Scientia Agricultura Sinica ›› 2020, Vol. 53 ›› Issue (9): 1904-1912.doi: 10.3864/j.issn.0578-1752.2020.09.016

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles     Next Articles

Effects of GnIH on Autophagy and Apoptosis of Porcine Ovarian Granulosa Cells via p38MAPK Signaling Pathway

Xin ZHANG,KongLin HUO,XingXing SONG,DuoNi ZHANG,Wen HU,ChuanHuo HU(),Xun LI()   

  1. College of Animal Science and Technology, Guangxi University, Nanning 530004
  • Received:2018-11-30 Accepted:2020-03-11 Online:2020-05-01 Published:2020-05-13
  • Contact: ChuanHuo HU,Xun LI E-mail:hch64815@gxu.edu.cn;lixun198@163.com

RichHTML

34

PDF

578

Abstract:

【Objective】Studies have shown that autophagy and apoptosis restrict each other. As one of the main regulatory pathways of apoptosis, p38MAPK signaling pathway also has the dual effects of promoting and inhibiting autophagy. It has been proved that gonadotropin inhibitory hormone (gonadotropin-inhibitory hormone, GnIH) has effects on autophagy and apoptosis, but the mechanism of action is not clear. This experiment was conducted to study the effects of GnIH on autophagy and apoptosis of porcine ovarian granulosa cells via p38MAPK signaling pathway and its mechanism. 【Method】Oval granulosa cells were extracted from pig ovaries and cultured in vitro. To explore the best time of GnIH on p38MAPK signaling pathway, according to the time gradient of incubation GnIH (0, 10, 30, 60, and 90 min), Western blot was used to detect the protein expression of p38 and p-p38 in pGCs. To verify the effect of GnIH on p38MAPK signaling pathway, the cells were divided into 4 groups (control, GnIH, p38 activating agent (U-46619), and U-46619 +GnIH), Western blot was used to detect the protein expression of p38 and p-p38. To investigate the effects of different concentrations of GnIH on autophagy and apoptosis: the cells were divided into 5 groups ( control, 10 -6mol·L -1 GnIH, 10 -8mol·L -1 GnIH, 10 -10mol·L -1 GnIH, and 10 -12mol·L -1 GnIH), Western blot was used to detect the protein expression of autophagy and apoptosis. To verify the effects of different concentrations of GnIH on autophagy and apoptosis through p38 signaling pathway: the cells were divided into 6 groups (control, U-46619, U-46619+10 -6 mol·L -1 GnIH, U-46619+10 -8mol·L -1 GnIH, U-46619+10 -10mol·L -1 GnIH, and U-46619+10 -12mol·L -1 GnIH), Western blot was used to detect the protein expression of autophagy and apoptosis. 【Result】After incubation with GnIH for 10 min, the protein expression of p38 and p-p38 was significantly decreased (P<0.05). The results suggested that the optimum action time of GnIH on p38MAPK signaling pathway was 10 min; U-46619 significantly promoted the phosphorylation of p38 in pGCs (P<0.05), while GnIH significantly inhibited p38 phosphorylation of pGCs (P<0.05). The results suggested that U-46619 activated the p38MAPK signaling pathway, and GnIH inhibited the activation of p38MAPK signaling pathway; When the concentration of GnIH was 10 -6 mol·L -1, the autophagy and apoptosis of pGCs increased significantly (P<0.05). With the decrease of GnIH concentration, the autophagy level of pGCs increased gradually (P<0.05), while the apoptosis level of pGCs decreased gradually (P<0.05). The results suggest that high concentration of GnIH promote autophagy and apoptosis. With the decrease of GnIH concentration, the autophagy level increased gradually, while the apoptosis level decreased gradually. After adding U-46619, GnIH significantly upregulated the autophagy of pGCs and down-regulated the apoptosis of pGCs (P<0.05), which suggested that different concentrations of GnIH affected the autophagy and apoptosis of pGCs through p38MAPK signaling pathway. 【Conclusion】GnIH might up-regulate the autophagy of pGCs and reduce the apoptosis of pGCs by inhibiting the activation of p38MAPK signaling pathway.

