Lead Intoxication Synergies of the Ethanol-Induced Toxic Responses in Neuronal Cells—PC12

Molecular Neurobiology

Volumn 52, Issue 3, 2015, Pages 1504-1520

  Kumar, V ^a,b   Tripathi, V K ^a,b   Jahan, S ^a,b   Agrawal, M ^a,b   Pandey, A ^a,b   Khanna, V K ^a,b   Pant, A B ^a,b  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b NATIONAL CHEMICAL LABORATORY   (India)

Author keywords

Ethanol; Neurotoxicity; Pb; PC12 cells

Indexed keywords

ACETYLCYSTEINE; ALCOHOL; CALCIUM ION; CASPASE 3; CASPASE 9; CYTOCHROME C; GLUTATHIONE; LEAD; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; NERVE PROTEIN;

ALCOHOL INTOXICATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; ENZYME ACTIVITY; LEAD POISONING; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE CELL; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PC12 CELL LINE; PROTEIN TRANSPORT; RAT; ANIMAL; CALCIUM SIGNALING; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION;

ACETYLCYSTEINE; ANIMALS; APOPTOSIS; CALCIUM SIGNALING; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ETHANOL; GENE EXPRESSION REGULATION; GLUTATHIONE; LEAD; LIPID PEROXIDATION; MEMBRANE POTENTIAL, MITOCHONDRIAL; NERVE TISSUE PROTEINS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PC12 CELLS; PROTEIN TRANSPORT; RATS; REACTIVE OXYGEN SPECIES;

EID: 84942833496     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8928-x     Document Type: Article

References (82)

