Reactive oxygen species regulated mitochondria-mediated apoptosis in PC12 cells exposed to chlorpyrifos

Toxicology and Applied Pharmacology

Volumn 263, Issue 2, 2012, Pages 148-162

  Lee, Jeong Eun ^a,b   Park, Jae Hyeon ^a,b   Shin, In Chul ^a   Koh, Hyun Chul ^a,b  

^a Hanyang University   (South Korea)

^b Hanyang Biomedical Research Institute   (South Korea)

Author keywords

Apoptosis; Chlorpyrifos; MAPK; Mitochondrial complex I activity; Reactive oxidative species

Indexed keywords

ACETYLCYSTEINE; CASPASE 3; CASPASE 9; CHLORPYRIFOS; COPPER ZINC SUPEROXIDE DISMUTASE; DOPAMINE; HEME OXYGENASE 1; LACTATE DEHYDROGENASE; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TYROSINE 3 MONOOXYGENASE;

AEROBIC METABOLISM; ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BIOTRANSFORMATION; CELL DEATH; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINE METABOLISM; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INHIBITION KINETICS; MITOCHONDRION; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CHLORPYRIFOS; DOPAMINE; FEMALE; GENE EXPRESSION REGULATION; HEME OXYGENASE-1; INSECTICIDES; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; OXIDATIVE STRESS; PC12 CELLS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SUBSTANTIA NIGRA; SUPEROXIDE DISMUTASE; TIME FACTORS;

RATTUS;

EID: 84865094711     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.06.005     Document Type: Article

References (70)

