Isoflavones Induce BEX2-Dependent Autophagy to Prevent ATR-Induced Neurotoxicity in SH-SY5Y Cells

Cellular Physiology and Biochemistry

Volumn 43, Issue 5, 2018, Pages 1866-1879

  Li, Peng ^a   Ma, Kun ^a   Wu, Hao Yu ^a   Wu, Yan Ping ^a   Li, Bai Xiang ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Atrazine; Autophagy; Brain expressed X linked 2; Isoflavones; Neurotoxicity; Prevention

Indexed keywords

3 METHYLADENINE; ATRAZINE; BRAIN EXPRESSED X LINKED 2 PROTEIN; BRAIN PROTEIN; CHOLECYSTOKININ OCTAPEPTIDE; CURCUMIN; ISOFLAVONE DERIVATIVE; POLYPHENOL DERIVATIVE; QUERCETIN; RESVERATROL; SEQUESTOSOME 1; SMALL INTERFERING RNA; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; BEX2 PROTEIN, HUMAN; NERVE PROTEIN; POLYPHENOL; STILBENE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CELL DEATH; CELL POPULATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MTOR SIGNALING; NEUROPROTECTION; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SH-SY5Y CELL LINE; WESTERN BLOTTING; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

APOPTOSIS; ATRAZINE; AUTOPHAGY; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL SURVIVAL; CURCUMIN; FLOW CYTOMETRY; HUMANS; ISOFLAVONES; NERVE TISSUE PROTEINS; POLYPHENOLS; QUERCETIN; REAL-TIME POLYMERASE CHAIN REACTION; SINCALIDE; STILBENES; TOR SERINE-THREONINE KINASES; TYROSINE 3-MONOOXYGENASE;

EID: 85031801566     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000484075     Document Type: Article

References (53)