1. Briggs D (2003) Environmental pollution and the global burden of disease. Br Med Bull 68:1–24
2. Tong S, von Schirnding YE, Prapamontol T (2000) Environmental lead exposure: a public health problem of global dimensions. Bull World Health Organ 78:1068–1077
3. Florea AM, Busselberg D (2006) Occurrence, use and potential toxic effects of metals and metal compounds. Biometals 19:419–427
4. Giordano G, Costa LG (2012) Developmental neurotoxicity: some old and new issues. ISRN Toxicol 2012:814795
5. Zheng W, Aschner M, Ghersi-Egea JF (2003) Brain barrier systems: a new frontier in metal neurotoxicological research. Toxicol Appl Pharmacol 192:1–11
6. Kolesarova A, Roychoudhury S, Slivkova J, Sirotkin A, Capcarova M, Massanyi P (2010) In vitro study on the effects of lead and mercury on porcine ovarian granulosa cells. J Environ Sci Health A Tox Hazard Subst Environ Eng 45:320–331
7. Mrugesh T, Dipa L, Manishika G (2011) Effect of lead on human erythrocytes: an in vitro study. Acta Pol Pharm 68:653–656
8. Conterato GM, Augusti PR, Somacal S, Einsfeld L, Sobieski R, Torres JR, Emanuelli T (2007) Effect of lead acetate on cytosolic thioredoxin reductase activity and oxidative stress parameters in rat kidneys. Basic Clin Pharmacol Toxicol 101:96–100
9. Dewanjee S, Sahu R, Karmakar S, Gangopadhyay M (2013) Toxic effects of lead exposure in Wistar rats: involvement of oxidative stress and the beneficial role of edible jute (Corchorus olitorius) leaves. Food Chem Toxicol 55:78–91
10. Hu H, Shih R, Rothenberg S, Schwartz BS (2007) The epidemiology of lead toxicity in adults: measuring dose and consideration of other methodologic issues. Environ Health Perspect 115:455–462
11. Lidsky TI, Schneider JS (2003) Lead neurotoxicity in children: basic mechanisms and clinical correlates. Brain 126:5–19
12. Lu X, Jin C, Yang J, Liu Q, Wu S, Li D, Guan Y, Cai Y (2013) Prenatal and lactational lead exposure enhanced oxidative stress and altered apoptosis status in offspring rats’ hippocampus. Biol Trace Elem Res 151:75–84
13. Sanders T, Liu Y, Buchner V, Tchounwou PB (2009) Neurotoxic effects and biomarkers of lead exposure: a review. Rev Environ Health 24:15–45
14. Chen L, Yang X, Jiao H, Zhao B (2003) Tea catechins protect against lead-induced ROS formation, mitochondrial dysfunction, and calcium dysregulation in PC12 cells. Chem Res Toxicol 16:1155–1161
15. Flora SJ, Saxena G, Mehta A (2007) Reversal of lead-induced neuronal apoptosis by chelation treatment in rats: role of reactive oxygen species and intracellular Ca(2+). J Pharmacol Exp Ther 322:108–116
16. He L, Poblenz AT, Medrano CJ, Fox DA (2000) Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J Biol Chem 275:12175–12184
17. Aimo L, Oteiza PI (2006) Zinc deficiency increases the susceptibility of human neuroblastoma cells to lead-induced activator protein-1 activation. Toxicol Sci 91:184–191
18. Patra RC, Rautray AK, Swarup D (2011) Oxidative stress in lead and cadmium toxicity and its amelioration. Vet Med Int 2011:457327
19. Hernandez M, Margalida A (2009) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109:837–842
20. Brust JC (2010) Ethanol and cognition: indirect effects, neurotoxicity and neuroprotection: a review. Int J Environ Res Public Health 7:1540–1557
21. Crews FT, Braun CJ, Hoplight B, Switzer RC 3rd, Knapp DJ (2000) Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcohol Clin Exp Res 24:1712–1723
22. Haorah J, Knipe B, Leibhart J, Ghorpade A, Persidsky Y (2005) Alcohol-induced oxidative stress in brain endothelial cells causes blood–brain barrier dysfunction. J Leukoc Biol 78:1223–1232
