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2000
Volume 32, Issue 7
  • ISSN: 0929-8673
  • E-ISSN: 1875-533X

Abstract

Introduction

Methamphetamine (METH) is an illicit psychoactive substance that can damage various organs in the body, especially the nervous system. We hypothesized that expression of homocysteine-inducible endoplasmic reticulum-resident with ubiquitin-like domain member 1 (Herpud1) protein would alleviate the induction of apoptosis following METH administration.

Methods

To test this hypothesis, we analysed the changes in Herpud1 expression and apoptosis in PC12 cells under different concentrations and exposure times of METH. Moreover, we examined the effects of Herpud1 knockdown on METH-induced neuronal apoptosis. Flow cytometry and Western blot analyses were used to evaluate apoptosis levels and the expression of apoptotic markers (cleaved caspase-3) in PC12 cells following Herpud1 knockdown by synthetic small interfering RNA (siRNA).

Results

Our results showed that Herpud1 expression was upregulated in PC12 cells following METH treatment, while endoplasmic reticulum stress (ERS) and apoptosis were also increased. Conversely, Herpud1 knockdown reduced METH-induced ERS and apoptosis levels .

Conclusion

These results suggest that Herpud1 plays an essential role in METH-induced neuronal ERS and apoptosis and may represent a potential therapeutic gene target in METH-induced neurotoxicity.

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2024-01-30
2025-09-07
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References

