Apidaecin Multipeptide Precursor Structure: a Putative Mechanism for Amplification of the Insect Antibacterial Response

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1993 Apr 1

PMID 8467807

Citations 20

Authors

T Capaci

P Casteels

P Tempst

Affiliations

Soon will be listed here.

Abstract

Apidaecins are the most prominent components of the honeybee humoral defense against microbial invasion. Our analysis of cDNA clones indicated that up to 12 of these short peptides (2 kDa) can be generated by processing of single precursor proteins; different isoforms are hereby linked in one promolecule. Assembly of the multipeptide precursors and the putative three-step maturation are strongly reminiscent of yeast alpha-mating factor. Bioactive apidaecins are flanked by the two 'processing' sequences, EAEPEAEP (or variants) and RR; joined together, they form a single unit that is repeated numerous times. The number of such repeats is variable and was reflected in the observed diversity of transcript lengths. Each such transcript is likely to be encoded by a different gene, forming a tight gene cluster. While transcriptional activation upon bacterial challenge is not exceptionally fast, the multigene and multipeptide precursor nature of the apidaecin genetic information allows for amplification of the response, resulting in a real overproduction of peptide antibiotic. Enhanced efficiency of the 'immune' response to bacterial infection through such a mechanism is, to our knowledge, unique among insects.

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References

Cavener D . Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987; 15(4):1353-61. PMC: 340553. DOI: 10.1093/nar/15.4.1353. View

Matsuyama K, Natori S . Molecular cloning of cDNA for sapecin and unique expression of the sapecin gene during the development of Sarcophaga peregrina. J Biol Chem. 1988; 263(32):17117-21. View

Sun S, Asling B, Faye I . Organization and expression of the immunoresponsive lysozyme gene in the giant silk moth, Hyalophora cecropia. J Biol Chem. 1991; 266(10):6644-9. View

Dimarcq J, Zachary D, Hoffmann J, Hoffmann D, Reichhart J . Insect immunity: expression of the two major inducible antibacterial peptides, defensin and diptericin, in Phormia terranovae. EMBO J. 1990; 9(8):2507-15. PMC: 552280. DOI: 10.1002/j.1460-2075.1990.tb07430.x. View

Sun S, Lindstrom I, Lee J, Faye I . Structure and expression of the attacin genes in Hyalophora cecropia. Eur J Biochem. 1991; 196(1):247-54. DOI: 10.1111/j.1432-1033.1991.tb15811.x. View

Kainz P, Schmiedlechner A, STRACK H . In vitro amplification of DNA fragments greater than 10 kb. Anal Biochem. 1992; 202(1):46-9. DOI: 10.1016/0003-2697(92)90203-j. View

Mahbubani M, Bej A, Miller R, Atlas R, Dicesare J, Haff L . Detection of bacterial mRNA using polymerase chain reaction. Biotechniques. 1991; 10(1):48-9. View

Reichhart J, Essrich M, Dimarcq J, Hoffmann D, Hoffmann J, Lagueux M . Insect immunity. Isolation of cDNA clones corresponding to diptericin, an inducible antibacterial peptide from Phormia terranovae (Diptera). Transcriptional profiles during immunization. Eur J Biochem. 1989; 182(2):423-7. DOI: 10.1111/j.1432-1033.1989.tb14848.x. View

Casteels P, Ampe C, Jacobs F, Vaeck M, Tempst P . Apidaecins: antibacterial peptides from honeybees. EMBO J. 1989; 8(8):2387-91. PMC: 401180. DOI: 10.1002/j.1460-2075.1989.tb08368.x. View

10.

Zasloff M . Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, and partial cDNA sequence of a precursor. Proc Natl Acad Sci U S A. 1987; 84(15):5449-53. PMC: 298875. DOI: 10.1073/pnas.84.15.5449. View

11.

Matsumoto N, Okada M, Takahashi H, Ming Q, Nakajima Y, Nakanishi Y . Molecular cloning of a cDNA and assignment of the C-terminal of sarcotoxin IA, a potent antibacterial protein of Sarcophaga peregrina. Biochem J. 1986; 239(3):717-22. PMC: 1147345. DOI: 10.1042/bj2390717. View

12.

Reichhart J, Meister M, Dimarcq J, Zachary D, Hoffmann D, Ruiz C . Insect immunity: developmental and inducible activity of the Drosophila diptericin promoter. EMBO J. 1992; 11(4):1469-77. PMC: 556595. DOI: 10.1002/j.1460-2075.1992.tb05191.x. View

13.

Sun S, Faye I . Cecropia immunoresponsive factor, an insect immunoresponsive factor with DNA-binding properties similar to nuclear-factor kappa B. Eur J Biochem. 1992; 204(2):885-92. DOI: 10.1111/j.1432-1033.1992.tb16708.x. View

14.

von Heijne G . A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986; 14(11):4683-90. PMC: 311474. DOI: 10.1093/nar/14.11.4683. View

15.

Fuller R, Brake A, Thorner J . Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2+-dependent serine protease. Proc Natl Acad Sci U S A. 1989; 86(5):1434-8. PMC: 286710. DOI: 10.1073/pnas.86.5.1434. View

16.

Boman H, Boman I, Andreu D, Li Z, MERRIFIELD R, Schlenstedt G . Chemical synthesis and enzymic processing of precursor forms of cecropins A and B. J Biol Chem. 1989; 264(10):5852-60. View

17.

Shaw G, Kamen R . A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986; 46(5):659-67. DOI: 10.1016/0092-8674(86)90341-7. View

18.

Bulet P, Cociancich S, Dimarcq J, Lambert J, Reichhart J, Hoffmann D . Insect immunity. Isolation from a coleopteran insect of a novel inducible antibacterial peptide and of new members of the insect defensin family. J Biol Chem. 1991; 266(36):24520-5. View

19.

Wicker C, Reichhart J, Hoffmann D, Hultmark D, Samakovlis C, Hoffmann J . Insect immunity. Characterization of a Drosophila cDNA encoding a novel member of the diptericin family of immune peptides. J Biol Chem. 1990; 265(36):22493-8. View

20.

Walldorf U, Richter S, Ryseck R, Steller H, Edstrom J, Bautz E . Cloning of heat-shock locus 93D from Drosophila melanogaster. EMBO J. 1984; 3(11):2499-504. PMC: 557719. DOI: 10.1002/j.1460-2075.1984.tb02163.x. View