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J. Biol. Chem., Vol. 279, Issue 23, 24116-24122, June 4, 2004

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Zebrafish Reveals Different and Conserved Features of Vertebrate Neuroglobin Gene Structure, Expression Pattern, and Ligand Binding^*

Christine Fuchs, Valeska Heib¶, Laurent Kiger||, Mark Haberkamp¶, Anja Roesner¶, Marc Schmidt¶, Djemel Hamdane||, Michael C. Marden||, Thomas Hankeln, and Thorsten Burmester¶**

From the Institute of Molecular Genetics, Johannes Gutenberg University of Mainz, D-55099 Mainz, Germany, ^¶Institute of Zoology, Johannes Gutenberg University of Mainz, D-55099 Mainz, Germany, and ^||INSERM U473, 84 rue du General Leclerc, F-94276 Le Kremlin-Bicetre, France

Neuroglobin has been identified as a respiratory protein that is primarily expressed in the mammalian nervous system. Here we present the first detailed analysis of neuroglobin from a non-mammalian vertebrate, the zebrafish Danio rerio. The zebrafish neuroglobin gene reveals a mammalian-type exon-intron pattern in the coding region (B12.2, E11.0, and G7.0), plus an additional 5'-non-coding exon. Similar to the mammalian neuroglobin, the zebrafish protein displays a hexacoordinate deoxy-binding scheme. Flash photolysis kinetics show the competitive binding on the millisecond timescale of external ligands and the distal histidine, resulting in an oxygen affinity of 1 torr. Western blotting, immune staining, and mRNA in situ hybridization demonstrate neuroglobin expression in the fish central nervous system and the retina but also in the gills. Neurons containing neuroglobin have a widespread distribution in the brain but are also present in the olfactory system. In the fish retina, neuroglobin is mainly present in the inner segments of the photoreceptor cells. In the gills, the chloride cells were identified to express neuroglobin. Neuroglobin appears to be associated with mitochondria-rich cell types and thus oxygen consumption rates, suggesting a myoglobin-like function of this protein in facilitated oxygen diffusion.

Received for publication, February 24, 2004 , and in revised form, March 22, 2004.

^* This work was supported by the Deutsche Forschungsgemeinschaft (Ha2103/3, Bu956/5), INSERM, the Délégation Générale pour l'Armement, and European Union (QLRT-2001-01548). 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 on-line version of this article (available at http://www.jbc.org) contains Figs. S1–S5 and Tables S1–S2.

Both authors contributed equally to this work.

^** To whom correspondence should be addressed: Institute of Zoology, University of Mainz, D-55099 Mainz, Germany. Tel.: 49-6131-39-24477; Fax: 49-6131-39-24652; E-mail: burmeste{at}uni-mainz.de.

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