细胞自噬对动物卵泡发育调控的研究进展

doi:10.16431/j.cnki.1671-7236.2022.11.024

Abstract

Abstract: The follicle is fundamental for female mammals to exert their reproductive capacity, and its development is a dynamic process that mainly involves the formation of primordial follicles, the recruitment of follicles, the selection of dominant follicles, the ovulation of mature follicles and the luteinization of follicles after ovulation.Follicle development is regulated by complex physiological activities, such as the endocrine system, autophagy, apoptosis, and so on.Aautophagy is an evolutionarily conserved stress-responsive process that forms autophagosomes by enveloping intracellular materials and delivering them to lysosomes for degradation to help cells maintain the intracellular material metabolic balance, which plays an important role in the process of follicle development, on the one hand it can alleviate the follicle damage caused by stress by degrading or recycling damaged proteins or harmful metabolites; On the other hand, it can cause follicular atresia by generating a large number of autophagosomes for excessive degradation of organelles.The regulation of follicular development by autophagy requires the involvement of multiple canonical signaling pathways, such as PI3K-Akt-mTOR, MAPK-ULK1, ERK1/2 and Sirt1-FOXO1-Atg7, which have been shown to regulate the physiological activity of follicle cells by promoting or inhibiting autophagy through independent actions or interactions under the stimulation of stresses, such as hormones, oxidative stress, and cell starvation.Different levels of autophagy are currently known to have different effects on the survival of follicle cells, but there are still relatively few studies on the level of autophagy that determines whether a cell can survive.In addition, studies on the regulation of follicular development by autophagy have focused on granulosa cells, while the role of oocyte maturation and follicular membrane cells has been less well reported.In this review, the authors briefly describe the role of autophagy in the formation of ovarian reserve, the development of growing follicles, the formation and regression of corpus luteum and follicular atresia.In addition, the effects of autophagy induced by chemicals and stress on follicular development are analyzed, which will provide a comprehensive understanding of the regulation of autophagy in follicular development.

Key words: autophagy; ovary; follicular development; granulosa cells

CLC Number:

S814.8

DONG Shucan, HOU Biwei, ZOU Xian, LI Yaokun, LIU Dewu, SUN Baoli, GUO Yongqing, DENG Ming, LIU Guangbin. Research Progress on Regulation of Follicle Development by Autophagy in Animals[J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(11): 4335-4345.

References

[1] BHARDWAJ J K, PALIWAL A, SARAF P, et al.Role of autophagy in follicular development and maintenance of primordial follicular pool in the ovary[J].Journal of Cellular Physiology, 2022, 237(2):1157-1170.
[2] SKINNER M K.Regulation of primordial follicle assembly and development[J].Human Reproduction Update, 2005, 11(5):461-471.
[3] CHOI J Y, JO M W, LEE E Y, et al.The role of autophagy in follicular development and atresia in rat granulosa cells[J].Fertility and Sterility, 2010, 93(8):2532-2537.
[4] REN W, SHO S, NAOKO K, et al.Activation of autophagy in early neonatal mice increases primordial follicle number and improves lifelong fertility[J].Biology of Reproduction, 2020, 102(2):399-411.
[5] SCHAEFER L, DIKIC I.Autophagy:Instructions from the extracellular matrix[J].Matrix Biology, 2021, 100-101:1-8.
[6] KITADA M, KOYA D.Autophagy in metabolic disease and ageing[J].Nature Reviews Endocrinology, 2021, 17(11):647-661.
[7] COLLIER J J, SUOMI F, OLAHOVA M, et al.Emerging roles of Atg7 in human health and disease[J].EMBO Molecular Medicine, 2021, 13(12):e14824.
[8] SONG Z H, YU H Y, WANG P, et al.Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice[J].Cell Death & Disease, 2015, 6:e1589.