Key words: autophagy, apoptosis, GnIH, p38MAPK, porcine, ovarian granulosa cells

Fig. 1

Immunoblot and statistical analysis of p38 and p-p38 proteins with different time of RFRP-3 (0, 10, 30, 60, 90 min, n=3) Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

Fig. 2

Immunoblot and statistical analysis of p38 and p-p38 proteins (control, GnIH, U-46619, GnIH+U-46619) (n=3) Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

Fig. 3

RFRP-3 concentration gradient (0, 10-6, 10-8, 10-10, 10-12) treated with pGCs.Western blot caspase-3, Bax and Bcl-2 and statistical analysis (n=3) Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

Fig. 4

RFRP-3 concentration gradient (0, 10-6, 10-8, 10-10, 10-12) treated with pGCs. Western blot Beclin-1, Atg12 and Atg5 and statistical analysis (n=3) Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E.M. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

Fig. 5

After incubated with p38 activator, RFRP-3 concentration gradient (0, 10-6, 10-8, 10-10, 10-12) was treated with pGCs.Western blot caspase-3,Bax and Bcl-2 and statistical analysis (n=3) Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

Fig. 6

After incubated with p38 activator, RFRP-3 concentration gradient (0, 10-6, 10-8, 10-10, 10-12) was treated with pGCs. Western blot Beclin-1,LC3 and Atg-5 and statistical analysis Densitometric quantification was performed using ImageJ with GAPDH as the internal control for normalization. Values are mean±S.E. Compared with control group, asterisk indicates significant difference. *P<0.05; **P<0.01"

