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Birth and death of neuropeptide Y receptor genes in relation to the teleost fish tetraploidization
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
2008 (English)In: Gene, ISSN 0378-1119, E-ISSN 1879-0038, Vol. 409, no 1-2, 61-71 p.Article in journal (Refereed) Published
Abstract [en]

Extensive evidence exists for a genome duplication in the fish lineage leading to the species-rich clade of the telcosts, comprising > 99% of the known actinopterygian (ray-finned) fish species. Our previous studies of the neuropeptide Y receptor (NPYR) gene family suggested an ancestral gnathostome repertoire of 7 genes in 3 subfamilies. However, studies in the zebrafish have earlier identified only 5 NPYR genes, despite the expected increase in gene number due to the teleost tetraploidization. Notably, receptors Y-1, Y-5 and Y-6 were missing in the zebrafish genome database and only Y-8 had been duplicated. We report here an investigation of the evolutionary history of the Y-1 subfamily (Y-1, Y-4, Y-6 and Y-8) and the Y-5 receptor. Seven basal actinopterygian species and a shark were investigated and a total of 22 gene fragments were cloned and analyzed. Our results show that subtypes Y-1, Y-5 and Y-6 still exist in species representing basal actinopterygian lineages (bichir, sturgeon, gar and bowfin) as well as in some basal teleost lineages. Surprisingly we identified a zebrafish Y-1 receptor, the first Y-1 receptor found in euteleosts. Thus, these findings confirm the ancestral gnathostome repertoire of 7 NPYR genes and show that many of these receptors are present in basal actinopterygians as well as some basal teleosts. NPYR losses seem to have occurred relatively recently in euteleosts because Y-1, Y-5 and Y-6 are absent in the genome databases of two pufferfishes as well as medaka and stickleback and Y-5 and Y-6 are absent in the zebrafish database. A duplicate of Y-8 seems to be the only remaining receptor gene resulting from the teleost tetraploidization. The unexpected absence of the two appetite-stimulating receptors Y-1 and Y-5 in some euteleosts, along with our discovery of duplicates of the peptide ligands NPY and PYY, has implications for the role of the NPY system in euteleost feeding behavior.

Place, publisher, year, edition, pages
2008. Vol. 409, no 1-2, 61-71 p.
Keyword [en]
genome, NPY, peptide YY, G-protein coupled receptor, GPCR, ray-finned fish
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:uu:diva-96165DOI: 10.1016/j.gene.2007.11.011ISI: 000253275800008OAI: oai:DiVA.org:uu-96165DiVA: diva2:170645
Available from: 2007-09-07 Created: 2007-09-07 Last updated: 2017-12-14Bibliographically approved
In thesis
1. Evolution of the Neuropeptide Y System in Vertebrates with Focus on Fishes
Open this publication in new window or tab >>Evolution of the Neuropeptide Y System in Vertebrates with Focus on Fishes
2007 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Gene families in vertebrates often contain more dulicates (paralogs) than in invertebrates. This has been attributed to genome duplications, i.e., tetraploidizations. Two of the gene families that have expanded in vertebrate evolution are the neuropeptide Y (NPY) family of peptides and the neuropeptide Y receptors (NPYR) that are involved in many brain functions including appetite regulation.

Two NPYR genes, Y2 and Y7, were cloned in the rainbow trout. Although they arose from a common ancestral gene in early vertebrate evolution, their ligand-binding properties are very similar. Two NPYR genes were cloned in the coelacanth Latimeria chalumnae and found to be orthologs of Y5 and Y6 discovered in mammals.

Analyses of gene families close to the NPYR genes in the pufferfishes T. nigroviridis and T. rubripes showed that at least 25 additional gene families had an evolutionary history similar to the NPYR family, thereby providing evidence for fish specific-duplications of these chromosomes. Cloning and phylogenetic analysis of 22 NPYR gene fragments from several ray-finned fishes showed that basal species seem to have the same repertoire as tetrapods. Despite the tetraploidization in the teleost fish lineage, many teleosts seem to have fever genes than the gnathostome ancestor due to gene loss. Only one duplicate seems to have survived.

The NPY peptide family was found to have expanded in the teleost tetraploidization with duplicates of both NPY and PYY (peptide YY) in some teleosts. Fourteen neighboring gene families were found to have evolved in a similar manner as the NPY-family genes. Positional information fascilitated orthology assignment of peptide genes in teleost fishes and allowed correction of previously misidentified genes.

In summary, the evolutionary history of the NPY and NPYR gene families involve large-scale duplication events coinciding with the proposed tetraploidizations. The appearance of new genes in early vertebrates and in teleost fishes probably had important implications for the evolution of new functions in this system.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2007. 59 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 272
Keyword
Molecular biology, neuropeptide Y, GPCR, evolution, gene duplication, vertebrates, ray-finned fishes, Molekylärbiologi
Identifiers
urn:nbn:se:uu:diva-8189 (URN)978-91-554-6958-0 (ISBN)
Public defence
2007-09-28, B22, BMC, Husargatan 3, Uppsala, 10:15
Opponent
Supervisors
Available from: 2007-09-07 Created: 2007-09-07Bibliographically approved

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