREUS;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIPTERA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; INSECT PROTEINS; LARVA; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PEPTIDE MAPPING; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; SARCOPHAGA BULLATA; STAPHYLOCOCCUS AUREUS;

EID: 47249153646     PISSN: 10752617     EISSN: 10991387     Source Type: Journal    
DOI: 10.1002/psc.967     Document Type: Article

References (62)

1. Bulet P, Stocklin R, Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004; 198: 169-184.
2. Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002; 415: 389-395.
3. Hancock REW. Peptide antibiotics. Lancet 1997; 349: 418-422.
4. Vizioli J, Salzet M. Antimicrobial peptides from animals: focus on invertebrates. Trends Pharmacol. Sci. 2002; 23: 494-496.
5. Boman HG. Antibacterial peptides: basic facts and emerging concepts. J. Int. Med. 2003; 254: 197-215.
6. Ryge TS, Hansen PR. Novel lysine-peptoid hybrids with antibacterial properties. J. Pept. Sci. 2005; 11: 727-734.
7. Tossi A. AMPs database, 2007; http://www.bbcm.univ.trieste.it/~tossi/ amsdb.html.
8. Steiner H, Hultmark D, Engstrom A, Bennich H, Boman HG. Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 1981; 292: 246-248.
9. Dimarcq JL, Bulet P, Hetru C, Hoffmann J. Cysteine-rich antimicrobial peptides in invertebrates. Biopolymers 1998; 47: 465-477.
10. Okada M, Natori S. Purification and characterization of an antibacterial protein from haemolymph of Sarcophaga peregrina (flesh-fly) larvae. Biochem. J. 1983; 211: 727-734.
11. Yamauchi H. Two novel insect defensins from larvae of the cupreous chafer, Anomala cuprea: purification, amino acid sequences and antibacterial activity. Insect Biochem. Mol. Biol. 2001; 320: 75-84.
12. Gobbo M, Biondi L, Filira F, Gennaro R, Benincasa M, Scolaro B, Rocchi R. Antimicrobial peptides: synthesis and antibacterial activity of linear and cyclic drosocin and apidaecin 1b analogues. J. Med. Chem. 2002; 45: 4494-4504.
13. Bulet P, Dimarcq JL, Hetru C, Lagueux M, Charlet M, Hegy G, Vandorsselaer A, Hoffmann JA. A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J. Biol. Chem. 1993; 268: 14893-14897.
14. Otvos L. The short proline-rich antibacterial peptide family. Cell. Mol. Life Sci. 2002; 59: 1138-1150.
15. Goumon Y, Lugardon K, Gadroy P, Strub JM, Welters ID, Stefano GB, Aunis D, Metz-Boutigue MH. Processing of proenkephalin-A in bovine chromaffin cells. Identification of natural derived fraginents by N-terminal sequencing and matrix-assisted laser desorption ionization-time of flight mass spectrometry. J. Biol. Chem. 2000; 275: 38355-38362.
16. Salzet M. Vertebrate innate immunity resembles a mosaic of invertebrate immune responses. Trends Immunol. 2001; 22: 285-288.
17. Brogden KA, De Lucca AJ, Bland J, Elliott S. Isolation of an ovine pulmonary surfactant-associated anionic peptide bactericidal for Pasteurella haemolytica. Proc. Natl. Acad. Sci. U.S.A. 1996; 93: 412-416.
18. Leem JY, Nishimura C, Kurata S, Shimada I, Kobayashi A, Natori S. Purification and characterization of N-beta-alanyl-5-S-glutathionyl-3,4-dihydroxyphenylalanine, a novel antibacterial substance of Sarcophaga peregrina (flesh fly). J. Biol. Chem. 1996; 271: 13573-13577.
19. Leem JY, Jeong IJ, Park KT, Park HY. Isolation of p-hydroxycinnamaldehyde as an antibacterial substance from the saw fly, Acantholyda parki, S. FEBS Lett. 1999; 442: 53-56.