23. Singh AK, Jiang Y, Gupta S, Benlhabib E (2007) Effects of chronic ethanol drinking on the blood brain barrier and ensuing neuronal toxicity in alcohol-preferring rats subjected to intraperitoneal LPS injection. Alcohol Alcohol 42:385–399
24. Costa LG, Guizzetti M, Burry M, Oberdoerster J (2002) Developmental neurotoxicity: do similar phenotypes indicate a common mode of action? A comparison of fetal alcohol syndrome, toluene embryopathy and maternal phenylketonuria. Toxicol Lett 127:197–205
25. Goodlett CR, Horn KH, Zhou FC (2005) Alcohol teratogenesis: mechanisms of damage and strategies for intervention. Exp Biol Med (Maywood) 230:394–406
26. Mulholland PJ, Self RL, Stepanyan TD, Little HJ, Littleton JM, Prendergast MA (2005) Thiamine deficiency in the pathogenesis of chronic ethanol-associated cerebellar damage in vitro. Neuroscience 135:1129–1139
27. Kroener S, Mulholland PJ, New NN, Gass JT, Becker HC, Chandler LJ (2012) Chronic alcohol exposure alters behavioral and synaptic plasticity of the rodent prefrontal cortex. PLoS ONE 7:e37541
28. Ridley NJ, Draper B, Withall A (2013) Alcohol-related dementia: an update of the evidence. Alzheimers Res Ther 5:3
29. Tiwari V, Kuhad A, Chopra K (2009) Suppression of neuro-inflammatory signaling cascade by tocotrienol can prevent chronic alcohol-induced cognitive dysfunction in rats. Behav Brain Res 203:296–303
30. de la Monte SM, Kril JJ (2014) Human alcohol-related neuropathology. Acta Neuropathol 127:71–90
31. Flanagan DE, Pratt E, Murphy J, Vaile JC, Petley GW, Godsland IF, Kerr D (2002) Alcohol consumption alters insulin secretion and cardiac autonomic activity. Eur J Clin Invest 32:187–192
32. Wang X, Ke Z, Chen G, Xu M, Bower KA, Frank JA, Zhang Z, Shi X, Luo J (2012) Cdc42-dependent activation of NADPH oxidase is involved in ethanol-induced neuronal oxidative stress. PLoS ONE 7:e38075
33. Ramachandran V, Watts LT, Maffi SK, Chen J, Schenker S, Henderson G (2003) Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons. J Neurosci Res 74:577–588
34. Kamens HM, Phillips TJ (2008) A role for neuronal nicotinic acetylcholine receptors in ethanol-induced stimulation, but not cocaine- or methamphetamine-induced stimulation. Psychopharmacology (Berl) 196:377–387
35. Probst-Hensch N, Braun-Fahrlaender C, Bodenmann A, Ackermann-Liebrich U (1993) Alcohol consumption and other lifestyle factors: avoidable sources of excess lead exposure. Soz Praventivmed 38:43–50
36. Telisman S, Cvitkovic P, Jurasovic J, Pizent A, Gavella M, Rocic B (2000) Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 108:45–53
37. Flora SJ, Kumar D, Sachan SR, Das Gupta S (1991) Combined exposure to lead and ethanol on tissue concentration of essential metals and some biochemical indices in rat. Biol Trace Elem Res 28:157–164
38. Flora SJ, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128:501–523
39. Gupta V, Gill KD (2000) Influence of ethanol on lead distribution and biochemical changes in rats exposed to lead. Alcohol 20:9–17
40. Kupraszewicz E, Brzoska MM (2013) Excessive ethanol consumption under exposure to lead intensifies disorders in bone metabolism: a study in a rat model. Chem Biol Interact 203:486–501
41. Agrawal M, Kumar V, Kashyap MP, Khanna VK, Randhawa GS, Pant AB (2011) Ischemic insult induced apoptotic changes in PC12 cells: protection by trans resveratrol. Eur J Pharmacol 666:5–11
42. Agrawal M, Kumar V, Singh AK, Kashyap MP, Khanna VK, Siddiqui MA, Pant AB (2013) trans-Resveratrol protects ischemic PC12 Cells by inhibiting the hypoxia associated transcription factors and increasing the levels of antioxidant defense enzymes. ACS Chem Neurosci 4:285–294
43. Akhtar MJ, Ahamed M, Kumar S, Siddiqui H, Patil G, Ashquin M, Ahmad I (2010) Nanotoxicity of pure silica mediated through oxidant generation rather than glutathione depletion in human lung epithelial cells. Toxicology 276:95–102
