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Evolution of the neuropeptide Y receptor family: gene and chromosome duplications deduced from the cloning and mapping of the five receptor subtype genes in pig.

ABSTRACT: Neuropeptide Y (NPY) receptors mediate a variety of physiological responses including feeding and vasoconstriction. To investigate the evolutionary events that have generated this receptor family, we have sequenced and determined the chromosomal localizations of all five presently known mammalian NPY receptor subtype genes in the domestic pig, Sus scrofa (SSC). The orthologs of the Y(1) and Y(2) subtypes display high amino acid sequence identities between pig, human, and mouse (92%-94%), whereas the Y(4), Y(5), and y(6) subtypes display lower identities (76%-87%). The lower identity of Y(5) is due to high sequence divergence in the large third intracellular loop. The NPY1R, NPY2R, and NPY5R receptor genes were localized to SSC8, the NPY4R to SSC14, and NPY6R to SSC2. Our comparisons strongly suggest that the tight cluster of NPY1R, NPY2R, and NPY5R on human chromosome 4 (HSA4) represents the ancestral configuration, whereas the porcine cluster has been split by two inversions on SSC8. These 3 genes, along with adjacent genes from 14 other gene families, form a cluster on HSA4 with extensive similarities to a cluster on HSA5, where NPY6R and >13 other paralogs reside, as well as another large cluster on HSA10 that includes NPY4R. Thus, these gene families have expanded through large-scale duplications. The sequence comparisons show that the NPY receptor triplet NPY1R-NPY2R-NPY5R existed before these large-scale duplications.

SUBMITTER: Wraith A

PROVIDER: S-EPMC311425 | biostudies-literature | 2000 Mar

REPOSITORIES: biostudies-literature

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Evolution of the neuropeptide Y receptor family: gene and chromosome duplications deduced from the cloning and mapping of the five receptor subtype genes in pig.

Wraith A A Törnsten A A Chardon P P Harbitz I I Chowdhary B P BP Andersson L L Lundin L G LG Larhammar D D

Genome research 20000301 3

Neuropeptide Y (NPY) receptors mediate a variety of physiological responses including feeding and vasoconstriction. To investigate the evolutionary events that have generated this receptor family, we have sequenced and determined the chromosomal localizations of all five presently known mammalian NPY receptor subtype genes in the domestic pig, Sus scrofa (SSC). The orthologs of the Y(1) and Y(2) subtypes display high amino acid sequence identities between pig, human, and mouse (92%-94%), whereas ...[more]

PMID: 10720571

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Project description:BACKGROUND: One of the many gene families that expanded in early vertebrate evolution is the neuropeptide (NPY) receptor family of G-protein coupled receptors. Earlier work by our lab suggested that several of the NPY receptor genes found in extant vertebrates resulted from two genome duplications before the origin of jawed vertebrates (gnathostomes) and one additional genome duplication in the actinopterygian lineage, based on their location on chromosomes sharing several gene families. In this study we have investigated, in five vertebrate genomes, 45 gene families with members close to the NPY receptor genes in the compact genomes of the teleost fishes Tetraodon nigroviridis and Takifugu rubripes. These correspond to Homo sapiens chromosomes 4, 5, 8 and 10. RESULTS: Chromosome regions with conserved synteny were identified and confirmed by phylogenetic analyses in H. sapiens, M. musculus, D. rerio, T. rubripes and T. nigroviridis. 26 gene families, including the NPY receptor genes, (plus 3 described recently by other labs) showed a tree topology consistent with duplications in early vertebrate evolution and in the actinopterygian lineage, thereby supporting expansion through block duplications. Eight gene families had complications that precluded analysis (such as short sequence length or variable number of repeated domains) and another eight families did not support block duplications (because the paralogs in these families seem to have originated in another time window than the proposed genome duplication events). RT-PCR carried out with several tissues in T. rubripes revealed that all five NPY receptors were expressed in the brain and subtypes Y2, Y4 and Y8 were also expressed in peripheral organs. CONCLUSION: We conclude that the phylogenetic analyses and chromosomal locations of these gene families support duplications of large blocks of genes or even entire chromosomes. Thus, these results are consistent with two early vertebrate tetraploidizations forming a paralogon comprising human chromosomes 4, 5, 8 and 10 and one teleost tetraploidization. The combination of positional and phylogenetic data further strengthens the identification of orthologs and paralogs in the NPY receptor family.

Project description:BackgroundPrevious studies in the Norwegian pig breeds Landrace and Duroc have revealed a QTL for levels of skatole located in the region 74.7-80.5 Mb on SSC7. Skatole is one of the main components causing boar taint, which gives an undesirable smell and taste to the pig meat when heated. Surgical castration of boars is a common practice to reduce the risk of boar taint, however, a selection for boars genetically predisposed for low levels of taint would help eliminating the need for castration and be advantageous for both economic and welfare reasons. In order to identify the causal mutation(s) for the QTL and/or identify genetic markers for selection purposes we performed a fine mapping of the SSC7 skatole QTL region.ResultsA dense set of markers on SSC7 was obtained by whole genome re-sequencing of 24 Norwegian Landrace and 23 Duroc boars. Subsets of 126 and 157 SNPs were used for association analyses in Landrace and Duroc, respectively. Significant single markers associated with skatole spanned a large 4.4 Mb region from 75.9-80.3 Mb in Landrace, with the highest test scores found in a region between the genes NOVA1 and TGM1 (p < 0.001). The same QTL was obtained in Duroc and, although less significant, with associated SNPs spanning a 1.2 Mb region from 78.9-80.1 Mb (p < 0.01). The highest test scores in Duroc were found in genes of the granzyme family (GZMB and GZMH-like) and STXBP6. Haplotypes associated with levels of skatole were identified in Landrace but not in Duroc, and a haplotype block was found to explain 2.3% of the phenotypic variation for skatole. The SNPs in this region were not associated with levels of sex steroids.ConclusionsFine mapping of a QTL for skatole on SSC7 confirmed associations of this region with skatole levels in pigs. The QTL region was narrowed down to 4.4 Mb in Landrace and haplotypes explaining 2.3% of the phenotypic variance for skatole levels were identified. Results confirmed that sex steroids are not affected by this QTL region, making these markers attractive for selection against boar taint.

Dataset Information

Evolution of the neuropeptide Y receptor family: gene and chromosome duplications deduced from the cloning and mapping of the five receptor subtype genes in pig.

Publications

Evolution of the neuropeptide Y receptor family: gene and chromosome duplications deduced from the cloning and mapping of the five receptor subtype genes in pig.

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