The role of Nrf2 in protection against Pb-induced oxidative stress and apoptosis in SH-SY5Y cells

Food and Chemical Toxicology

Volumn 86, Issue , 2015, Pages 191-201

  Ye, Fang ^a   Li, Xiaoyi ^a   Li, Lili ^a   Lyu, Ling ^a   Yuan, Jing ^a   Chen, Jun ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Antioxidant gene; Lead; Neurotoxicity; Nrf2; Oxidative stress

Indexed keywords

ACETYLCYSTEINE; DIPHENYLIODONIUM SALT; GLUTAMYLCYSTEINE LIGASE CATALYTIC UNIT; GLUTAMYLCYSTEINE LIGASE MODULATORY UNIT; GLUTATHIONE TRANSFERASE A1; HEME OXYGENASE 1; LEAD ACETATE; LIGASE; MESSENGER RNA; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE QUINONE OXIDOREDUCTASE 1; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; NFE2L2 PROTEIN, HUMAN; ORGANOMETALLIC COMPOUND;

ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; BIOACCUMULATION; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA TRANSCRIPTION; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; GENE EXPRESSION REGULATION; GENE SILENCING; HUMANS; NF-E2-RELATED FACTOR 2; ORGANOMETALLIC COMPOUNDS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER;

EID: 84945942085     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2015.10.009     Document Type: Article

References (52)

