The PERK-eIF2α signaling pathway is involved in TCDD-induced ER stress in PC12 cells

NeuroToxicology

Volumn 44, Issue , 2014, Pages 149-159

  Duan, Zhiqing ^a,b   Zhao, Jianya ^a   Fan, Xikang ^a   Tang, Cuiying ^a   Liang, Lingwei ^a   Nie, Xiaoke ^a   Liu, Jiao ^a   Wu, Qiyun ^a   Xu, Guangfei ^a  

^a NANTONG UNIVERSITY   (China)

^b AFFILIATED PEOPLE S HOSPITAL OF JIANGSU UNIVERSITY   (China)

Author keywords

EIF2 ; ER stress; PC12 cells; PERK; TCDD

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ACTIVATING TRANSCRIPTION FACTOR 6; ALPHA NAPHTHOFLAVONE; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE R; SALUBRINAL; SMALL INTERFERING RNA; CINNAMIC ACID DERIVATIVE; PERK KINASE; THIOUREA; GLUCOSE REGULATED PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 2ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ELECTRON MICROSCOPY; EMBRYO; ENDOPLASMIC RETICULUM STRESS; IMMUNOFLUORESCENCE; NEUROTOXICITY; NONHUMAN; PC12 CELL LINE; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; RAT; RNA TRANSLATION; TRANSMISSION ELECTRON MICROSCOPY; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; ENDOPLASMIC RETICULUM; ENZYMOLOGY; METABOLISM; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; ANIMAL CELL; ANIMAL TISSUE; CELL DEATH; FEMALE; NERVE CELL; SENSOR;

ANIMALS; APOPTOSIS; CINNAMATES; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; PC12 CELLS; RATS; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN; THIOUREA; UNFOLDED PROTEIN RESPONSE;

EID: 84903709270     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.06.005     Document Type: Article

References (51)