[9] PENG Y, GUO L, GU A, et al.Electroacupuncture alleviates polycystic ovary syndrome-like symptoms through improving insulin resistance, mitochondrial dysfunction, and endoplasmic reticulum stress via enhancing autophagy in rats[J].Molecular Medicine, 2020, 26(1):73.
[10] ZHANG C, HU J, WANG W, et al.HMGB1-induced aberrant autophagy contributes to insulin resistance in granulosa cells in PCOS[J].FASEB Journal, 2020, 34(7):9563-9574.
[11] FORTUNE J E.The early stages of follicular development:Activation of primordial follicles and growth of preantral follicles[J].Animal Reproduction Science, 2003, 78(3-4):135-163.
[12] BJORVANG R D, HASSAN J, STEFOPOULOU M, et al.Persistent organic pollutants and the size of ovarian reserve in reproductive-aged women[J].Environment International, 2021, 155:106589.
[13] DE FELICI M, SCALDAFERRI M L, LOBASCIO M, et al.Experimental approaches to the study of primordial germ cell lineage and proliferation[J].Human Reproduction Update, 2004, 10(3):197-206.
[14] EDSON M A, NAGARAJA A K, MATZUK M M.The mammalian ovary from genesis to revelation[J].Endocrine Reviews, 2009, 30(6):624-712.
[15] MAY-PANLOUP P, BOUCRET L, CHAO DE LA BARCA J M, et al.Ovarian ageing:The role of mitochondria in oocytes and follicles[J].Human Reproduction Update, 2016, 22(6):725-743.
[16] BAERWALD A R, ADAMS G P, PIERSON R A.Ovarian antral folliculogenesis during the human menstrual cycle:A review[J]. Human Reproduction Update, 2012, 18(1):73-91.
[17] ZHANG H, LIU K.Cellular and molecular regulation of the activation of mammalian primordial follicles:Somatic cells initiate follicle activation in adulthood[J]. Human Reproduction Update, 2015, 21(6):779-786.
[18] KUMARIYA S, UBBA V, JHA R K, et al.Autophagy in ovary and polycystic ovary syndrome:Role, dispute and future perspective[J].Autophagy, 2021, 17(10):2706-2733.
[19] LEVY J M M, TOWERS C G, THORBURN A.Targeting autophagy in cancer[J].Nature Reviews Cancer, 2017, 17(9):528-542.
[20] ALLEN E A, BAEHRECKE E H.Autophagy in animal development[J].Cell Death & Differentiation, 2020, 27(3):903-918.
[21] MIZUSHIMA N, KOMATSU M.Autophagy:Renovation of cells and tissues[J].Cell, 2011, 147(4):728-741.
[22] MATSUZAWA-ISHIMOTO Y, HWANG S, CADWELL K.Autophagy and Inflammation[J].Annual Review of Immunology, 2018, 36:73-101.
[23] HUANG T, WAN X, ALVAREZ A A, et al.MIR93(microRNA-93) regulates tumorigenicity and therapy response of glioblastoma by targeting autophagy[J].Autophagy, 2019, 15(6):1100-1111.
[24] YIN N, WU C, QIU J, et al.Protective properties of heme oxygenase-1 expressed in umbilical cord mesenchymal stem cells help restore the ovarian function of premature ovarian failure mice through activating the JNK/Bcl-2 signal pathway-regulated autophagy and upregulating the circulating of CD8⁺CD28^- T cells[J].Stem Cell Research & Therapy, 2020, 11(1):49.
[25] IZADI M, ALI T A, POURKARIMI E.Over fifty years of life, death, and cannibalism:A historical recollection of apoptosis and autophagy[J].International Journal of Molecular Sciences, 2021, 22(22):12466.
[26] WU H, LIU C, YANG Q, et al.miR145-3p promotes autophagy and enhances bortezomib sensitivity in multiple myeloma by targeting HDAC4[J].Autophagy, 2020, 16(4):683-697.