20. Meylaers K, Cerstiaens A, Vierstraete E, Baggerman G, Michiels CW, De Loof A, Schoofs L. Antimicrobial compounds of low molecular mass are constitutively present in insects: characterisation of beta-alanyl-tyrosine. Curr. Pharm. Des. 2003; 9: 159-174.
21. Fogaca AC, da Silva PI, Miranda MTM, Bianchi AG, Miranda A, Ribolla PEM, Daffre S. Antimicrobial activity of a bovine hemoglobin fragment in the tick Boophilus microplus. J. Biol. Chem. 1999; 274: 25330-25334.
22. Huang HW. Action of antimicrobial peptides: two-state model. Biochemistry 2000; 39: 8347-8352.
23. Shai Y. 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 Biomembr. 1999; 1462: 55-70.
24. Silvestro L, Weiser JN, Axelsen PH. Antibacterial and antimembrane activities of cecropin A in Escherichia coli. Antimicrob. Agents Chemother. 2000; 44: 602-607.
25. Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 2003; 55: 27-55.
26. Kragol G, Lovas S, Varadi G, Condie BA, Hoffmann R, Otvos L. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 2001; 49: 3016-3026.
27. Otvos LOI, Rogers ME, Consolvo PJ, Condie BA, Lovas S, Bulet P, Blaszczyk-Thurin M. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 2000; 39: 14150-14159.
28. Basak A, Ernst B, Brewer D, Seidah NG, Munzer JS, Lazure C, Lajoie GA. Histidine-rich human salivary peptides are inhibitors of proprotein convertases furin and PC7 but act as substrates for PC1. J. Pept. Res. 1997; 49: 596-603.
29. Verbanac D, Zanetti M, Romeo D. Chemotactic and protease-inhibiting activities of antibiotic peptide precursors. FEBS Lett. 1993; 317: 255-258.
30. Yan H, Hancock RE. Synergistic interactions between mammalian antimicrobial defense peptides. Antimicrob. Agents Chemother. 2001; 45: 1558-1560.
31. Dimarcq JL, Hunneyball I. Pharma-entomology: when bugs become drugs. Drug Discov. Today 2003; 8: 107-110.
32. Otvos L. Antibacterial peptides isolated from insects. J. Pept. Sci. 2000; 6: 497-511.
33. Royet J. Infectious non-self recognition in invertebrates: lessons from Drosophila and other insect models. Mol. Immunol. 2004; 41: 1063-1075.
34. Chase MR, Raina K, Bruno J, Sugumaran M. Purification, characterization and molecular cloning of prophenoloxidases from Sarcophaga bullata. Insect Biochem. Mol. Biol. 2000; 30: 953-967.
35. Leclerc V, Pelte N, Chamy LE, Martinelli C, Ligoxygakis P, Hoffmann JA, Reichhart JM. Prophenoloxidase activation is not required for survival to microbial infections in Drosophila. EMBO Rep. 2006; 7: 231-235.
36. Vilmos P, Kurucz E. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol. Lett. 1998; 62: 59-66.
37. Iwanaga S, Lee BL. Recent advances in the innate immunity of invertebrate animals. J. Biochem. Mol. Biol. 2005; 38: 128-150.
38. Hoffmann JA, Reichhart JM. Drosophila innate immunity: an evolutionary perspective. Nature Immunol. 2002; 3: 121-126.
39. Hultmark D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 2003; 15: 12-19.
40. Tzou P, De Gregorio E, Lemaitre B. How Drosophila combats microbial infection: a model to study innate immunity and hostpathogen interactions. Curr. Opin. Microbiol. 2002; 5: 102-110.
41. Leclerc V, Reichhart JM. The immune response of Drosophila melanogaster. Immunol. Rev. 2004; 198: 59-71.
42. Fraenkel G. Molting and development in undersized fly larvae. In The Insect Integument. Hepburn AR (ed.). Elsevier: Amsterdam, 1976; 323-338.
43. Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007; 25: 697-743.
