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Novel Polymorphisms of Adrenergic, Alpha-1B-, Receptor and Peroxisome Proliferator-activated Receptor Gamma, Coactivator 1 Beta Genes and Their Association with Egg Production Traits in Local Chinese Dagu Hens

  • Mu, F. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University) ;
  • Jing, Y. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University) ;
  • Qin, N. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University) ;
  • Zhu, H.Y. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University) ;
  • Liu, D.H. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University) ;
  • Yuan, S.G. (Jilin Grain Group Agriculture and Livestock Co., Ltd.) ;
  • Xu, R.F. (Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Jilin Agricultural University)
  • Received : 2015.09.23
  • Accepted : 2015.11.24
  • Published : 2016.09.01

Abstract

Adrenergic, alpha-1B-, receptor (ADRA1B) and peroxisome proliferator-activated receptor gamma, coactivator 1 beta (PPARGC1B) genes are involved in regulation of hen ovarian development. In this study, these two genes were investigated as possible molecular markers associated with hen-housed egg production, egg weight (EW) and body weight in Chinese Dagu hens. Samples were analyzed using the polymerase chain reaction-single strand conformation polymorphism (PCR-SSCP) technique, followed by sequencing analysis. Two novel single nucleotide polymorphisms (SNPs) were identified within the candidate genes. Among them, an A/G transition at base position 1915 in exon 2 of ADRA1B gene and a T/C mutation at base position 6146 in the 3'- untranslated region (UTR) of PPARGC1B gene were found to be polymorphic and named SNP A1915G and T6146C, respectively. The SNP A1915G (ADRA1B) leads to a non-synonymous substitution (aspartic acid 489-to-glycine). The 360 birds from the Dagu population were divided into genotypes AA and AG, allele A was found to be present at a higher frequency. Furthermore, the AG genotype correlated with significantly higher hen-housed egg production (HHEP) at 30, 43, 57, and 66 wks of age and with a higher EW at 30 and 43 wks (p<0.05). For the SNP T6146C (PPARGC1B), the hens were typed into TT and TC genotypes, with the T allele shown to be dominant. The TC genotype was also markedly correlated with higher HHEP at 57 and 66 wks of age and EW at 30 and 43 wks (p<0.05). Moreover, four haplotypes were reconstructed based on these two SNPs, with the AGTC haplotype found to be associated with the highest HHEP at 30 to 66 wks of age and with higher EW at 30 and 43 wks (p<0.05). Collectively, the two SNPs identified in this study might be used as potential genetic molecular markers favorable in the improvement of egg productivity in chicken breeding.