[1] 谢敏, 姜法贵, 郭燕君 . 卵泡发育和闭锁过程中颗粒细胞自噬和凋亡关系的研究. 四川生理科学杂志, 2015,37(2):85-88.
XIE M, JIANG F G, GUO Y J . Study on the relationship between autophagy and apoptosis of granulosa cells during follicular development and atresia. Sichuan Journal of Physiology, 2015,37(2):85-88. (in Chinese)
[2] 赵红秋 . 浅析提高母猪生产性能的措施. 今日畜牧兽医, 2019,35(4):69.
ZHAO H Q . Analysis on the measures to improve the performance of sows. Animal Husbandry Veterinary Surgeons Today, 2019,35(4):69. (in Chinese)
[3] TSUTSUI K, SAIGOH E, UKENA K, TERANISHI H, FUJISAWA Y, KIKUCHI M, ISHII S, PETER J . A novel avian hypoth- alamic peptide inhibiting gonadotropin release. Biochemical and Biophysical Research Communication, 2000,275(2):661-667.
doi: 10.1006/bbrc.2000.3350 pmid: 10964719
[4] TSUTSUI K, UBUKA T, BENTLEY G E, KRIEGSFELD L . Gonadotropin-inhi-bitory hormone(GnIH): discovery, progress and prospect. General and Comparative Endocrinology, 2012,177(3):305-314.
doi: 10.1016/j.ygcen.2012.02.013
[5] 龚金秋, 阳美霞, 唐娇美, 曾杰, 王水莲 . RFRP-3对哺乳动物生殖激素的调节作用. 中兽医医药杂志, 2017(4):31-33.
GONG J Q, YANG M X, TANG J M, ZENG J, WANG S L . Regulatory effect of RFRP-3 on reproductive hormones in mammals. Journal of Chinese Veterinary Medicine, 2017(4):31-33. (in Chinese)
[6] 韩兴绘, 俞建 . RFRP-3/GPR147信号通路在哺乳动物生殖系统中作用的研究进展. 中国中西医结合儿科学, 2016,8(3):253-257.
HAN X H, YU J . Progress in the study of the role of RFRP-3/GPR147 signaling pathway in the reproductive system of mammals. Chinese Integrated Traditional Chinese and Western Medicine Pediatrics, 2016,8(3):253-257. (in Chinese)
[7] KIM J S, BROWNJOHN P W, DYER B S, BELTRAMO M, WALKER C S, HAY D L, PAINTER G F, TYNDALL J D, ANDERSON G M . Anxiogenic and stressor effects of the hypothalamic neuropeptide rfrp-3 are overcome by the NPFFR antagonist GJ14. Endocrinology, 2015,156(11):4152-4162.
doi: 10.1210/en.2015-1532 pmid: 26259035
[8] BENTLEY G E, UBUKA T, MCGUIRE N L, CALISI R, PERFITO N, KRIEGSFELD L J, WINGFIELD J C, TSUTSUI K . Gonadotrophin- inhibitory hormone: A multifunctional neuropeptide. Journal of Neuroendocrinology, 2009,21 276-281.
doi: 10.1111/j.1365-2826.2009.01851.x pmid: 19210295
[9] BENTLEY G E, WILSTERMAN K, ERNST D K, LYNN S E, DICKENS M J, CALISI R M, KRIEGSFELD L J, KAUFER D, GERAGHTY A C, MCGUIRE N L, LOPES P C, TSUTSUI K . Neural versus gonadal GnIH: are they independent systems A mini-review. Integrative and Comparative Biology, 2017,57 1194-1203.
doi: 10.1093/icb/icx085 pmid: 28992195
[10] RIZWAN M Z, HARBID A A, INGLIS M A, QUENNELL J H, ANDERSON G M . Evidence that hypothalamic RFamide related peptide-3 neurones are not leptin-responsive in mice and rats. Journal of Neuroendocrinology, 2014,26:247-257.
doi: 10.1111/jne.12140 pmid: 24612072
[11] LI X, SU J, LEI Z, ZHAO Y Y, JIN M M, FANG R, ZHENG L C, JIAO Y . Gonadotropin-inhibitory hormone (GnIH) and its receptor in the female pig: cDNA cloning, expression in tissues and expression pattern in the reproductive axis during the estrous cycle. Peptides, 2012,36(2):176-185.
doi: 10.1016/j.peptides.2012.05.008 pmid: 22664321
[12] KERR J F, WYLLIE A H, CURRIE A R . Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. British Journal of Cancer, 1972,26(4):239-257.
doi: 10.1038/bjc.1972.33 pmid: 4561027
[13] OBEID L M, LINARDIC C M, KAROLAK L A, & HANNUN Y A . Programmed cell death. Science, 1993,259(5102), 1769-1771.
doi: 10.1126/science.8456305 pmid: 8456305
