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| Research Progress on Follicle Selection and Atresia Regulatory Mechanism in Chicken (Gallus gallus) |
| ZHANG Wen-Hui, NIE Rui-Xue, LING Yao, LI Jun-Ying, ZHANG Bo, ZHANG Hao* |
| College of Animal Science and Technology, China Agricultural University, Beijing 100193, China |
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Abstract The number and proportion of developmental follicles and atretic follicles in different stages of chicken ovary are related to egg production performance. A well-organized order of follicles is very important to improve egg production and maintain the continuity of egg production. In this paper, the physiological phenotypic changes during follicle selection and atresia in chickens were analyzed and the main regulatory mechanisms were summarized, and the roles of granulosa autophagy, apoptosis and inflammation in follicular atresia were discussed. The future research direction and suggestions are put forward, which has important reference value for analyzing the genetic mechanism of chicken egg laying traits.
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Received: 08 May 2023
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Corresponding Authors:
* zhanghao827@163.com
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[1] 黄璘. 2022. 内质网应激在鸡小白卵泡闭锁中的作用研究[D]. 硕士毕业论文, 广西大学, 导师: 刘兴廷. pp.23-50.
(Huang L.2022. The role of endoplasmic reticulum stress in chicken small white follicular atresia[D]. Thesis for M.S., Guangxi University, Supervisor: Liu X T, pp. 23-50.)
[2] 林欣. 2018. 蛋鸡退化卵泡衰退的机制及其功能的研究[D]. 博士毕业论文, 浙江大学, 导师: 张才乔. pp.11-15.
(Lin X.2018. Degradation and functions of the regressed ovarian follicles in the laying chickens[D]. Thesis for Ph.D., Zhejiang University, Supervisor: Zhang C Q, pp.11-15.)
[3] 张昊, 陈芳, 梁振华, 等. 2014. 家禽卵泡闭锁研究进展[J]. 湖北畜牧兽医, 35(10): 61-65.
(Zhang H, Chen F, Liang Z H, et al.2014. Research progress on poultry follicular atresia[J]. Hubei Journal of Animal and Veterinary Sciences, 35(10): 61-65.)
[4] 张颖, 李先强, 李亚娜, 等. 2022. 颗粒细胞凋亡影响家禽卵泡闭锁的研究进展[J]. 中国畜牧兽医, 49(12): 4725-4733.
(Zhang Y, Li X Q, Li Y N, et al.2022. Research progress on effects of granulosa cell apoptosis on follicle atresia in poultry[J]. China Animal Husbandry & Veterinary Medicine, 49(12): 4725-4733.)
[5] 邹坤, 路丽丽, Amponsah C A, 等. 2020. 家禽卵泡闭锁机制的研究进展[J]. 生物技术通报, 36(04): 185-191.
(Zou K, Lu L, Amponsah C A, et al.2020. Research progress on mechanism of poultry follicular atresia[J]. Biotechnology Bulletin, 36(04): 185-191.)
[6] Bianco S, Bellefleur A M, Beaulieu E, et al.2019. The ovulatory signal precipitates LRH-1 transcriptional switching mediated by differential chromatin accessibility[J]. Cell Reports, 28(9): 2443.
[7] Chen F, Jiang X, Chen X, et al.2007. Effects of downregulation of inhibin alpha gene expression on apoptosis and proliferation of goose granulosa cells[J]. Journal of Genetics and Genomics, 34(12): 1106-1113.
[8] Devesa J, Caicedo D.2019. The role of growth hormone on ovarian functioning and ovarian angiogenesis[J]. Frontiers in Endocrinology, 10: 450.
[9] Duffy D M, Ko C, Jo M, et al.2019. Ovulation: Parallels with inflammatory processes[J]. Endocrine Reviews, 40(2): 369-416.
[10] Fan Y, Zhang C S, Zhu G Y.2019. Profiling of rna n6-methyladenosine methylation during follicle selection in chicken ovary[J]. Poultry Science, 98(11): 6117-6124.
[11] Finn R N.2007. Vertebrate yolk complexes and the functional implications of phosvitins and other subdomains in vitellogenins[J]. Biology of Reproduction, 76(6): 926-935.
[12] Guzman A, Hughes C H K, Murphy B D.2021. Orphan nuclear receptors in angiogenesis and follicular development[J]. Reproduction, 162(3): R35-R54.