Keywords

References

  1. Aguado, L. and S. R. Ojeda. 1986. Prepubertal rat ovary: Hormonal modulation of beta-adrenergic receptors and of progesterone response to adrenergic stimulation. Biol. Reprod. 34:45-50. https://doi.org/10.1095/biolreprod34.1.45
  2. Akhmetov, I. I., D. V. Popov, S. S. Missina, O. L. Vinogradova, and V. A. Rogozkin. 2009. The analysis of PPARGC1B gene polymorphism in athletes. Ross. Fiziol. Zh. Im. I. M. Sechenova 95:1247-1253.
  3. Allen, L. F., R. J. Lefkowitz, M. G. Caron, and S. Cotecchia. 1991. G-protein-coupled receptor genes as protooncogenes: Constitutively activating mutation of the alpha 1B-adrenergic receptor enhances mitogenesis and tumorigenicity. Proc. Natl. Acad. Sci. USA. 88:11354-11358. https://doi.org/10.1073/pnas.88.24.11354
  4. Biscarini, F., H. Bovenhuis, E. D. Ellen, S. Addo, and J. A. M. van Arendonk. 2010. Estimation of heritability and breeding values for early egg production in laying hens from pooled data. Poult. Sci. 89:1842-1849. https://doi.org/10.3382/ps.2010-00730
  5. Brunstrom, B., J. Axelsson, A. Mattsson, and K. Halldin. 2009. Effects of estrogens on sex differentiation in Japanese quail and chicken. Gen. Comp. Endocrinol. 163:97-103. https://doi.org/10.1016/j.ygcen.2009.01.006
  6. Cui, J. X., H. L. Du, Y. Liang, X. M. Deng, N. Li, and X. Q. Zhang. 2006. Association of polymorphisms in the promoter region of chicken prolactin with egg production. Poult. Sci. 85:26-31. https://doi.org/10.1093/ps/85.1.26
  7. Drummond, A. E., A. J. Baillie, and J. K. Findlay. 1999. Ovarian estrogen receptor alpha and beta mRNA expression: Impact of development and estrogen. Mol. Cell. Endocrinol. 149:153-161. https://doi.org/10.1016/S0303-7207(98)00247-0
  8. Drummond, A. E. and P. J. Fuller. 2012. Ovarian actions of estrogen receptor-${\beta}$: An update. Semin. Reprod. Med. 30:32-38. https://doi.org/10.1055/s-0031-1299595
  9. Eason, M. G. and S. B. Liggett. 1995. Identification of a Gs coupling domain in the amino terminus of the third intracellular loop of the alpha 2A-adrenergic receptor. Evidence for distinct structural determinants that confer Gs versus Gi coupling. J. Biol. Chem. 270:24753-24760. https://doi.org/10.1074/jbc.270.42.24753
  10. Feng, X. P., U. Kuhnlein, S. E. Aggrey, J. S. Gavora, and D. Zadworny. 1997. Trait association of genetic markers in the growth hormone and the growth hormone receptor gene in a White Leghorn strain. Poult. Sci. 76:1770-1775. https://doi.org/10.1093/ps/76.12.1770
  11. Gao, B. and G. Kunos. 1993. Isolation and characterization of the gene encoding the rat alpha 1B adrenergic receptor. Gene 131:243-237. https://doi.org/10.1016/0378-1119(93)90300-R
  12. Handschin, C. and B. M. Spiegelman. 2006. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27:728-735. https://doi.org/10.1210/er.2006-0037
  13. Hossain, M. M., N. Ghanem, M. Hoelker, F. Rings, C. Phatsara, E. Tholen, K. Schellander, and D. Tesfaye. 2009. Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genomics 10:443. https://doi.org/10.1186/1471-2164-10-443
  14. Hrabia, A., Y. Ha, and K. Shimada. 2004. Expression of estrogen receptor alpha mRNA in theca and granulosa layers of the ovary in relation to follicular growth in quail. Folia Biol. (Krakow) 52:191-195. https://doi.org/10.3409/1734916044527458
  15. Hrabia, A., M. Wilk, and J. Rzasa. 2008. Expression of alpha and beta estrogen receptors in the chicken ovary. Folia Biol. (Krakow) 56:187-191. https://doi.org/10.3409/fb.56_3-4.187-191
  16. Jewell-Motz, E. A., E. T. Donnelly, M. G. Eason, and S. B. Liggett. 1997. Role of the amino terminus of the third intracellular loop in agonist-promoted down-regulation of the alpha-2A adrenergic receptor. Biochemistry 36:8858-8863. https://doi.org/10.1021/bi970487x
  17. John, E., A. Wienecke-Baldacchino, M. Liivrand M, Heinaniemi, C. Carlberg, and L. Sinkkonen. 2012. Dataset integration identifies transcriptional regulation of microRNA genes by $PPAR{\gamma}$ in differentiating mouse 3T3-L1 adipocytes. Nucl. Acids Res. 40:4446-4460. https://doi.org/10.1093/nar/gks025
  18. Kim, M. H., D. S. Seo, and Y. Ko. 2004. Relationship between egg productivity and insulin-like growth factor-I genotypes in Korean native Ogol chickens. Poult. Sci. 83:1203-1208. https://doi.org/10.1093/ps/83.7.1203