[27] DIKIC I, ELAZAR Z.Mechanism and medical implications of mammalian autophagy[J].Nature Reviews Molecular Cell Biology, 2018, 19(6):349-364.
[28] TWU W I, LEE J Y, KIM H, et al.Contribution of autophagy machinery factors to HCV and SARS-CoV-2 replication organelle formation[J].Cell Reports, 2021, 37(8):110049.
[29] XIA X, WANG X, QIN W, et al.Emerging regulatory mechanisms and functions of autophagy in fish[J].Aquaculture, 2019, 511:13242.
[30] STRONG L M, CHANG C M, RILEY J F, et al.Structural basis for membrane recruitment of ATG16L1 by WIPI2 in autophagy[J].eLife, 2021, 10:e70372.
[31] KORKMAZ G, LE SAGE C, TEKIRDAG K A, et al.miR-376b controls starvation and mTOR inhibition-related autophagy by targeting ATG4C and BECN1[J].Autophagy, 2012, 8(2):165-176.
[32] ZHANG X, WU W K, XU W, et al.C-X-C motif chemokine 10 impairs autophagy and autolysosome formation in non-alcoholic steatohepatitis[J].Theranostics, 2017, 7(11):2822-2836.
[33] LEOPARDO N P, VELAZQUEZ M E, CORTASA S, et al.A dual death/survival role of autophagy in the adult ovary of Lagostomus maximus (Mammalia- Rodentia)[J].PLoS One, 2020, 15(5):e0232819.
[34] CHAUBE S K, PRASAD P V, THAKUR S C, et al.Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro[J].Apoptosis, 2005, 10(4):863-874.
[35] TRIPATHI A, PREMKUMAR K V, PANDEY A N, et al.Melatonin protects against clomiphene citrate-induced generation of hydrogen peroxide and morphological apoptotic changes in rat eggs[J].European Journal of Pharmacology, 2011, 667(1-3):419-424.
[36] TRIPATHI A, SHRIVASTAV T G, CHAUBE S K.An increase of granulosa cell apoptosis mediates aqueous neem (Azadirachta indica) leaf extract-induced oocyte apoptosis in rat[J].Journal of International Medical Research, 2013, 3(1):27-36.
[37] RODRIGUES P, LIMBACK D, MCGINNIS L, et al.Germ-somatic cell interactions are involved inestablishing the follicle reserve in mammals[J].Frontiers in Cell and Developmental Biology, 2021, 9:674137.
[38] TOOTHAKER J M, ROOSA K, VOSS A, et al.Oocyte survival and development during follicle formation and folliculogenesis in mice lacking aromatase[J].Endocring Research, 2022, 47(2):45-55.
[39] PEPLING M E.Follicular assembly:Mechanisms of action[J].Reproduction, 2012, 143(2):139-149.
[40] GAWRILUK T R, HALE A N, FLAWS J A, et al.Autophagy is a cell survival program for female germ cells in the murine ovary[J].Reproduction, 2011, 141(6):759-765.
[41] TU Z H, MU X Y, LI Q Y, et al.Autophagy participates in cyst breakdown and primordial folliculogenesis by reducing reactive oxygen species levels in perinatal mouse ovaries[J].Journal of Cellular Physiology, 2019, 234(5):6125-6135.
[42] SUN X, KLINGER F G, LIU J, et al.miR-378-3p maintains the size of mouse primordial follicle pool by regulating cell autophagy and apoptosis[J].Cell Death & Disease, 2020, 11(9):737.
[43] SUN Y C, WANG Y Y, SUN X F, et al.The role of autophagy during murine primordial follicle assembly[J].Aging, 2018, 10(2):197-211.
[44] NAGAMATSU G.Regulation of primordial follicle formation, dormancy, and activation in mice[J].The Journal of Reproduction and Development, 2021, 67(3):189-195.
[45] SILVA J R V, LIMA F E O, SOUZA A L P, et al.Interleukin-1beta and TNF-alpha systems in ovarian follicles and their roles during follicular development, oocyte maturation and ovulation[J].Zygote, 2020, 28(4):270-277.