1. Ansari M.A., Maayah Z.H., Bakheet S.A., El-Kadi A.O., Korashy H.M. The role of aryl hydrocarbon receptor signaling pathway in cardiotoxicity of acute lead intoxication in vivo and in vitro rat model. Toxicology 2013, 306:40-49.
2. Baranowska-Bosiacka I., Struzynska L., Gutowska I., Machalinska A., Kolasa A., Klos P., Czapski G.A., Kurzawski M., Prokopowicz A., Marchlewicz M., Safranow K., Machalinski B., Wiszniewska B., Chlubek D. Perinatal exposure to lead induces morphological, ultrastructural and molecular alterations in the hippocampus. Toxicology 2013, 303:187-200.
3. Basha M.R., Wei W., Brydie M., Razmiafshari M., Zawia N.H. Lead-induced developmental perturbations in hippocampal Sp1 DNA-binding are prevented by zinc supplementation: in vivo evidence for Pb and Zn competition. Int. J. Dev. Neurosci. Off. J. Int. Soc. Dev. Neurosci. 2003, 21:1-12.
4. Bleecker M.L., Ford D.P., Lindgren K.N., Hoese V.M., Walsh K.S., Vaughan C.G. Differential effects of lead exposure on components of verbal memory. Occup. Environ. Med. 2005, 62:181-187.
5. Bokara K.K., Brown E., McCormick R., Yallapragada P.R., Rajanna S., Bettaiya R. Lead-induced increase in antioxidant enzymes and lipid peroxidation products in developing rat brain. Biometals Int. J. Role Metal Ions Biol. Biochem. Med. 2008, 21:9-16.
6. Cheng X., Siow R.C., Mann G.E. Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxid. Redox Signal. 2011, 14:469-487.
7. Chetty C.S., Reddy G.R., Murthy K.S., Johnson J., Sajwan K., Desaiah D. Perinatal lead exposure alters the expression of neuronal nitric oxide synthase in rat brain. Int. J. Toxicol. 2001, 20:113-120.
8. Chetty C.S., Vemuri M.C., Campbell K., Suresh C. Lead-induced cell death of human neuroblastoma cells involves GSH deprivation. Cell. Mol. Biol. Lett. 2005, 10:413-423.
9. Chetty C.S., Vemuri M.C., Reddy G.R., Suresh C. Protective effect of 17-beta-estradiol in human neurocellular models of lead exposure. Neurotoxicology 2007, 28:396-401.
10. Cordova E.J., Valenzuela O.L., Sanchez-Pena L.C., Escamilla-Guerrero G., Hernandez-Zavala A., Orozco L., Del Razo L.M. Nuclear factor erythroid 2-related factor gene variants and susceptibility of arsenic-related skin lesions. Hum. Exp. Toxicol. 2014, 33:582-589.
11. Devi S.S., Biswas A.R., Biswas R.A., Vinayagamoorthy N., Krishnamurthi K., Shinde V.M., Hengstler J.G., Hermes M., Chakrabarti T. Heavy metal status and oxidative stress in diesel engine tuning workers of central Indian population. J. Occup. Environ. Med./Am. Coll. Occup. Environ. Med. 2007, 49:1228-1234.
12. Ercal N., Gurer-Orhan H., Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr. Top. Med. Chem. 2001, 1:529-539.
13. Flora S.J., Pande M., Kannan G.M., Mehta A. Lead induced oxidative stress and its recovery following co-administration of melatonin or N-acetylcysteine during chelation with succimer in male rats. Cell. Mol. Biol. 2004, 50. Online Pub, OL543-551.
14. Flora S.J., Pande M., Mehta A. Beneficial effect of combined administration of some naturally occurring antioxidants (vitamins) and thiol chelators in the treatment of chronic lead intoxication. Chem. Biol. Interact. 2003, 145:267-280.
15. Garza A., Vega R., Soto E. Cellular mechanisms of lead neurotoxicity. Med. Sci. Monit. 2006, 12:RA57-65.
16. He L., Poblenz A.T., Medrano C.J., Fox D.A. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J. Biol. Chem. 2000, 275:12175-12184.
17. Hsu P.C., Guo Y.L. Antioxidant nutrients and lead toxicity. Toxicology 2002, 180:33-44.
18. Hu F., Xu L., Liu Z.H., Ge M.M., Ruan D.Y., Wang H.L. Developmental lead exposure alters synaptogenesis through inhibiting canonical Wnt pathway in vivo and in vitro. PLoS One 2014, 9:e101894.
19. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
20. Keum Y.S., Chang P.P., Kwon K.H., Yuan X., Li W., Hu L., Kong A.N. 3-Morpholinopropyl isothiocyanate is a novel synthetic isothiocyanate that strongly induces the antioxidant response element-dependent Nrf2-mediated detoxifying/antioxidant enzymes in vitro and in vivo. Carcinogenesis 2008, 29:594-599.
21. Kobayashi M., Yamamoto M. Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Redox Signal. 2005, 7:385-394.
22. Korashy H.M., El-Kadi A.O. Transcriptional regulation of the NAD(P)H:quinone oxidoreductase 1 and glutathione S-transferase ya genes by mercury, lead, and copper. Drug Metab. Dispos. Biol. Fate Chem. 2006, 34:152-165.
23. Korashy H.M., El-Kadi A.O. Transcriptional and posttranslational mechanisms modulating the expression of the cytochrome P450 1A1 gene by lead in HepG2 cells: a role of heme oxygenase. Toxicology 2012, 291:113-121.
24. Lee J.M., Li J., Johnson D.A., Stein T.D., Kraft A.D., Calkins M.J., Jakel R.J., Johnson J.A. Nrf2, a multi-organ protector?. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2005, 19:1061-1066.
25. Li W., Kong A.N. Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 2009, 48:91-104.
