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The sea lamprey tryptophan hydroxylase: new insight into the evolution of the serotonergic system of vertebrates

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Abstract

Recent research has shown that at least two tryptophan hydroxylase (Tph) genes are present in gnathostome vertebrates, but it is not known when the duplication of the ancestral Tph gene took place during evolution. By their position as an out-group of gnathostomes, lampreys (agnathans) are key models to understand molecular evolution in vertebrates. Here, we report the cloning of a Tph cDNA of the sea lamprey and the pattern of Tph mRNA expression in larval and postmetamorphic (young adult) sea lampreys using in situ hybridization. Phylogenetic analysis indicated that the lamprey Tph is an orthologue of Tphs of other vertebrates and suggested that the duplication of the ancestral Tph gene occurred before the separation of agnathans and gnathostomes, although alternative hypothesis are also discussed in the present study. In the sea lamprey brain, the Tph transcript was expressed in perikarya of the pineal organ, the retina, the diencephalic and rhombencephalic nuclei reported previously with serotonin immunohistochemistry and in small cells of the spinal cord, with a pattern similar to that observed with anti-serotonin antibodies. This suggests that expression of this Tph gene is shared by all lamprey serotonergic brain populations, unlike that reported in zebrafish and mammals for their different Tph genes. However, no Tph expression was observed in peripheral serotonergic cells, which, unlike in other vertebrates, are widely distributed in lampreys. Our results suggest that the selection of Tph2 to be expressed in raphe neurons may have occurred along the line leading to gnathostomes.

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Acknowledgments

This work was supported by a grant from the Xunta de Galicia (INCITE08PXIB200063PR) to M.C.R. A.B–I. was also supported by a Shriners Hospitals Postdoctoral Research Fellowship. The authors thank Ms. Cindy Laramore for her advice when cloning the Tph cDNA. We also thank the valuable suggestions of an anonymous reviewer on the discussion of Tph phylogeny.

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Authors and Affiliations

  1. Department of Cell Biology and Ecology, CIBUS, Faculty of Biology, University of Santiago de Compostela, 15782, Santiago de Compostela, Spain

    María Eugenia Cornide-Petronio, Ramón Anadón & María Celina Rodicio

  2. Shriners Hospitals Pediatric Research Center (Center for Neural Repair and Rehabilitation), Temple University School of Medicine, Rm. 680A, MERB, 3500 North Broad Street, Philadelphia, PA, 19140, USA

    Antón Barreiro-Iglesias

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  1. María Eugenia Cornide-Petronio
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  2. Ramón Anadón
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  3. María Celina Rodicio
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  4. Antón Barreiro-Iglesias
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Correspondence to Antón Barreiro-Iglesias.

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Cornide-Petronio, M.E., Anadón, R., Rodicio, M.C. et al. The sea lamprey tryptophan hydroxylase: new insight into the evolution of the serotonergic system of vertebrates. Brain Struct Funct 218, 587–593 (2013). https://doi.org/10.1007/s00429-012-0412-7

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  • DOI: https://doi.org/10.1007/s00429-012-0412-7

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