[46] YEUNG C K, WANG G, YAO Y, et al.BRE modulates granulosa cell death to affect ovarian follicle development and atresia in the mouse[J].Cell Death & Disease, 2017, 8(3):e2697.
[47] LIN M, HUA R, MA J, et al.Bisphenol A promotes autophagy in ovarian granulosa cells by inducing AMPK/mTOR/ULK1 signalling pathway[J].Environment International, 2021, 147:106298.
[48] CHOI J, JO M, LEE E, et al.Akt is involved in granulosa cell autophagy regulation via mTOR signaling during rat follicular development and atresia[J].Reproduction, 2014, 147(1):73-80.
[49] YUAN J, ZHANG Y, SHENG Y, et al.MYBL2 guides autophagy suppressor VDAC2 in the developing ovary to inhibit autophagy through a complex of VDAC2-BECN1-BCL2L1 in mammals[J].Autophagy, 2015, 11(7):1081-1098.
[50] FURLONG H C, STAMPFLI M R, GANNON A M, et al.Cigarette smoke exposure triggers the autophagic cascade via activation of the AMPK pathway in mice[J].Biology of Reproduction, 2015, 93(4):93.
[51] SONG B S, KIM J S, KIM Y H, et al.Induction of autophagy during in vitro maturation improves the nuclear and cytoplasmic maturation of porcine oocytes[J].Reproduction, Fertility, and Development, 2014, 26(7):974-981.
[52] LEE S E, KIM E Y, CHOI H Y, et al.Rapamycin rescues the poor developmental capacity of aged porcine oocytes[J].Asian-Australasian Journal of Animal Sciences, 2014, 27(5):635-647.
[53] SERKE H, VILSER C, NOWICKI M, et al.Granulosa cell subtypes respond by autophagy or cell death to oxLDL-dependent activation of the oxidized lipoprotein receptor 1 and Toll-like 4 receptor[J].Autophagy, 2009, 5(7):991-1003.
[54] ZHOU J, PENG X, MEI S.Autophagy in ovarian follicular development and atresia[J].International Journal of Biological Sciences, 2019, 15(4):726-737.
[55] PARK Y, PARK Y B, LIM S W, et al.Time series ovarian transcriptome analyses of the porcine estrous cycle reveals gene expression changes during steroid metabolism and corpus luteum development[J].Animals (Basel), 2022, 12(3):376-390.
[56] BAO H, SUN Y, YANG N, et al.Uterine Notch2 facilitates pregnancy recognition and corpus luteum maintenance via upregulating decidual Prl8a2[J].PLoS Genetics, 2021, 17(8):e1009786.
[57] TANG Z, ZHANG Z, LIN Q, et al.HIF-1alpha/BNIP3-mediated autophagy contributes to the luteinization of granulosa cells during the formation of corpus luteum[J].Frontiers in Cell and Developmental Biology, 2020, 8:619924.
[58] GAWRILUK T R, KO C, HONG X, et al.Beclin-1 deficiency in the murine ovary results in the reduction of progesterone production to promote preterm labor[J].Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(40):E4194-E4203.
[59] GAWRILUK T R, RUCKER E B.BECN1, corpus luteum function, and preterm labor[J].Autophagy, 2015, 11(1):183-184.
[60] TANG Z, ZHANG Z, ZHANG H, et al.Autophagy attenuation hampers progesterone synthesis during the development of pregnant corpus luteum[J].Cells, 2019, 9(1):71-88.
[61] MANSOUR A, MANABU K, AHMED Z B, et al.Status of autophagy, lysosome activity and apoptosis during corpus luteum regression in cattle[J].Journal of Reproduction and Development, 2015, 61(3):229-236.
[62] PRZYGRODZKA E, MONACO C F, PLEWES M R, et al.Protein kinase a and 5'-AMP-activated protein kinase signaling pathways exert opposite effects on induction of autophagy in luteal cells[J].Frontiers in Cell and Developmental Biology, 2021, 9:723563.