1. Still Poisoning the Well: Atrazine Continues to Contaminate Surface Water and Drinking Water in the United States. 2017/8/12. http://adams.vtls.com:9020/vital/access/manager/Repository/kcpl:9699
2. Decision Documents for Atrazine. 2017/8/12. http://www.epa.gov/opp00001/chem-search/reg-actions/ reregistration/red-PC-080803-080801-Apr-080806.pdf
3. Basic Information about Atrazine in Drinking Water. 2017/8/12. http://water.epa.gov/drink/ contaminants/basicinformation/atrazine.cfm
4. USDA National Agricultural Statistics Service. 2017/8/12. http://quickstats.nass.usda. gov/?sectordesc=ENVIRONMENTAL
5. Adgate JL, Barr DB, Clayton CA, Eberly LE, Freeman N, Lioy PJ, Needham LL, Pellizzari ED, Quackenboss JJ, Roy, A: Measurement of children's exposure to pesticides: analysis of urinary metabolite levels in a probability-based sample. Environ Health Perspect 2001;109:583-590.
6. Bakke B, De Roos AJ, Barr DB, Stewart PA, Blair A, Freeman LB, Lynch CF, Allen RH, Alavanja MC, Vermeulen R: Exposure to atrazine and selected non-persistent pesticides among corn farmers during a growing season. J Expo Sci Environ Epidemiol 2009;19:544-554.
7. Curwin BD, Hein MJ, Sanderson WT, Striley C, Heederik D, Kromhout H, Reynolds SJ, Alavanja MC: Urinary pesticide concentrations among children, mothers and fathers living in farm and non-farm households in iowa. Ann Occup Hyg 2007;51:53-65.
8. Jablonowski ND, Schaffer A, Burauel P: Still present after all these years: persistence plus potential toxicity raise questions about the use of atrazine. Environ Sci Pollut Res Int 2011;18:328-331.
9. Konstantinou IK, Hela DG, Albanis TA. The status of pesticide pollution in surface waters (rivers and lakes) of Greece. Part I. Review on occurrence and levels. Environ Pollut 2006;141:555-570.
10. Campos-Pereira FD, Oliveira CA, Pigoso AA, Silva-Zacarin EC, Barbieri R, Spatti EF, Marin-Morales MA, Severi-Aguiar GD: Early cytotoxic and genotoxic effects of atrazine on Wistar rat liver: a morphological, immunohistochemical, biochemical, and molecular study. Ecotoxicol Environ Saf 2012;78:170-177.
11. Foradori CD, Hinds LR, Quihuis AM, Lacagnina AF, Breckenridge CB, Handa RJ: The differential effect of atrazine on luteinizing hormone release in adrenalectomized adult female Wistar rats. Biol Reprod 2011;85:684-689.
12. Foradori CD, Zimmerman AD, Hinds LR, Zuloaga KL, Breckenridge CB, Handa RJ: Atrazine inhibits pulsatile gonadotropin-releasing hormone (GnRH) release without altering GnRH messenger RNA or protein levels in the female rat. Biol Reprod 2013;88:9.
13. Liu Z, Fu Z, Jin Y: Immunotoxic effects of atrazine and its main metabolites at environmental relevant concentrations on larval zebrafish (Danio rerio). Chemosphere 2017;166:212-220.
14. Rayner JL, Fenton SE: Atrazine: an environmental endocrine disruptor that alters mammary gland development and tumor susceptibility; in Environment and breast cancer. Springer, 2011, pp 167-183.
15. Lin Z, Dodd CA, Xiao S, Krishna S, Ye X, Filipov NM: Gestational and lactational exposure to atrazine via the drinking water causes specific behavioral deficits and selectively alters monoaminergic systems in C57BL/6 mouse dams, juvenile and adult offspring. Toxicol Sci 2014;141:90-102.
16. Pogrmic-Majkic K, Fa S, Samardzija D, Hrubik J, Kaisarevic S, Andric N: Atrazine activates multiple signaling pathways enhancing the rapid hCG-induced androgenesis in rat Leydig cells. Toxicology 2016;368-369:37- 45.
17. Wang H, Mu S, Zhang F, Wang H, Liu H, Zhang H, Kang X. Effects of Atrazine on the Development of Neural System of Zebrafish, Danio rerio. BioMed Res Int 2015;2015:976068.
18. Bardullas U, Giordano M, Rodriguez VM: Chronic atrazine exposure causes disruption of the spontaneous locomotor activity and alters the striatal dopaminergic system of the male Sprague-Dawley rat. Neurotoxicol Teratol 2011;33:263-272.
19. Bardullas U, Giordano M, Rodriguez VM: Atrazine is primarily responsible for the toxicity of long-term exposure to a combination of atrazine and inorganic arsenic in the nigrostriatal system of the albino rat. Neurotoxicol Teratol 2013;40:59-66.
20. Brown TP, Rumsby PC, Capleton AC, Rushton L, Levy LS: Pesticides and Parkinson's disease - Is there a link? Environ Health Perspect 2005;114:156-164.
21. Hines CJ, Deddens JA, Lu C, Fenske R, Striley CA: Mixed-effect models for evaluating multiple measures of atrazine exposure among custom applicators. J Occup Environ Hyg 2006;3:274-283.
22. Priyadarshi A, Khuder SA, Schaub EA, Shrivastava S: A meta-analysis of Parkinson's disease and exposure to pesticides. Neurotoxicology 2000;21:435-440.
23. Rodriguez VM, Limon-Pacheco JH, Mendoza-Trejo MS, Gonzalez-Gallardo A, Hernandez-Plata I, Giordano M: Repeated exposure to the herbicide atrazine alters locomotor activity and the nigrostriatal dopaminergic system of the albino rat. Neurotoxicology 2013;34:82-94.
24. Cooper JR, Bloom FE, Roth RH: The Biochemical Basis of Neuropharmacology. USA, Oxford University Press, 2003.
25. Lin Z, Dodd CA, Filipov NM: Short-term atrazine exposure causes behavioral deficits and disrupts monoaminergic systems in male C57BL/6 mice. Neurotoxicol Teratol 2013;39:26-35.