1. Abcouwer S.F., Marjon P.L., Loper R.K., Vander Jagt D.L. Response of VEGF expression to amino acid deprivation and inducers of endoplasmic reticulum stress. Invest Ophthalmol Vis Sci 2002, 43:2791-2798.
2. Baumann O., Walz B. Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 2001, 205:149-214.
3. Bernales S., Soto M.M., McCullagh E. Unfolded protein stress in the endoplasmic reticulum and mitochondria: a role in neurodegeneration. Front Aging Neurosci 2012, 4:5.
4. Bertolotti A., Zhang Y., Hendershot L.M., Harding H.P., Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000, 2:326-332.
5. Busciglio J., Yankner B.A. Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 1995, 378:776-779.
6. Butler R.A., Kelley M.L., Olberding K.E., Gardner G.R., Van Beneden R.J. Aryl hydrocarbon receptor (AhR)-independent effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on softshell clam (Mya arenaria) reproductive tissue. Comp Biochem Physiol Toxicol Pharmacol 2004, 138:375-381.
7. Chen J.C., Wu M.L., Huang K.C., Lin W.W. HMG-CoA reductase inhibitors activate the unfolded protein response and induce cytoprotective GRP78 expression. Cardiovasc Res 2008, 80(1):138-150.
8. Cribb A.E., Peyrou M., Muruganandan S., Schneider L. The endoplasmic reticulum in xenobiotic toxicity. Drug Metab Rev 2005, 37:405-442.
9. Giacomini S.M., Hou L., Bertazzi P.A., Baccarelli A. Dioxin effects on neonatal and infant thyroid function: routes of perinatal exposure, mechanisms of action and evidence from epidemiology studies. Int Arch Occup Environ Health 2006, 79:396-404.
10. Gies A., Neumeier G., Rappolder M., Konietzka R. Risk assessment of dioxins and dioxin-like PCBs in food - comments by the German Federal Environmental Agency. Chemosphere 2007, 67:S344-S349.
11. Greene L.A., Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 1976, 73:2424-2428.
12. Guo J., Sartor M., Karyala S., Medvedovic M., Kann S., Puga A., et al. Expression of genes in the TGF-beta signaling pathway is significantly deregulated in smooth muscle cells from aorta of aryl hydrocarbon receptor knockout mice. Toxicol Appl Pharmacol 2004, 194:79-89.
13. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000, 6(5):1099-1108.
14. Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 2012, 13:89-102.
15. Huff J., Lucier G., Tritscher A. Carcinogenicity of TCDD: experimental, mechanistic, and epidemiologic evidence. Annu Rev Pharmacol Toxicol 1994, 34:343-372.
16. Jacobson J.L., Jacobson S.W. Evidence for PCBs as neurodevelopmental toxicants in humans. Neurotoxicology 1997, 18:415-424.
17. Jacobson J.L., Jacobson S.W. Teratogen update: polychlorinated biphenyls. Teratology 1997, 55:338-347.
18. Jung J.E., Moon J.Y., Ghil S.H., Yoo B.S. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) inhibits neurite outgrowth in differentiating human SH-SY5Y neuroblastoma cells. Toxicol Lett 2009, 188:153-156.
19. Kakeyama M., Tohyama C. Developmental neurotoxicity of dioxin and its related compounds. Ind Health 2003, 41:215-230.
20. Kerger B.D., Leung H.W., Scott P., Paustenbach D.J., Needham L.L., Patterson D.G., et al. Age- and concentration-dependent elimination half-life of 2,3,7,8-tetrachlorodibenzo-p-dioxin in Seveso children. Environ Health Perspect 2006, 114:1596-1602.
21. Kim H., Tu H.C., Ren D., Takeuchi O., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol Cell 2009, 36(3):487-499.
22. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Disc 2008, 7:1013-1030.
23. Kwon Y.I., Yeon J.D., Oh S.M., Chung K.H. Protective effects of ursodeoxycholic acid against 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced testicular damage in mice. Toxicol Appl Pharmacol 2004, 194(3):239-247.
24. Lin C.H., Juan S.H., Wang C.Y., Sun Y.Y., Chou C.M., Chang S.F., et al. Neuronal activity enhances aryl hydrocarbon receptor-mediated gene expression and dioxin neurotoxicity in cortical neurons. J Neurochem 2008, 104:1415-1429.
25. Lindholm D., Wootz H., Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006, 13:385-392.
26. Lucier G.W., Portier C.J., Gallo M.A. Receptor mechanisms and dose-response models for the effects of dioxins. Environm Health Perspect 1993, 101:36-44.
27. Morales-Hernandez A., Sanchez-Martin F.J., Hortigon-Vinagre M.P., Henao F., Merino J.M. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis by disruption of intracellular calcium homeostasis in human neuronal cell line SHSY5Y. Apoptosis 2012, 17:1170-1181.
28. Needham L.L., Gerthoux P.M., Patterson D.G., Brambilla P., Turner W.E., Beretta C., et al. Serum dioxin levels in Seveso, Italy, population in 1976. Teratog Carcinog Mutagen 1997, 17:225-240.
29. Nishijo M., Kuriwaki J., Hori E., Tawara K., Nakagawa H., Nishijo H. Effects of maternal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin on fetal brain growth and motor and behavioral development in offspring rats. Toxicol Lett 2007, 173:41-47.
30. Nishiumi S., Yabushita Y., Furuyashiki T., Fukuda I., Ashida H. Involvement of SREBPs in 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced disruption of lipid metabolism in male guinea pig. Toxicol Appl Pharmacol 2008, 229(3):281-289.
31. Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H.P., Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 2003, 22(5):1180-1187.
32. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004, 11:381-389.
33. Pelclova D., Urban P., Preiss J., Lukas E., Fenclova Z., Navratil T., et al. Adverse health effects in humans exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Rev Environ Health 2006, 21:119-138.
34. Sanchez-Martin F.J., Fernandez-Salguero P.M., Merino J.M. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis in neural growth factor (NGF)-differentiated pheochromocytoma PC12 cells. Neurotoxicology 2010, 31:267-276.
35. Sanchez-Martin F.J., Fernandez-Salguero P.M., Merino J.M. Aryl hydrocarbon receptor-dependent induction of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin in cerebellar granule cells from mouse. J Neurochem 2011, 118:153-162.
36. Sanfeliu C., Cristofol R., Toran N., Rodriguez-Farre E., Kim S.U. Use of human central nervous system cell cultures in neurotoxicity testing. Toxicol In Vitro 1999, 13:753-759.
37. Schantz S.L., Bowman R.E. Learning in monkeys exposed perinatally to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Neurotoxicol Teratol 1989, 11:13-19.
38. Schantz S.L., Ferguson S.A., Bowman R.E. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on behavior of monkeys in peer groups. Neurotoxicol Teratol 1992, 14:433-446.
39. 2+ depletion suppresses protein synthesis and induces activation-enhanced cell death in mast cells. J Biol Chem 2002, 277:13812-13820.
40. Sul D., Kim H.S., Cho E.K., Lee M., Jung W.W., Hwang K.W., et al. 2,3,7,8-TCDD neurotoxicity in neuroblastoma cells is caused by increased oxidative stress, intracellular calcium levels, and tau phosphorylation. Toxicology 2009, 255:65-71.
41. Tai P.T., Nishijo M., Kido T., Nakagawa H., Maruzeni S., Naganuma R., et al. Dioxin concentrations in breast milk of Vietnamese nursing mothers: a survey four decades after the herbicide spraying. Environ Sci Technol 2011, 45:6625-6632.
42. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649.
43. Wan C., Chen J., Hu B., Zou H., Li A., Guo A., et al. Downregulation of UBE2Q1 is associated with neuronal apoptosis in rat brain cortex following traumatic brain injury. J Neurosci Res 2014, 92:1-12.
44. Wan C., Jiang J., Mao H., Cao J., Wu X., Cui G. Involvement of upregulated p53-induced death domain protein (PIDD) in neuronal apoptosis after rat traumatic brain injury. J Mol Neurosci 2013, 51:695-702.
45. Xie H.Q., Xu H.M., Fu H.L., Hu Q., Tian W.J., Pei X.H., et al. AhR-mediated effects of dioxin on neuronal acetylcholinesterase expression in vitro. Environ Health Perspect 2013, 121:613-618.
46. Xu G., Duan Z., Chen G., Nie X., Liu J., Zhang Y., Li Y., Wan C., Jiang J. Role of mitogen-activated protein kinase cascades in 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced apoptosis in neuronal pheochromocytoma cells. Hum Exp Toxicol 2013.
47. Yang D., Li Y., Yuan X., Matoney L., Yan B. Regulation of rat carboxylesterase expression by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): a dose-dependent decrease in mRNA levels but a biphasic change in protein levels and activity. Toxicol Sci 2001, 64:20-27.
48. Yang Y., Chen X., Ding F., Zhang P., Liu J., Gu X. Biocompatibility evaluation of silk fibroin with peripheral nerve tissues and cells in vitro. Biomaterials 2007, 28:1643-1652.
49. Yuan T., Luo B.L., Wei T.H., Zhang L., He B.M., Niu R.C. Salubrinal protects against cigarette smoke extract-induced HBEpC apoptosis likely via regulating the activity of PERK-eIF2alpha signaling pathway. Arch Med Res 2012, 43:522-529.
50. Zhou J., Liu C.Y., Back S.H., Clark R.L., Peisach D., Xu Z., et al. The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response. Proc Natl Acad Sci U S A 2006, 103:14343-14348.
51. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12:982-995.