1. Adler V., Yin Z., Tew K.D., Ronai Z. Role of redox potential and reactive oxygen species in stress signaling. Oncogene 1999, 18:6011-6014.
2. Bae J.W., Kim M.J., Jang C.G., Lee S.Y. Protective effects of heme oxygenase-1 against MPP+-induced cytotoxicity in PC12 cells. Neurol. Sci. 2010, 31:307-313.
3. Bao W., Behm D.J., Nerurkar S.S., Ao Z., Bentley R., Mirabile R.C., Johns D.G., Woods T.N., Doe C.P., Coatney R.W., Ohlstein J.F., Douglas S.A., Willette R.N., Yue T.L. Effects of p38 MAPK inhibitor on angiotensin II-dependent hypertension, organ damage, and superoxide anion production. J. Cardiovasc. Pharmacol. 2007, 49:362-368.
4. Barlow B.K., Lee D.W., Cory-Slechta D.A., Opanashuk L.A. Modulation of antioxidant defense systems by the environmental pesticide maneb in dopaminergic cells. Neurotoxicology 2005, 26:63-75.
5. Basha P.M., Poojary A. Chlorpyrifos induced region specific vulnerability in rat CNS and modulation by age and cold stress: an interactive study. Neurochem. Res. 2011, 36:241-249.
6. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U. S. A. 2001, 20:13681-13686.
7. Bharath S., Hsu M., Kaur D., Rajagopalan S., Andersen J.K. Glutathione, iron and Parkinson's disease. Biochem. Pharmacol. 2002, 64:1037-1048.
8. Bi J., Jiang B., Hao S., Zhang A., Dong Y., Jiang T., An L. Catalpol attenuates nitric oxide increase via ERK signing pathways induced by rotenone in mesencephalic neurons. Neurochem. Int. 2009, 54:264-270.
9. Black A.T., Gray J.P., Shakarjian M.P., Laskin D.L., Heck D.E., Laskin J.D. Increased oxidative stress and antioxidant expression in mouse keratinocytes following exposure to paraquat. Toxicol. Appl. Pharmacol. 2008, 231:384-392.
10. Bogdanov M.B., Andreassen O.A., Dedeoglu A., Ferrante R.J., Beal M.F. Increased oxidative damage to DNA in a transgenic mouse model of Huntington's disease. J. Neurochem. 2001, 6:1246-1249.
11. Bonneh-Barkay D., Langston W.J., Di Monte D.A. Toxicity of redox cycling pesticides in primary mesencephalic cultures. Antioxid. Redox Signal. 2005, 7:649-653.
12. Caughlan A., Newhouse K., Namgung U., Xia Z. Chlorpyrifos induces apoptosis in rat cortical neurons that is regulated by a balance between p38 and ERK/JNK MAP kinases. Toxicol. Sci. 2004, 78:125-134.
13. Chen K., Gunter K., Maines M.D. Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 2000, 75:304-313.
14. Chen J., Rusnak M., Lombroso P.J., Sidhu A. Dopamine promotes striatal neuronal apoptotic death via ERK signaling cascades. Eur. J. Neurosci. 2009, 29:287-306.
15. Chen-Roetling J., Benvenisti-Zarom L., Regan R.F. Cultured astrocytes from heme oxygenase-1 knockout mice are more vulnerable to heme-mediated oxidative injury. J. Neurosci. Res. 2005, 82:802-810.
16. Choi W.S., Palmiter R.D., Xia Z. Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson's disease model. J. Cell Biol. 2011, 192:873-882.
17. Cleeter M.W.J., Cooper J.M., Schapira A.H.V. Irreversible inhibition of mitochondrial complex I by 1-methyl-4-phenylpyridinium: evidence for free radical involvement. J. Neurochem. 1992, 58:786-789.
18. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
19. Dhingra S., Sharma A.K., Singla D.K., Singal P.K. p38 and ERK1/2 MAPKs mediate the interplay of TNF-alpha and IL-10 in regulating oxidative stress and cardiac myocyte apoptosis. Am. J. Physiol. Heart Circ. Physiol. 2007, 293:H3524-H3531.
20. Dinis-Oliveira R.J., Remião F., Carmo H., Duarte J.A., Navarro A.S., Bastos M.L., Carvalho F. Paraquat exposure as an etiological factor of Parkinson's disease. Neurotoxicology 2006, 27:1110-1112.
21. Farag A.T., El Okazy A.M., El-Aswed A.F. Developmental toxicity study of chlorpyrifos in rats. Reprod. Toxicol. 2003, 17:203-208.
22. Fridovich I. The biology of oxygen radicals. Science 1978, 201:875-880.
23. Gonzalez-Zulueta M., Ensz L.M., Nukhina G., Lebovitz R.M., Zwacka R.M., Engelhardt J.F., Oberley L.W., Dawson V.L., Dawson T.M. Manganese superoxide dismutase protects nNOS neurons from NMDA and nitric oxide-mediated neurotoxicity. J. Neurosci. 1998, 18:2040-2055.
24. Gorell J.M., Johonson C.C., Rybicki B.A., Peterson E.L., Richardson R.J. The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living. Neurology 1998, 50:1346-1350.
25. Gills J.J., Castillo S.S., Zhang C., Petukhov P.A., Memmott R.M., Hollingshead M., Warfel N., Han J., Kozikowski A.P., Dennis P.A. Phosphatidylinositol ether lipid analogues that inhibit AKT also independently activate the stress kinase, p38alpha, through MKK3/6-independent and -dependent mechanisms. J. Biol. Chem. 2007, 14:27020-27029.