26. Lidsky T.I., Schneider J.S. Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain J. Neurol. 2003, 126:5-19.
27. Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 2013, 53:401-426.
28. Maher J.M., Dieter M.Z., Aleksunes L.M., Slitt A.L., Guo G., Tanaka Y., Scheffer G.L., Chan J.Y., Manautou J.E., Chen Y., Dalton T.P., Yamamoto M., Klaassen C.D. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 2007, 46:1597-1610.
29. Marchlewicz M., Baranowska-Bosiacka I., Kolasa A., Kondarewicz A., Chlubek D., Wiszniewska B. Disturbances of energetic metabolism in rat epididymal epithelial cells as a consequence of chronic lead intoxication. Biometals Int. J. Role Metal Ions Biol. Biochem. Med. 2009, 22:877-887.
30. Martin D., Rojo A.I., Salinas M., Diaz R., Gallardo G., Alam J., De Galarreta C.M., Cuadrado A. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem. 2004, 279:8919-8929.
31. Motohashi H., Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med. 2004, 10:549-557.
32. Needleman H. Lead poisoning. Annu. Rev. Med. 2004, 55:209-222.
33. Nguyen T., Sherratt P.J., Huang H.C., Yang C.S., Pickett C.B. Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J. Biol. Chem. 2003, 278:4536-4541.
34. Nioi P., McMahon M., Itoh K., Yamamoto M., Hayes J.D. Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 2003, 374:337-348.
35. Patra R.C., Swarup D., Dwivedi S.K. Antioxidant effects of alpha tocopherol, ascorbic acid and L-methionine on lead induced oxidative stress to the liver, kidney and brain in rats. Toxicology 2001, 162:81-88.
36. Patrick L. Lead toxicity part II: the role of free radical damage and the use of antioxidants in the pathology and treatment of lead toxicity. Altern. Med. Rev. J. Clin. Ther. 2006, 11:114-127.
37. Prins J.M., Park S., Lurie D.I. Decreased expression of the voltage-dependent anion channel in differentiated PC-12 and SH-SY5Y cells following low-level Pb exposure. Toxicol. Sci. Off. J. Soc. Toxicol. 2010, 113:169-176.
38. Rangasamy T., Guo J., Mitzner W.A., Roman J., Singh A., Fryer A.D., Yamamoto M., Kensler T.W., Tuder R.M., Georas S.N., Biswal S. Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J. Exp. Med. 2005, 202:47-59.
39. Rosse T., Olivier R., Monney L., Rager M., Conus S., Fellay I., Jansen B., Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 1998, 391:496-499.
40. Rubio V., Zhang J., Valverde M., Rojas E., Shi Z.Z. Essential role of Nrf2 in protection against hydroquinone- and benzoquinone-induced cytotoxicity. Toxicol. In vitro Int. J. Publ. Assoc. BIBRA 2011, 25:521-529.
41. Rushworth S.A., MacEwan D.J., O'Connell M.A. Lipopolysaccharide-induced expression of NAD(P)H:quinone oxidoreductase 1 and heme oxygenase-1 protects against excessive inflammatory responses in human monocytes. J. Immunol. 2008, 181:6730-6737.
42. Rushworth S.A., Shah S., MacEwan D.J. TNF mediates the sustained activation of Nrf2 in human monocytes. J. Immunol. 2011, 187:702-707.
43. Saxena G., Pathak U., Flora S.J. Beneficial role of monoesters of meso-2,3-dimercaptosuccinic acid in the mobilization of lead and recovery of tissue oxidative injury in rats. Toxicology 2005, 214:39-56.
44. Seddik L., Bah T.M., Aoues A., Slimani M., Benderdour M. Elucidation of mechanisms underlying the protective effects of olive leaf extract against lead-induced neurotoxicity in Wistar rats. J. Toxicol. Sci. 2011, 36:797-809.
45. Shalan M.G., Mostafa M.S., Hassouna M.M., El-Nabi S.E., El-Refaie A. Amelioration of lead toxicity on rat liver with Vitamin C and silymarin supplements. Toxicology 2005, 206:1-15.
46. Son Y.O., Pratheeshkumar P., Roy R.V., Hitron J.A., Wang L., Zhang Z., Shi X. Nrf2/p62 signaling in apoptosis resistance and its role in cadmium-induced carcinogenesis. J. Biol. Chem. 2014, 289:28660-28675.
47. Talalay P., Dinkova-Kostova A.T., Holtzclaw W.D. Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv. Enzym. Regul. 2003, 43:121-134.
48. Vaziri N.D., Lin C.Y., Farmand F., Sindhu R.K. Superoxide dismutase, catalase, glutathione peroxidase and NADPH oxidase in lead-induced hypertension. Kidney Int. 2003, 63:186-194.
49. Wang Y., Fang J., Huang S., Chen L., Fan G., Wang C. The chronic effects of low lead level on the expressions of Nrf2 and Mrp1 of the testes in the rats. Environ. Toxicol. Pharmacol. 2013, 35:109-116.
50. Wilson M.A., Johnston M.V., Goldstein G.W., Blue M.E. Neonatal lead exposure impairs development of rodent barrel field cortex. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5540-5545.
51. Wolter K.G., Hsu Y.T., Smith C.L., Nechushtan A., Xi X.G., Youle R.J. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 1997, 139:1281-1292.
52. Xu J., Lian L.J., Wu C., Wang X.F., Fu W.Y., Xu L.H. Lead induces oxidative stress, DNA damage and alteration of p53, Bax and Bcl-2 expressions in mice. Food Chem. Toxicol. Int. J. Publ. Br. Ind. Biol. Res. Assoc. 2008, 46:1488-1494.