China Animal Husbandry and Veterinary Medicine ›› 2024, Vol. 51 ›› Issue (11): 4722-4731.doi: 10.16431/j.cnki.1671-7236.2024.11.007
• Physiological and Biochemical • Previous Articles
LI Jingxuan, LONG Cheng, QI Xiaolong
Received:
2024-02-19
Published:
2024-10-31
CLC Number:
LI Jingxuan, LONG Cheng, QI Xiaolong. Research Progress on the Effect of Endoplasmic Reticulum Stress on Testosterone Synthesis in the Leydig Cells[J]. China Animal Husbandry and Veterinary Medicine, 2024, 51(11): 4722-4731.
[1] NGUYEN T,MILLS J C,CHO C J.The coordinated management of ribosome and translation during injury and regeneration[J].Frontiers in Cell and Developmental Biology,2023,11:1186638. [2] LIU L N,ZHANG M J,JIANG F J,et al.High cholesterol diet-induced testicular dysfunction in rats[J].Hormones (Athens),2023,22(4):685-694. [3] CELIK C,LEE S Y T,YAP W S,et al.Endoplasmic reticulum stress and lipids in health and diseases[J].Progress in Lipid Research,2023,89:101198. [4] PARK S J,KIM T S,PARK C K,et al.hCG-induced endoplasmic reticulum stress triggers apoptosis and reduces steroidogenic enzyme expression through activating transcription factor 6 in Leydig cells of the testis[J].Journal of Molecular Endocrinology,2013,50(2):151-166. [5] HOTAMISLIGIL G S,DAVIS R J.Cell signaling and stress responses[J].Cold Spring Harbor Perspectives in Biology,2016,8(10):a006072. [6] 王立堃.内质网应激下的内质网-线粒体互作[J].中国科学:生命科学,2022,52(1):46-57. WANG L K.The endoplasmic reticulum-mitochondrial interaction under endoplasmic reticulum stress[J].Scientia Sinica(Vitae),2022,52(1):46-57.(in Chinese) [7] HETZ C,PAPA F R.The unfolded protein response and cell fate control[J].Molecular Cell,2018,69(2):169-181. [8] CHERUBINI A,ZITO E.ER stress as a trigger of UPR and ER-phagy in cancer growth and spread[J].Frontiers in Oncology.2022,12:997235. [9] CABRAL-MIRANDA F,TAMBURINI G,MARTINEZ G,et al.Unfolded protein response IRE1/XBP1 signaling is required for healthy mammalian brain aging[J].The EMBO Journal,2022,41(22):e111952. [10] HUANG S J,XING Y Y,LIU Y.Emerging roles for the ER stress sensor IRE1α in metabolic regulation and disease[J].The Journal of Biological Chemistry,2019,294(49):18726-18741. [11] XU B T,XU J P,CAI N B,et al.Roflumilast prevents ischemic stroke-induced neuronal damage by restricting GSK3β-mediated oxidative stress and IRE1α/TRAF2/JNK pathway[J].Free Radical Biology & Medicine,2021,163:281-296. [12] YOSHIDA H,MATSUI T,YAMAMOTO A,et al.XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor[J].Cell,2001,107(7):881-891. [13] OAKES S A,PAPA F R.The role of endoplasmic reticulum stress in human pathology[J].Annual Review of Pathology,2015,10:173-194. [14] KOPP M C,LARBURU N,DURAIRAJ V,et al.UPR proteins IRE1 and PERK switch BiP from chaperone to ER stress sensor[J].Nature Structural & Molecular Biology,2019,26(11):1053-1062. [15] VANHOUTTE D,SCHIPS T G,VO A,et al.Thbs1 induces lethal cardiac atrophy through PERK-ATF4 regulated autophagy[J]. Nature Communications,2021,12(1):3928. [16] ZHANG R,JIANG M,ZHANG J B,et al.Regulation of the cerebrovascular smooth muscle cell phenotype by mitochondrial oxidative injury and endoplasmic reticulum stress in simulated microgravity rats via the PERK-eIF2α-ATF4-CHOP pathway[J].Biochimica et Biophysica Acta.Molecular Basis of Disease,2020,1866(8):165799. [17] MÁRTON M,BÁNHEGYI G,GYÖNGYÖSI N,et al.A systems biological analysis of the ATF4-GADD34-CHOP regulatory triangle upon endoplasmic reticulum stress[J].FEBS Open Bio,2022,12(11):2065-2082. [18] SOMMER T,JAROSCH E.BiP binding keeps ATF6 at bay[J].Developmental Cell,2002,3(1):1-2. [19] PEOTTER J,KASBERG W,PUSTOVA I,et al.COPⅡ-mediated trafficking at the ER/ERGIC