Occurrence of Two Distinct Urotensin II-Related Peptides in Zebrafish Provides New Insight into the Evolutionary History of the Urotensin II Gene Family

Author:

Parmentier Caroline1,Hameury Emilie23,Dubessy Christophe23,Quan Feng B.4,Habert Damien1,Calas André5,Vaudry Hubert23,Lihrmann Isabelle23,Tostivint Hervé234

Affiliation:

1. Centre National de la Recherche Scientifique (CNRS) Unité Mixte de Recherche (UMR) 7224 (C.P., A.C.), Institut National de la Santé et de la Recherche Médicale (INSERM) UMR 952, Physiopathologie des Maladies du Système Nerveux Central, Université Pierre et Marie Curie, 75252 Paris, France;

2. INSERM Unité 982 (E.H., C.D., H.V., I.L., H.T.), Différenciation et Communication Neuronale et Neuroendocrine, 76821 Mont-Saint-Aignan, France;

3. Institut Fédératif de Recherches Multidisciplinaires sur les Peptides 23 (E.H., C.D., H.V., I.L., H.T.), Plateforme de Recherche en Imagerie Cellulaire de Haute-Normandie, Université de Rouen, 76821 Mont-Saint-Aignan, France;

4. CNRS UMR 7221 (F.B.Q., D.H., H.T.), Evolution des Régulations Endocriniennes, Muséum National d'Histoire Naturelle, 75231 Paris, France;

5. CNRS UMR 5297 (A.C.), Institut Interdisciplinaire de Neurosciences, Université de Bordeaux 2, 33077 Bordeaux, France

Abstract

The urotensin II (UII) family is currently known to consist of two paralogous peptides, namely UII and UII-related peptide (URP). In contrast to UII, which has been identified in all vertebrate classes so far, URP has only been characterized in tetrapods. We report here the occurrence of two distinct URP genes in teleosts, which we have named URP1 and URP2. Synteny analysis revealed that teleost URP1 and URP2 genes and tetrapod URP genes represent three distinct paralog genes that, together with the UII gene, probably arose from the two rounds of tetraploidization, which took place early in vertebrate evolution. The absence of URP in fish indicates that the corresponding gene has been lost in the teleost lineage, whereas it is likely that both the URP1 and URP2 genes have been lost in the tetrapod lineage. Quantitative RT-PCR analysis revealed that the URP2 gene is mainly expressed in the spinal cord and the brain in adult zebrafish. In situ hybridization experiments showed that in zebrafish embryos, URP2 mRNA-containing cells are located in the floor plate of the neural tube. In adult, URP2-expressing cells occur in close contact with the ventral side of the ependymal canal along the whole spinal cord, whereas in the brain, they are located below the fourth ventricle. These URP-expressing cells may correspond to cerebrospinal fluid-contacting neurons. In conclusion, our study reveals the occurrence of four distinct UII paralogous systems in vertebrates that may exert distinct functions, both in tetrapods and teleosts.

Publisher

The Endocrine Society

Subject

Endocrinology

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