Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (15): 3050-3061.doi: 10.3864/j.issn.0578-1752.2022.15.015

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

CTNNB1 Regulates the Function of Porcine Ovarian Granulosa Cells

LI LiYing(),HE YingTing,ZHONG YuYi,ZHOU XiaoFeng,ZHANG Hao,YUAN XiaoLong,LI JiaQi,CHEN ZanMou()   

  1. College of Animal Science, South China Agricultural University/Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding/National Engineering Technology Research Center for Breeding Swine Industry, Guangzhou 510642
  • Received:2021-03-08 Accepted:2022-06-25 Online:2022-08-01 Published:2022-08-02
  • Contact: ZanMou CHEN E-mail:leeleeying@163.com;zmchen@scau.edu.cn

Abstract:

【Objective】The ovarian granulosa cells proliferation and differentiation are important to the initiation of primordial follicle growth. The excessive of ovarian granulosa cells apoptosis is one of the main reasons for follicular atresia. Therefore, the functions of ovarian granulosa cells are very important for follicular growth, development, ovulation, hormone secretion and so on. The objective of this study was to investigate the effects of CTNNB1 on the function of granulosa cells proliferation, apoptosis and steroid hormone secretion during porcine follicle development, so as to provide a reference for the molecular regulation mechanism of porcine follicular development. 【Method】In this study, the expressions of CTNNB1 in porcine ovary, muscle, brain and other 9 tissues were detected by RNA extraction and qRT-PCR. Then, qRT-PCR and Western blot were used to explore the expression of CTNNB1 in different stages of porcine ovarian tissue, as well as granulosa cells of small (≤3 mm), medium (3-6 mm) and large (≥6 mm) follicles. The eukaryotic expression vector and siRNA of CTNNB1 were constructed and transfected into porcine ovarian granulosa cells. The effects of CTNNB1 on the proliferation, apoptosis and steroid hormone secretion of granulosa cells were detected by EdU, annexin V-FITC/PI double staining assay, flow cytometry, and ELISA. Finally, qRT-PCR was also applied to explore the effect of CTNNB1 on the expression of genes related to steroid hormone synthesis. 【Result】The expression of CTNNB1 mRNA in ovary was higher than that in other tissues. The expression of CTNNB1 mRNA in ovaries of in-sexually-mature sows was significantly higher than that of pre-sexually-mature and post-sexually-mature sows. The expression of CTNNB1 in the follicles was gradually increased with the development of follicles, and the expression of CTNNB1 in granulosa cells of follicles was also increased with the development of follicles. In addition, the expression of CTNNB1 in granulosa cells as well as medium and large follicles was extremely higher than that in small follicles. CTNNB1 could promote the proliferation of granulosa cells and inhibit the apoptosis of granulosa cells. Moreover, CTNNB1 could also up-regulate the transcription level of CYP1A1 and HSD17B7, and down-regulate the transcription level of CYP11A1, ESR1, ESR2, FSHR, LHR and NR5A1, which were related to steroid hormone synthesis, thereby promoting the secretion of estrogen and suppressing the secretion of androgen and progesterone in granulosa cells. 【Conclusion】The above results confirmed that CTNNB1 regulated the function of granulosa cells by stimulating its proliferation and secretion of estrogen, and restraining its apoptosis and secretion of androgen and progesterone, thereby promoting the growth and development of follicles.

Key words: porcine, ovary, follicles, granulosa cells, CTNNB1

Table 1

PCR Primers"