  1. (UNODC), U.N.O.o.D.a.C., World Drug Report. 2020. Available from: https://wdr.unodc.org/wdr2020/index2020.html
  2. ZhangY. LiL. WangQ. ShenM. HanW. YangX. ChenL. MaA. ZhouZ. Simultaneous determination of metabolic and elemental markers in methamphetamine-induced hepatic injury to rats using LC-MS/MS and ICP-MS.Anal. Bioanal. Chem.2019411153361337210.1007/s00216‑019‑01810‑531119349
    [Google Scholar]
  3. SunX. WangY. XiaB. LiZ. DaiJ. QiuP. MaA. LinZ. HuangJ. WangJ. XieW.B. WangJ. Methamphetamine produces cardiac damage and apoptosis by decreasing melusin.Toxicol. Appl. Pharmacol.201937811454310.1016/j.taap.2019.03.01530904475
    [Google Scholar]
  4. OrcholskiM.E. KhurshudyanA. ShamskhouE.A. YuanK. ChenI.Y. KodaniS.D. MorisseauC. HammockB.D. HongE.M. AlexandrovaL. AlastaloT.P. BerryG. ZamanianR.T. de Jesus PerezV.A. Reduced carboxylesterase 1 is associated with endothelial injury in methamphetamine-induced pulmonary arterial hypertension.Am. J. Physiol. Lung Cell. Mol. Physiol.20173132L252L26610.1152/ajplung.00453.201628473326
    [Google Scholar]
  5. Tabatabaei MirakabadF.S. KhoramgahM.S. AbdollahifarM.A. TehraniA.S. Rezaei-TaviraniM. NiknazarS. TahmasebiniaF. MahmoudiaslG.R. KhoshsiratS. AbbaszadehH.A. NUPR1- CHOP experssion, autophagosome formation and apoptosis in the postmortem striatum of chronic methamphetamine user.J. Chem. Neuroanat.202111410194210.1016/j.jchemneu.2021.10194233675952
    [Google Scholar]
  6. MoratallaR. KhairnarA. SimolaN. GranadoN. García-MontesJ.R. PorcedduP.F. TizabiY. CostaG. MorelliM. Amphetamine-related drugs neurotoxicity in humans and in experimental animals: Main mechanisms.Prog. Neurobiol.201715514917010.1016/j.pneurobio.2015.09.01126455459
    [Google Scholar]
  7. HuX. LiZ. LinR. ShanJ. YuQ. WangR. LiaoL. YanW. WangZ. ShangL. HuangY. ZhangQ. XiongK. Guidelines for regulated cell death assays: A systematic summary, a categorical comparison, a prospective.Front. Cell Dev. Biol.2021963469010.3389/fcell.2021.63469033748119
    [Google Scholar]
  8. BowyerJ.F. TranterK.M. RobinsonB.L. HanigJ.P. FaubionM.G. SarkarS. The time course of blood brain barrier leakage and its implications on the progression of methamphetamine-induced seizures.Neurotoxicology20186913014010.1016/j.neuro.2018.09.00830282018
    [Google Scholar]
  9. BagheriM. MokriA. KhosraviA. KabirK. Effect of abstinence on depression, anxiety, and quality of life in chronic methamphetamine users in a therapeutic community.Int. J. High Risk Behav. Addict.201543e2390310.5812/ijhrba.2390326495258
    [Google Scholar]
  10. HanB. CottoJ. EtzK. EinsteinE.B. ComptonW.M. VolkowN.D. Methamphetamine overdose deaths in the us by sex and race and ethnicity.JAMA Psychiatry202178556456710.1001/jamapsychiatry.2020.432133471025
    [Google Scholar]
  11. ShaerzadehF. StreitW.J. HeysieattalabS. KhoshboueiH. Methamphetamine neurotoxicity, microglia, and neuroinflammation.J. Neuroinflammation201815134110.1186/s12974‑018‑1385‑030541633
    [Google Scholar]
  12. ShinE.J. TranH.Q. NguyenP.T. JeongJ.H. NahS.Y. JangC.G. NabeshimaT. KimH.C. Role of mitochondria in methamphetamine-induced dopaminergic neurotoxicity: Involvement in oxidative stress, neuroinflammation, and pro-apoptosis-a review.Neurochem. Res.2018431667810.1007/s11064‑017‑2318‑528589520
    [Google Scholar]
  13. YanJ. XiongK. GuoL-M. WangZ. LiS-P. WangM. YanW-T. LiuF-X. WangC-D. ZhangX-D. ChenD. RIP3/MLKL-mediated neuronal necroptosis induced by methamphetamine at 39°C.Neural Regen. Res.202015586587410.4103/1673‑5374.26890231719251
    [Google Scholar]