[14] ZHANG H, KONG X X, KANG J S, SU J, LI Y, ZHONG J T, SUN L K . Oxidative stress induces parallel autophagy and mitochondria dysfunction in Human Glioma U251 Cells. Toxicological Sciences, 2009.110(2):376-388.
doi: 10.1093/toxsci/kfp101 pmid: 19451193
[15] 汪宇, 周桃, 孙韩艳, 黄蓓 , 姜黄素类似物EF24诱导A549细胞自噬及凋亡关系的研究. 中国细胞生物学学报, 2012,34(6):590-596.
WANG Y, ZHOU T, SUN H Y, HUANG P . Study on the relationship between autophagy and apoptosis in A549 cells induced by curcumin analogue EF24. Chinese Journal of Cell Biology, 2012,34(6):590-596. (in Chinese)
[16] EISENBERG-LERNER A, BIALIK S, SIMON H U, KIMCHI A . Life and death partners: Apoptosis, autophagy and the cross-talk between them. Cell Death and Differentiation, 2009,16(7):966-975.
doi: 10.1038/cdd.2009.33 pmid: 19325568
[17] CHOI J, JO M, LEE E, CHOI D . Induction of apoptotic cell death via accumulation of autophagosomes in rat granulosa cells. Fertility and Sterility, 2011,95(4):1482-1486.
doi: 10.1016/j.fertnstert.2010.06.006 pmid: 20630503
[18] CARDENAS H, POPE W F . Control of ovulation rate in swine. Animal Science, 2002,80:36-46.
[19] CHOI J Y, JO M W, LEE E Y, YOON B K, CHOI D S . The role of autophagy in follicular development and atresia in rat granulosa cells. Fertility and Sterility, 2010,93(8):2532-2537.
doi: 10.1016/j.fertnstert.2009.11.021
[20] HUŁAS-STASIAK M. GAWRON A . Follicular atresia in the prepubertal spiny mouse (Acomys cahirinus) ovary. Apoptosis, 2011,16(10):967-975.
doi: 10.1007/s10495-011-0626-9 pmid: 21739276
[21] MORAIS R D V S, THOMÉ R G, LEMOS F S, RIZZO N B E . Autophagy and apoptosis interplay during follicular atresia in fish ovary: A morphological and immunocytochemical study. Cell and Tissue Research, 2012,347(2):467-478.
doi: 10.1007/s00441-012-1327-6
[22] TAMURA M, NAKAGAWA Y, SHIMIZU H, YAMADA N, MIYANO T, MIYAZAKI H . HCellular functions of mitogen-activated protein kinases and protein tyrosine phosphatases in ovarian granulosa cells. Reproduction and Development, 2004Feb;50(1):47-55.
doi: 10.1262/jrd.50.47 pmid: 15007201
[23] VILLADIAZ L G, MIYANO T . Activation of p38 MAPK during porcine oocyte maturation. Biology of Reproduction, 2004,71(2):691-696.
doi: 10.1095/biolreprod.103.026310 pmid: 15115730
[24] SINGH P, KRISHNA A, TSUTSUI K . Effects of gonadotropin-inhibitory hormone on folliculogenesis and steroidogenesis of cyclic mice. Fertility & Sterility, 2011,95(4):1397-1404.
doi: 10.1016/j.fertnstert.2010.03.052 pmid: 20452585
[25] 李卉, 马云, 马波, 高扬, 宋辉 . 不同周龄小鼠GnIH的血清含量及卵巢表达研究. 农业科学研究, 2017(4):13-15.
LI H, MA Y, MA B, GAO Y, SONG H . Study on serum content and ovarian expression of GnIH in mice of different weeks of age. Agricultural Science Research, 2017(4):13-15. (in Chinese)
[26] 汪瑶, 李珣, 李敏婕, 国梦婕, 雷治海 . GnIH对母猪生殖调控的研究. 中国农业科学, 2014,47(18):3716-3724.
WANG Y, LI X, LI M J, GUO M J, LEI Z H . Study on reproductive regulation of sows by GnIH. Scientia Agricultura Sinica, 2014,47(18):3716-3724. (in Chinese)
[27] MADDINENI S R, OCÓN-GROVE O M, KRZYSIK-WALKER S M, HENDRICKS G L, RAMACHANDRAN R . Gonadotropin-inhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: Potential role of GnIH in follicular maturation. Reproduction, 2008,135(2):267-274.
doi: 10.1530/REP-07-0369 pmid: 18239054
[28] 张蕊, 常玲玲, 穆春宇, 付胜勇, 汤青萍, 卜柱 . GnIH/GnRH对鸟类排卵的调控作用. 中国家禽, 2018(1):42-45.
ZHANG R, CHANG L L, MU C Y, FU S Y, TANG Q P, PU Z . Regulation of GnIH/GnRH on ovulatory activity in birds. Chinese Poultry, 2018(1):42-45. (in Chinese)