引物名称Name 引物序列Sequence (5′→3′) 产物长度Length (bp)
CTNNB1 F: GGGGTACCATGGCTACCCAAGCTGATTTG
R: CGCTCGAGTTACAGGTCAGTATCAAACCAGGC
2346
CTNNB1-RT
F: GCTGTTCGCCTTCACTAC
R: CTGATGAGCACGAACCAG
186
GAPDH-RT
F: TCGGAGTGAACGGATTTG
R: TCACCCCATTTGATGTTGG
250
STARD1-RT
F: GCTTTTCCACTCTAGGGCGA
R: AAGCTCCTGGCTGGATGAAC
184
CYP1A1-RT
F: TATCCTCCGTTACCTGCCCA
R: TGCGCCCCTTCTCAAAGATT
119
CYP11A1-RT
F: CGCTCAGTCCTGGTCAAAGG
R: TTCCAAGTTGCCGAGCTTCT
267
CYP17A1-RT
F: AAGCCAAGACGAACGCAGAAAG
R: TAGATGGGGCACGATTGAAACC
228
CYP19A1-RT
F: TTCCTTGGCTGTACAGAAAGTATGA
R: GGTGTCTGGTGCTGCAATTAG
221
HSD3B1-RT F: ATCGTCCACTTGTTGCTGGA
R: TGCTCTGGAGCTTAGAAAATTCC
103
HSD17B1-RT
F: GGGAGGCCTGATAGGTGAGT
R: GGGCGGTAACTCACTGGAC
271
HSD17B7-RT
F: TGGACTTCACCTGTGCTTGG
R: TGCTGACATCCACTTGCACA
116
ESR1-RT
F: ATGGCCATGGAATCTGCCAA
R: CCCCTTTCATCATGCCCACT
241
ESR2-RT
F: GCCGACAAGGAACTGGTACA
R: GAGCAAAGATGAGCTTGCCG
169
FSHR-RT
F: CGCGGTTGAACTGAGGTTTG
R: TTGGGAAGGTTCTGGAAGGC
222
LHR-RT
F: ACATAACCACCGTACCAGCA
R: GGAAGGCGTCATTGTGCATC
177
NR5A1-RT F: CTGCTGGAGTGAGCTGCATGT
R: ACTTGAGGCAGACGAACTCCT
218

Fig. 1

Tissue expression profile of CTNNB1"

Fig. 2

The expression of CTNNB1 in ovary A: The expression of CTNNB1 mRNA in porcine ovaries of different stages. B, C: The expression of CTNNB1 in small, medium and large follicles. D, E: The expression of CTNNB1 in granulosa cells of small, medium and large follicles"

Fig. 3

The detection of CTNNB1 expression efficiency in granulosa cells A, B: The overexpression efficiency of CTNNB1. C, D: The interference efficiency of CTNNB1"

Fig. 4

The effect of CTNNB1 on the proliferation of granulosa cells"

Fig. 5

The effect of CTNNB1 on apoptosis of granulosa cells"

Fig. 6

The effect of CTNNB1 on steroid hormone secretion of granulosa cells A: The secretion of steroid hormone in granulosa cells after overexpressing CTNNB1. B: The secretion of steroid hormone in granulosa cells after interfering with CTNNB1. C: The effect of CTNNB1 on mRNA expression of genes involved in steroid hormone synthesis"