  14. XiongK. LiaoH. LongL. DingY. HuangJ. YanJ. Necroptosis contributes to methamphetamine-induced cytotoxicity in rat cortical neurons.Toxicol. In vitro 20163516316810.1016/j.tiv.2016.06.00227288563
    [Google Scholar]
  15. YanW.T. ZhaoW.J. HuX.M. BanX.X. NingW.Y. WanH. ZhangQ. XiongK. PANoptosis-like cell death in ischemia/reperfusion injury of retinal neurons.Neural Regen. Res.202318235736335900430
    [Google Scholar]
  16. YangY. LiZ. HuX. WanH. ZhangQ. XiaoR. XiongK. Insight into crosstalk between mitophagy and apoptosis/necroptosis: Mechanisms and clinical applications in ischemic stroke.Curr. Med. Sci.202242223724810.1007/s11596‑022‑2579‑335391618
    [Google Scholar]
  17. ChenX. Cubillos-RuizJ.R. Endoplasmic reticulum stress signals in the tumour and its microenvironment.Nat. Rev. Cancer2021212718810.1038/s41568‑020‑00312‑233214692
    [Google Scholar]
  18. OakesS.A. PapaF.R. The role of endoplasmic reticulum stress in human pathology.Annu. Rev. Pathol.201510117319410.1146/annurev‑pathol‑012513‑10464925387057
    [Google Scholar]
  19. KeR. WangY. HongS. XiaoL. Endoplasmic reticulum stress related factor IRE1α regulates TXNIP/NLRP3-mediated pyroptosis in diabetic nephropathy.Exp. Cell Res.2020396211229310.1016/j.yexcr.2020.11229332950473
    [Google Scholar]
  20. MerighiA. LossiL. Endoplasmic reticulum stress signaling and neuronal cell death.Int. J. Mol. Sci.202223231518610.3390/ijms23231518636499512
    [Google Scholar]
  21. ChenY. LiY. GuoL. HongJ. ZhaoW. HuX. ChangC. LiuW. XiongK. Bibliometric analysis of the inflammasome and pyroptosis in brain.Front. Pharmacol.20211162650210.3389/fphar.2020.62650233551822
    [Google Scholar]
  22. GuptaP. TiwariS. SinghA. PalA. MishraA. SinghS. Rivastigmine attenuates the Alzheimer’s disease related protein degradation and apoptotic neuronal death signalling.Biochem. J.202147871435145110.1042/BCJ2020075433660768
    [Google Scholar]
  23. GaoY. LuoC. YaoY. HuangJ. FuH. XiaC. YeG. YuL. HanJ. FanY. TaoL. IL-33 alleviated brain damage via anti-apoptosis, endoplasmic reticulum stress, and inflammation after epilepsy.Front. Neurosci.20201489810.3389/fnins.2020.0089832982679
    [Google Scholar]
  24. ZhuY. YuJ. GongJ. ShenJ. YeD. ChengD. XieZ. ZengJ. XuK. ShenJ. ZhouH. WengY. PanJ. ZhanR. PTP1B inhibitor alleviates deleterious microglial activation and neuronal injury after ischemic stroke by modulating the ER stress-autophagy axis via PERK signaling in microglia.Aging20211333405342710.18632/aging.20227233495405
    [Google Scholar]
  25. ShachamT. PatelC. LederkremerG.Z. PERK pathway and neurodegenerative disease: To inhibit or to activate?Biomolecules202111335410.3390/biom1103035433652720
    [Google Scholar]
  26. HayashiT. JustinovaZ. HayashiE. CormaciG. MoriT. TsaiS.Y. BarnesC. GoldbergS.R. SuT.P. Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats.J. Pharmacol. Exp. Ther.201033231054106310.1124/jpet.109.15924419940104
    [Google Scholar]
  27. BeauvaisG. AtwellK. JayanthiS. LadenheimB. CadetJ.L. Involvement of dopamine receptors in binge methamphetamine-induced activation of endoplasmic reticulum and mitochondrial stress pathways.PLoS One2011612e2894610.1371/journal.pone.002894622174933
    [Google Scholar]
  28. LiaoL. LuS. YanW. WangS. GuoL. YangY. HuangK. HuX. ZhangQ. YanJ. XiongK. The role of HSP90α in methamphetamine/hyperthermia-induced necroptosis in rat striatal neurons.Front. Pharmacol.20211271639410.3389/fphar.2021.71639434349659
    [Google Scholar]
  29. SchwarzD.S. BlowerM.D. The endoplasmic reticulum: Structure, function and response to cellular signaling.Cell. Mol. Life Sci.2016731799410.1007/s00018‑015‑2052‑626433683
