Ginsenoside Rg3 protects mouse leydig cells against triptolide by downregulation of miR-26a

References

• Wu CY, Yu TJ, Chen MJ. Age related testosterone level changes and male andropause syndrome. Chang Gung Med J. 2000;23(6):348–353.10958037
   PubMedGoogle Scholar
• Chung HJ, Noh Y, Kim MS, et al. Steroidogenic effects of Taraxacum officinale extract on the levels of steroidogenic enzymes in mouse leydig cells. Anim Cells Syst (Seoul). 2018;22(6):407–414. doi:10.1080/19768354.2018.145354530533263
   PubMed Web of Science ®Google Scholar
• Yang F, Wei Y, Liao B, et al. Lycium barbarum polysaccharide prevents cisplatin-induced MLTC-1 cell apoptosis and autophagy via regulating endoplasmic reticulum stress pathway. Drug Des Devel Ther. 2018;12:3211–3219. doi:10.2147/DDDT.S176316
   PubMed Web of Science ®Google Scholar
• Gao F, Li G, Liu C, et al. Autophagy regulates testosterone synthesis by facilitating cholesterol uptake in Leydig cells. J Cell Biol. 2018;217(6):2103–2119. doi:10.1083/jcb.20171007829618492
   PubMed Web of Science ®Google Scholar
• Zhao J, Ren S, Liu C, et al. Di-(2-Ethylhexyl) phthalate increases obesity-induced damage to the male reproductive system in mice. Oxid Med Cell Longev. 2018;2018:1861984. doi:10.1155/2018/186198429887939
   PubMed Web of Science ®Google Scholar
• Ferlin A, De Toni L, Agoulnik AI, et al. Protective role of testicular hormone INSL3 from atrophy and weakness in skeletal muscle. Front Endocrinol (Lausanne). 2018;9:562. doi:10.3389/fendo.2018.0042030323788
   PubMed Web of Science ®Google Scholar
• O’Reilly MW, Glisic M, Kumarendran B, et al. Serum testosterone, sex hormone-binding globulin and sex-specific risk of incident type 2 diabetes in a retrospective primary care cohort. Clin Endocrinol (Oxf). 2019;90(1):145–154. doi:10.1111/cen.1386230256433
   PubMed Web of Science ®Google Scholar
• O’Hara L, McInnes K, Simitsidellis I, et al. Autocrine androgen action is essential for leydig cell maturation and function, and protects against late-onset leydig cell apoptosis in both mice and men. Faseb J. 2015;29(3):894–910. doi:10.1096/fj.14-25572925404712
   PubMed Web of Science ®Google Scholar
• Ni C, Fang Y, Chen X, et al. Stem Leydig cell regeneration in the adult rat testis is inhibited after a short-term triphenyltin exposure. Toxicol Lett. 2019;306:80–89. doi:10.1016/j.toxlet.2019.02.01030772500
   PubMed Web of Science ®Google Scholar
• Tang M, Wang W, Cheng L, et al. The inhibitory effects of 20(R)-ginsenoside Rg3 on the proliferation, angiogenesis, and collagen synthesis of hypertrophic scar derived fibroblasts in vitro. Iran J Basic Med Sci. 2018;21(3):309–317.29511498
   PubMed Web of Science ®Google Scholar
• Choi KT. Botanical characteristics, pharmacological effects and medicinal components of Korean Panax ginseng C A Meyer. Acta Pharmacol Sin. 2008;29(9):1109–1118. doi:10.1111/j.1745-7254.2008.00789.x18718180
   PubMed Web of Science ®Google Scholar
• Su X, Zhang D, Zhang H, Zhao K, Hou W. Preparation and characterization of angiopep-2 functionalized ginsenoside-Rg3 loaded nanoparticles and the effect on C6 glioma cells. Pharm Dev Technol. 2019;1–37. doi:10.1080/10837450.2018.1551901
   Web of Science ®Google Scholar
• Li X, Tsauo J, Geng C, et al. Ginsenoside Rg3 decreases NHE1 expression via inhibiting EGF-EGFR-ERK1/2-HIF-1 alpha pathway in hepatocellular carcinoma: a novel antitumor mechanism. Am J Chin Med. 2018;46:1–17.29298518
   PubMed Web of Science ®Google Scholar
• Wang H, Wu W, Wang G, et al. Protective effect of ginsenoside Rg3 on lung injury in diabetic rats. J Cell Biochem. 2019;120:3323–3330.