[1] KUMAR T R, WANG Y, LU N F, MATZUK M M. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics, 1997, 15(2): 201-204. doi: 10.1038/ng0297-201.
doi: 10.1038/ng0297-201
[2] MATSUDA F, INOUE N, MANABE N, OHKURA S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. The Journal of Reproduction and Development, 2012, 58(1): 44-50. doi: 10.1262/jrd.2011-012.
doi: 10.1262/jrd.2011-012
[3] HUNTER M G. Oocyte maturation and ovum quality in pigs. Reviews of Reproduction, 2000, 5(2): 122-130. doi: 10.1530/ror.0.0050122.
doi: 10.1530/ror.0.0050122
[4] MCGEE E A, HSUEH A J W. Initial and cyclic recruitment of ovarian follicles. Endocrine Reviews, 2000, 21(2): 200-214. doi: 10.1210/edrv.21.2.0394.
doi: 10.1210/edrv.21.2.0394
[5] SIMPSON E R, CLYNE C, RUBIN G, BOON W C, ROBERTSON K, BRITT K, SPEED C, JONES M. Aromatase-A brief overview. Annual Review of Physiology, 2002, 64: 93-127. doi: 10.1146/annurev.physiol.64.081601.142703.
doi: 10.1146/annurev.physiol.64.081601.142703
[6] TIWARI M, PRASAD S, TRIPATHI A, PANDEY A N, ALI I, SINGH A K, SHRIVASTAV T G, CHAUBE S K. Apoptosis in mammalian oocytes: A review. Apoptosis: an International Journal on Programmed Cell Death, 2015, 20(8): 1019-1025. doi: 10.1007/s10495-015-1136-y.
doi: 10.1007/s10495-015-1136-y
[7] 黄向月, 熊显荣, 韩杰, 杨显英, 王艳, 王斌, 李键. KDM1A在牦牛卵泡发育过程中的表达. 中国农业科学, 2019, 52(24): 4624-4631. doi: 10.3864/j.issn.0578-1752.2019.24.016.
doi: 10.3864/j.issn.0578-1752.2019.24.016
HUANG X Y, XIONG X R, HAN J, YANG X Y, WANG Y, WANG B, LI J. Expression pattern of KDM1A in the development of yak follicles. Scientia Agricultura Sinica, 2019, 52(24): 4624-4631. doi: 10.3864/j.issn.0578-1752.2019.24.016. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2019.24.016
[8] 张静, 张姬越, 岳永起, 赵丹, 范依琳, 马妍, 熊燕, 熊显荣, 字向东, 李键, 杨丽雪. LKB1基因对卵巢颗粒细胞类固醇激素生成相关基因的调控作用. 中国农业科学, 2022, 55(10): 2057-2066.
ZHANG J, ZHANG J Y, YUE Y Q, ZHAO D, FAN Y L, MA Y, XIONG Y, XIONG X R, ZI X D, LI J, YANG L X. LKB1 regulates steroids synthesis related genes expression in bovine granulosa cells. Scientia Agricultura Sinica, 2022, 55(10): 2057-2066. (in Chinese)
[9] 卢锦, 朱艳. 卵泡发育及其调节因素的研究进展. 医学综述, 2008, 14(4): 507-509. doi: 10.3969/j.issn.1006-2084.2008.04.012.
doi: 10.3969/j.issn.1006-2084.2008.04.012
LU J, ZHU Y. The progress of follicular development and its regulatory factors. Medical Recapitulate, 2008, 14(4): 507-509. doi: 10.3969/j.issn.1006-2084.2008.04.012. (in Chinese)
doi: 10.3969/j.issn.1006-2084.2008.04.012
[10] 苏宁, 张清学. 卵泡体外培养的研究进展. 国外医学(计划生育、生殖健康分册), 2006, 25(1): 24-27. doi: 10.3969/j.issn.1674-1889.2006.01.008.
doi: 10.3969/j.issn.1674-1889.2006.01.008
SU N, ZHANG Q X. Research progress of follicle culture in vitro. Journal of International Reproductive Health/Family Planning, 2006, 25(1): 24-27. doi: 10.3969/j.issn.1674-1889.2006.01.008. (in Chinese)
doi: 10.3969/j.issn.1674-1889.2006.01.008
[11] 袁晓华, 张莉莉, 盛喜霞, 杨春荣, 王亚琴. PGRMC1介导孕酮抑制卵泡发育的作用及机制研究. 海南医学, 2019, 30(1): 1-5. doi: 10.3969/j.issn.1003-6350.2019.01.001.
doi: 10.3969/j.issn.1003-6350.2019.01.001