[29] FRANOIS H, LANGLOIS I, MULSANT P, BONNET A, BENNE F, GASSER F . Gonadotropins induce accumulation of insulin-like growth factor I mRNA in pig granulosa cells in vitro. Molecular & Cellular Endocrinology, 1992,86(3):205-211.
doi: 10.1016/0303-7207(92)90145-v pmid: 1511789
[30] CALONI F, RANZENIGO G, CREMONESI F, SPICER L J . Effects of a trichothecene, T-2 toxin, on proliferation and steroid production by porcine granulosa cells. Toxicon, 2009,54(3):337-344.
doi: 10.1016/j.toxicon.2009.05.002 pmid: 19463844
[31] BENTLEY G E, UBUKA T, MCGUIRE N L, CHOWDHURY V S, MORITA Y, YANO T, HASUNUMA I, BINNS M, WINGFIELD J C, TSUTSUI K . Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. General & Comparative Endocrinology, 2008,156(1):34-43.
doi: 10.1016/j.ygcen.2007.10.003 pmid: 18031743
[32] UBUKA T, UKENA K, SHARP P J, BENTLEY G E, TSUTSUI K . Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology, 2006,147(3):187-194.
doi: 10.7326/0003-4819-147-3-200708070-00008 pmid: 17679707
[33] WANG X Y, GUO G L, ZHANG X, LI M, XIAO K, HU C H, LI X . Effect of RFRP-3, the mammalian ortholog of GnIH, on the epididymis of male rats. Theriogenology, 2018. DOI: 10. 1016/ j. theriogenology. 2018. 05. 029.
doi: 10.1016/j.theriogenology.2018.05.029 pmid: 29913425
[34] SON Y L, UBUKA T, SOGA T, YAMAMOTO K, BENTLEY G E, TSUTSUI K . Inhibitory action of gonadotropin-inhibitory hormone on the signaling pathways induced by kisspeptin and vasoactive intestinal polypeptide in GnRH neuronal cell line, GT1-7. Faseb Journal Official Publication of the Federation of American Societies for Experimental Biology, 2016,30(6):2198.
doi: 10.1096/fj.201500055 pmid: 26929433
[35] DAVE A, KRISHNA A, TSUTSUI K . Direct effects of RFRP-1, a mammalian GnIH ortholog, on ovarian activities of the cyclic mouse. General and Comparative Endocrinology, 2017,252:193-199.
doi: 10.1016/j.ygcen.2017.06.024 pmid: 28658602
[36] WANG X F, ZHOU Q M, LU Y Y, ZHANG T L, SU S B . Glycyrrhetinic acid potently suppresses breast cancer invasion and metastasis by impairing the p38 MAPK–AP1 functional axis. Expert Opinion on Therapeutic Targets, 2015,19(5) : 577-587.
doi: 10.1517/14728222.2015.1012156 pmid: 25828376
[37] TUNG C L, JIAN Y J, CHEN J C, WANG T J, CHEN W C, ZHENG H Y, CHANG P Y, LIAO K S, LIN Y W . Curcumin downregulates p38MAPK-dependent X-ray repair cross-complement group 1( XRCC1) expression to enhance cisplatin-induced cytotoxicity in human lung cancer cells. Naunyn-Schmiedeberg’s Archives of Pharmacology, 2016,389(6):657-666.
doi: 10.1007/s00210-016-1235-5
[38] CALDER M D, WATSON P H, WATSON A J . Culture medium, gas atmosphere and MAPK inhibition affect regulation of RNA-binding protein targets during mouse preimplantation development. Reproduction, 2011,142(5):689-698.
doi: 10.1530/REP-11-0082 pmid: 21846809
[39] INAGAKI K, OTSUKA F, MIYOSHI T, YAMASHITA M, TAKAHASHI M, GOTO J, SUZUKI J, MAKINO H . Hp38- Mitogen- activated protein kinase stimulated steroidogenesis in granulosa cell-oocyte cocultures: role of bone morphogenetic proteins 2 and 4. Endocrinology, 2009,150(4):1921-1930.
doi: 10.1210/en.2008-0851 pmid: 19022884
[40] NIKOLETOPOULOU V, MARKAKI M, PALIKARAS K, TAVERNARAKIS N . Crosstalk between apoptosis, necrosis and autophagy. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 2013,1833(12):3448-3459.
doi: 10.1016/j.bbamcr.2013.06.001 pmid: 23770045
[1] LIU YuFang,CHEN YuLin,ZHOU ZuYang,CHU MingXing. miR-221-3p Regulates Ovarian Granulosa Cells Apoptosis by Targeting BCL2L11 in Small-Tail Han Sheep [J]. Scientia Agricultura Sinica, 2022, 55(9): 1868-1876.
