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Dietary calcium deficiency suppresses follicle selection in laying ducks through mechanism involving cyclic adenosine monophosphate-mediated signaling pathway

  • W. Chen (a1) (a2) (a3) (a4) (a5), W. G. Xia (a1) (a2) (a3) (a4) (a5), D. Ruan (a1) (a2) (a3) (a4) (a5), S. Wang (a1) (a2) (a3) (a4) (a5), K. F. M. Abouelezz (a1) (a2) (a3) (a4) (a5) (a6), S. L. Wang (a1) (a2) (a3) (a4) (a5), Y. N. Zhang (a1) (a2) (a3) (a4) (a5) and C. T. Zheng (a1) (a2) (a3) (a4) (a5)...

Abstract

Ovarian follicle selection is a natural biological process in the pre-ovulatory hierarchy in birds that drives growing follicles to be selected within the ovulatory cycle. Follicle selection in birds is strictly regulated, involving signaling pathways mediated by dietary nutrients, gonadotrophic hormones and paracrine factors. This study aimed to test the hypothesis that dietary Ca may participate in regulating follicle selection in laying ducks through activating the signaling pathway of cyclic adenosine monophosphate (cAMP)/protein kinase A (PKA)/extracellular signal-regulated kinase (ERK), possibly mediated by gonadotrophic hormones. Female ducks at 22 weeks of age were initially fed one of two Ca-deficient diets (containing 1.8% or 0.38% Ca) or a Ca-adequate control diet (containing 3.6% Ca) for 67 days (depletion period), then all birds were fed the Ca-adequate diet for an additional 67 days (repletion period). Compared with the Ca-adequate control, ducks fed 0.38% Ca during the depletion period had significantly decreased (P < 0.05) numbers of hierarchical follicles and total ovarian weight, which were accompanied by reduced egg production. Plasma concentration of FSH was decreased by the diet containing 1.8% Ca but not by that containing 0.38%. The ovarian content of cAMP was increased with the two Ca-deficient diets, and phosphorylation of PKA and ERK1/2 was increased with 0.38% dietary Ca. Transcripts of ovarian estradiol receptor 2 and luteinizing hormone receptor (LHR) were reduced in the ducks fed the two Ca-deficient diets (P < 0.05), while those of the ovarian follicle stimulating hormone receptor (FSHR) were decreased in the ducks fed 0.38% Ca. The transcript abundance of ovary gap junction proteins, A1 and A4, was reduced with the Ca-deficient diets (P < 0.05). The down-regulation of gene expression of gap junction proteins and hormone receptors, the increased cAMP content and the suppressed hierarchical follicle numbers were reversed by repletion of dietary Ca. These results indicate that dietary Ca deficiency negatively affects follicle selection of laying ducks, independent of FSH, but probably by activating cAMP/PKA/ERK1/2 signaling pathway.

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Corresponding author

E-mail: zhengcht@163.com

References

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Abe, E, Horikawa, H, Masumura, T, Sugahara, M, Kubota, M and Suda, T 1982. Disorders of cholecalciferol metabolism in old egg-laying hens. The Journal of Nutrition 112, 436446.
Ackert, CL, Gittens, JE, O’Brien, MJ, Eppig, JJ and Kidder, GM 2001. Intercellular communication via connexin 43 gap junctions is required for ovarian folliculogenesis in the mouse. Developmental Biology 233, 258270.
Bruggeman, V, Onagbesan, O, D’Hondt, E, Buys, N, Safi, M, Vanmontfort, D, Berghman, L, Vandesande, F and Decuypere, E 1999. Effects of timing and duration of feed restriction during rearing on reproductive characteristics in broiler breeder females. Poultry Science 78, 14241434.
Chen, SW, Dziuk, PJ and Francis, BM 1994. Effect of four environmental toxicants on plasma Ca and estradiol 17β and hepatic P450 in laying hens. Environmental Toxicology and Chemistry 13, 789796.
Chen, W, Zhao, F, Tian, ZM, Zhang, HX, Ruan, D, Li, Y, Wang, S, Zheng, CT and Lin, YC 2015. Dietary calcium deficiency in laying ducks impairs eggshell quality by suppressing shell biomineralization. Journal of Experimental Biology 218, 33363343.
Chen, W, Tian, ZM, Luo, X, Zhao, F, Ruan, D, Wang, SL, Wang, S, Zheng, CT, and Lin, YC 2016. Calcium deficiency suppresses follicle growth in laying ducks. In Proceedings of the 2nd International Conference on Livestock Nutrition, 21–22 July 2016, Brisbane, Australia, pp. 61.
Cheon, B, Lee, HC, Wakai, T and Fissore, RA 2013. Ca2+ influx and the store-operated Ca2+ entry pathway undergo regulation during mouse oocyte maturation. Molecular Biology of the Cell 24, 13961410.
Cho, JH, Cho, SD, Hu, HB, Kim, SH, Lee, SK, Lee, YS and Kang, KS 2002. The roles of ERK1/2 and p38MAP kinases in the preventive mechanisms of mushroom Phellinus Iinteus against in the inhibition of gap junctional intercellular communication by hydrogen peroxide. Carcinogenesis 23, 11631169.
Dupré, A, Daldello, EM, Nairn, AC, Jessus, C and Haccard, O 2014. Phosphorylation of ARPP19 by protein kinase A prevents meiosis resumption in Xenopus oocytes. Nature Communication 5, 3318.
Fernandes, G, Dasai, N, Kozlova, N, Mojadadi, A, Gall, M, Drew, E, Barratt, E, Madamidola, OA, Brown, SG, Milne, AM, Martins da Silva, SJ, Whalley, KM, Barratt, CL and Jovanović, A 2009. A spontaneous increase in intracellular Ca2+ in metaphase II human oocytes invitro can be prevented by drugs targeting ATP-sensitive K+ channels. Human Reproduction 31, 287297.
Halls, ML and Cooper, DM 2011. Regulation by Ca2+-signaling pathways of adenylyl cyclases. Cold Spring Harbor Perspectives in Biology 3, a004143.
Hojo, M, Suthanthiran, M, Helseth, G and August, P 1999. Lymphocyte intracellular free calcium concentration is increased in preeclampsia. American Journal of Obstetrics & Gynecology 180, 12091214.
Johnson, AL 2015a. Ovarian follicle selection, and granulosa cell differentiation. Poultry Science 94, 781785.
Johnson, AL 2015b. The avian ovary and follicle development: some comparative and practical insight. Turkish Journal of Veterinary and Animal Sciences 38, 660669.
Johnson, AL and Lee, J 2016. Granulosa cell responsiveness to follicle stimulating hormone during early growth of hen ovarian follicles. Poultry Science 95, 108114.
Johnson, AL and Woods, DC 2009. Dynamics of avian ovarian follicle development: cellular mechanisms of granulosa cell differentiation. General and Comparative Endocrinology 163, 1217.
Laporta, L, Micera, E, Surdo, NC, Moramarco, AM, Di Modugno, G and Zarrilli, A 2011. A functional study on L-type calcium channels in granulosa cells of small follicles in laying and forced molt hens. Animal Reproduction Science 126, 265270.
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402408.
Miao, YL and Williams, CJ 2012. Calcium signaling in mammalian egg activation and embryo development: the influence of subcellular localization. Molecular Reproduction and Development 79, 742756.
Miller, N, Biron-Shental, T, Sukenik-Halevy, R, Klement, AH, Sharony, R and Berkovitz, A 2016. Oocyte activation by calcium ionophore and congenital birth defects: a retrospective cohort study. Fertility and Sterility 106, 590596.
Mizushima, S, Takagi, S, Ono, T, Atsumi, Y, Tsukada, A, Saito, N and Shimada, K 2007. Possible role of calcium on oocyte development after intracytoplasmic sperm injection in quail (Coturnix japonica). Journal of Experimental Zoology 307, 647653.
Nunes, C, Silva, JV, Silva, V, Torgal, I and Fardilha, M 2015. Signaling pathways involved in oocyte growth, acquisition of competence and activation. Human Fertility 18, 149155.
Park, M, Choi, YJ, Kwon, DN, Park, C, Bui, HT, Gurunathan, S, Cho, SG, Song, H, Seo, HG, Min, G and Kim, JH 2013. Intraovarian transplantation of primordial follicles fails to rescue chemotherapy injured ovaries. Scientific Report 3, 1384.
Safaa, HM, Serrano, MP, Valencia, DG, Frikha, M, Jiménez-Moreno, E and Mateos, GG 2008. Productive performance and egg quality of brown egg-laying hens in the late phase of production as influenced by level and source of calcium in the diet. Poultry Science 87, 20432051.
Stanford, M 2006. Effects of UVB radiation on calcium metabolism in psittacine birds. Veterinary Record 159, 236241.
Teng, Z, Wang, C, Wang, Y, Huang, K, Xiang, X, Niu, W, Feng, L, Zhao, L, Yan, H and Zhang, H 2016. Gap junctions are essential for murine primordial follicle assembly immediately before birth. Reproduction 151, 105115.
Tilly, JL, Kowalski, KI, Johnson, AL and Hsueh, JW 1991. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129, 27992801.
Tiwari, M, Prasad, S, Shrivastav, TG and Chaube, SK 2017. Calcium signaling during meiotic cell cycle regulation and apoptosis in mammalian oocytes. Journal of Cellular Physiology 232, 976981.
Von Stetina, JR and Orr-Weaver, TL 2011. Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harbor Perspectives in Biology 3, a005553.
Wakai, T, Vanderheyden, V and Fissore, RA 2011. Ca2+ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harbor Perspectives in Biology 3, a006767.
Wojtusik, J, and Johnson, PA 2012. Vitamin D regulates Anti-Mullerian hormone expression in granulosa cells of the hen. Biology of Reproduction 86, 17.
Woods, DC and Johnson, AL 2015. Regulation of follicle-stimulating hormone-receptor messenger RNA in hen granulosa cells relative to follicle selection. Biology of Reproduction 72, 643650.
Xia, WG, Zhang, HX, Lin, YC and Zheng, CT 2015. Evaluation of dietary calcium requirements for laying Longyan shelducks. Poultry Science 94, 29322937.
Zeleznik, AJ 2004. The physiology of follicle selection. Reproductive Biology and Endocrinology 2, 31.
Zou, J, Salarian, M, Chen, YY, Veenstra, R, Louis, CF and Yang, JJ 2014. Gap junction regulation by calmodulin. FEBS Letters 588, 14301438.

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Dietary calcium deficiency suppresses follicle selection in laying ducks through mechanism involving cyclic adenosine monophosphate-mediated signaling pathway

  • W. Chen (a1) (a2) (a3) (a4) (a5), W. G. Xia (a1) (a2) (a3) (a4) (a5), D. Ruan (a1) (a2) (a3) (a4) (a5), S. Wang (a1) (a2) (a3) (a4) (a5), K. F. M. Abouelezz (a1) (a2) (a3) (a4) (a5) (a6), S. L. Wang (a1) (a2) (a3) (a4) (a5), Y. N. Zhang (a1) (a2) (a3) (a4) (a5) and C. T. Zheng (a1) (a2) (a3) (a4) (a5)...

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