YUAN X H, ZHANG L L, SHENG X X, YANG C R, WANG Y Q. Role of PGRMC1 in the process of progesterone inhibiting follicle development and the related mechanism. Journal of Hainan Medical University, 2019, 30(1): 1-5. doi: 10.3969/j.issn.1003-6350.2019.01.001. (in Chinese)
doi: 10.3969/j.issn.1003-6350.2019.01.001
[12] 张晓娜, 杨镒峰, 常彤, 许保增. 雌激素、雄激素在卵泡发育中的作用及应用. 特产研究, 2017, 39(3): 50-54. doi: 10.16720/j.cnki.tcyj.2017.03.011.
doi: 10.16720/j.cnki.tcyj.2017.03.011
ZHANG X N, YANG Y F, CHANG T, XU B Z. The role of estrogen and/or androgen in the follicle development and its application. Special Wild Economic Animal and Plant Research, 2017, 39(3): 50-54. doi: 10.16720/j.cnki.tcyj.2017.03.011. (in Chinese)
doi: 10.16720/j.cnki.tcyj.2017.03.011
[13] BERNDT J D, MOON R T. Cell biology. Making a point with Wnt signals. Science, 2013, 339(6126): 1388-1389. doi: 10.1126/science.1236641.
doi: 10.1126/science.1236641
[14] NUSSE R. Wnt signaling in disease and in development. Cell Research, 2005, 15(1): 28-32. doi: 10.1038/sj.cr.7290260.
doi: 10.1038/sj.cr.7290260
[15] LIU J Q, XIAO Q, XIAO J N, NIU C X, LI Y Y, ZHANG X J, ZHOU Z W, SHU G, YIN G. Wnt/β-catenin signalling: Function, biological mechanisms, and therapeutic opportunities. Signal Transduction and Targeted Therapy, 2022, 7(2):23.
doi: 10.1038/s41392-022-00879-2
[16] FAN H Y, O'CONNOR A, SHITANAKA M, SHIMADA M, LIU Z L, RICHARDS J S. Β-catenin (CTNNB1) promotes preovulatory follicular development but represses LH-mediated ovulation and luteinization. Molecular Endocrinology, 2010, 24(8): 1529-1542. doi: 10.1210/me.2010-0141.
doi: 10.1210/me.2010-0141
[17] JEPPESEN J V, KRISTENSEN S G, NIELSEN M E, HUMAIDAN P, DAL CANTO M, FADINI R, SCHMIDT K T, ERNST E, YDING ANDERSEN C. LH-receptor gene expression in human granulosa and cumulus cells from antral and preovulatory follicles. The Journal of Clinical Endocrinology and Metabolism, 2012, 97(8): E1524-E1531. doi: 10.1210/jc.2012-1427.
doi: 10.1210/jc.2012-1427
[18] SANCHEZ A M, GIORGIONE V, VIGANÒ P, PAPALEO E, CANDIANI M, MANGILI G, PANINA-BORDIGNON P. Treatment with anticancer agents induces dysregulation of specific Wnt signaling pathways in human ovarian luteinized granulosa cells in vitro. Toxicological Sciences, 2013, 136(1): 183-192. doi: 10.1093/toxsci/kft175.
doi: 10.1093/toxsci/kft175
[19] CASTAÑON B I, STAPP A D, GIFFORD C A, SPICER L J, HALLFORD D M, GIFFORD J A H. Follicle-stimulating hormone regulation of estradiol production: Possible involvement of WNT2 and β-catenin in bovine granulosa cells. Journal of Animal Science, 2012, 90(11): 3789-3797. doi: 10.2527/jas.2011-4696.
doi: 10.2527/jas.2011-4696
[20] PARAKH T N, HERNANDEZ J A, GRAMMER J C, WECK J, HUNZICKER-DUNN M, ZELEZNIK A J, NILSON J H. Follicle- stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33): 12435-12440. doi: 10.1073/pnas.0603006103.
doi: 10.1073/pnas.0603006103
[21] HERNANDEZ G J A. The role of WNT signaling in adult ovarian folliculogenesis. Reproduction (Cambridge, England), 2015, 150(4): R137-R148. doi: 10.1530/REP-14-0685.
