Antimicrobial peptide defense in Drosophila

BioEssays

Volumn 19, Issue 11, 1997, Pages 1019-1026

  Meister, Marie ^a   Lemaitre, Bruno ^a   Hoffmann, Jules A ^a  

^a INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0031281940     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.950191112     Document Type: Review

References (88)

1. Kushner, I. (1982). The phenomenon of the acute phase response. Ann. NY Acad. Sci. 389, 39-48.
2. Hultmark, D. (1993). Immune reactions in Drosophila and other insects: a model for innate immunity. Trends Genet. 9, 178-183.
3. Hoffmann, J.A. (1995). Innate immunity of insects. Curr. Opin. Immunol. 7, 4-10
4. Boman, H.G. (1995). Peptide antibiotics and their role in innate immunity. Ann. Rev. Immunol. 13, 61-92.
5. Hoffmann, J.A., Reichhart, J.M. and Hetru, C. (1996). Innate immunity in higher insects. Curr. Opin. Immunol. 8, 8-13.
6. Ratcliffe, N.A. (1993). Cellular defense responses of insects: unresolved problems. in Parasites and Pathogens of Insects, Vol 1. (ed. N. E. Beckage, S.N. Thompson and B.A. Federici), pp. 267-304. Academic Press, San Diego.
7. Faye, I., Pye, A., Rasmuson, T., Boman, H.G. and Boman, I.A. (1975). Insect immunity. Simultaneous induction of antibacterial activity and selective synthesis of some hemolymph proteins in diapausing pupae of Hyalophora cecropia and Samia cynthia. Infect. Immun. 12, 1426-1438.
8. Natori, S. (1977). Bactericidal substance induced in the haemolymph of Sarcophaga peregrina larvae. J. Insect Physiol. 23, 1169-1173.
9. Keppi, E., Zachary, D., Robertson, M., Hoffmann, D. and Hoffmann, J.A. (1986). Induced antibacterial proteins in the haemolymph of Phormia terranovae (Diptera). Insect Biochem. 16, 395-402.
10. Steiner, H., Hultmark, D., Engström, A., Bennich, H. and Boman, H.G. (1981). Sequence and specificity of two antibacterial proteins involved in insect immunity. Nature 292, 246-248.
11. Hetru, C., Bulet, P., Cociancich, S., Dimarcq, J.L., Hoffmann, D. and Hoffmann, J.A. (1994). Antibacterial peptides/polypeptides in the insect host defense: a comparison with vertebrate antibacterial peptides/polypeptides. In Phylogenetic Perspectives In Immunity: The Insect Host Defense (ed. J. A. Hoffmann, C. A. Janeway and S. Natori), pp. 43-65. RG Landes Company, Austin.
12. Boman, H.G. (1994). Cecropins: antibacterial peptides from insects and pigs. In Phylogenetic Perspectives In Immunity: The Insect Host Defense (ed. J. A. Hoffmann, C. A. Janeway and S. Natori), pp. 3-17. RG Landes Company, Austin.
13. Kang, D., Liu, G., Gunne, H. and Steiner, H. (1996). PCR differential display of immune gene expression in Trichoplusiani. Insect Biochem. Mol. Biol. 26, 177-184.
14. Zhou, X., Nguyen, T. and Kimbrell, D.A. (1997). Identification and characterization of the cecropin antibacterial protein gene locus in Drosophila virilis. J. Mol. Evol. 44, 272-281.
15. Lee, J.Y. et al. (1989). Antibacterial peptides from pig intestine: isolation of a mammalian cecropin. Proc. Natl Acad. Sci. USA 86, 9159-9162.
16. 1H NMR study of recombinant insect defensin A in water: resonance assignments, secondary structure and global folding. J. Biomol. NMR 2, 235-256.
17. Cornet, B., Bonmatin, J.M., Hetru, C., Hoffmann, J.A., Ptak, M. and Vovelle, F. (1995) Refined three-dimensional solution structure of insect defensin A. Structure 3, 435-448.