[13] Han S S, Wang J P, Cui C, et al.2022. Fibromodulin is involved in autophagy and apoptosis of granulosa cells affecting the follicular atresia in chicken[J]. Poultry Science, 101(1). DOI:10.1016/j.psj.2021.101524.
[14] Hlokoe V R, Tyasi T L, Gunya B.2022. Chicken ovarian follicles morphology and growth differentiation factor 9 gene expression in chicken ovarian follicles: Review[J]. Heliyon, 8(1): e08742.
[15] Hrabia A, Wolak D, Kwasniewska M, et al.2019. Expression of gelatinases (MMP-2 and MMP-9) and tissue inhibitors of metalloproteinases (TIMP-2 and TIMP-3) in the chicken ovary in relation to follicle development and atresia[J]. Theriogenology, 125: 268-276.
[16] Huang S J, Purevsuren L, Jin F, et al.2021. Effect of anti-müllerian hormone on the development and selection of ovarian follicle in hens[J]. Poultry Science, 100(3). DOI: 10.1016/j.psj.2020.12.056.
[17] Hughes C H K, Murphy B D2021. Nuclear receptors: Key regulators of somatic cell functions in the ovulatory process[J]. Molecular Aspects of Medicine, 78. DOI: 10.1016/j.mam.2020.100937.
[18] Hughes F M, Gorospe W C.1991. Biochemical-identification of apoptosis (programmed cell-death) in granulosa-cells - evidence for a potential mechanism underlying follicular atresia[J]. Endocrinology, 129(5): 2415-2422.
[19] Jing R X, Gu L T, Li J Q, et al.2018. A transcriptomic comparison of theca and granulosa cells in chicken and cattle follicles reveals ESR2 as a potential regulator of CYP19A1 expression in the theca cells of chicken follicles[J]. Comparative Biochemistry and Physiology Part D-Genomics & Proteomics, 27: 40-53.
[20] Johnson A L.2015. Reproduction in the female[M]//, Scanes C G (eds.). Sturkie's Avian Physiology, 6th Edition. Academic Press, pp. 635-665.
[21] Kania E, Pajak B, Orzechowski A.2015. Calcium homeostasis and ER stress in control of autophagy in cancer cells[J]. Biomed Research International, 2015: 352794.
[22] Kim D, Lee J, Johnson A L.2016. Vascular endothelial growth factor and angiopoietins during hen ovarian follicle development[J]. General and Comparative Endocrinology, 232: 25-31.
[23] Kumariya S, Ubba V, Jha R K, et al.2021. Autophagy in ovary and polycystic ovary syndrome: Role, dispute and future perspective[J]. Autophagy, 17(10): 2706-2732.
[24] Kuo S W, Ke F C, Chang G D, et al.2011. Potential role of follicle-stimulating hormone (FSH) and transforming growth factor (TGFBETA1) in the regulation of ovarian angiogenesis[J]. Journal of Cellular Physiology, 226(6): 1608-1619.
[25] Kurowska P, Mlyczynska E, Dawid M, et al.2021. Adipokines change the balance of proliferation/apoptosis in the ovarian cells of human and domestic animals: A comparative review[J]. Animal Reproduction Science, 228: 106737.
[26] Lemcke R A, Stephens C S, Hildebrandt K A, et al.2018. Anti-mullerian hormone type II receptor in avian follicle development[J]. Biology of Reproduction, 99(6): 1227-1234.
[27] Lesniak-Walentyn A, Hrabia A.2017. Expression and localization of matrix metalloproteinases (MMP-2,-7,-9) and their tissue inhibitors (TIMP-2,-3) in the chicken oviduct during pause in laying induced by tamoxifen[J]. Theriogenology, 88: 50-60.
[28] Li C J, Lin L T, Tsai H W, et al.2021. The molecular regulation in the pathophysiology in ovarian aging[J]. Aging and Disease, 12(3): 934-949.
[29] Li J, Leghari I H, He B, et al.2014. Estrogen stimulates expression of chicken hepatic vitellogenin II and very low-density apolipoprotein II through ER-alpha[J]. Theriogenology, 82(3): 517-524.
[30] Lillpers K, Wilhelmson M.1993. Age-dependent changes in oviposition pattern and egg-production traits in the domestic hen[J]. Poultry Science, 72(11): 2005-2011.
[31] Lin X, Liu X T, Ma Y F, et al.2018. Coherent apoptotic and autophagic activities involved in regression of chicken postovulatory follicles[J]. Aging-Us, 10(4): 819-832.