doi: 10.1530/REP-14-0685
[22] 杨有福, 耿果霞, 陈华丽, 程建勇, 李青旺. Wortmannin抑制Wnt/β-Catenin通路对猪卵巢颗粒细胞发育的影响. 家畜生态学报, 2019, 40(9): 19-25. doi: 10.3969/j.issn.1673-1182.2019.09.004.
doi: 10.3969/j.issn.1673-1182.2019.09.004
YANG Y F, GENG G X, CHEN H L, CHENG J Y, LI Q W. Effect of inhibition of Wnt/β-catenin signaling by wortmannin on development of porcine granulosa cells. Acta Ecologae Animalis Domastici, 2019, 40(9): 19-25. doi: 10.3969/j.issn.1673-1182.2019.09.004. (in Chinese)
doi: 10.3969/j.issn.1673-1182.2019.09.004
[23] 张嘉美, 赵宁, 吴晓玲, 邓光存. Wnt/β-catenin信号通路对细胞凋亡和坏死的调控研究进展. 中国细胞生物学学报, 2015, 37(9): 1309-1316.
ZHANG J M, ZHAO N, WU X L, DENG G C. Progress in regulative role of Wnt/β-catenin signaling pathway in apoptosis and necrosis. Chinese Journal of Cell Biology, 2015, 37(9): 1309-1316. (in Chinese)
[24] 高萍, 钟玉宜, 张爱玲. 母猪卵巢颗粒细胞的分离培养及鉴定. 广东农业科学, 2014, 41(4): 131-135, 237. doi: 10.16768/j.issn.1004-874x.2014.04.038.
doi: 10.16768/j.issn.1004-874x.2014.04.038
GAO P, ZHONG Y Y, ZHANG A L. Separation, culture and identification of sow ovarian granulose cells. Guangdong Agricultural Sciences, 2014, 41(4): 131-135, 237. doi: 10.16768/j.issn.1004-874x.2014.04.038. (in Chinese)
doi: 10.16768/j.issn.1004-874x.2014.04.038
[25] 朱丽, 郭成志, 邓思君, 鲁银, 魏强, 袁慧. 猪卵巢颗粒细胞分离培养及鉴定. 中国兽医杂志, 2011, 47(4): 21-22, 98.
ZHU L, GUO C Z, DENG S J, LU Y, WEI Q, YUAN H. Isolation, culture and identification of porcine ovary granulosa cells. Chinese Journal of Veterinary Medicine, 2011, 47(4): 21-22, 98. (in Chinese)
[26] CRAIG J, ORISAKA M, WANG H M, ORISAKA S, THOMPSON W, ZHU C, KOTSUJI F, TSANG B K. Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Frontiers in Bioscience, 2007, 12: 3628-3639. doi: 10.2741/2339.
doi: 10.2741/2339
[27] 王莉. β-catenin在猪卵巢组织中的表达以及对猪卵巢颗粒细胞凋亡及类固醇生成酶的影响[D]. 南京: 南京农业大学, 2010.
WANG L. Expression of β-catenin in pig’s ovary and the effect of β-catenin on porcine granulosa cells apotosis and steroidogenesis related enzyme[D]. Nanjing: Nanjing Agricultural University, 2010. (in Chinese)
[28] 刘忠华, 马所峰, 岳奎忠, 刘海兰, 陈清轩, 谭景和. 发情周期不同时期猪卵泡颗粒细胞凋亡的观察. 动物学报, 2002, 48(6): 759-763. doi: 10.3969/j.issn.1674-5507.2002.06.008.
doi: 10.3969/j.issn.1674-5507.2002.06.008
LIU Z H, MA S F, YUE K Z, LIU H L, CHEN Q X, TAN J H. Granulosa cell apoptosis during the porcine estrous cycle. Acta Laboratorium Animalis Scientia Sinica, 2002, 48(6): 759-763. doi: 10.3969/j.issn.1674-5507.2002.06.008. (in Chinese)
doi: 10.3969/j.issn.1674-5507.2002.06.008
[29] ZHANG J B, LIU Y, YAO W, LI Q F, LIU H L, PAN Z X. Initiation of follicular atresia: gene networks during early atresia in pig ovaries. Reproduction (Cambridge, England), 2018, 156(1): 23-33. doi: 10.1530/REP-18-0058.
doi: 10.1530/REP-18-0058
[30] 马梦楠, 王慧明, 王苗苗, 姚望, 张金璧, 潘增祥. 猪卵泡闭锁过程中circINHBB的鉴定及其对颗粒细胞凋亡的影响. 中国农业科学, 2021, 54(18): 3998-4007. doi: 10.3864/j.issn.0578-1752.2021.18.017.
doi: 10.3864/j.issn.0578-1752.2021.18.017