44. Zdarek J. Endocrine control of the pupariation behavior in flies. Gen. Comp. Endocrinol. 1980; 40: 361-361.
45. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685,
46. Schagger H, von Jagow G. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 1987; 166: 368-379.
47. Mossine VV, Glinsky GV, Feather MS. The preparation and characterization of some Amadori compounds (1-amino-1-deoxy-D-fructose derivatives) derived from a series of aliphatic omega-amino acids. Carbohydr. Res. 1994; 262: 257-270.
48. Kasicka V, Prusik Z, Sazelova P, Jiracek J, Barth T. Theory of the correlation between capillary and free-flow zone electrophoresis and its use for the conversion of analytical capillary separations to continuous free-flow preparative processes. Application to analysis and preparation of fragments of insulin. J. Chromatogr., A 1998; 796: 211-220.
49. Sugumaran M. Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res. 2002; 15: 2-9.
50. Levenbook L, Bodnaryk RP, Spande TF. Beta-alanyl-L-tyrosine. Chemical synthesis, properties and occurrence in larvae of the fleshfly Sarcophaga bullata Parker. Biochem. J. 1969; 118: 837-841.
51. Chiou SJ, Cerstiaens A, Kotanen SP, De Loof A, Schoofs L. Insect larvae contain substances toxic to adults: the discovery of paralysins. J. Insect Physiol. 1998; 44: 405-411.
52. Chiou SJ, Kotanen S, Cerstiaens A, Daloze D, Pasteels JM, Lesage A, Drijfhout JW, Verhaert P, Dillen L, Claeys M, De MH, Nuttin B, De LA, Schoofs L. Purification of toxic compounds from larvae of the gray fleshfly: the identification of paralysins. Biochem. Biophys. Res. Commun. 1998; 246: 457-462.
53. Dunn PE, Fader RG, Regnie FE. Metabolism of beta-Alanyl-L-Tyrosine in Sarcophaga bulllata. J. Insect Physiol. 1977; 23: 1021-1029.
54. Hekmat-Scafe DS, Scafe CR, Mckinney AJ, Tanouye MA. Genomewide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Cold Spring Harbor Lab. Press 2002; 12: 1357-1369.
55. Levy F, Bulet P, Ehret-Sabatier L. Proteomic analysis of the systemic immune response of Drosophila. Mol. Cell Proteomics 2004; 3: 156-166.
56. Yoshiga T, Georgieva T, Dunkov BC, Harizanova N, Ralchev K, Law JH. Drosophila melanogaster transferrin. Cloning, deduced protein sequence, expression during the life cycle, gene localization and up-regulation on bacterial infection. Eur. J. Biochem. 1999; 260: 414-420.
57. Stafford JL, Neumann NF, Belosevic M. Products of proteolytic cleavage of transferrin induce nitric oxide response of goldfish macrophages. Dev. Comp. Immunol. 2001; 25: 101-115.
58. Gomme PT, McCann KB, Bertolini J. Transferrin: structure, function and potential therapeutic actions. Drug Discov. Today 2005; 10: 267-273.
59. Hanzawa H, Shimada I, Kuzuhara T, Komano H, Kohda D, Inagaki F, Natori S, Arata Y. H-1 nuclear-magnetic-resonance study of the solution conformation of an antibacterial protein, sapecin. FEBS Lett. 1990; 269: 413-420.
60. Yamada K, Natori S. Purification, Sequence and antibacterial activity of 2 novel sapecin homologs from Sarcophaga embryonic-cells - similarity of sapecin-B to charybdotoxin. Biochem. J. 1993; 291: 275-279.
61. Matsuyama K, Natori S. Purification of three antibacterial proteins from the culture medium of NIH-Sape-4, an embryonic cell line of Sarcophaga peregrina. J. Biol. Chem. 1988; 263: 17112-17116.
62. Yamada K, Natori S. Purification, sequence and antibacterial activity of two novel sapecin homologues from Sarcophaga embryonic cells: similarity of sapecin B to charybdotoxin. Biochem. J. 1993; 291(Pt 1): 275-279.