26. Gupta R.C. Brain regional heterogeneity and toxicological mechanisms of organophosphates and carbamates. Toxicol. Mech. Methods 2004, 14:103-143.
27. Hartley A., Stone J.M., Heron C., Cooper J.M., Schapira A.H. Complex I inhibitors induce dose-dependent apoptosis in PC12 cells: relevance to Parkinson's disease. J. Neurochem. 1994, 63:1987-1990.
28. Huang X., Moir R.D., Tanzi R.E., Bush A.I., Rogers J.T. Redox-active metals, oxidative stress, and Alzheimer's disease pathology. Ann. N. Y. Acad. Sci. 2004, 1012:153-163.
29. Huang E., Ong W.Y., Go M.L., Garey L.J. Heme oxygenase-1 activity after excitotoxic injury: immunohistocymical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainite treatment. J. Neurosci. Res. 2005, 80:268-278.
30. Hasegawa E., Takeshige K., Oishi T., Murai Y., Minakami S. 1-methyl-4-phenylpyridinium (MPP+) induces NADA-dependent superoxide formation and enhances NADA-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem. Biophys. Res. Commun. 1990, 170:1049-1055.
31. Hsuan S.L., Klintworth H.M., Xia Z. Basic fibroblast growth factor protects against rotenone-induced dopaminergic cell death through activation of extracellular signal-regulated kinases 1/2 and phosphatidylinositol-3 kinase pathways. J. Neurosci. 2006, 26:4481-4491.
32. Jenner P., Olanow C.W. Understanding cell death in Parkinson's disease. Ann. Neurol. 1998, 44:S72-S84.
33. Kalender Y., Yel M., Kalender S. Doxorubicin hapatotoxicity and hepatic free radical metabolism in rats: the effects of vitamine E and catechin. Toxocology 2005, 211:197-206.
34. Kang D., Miyako K., Kuribayashi F., Hasegawa E., Mitsumoto A., Nagano T., Kakeshige K. Changes of energy metabolism induced by 1-methyl-4-phenylpyridinium (MPP+)-releted compounds in rat pheochromocytoma PC12 cells. Arch. Biochem. Biophys. 1997, 337:75-80.
35. Karaoz E., Glutekin F., Akdogan M., Oncu M., Gokcimen A. Protective role of melatonin and combination of vitamin C and vitamin E on lung toxicity induced by chlorpyrifos-ethyl in rats. Exp. Toxicol. Pathol. 2002, 54:97-108.
36. Kitazawa M., Anantharam V., Kanthasamy A.G. Dieldrin induced oxidative stress and neurocheminal changes contribute to apoptotic cell death in dopaminergic cells. Free Radic. Biol. Med. 2001, 31:1473-1485.
37. Klivenyl P., St Clair D., Wermer M., Yen H.C., Oberley T., Yang L., Beal M.F. Manganese superoxide dismutase overexpression attenuates MPTP toxicity. Neurobiol. Dis. 1998, 5:253-258.
38. Ku B.M., Lee Y.K., Jeong J.Y., Mun J., Han J.Y., Roh G.S., Kim H.J., Cho G.J., Choi W.S., Yi G.S., Kang S.S. Ethanol-induced oxidative stress is mediated by p38 MAPK pathway in mouse hippocampal cells. Neurosci. Lett. 2007, 419:64-67.
39. Kurosaki R., Muramatsu Y., Kato H., Araki T. Biochemical, behavioral and immunohistochemical alterations in MPTP-treated mouse model of Parkinson's disease. Pharmacol. Biochem. Behav. 2004, 78:143-153.
40. Mansour S.A., Mossa A.H. Lipid peroxidation and oxidative stress in rat erythrocytes induced by chlorpyrifos and the protective effect of zinc. Pestic. Biochem. Phys. 2009, 93:34-39.
41. Mehta A., Verma R.S., Srivastava N. Chlorpyrifos induced alterations in the levels of hydrogen peroxide, nitrate and nitrite in rat brain and liver. Pestic. Biochem. Phys. 2009, 94:55-59.
42. Mielke E., Herdegen T. JNK and p38 stress kinases-degenerative effectors of signal-transduction-cascades in the nervous system. Prog. Neurobiol. 2000, 61:45-60.
43. Mochizuki H., Goto K., Mori H., Mizuno Y. Histochemical detection of apoptosis in Parkinson's disease. J. Neurol. Sci. 1996, 137:120-123.
44. Molina-Jiménez M.F., Sánchez-Reus M.I., Cascales M., Andrés D., Benedí J. Effect of fraxetin on antioxidant defense and stress proteins in human neuroblastoma cell model of rotenone neurotoxicity. Comparative study with myricetin and N-acetylcysteine. Toxicol. Appl. Pharmacol. 2005, 209:214-225.
45. Mori A., Ohashi S., Nakai M., Moriizumi T., Mitsumoto Y. Neural mechanisms underlying motor dysfunction as detected by the tail suspension test in MPTP-treated C57BL/6 mice. Neurosci. Res. 2005, 51:265-274.
46. Morno M., Cañadas F., Cardona D., Suñol C., Campa L., Sánchez-Amate M.C., Flores P., Sanchez-Santed F. Long-term monoamine changes in the striatum and nucleus accumbens after acute chlorpyrifos exposure. Toxicol. Lett. 2008, 176:162-167.