  19. Kodama. D. and A. Togari. 2013. Noradrenaline stimulates cell proliferation by suppressing potassium channels via G(i/o) - protein-coupled ${\alpha}$(1B) -adrenoceptors in human osteoblasts. Br. J. Pharmacol. 168:1230-1239. https://doi.org/10.1111/bph.12000
  20. Kressler, D., S. N. Schreiber, D. Knutti, and A. Kralli. 2002. The PGC-1-related protein PERC is a selective coactivator of estrogen receptor alpha. J. Biol. Chem. 277:13918-13925. https://doi.org/10.1074/jbc.M201134200
  21. Lee, S. H., A. S. Jang, S. Woo Park, J. S. Park, Y. K. Kim, S. T. Uh, Y. H. Kim, I. Y. Chung, B. L. Park, H. D. Shin, and C. S. Park. 2011. Genetic effect of single-nucleotide polymorphisms in the PPARGC1B gene on airway hyperreactivity in asthmatic patients. Clin. Exp. Allergy 41:1533-1544. https://doi.org/10.1111/j.1365-2222.2011.03801.x
  22. Lin, J. D. 2009. Minireview: the PGC-1 coactivator networks: chromatin-remodeling and mitochondrial energy metabolism. Mol. Endocrinol. 23:2-10. https://doi.org/10.1210/me.2008-0344
  23. Linville, R. C., D. Pomp, R. K. Johnson, and M. F. Rothschild. 2001. Candidate gene analysis for loci affecting litter size and ovulation rate in swine. J. Anim. Sci. 79:60-67. https://doi.org/10.2527/2001.79160x
  24. Liu, W. J., D. X. Sun, Y. Yu, G Li, S. Q. Tang, Y. Zhang, Y. C. Wang, and Y. Zhang. 2010. Association of Janus kinase 2 polymorphisms with growth and reproduction traits in chickens. Poult. Sci. 89:2573-2579. https://doi.org/10.3382/ps.2010-00988
  25. Luo, P. T., R. Q. Yang, and N. Yang. 2007. Estimation of genetic parameters for cumulative egg numbers in a broiler dam line by using a random regression model. Poult. Sci. 86:30-36. https://doi.org/10.1093/ps/86.1.30
  26. Mallat, Y., E. Tritsch, R. Ladouce, D. L. Winter, B. Friquet, Z. Li, and M. Mericskay. 2014. Proteome modulation in H9c2 cardiac cells by microRNAs miR-378 and miR-378. Mol. Cell Proteomics 13:18-29. https://doi.org/10.1074/mcp.M113.030569
  27. McDerment, N. A., P. W. Wilson, D. Waddington, I. C. Dunn, and P. M. Hocking. 2012. Identification of novel candidate genes for follicle selection in the broiler breeder ovary. BMC Genomics 13:494. https://doi.org/10.1186/1471-2164-13-494
  28. Olah, M. E. and G. L. Stiles. 1998. Adenosine receptor-mediated signal transduction. In: Effects of Extracellular Adenosine and ATP on Cardiac Myocytes (Eds. A. Pelleg, L. Belardinelli). R. G. Landes Company, Austin, TX, USA. pp. 7-38.
  29. Olah, M. E. and G. L. Stiles. 2000. The role of receptor structure in determining adenosine receptor activity. Pharmacol. Ther. 85:55-75. https://doi.org/10.1016/S0163-7258(99)00051-0
  30. Onagbesan, O. M., S. Metayer, K. Tona, J. Williams, E. Decuypere, and V. Bruggeman. 2006. Effects of genotype and feed allowance on plasma luteinizing hormones, follicle-stimulating hormones, progesterone, estradiol levels, follicle differentiation, and egg production rates of broiler breeder hens. Poult. Sci. 85:1245-1258. https://doi.org/10.1093/ps/85.7.1245
  31. Park, K. S., H. D. Shin, B. L. Park, H. S. Cheong, Y. M. Cho, H. K. Lee, J. Y. Lee, J. K. Lee, H. T. Kim, C. S. Park, B. G. Han, K. Kimm, and B. Oh. 2006. Putative association of peroxisome proliferator-activated receptor gamma co-activator 1beta (PPARGC1B) polymorphism with Type 2 diabetes mellitus. Diabet. Med. 23:635-642.
  32. Piirainen, H., Y. Ashok, R. T. Nanekar, and V. P. Jaakola. 2011. Structural features of adenosine receptors: from crystal to function. Biochim. Biophys. Acta. 1808:1233-1244. https://doi.org/10.1016/j.bbamem.2010.05.021
  33. Ping, P. and J. E. Faber. 1993. Characterization of alpha-adrenoceptor gene expression in arterial and venous smooth muscle. Am. J. Physiol. 265:H1501-H1509. https://doi.org/10.1152/ajpcell.1993.265.6.C1501
  34. Port, J. D. and M. R. Bristow. 2001. Altered beta-adrenergic receptor gene regulation and signaling in chronic heart failure. J. Mol. Cell. Cardiol. 33:887-905. https://doi.org/10.1006/jmcc.2001.1358