   Web of Science ®Google Scholar
• Chen J, Liu GZ, Sun Q, et al. Protective effects of ginsenoside Rg3 on TNF-alpha-induced human nucleus pulposus cells through inhibiting NF-kappaB signaling pathway. Life Sci. 2019;216:1–9. doi:10.1016/j.lfs.2018.11.02230428306
   PubMed Web of Science ®Google Scholar
• Lee WJ, Kim YS, Shim WS. Korean red ginseng extract and ginsenoside Rg3 have anti-pruritic effects on chloroquine-induced itch by inhibition of MrgprA3/TRPA1-mediated pathway. J Ginseng Res. 2018;42(4):470–475. doi:10.1016/j.jgr.2017.05.00430337807
   PubMed Web of Science ®Google Scholar
• Liu T, Peng YF, Jia C, et al. Ginsenoside Rg3 improves erectile function in streptozotocin-induced diabetic rats. J Sex Med. 2015;12(3):611–620. doi:10.1111/jsm.1277925442300
   PubMed Web of Science ®Google Scholar
• Cao Y, Ye Q, Zhuang M, et al. Ginsenoside Rg3 inhibits angiogenesis in a rat model of endometriosis through the VEGFR-2-mediated PI3K/Akt/mTOR signaling pathway. PLoS One. 2017;12(11):e0186520. doi:10.1371/journal.pone.018652029140979
   PubMed Web of Science ®Google Scholar
• Huynh PN, Hikim AP, Wang C, et al. Long-term effects of triptolide on spermatogenesis, epididymal sperm function, and fertility in male rats. J Androl. 2000;21(5):689–699.10975416
   PubMed Web of Science ®Google Scholar
• Huang ZJ, Que HQ, Peng HY, et al. [Reproductive toxicity of triptolide and its mechanism in male rats]. Zhongguo Zhong Yao Za Zhi. 2015;40(23):4655–4659.27141679
   PubMedGoogle Scholar
• Hikim AP, Lue YH, Wang C, et al. Posttesticular antifertility action of triptolide in the male rat: evidence for severe impairment of cauda epididymal sperm ultrastructure. J Androl. 2000;21(3):431–437.10819451
   PubMedGoogle Scholar
• Pardo M, Abrial E, Jope RS, Beurel E. GSK3beta isoform-selective regulation of depression, memory and hippocampal cell proliferation. Genes Brain Behav. 2016;15(3):348–355. doi:10.1111/gbb.1228326749572
   PubMed Web of Science ®Google Scholar
• Narasimhan G, Henderson J, Luong HT, et al. OBG-like ATPase 1 inhibition attenuates angiotensin II-induced hypertrophic response in human ventricular myocytes via GSK-3beta/beta-catenin signaling. Clin Exp Pharmacol Physiol. 2019. doi:10.1111/1440-1681.13101
   PubMed Web of Science ®Google Scholar
• Teng Y, Wang Y, Fu J, et al. Cyclin T2: a novel miR-15a target gene involved in early spermatogenesis. FEBS Lett. 2011;585(15):2493–2500. doi:10.1016/j.febslet.2010.11.02221740905
   PubMed Web of Science ®Google Scholar
• Li F, Wei H, Li H, et al. miR-26a prevents neural stem cells from apoptosis via beta-catenin signaling pathway in cardiac arrest-induced brain damage. Biosci Rep. 2019. doi:10.1042/BSR20181635
   Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.126211846609
   PubMed Web of Science ®Google Scholar
• Umehara T, Kawashima I, Kawai T, et al. Neuregulin 1 regulates proliferation of leydig cells to support spermatogenesis and sexual behavior in adult mice. Endocrinology. 2016;157(12):4899–4913. doi:10.1210/en.2016-147827732090
   PubMed Web of Science ®Google Scholar
• Bouhallier F, Allioli N, Lavial F, et al. Role of miR-34c microRNA in the late steps of spermatogenesis. Rna. 2010;16(4):720–731. doi:10.1261/rna.196381020150330
   PubMed Web of Science ®Google Scholar
• Wu J, Bao J, Kim M, et al. Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc Natl Acad Sci U S A. 2014;111(28):E2851–2857. doi:10.1073/pnas.140777711124982181
   PubMed Web of Science ®Google Scholar
• Presslauer C, Tilahun Bizuayehu T, Kopp M, Fernandes JM, Babiak I. Dynamics of miRNA transcriptome during gonadal development of zebrafish. Sci Rep. 2017;7:43850. doi:10.1038/srep4385028262836
   PubMed Web of Science ®Google Scholar
• Kasimanickam VR, Kasimanickam RK. Differential expression of microRNAs in sexually immature and mature canine testes. Theriogenology. 2015;83(3):394–398.e391.25459426
   PubMed Web of Science ®Google Scholar
• Wu J, Bao J, Wang L, Hu Y, Xu C. MicroRNA-184 downregulates nuclear receptor corepressor 2 in mouse spermatogenesis. BMC Dev Biol. 2011;11:64. doi:10.1186/1471-213X-11-3122017809
   PubMed Web of Science ®Google Scholar
• Ma J, Fan Y, Zhang J, et al. Testosterone-dependent miR-26a-5p and let-7g-5p act as signaling mediators to regulate sperm apoptosis via targeting PTEN and PMAIP1. Int J Mol Sci. 2018;19(4). doi:10.3390/ijms19041233.