    [Google Scholar]
  30. LuS. LiaoL. ZhangB. YanW. ChenL. YanH. GuoL. LuS. XiongK. YanJ. Antioxidant cascades confer neuroprotection in ethanol, morphine, and methamphetamine preconditioning.Neurochem. Int.201913110454010.1016/j.neuint.2019.10454031470038
    [Google Scholar]
  31. MustafaY.F. Harmful free radicals in aging: A narrative review of their detrimental effects on health.Indian J. Clin. Bioche2023
    [Google Scholar]
  32. HetzC. ZhangK. KaufmanR.J. Mechanisms, regulation and functions of the unfolded protein response.Nat. Rev. Mol. Cell Biol.202021842143810.1038/s41580‑020‑0250‑z32457508
    [Google Scholar]
  33. JayanthiS. DaiwileA.P. CadetJ.L. Neurotoxicity of methamphetamine: Main effects and mechanisms.Exp. Neurol.202134411379510.1016/j.expneurol.2021.11379534186102
    [Google Scholar]
  34. WongprayoonP. GovitrapongP. Melatonin protects SH-SY5Y neuronal cells against methamphetamine-induced endoplasmic reticulum stress and apoptotic cell death.Neurotox. Res.201731111010.1007/s12640‑016‑9647‑z27370255
    [Google Scholar]
  35. QieX. WenD. GuoH. XuG. LiuS. ShenQ. LiuY. ZhangW. CongB. MaC. Endoplasmic reticulum stress mediates methamphetamine-induced blood–brain barrier damage.Front. Pharmacol.2017863910.3389/fphar.2017.0063928959203
    [Google Scholar]
  36. ShahA. KumarA. Methamphetamine-mediated endoplasmic reticulum (ER) stress induces type-1 programmed cell death in astrocytes via ATF6, IRE1α and PERK pathways.Oncotarget2016729461004611910.18632/oncotarget.1002527323860
    [Google Scholar]
  37. XiongK. LongL. ZhangX. QuH. DengH. DingY. CaiJ. WangS. WangM. LiaoL. HuangJ. YiC. YanJ. Overview of long non-coding RNA and mRNA expression in response to methamphetamine treatment in vitro.Toxicol. In Vitro 20174411010.1016/j.tiv.2017.06.00928619521
    [Google Scholar]
  38. LuS. YangY. LiaoL. YanW. XiongK. YanJ. iTRAQ-based proteomic analysis of the rat striatum in response to methamphetamine preconditioning.Acta Biochim. Biophys. Sin.202153563663910.1093/abbs/gmab02433742667
    [Google Scholar]
  39. KokameK. AgarwalaK.L. KatoH. MiyataT. Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress.J. Biol. Chem.200027542328463285310.1074/jbc.M00206320010922362
    [Google Scholar]
  40. KnyM. StanderaS. Hartmann-PetersenR. KloetzelP.M. SeegerM. Herp regulates Hrd1-mediated ubiquitylation in a ubiquitin-like domain-dependent manner.J. Biol. Chem.201128675151515610.1074/jbc.M110.13455121149444
    [Google Scholar]
  41. ParedesF. ParraV. TorrealbaN. Navarro-MarquezM. GaticaD. Bravo-SaguaR. TroncosoR. PennanenC. QuirogaC. ChiongM. CaesarC. TaylorW.R. MolgóJ. San MartinA. JaimovichE. LavanderoS. HERPUD1 protects against oxidative stress-induced apoptosis through downregulation of the inositol 1,4,5-trisphosphate receptor.Free Radic. Biol. Med.20169020621810.1016/j.freeradbiomed.2015.11.02426616647
    [Google Scholar]
  42. DingW. ChenR. WuC. ChenW. ZhangH. FanX. WangH. JiY. XieL. NingX. ShenL. Increased expression of HERPUD1 involves in neuronal apoptosis after intracerebral hemorrhage.Brain Res. Bull.2017128404710.1016/j.brainresbull.2016.11.00627871950
    [Google Scholar]
  43. ChenF. WenX. LinP. ChenH. WangA. JinY. HERP depletion inhibits zearalenone-induced apoptosis through autophagy activation in mouse ovarian granulosa cells.Toxicol. Lett.201930111010.1016/j.toxlet.2018.10.02630394307
    [Google Scholar]
  44. LiuC. XuX. HuangC. ZhangL. ShangD. CaiW. WangY. Circ_002664/miR-182–5p/Herpud1 pathway importantly contributes to OGD/R-induced neuronal cell apoptosis.Mol. Cell. Probes20205310158510.1016/j.mcp.2020.10158532376213