[63] TANG Z, CHEN J, ZHANG Z, et al.HIF-1alpha activation promotes luteolysis by enhancing ROS levels in the corpus luteum of pseudopregnant rats[J].Oxidative Medicine and Cellular Longevity, 2021, 2021:1764929.
[64] GRZESIAK M, MICHALIK A, RAK A, et al.The expression of autophagy-related proteins within the corpus luteum lifespan in pigs[J].Domestic Animal Endocrinology, 2018, 64:9-16.
[65] HULAS-STASIAK M, GAWRON A.Follicular atresia in the prepubertal spiny mouse (Acomys cahirinus) ovary[J].Apoptosis, 2011, 16(10):967-975.
[66] ZHENG Y, MA L, LIU N, et al.Autophagy and apoptosis of porcine ovarian granulosa cells during follicular development[J].Animals (Basel), 2019, 9(12):1111.
[67] YADAV P K, TIWARI M, GUPTA A, et al.Germ cell depletion from mammalian ovary:Possible involvement of apoptosis and autophagy[J].Journal of Biomedical Science, 2018, 25(1):36.
[68] SHEN M, JIANG Y, GUAN Z, et al.FSH protects mouse granulosa cells from oxidative damage by repressing mitophagy[J].Scientific Reports, 2016, 6:38090.
[69] SHEN M, JIANG Y, GUAN Z, et al.Protective mechanism of FSH against oxidative damage in mouse ovarian granulosa cells by repressing autophagy[J].Autophagy, 2017, 13(8):1364-1385.
[70] SHEN M, CAO Y, JIANG Y, et al.Melatonin protects mouse granulosa cells against oxidative damage by inhibiting FOXO1-mediated autophagy:Implication of an antioxidation-independent mechanism[J].Redox Biology, 2018, 18:138-157.
[71] ZHANG J Q, REN Q L, CHEN J F, et al.Autophagy contributes to oxidative stress-induced apoptosis in porcine granulosa cells[J].Reproductive Sciences, 2021, 28(8):2147-2160.
[72] HE M, ZHANG T, ZHU Z, et al.LSD1 contributes to programmed oocyte death by regulating the transcription of autophagy adaptor SQSTM1/p62[J].Aging Cell, 2020, 19(3):e13102.
[73] GE W, LI L, DYCE P W, et al.Establishment and depletion of the ovarian reserve:Physiology and impact of environmental chemicals[J].Cellular and Molecular Life Sciences, 2019, 76(9):1729-1746.
[74] KONSTANTINIDOU F, STUPPIA L, GATTA V.Looking inside the world of granulosa cells:The noxious effects of cigarette smoke[J].Biomedicines, 2020, 8(9):309.
[75] YUAN X, TIAN G G, PEI X, et al.Spermidine induces cytoprotective autophagy of female germline stem cells in vitro and ameliorates aging caused by oxidative stress through upregulated sequestosome-1/p62 expression[J].Cell And Bioscience, 2021, 11(1):107.
[76] WANG W, LUO S M, MA J Y, et al.Cytotoxicity and DNA damage caused from diazinon exposure by inhibiting the PI3K-Akt pathway in porcine ovarian granulosa cells[J].Journal of Agricultural and Food Chemistry, 2019, 67(1):19-31.
[77] HE J, YAO G, HE Q, et al.Theaflavin 3, 3'-digallate delays ovarian aging by improving oocyte quality and regulating granulosa cell function[J].Oxidative Medicine and Cellular Longevity, 2021, 2021:7064179.
[78] OMMATI M M, SHI X, LI H, et al.The mechanisms of arsenic-induced ovotoxicity, ultrastructural alterations, and autophagic related paths:An enduring developmental study in folliculogenesis of mice[J].Ecotoxicology and Environmental Safety, 2020, 204:110973.