MA M N, WANG H M, WANG M M, YAO W, ZHANG J B, PAN Z X. Identification of circINHBB during follicular atresia and its effect on granulosa cell apoptosis. Scientia Agricultura Sinica, 2021, 54(18): 3998-4007. doi: 10.3864/j.issn.0578-1752.2021.18.017. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2021.18.017
[31] BOERBOOM D, WHITE L D, DALLE S, COURTY J, RICHARDS J S. Dominant-stable beta-catenin expression causes cell fate alterations and Wnt signaling antagonist expression in a murine granulosa cell tumor model. Cancer Research, 2006, 66(4): 1964-1973. doi: 10.1158/0008-5472.CAN-05-3493.
doi: 10.1158/0008-5472.CAN-05-3493
[32] TETSU O, MCCORMICK F. Β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 1999, 398(6726): 422-426. doi: 10.1038/18884.
doi: 10.1038/18884
[33] HE T C, SPARKS A B, RAGO C, HERMEKING H, ZAWEL L, DA COSTA L T, MORIN P J, VOGELSTEIN B, KINZLER K W. Identification of c-MYC as a target of the APC pathway. Science, 1998, 281(5382): 1509-1512. doi: 10.1126/science.281.5382.1509.
doi: 10.1126/science.281.5382.1509
[34] HERNANDEZ A G, BAHR J M. Role of FSH and epidermal growth factor (EGF) in the initiation of steroidogenesis in granulosa cells associated with follicular selection in chicken ovaries. Reproduction (Cambridge, England), 2003, 125(5): 683-691.
doi: 10.1530/rep.0.1250683
[35] PARAKH T N, HERNANDEZ J A, GRAMMER J C, WECK J, HUNZICKER-DUNN M, ZELEZNIK A J, NILSON J H. Follicle- stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(33): 12435-12440.doi: 10.1073/pnas.0603006103.
doi: 10.1073/pnas.0603006103
[36] 张金璧, 姚望, 潘增祥, 刘红林. FSH处理对猪颗粒细胞中类固醇合成酶基因的表达及其调控区组蛋白H3修饰的影响. 中国农业科学, 2018, 51(18): 3582-3590. doi: 10.3864/j.issn.0578-1752.2018.18.014.
doi: 10.3864/j.issn.0578-1752.2018.18.014
ZHANG J B, YAO W, PAN Z X, LIU H L. Effects of FSH treatment on steroidogenic enzymes expression and histone H3 modification in pig granulosa cells. Scientia Agricultura Sinica, 2018, 51(18): 3582-3590. doi: 10.3864/j.issn.0578-1752.2018.18.014. (in Chinese)
doi: 10.3864/j.issn.0578-1752.2018.18.014
[37] HERNANDEZ GIFFORD J A, HUNZICKER-DUNN M E, NILSON J H. Conditional deletion of beta-catenin mediated by Amhr2cre in mice causes female infertility. Biology of Reproduction, 2009, 80(6): 1282-1292. doi: 10.1095/biolreprod.108.072280.
doi: 10.1095/biolreprod.108.072280
[38] 李轶, 梁晓燕, 庄广伦. 雄激素对卵泡发育影响的双重性. 生殖医学杂志, 2008, 17(6): 423-424. doi: 10.3969/j.issn.1004-3845.2008.06.011.
doi: 10.3969/j.issn.1004-3845.2008.06.011
LI Y, LIANG X Y, ZHUANG G L. The dualism effect of androgen on follicular development. Journal of Reproductive Medicine, 2008, 17(6): 423-424. doi: 10.3969/j.issn.1004-3845.2008.06.011. (in Chinese)
doi: 10.3969/j.issn.1004-3845.2008.06.011
[39] 张金璧. 类固醇激素合成酶及相关受体表达与猪卵泡闭锁过程的关系研究[D]. 南京: 南京农业大学, 2010.
ZHANG J B. Relationship between changes of steroidogenesis enzymes and related hormone reseptors gene expression and follicular atresia of swine[D]. Nanjing: Nanjing Agricultural University, 2010. (in Chinese)
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