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J. Biol. Chem., Vol. 279, Issue 42, 43828-43837, October 15, 2004

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Up-regulation of Neurohemerythrin Expression in the Central Nervous System of the Medicinal Leech, Hirudo medicinalis, following Septic Injury^*

David Vergote, Pierre-Eric Sautière, Franck Vandenbulcke, Didier Vieau, Guillaume Mitta, Eduardo R. Macagno¶, and Michel Salzet||

From the Laboratoire de Neuroimmunologie des Annélides, UMR 8017 CNRS, IFR 17 INSERM, Université des Sciences et Technologies de Lille, 59655 Villeneuve d'Ascq, France, the Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne Parasitologie Fonctionnelle et Évolutive, UMR 5555 CNRS, Université de Perpignan, 66860 Perpignan Cedex, France, and the ^¶Section of Cell and Developmental Biology, Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093

We report here some results of a proteomic analysis of changes in protein expression in the leech Hirudo medicinalis in response to septic injury. Comparison of two-dimensional protein gels revealed several significant differences between normal and experimental tissues. One protein found to be up-regulated after septic shock was identified, through a combination of Edman degradation, mass spectrometry, and molecular cloning, as a novel member of the hemerythrin family, a group of non-heme-iron oxygen transport proteins found in four invertebrate phyla: sipunculids, priapulids, brachiopods, and annelids. We found by in situ hybridization and immunocytochemistry that the new leech protein, which we have called neurohemerythrin, is indeed expressed in the leech central nervous system. Both message and protein were detected in the pair of large glia within the ganglionic neuropile, in the six packet glia that surround neuronal somata in each central ganglion, and in the bilateral pair of glia that separate axonal fascicles in the interganglionic connective nerves. No expression was detected in central neurons or in central nervous system microglia. Expression was also observed in many other, non-neuronal tissues in the body wall. Real-time PCR experiments suggest that neurohemerythrin is up-regulated posttranscriptionaly. We consider potential roles of neurohemerythrin, associated with its ability to bind oxygen and iron, in the innate immune response of the leech nervous system to bacterial invasion.

Received for publication, March 19, 2004 , and in revised form, July 14, 2004.

^* This work was supported in part by the Centre National de la Recherche Scientifique, the Ministère de l'Education Nationale, de la Recherche et des Technologies, the Fond Economique du Développement Européen et Régional, the Conseil Régional Nord-Pas-de-Calais, the Génopôle de Lille, the Plateau de Protéomique de l'Université des Sciences et Technologies de Lille, and the National Institutes of Health-Fogarty Grant. 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) AY521548 (for the nucleotide and amino acid sequences for neurohemerythrin gene and protein).

^|| 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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