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Effects of Variants in Proopiomelanocortin and Neuropeptide Y Genes on Growth, Carcass, and Meat Quality Traits in Rabbits

  • Liu, Wen-Chao (Institute of Animal Genetics and Breeding, Sichuan Agricultural University) ;
  • Chen, Shi-Yi (Institute of Animal Genetics and Breeding, Sichuan Agricultural University) ;
  • Jia, Xian-Bo (Institute of Animal Genetics and Breeding, Sichuan Agricultural University) ;
  • Wang, Jie (Institute of Animal Genetics and Breeding, Sichuan Agricultural University) ;
  • Lai, Song-Jia (Institute of Animal Genetics and Breeding, Sichuan Agricultural University)
  • Received : 2013.12.09
  • Accepted : 2014.03.14
  • Published : 2014.05.01

Abstract

Appetite-related neuropeptides proopiomelanocortin (POMC) and Neuropeptide Y (NPY) are essential for regulating feeding behavior and energy homeostasis. The objective of this study was to evaluate the effects of variants in POMC and NPY genes on growth, carcass and meat quality traits in rabbits. A total of six SNPs were identified for POMC (n = 2) and NPY (n = 4) genes by direct sequencing. Three SNPs were subsequently genotyped by using MassArray system (Sequenom iPLEXassay) in 235 individuals, which belong to three meat rabbit breeds, including 93 Ira rabbits; 81 Champagne rabbits and 61 Tianfu black rabbits. The SNP c.112-12G>T was in intron-exon boundaries (intron 1) of POMC gene, and the association analysis showed that individuals with TT genotype had a greater 84 d body weight (BW84), eviscerated weight and semi-eviscerated weight than those with GT genotype (p<0.05); the TT individuals were also higher than those GG in the ripe meat ratio (RMR) (p<0.05). The g.1778G>C SNP, which was in complete linkage with other three SNPs (g.1491G>A, g.1525G>T and g.1530C>T) in intron 1 of NPY gene, was significantly correlated with eviscerated slaughter percentage and semi-eviscerated slaughter percentage in rabbits, and the individuals with CC genotype had a better performance than CG genotype (p<0.05). These findings would provide primary clues for the biological roles of POMC and NPY underlying the rabbit growth-related traits.