interface[J].Traffic (Copenhagen,Denmark),2019,20(7):491-503. [20] MESGARZADEH J S,ROMINE I C,SMITH-COHEN E M,et al.ATF6 activation reduces amyloidogenic transthyretin secretion through increased interactions with endoplasmic reticulum proteostasis factors[J].Cells,2022,11(10):1661. [21] VIDAL R L,SEPULVEDA D,TRONCOSO-ESCUDERO P,et al.Enforced dimerization between XBP1 s and ATF6f enhances the protective effects of the UPR in models of neurodegeneration[J].Molecular Therapy,2021,29(5):1862-1882. [22] SHARMA R B,DARKO C,ALONSO L C.Intersection of the ATF6 and XBP1 ER stress pathways in mouse islet cells[J]. The Journal of Biological Chemistry,2020,295(41):14164-14177. [23] ELETTO D,ELETTO D,BOYLE S,et al.PDIA6 regulates insulin secretion by selectively inhibiting the RIDD activity of IRE1[J]. FASEB Journal,2016,30(2):653-665. [24] TREMBLAY J J.Molecular regulation of steroidogenesis in endocrine Leydig cells[J].Steroids,2015,103:3-10. [25] 常雪蕊,郭 勇,齐晓龙,等.睾丸间质细胞线粒体调控睾酮合成的研究进展[J].中国畜牧兽医,2022,49(1):265-272. CHANG X R,GUO Y,QI X L,et al.Research progress on testosterone synthesis regulated by mitochondria of Leydig cells[J].China Animal Husbandry & Veterinary Medicine, 2022,49(1):265-272.(in Chinese) [26] HALE D B.Testicular macrophage modulation of Leydig cell steroidogenesis[J].Journal of Reprpductive Immunology,2002,57(1-2):3-18. [27] GALANO M,LI Y,LI L,et al.Role of constitutive STAR in Leydig cells[J].International Journal of Molecular Sciences,2021,22(4):2021. [28] YE L,SU Z J,GE R S.Inhibitors of testosterone biosynthetic and metabolic activation enzymes[J]. Molecules,2011,16(12):9983-10001. [29] ZIRKIN B R,EWING L L,KROMANN N,et al.Testosterone secretion by rat,rabbit,guinea pig,dog,and hamster testes perfused in vitro:Correlation with Leydig cell ultrastructure[J].Endocrinology,1980,107(6):1867-1874. [30] MOTOHASHI M,WEMPE M F,MUTOU T,et al.Male rats exposed in utero to di(n-butyl) phthalate:Age-related changes in Leydig cell smooth endoplasmic reticulum and testicular testosterone-biosynthesis enzymes/proteins[J].Reproductive Toxicology (Elmsford,N.Y.),2016,59:139-146. [31] ZIRKIN B R,PAPADOPOULOS V.Leydig cells:Formation,function,and regulation[J].Biology of Reproduction,2018,99(1):101-111. [32] RIGOTTI A,MIETTINEN H E,KRIEGER M.The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues[J].Endocrine Reviews,2003,24(3):357-387. [33] SCHREIBER J R,WEINSTEIN D B,HSUEH A J.Lipoproteins stimulate androgen production by cultured rat testis cells[J].Journal of Steroid Biochemistry,1982,16(1):39-43. [34] MURPHY D J.The biogenesis and functions of lipid bodies in animals,plants and microorganisms[J].Progress in Lipid Research,2001,40(5):325-438. [35] HALL P F.Cytochromes P-450 and the regulation of steroid synthesis[J].Steroids,1986,48(3-4):131-196. [36] 张 鹏,曹伟灵,叶陈丽,等.转运蛋白分子相关疾病及其可能作用机制研究进展[J].中国药理学与毒理学杂志,2022,36(1):62-70. ZHANG P,CAO W L,YE C L,et al.Research progress in translocator protein related diseases and possible mechanisms[J]. Chinese Journal of Pharmacology and Toxicology, 2022,36(1):62-70.(in Chinese) [37] WANG X,LI M X,ZHANG X G,et al.CYP11A1 upregulation leads to trophoblast oxidative stress and fetal neurodevelopmental toxicity that can be rescued by vitamin D[J].Frontiers in Molecular Biosciences,2021,7:608447. [38] PAYNE A H,HALES D B.Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones[J].Endocrine Reviews,2004,25(6):947-970. [39] QIAO X Y,YE L,LU J L,et al.Curcumin analogues exert potent inhibition on human and rat gonadal 3β-hydroxysteroid dehydrogenases as potential therapeutic agents:Structure-activity relationship and in silico docking[J].Journal of Enzyme Inhibition and Medicinal Chemistry,2023,38(1):2205052. [40] XIA Y P,YANG X B,LU J C,et al.The endoplasmic reticulum stress and related signal pathway mediated the glyphosate-induced testosterone synthesis inhibition in TM3 cells[J].Environmental Pollution (Barking,Essex:1987),2020,260:113949. [41] 陈昌波.