    [Google Scholar]
  45. ZhouN. QiaoH. ZengM. YangL. ZhouY. GuanQ. Circ_002117 binds to microRNA-370 and promotes endoplasmic reticulum stress-induced apoptosis in gastric cancer.Cancer Cell Int.202020146510.1186/s12935‑020‑01493‑432999631
    [Google Scholar]
  46. MustafaY.F. Al-AbdeenS.H.Z. KhalilR.R. MohammedE.T. Novel functionalized phenyl acetate derivatives of benzo [e]-bispyrone fused hybrids: Synthesis and biological activities.Results Chem.20235100942
    [Google Scholar]
  47. GaoF. ZhangJ. NiT. LinN. LinH. LuoH. GuoH. ChiJ. Herpud1 deficiency could reduce amyloid-β40 expression and thereby suppress homocysteine-induced atherosclerosis by blocking the JNK/AP1 pathway.J. Physiol. Biochem.202076338339110.1007/s13105‑020‑00741‑532488540
    [Google Scholar]
  48. SaiX. KawamuraY. KokameK. YamaguchiH. ShiraishiH. SuzukiR. SuzukiT. KawaichiM. MiyataT. KitamuraT. De StrooperB. YanagisawaK. KomanoH. Endoplasmic reticulum stress-inducible protein, Herp, enhances presenilin-mediated generation of amyloid beta-protein.J. Biol. Chem.200227715129151292010.1074/jbc.M11237220011799129
    [Google Scholar]
  49. MiuraH. HashidaK. SudoH. AwaY. Takarada-IemataM. KokameK. TakahashiT. MatsumotoM. KitaoY. HoriO. Deletion of Herp facilitates degradation of cytosolic proteins.Genes Cells201015884385310.1111/j.1365‑2443.2010.01422.x20604806
    [Google Scholar]
  50. QuirogaC. GaticaD. ParedesF. BravoR. TroncosoR. PedrozoZ. RodriguezA.E. ToroB. ChiongM. VicencioJ.M. HetzC. LavanderoS. Herp depletion protects from protein aggregation by up-regulating autophagy.Biochim. Biophys. Acta Mol. Cell Res.20131833123295330510.1016/j.bbamcr.2013.09.00624120520
    [Google Scholar]
  51. GeorgeA.K. BeheraJ. KellyK.E. MondalN.K. RichardsonK.P. TyagiN. Exercise mitigates alcohol induced endoplasmic reticulum stress mediated cognitive impairment through atf6-herp signaling.Sci. Rep.201881515810.1038/s41598‑018‑23568‑z29581524
    [Google Scholar]
  52. WuH. WangJ. CaoM. LiangJ. WuD. GuX. KeK. Effects of homocysteine-induced endoplasmic reticulum protein on endoplasmic reticulum stress, autophagy, and neuronal apoptosis following intracerebral hemorrhage.IBRO Rep.2020920721710.1016/j.ibror.2020.08.00432984639
    [Google Scholar]
  53. ChenP.H. WuJ. XuY. DingC.K.C. MestreA.A. LinC.C. YangW.H. ChiJ.T. Zinc transporter ZIP7 is a novel determinant of ferroptosis.Cell Death Dis.202112219810.1038/s41419‑021‑03482‑533608508
    [Google Scholar]
  54. DamaseT.R. SukhovershinR. BoadaC. TaraballiF. PettigrewR.I. CookeJ.P. The limitless future of RNA therapeutics.Front. Bioeng. Biotechnol.2021962813710.3389/fbioe.2021.62813733816449
    [Google Scholar]
  55. NambudiriV.E. WidlundH.R. Small interfering RNA.J. Invest. Dermatol.2013133121410.1038/jid.2013.41124216786
    [Google Scholar]
  56. HuangE. HuangH. GuanT. LiuC. QuD. XuY. YangJ. YanL. XiongY. LiangT. WangQ. ChenL. Involvement of C/EBPβ-related signaling pathway in methamphetamine-induced neuronal autophagy and apoptosis.Toxicol. Lett.2019312112110.1016/j.toxlet.2019.05.00331059759
    [Google Scholar]
  57. XuX. HuangE. LuoB. CaiD. ZhaoX. LuoQ. JinY. ChenL. WangQ. LiuC. LinZ. XieW.B. WangH. Methamphetamine exposure triggers apoptosis and autophagy in neuronal cells by activating the C/EBPbeta-related signaling pathway.FASEB J.2018fj201701460RRR
    [Google Scholar]
  58. XuX. HuangE. TaiY. ZhaoX. ChenX. ChenC. ChenR. LiuC. LinZ. WangH. XieW.B. Nupr1 modulates methamphetamine-induced dopaminergic neuronal apoptosis and autophagy through CHOP-Trib3-mediated endoplasmic reticulum stress signaling pathway.Front. Mol. Neurosci.20171020310.3389/fnmol.2017.0020328694771