26. Beal MF: Experimental models of Parkinson's disease. Nat Rev Neurosci 2001;2:325-324.
27. Ma K, Wu H-Y, Zhang B, He X, Li B-X: Neurotoxicity effects of atrazine-induced SH-SY5Y human dopaminergic neuroblastoma cells via microglial activation. Mol BioSyst 2015;11:2915-2924.
28. Abarikwu SO, Farombi EO, Kashyap MP, Pant AB: Kolaviron protects apoptotic cell death in PC12 cells exposed to atrazine. Free Radic Res 2011;45:1061-1073.
29. Björklund A, Dunnett SB: Dopamine neuron systems in the brain: an update. Trends Neurosci 2007;30:194-202.
30. Filipov NM, Stewart MA, Carr RL, Sistrunk SC: Dopaminergic toxicity of the herbicide atrazine in rat striatal slices. Toxicology 2007;232:68-78.
31. Levine B, Klionsky DJ: Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004;6:463-477.
32. Thayyullathil F, Rahman A, Pallichankandy S, Patel M, Galadari S: ROS-dependent prostate apoptosis response-4 (Par-4) up-regulation and ceramide generation are the prime signaling events associated with curcumin-induced autophagic cell death in human malignant glioma. FEBS Open Bio 2014;4:763-776.
33. Alvarez E, Zhou W, Witta SE, Freed CR: Characterization of the Bex gene family in humans, mice, and rats. Gene 2005;357:18-28.
34. Foltz G, Ryu G-Y, Yoon J-G, Nelson T, Fahey J, Frakes A, Lee H, Field L, Zander K, Sibenaller Z: Genome-wide analysis of epigenetic silencing identifies BEX1 and BEX2 as candidate tumor suppressor genes in malignant glioma. Cancer Res 2006;66:6665-6674.
35. Lin C-Y, Tsai C-W: Carnosic acid attenuates 6-hydroxydopamine-induced neurotoxicity in SH-SY5Y cells by inducing autophagy through an enhanced interaction of parkin and Beclin1. Mol Neurobiol 2017;54:2813- 2822.
36. Lin T-K, Chen S-D, Chuang Y-C, Lin H-Y, Huang C-R, Chuang J-H, Wang P-W, Huang S-T, Tiao M-M, Chen J-B: Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy. Int J Mol Sci 2014;15:1625-1646.
37. Song X-Y, Li J-N, Wu Y-P, Zhang B, Li B-X: Atrazine causes autophagy-and apoptosis-related neurodegenerative effects in dopaminergic neurons in the rat nigrostriatal dopaminergic system. Int J Mol Sci 2015;16:13490-13506.
38. Choi AM, Ryter SW, Levine B: Autophagy in human health and disease. N Engl J Med 2013;368:651-662.
39. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Øvervatn A, Stenmark H, Johansen T: p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005;171:603-614.
40. De Lella Ezcurra AL, Chertoff M, Ferrari C, Graciarena M, Pitossi F: Chronic expression of low levels of tumor necrosis factor-α in the substantia nigra elicits progressive neurodegeneration, delayed motor symptoms and microglia/macrophage activation. Neurobiol Dis 2010;37:630-640.
41. Kim JY, Cho TJ, Woo BH, Choi KU, Lee CH, Ryu MH, Park HR: Curcumin-induced autophagy contributes to the decreased survival of oral cancer cells. Arch Oral Biol 2012;57:1018-1025.
42. Zoncu R, Sabatini DM, Efeyan A: mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011;12:21-35.
43. Liu Q, Xu C, Kirubakaran S, Zhang X, Hur W, Liu Y, Kwiatkowski NP, Wang J, Westover KD, Gao P: Characterization of Torin2, an ATP-competitive inhibitor of mTOR, ATM, and ATR. Cancer Res 2013;73:2574-2586.
44. Chen D, Zhang Z, Yao H, Liang Y, Xing H, Xu S: Effects of atrazine and chlorpyrifos on oxidative stress-induced autophagy in the immune organs of common carp (Cyprinus carpio L.). Fish Shellfish Immunol 2015;44:12-20.
45. Naderi A, Liu J, Bennett IC: BEX2 regulates mitochondrial apoptosis and G1 cell cycle in breast cancer. Int J Cancer 2010;126:1596-1610.
46. Hu Z, Wang Y, Huang F, Chen R, Li C, Wang F, Goto J, Kwiatkowski DJ, Wdzieczak-Bakala J, Tu P: Brain-expressed X-linked 2 is pivotal for hyperactive mechanistic target of Rapamycin (mTOR)-mediated tumorigenesis. J Biol Chem 2015;290:25756-25765.
47. Dong L, Ni J, Hu W, Yu C, Li H: Upregulation of long non-coding RNA plncRNA-1 promotes metastasis and induces epithelial-mesenchymal transition in hepatocellular carcinoma. Cell Physiol Biochem 2016;38:836-846.
48. Li C, Chen J, Zhang K, Feng B, Wang R, Chen L: Progress and prospects of long noncoding RNAs (lncRNAs) in hepatocellular carcinoma. Cell Physiol Biochem 2015;36:423-434.
49. Li J, Wang X, Tang J, Jiang R, Zhang W, Ji J, Sun B. HULC and Linc00152 act as novel biomarkers in predicting diagnosis of hepatocellular carcinoma. Cell Physiol Biochem 2015;37:687-696.
50. Pan Y, Li C, Chen J, Zhang K, Chu X, Wang R, Chen L: The emerging roles of long noncoding RNA ROR (lincRNA-ROR) and its possible mechanisms in human cancers. Cell Physiol Biochem 2016;40:219-229.
51. Wang F, Yang H, Deng Z, Su Y, Fang Q, Yin Z: HOX antisense lincRNA HOXA-AS2 promotes tumorigenesis of hepatocellular carcinoma. Cell Physiol Biochem 2016;40:287-296.
52. Taft RJ, Pang K C, Mercer TR, Dinger M, Mattick JS: Non-coding RNAs: regulators of disease. J Pathol 2010;220:126-139.
53. Huang R, Wang X, Zhang W, Zhangyuan G, Jin K, Yu W, Xie Y, Xu X, Wang H, Sun B: Down-regulation of LncRNA DGCR5 correlates with poor prognosis in hepatocellular carcinoma. Cell Physiol Biochem 2016;40:707-715.