[79] CAO X Y, LIU J, ZHANG Y J, et al.Exposure of adult mice to perfluorobutanesulfonate impacts ovarian functions through hypothyroxinemia leading to down-regulation of Akt-mTOR signaling[J].Chemosphere, 2020, 244:125497.
[80] GAO J G, YANG J K, ZHU L, et al.Acrylamide impairs the developmental potential of germinal vesicle oocytes by inducing mitochondrial dysfunction and autophagy/apoptosis in mice[J].Human & Experimental Toxicology, 2021, 40(12 Suppl):S370-S380.
[81] CUI J, LI Y, ZHANG W, et al.Alginic acid induces oxidative stress-mediated hormone secretion disorder, apoptosis and autophagy in mouse granulosa cells and ovaries[J].Toxicology, 2022, 467:153099.
[82] WANG J L, RUAN W L, HUANG B S, et al.Tri-ortho-cresyl phosphate induces autophagy of mouse ovarian granulosa cells[J].Reproduction, 2019, 158(1):61-69.
[83] DUAN X, DAI X X, WANG T, et al.Melamine negatively affects oocyte architecture, oocyte development and fertility in mice[J].Human Reproduction, 2015, 30(7):1643-1652.
[84] TANG Z G, ZHANG Z H, TANG Y D, et al.Effects of dimethyl carbonate-induced autophagic activation on follicular development in the mouse ovary[J].Experimental and Therapeutic Medicine, 2017, 14(6):5981-5989.
[85] CHEN Z, ZUO X, LI H, et al.Effects of melatonin on maturation, histone acetylation, autophagy of porcine oocytes and subsequent embryonic development[J].Animal Science Journal, 2017, 88(9):1298-1310.
[86] HALE B J, HAGER C L, SEIBERT J T, et al.Heat stress induces autophagy in pig ovaries during follicular development[J].Biology of Reproduction, 2017, 97(3):426-437.
[87] YADAV A K, YADAV P K, CHAUDHARY G R, et al.Autophagy in hypoxic ovary[J].Cellular and Molecular Life Sciences, 2019, 76(17):3311-3322.
[88] HOU Y C, CHITTARANJAN S, BARBOSA S G, et al.Effector caspase Dcp-1 and IAP protein bruce regulate starvation-induced autophagy during drosophila melanogaster oogenesis[J]. Journal of Cell Biology, 2008, 182(6):1127-1139.
[89] GALLUZZI L, GREEN D R.Autophagy-independent functions of the autophagy machinery[J].Cell, 2019, 177(7):1682-1699.

Research Progress on Regulation of Follicle Development by Autophagy in Animals

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	XU Yuanyuan, ZHENG Haiying, YANG Chunyan, DENG Tingxian, HUANG Chenqian, FENG Chao, LU Xingrong, DUAN Anqin, MO Xia, MA Xiaoya, SHANG Jianghua. Effects of Inhibition of BMP/Smad Signaling Pathway on the Growth and Steroid Hormone Synthesis of Buffalo Ovarian Granulosa Cells [J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(6): 2354-2362.
[2]	XIAO Peng, SHANG Jianghua, YANG Chunyan, LI Mengqi, DUAN Anqin, MA Xiaoya, FENG Chao, HUANG Chenqian, ZHANG Bo, ZHOU Jinchen, WEI Kelong, ZHENG Wei, ZHENG Haiying. Effects of Alpha-linolenic Acid on Buffalo Ovarian Granulosa Cells Cultured in vitro [J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(6): 2380-2387.
[3]	PIAN Huifang, DU Xubin, LI Yan, ZHANG Yuchen, LIU Fei, YU Debing. Sequencing Analysis of the Full-length Transcriptome of Granulosa Cells of Small Yellow Follicle in Hy-Line Variety Brown [J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(5): 1754-1763.