[32] Lin X, Ma Y, Qian T, et al.2019a. Basic fibroblast growth factor promotes prehierarchical follicle growth and yolk deposition in the chicken[J]. Theriogenology, 139: 90-97.
[33] Lin X, Ma Y F, Qian T F, et al.2019b. Basic fibroblast growth factor promotes prehierarchical follicle growth and yolk deposition in the chicken[J]. Theriogenology, 139: 90-97.
[34] Lipar J L, Ketterson E D, Nolan V, et al.1999. Egg yolk layers vary in the concentration of steroid hormones in two avian species[J]. General and Comparative Endocrinology, 115(2): 220-227.
[35] Liu X T, Lin X, Zhang S Y, et al.2018. Lycopene ameliorates oxidative stress in the aging chicken ovary via activation of NRF2/HO-1 pathway[J]. Aging-Us, 10(8): 2016-2036.
[36] Ma Y, Yao J, Zhou S, et al.2020. Enhancing effect of fsh on follicular development through yolk formation and deposition in the low-yield laying chickens[J]. Theriogenology, 157: 418-430.
[37] Martin N, Bernard D.2018. Calcium signaling and cellular senescence[J]. Cell Calcium, 70: 16-23.
[38] Matsuda F, Inoue N, Manabe N, et al.2012. Follicular growth and atresia in mammalian ovaries: Regulation by survival and death of granulosa cells[J]. Journal of Reproduction and Development, 58(1): 44-50.
[39] Meinsohn M C, Smith O E, Bertolin K, et al.2019. The orphan nuclear receptors steroidogenic factor-1 and liver receptor homolog-1: Structure, regulation, and essential roles in mammalian reproduction[J]. Physiological Reviews, 99(2): 1249-1279.
[40] Mihm M, Evans A C O.2008. Mechanisms for dominant follicle selection in monovulatory species: A comparison of morphological, endocrine and intraovarian events in cows, mares and women[J]. Reproduction in Domestic Animals, 43: 48-56.
[41] Ocłoń E, Hrabia A.2021. Mirna expression profile in chicken ovarian follicles throughout development and mirna-mediated MMP expression[J]. Theriogenology, 160: 116-127.
[42] Onagbesan O, Bruggeman V, Decuypere E.2009. Intra-ovarian growth factors regulating ovarian function in avian species: A review[J]. Animal Reproduction Science, 111(2-4): 121-140.
[43] Pertynska-Marczewska M, Diamanti-Kandarakis E.2017. Aging ovary and the role for advanced glycation end products[J]. Menopause-the Journal of the North American Menopause Society, 24(3): 345-351.
[44] Rizov M, Andreeva P, Dimova I.2017. Molecular regulation and role of angiogenesis in reproduction[J]. Taiwanese Journal of Obstetrics & Gynecology, 56(2): 127-132.
[45] Schneider W J.2009. Receptor-mediated mechanisms in ovarian follicle and oocyte development[J]. General and Comparative Endocrinology, 163(1-2): 18-23.
[46] Sechman A, Grzegorzewska A K, Grzesiak M, et al.2020. Nitrophenols suppress steroidogenesis in prehierarchical chicken ovarian follicles by targeting STAR, HSD3B1, and CYP19A1 and downregulating LH and estrogen receptor expression[J]. Domestic Animal Endocrinology, 70: 106378.
[47] Stephens C S, Johnson P A.2016. Bone morphogenetic protein 15 may promote follicle selection in the hen[J]. General and Comparative Endocrinology, 235: 170-176.
[48] Sun T, Xiao C, Yang Z, et al.2022a. Grade follicles transcriptional profiling analysis in different laying stages in chicken[J]. BMC Genomics, 23(1): 492.
[49] Sun X, Chen X X, Zhao J H, et al.2021a. Transcriptome comparative analysis of ovarian follicles reveals the key genes and signaling pathways implicated in hen egg production[J]. BMC Genomics, 22(1): 1-20.
[50] Sun X, Liswaniso S, Shan X S, et al.2022b. The opposite effects of VGLL1 and VGLL4 genes on granulosa cell proliferation and apoptosis of hen ovarian prehierarchical follicles[J]. Theriogenology, 181: 95-104.
[51] Sun X, Niu X T, Qin N, et al.2021b. Novel insights into the regulation of LATS2 kinase in prehierarchical follicle development via the hippo pathway in hen ovary[J]. Poultry Science, 100(12): 101454.