18. Cociancich, S. et al. (1993). Purification and characterization of a scorpion defensin, a 4kDa antibacterial peptide presenting structural similarities with insect defensins and scorpion toxins. Biochem. Biophys. Res. Commun. 194, 17-22.
19. Ehret-Sabatier, L. et al. (1996). Characterization of novel cysteine-rich antimicrobial peptides from scorpion blood. J. Biol. Chem. 271, 29537-29544.
20. Charlet, M., Chernysh, S., Philippe, H., Hetru, C., Hoffmann, J.A. and Bulet, P. (1996). Innate immunity. Isolation of several cystein-rich antimicrobial peptides from the blood of a mollusc, Mytilus edulis. J. Biol. Chem. 271, 21808-21813.
21. Hubert, F., Noël, T. and Roch, P. (1996). A member of the arthropod defensin family from edible Mediterranean mussels (Mytilus galloprovincialis). Eur. J. Biochem. 240, 302-306.
22. Matsuyama, K. and Natori, S. (1988). Molecular cloning of cDNA for sapecin and unique expression of the sapecin gene during the development of Sarcophaga peregrina. J. Biol. Chem. 263, 17117-17121.
23. Yamada, K. and Natori, S. (1993). Purification, sequence and antibacterial activity of two novel sapecin homologues from Sarcophaga embryonic cells: similarity of sapecin B to charybdotoxin. Biochem. J. 291, 275-279.
24. Selsted, M.E., Brown, D.M., DeLange, R.J. and Lehrer, R.I. (1983). Primary structures of MCP-1 and MCP-2, natural peptide antibiotics of rabbit lung macrophages. J. Biol. Chem. 258, 14485-14489.
25. Lambert, J. et al. (1989). Insect immunity: isolation from immune blood of the dipteran Phormia terranova of two insect antibacterial peptides with sequence homology to rabbit lung macrophage bactericidal peptides. Proc. Natl. Acad. Sci. USA 86, 262-266.
26. Pardi, A., Hare, D.R., Selsted, M.E., Morisson, R.D., Bassolino, D.A. and Bach, A.C. (1988). Solution structures of the rabbit neutrophil defensin NP-5. J. Mol. Biol. 201, 625-636.
27. Cociancich, S., Ghazi, A., Hetru, C., Hoffmann, J. A. and Letellier, L. (1993). Insect defensin, an inducible antibacterial peptide, forms voltage-dependent channels in Micrococcus luteus. J. Biol. Chem. 268, 19239-19245.
28. Fehlbaum, P. et al. (1994). Insect immunity: septic injury of Drosophila induces the synthesis of a potent antifungal peptide with sequence homology to plant antifungal peptides. J. Biol. Chem. 269, 33159-33163.
29. Terras, F.R.G. et al. (1992). Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267, 15301-15309.
30. Broekaert, W.F., Terras, F.R.G., Cammue, B.P.A. and Osborn, R.W. (1995). Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol. 108, 1353-1358.
31. Fehlbaum, P. et al. (1996). Structure-activity analysis of thanatin, a 21-residue inducible insect defense peptide with sequence homology to frog skin antimicrobial peptides. Proc. Natl Acad. Sci. USA 93, 1221-1225.
32. Morikawa, N., Hagiwara, K. and Nakajima, T. (1992). Brevinin-1 and -2, unique antimicrobial peptides from the skin of the frog, Rana brevipoda porsa. Bioch. Biophys. Res. Commun. 189, 184-190.
33. Casteels, P., Ampe, C., Jacobs, F., Vaeck, M. and Temspt, P. (1989). Apidaecins: antibacterial peptides from honeybees. EMBO J. 8, 2387-2391.
34. Casteels, P. et al. (1990). Isolation and characterization of abaecin, a major antibacterial response peptide in the honey bee (Apis mellifera). Eur. J. Biochem. 187, 381-386.