44. Siddiqui MA, Kashyap MP, Kumar V, Al-Khedhairy AA, Musarrat J, Pant AB (2010) Protective potential of trans-resveratrol against 4-hydroxynonenal induced damage in PC12 cells. Toxicol In Vitro 24:1592–1598
45. Ghosh S, Patel N, Rahn D, McAllister J, Sadeghi S, Horwitz G, Berry D, Wang KX, Swerdlow RH (2007) The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells. Mol Pharmacol 71:1695–1702
46. Waterhouse NJ, Steel R, Kluck R, Trapani JA (2004) Assaying cytochrome C translocation during apoptosis. Methods Mol Biol 284:307–313
47. Cezard C, Demarquilly C, Boniface M, Haguenoer JM (1992) Influence of the degree of exposure to lead on relations between alcohol consumption and the biological indices of lead exposure: epidemiological study in a lead acid battery factory. Br J Ind Med 49:645–647
48. Molina MF, Sanchez-Reus I, Iglesias I, Benedi J (2003) Quercetin, a flavonoid antioxidant, prevents and protects against ethanol-induced oxidative stress in mouse liver. Biol Pharm Bull 26:1398–1402
49. Flora SJS, Gautam P, Kushwaha P (2012) Lead and ethanol co-exposure lead to blood oxidative stress and subsequent neuronal apoptosis in rats. Alcohol and alcoholism:agr152
50. Suntres ZE (2002) Role of antioxidants in paraquat toxicity. Toxicology 180:65–77
51. Shavali S, Sens DA (2008) Synergistic neurotoxic effects of arsenic and dopamine in human dopaminergic neuroblastoma SH-SY5Y cells. Toxicol Sci 102:254–261
52. Bolin CM, Basha R, Cox D, Zawia NH, Maloney B, Lahiri DK, Cardozo-Pelaez F (2006) Exposure to lead and the developmental origin of oxidative DNA damage in the aging brain. FASEB J 20:788–790
53. Fazakas Z, Lengyel Z, Nagymajtenyi L (2005) Combined effects of subchronic exposure to lead, mercury and alcohol on the spontaneous and evoked cortical activity in rats. Arhiv za higijenu rada i toksikologiju 56:249–256
54. Kashyap MP, Singh AK, Siddiqui MA, Kumar V, Tripathi VK, Khanna VK, Yadav S, Jain SK, Pant AB (2010) Caspase cascade regulated mitochondria mediated apoptosis in monocrotophos exposed PC12 cells. Chem Res Toxicol 23:1663–1672
55. Galluzzi L, Morselli E, Kepp O, Tajeddine N, Kroemer G (2008) Targeting p53 to mitochondria for cancer therapy. Cell Cycle 7:1949–1955
56. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163
57. Namazi MR (2009) Cytochrome-P450 enzymes and autoimmunity: expansion of the relationship and introduction of free radicals as the link. J Autoimmune Dis 6:4
58. Poplawski T, Pawlowska E, Wisniewska-Jarosinska M, Ksiazek D, Wozniak K, Szczepanska J, Blasiak J (2009) Cytotoxicity and genotoxicity of glycidyl methacrylate. Chem Biol Interact 180:69–78
59. Segui B, Legembre P (2010) Redistribution of CD95 into the lipid rafts to treat cancer cells? Recent Pat Anticancer Drug Discov 5:22–28
60. Moll UM, Wolff S, Speidel D, Deppert W (2005) Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 17:631–636
61. Yu J, Zhang L (2005) The transcriptional targets of p53 in apoptosis control. Biochem Biophys Res Commun 331:851–858
62. Bargonetti J, Manfredi JJ (2002) Multiple roles of the tumor suppressor p53. Curr Opin Oncol 14:86–91
63. Cui Q, Yu JH, Wu JN, Tashiro S, Onodera S, Minami M, Ikejima T (2007) P53-mediated cell cycle arrest and apoptosis through a caspase-3- independent, but caspase-9-dependent pathway in oridonin-treated MCF-7 human breast cancer cells. Acta Pharmacol Sin 28:1057–1066
64. Saleh AM, Vijayasarathy C, Masoud L, Kumar L, Shahin A, Kambal A (2003) Paraoxon induces apoptosis in EL4 cells via activation of mitochondrial pathways. Toxicol Appl Pharmacol 190:47–57