枸杞多糖对双酚A染毒小鼠生精功能的保护及睾丸CYP17A1表达的影响[D].西安:中国人民解放军空军军医大学,2019. CHEN C B.Effect of protecting spermatogenesis and regulating the expressionof CYP17A1 on the tests of BPA-infected mice by LBP gavage[D].Xi’an:Air Force Medical University,2019.(in Chinese) [42] VON SPRECKELSEN B,AKSGLAEDE L,JOHANNSEN T H,et al.Prepubertal and pubertal gonadal morphology,expression of cell lineage markers and hormonal evaluation in two 46,XY siblings with 17β-hydroxysteroid dehydrogenase 3 deficiency[J].Journal of Pediatric Endocrinology & Metabolism:JPEM,2022,35(7):953-961. [43] DING J J,YOU S P,ZHANG J X,et al.Rational design of 17β-hydroxysteroid dehydrogenase type 3 for improving testosterone production with an engineered Pichia pastoris[J].Bioresource Technology,2021,341:125833. [44] HETZ C.The unfolded protein response:Controlling cell fate decisions under ER stress and beyond[J].Nature Reviews.Molecular Cell Biology,2012,13(2):89-102. [45] CAMPOS G,SCHMIDT-HECK W,GHALLAB A,et al.The transcription factor CHOP,a central component of the transcriptional regulatory network induced upon CCl4 intoxication in mouse liver,is not a critical mediator of hepatotoxicity[J].Archives of Toxicology.2014,88(6):1267-1280. [46] YAO Y F,LU Q L,HU Z K,et al.A non-canonical pathway regulates ER stress signaling and blocks ER stress-induced apoptosis and heart failure[J].Nature Communications,2017,8(1):133. [47] YI S Y,CHEN K,ZHANG L H,et al.Endoplasmic reticulum stress is involved in stress-induced hypothalamic neuronal injury in rats via the PERK-ATF4-CHOP and IRE1-ASK1-JNK pathways[J].Frontiers in Cellular Neuroscience,2019,13:190. [48] KORENNYKH A,WALTER P.Structural basis of the unfolded protein response[J].Annual Review of Cell and Developmental Biology,2012,28:251-277. [49] LIU Z X,SHI Q,SONG X F,et al.Activating transcription factor 4 (ATF4)-ATF3-C/EBP homologous protein (CHOP) cascade shows an essential role in the ER stress-induced sensitization of tetrachlorobenzoquinone-challenged PC12 cells to ROS-mediated apoptosis via death receptor 5 (DR5) signaling[J].Chemical Research in Toxicology,2016,29(9):1510-1518. [50] XU W L,GAO L S,LI T,et al.Apelin-13 alleviates early brain injury after subarachnoid hemorrhage via suppression of endoplasmic reticulum stress-mediated apoptosis and blood-brain barrier disruption:Possible involvement of ATF6/CHOP Pathway[J].Neuroscience,2018,388:284-296. [51] SONG C,WANG Z,CAO J,et al.Hesperetin protects hippocampal neurons from the neurotoxicity of aflatoxin B1 in mice[J]. Ecotoxicology and Environmental Safety,2023,269:115782. [52] KVANSAKUL M,CARIA S,HINDS M G.The Bcl-2 family in host-virus interactions[J].Viruses,2017,9(10):290. [53] IURLARO R,MUÑOZ-PINEDO C.Cell death induced by endoplasmic reticulum stress[J].The FEBS Journal,2016,283(14):2640-2652. [54] LI T L,SU L,LEI Y J,et al.DDIT3 and KAT2A proteins regulate TNFRSF10A and TNFRSF10B expression in endoplasmic reticulum stress-mediated apoptosis in human lung cancer cells[J].The Journal of Biological Chemistry,2015,290(17):11108-11118. [55] KIM J H,PARK S J,KIM T S,et al.Testosterone production by a Leydig tumor cell line is suppressed by hyperthermia-induced endoplasmic reticulum stress in mice[J]. Life Sciences,2016,146:184-191. [56] LIU H L,DING S S,NIE H P,et al.PM2.5 exposure at different concentrations and modes induces reproductive toxicity in male rats mediated by oxidative and endoplasmic reticulum stress[J].Ecotoxicology and Environmental Safety,2022,244:114042. [57] GAO Y,WU X C,ZHAO S Q,et al.Melatonin receptor depletion suppressed hCG-induced testosterone expression in mouse Leydig cells[J].Cellular & Molecular Biology Letters,2019,24:21. [58] WEN S Y,CHEN Y B,TANG Y Z,et al.Male reproductive toxicity of polystyrene microplastics:Study on the endoplasmic reticulum stress signaling pathway[J].Food and Chemical Toxicology,2023,172:113577. [59] 李幸幸,刘 俊,徐忠诚,等.