CYP19A1调控内源性雌激素合成促进牦牛COCs细胞自噬和早期发育能力

doi:10.11843/j.issn.0366-6964.2022.12.014

Abstract

Abstract: The aim of this study was to investigate the effects of cytochrome P450arom (CYP19A1) on the secretion of endogenous 17β-estradiol (E₂), and its effects on autophagy of oocyte and subsequent embryonic development were also evaluated. During the in vitro culture of the yak cumulus-oocyte complexes (COCs), saline, E₂ (10^-7 mol·L^-1), aflatoxin B1 (AFB1) and bisphenol A (BPA) were respectively supplemented to M199 at same volume. The expression and location of CYP19A1 in COCs from different groups were detected by qRT-PCR, Western blot and immunofluorescence, as well as the autophagy related genes 5(ATG5), Bcl-2 homologous domain protein (BECLIN1) and microtubule associated protein light chain 3 (LC3). The levels of endogenous E₂ in mature medium of COCs from the groups treated with saline, AFB1 and BPA were measured by enzyme-linked immunosorbent assay (ELISA). Rates of mature oocyte, cleavage embryo and blastocyst were calculated and compared among different groups. The results showed that both gene and protein levels of CYP19A1 were enhanced significantly in the AFB1 group, along with the increase of the endogenous secretion of E₂, ATG, BECLIN1 and LC3 levels in mature COCs (P<0.05). The level of CYP19A1 were reduced significantly in the E₂ group, while the expression of autophagy related factors in mature COCs were enhanced (P<0.05). In BPA treatment group, the CYP19A1 and endogenous E₂ were significantly reduced (P<0.05), which leading to the lower expressions of ATG5, BECLIN1 and LC3 (P<0.05). Comparing to the control group, the rates of mature oocyte and cleavage embryo were enhanced by E₂ and AFB1 (P<0.05), but reduced in BPA group (P<0.05). There was no significant difference about blastocyst rates among 4 groups (P>0.05). It can be concluded that endogenous E₂ was positive regulated by CYP19A1 during COCs maturation, furthermore both endogenous and exogenous E₂ can induce autophagy and improved the early developmental capacities of yak oocyte. The results provide a theoretical basis for further exploring the molecular mechanism of reproductive hormones regulating the maturation of oocytes in mammalian.

Key words: E₂, autophagy, cytochrome P450, oocyte maturation, embryo development

CLC Number:

S823.85

WANG Libin, WANG Meng, SUN Ying, CHEN Rui, ZHANG Tiantian, HUANG Zhenhua, ZHANG Qian, YU Sijiu, PAN Yangyang. CYP19A1 Promotes Autophagy and Early Developmental Ability of Yak Oocytes by Regulating the Levels of Endogenous Estradiol[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(12): 4283-4295.