35. Bulet, P. et al. (1993). A novel inducible antibacterial peptide of Drosophila carries an O-glycosylated substitution. J. Biol. Chem. 268, 14893-14897.
36. Cociancich, S. et al. (1994). Novel inducible antibacterial peptides from a hemipteran insect, Pyrrhocoris apterus. Biochem. J. 300, 567-575.
37. Chernysh, S., Cociancich, S., Briand, J.P., Hetru, C. and Bulet, P. (1996). The inducible antibacterial peptides of the hemipteran insect Palomena prasina: identification of a unique family of proline-rich peptides and of a novel insect defensin. J. Insect Physiol. 42, 81-89.
38. Hara, S. and Yamakawa, M. (1995). A novel antibacterial peptide family isolated from the silkworm, Bombyx mori. Biochem. J. 310, 651-656.
39. Casteels, P. and Tempst, P. (1994). Apidaecin-type peptide antibiotics function through a non-poreforming mechanisms involving stereospecificity. Biochem. Biophys. Res. Comm. 199, 339-345.
40. Bulet, P., Urge, L., Ohresser, S., Hetru, C. and Otvös, L. (1996). Enlarged scale chemical synthesis and range of activity of drosocin, an O-glycosylated antibacterial peptides of Drosophila. Eur. J. Biochem. 238, 64-69.
41. Frank, R.W., Gennaro, R., Schneider, K., Przybylski, M. and Romeo, D. (1990). Amino-acid sequences of two proline-rich bactenecins, antimicrobial peptides of bovine neutrophils. J. Biol. Chem. 265, 18871-18874.
42. Agerberth, B. et al. (1991). Amino-acid sequence of PR-39. Isolation from pig intestine of a new member of the family of proline-arginine-rich antibacterial peptides. Eur. J. Biochem. 202, 849-854.
43. Hultmark, D., Engström, A., Andersson, K., Steiner, H., Bennich, H. and Boman, H.G. (1983). Insect immunity. Attacins, a family of antibaterial proteins from Hyalophora cecropia, EMBO J. 2, 571-576.
44. Dimarcq, J.L. et al. (1988). Insect Immunity. Purification and characterization of a family of novel inducible antibacterial proteins from immunized larvae of the dipteran Phormia terranovae and complete amino-acid sequence of the predominant member, diptericin A. Eur. J. Biochem. 171, 17-22.
45. Carlsson, A., Engström, P., Palva, E.T. and Bennich, H. (1991). Attacin, an antibacterial protein from Hyalophora cecropia, inhibits synthesis of outer membrane proteins in Escherichia coli by interfering with omp gene transcription. Infection and Immunity, 1991, 3040-3045.
46. Mohrig, W. and Messner, B. (1968). Immunoreaktionen bei Insekten. I Lysozym als grundlegender antibakterieller Faktor im humoralen Abwehrmechanismus des Insekten. Biol. Zbl. 87, 439-470.
47. Chadwick, J.S. (1970). Relation of lysozyme concentration to acquired immunity against Pseudomonas aeruginosa in Galleria mellonella. J. Invert. Path. 15, 455-456.
48. Mulnix A.B. and Dunn P.E. (1994). Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 24, 271-281.
49. Lockey, T.D. and Ourth, D.D. (1996). Purification and characterization of lysozyme from hemolymph of Heliothis virescens larvae. Biochem. Biophys. Res. Commun. 220, 502-508.
50. Sun, S.C., Asling, B. and Faye, I. (1991). Organization and expression of the immunoresponsive lysozyme gene in the giant silk moth, Hyalophora cecropia. J. Biol. Chem. 266, 6644-6649.
51. Kylsten, P., Kimbrell, D.A., Daffre, S., Samakovlis, C. and Hultmark, D. (1992). The lysozyme locus in Drosophila melanogaster. different genes are expressed in midgut and salivary glands. Mol. Gen. Genet. 232, 335-343.