  35. Qin, N., X. C. Fan, Y. Y. Zhang, X. X. Xu, T. L. Tyasi, Y. Jing, F. Mu, M. L. Wei, and R. F. Xu. 2015a. New insights into implication of the SLIT/ROBO pathway in the prehierarchical follicle development of hen ovary. Poult. Sci. 94:2235-2246. https://doi.org/10.3382/ps/pev185
  36. Qin, N., Q. Liu, Y. Y. Zhang, X. C. Fan, X. X. Xu, Z. C. Lv, M. L. Wei, Y. Jing, F. Mu, and R. F. Xu. 2015b. Association of novel polymorphisms of forkhead box L2 and growth differentiation factor-9 genes with egg production traits in local chinese Dagu hens. Poult. Sci. 94:88-95. https://doi.org/10.3382/ps/peu023
  37. Ramarao, C. S., J. M. Denker, D. M. Perez, R. J. Gaivin, R. P. Riek, and R. M. Graham. 1992. Genomic organization and expression of the human alpha 1B-adrenergic receptor. J. Biol. Chem. 267:21936-21945.
  38. Rothschild, M. F. and M. Soller. 1997. Candidate gene analysis to detect genes controlling traits of economic importance in domestic livestock. Probe 8:13-20.
  39. Sambrook, J. and D. W. Russell. 2001. Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York, USA.
  40. Scheer, A., T. Costa, F. Fanelli, P. G. De Benedetti, S. Mhaouty-Kodja, L. Abuin, M. Nenniger-Tosato, and S. Cotecchia. 2000. Mutational analysis of the highly conserved arginine within the Glu/Asp-Arg-Tyr motif of the alpha(1b)-adrenergic receptor: effects on receptor isomerization and activation. Mol. Pharmacol. 57:219-231.
  41. Shim, J. O., C. Y. Shin, T. S. Lee, S. J. Yang, J. Y. An, H. J. Song, T. H. Kim, I. H. Huh, and U. D. Soh. 2002. Signal transduction mechanism via adenosine A1 receptor in the cat esophageal smooth muscle cells. Cell. Signal. 14:365-372. https://doi.org/10.1016/S0898-6568(01)00270-4
  42. Stephens, M., N. J. Smith, and P. Donnelly. 2001. A new statisticalmethod for haplotype reconstruction frompopulation data. Am. J. Hum. Genet. 68:978-989. https://doi.org/10.1086/319501
  43. St-Pierre, J., J. Lin, S. Krauss, P. T. Tarr, R. Yang, C. B. Newgard, and B. M. Spiegelman. 2003. Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells. J. Biol. Chem. 278:26597-26603. https://doi.org/10.1074/jbc.M301850200
  44. Su, H., F. G. Silversides, and P. Villeneuve. 1996. Effects of sex-linked imperfect albinism (sal-s) in the chicken on the relationships of plasma concentrations of progesterone and17 beta-estradiol with egg production. Poult. Sci. 75:13-19. https://doi.org/10.3382/ps.0750013
  45. Tcherepanova, I., P. Puigserver, J. D. Norris, B. M. Spiegelman, and D. P. McDonnell. 2000. Modulation of estrogen receptor-alpha transcriptional activity by the coactivator PGC-1. J. Biol. Chem. 275:16302-16308. https://doi.org/10.1074/jbc.M001364200
  46. Venturini, G. C., R. P. Savegnago, B. N. Nunes, M. C. Ledur, G. S. Schmidt, L. El Faro, and D. P. Munari. 2013. Genetic parameters and principal component analysis for egg production from White Leghorn hens. Poult. Sci. 92:2283-2289. https://doi.org/10.3382/ps.2013-03123
  47. Waldrop, B. A., D. Mastalerz, M. T. Piascik, and G. R. Post. 2002. alpha(1B)- and alpha(1D)-Adrenergic receptors exhibit different requirements for agonist and mitogen-activated protein kinase activation to regulate growth responses in rat 1 fibroblasts. J. Pharmacol. Exp. Ther. 300:83-90. https://doi.org/10.1124/jpet.300.1.83
  48. Yang, S., S. Wang, A. Luo, T. Ding, Z. Lai, W. Shen, X. Ma, C. Cao, L. Shi, J. Jiang, F. Rong, L. Ma, Y. Tian, X. Du, Y. Lu, Y. Li, and S. Wang. 2013. Expression patterns and regulatory functions of microRNAs during the initiation of primordial follicle development in the neonatal mouse ovary. Biol. Reprod. 89:126. https://doi.org/10.1095/biolreprod.113.107730
  49. Yao, N., C. L. Lu, J. J. Zhao, H. F. Xia, D. G. Sun, X. Q. Shi, C. Wang, D. Li, Y. Cui, and X. Ma. 2009. A network of miRNAs expressed in the ovary are regulated by FSH. Front. Biosci. (Landmark Ed). 14:3239-3245.
  50. Yeh, F. C., R. C. Yang, T. B. J. Boyle, Z. H. Ye, and J. X. Mao. 1997. POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Edmonton, Alberta, Canada.
  51. Zhang, L., D. Y. Li, Y. P. Liu, Y. Wang, X. L. Zhao, and Q. Zhu. 2012. Genetic effect of the prolactin receptor gene on egg production traits in chickens. Genet. Mol. Res. 11:4307-4315. https://doi.org/10.4238/2012.October.2.1

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