References 41

[1]	MAKSURA H,AKON N,ISLAM N,et al.Effects of estradiol on in vitro maturation of buffalo and goat oocytes[J].Reprod Med Biol,2021,20(1):62-70.
[2]	CONCANNON P,TSUTSUI T,SHILLE V.Embryo development,hormonal requirements and maternal responses during canine pregnancy[J].J Reprod Fertil Suppl,2001,57:169-179.
[3]	ABDOON A S S,KANDIL O M,OTOI T,et al.Influence of oocyte quality,culture media and gonadotropins on cleavage rate and development of in vitro fertilized buffalo embryos[J].Anim Reprod Sci,2001,65(3-4):215-223.
[4]	PAWSHE C H,PALANISAMY A,TANEJA M,et al.Comparison of various maturation treatments on in vitro maturation of goat oocytes and their early embryonic development and cell numbers[J].Theriogenology,1996,46(6):971-982.
[5]	GAVALI S,GUPTA M K,DASWANI B,et al.Estrogen enhances human osteoblast survival and function via promotion of autophagy[J].Biochim Biophys Acta (BBA)-Mol Cell Res,2019,1866(9):1498-1507.
[6]	MENG Q H,LI Y,JI T T,et al.Estrogen prevent atherosclerosis by attenuating endothelial cell pyroptosis via activation of estrogen receptor α-mediated autophagy[J].J Adv Res,2021,28:149-164.
[7]	XIANG J,LIU X,REN J,et al.How does estrogen work on autophagy?[J].Autophagy,2019,15(2):197-211.
[8]	XIE Z P,KLIONSKY D J.Autophagosome formation:core machinery and adaptations[J].Nat Cell Biol,2007,9(10):1102-1109.
[9]	ZHOU J L,YAO W,LI C Y,et al.Administration of follicle-stimulating hormone induces autophagy via upregulation of HIF-1α in mouse granulosa cells[J].Cell Death Dis,2017,8(8):e3001.
[10]	DUAN J X,CHEN H L,XU D J,et al.17β-estradiol improves the developmental ability,inhibits reactive oxygen species levels and apoptosis of porcine oocytes by regulating autophagy events[J].J Steroid Biochem Mol Biol,2021,209:105826.
[11]	许涛,潘阳阳,何翃闳,等.TNF-α对牦牛卵母细胞HIF-1α和HSP70的表达及后续胚胎发育能力的影响[J].畜牧兽医学报, 2019,50(6):1198-1207.XU T,PAN Y Y,HE H H,et al.The effects of tumor necrosis factor-α(TNF-α) on the expression of HIF-1α and HSP70 in yak oocytes and the subsequent embryo development[J].Acta Veterinaria et Zootechnica Sinica,2019,50(6):1198-1207.(in Chinese)
[12]	JIN K,ZUO Q S,SONG J Z,et al.CYP19A1 (aromatase) dominates female gonadal differentiation in chicken (Gallus gallus) embryos sexual differentiation[J].Biosci Rep,2020,40(10):BSR20201576.
[13]	CHAURASIYA V,KUMARI S,ONTERU S K,et al.miR-326 down-regulate CYP19A1 expression and estradiol-17b production in buffalo granulosa cells through CREB and C/EBP-β[J].J Steroid Biochem Mol Biol,2020,199:105608.
[14]	GUAN H Y,XIA H X,CHEN X Y,et al.Toll-like receptor 4 inhibits estradiol secretion via NF-κB signaling in human granulosa cells[J].Front Endocrinol,2021,12:629554.
[15]	ANCELIN M L,NORTON J,CANONICO M,et al.Aromatase (CYP19A1) gene variants,sex steroid levels,and late-life depression[J].Depress Anxiety,2020,37(2):146-155.
[16]	BAUMGARTEN S C,CONVISSAR S M,ZAMAH A M,et al.FSH regulates IGF-2 expression in human granulosa cells in an AKT-dependent manner[J].J Clin Endocrinol Metab,2015,100(8):E1046-E1055.
[17]	PAN Y Y,WANG M,WANG L B,et al.Estrogen improves the development of yak (Bos grunniens) oocytes by targeting cumulus expansion and levels of oocyte-secreted factors during in vitro maturation[J].PLoS One,2020,15(9):e0239151.
[18]	STORVIK M,HUUSKONEN P,KYLLÖNEN T,et al.Aflatoxin B1-a potential endocrine disruptor-up-regulates CYP19A1 in JEG-3 cells[J].Toxicol Lett,2011,202(3):161-167.
[19]	XU H F,ZHANG X L,YE Y Z,et al.Bisphenol A affects estradiol metabolism by targeting CYP1A1 and CYP19A1 in human placental JEG-3 cells[J].Toxicol In Vitro,2019,61:104615.
[20]	THELLIN O,ELMOUALIJ B,HEINEN E,et al.A decade of improvements in quantification of gene expression and internal standard selection[J].Biotechnol Adv,2009,27(4):323-333.