52. Kylsten, P., Samakovlis, C. and Hultmark, D. (1990). The cecropin locus in Drosophila: a compact gene cluster involved in the response to infection EMBO J. 9, 217-224.
53. Tryselius, Y., Samakovlis, C., Kimbrell, D.A. and Hultmark, D. (1992). CecC, a cecropin gene expressed during metamorphosis in Drosophila pupae. Eur. J. Biochem. 204, 395-399.
54. Dimarcq, J.L. et al. (1994). Characterization and transcriptional profiles of a Drosophila gene encoding an insect defensin. A study in insect immunity. Eur. J. Biochem. 221, 201-209.
55. Charlet, M., Lagueux, M., Reichhart, J.M., Hoffmann, D., Braun, A. and Meister, M. (1996). Cloning of the gene encoding the antibacterial peptide drosocin involved in Drosophila immunity. Expression studies during the immune response. Eur. J. Biochem. 241, 699-706.
56. Levashina, E.A., Ohresser, S., Bulet, P., Reichhart, J.M., Hetru, C. and Hoffmann, J.A. (1995). Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur. J. Biochem. 233, 694-700.
57. Åsling, B., Dushay, M.S. and Hultmark, D. (1995) Identification of early genes in the Drosophila immune response by PCR-based differential display: the Attacin A gene and the evolution of attacin-like proteins. Insect Biochem. Mol. Biol. 25, 511-518.
58. Reichhart, J.M. et al. (1992). Insect immunity: developmental and inducible activity of the Drosophila diptericin promoter. EMBO J. 11, 1469-1477.
59. Sun, S.C., Lindstrom, I., Lee, J.Y. and Faye, I. (1991) Structure and expression of the attacin genes in Hyalophora cecropia. Eur. J. Biochem. 196, 247-254.
60. Engström, Y., Kadalayil, L., Sun, S.C., Samakovlis, C., Hultmark, D. and Faye, I. (1993). KB-like motifs regulate the induction of immune genes in Drosophila. J. Mol. Biol. 232, 327-333.
61. Kappler, C., Meister, M., Lagueux, M., Gateff, E., Hoffmann, J.A. and Reichhart, J. M. (1993). Insect Immunity. Two 17 bp repeats nesting a κ-B-related sequence confer inducibility to the diptencin gene and bind a polypeptide in bacteria-challenged Drosophila. EMBO J. 12, 1561-1568.
62. Georgel, P., Meister, M., Kappler, C., Lemaitre, B., Reichhart, J.M. and Hoffmann, J.A. (1993), Insect immunity: the diptericin promoter contains multiple functional regulatory sequences homologous to mammalian acute-phase response elements. Biochem. Biophys. Res. Commun. 197, 508-517.
63. Georgel, P. et al. (1995). Drosophila immunity. A sequence homologous to mammalian Interferon consensus response element enhances the activity of the diptericin promoter. Nucleic Acids Res. 23, 1140-1145.
64. Meister, M., Braun, A., Kappler, C., Reichhart, J.M. and Hoffmann, J. A. (1994). Insect immunity. A transgenic analysis in Drosophila defines several functional domains in the diptericin promoter. EMBO J. 13, 5958-5966
65. Grilli, M., Chiu, J.J.S. and Lenardo, M.J. (1993). NF-κB and Rel: participants in a multiform transcriptional regulatory system. Internat. Rev. Cytol. 143, 1-62.
66. Baeuerle, P. A. and Henkel, T. (1994). Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12, 141-179.
67. Steward, R. (1987). Dorsal, an embryonic polarity gene in Drosophila, is homologous to the vertebrate proto-oncogene, c-rel. Science 238, 692-694.
68. Govind, S. and Steward, R. (1991). Dorsoventral pattern formation in Drosophila: signal transduction and nuclear targeting. Trends Genet. 7, 119-125.
69. Wasserman, S.A. (1993). A conserved signal transduction pathway regulating the activity of the rel-like proteins dorsal and NF-κB. Mol. Biol. Cell 4, 767-771.