    [Google Scholar]
  59. RoufayelR. MurshidN. CDK5: Key regulator of apoptosis and cell survival.Biomedicines2019748810.3390/biomedicines704008831698798
    [Google Scholar]
  60. XiaoN. ZhangF. ZhuB. LiuC. LinZ. WangH. XieW.B. CDK5-mediated tau accumulation triggers methamphetamine-induced neuronal apoptosis via endoplasmic reticulum-associated degradation pathway.Toxicol. Lett.20182929710710.1016/j.toxlet.2018.04.02729705343
    [Google Scholar]
  61. HuangY. WangS. HuangF. ZhangQ. QinB. LiaoL. WangM. WanH. YanW. ChenD. LiuF. JiangB. JiD. XiaX. HuangJ. XiongK. c-FLIP regulates pyroptosis in retinal neurons following oxygen-glucose deprivation/recovery via a GSDMD-mediated pathway.Ann. Anat.202123515167210.1016/j.aanat.2020.15167233434657
    [Google Scholar]
  62. HuH. TianM. DingC. YuS. The C/EBP homologous protein (CHOP) transcription factor functions in endoplasmic reticulum stress-induced apoptosis and microbial infection.Front. Immunol.20199308310.3389/fimmu.2018.0308330662442
    [Google Scholar]
  63. ZhangQ. XiongK. YanW-T. YangY-D. HuX-M. NingW-Y. LiaoL-S. LuS. ZhaoW-J. Do pyroptosis, apoptosis, and necroptosis (PANoptosis) exist in cerebral ischemia? Evidence from cell and rodent studies.Neural Regen. Res.20221781761176810.4103/1673‑5374.33153935017436
    [Google Scholar]
  64. XiongK. YanW-T. LuS. YangY-D. NingW-Y. CaiY. HuX-M. ZhangQ. Research trends, hot spots and prospects for necroptosis in the field of neuroscience.Neural Regen. Res.20211681628163710.4103/1673‑5374.30303233433494
    [Google Scholar]
  65. KumarV. MaityS. ER stress-sensor proteins and ER-mitochondrial crosstalk-signaling beyond (ER) stress response.Biomolecules202111217310.3390/biom1102017333525374
    [Google Scholar]
  66. GoB.S. KimJ. YangJ.H. ChoeE.S. Psychostimulant-induced endoplasmic reticulum stress and neurodegeneration.Mol. Neurobiol.20175464041404810.1007/s12035‑016‑9969‑027314686
    [Google Scholar]
  67. KimC. KimB. Anti-cancer natural products and their bioactive compounds inducing ER stress-mediated apoptosis: A review.Nutrients2018108102110.3390/nu1008102130081573
    [Google Scholar]
  68. YaoS. TianH. MiaoC. ZhangD.W. ZhaoL. LiY. YangN. JiaoP. SangH. GuoS. WangY. QinS. D4F alleviates macrophage-derived foam cell apoptosis by inhibiting CD36 expression and ER stress-CHOP pathway.J. Lipid Res.201556483684710.1194/jlr.M05540025635126
    [Google Scholar]
  69. LinH. ZhangJ. MengL.P. NiT.J. GaoF.D. ChiJ.F. GuoH.Y. XuF.K. Impact of Herpud1 in the homocysteine-induced phenotypic switching of vascular smooth muscle cells.Zhonghua Xin Xue Guan Bing Za Zhi201947756156931365998
    [Google Scholar]
  70. ChenF. LinP. WangN. YangD. WenX. ZhouD. WangA. JinY. Herp depletion inhibits zearalenone-induced cell death in RAW 264.7 macrophages.Toxicol. In Vitro 20163211512210.1016/j.tiv.2015.12.01426723276
    [Google Scholar]
  71. LinH. PanS. MengL. ZhouC. JiangC. JiZ. ChiJ. GuoH. MicroRNA-384-mediated Herpud1 upregulation promotes angiotensin II-induced endothelial cell apoptosis.Biochem. Biophys. Res. Commun.2017488345346010.1016/j.bbrc.2017.05.03528483519
    [Google Scholar]
  72. YangL. MuY. CuiH. LiangY. SuX. MiR-9-3p augments apoptosis induced by H2O2 through down regulation of Herpud1 in glioma.PLoS One2017124e017483910.1371/journal.pone.017483928430789
    [Google Scholar]
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  • Article Type:
    Research Article
Keyword(s): apoptosis; caspase-3; ER stress; Herpud1; METH; neurotoxicity
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