[21]	田志龙,刘秋月,王翔宇,等.CYP11A1、CYP17A1、CYP19A1基因在小尾寒羊下丘脑-垂体-卵巢轴的表达[J].中国农业大学学报, 2019,24(4):87-93.TIAN Z L,LIU Q Y,WANG X Y,et al.Expression of CYP11A1,CYP17A1 and CYP19A1 genes in hypothalamus-pituitary-ovary axis of small tail han sheep[J].Journal of China Agricultural University,2019,24(4):87-93.(in Chinese)
[22]	KHATRI R,KULICK N,REMENTER R J B,et al.Pregnancy-related hormones increase nifedipine metabolism in human hepatocytes by inducing CYP3A4 Expression[J].J Pharm Sci,2021,110(1):412-421.
[23]	李艳敏,李翠翠,郑航,等.雌激素通过ER-α调控CYP2C8在鸡肝中的表达[J].畜牧兽医学报,2016,47(12):2362-2369.LI Y M,LI C C,ZHENG H,et al.Expression of CYP2C8 is regulated by estrogen through ER-α in liver of chicken[J].Acta Veterinaria et Zootechnica Sinica,2016,47(12):2362-2369.(in Chinese)
[24]	KHAWAR M B,LIU C,GAO F Y,et al.Sirt1 regulates testosterone biosynthesis in Leydig cells via modulating autophagy[J].Protein Cell,2021,12(1):67-75.
[25]	HADDAD M,EID S,HARB F,et al.Activation of 20-HETE synthase triggers oxidative injury and peripheral nerve damage in type 2 diabetic mice[J].J Pain,2022,23(8):1371-1388.
[26]	XU D,SUN F L,BI J,et al.Effects of E2 binding enzyme UBC9 on porcine oocyte maturation,apoptosis and embryo development[J].Reprod Domest Anim,2020,55(11):1526-1534.
[27]	TAKETSURU H,HIRAO Y,TAKENOUCHI N,et al.Effect of androstenedione on the growth and meiotic competence of bovine oocytes from early antral follicles[J].Zygote,2012,20(4):407-415.
[28]	HILKER R E,PAN B,ZHAN X S,et al.MicroRNA-21 enhances estradiol production by inhibiting WT1 expression in granulosa cells[J].J Mol Endocrinol,2021,68(1):11-22.
[29]	HE H H,ZHANG H Z,PAN Y Y,et al.Low oxygen concentration improves yak oocyte maturation and inhibits apoptosis through HIF-1 and VEGF[J].Reprod Domest Anim,2022,57(4):381-392.
[30]	LUO H J,LIU M R,LUO S J,et al.Dynamic monitoring of GPER-mediated estrogenic effects in breast cancer associated fibroblasts:an alternative role of estrogen in mammary carcinoma development[J].Steroids,2016,112:1-11.
[31]	DUAN J X,CHEN H L,LI Y,et al.17β-estradiol enhances porcine meiosis resumption from autophagy-induced gap junction intercellular communications and connexin 43 phosphorylation via the MEK/ERK signaling pathway[J].J Agric Food Chem, 2021,69(40):11847-11855.
[32]	SHEN H H,ZHANG T,YANG H L,et al.Ovarian hormones-autophagy-immunity axis in menstruation and endometriosis[J]. Theranostics,2021,11(7):3512-3526.
[33]	CHEN Y B,WANG J,XU D H,et al.m6A mRNA methylation regulates testosterone synthesis through modulating autophagy in Leydig cells[J].Autophagy,2021,17(2):457-475.
[34]	MIZUSHIMA N,YOSHIMORI T.How to interpret LC3 immunoblotting[J].Autophagy,2007,3(6):542-545.
[35]	SHAO T,KE H N,LIU R,et al.Autophagy regulates differentiation of ovarian granulosa cells through degradation of WT1[J].Autophagy,2022,18(8):1864-1878.
[36]	ZHANG X,ZHAO S,YUAN Q Q,et al.TXNIP,a novel key factor to cause Schwann cell dysfunction in diabetic peripheral neuropathy,under the regulation of PI3K/Akt pathway inhibition-induced DNMT1 and DNMT3a overexpression[J].Cell Death Dis,2021,12(7):642.
[37]	LUO Z,XU X,SHO T,et al.ROS-induced autophagy regulates porcine trophectoderm cell apoptosis,proliferation,and differentiation[J].Am J Physiol Cell Physiol,2019,316(2):C198-C209.
[38]	OLMO R,CABRERA J,DÍAZ-MANZANO F E,et al.Root-knot nematodes induce gall formation by recruiting developmental pathways of post-embryonic organogenesis and regeneration to promote transient pluripotency[J].New Phytol,2020, 227(1): 200-215.
[39]	VIGNEAULT C,MCGRAW S,MASSICOTTE L,et al.Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition[J].Biol Reprod,2004,70(6):1701-1709.
[40]	PRAKASH B S,SARKAR M,MONDAL M.An update on reproduction in yak and mithun[J].Reprod Domest Anim,2008, 43(S2):217-223.
[41]	ZI X D.Reproduction in female yaks (Bos grunniens) and opportunities for improvement[J].Theriogenology, 2003, 59(5-6): 1303-1312.