复方丹参滴丸通过调控IRE1-TRAF2-ASK1-JNK通路降低内质网应激和自噬保护血管平滑肌细胞[J].中国药理学通报,2022,38(5):776-783. LI X X,LIU J,XU Z C,et al.Fufang danshen dropping pill protect vascular smooth muscle cells by reducing endoplasmic reticulum stress and autophagy through regulating IRE1-TRAF2-ASK1-JNK pathway[J]. Chinese Pharmacological Bulletin,2022,38(5):776-783.(in Chinese) [60] 孔凡镇,韩 芳,石玉秀.内质网应激跨膜蛋白IRE1α及下游信号分子ASK1、JNK在PTSD大鼠中缝背核应答URP的分子机制[J].解剖科学进展,2018,24(1):91-96. KONG F Z,HAN F,SHI Y X.The molecular mechanism of IRE1α,ASK1 and JNK in response to unfolded protein respones in the dorsal raphe nucleus of post-traumatic stress disorder rats[J].Progress of Anatomical Sciences,2018,24(1):91-96.(in Chinese) [61] 李 铭,邹 颖,郭 寒,等.钙离子在内质网应激中的作用[J].动物医学进展,2018,39(9):112-116. LI M,ZOU Y,GUO H,et al.Effect of calcium ions on endoplasmic reticulum stress[J].Progress in Veterinary Medicine,2018,39(9):112-116.(in Chinese) [62] TIAN Y,WANG L,QIU Z Q,et al.Autophagy triggers endoplasmic reticulum stress and C/EBP homologous protein-mediated apoptosis in OGD/R-treated neurons in a caspase-12-independent manner[J]. Journal of Neurophysiology,2021,126(5):1740-1750. [63] 温静静,董玉娟,王大壮,等.Caspase12和Caspase3在内质网应激介导的HCC细胞凋亡中的作用[J].贵州医科大学学报,2022,47(2):197-202. WEN J J,DONG Y J,WANG D Z,et al.Role of Caspase12 and Caspase3 in endoplasmic reticulum stress mediated apoptosis of HCC[J].Journal of Guizhou Medical University,2022,47(2):197-202.(in Chinese) [64] GHOSH S,CHOWDHURY S,DAS A K,et al.Taurine ameliorates oxidative stress induced inflammation and ER stress mediated testicular damage in STZ-induced diabetic Wistar rats[J].Food and Chemical Toxicology,2019,124:64-80. [65] 高 磊.衰老引起的内质网应激通过小鼠睾丸间质细胞生物钟调控睾酮合成的机制研究[D].杨凌:西北农林科技大学,2019. GAO L.Mechanism of aging-mediated ER stress regulating testosterone synthesis through circadian clockwork in mouse Leydig cells[D].Yangling:Northwest A&F University,2019.(in Chinese) [66] ZHAO Y T,QI Y W,HU C Y,et al.Advanced glycation end products inhibit testosterone secretion by rat Leydig cells by inducing oxidative stress and endoplasmic reticulum stress[J].International Journal of Molecular Medicine,2016;38(2):659-665. [67] ZHANG G L,DAI D Z,ZHANG C,et al.Apocynin and raisanberine alleviate intermittent hypoxia induced abnormal StAR and 3β-HSD and low testosterone by suppressing endoplasmic reticulum stress and activated p66Shc in rat testes[J].Reproductive Toxicology (Elmsford,N.Y.),2013,36:60-70. [68] 崔艳华.褪黑素通过抑制内质网应激缓解小鼠睾丸损伤和精原干细胞凋亡[D].杨凌:西北农林科技大学,2018. CUI Y H.Melatonin relieves busulfan-induced spermatogonial stem cell apoptosis of mouse testis by inhibiting endoplasmic reticulum stress[D].Yangling:Northwest A&F University,2018.(in Chinese) [69] 梁晓飞.钙离子诱导内质网应激在小鼠肺成纤维细胞凋亡中的作用[D].唐山:华北理工大学,2016. LIANG X F.Role of the emdopladmic reticulum stress induced by Ca2+in the apoptosis of mouse lung fibroblasts[D].Tangshan:North China University of Science and Technology,2016.(in Chinese) [70] 袁春阳.钙离子在微囊藻毒素-LR诱导小鼠雄性生殖细胞凋亡中的作用[D].合肥:安徽医科大学,2018. YUAN C Y.The role of calcium ion in the apoptosis of male germ cellsinduced by microcystin [D].Hefei:Anhui Medical University,2018.(in Chinese) |
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