Keywords

References

  1. Baker, M., N. Gaukrodger, B. M. Mayosi, H. Imrie, M. Farrall, H. Watkins, J. M. C. Connell, P. J. Avery, and B. Keavney. 2005. Association between common polymorphisms of the proopiomelanocortin gene and body fat distribution a family study. Diabetes 54:2492-2496. https://doi.org/10.2337/diabetes.54.8.2492
  2. Bazhan, N. and D. Zelena. 2013. Food-intake regulation during stress by the hypothalamo-pituitary-adrenal axis. Brain Res. Bull. 95:46-53. https://doi.org/10.1016/j.brainresbull.2013.04.002
  3. Botstein, D., R. L. White, M. Skolnick, and R. W. Davis. 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am. J. Hum. Genet. 32:314-331.
  4. Bray, M. S., E. Boerwinkle, and C. L. Hanis. 2000. Sequence variation within the neuropeptide Y gene and obesity in Mexican Americans. Obes. Res. 8:219-226. https://doi.org/10.1038/oby.2000.25
  5. Buchanan, F. C., T. D. Thue, P. Yu, and D. C. Winkelman-Sim. 2005. Single nucleotide polymorphisms in the corticotrophin-releasing hormone and pro-opiomelancortin genes are associated with growth and carcass yield in beef cattle. Anim. Genet. 36:127-131. https://doi.org/10.1111/j.1365-2052.2005.01255.x
  6. Cai, G., S. A. Cole, R. A. Bastarrachea-Sosa, J. W. MacCluer, J. Blangero, and A. G. Comuzzie. 2004. Quantitative trait locus determining dietary macronutrient intakes is located on human chromosome 2p22. Am. J. Clin. Nutr. 80:1410-1414.
  7. Casas, E., J. W. Keele, S. D. Shackelford, M. Koohmaraie, and R. T. Stone. 2004. Identification of quantitative trait loci for growth and carcass composition in cattle. Anim. Genet. 35:2-6. https://doi.org/10.1046/j.1365-2052.2003.01067.x
  8. Chen, F. Y., H. Niu, J. Q. Wang, C. Z. Lei, X. Y. Lan, C. L. Zhang, M. J. Li, L. S. Hua, J. Wang, and H. Chen. 2011. Polymorphism of DLK1 and CLPG gene and their association with phenotypic traits in Chinese cattle. Mol. Biol. Rep. 38: 243-248. https://doi.org/10.1007/s11033-010-0101-7
  9. Clark, J. T., P. S. Kalra, and S. P. Kalra. 1985. Neuropeptide Y stimulates feeding but inhibits sexual behavior in rats. Endocrinology 117:2435-2442. https://doi.org/10.1210/endo-117-6-2435
  10. Delplanque, J., M. Barat-Houari, C. Dina, P. Gallina, K. Clement, B. Guy-Grand, F. Vasseur, P. Boutin, and P. Froguel. 2000. Linkage and association studies between the proopiomelanocortin (POMC) gene and obesity in caucasian families. Diabetologia 43:1554-1557. https://doi.org/10.1007/s001250051568
  11. Ding, B., B. Kull, Z. Liu, S. Mottagui-Tabar, H. Thonberg, H. F. Gu, A. J. Brookes, L. Grundemar, C. Karlsson, and A. Hamsten. 2005. Human neuropeptide Y signal peptide gain-of-function polymorphism is associated with increased body mass index: possible mode of function. Regul. Pept. 127:45-53. https://doi.org/10.1016/j.regpep.2004.10.011
  12. Fontanesi, L., E. Scotti, K. Cisarova, P. D. Battista, S. Dall'Olio, D. Fornasini, and A. Frabetti. 2013. A missense mutation in the rabbit melanocortin 4 receptor (MC4R) gene is associated with finisching weight in a meat rabbit line. Anim. Biotechnol. 24: 268-277. https://doi.org/10.1080/10495398.2013.781034
  13. Guan, X., H. Yu, and L. H. Vander Ploeg. 1998. Evidence of altered hypothalamic pro-opiomelanocortin/neuropeptide Y mRNA expression in tubby mice. Mol. Brain Res. 59:273-279. https://doi.org/10.1016/S0169-328X(98)00150-8
  14. Hadley, M. E. and C. Haskell Luevano. 1999. The proopiomelanocortin system. Ann. NY Acad. Sci. 885:1-21.
  15. Hager, J., C. Dina, S. Francke, S. Dubois, M. Houari, V. Vatin, E. Vaillant, N. Lorentz, A. Basdevant, and K. Clement. 1998. A genome-wide scan for human obesity genes reveals a major susceptibility locus on chromosome 10. Nat. Genet. 20:304-308. https://doi.org/10.1038/3123
  16. Hillebrand, J., D. De Wied, and R. Adan. 2002. Neuropeptides, food intake and body weight regulation: a hypothalamic focus. Peptides 23:2283-2306. https://doi.org/10.1016/S0196-9781(02)00269-3
  17. Hixson, J. E., L. Almasy, S. Cole, S. Birnbaum, B. D. Mitchell, M. C. Mahaney, M. P. Stern, J. W. MacCluer, J. Blangero, and A. G. Comuzzie. 1999. Normal variation in leptin levels is associated with polymorphisms in the proopiomelanocortin gene, POMC. J. Clin. Endocrinol. Metab. 84:3187-3191.
  18. Kalra, S. P., M. G. Dube, A. Sahu, C. P. Phelps, and P. S. Kalra. 1991. Neuropeptide Y secretion increases in the paraventricular nucleus in association with increased appetite for food. Pro. Natl. Acad. Sci. 88:10931-10935. https://doi.org/10.1073/pnas.88.23.10931
  19. Karvonen, M. K., U. Pesonen, M. Koulu, L. Niskanen, M. Laakso, A. Rissanen, and J. M. Dekker. 1998. Association of a leucine (7)-to-proline (7) polymorphism in the signal peptide of neuropeptide Y with high serum cholesterol and LDL cholesterol levels. Nat. Med. 4:1434-1437. https://doi.org/10.1038/4027
  20. Kilpinen, H., S. M. Waszak, A. R. Gschwind, S. K. Raghav, R. M. Witwicki, A. Orioli, E. Migliavacca, M. Wiederkehr, M. Gutierrez-Arcelus, and N. I. Panousis. 2013. Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342:744-747. https://doi.org/10.1126/science.1242463