65. Dejean LM, Martinez-Caballero S, Guo L, Hughes C, Teijido O, Ducret T, Ichas F, Korsmeyer SJ, Antonsson B, Jonas EA, Kinnally KW (2005) Oligomeric Bax is a component of the putative cytochrome c release channel MAC, mitochondrial apoptosis-induced channel. Mol Biol Cell 16:2424–2432
66. Wang S, Yan-Neale Y, Cai R, Alimov I, Cohen D (2006) Activation of mitochondrial pathway is crucial for tumor selective induction of apoptosis by LAQ824. Cell Cycle 5:1662–1668
67. Galluzzi L, Blomgren K, Kroemer G (2009) Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 10:481–494
68. Zhao M, Zhang Y, Wang C, Fu Z, Liu W, Gan J (2009) Induction of macrophage apoptosis by an organochlorine insecticide acetofenate. Chem Res Toxicol 22:504–510
69. Wang X, Zhu C, Hagberg H, Korhonen L, Sandberg M, Lindholm D, Blomgren K (2004) X-linked inhibitor of apoptosis (XIAP) protein protects against caspase activation and tissue loss after neonatal hypoxia-ischemia. Neurobiol Dis 16:179–189
70. 2+ signal generation and pancreatitis. Cell Calcium 45:634–642
71. Dostalek M, Hardy KD, Milne GL, Morrow JD, Chen C, Gonzalez FJ, Gu J, Ding X, Johnson DA, Johnson JA, Martin MV, Guengerich FP (2008) Development of oxidative stress by cytochrome P450 induction in rodents is selective for barbiturates and related to loss of pyridine nucleotide-dependent protective systems. J Biol Chem 283:17147–17157
72. Lupp A, Kuhn UD, Karge E, Adam G, Fleck C (2006) In vitro investigations on the differential pro-oxidant and/or antioxidant properties of cyclosporin A and tacrolimus in human and rat liver microsomes. Int J Clin Pharmacol Ther 44:225–232
73. Mari M, Cederbaum AI (2001) Induction of catalase, alpha, and microsomal glutathione S-transferase in CYP2E1 overexpressing HepG2 cells and protection against short-term oxidative stress. Hepatology 33:652–661
74. Hewitt R, Forero A, Luncsford PJ, Martin FL (2007) Enhanced micronucleus formation and modulation of BCL-2:BAX in MCF-7 cells after exposure to binary mixtures. Environ Health Perspect 115(Suppl 1):129–136
75. Cederbaum AI (2006) CYP2E1—biochemical and toxicological aspects and role in alcohol-induced liver injury. Mt Sinai J Med 73:657–672
76. Gong P, Cederbaum AI (2006) Nrf2 is increased by CYP2E1 in rodent liver and HepG2 cells and protects against oxidative stress caused by CYP2E1. Hepatology 43:144–153
77. Bradford BU, Kono H, Isayama F, Kosyk O, Wheeler MD, Akiyama TE, Bleye L, Krausz KW, Gonzalez FJ, Koop DR, Rusyn I (2005) Cytochrome P450 CYP2E1, but not nicotinamide adenine dinucleotide phosphate oxidase, is required for ethanol-induced oxidative DNA damage in rodent liver. Hepatology 41:336–344
78. Raza H, John A (2006) 4-Hydroxynonenal induces mitochondrial oxidative stress, apoptosis and expression of glutathione S-transferase A4-4 and cytochrome P450 2E1 in PC12 cells. Toxicol Appl Pharmacol 216:309–318
79. Kashyap MP, Singh AK, Kumar V, Tripathi VK, Srivastava RK, Agrawal M, Khanna VK, Yadav S, Jain SK, Pant AB (2011) Monocrotophos induced apoptosis in PC12 cells: role of xenobiotic metabolizing cytochrome P450s. PLoS ONE 6:e17757
80. Engle MR, Singh SP, Czernik PJ, Gaddy D, Montague DC, Ceci JD, Yang Y, Awasthi S, Awasthi YC, Zimniak P (2004) Physiological role of mGSTA4-4, a glutathione S-transferase metabolizing 4-hydroxynonenal: generation and analysis of mGsta4 null mouse. Toxicol Appl Pharmacol 194:296–308
81. Wang L, Yang Y, Dwivedi S, Xu Y, Chu ET, Li J, Fitchett K, Boor PJ (2006) Manipulating glutathione-S-transferases may prevent the development of tolerance to nitroglycerin. Cardiovasc Toxicol 6:131–144
82. Li CY, Lee JS, Ko YG, Kim JI, Seo JS (2000) Heat shock protein 70 inhibits apoptosis downstream of cytochrome c release and upstream of caspase-3 activation. J Biol Chem 275:25665–25671