70. Hashimoto, C., Hudson, K.L. and Anderson, K.V. (1988). The Toll gene of Drosophila, required for dorso-ventral embryonic polarity, appears to encode a transmembrane protein. Cell 52, 269-279.
71. Gay, N.J. and Keith, F.J. (1991). Drosophila Toll and IL-1 receptor. Nature 351, 355-356.
72. Cao, Z., Henzel, W.J. and Gao, X. (1996). IRAK: a kinase associated with the Interleukin-1 receptor. Science 271, 1128-1131.
73. Trofimova, M., Sprenkle, A.B., Green, M., Sturgill, T.W., Goebl, M.G. and Harrington, M.A. (1996). Developmental and tissue-specific expression of mouse pelle-like protein kinase. J. Biol. Chem. 271, 17609-17612.
74. Lemaitre, B. et al. (1995). Functional analysis and regulation of nuclear import of dorsal during the immune response in Drosophila. EMBO J. 14, 536-545.
75. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J.M. and Hoffmann, J. A. (1996). The dorsoventral regulatory gene cassette spaetzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 1-20.
76. Lemaitre, B. et al. (1995). A recessive mutation, immune deficiency (imd), defines two distinct control pathways in the Drosophila host defense. Proc. Natl. Acad. Sci. USA 92, 9465-9469.
77. Reichhart, J.M., Georgel, P., Meister, M., Lemaitre, B., Kappler, C. and Hoffmann, J.A. (1993). Expression and nuclear translocation of the rel/NF-κB-related morphogen dorsal during the immune response of Drosophila. C. R. Acad. Sci. Paris/Life Sciences 316, 1218-1224.
78. Ip, Y.T. et al. (1993). Dif, a dorsal-related gene that mediates an immune response in Drosophila. Cell 75, 753-763.
79. Dushay, M., Asling, B. and Hultmark, D. (1996). Origins of immunity: relish, a compound Rel-like gene in the antibacterial defense of Drosophila. Proc. Natl Acad. Sci. USA 93, 10343-10347.
80. Petersen, U.M., Björklund, G., Ip, Y.T. and Engström, Y. (1995). The dorsal-related immunity factor, Dif, is a sequence-specific trans-activator of Drosophila cecropin gene expression. EMBO J. 14, 3146-3158.
81. Schneider, D.S., Jin, Y., Morisato, D. and Anderson, K.V. (1994). A processed form of the Spätzle protein defines dorsal-ventral polarity in the Drosophila embryo. Development 120, 1243-1250.
82. Morisato, D. and Anderson, K.V. (1995). Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu. Rev. Genet 29, 371-399.
83. McDonald, N.Q. and Hendrickson, W.A. (1993) A structural superfamily of growth factors containing a cysteine knot motif. Cell 73, 421-424.
84. Bergner, A. et al. (1996) Crystal structure of coagulogen, the clotting protein from horseshoe crab: a structural homologue of nerve groxth factor. EMBO J. 15, 6789-6797.
85. Belvin, M.P. and Anderson, K.V. (1996) A conserved signaling pathway: the Drosophila Toll-Dorsal pathway. Annu. Rev. Cell Dev. Biol. 12, 393-416.
86. Pearson, A., Lux, A. and Krieger, M. (1995). Expression cloning of dSR-Cl, a class C macrophage-specific scavenger receptor from Drosophila melanogaster. Proc. Natl Acad. Sci. USA 92, 4056-4060.
87. Franc, N.C., Dimarcq, J.L., Lagueux, M., Hoffmann, J.A. and Ezekowitz, R.A.B. (1996). Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431-443.
88. Rizki, T.M. and Rizki, R.M. (1984). The cellular defense system of Drosophila melanogaster. In Insect Ultrastructure, Vol. 2. (ed. R. C. King and H. Akai), pp. 579-604. Plenum Publishing Corporation.