  21. Krude, H., H. Biebermann, W. Luck, R. Horn, G. Brabant, and A. Gruters. 1998. Severe early-onset obesity, adrenal insufficiency and red hair pigmentation caused by POMC mutations in humans. Nat. Genet. 19:155-157. https://doi.org/10.1038/509
  22. Lee, M. and S. L. Wardlaw. 2007. The central melanocortin system and the regulation of energy balance. Front. Biosci. 12:3994-4010. https://doi.org/10.2741/2366
  23. Li, A. J. and S. Ritter. 2004. Glucoprivation increases expression of neuropeptide Y mRNA in hindbrain neurons that innervate the hypothalamus. Eur. J. Neurosci. 19:2147-2154. https://doi.org/10.1111/j.1460-9568.2004.03287.x
  24. Li, G., C. V. Mobbs, and P. J. Scarpace. 2003. Central pro-opiomelanocortin gene delivery results in hypophagia, reduced visceral adiposity, and improved insulin sensitivity in genetically obese Zucker rats. Diabetes 52:1951-1957. https://doi.org/10.2337/diabetes.52.8.1951
  25. Mattevi, V. S., V. M. Zembrzuski, and M. H. Hutz. 2002. Association analysis of genes involved in the leptin-signaling pathway with obesity in Brazil. Int. J. Obes. 26:1179-1185. https://doi.org/10.1038/sj.ijo.0802067
  26. Mercer, R. E., M. J. Chee, and W. F. Colmers. 2011. The role of NPY in hypothalamic mediated food intake. Front. Neuroendocrinol. 32:398-415. https://doi.org/10.1016/j.yfrne.2011.06.001
  27. Mizoshita, K., T. Watanabe, H. Hayashi, C. Kubota, H. Yamakuchi, J. Todoroki, and Y. Sugimoto. 2004. Quantitative trait loci analysis for growth and carcass traits in a half-sib family of purebred Japanese Black (Wagyu) cattle. J. Anim. Sci. 82: 3415-3420.
  28. Nieuwenhuizen, A. G. and F. Rutters. 2008. The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol. Behav. 94:169-177. https://doi.org/10.1016/j.physbeh.2007.12.011
  29. Olza, J., M. Gil-Campos, R. Leis, A. I. Ruperez, R. Tojo, R. Canete, A. Gil, and C. M. Aguilera. 2013. Influence of variants in the NPY gene on obesity and metabolic syndrome features in Spanish children. Peptides 45:22-27. https://doi.org/10.1016/j.peptides.2013.04.007
  30. Rotimi, C. N., A. G. Comuzzie, W. I. Lowe, A. Luke, J. Blangero, and R. S. Cooper. 1999. The quantitative trait locus on chromosome 2 for serum leptin levels is confirmed in African-Americans. Diabetes -American Diabetes Association 48:643-644.
  31. Sherman, E. L., J. D. Nkrumah, B. M. Murdoch, C. Li, Z. Wang, A. Fu, and S. S. Moore. 2008. Polymorphisms and haplotypes in the bovine neuropeptide Y, growth hormone receptor, ghrelin, insulin-like growth factor 2, and uncoupling proteins 2 and 3 genes and their associations with measures of growth, performance, feed efficiency, and carcass merit in beef cattle. J. Anim. Sci. 86:1-16. https://doi.org/10.2527/jas.2007-0687
  32. Takeuchi, S., K. Teshigawara, and S. Takahashi. 1999. Molecular cloning and characterization of the chicken pro-opiomelanocortin (POMC) gene. Biochim. Biophys. Acta Mol. Cell Res. 1450:452-459. https://doi.org/10.1016/S0167-4889(99)00046-4
  33. Thue, T. D. and F. C. Buchanan. 2003. Linkage mapping of POMC to bovine chromosome 11. Anim. Genet. 34:149-150. https://doi.org/10.1046/j.1365-2052.2003.00965_3.x
  34. Tritos, N. A., J. K. Elmquist, J. W. Mastaitis, J. S. Flier, and E. Maratos-Flier. 1998. Characterization of expression of hypothalamic appetite-regulating peptides in obese hyperleptinemic brown adipose tissue-deficient (uncoupling protein-promoter-driven diphtheria toxin A) mice. Endocrinology 139:4634-4641.
  35. Van Rossum, C., H. Pijl, R. Adan, B. Hoebee, and J. C. Seidell. 2006. Polymorphisms in the NPY and AGRP genes and body fatness in Dutch adults. Int. J. Obes. 30:1522-1528. https://doi.org/10.1038/sj.ijo.0803314
  36. Wang, C. L., C. L. Meng, S. X. Cao, J. Zhang, C. H. Meng, H. L. Wang, Y. F. Fang, D. D. Zhu, and D. G. Mao. 2013. Single nuclear polymorphism in exon 3 of POMC gene and the association with growth traits in Hu sheep and East Friesian Hu crossbred sheep. Hereditas (Beijing) 35:1-9. https://doi.org/10.3724/SP.J.1005.2013.00001
  37. Zhang, C. L., Y. H. Wang, H. Chen, C. Z. Lei, X. T. Fang, J. Q. Wang, G. B. Ma, H. Niu, and J. Xiao. 2009. The polymorphism of bovine POMC gene and its association with the growth traits of Nanyang cattle. Hereditas (Beijing) 31:1221-1225. https://doi.org/10.3724/SP.J.1005.2009.01221
  38. Zhang, G. W., L. Gao, S. Y. Chen, X. B. Zhao, Y. F. Tian, X. Wang, X. S. Deng, and S. J. Lai. 2013. Single nucleotide polymorphisms in the FTO gene and their association with growth and meat quality traits in rabbits. Gene 527:553-557. https://doi.org/10.1016/j.gene.2013.06.024
  39. Zhang, G. W., H. Z. Wang, S. Y. Chen, Z. C. Li, W. X. Zhang, and S. J. Lai. 2011. A reduced incidence of digestive disorders in rabbits is associated with allelic diversity at the TLR4 locus. Vet. Immunol. Immunopathol. 144:482-486. https://doi.org/10.1016/j.vetimm.2011.08.009
  40. Zhang, L., A. L. Zhang, L. Z. Zhang, Q. Zhang, C. L. Zhang, X. Y. Lan, and H. Chen. 2011. Association analysis between variants in bovine NPY gene and growth traits in Nanyang cattle (Bos tarus). Gen. Comp. Endocrinol. 170:189-192. https://doi.org/10.1016/j.ygcen.2010.10.004

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