CYP19A1 Promotes Autophagy and Early Developmental Ability of Yak Oocytes by Regulating the Levels of Endogenous Estradiol

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 41

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	LIU Yueyang, LI Mengyuan, NIE Xueyi, MA Yabo, HOU Yuxin, MA Boli, YANG Yi, XU Jinrui. The Regulation of Calcium-binding Protein S100A4 on Autophagy in THP-1 Cells Infected with Bacillus Calmette-Guérin [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(1): 311-322.
[2]	WANG Chongnian, YU Jialin, GONG Zhaoqian, WU Xiaoling, DENG Guangcun. Regulation of BCG-induced Autophagy in Macrophages RAW264.7 by PLIN2 [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 2134-2146.
[3]	WANG Han, MENG Lijie, LIU Wenjiao, XU Yongjian, GONG Ting. Effect of TAS1R3 Gene Interference on Autophagy Related Factors in Leydig Cells of Xiang Pig [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(4): 1525-1534.
[4]	ZHANG Chengcheng, SUN Jiahao, WANG Xiuling, ZHANG Xiaorong, WU Yantao. Beclin1 Interacts with the Nonstructural Protein NS5A of CSFV and Promotes Virus Proliferation [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(2): 715-725.
[5]	MA Tianwen, YU Yue, LÜ Liangyu, JIA Lina, RUAN Hongri, WANG Haoran, WANG Xinyu, ZHANG Yuxin, ZHANG Jiantao, GAO Li. Effects of Bilobalide on Autophagy, Proliferation and Apoptosis of IL-1β-induced ATDC5 Chondrocytes [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(2): 837-846.
[6]	MENG Meijuan, WANG Yan, HUO Ran, LI Xuerui, CHANG Guangjun, SHEN Xiangzhen. Effect of Inhibition of PERK on LPS Induced Autophagy in Bovine Mammary Epithelial Cells [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(1): 351-360.
[7]	WEN Shuangquan, WANG Li, ZHANG Wenhua, XU Mingchang, ZOU Hui, GU Jianhong, LIU Xuezhong, BIAN Jianchun, LIU Zongping, YUAN Yan. Effects of Fas on Autophagosomes Formation Induced by Cadmium Exposure in Rat Cerebral Cortex [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(5): 1608-1614.
[8]	CAO Qianying, ZHENG Hao, WANG Yaling, ZOU Hui, GU Jianhong, YUAN Yan, LIU Xuezhong, LIU Zongping, BIAN Jianchun. Mechanism of Autophagy Block in PC12 Cells Induced by Zearalenone [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(4): 1270-1279.
[9]	YIN Yanling, HUANG Shuang, YAO Qian, WU Jiangping, GUO Haochen, YANG Xin, SONG Junke, ZHAO Guanghui. The Mechanisms of Circular RNA ciRS-7 Affecting the Propagation of Cryptosporidium parvum in HCT-8 Cells via Targeting miR-219a-5p [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 3989-3999.
[10]	CHEN Qi, DU Changzheng, ZHENG Xuedi, MA Boli, XU Jinrui, YANG Yi. Regulation on BCG-induced Autophagy by Wnt5a-mediated Wnt/Ca²⁺ Pathway in BAECs [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(11): 4071-4080.
[11]	JIA Yanyan, ZHAO Yingying, YU Zuhua, HE Lei, LIAO Chengshui, LI Jing, YU Chuan, ZHANG Chunjie, LI Yinju. Construction and Influence of Beclin-1 Gene shRNA Lentiviral Vector on Autophagy and Virability of B16F10 Cell [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(9): 2609-2616.
[12]	LUO Jia, XU Jinrui, LI Wu, WANG Yujiong. The Effect of BCG-induced RAW264.7 Cells Fatty Acid Oxidation on Autophagy and Pro-inflammatory Cytokines Expression [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(9): 2617-2625.
[13]	ZHANG Jinhua, GAO Mingxing, LIU Zelin, GU Changqin. Effects of Autophagy Regulators on Apoptosis in the Brain of Mice Infected with Japanese Encephalitis Virus [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(2): 506-514.
[14]	LI Yangguang, WU Ying, WANG Mingshu, CHENG Anchun. Research Progress of Herpes Virus ICP22 Protein [J]. Acta Veterinaria et Zootechnica Sinica, 2021, 52(1): 9-18.
[15]	YU Jialin, XU Yanan, HAN Lu, MA Qinmei, WU Xiaoling, DENG Guangcun. Role of Fatty Acid Binding Protein 4 in Regulating Macrophage Autophagy Induced by BCG Infection [J]. Acta Veterinaria et Zootechnica Sinica, 2020, 51(9): 2265-2274.