[4]	CHENG Qian, GAO Qingqing, WANG Yuhe, HUAN Changchao, GAO Song. Effects of Avian Pathogenic Escherichia coli Outer Membrane Protein OmpA on Autophagy of DF-1 Cells [J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(5): 1971-1980.
[5]	WEI Chunyan, GUO Jia, ZHU Dexin, ZHANG Wei, ZHU Jiale, DEN Xingmei, JIA Sifeng, LIU Liangbo, ZHANG Hui. Construction of Deletion Strain of Brucella BPE159 Gene and Effect of BPE159 Protein on Expression of Cellular Autophagy Factors [J]. China Animal Husbandry and Veterinary Medicine, 2023, 50(1): 26-36.
[6]	YU Kai, ZHAO Yufen, WENG Yu, WANG Qin, HAO Shaoyu, YU Boyang, DU Chenguang, SUBUDENG Gerile, LI Haijun. Effects of Dihydrotestosterone on Proliferation and Expression of Anti-Müllerian Hormone of Mouse Granulosa Cells [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(8): 3036-3043.
[7]	BAI Shaocheng, ZHOU Juan, JIN Rongshuai, WANG Fan, LU Tingting, TANG Xianwei, ZHAO Bohao, WU Xinsheng, CHEN Yang. Cloning and Bioinformatics Analysis of CYP11A1 Gene in New Zealand White Rabbits and Its Effects on Reproduction-related Genes [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(7): 2484-2496.
[8]	HU Wen, HUO Konglin, SONG Xingxing, ZHANG Xin, ZHANG Duoni, LUO Rongrong, XU Wenhao, LI Xun. Effects of Gonadotropin Inhibitory Hormone on Gonadal Reproductive Function and Glucose Metabolism in SD Rats [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(6): 2239-2249.
[9]	WANG Zihang, DENG Xingmei, QIU Runhui, ZHU Dexin, LI Jia, TAO Tingting, ZHU Jiale, SUN Zhihua, ZHANG Hui. Regulation of Long Noncoding RNAs in Autophagy Induced by PEDV Infected Vero-E6 Cells [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(5): 1942-1950.
[10]	SHI Yuzhu, LUO Rutang, CHEN Chao, WU Xu, LI Ang. Cloning, Bioinformatics and Tissue Expression Analysis of GDF9 Genes in Muscovy Duck [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(3): 817-829.
[11]	WANG Yueli, SHAO Zhiran, YI Jihai, WANG Yong, WANG Zhen, CHEN Chuangfu. miR-145a-3p Regulates Brucella Induced Mouse Macrophage RAW264.7 Autophagy by Targeting ATG14 [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(3): 1117-1125.
[12]	ZHANG Peiying, SONG Pengyan, ZHOU Ying, CHEN Xiaoyong, ZHOU Rongyan. Analysis of Differentially Expressed Genes in Glucose-induced Senescence of Sheep Follicular Granulosa Cells Based on RNA-Seq Data [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(2): 631-640.
[13]	ZHAO Xiaoyu, WU Yingping, LI Haiying, YAO Yingying, LI Jiahui, YAO Yang, LU Qingqing. Construction of Ovarian Transcriptional Profiles and Analysis of Follicle Development-Related Genes in Yili Geese at Various Stages Before and After Egg Laying [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(12): 4674-4687.
[14]	ZHANG Ying, LI Xianqiang, LI Yana, WANG Jiaxiang, WU Yan, PI Jinsong, CHEN Lin. Research Progress on Effects of Granulosa Cell Apoptosis on Follicle Atresia in Poultry [J]. China Animal Husbandry and Veterinary Medicine, 2022, 49(12): 4725-4733.
[15]	LU Huan, NIU Xi, HUANG Yali, LI Sheng, RAN Xueqin, HUANG Shihui, WANG Jiafu. Screening of Candidate miRNA for Regulating Xiang Pig Reproduction [J]. China Animal Husbandry and Veterinary Medicine, 2021, 48(9): 3118-3127.