   Web of Science ®Google Scholar
• Kang PC, Leng KM, Liu YP, et al. miR-191 inhibition induces apoptosis through reactivating secreted frizzled-related protein-1 in cholangiocarcinoma. Cell Physiol Biochem. 2018;49(5):1933–1942. doi:10.1159/00049365430235453
   PubMedGoogle Scholar
• Sun D, Dong W, Jin B, et al. Mechanisms of Yangjing Capsule in leydig cell apoptosis and testosterone synthesis via promoting StAR expression. Biol Pharm Bull. 2018;41(9):1401–1405. doi:10.1248/bpb.b18-0020529984732
   PubMed Web of Science ®Google Scholar
• Ma B, Qi H, Li J, et al. Triptolide disrupts fatty acids and peroxisome proliferator-activated receptor (PPAR) levels in male mice testes followed by testicular injury: a GC-MS based metabolomics study. Toxicology. 2015;336:84–95. doi:10.1016/j.tox.2015.07.00826219505
   PubMed Web of Science ®Google Scholar
• Dhar P, Singla N. Histomorphological and biochemical changes induced by triptolide treatment in male lesser bandicoot rat, bandicota bengalensis. Pestic Biochem Physiol. 2014;116:49–55. doi:10.1016/j.pestbp.2014.09.00925454520
   PubMed Web of Science ®Google Scholar
• Kopalli SR, Cha KM, Hwang SY, Jeong MS, Kim SK. Korean red ginseng (Panax ginseng Meyer) with enriched Rg3 ameliorates chronic intermittent heat stress-induced testicular damage in rats via multifunctional approach. J Ginseng Res. 2019;43(1):135–142. doi:10.1016/j.jgr.2018.06.00430662302
   PubMed Web of Science ®Google Scholar
• Lee SH, Choi KH, Cha KM, et al. Protective effects of Korean red ginseng against sub-acute immobilization stress-induced testicular damage in experimental rats. J Ginseng Res. 2019;43(1):125–134. doi:10.1016/j.jgr.2017.09.00230662301
   PubMed Web of Science ®Google Scholar
• Eskandari M, Ghalyanchi Langeroudi A, Zeighami H, et al. Co-administration of ginseng and ciprofloxacin ameliorates epididymo-orchitis induced alterations in sperm quality and spermatogenic cells apoptosis following infection in rats. Andrologia. 2017;49(3). doi:10.1111/and.12621.
   PubMed Web of Science ®Google Scholar
• Procopio MS, de Avelar GF, Costa GMJ, et al. MicroRNAs in Sertoli cells: implications for spermatogenesis and fertility. Cell Tissue Res. 2017;370(3):335–346. doi:10.1007/s00441-017-2667-z28779347
   PubMed Web of Science ®Google Scholar
• Bai JF, Wang YK, Wang P, et al. Uncovering male fertility transition responsive miRNA in a wheat photo-thermosensitive genic male sterile line by deep sequencing and degradome analysis. Front Plant Sci. 2017;8:1370. doi:10.3389/fpls.2017.0137028848574
   PubMed Web of Science ®Google Scholar
• Gao F, Al-Azayzih A, Somanath PR. Discrete functions of GSK3α and GSK3β isoforms in prostate tumor growth and micrometastasis. Oncotarget. 2015;6(8):5947–5962. doi:10.18632/oncotarget.333525714023
   PubMedGoogle Scholar
• Si H, Zhang Y, Song Y, Li L. Overexpression of adrenomedullin protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis via the Akt/GSK3β and Bcl-2 signaling pathways. Int J Mol Med. 2018;41(6):3342–3352.29512737
   PubMed Web of Science ®Google Scholar
• Kim JE, Lim JH, Jeon GS, et al. Extrinsic apoptosis pathway altered by glycogen synthase kinase-3beta inhibitor influences the net drug effect on NSC-34 motor neuron-like cell survival. Biomed Res Int. 2017;2017:4163839. doi:10.1155/2017/416383929082245
   PubMed Web of Science ®Google Scholar
• Yu J, Zheng J, Lin J, et al. Indirubin-3-oxime prevents H2O2-induced neuronal apoptosis via concurrently inhibiting GSK3beta and the ERK pathway. Cell Mol Neurobiol. 2017;37(4):655–664. doi:10.1007/s10571-016-0402-z27412761
   PubMed Web of Science ®Google Scholar