[52] Tyasi T L, Sun X, Shan X S, et al.2020. Effects of RAC1 on proliferation of hen ovarian prehierarchical follicle granulosa cells[J]. Animals, 10(9). DOI: 10.3390/ani10091589.
[53] Wang J, Zhao C C, Li J Q, et al.2017a. Transcriptome analysis of the potential roles of FOXL2 in chicken pre-hierarchical and pre-ovulatory granulosa cells[J]. Comparative Biochemistry and Physiology D-Genomics & Proteomics, 21: 56-66.
[54] Wang Y Y, Chen Q Y, Liu Z M, et al.2017b. Transcriptome analysis on single small yellow follicles reveals that WNT4 is involved in chicken follicle selection[J]. Frontiers in Endocrinology, 8: 317.
[55] Woods D C, Johnson A L.2005. Regulation of follicle-stimulating hormone-receptor messenger rna in hen granulosa cells relative to follicle selection[J]. Biology of Reproduction, 72(3): 643-650.
[56] Wu Y, Zhang Q, Zhang R.2017. Kaempferol targets estrogen-related receptor alpha and suppresses the angiogenesis of human retinal endothelial cells under high glucose conditions[J]. Experimental and Therapeutic Medicine, 14(6): 5576-5582.
[57] Yao J W, Ma Y F, Lin X, et al.2020a. The attenuating effect of the intraovarian bone morphogenetic protein 4 on age-related endoplasmic reticulum stress in chicken follicular cells[J]. Oxidative Medicine and Cellular Longevity, 2020: 4175613.
[58] Yao J W, Ma Y F, Zhou S, et al.2020b. Metformin prevents follicular atresia in aging laying chickens through activation of PI3K/AKT and calcium signaling pathways[J]. Oxidative Medicine and Cellular Longevity, 2020(7):1-23.
[59] Yilmaz O, Prat F, Ibanez A J, et al.2015. Estrogen-induced yolk precursors in european sea bass, dicentrarchus labrax: Status and perspectives on multiplicity and functioning of vitellogenins[J]. General and Comparative Endocrinology, 221: 16-22.
[60] Yoshino T, Suzuki T, Nagamatsu G, et al.2021. Generation of ovarian follicles from mouse pluripotent stem cells[J]. Science, 373(6552): eabe0237.
[61] Yuan S Z, Wen J Y, Cheng J, et al.2016. Age-associated up-regulation of EGR1 promotes granulosa cell apoptosis during follicle atresia in mice through the NF-B pathway[J]. Cell Cycle, 15(21): 2895-2905.
[62] Zhang C Y, Hu J W, Wang W S, et al.2020. HMGB1-induced aberrant autophagy contributes to insulin resistance in granulosa cells in pcos[J]. FASEB Journal, 34(7): 9563-9574.
[63] Zhao F, Zhao W M, Ren S W, et al.2014. Roles of SIRT1 in granulosa cell apoptosis during the process of follicular atresia in porcine ovary[J]. Animal Reproduction Science, 151(1-2): 34-41.
[64] Zheng W J, Zhang H, Gorre N, et al.2014. Two classes of ovarian primordial follicles exhibit distinct developmental dynamics and physiological functions[J]. Human Molecular Genetics, 23(4): 920-928.
[65] Zhong C H, Liu Z M, Qiao X B, et al.2021. Integrated transcriptomic analysis on small yellow follicles reveals that sosondowah ankyrin repeat domain family member a inhibits chicken follicle selection[J]. Animal Bioscience, 34(8): 1-13.
[66] Zhou J W, Peng X W, Mei S Q.2019. Autophagy in ovarian follicular development and atresia[J]. International Journal of Biological Sciences, 15(4): 726-737.
[67] Zhou S, Ma Y F, Zhao D, et al.2020. Transcriptome profiling analysis of underlying regulation of growing follicle development in the chicken[J]. Poultry Science, 99(6): 2861-2872.
[68] Zhu G Y, Kang L, Wei Q Q, et al.2014. Expression and regulation of MMP1, MMP3, and MMP9 in the chicken ovary in response to gonadotropins, sex hormones, and TGFB1[J]. Biology of Reproduction, 90(3): 57.
[69] Zhu H Y, Qin N, Xu X X, et al.2019. Synergistic inhibition of CSAL1 and CSAL3 in granulosa cell proliferation and steroidogenesis of hen ovarian prehierarchical development[J]. Biology of Reproduction, 101(5): 986-1000. |
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