47. Murakami K., Kondo T., Epstein C.J., Chan P.H. Overexpression of CuZn-superoxide dismutase reduces hippocampal injury after global ischemia in transgenic mice. Stroke 1997, 28:1797-1804.
48. Newhouse K., Hsuan S.L., Chang S.H., Cai B., Wang Y., Xia Z. Rotenone-induced apoptosis is mediate by p38 and JNK MAP kinases in human dopaminergic SH-SY5Y cells. Toxicol. Sci. 2004, 79:137-146.
49. Owen A.D., Schapira A.H., Jenner P., Marsden C.D. Oxidative stress and Parkinson's disease. Ann. N.Y. Acad. Sci. 1996, 786:217-223.
50. Perier J., Bové D.C., Wu D.C., Dehay B., Choi D.K., Jackson-Lewis V., Rathke-Hartlieb S., Bouillet P., Strasser A., Schulz J.B., Przedborski S., Vila M. Two molecular pathways initiate mitochondria-dependent dopaminergic neurodegeneration in experimental Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8161-8166.
51. Prezdborski S., Kostic V., Jackson-Lewis V., Naini A.B., Sinometti S., Fahn S., Carlson E., Epstein C.J., Cadet J.L. Transgenic mice with increase Cu/Zn-superoxide dismutase activity are resistant to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity. J. Neurosci. 1992, 12:1658-1667.
52. Quia D., Seidler F.J., Slotkin T.A. Oxidative mechanisms contributing to the developmental neurotoxicity of nicotine and chlorpyrifos. Toxicol. Appl. Pharmacol. 2005, 206:17-26.
53. Rahman M.F., Mahboob M., Danadevi K., Saleha Banu B., Grover P. Assessment of genotoxic effects of chlorpyrifos and acephate by comet assay in mice leucocytes. Mutat. Res. 2002, 516:139-147.
54. Ramsay R.R., Krueger M.J., Youngster S.K., Gluck M.R., Casida J.E., Singer T.P. Interaction of 1-methyl-4-phenylpyridinium ion (MPP) and its analogs with the rotenone/piericidin binding site of NADH dehydrogenase. J. Neurochem. 1991, 56:1184-1190.
55. Saito Y., Nishio K., Oqawa Y., Kinumi T., Yoshida Y., Masuo Y., Niki E. Molecular mechanisms of 6-hydroxydopamine-induced cytotoxicity in PC12 cells: involvement of hydrogen peroxide-dependent and -independent action. Free Radic. Biol. Med. 2007, 42:675-685.
56. Saulsbury M.D., Heyliger S.O., Wang K., Round D. Characterization of chlorpyrifos-induced apoptosis in placental cells. Toxicology 2008, 244:98-110.
57. Saulsbury M.D., Heyliger S.O., Wang K., Johnson D.J. Chlorpyrifos induces oxidative stress in oligodendrocyte progenitor cells. Toxicology 2004, 259:1-9.
58. Schapira A.H., Cooper J.M., Dexter D., Jenner P., Clark J.B., Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. Lancet 1989, 1:1269.
59. Schipper H.M. Heme oxygenase expression in human central nervous system disorders. Free Radic. Biol. Med. 2004, 37:1995-2011.
60. Sherer T.B., Kin J.H., Betarbet R., Greenamyre J.T. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and α-synuclein aggregation. Exp. Neurol. 2003, 179:9-16.
61. Sherer T.B., Betarbet C.M., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., Miller G.W., Yagi T., Matsuno-Yagi A., Greenamyre J.T. Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 2003, 23:10756-10764.
62. Smith A., Alam J., Escriba P.V., Morgan W.T. Regulation of heme oxygenase and metallothionein gene expression by the heme analogs, cobalt-, and tinprotoporphyrin. J. Biol. Chem. 1993, 268:7365-7371.
63. Takeda A., Perry G., Abraham N.G., Dwyer B.E., Kutty R.K., Laitinen J.T., Petersen R.B., Smith M.A. Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau. J. Biol. Chem. 2000, 275:5395-5399.
64. Taylor E.R., Hurrell F., Shannon R.J., Lin T.K., Hirst J., Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 2003, 19603-19613.
65. Tischler A.S. Chromaffin cells as models of endocrine cells and neurons. Ann. N. Y. Acad. Sci. 2002, 971:366-370.
66. Verma R.S., Mehta A., Srivastava N. In vivo chlorpyrifos oxidative stress: attenuation by antioxidant vitamins. Pestic. Biochem. Physiol. 2007, 88:191-196.
67. Wang Y., Zhang Y., Wei Z., Li H., Zhou H., Zhang Z., Zhang Z. JNK inhibitor protects dopaminergic neurons by reducing COX-2 expression in the MPTP mouse model of subacute Parkinson's disease. J. Neurol. Sci. 2009, 15:172-177.
68. Yu C., Rahmani M., Dent P., Grant S. The hierarchical relationship between MAPK signaling and ROS generation in human leukemia cells undergoing apoptosis in response to the proteasome inhibitor Bortezomib. Exp. Cell Res. 2004, 295:555-566.
69. Zelko I.N., Mariani T.J., Folz R.J. Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic. Biol. Med. 2002, 33:337-349.
70. Zhang Y., Dawson V.L., Dawson T.M. Oxidative stress and genetics in the pathogenesis of Parkinson's disease. Neurobiol. Dis. 2000, 7:240-250.