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J. Biol. Chem., Vol. 279, Issue 30, 30973-30982, July 23, 2004

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Molecular Characterization of Two Novel Antibacterial Peptides Inducible upon Bacterial Challenge in an Annelid, the Leech Theromyzon tessulatum^*

Aurélie Tasiemski, Franck Vandenbulcke, Guillaume Mitta, Jérôme Lemoine¶, Christophe Lefebvre, Pierre-Eric Sautière, and Michel Salzet||

From the Centre National de la Recherche Scientifique, Laboratoire de Neuroimmunologie UMR 8017, SN3, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, France and the ^¶Centre National de la Recherche Scientifique, Laboratoire de Glycobiologie Structurale et Fonctionnelle UMR 8576, C9, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, France

Two novel antimicrobial peptides named theromacin and theromyzin were isolated and characterized from the coelomic liquid of the leech Theromyzon tessulatum. Theromacin is a 75-amino acid cationic peptide containing 10 cysteine residues arranged in a disulfide array showing no similarities with other known antimicrobial peptides. Theromyzin is an 86-amino acid linear peptide and constitutes the first anionic antimicrobial peptide observed in invertebrates. Both peptides exhibit activity directed against Gram-positive bacteria. Theromacin and theromyzin cDNAs code precursor molecules containing a putative signal sequence directly followed by the mature peptide. The enhancement of theromacin and theromyzin mRNA levels has been observed after blood meal ingestion and upon bacterial challenge. In situ hybridization revealed that both genes are expressed in large fat cells in contact with coelomic cavities. Gene products were immunodetected in large fat cells, in intestinal epithelia, and at the epidermis level. In addition, a rapid release of the peptides into the coelomic liquid was observed after bacterial challenge. The presence of antimicrobial peptide genes in leeches and their expression in a specific tissue functionally resembling the insect fat body provide evidence for the first time of an antibacterial response in a lophotrochozoan comparable to that of holometabola insects.

Received for publication, November 6, 2003 , and in revised form, April 9, 2004.

^* This work was supported by the Agence Nationale de Valorisation de la Recherche, the CNRS, the Ministére de l'Education Nationale de la Recherche et de la Technologie, the Fonds Europeens de Developpement Régional, the Genopole, and the Conseil Régional Nord-Pas de Calais. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY434032 and AY434033.

Present address: Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université de Perpignan, Ave. de Villeneuve, 66860 Perpignan Cedex, France.

^|| To whom correspondence should be addressed. Tel.: 33-3-20-43-68-39; Fax: 33-3-20-43-40-54; E-mail: michel.salzet{at}univ-lille1.fr.

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