[2] WANG JiaMin,SHI JiaChen,MA FangFang,CAI Yong,QIAO ZiLin. Effects of Soy Isoflavones on the Proliferation and Apoptosis of Yak Ovarian Granulosa Cells [J]. Scientia Agricultura Sinica, 2022, 55(8): 1667-1675.
[3] LI WenHui,HE YiJing,JIANG Yao,ZHAO HongYu,PENG Lei,LI Jia,RUI Rong,JU ShiQiang. Effects of FB1 on Apoptosis and Autophagy of Porcine Oocytes in vitro Maturation [J]. Scientia Agricultura Sinica, 2022, 55(6): 1241-1252.
[4] CHEN Yu,ZHU HaoZhe,CHEN YiChun,LIU Zheng,DING Xi,GUO Yun,DING ShiJie,ZHOU GuangHong. Differentiation of Porcine Muscle Stem Cells in Three-Dimensional Hydrogels [J]. Scientia Agricultura Sinica, 2022, 55(22): 4500-4512.
[5] MingJie XING,XianHong GU,XiaoHong WANG,Yue HAO. Effects of IL-15 Overexpression on Myoblast Differentiation of Porcine Skeletal Muscle Cells [J]. Scientia Agricultura Sinica, 2022, 55(18): 3652-3663.
[6] YANG ChangPei,WANG NaiXiu,WANG Kai,HUANG ZiQing,LIN HaiLan,ZHANG Li,ZHANG Chen,FENG LuQiu,GAN Ling. Effects and Mechanisms of Exogenous GABA Against Oxidative Stress in Piglets [J]. Scientia Agricultura Sinica, 2022, 55(17): 3437-3449.
[7] LI LiYing,HE YingTing,ZHONG YuYi,ZHOU XiaoFeng,ZHANG Hao,YUAN XiaoLong,LI JiaQi,CHEN ZanMou. CTNNB1 Regulates the Function of Porcine Ovarian Granulosa Cells [J]. Scientia Agricultura Sinica, 2022, 55(15): 3050-3061.
[8] Qun ZHOU,XiaoFei CHEN,RuiCi KAN,Yu LI,Hui CAO,YanLing PENG,Bin ZHANG. Molecular Epidemiological Investigation of Porcine Group A Rotavirus in Sichuan from 2017 to 2019 [J]. Scientia Agricultura Sinica, 2021, 54(5): 1063-1072.
[9] FENG YunKui,WANG Jian,MA JinLiang,ZHANG LiuMing,LI YongJun. Effects of miR-31-5p on the Proliferation and Apoptosis of Hair Follicle Stem Cells in Goat [J]. Scientia Agricultura Sinica, 2021, 54(23): 5132-5143.
[10] CHEN HuiFang,HUANG QiLiang,HU ZhiChao,PAN XiaoTing,WU ZhiSheng,BAI YinShan. Expression Differences and Functional Analysis of Exosomes microRNA in Porcine Mature and Atretic Follicles [J]. Scientia Agricultura Sinica, 2021, 54(21): 4664-4676.
[11] MA MengNan,WANG HuiMing,WANG MiaoMiao,YAO Wang,ZHANG JinBi,PAN ZengXiang. Identification of circINHBB During Follicular Atresia and Its Effect on Granulosa Cell Apoptosis [J]. Scientia Agricultura Sinica, 2021, 54(18): 3998-4007.
[12] DU Xing,ZENG Qiang,LIU Lu,LI QiQi,YANG Liu,PAN ZengXiang,LI QiFa. Identification of the Core Promoter of Linc-NORFA and Its Transcriptional Regulation in Erhualian Pig [J]. Scientia Agricultura Sinica, 2021, 54(15): 3331-3342.
[13] LI RunTing,CHEN LongXin,ZHANG LiMeng,HE HaiYing,WANG Yong,YANG RuoChen,DUAN ChunHui,LIU YueQin,WANG YuQin,ZHANG YingJie. Transient Expression and the Effect on Proliferation and Apoptosis of Granule Cell Stimulating Factor in Ovarian Fibroblasts [J]. Scientia Agricultura Sinica, 2021, 54(11): 2434-2444.
[14] HUANG Feng,WEI QiChao,LI Xia,LIU ChunMei,ZHANG ChunHui. Research Progress on Mechanisms of Apoptosis to Postmortem Tenderization in Muscle [J]. Scientia Agricultura Sinica, 2021, 54(10): 2192-2202.
[15] PAN YangYang,WANG Meng,RUI Xian,WANG LiBin,HE HongHong,WANG JingLei,MA Rui,XU GengQuan,CUI Yan,FAN JiangFeng,YU SiJiu. RNA-Binding Motif Protein 3(RBM3) Expression is Regulated by Insulin-Like Growth Factor (IGF-1) for Protecting Yak (Bos grunniens) Cumulus Cells from Apoptosis During Hypothermia Stress [J]. Scientia Agricultura Sinica, 2020, 53(11): 2285-2296.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd