Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T01:05:30.211Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  05 May 2020

W. Chen ,
W. G. Xia ,
D. Ruan ,
S. Wang ,
K. F. M. Abouelezz ,
S. L. Wang ,
Y. N. Zhang  and
C. T. Zheng
W. Chen
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
W. G. Xia
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
D. Ruan
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
S. Wang
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
K. F. M. Abouelezz
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Department of Poultry Production, Faculty of Agriculture, Assiut University, AssiutCP 71526, Egypt
S. L. Wang
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
Y. N. Zhang
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
C. T. Zheng*
Affiliation:
Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou510640, China State Key Laboratory of Livestock and Poultry Breeding, Guangzhou510640, China Key Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangzhou510640, China Guangdong Public Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China Guangdong Key Laboratory of Animal Breeding and Nutrition, Guangzhou510640, China
*
†E-mail: [email protected]
Get access

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.

Keywords

hierarchical folliclesgonadotrophic hormonesgranulosa cellprotein kinase Aextracellular signal-regulated kinase
Type
Research Article
Information
animal , Volume 14 , Issue 10 , October 2020 , pp. 2100 - 2108
Copyright
© The Animal Consortium 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 436–446.10.1093/jn/112.3.436CrossRefGoogle ScholarPubMed
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, 258–270.10.1006/dbio.2001.0216CrossRefGoogle ScholarPubMed
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, 1424–1434.10.1093/ps/78.10.1424CrossRefGoogle ScholarPubMed
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, 789–796.10.1002/etc.5620130514CrossRefGoogle Scholar
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, 3336–3343.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 1396–1410.CrossRefGoogle ScholarPubMed
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, 1163–1169.10.1093/carcin/23.7.1163CrossRefGoogle Scholar
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, 3318.10.1038/ncomms4318CrossRefGoogle ScholarPubMed
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, 287–297.Google Scholar
Halls, ML and Cooper, DM 2011. Regulation by Ca2+-signaling pathways of adenylyl cyclases. Cold Spring Harbor Perspectives in Biology 3, a004143.10.1101/cshperspect.a004143CrossRefGoogle ScholarPubMed
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, 1209–1214.10.1016/S0002-9378(99)70618-6CrossRefGoogle ScholarPubMed
Johnson, AL 2015a. Ovarian follicle selection, and granulosa cell differentiation. Poultry Science 94, 781–785.10.3382/ps/peu008CrossRefGoogle ScholarPubMed
Johnson, AL 2015b. The avian ovary and follicle development: some comparative and practical insight. Turkish Journal of Veterinary and Animal Sciences 38, 660–669.10.3906/vet-1405-6CrossRefGoogle Scholar
Johnson, AL and Lee, J 2016. Granulosa cell responsiveness to follicle stimulating hormone during early growth of hen ovarian follicles. Poultry Science 95, 108–114.10.3382/ps/pev318CrossRefGoogle ScholarPubMed
Johnson, AL and Woods, DC 2009. Dynamics of avian ovarian follicle development: cellular mechanisms of granulosa cell differentiation. General and Comparative Endocrinology 163, 12–17.CrossRefGoogle ScholarPubMed
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, 265–270.10.1016/j.anireprosci.2011.06.007CrossRefGoogle Scholar
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, 402–408.10.1006/meth.2001.1262CrossRefGoogle Scholar
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, 742–756.10.1002/mrd.22078CrossRefGoogle ScholarPubMed
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, 590–596.CrossRefGoogle ScholarPubMed
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, 647–653.10.1002/jez.a.418CrossRefGoogle Scholar
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, 149–155.10.3109/14647273.2015.1006692CrossRefGoogle ScholarPubMed
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, 1384.10.1038/srep01384CrossRefGoogle ScholarPubMed
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, 2043–2051.10.3382/ps.2008-00110CrossRefGoogle ScholarPubMed
Stanford, M 2006. Effects of UVB radiation on calcium metabolism in psittacine birds. Veterinary Record 159, 236–241.10.1136/vr.159.8.236CrossRefGoogle ScholarPubMed
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, 105–115.10.1530/REP-15-0282CrossRefGoogle ScholarPubMed
Tilly, JL, Kowalski, KI, Johnson, AL and Hsueh, JW 1991. Involvement of apoptosis in ovarian follicular atresia and postovulatory regression. Endocrinology 129, 2799–2801.10.1210/endo-129-5-2799CrossRefGoogle ScholarPubMed
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, 976–981.10.1002/jcp.25670CrossRefGoogle ScholarPubMed
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, a005553.10.1101/cshperspect.a005553CrossRefGoogle ScholarPubMed
Wakai, T, Vanderheyden, V and Fissore, RA 2011. Ca2+ signaling during mammalian fertilization: requirements, players, and adaptations. Cold Spring Harbor Perspectives in Biology 3, a006767.10.1101/cshperspect.a006767CrossRefGoogle ScholarPubMed
Wojtusik, J, and Johnson, PA 2012. Vitamin D regulates Anti-Mullerian hormone expression in granulosa cells of the hen. Biology of Reproduction 86, 1–7.10.1095/biolreprod.111.094110CrossRefGoogle ScholarPubMed
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, 643–650.10.1095/biolreprod.104.033902CrossRefGoogle Scholar
Xia, WG, Zhang, HX, Lin, YC and Zheng, CT 2015. Evaluation of dietary calcium requirements for laying Longyan shelducks. Poultry Science 94, 2932–2937.10.3382/ps/pev281CrossRefGoogle ScholarPubMed
Zeleznik, AJ 2004. The physiology of follicle selection. Reproductive Biology and Endocrinology 2, 31.10.1186/1477-7827-2-31CrossRefGoogle ScholarPubMed
Zou, J, Salarian, M, Chen, YY, Veenstra, R, Louis, CF and Yang, JJ 2014. Gap junction regulation by calmodulin. FEBS Letters 588, 1430–1438.10.1016/j.febslet.2014.01.003CrossRefGoogle ScholarPubMed
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material

Download Chen et al. supplementary material(File)
File 26.2 KB