Cypermethrin-Induced Nigrostriatal Dopaminergic Neurodegeneration Alters the Mitochondrial Function:A Proteomics Study

Molecular Neurobiology

Volumn 51, Issue 2, 2015, Pages 448-465

  Agrawal, Sonal ^a,b   Singh, Ashish ^a   Tripathi, Pratibha ^a   Mishra, Manisha ^c   Singh, Pradhyumna Kumar ^c   Singh, Mahendra Pratap ^a,b  

^a CSIR INDIAN INSTITUTE OF TOXICOLOGY RESEARCH   (India)

^b ACADEMY OF SCIENTIFIC AND INNOVATIVE RESEARCH ACSIR   (India)

^c CSIR NATIONAL BOTANICAL RESEARCH INSTITUTE   (India)

Author keywords

Cypermethrin; Mitochondrial complex I; Mitochondrial dysfunction; Mitochondrial proteome; Parkinson s disease

Indexed keywords

CARBIDOPA PLUS LEVODOPA; CASPASE 3; CYPERMETHRIN; DOPAMINE; HEME OXYGENASE 1; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BCL 2; PROTEIN P53; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; INSECTICIDE; MITOCHONDRIAL PROTEIN; PYRETHROID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; MALE; MICROGLIA; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN EXPRESSION; PROTEOMICS; RAT; REGULATORY MECHANISM; STRIATONIGRAL DEGENERATION; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; CORPUS STRIATUM; DEGENERATIVE DISEASE; DRUG EFFECTS; GENETICS; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SUBSTANTIA NIGRA; WISTAR RAT;

AMINO ACID SEQUENCE; ANIMALS; CORPUS STRIATUM; DOPAMINERGIC NEURONS; INSECTICIDES; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; NEURODEGENERATIVE DISEASES; PROTEOMICS; PYRETHRINS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA;

EID: 84924989783     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8696-7     Document Type: Article

References (72)

1. Yadav S, Dixit A, Agrawal S, Singh A, Srivastava G, Singh AK, Srivastava PK, Prakash O, Singh MP (2012) Rodent models and contemporary molecular techniques: notable feats yet incomplete explanations of Parkinson’s disease pathogenesis. Mol Neurobiol 46:495–512
2. Singh AK, Tiwari MN, Upadhyay G, Patel DK, Singh D, Prakash O, Singh MP (2012) Long-term exposure to cypermethrin induces the nigrostriatal dopaminergic neurodegeneration in adult rats: postnatal exposure enhances the susceptibility during adulthood. Neurobiol Aging 33:404–415
3. Tiwari MN, Singh AK, Ahmed I, Upadhyay G, Singh D, Patel DK, Singh C, Prakash O, Singh MP (2010) Effects of cypermethrin on monoamine transporters, xenobiotic metabolizing enzymes and lipid peroxidation in the rat nigrostriatal system. Free Radic Res 44:1416–1424
4. Singh AK, Tiwari MN, Dixit A, Upadhyay G, Patel DK, Singh D, Prakash O, Singh MP (2011) Nigrostriatal proteomics of cypermethrin-induced dopaminergic neurodegeneration microglial activation dependent and independent regulations. Toxicol Sci 122:526–538
5. Autere J, Moilanen JS, Finnilä S, Soininen H, Mannermaa A, Hartikainen P, Hallikainen M, Majamaa K (2004) Mitochondrial DNA polymorphisms as risk factors for Parkinson’s disease and Parkinson’s disease dementia. Hum Genet 115:29–35
6. Andrews ZB, Horvath B, Barnstable CJ, Elsworth J, Yang L, Beal MF, Roth RH, Matthews RT, Horvath TL (2005) Uncoupling protein-2 is critical for nigral dopamine cell survival in a mouse model of Parkinson’s disease. J Neurosci 25:184–191
7. Pennington K, Peng J, Hung CC, Banks RE, Robinson PA (2010) Differential effects of wild-type and A53T mutant isoform of alpha-synuclein on the mitochondrial proteome of differentiated SH-SY5Y cells. J Proteome Res 9:2390–2401
8. Johnson MD, Yu LR, Corads TP, Kinoshita Y, Uo T, McBee JK, Veenstra TD, Morrison RS (2005) The proteomics of neurodegeneration. Am J Pharmacogenom 5:259–270
9. Patel S, Sinha A, Singh MP (2007) Identification of differentially expressed proteins in striatum of maneb-and paraquat-induced Parkinson’s disease phenotype in mouse. Neurotoxicol Teratol 29:578–585
10. Chen X, Li J, Hou J, Xie Z, Yang F (2010) Mammalian mitochondrial proteomics: insights into mitochondrial functions and mitochondria-related diseases. Expert Rev Proteomics 7:333–345
11. Dixit A, Srivastava G, Verma D, Mishra M, Singh PK, Prakash O, Singh MP (2013) Minocycline, levodopa and MnTMPyP induced changes in the mitochondrial proteome profile of MPTP and maneb and paraquat mice models of Parkinson’s disease. Biochim Biophys Acta 1832:1227–1240
12. Huang CL, Lee YC, Yang YC, Kuo TY, Huang NK (2012) Minocycline prevents paraquat-induced cell death through attenuating endoplasmic reticulum stress and mitochondrial dysfunction. Toxicol Lett 209:203–210
13. Jung BD, Shin EJ, Nguyen XK, Jin CH, Bach JH, Park SJ, Nah SY, Wie MB, Bing G, Kim HC (2010) Potentiation of methamphetamine neurotoxicity by intrastriatal lipopolysaccharide administration. Neurochem Int 56:229–244
14. Shin JY, Park HJ, Ahn YH, Lee PH (2009) Neuroprotective effect of L-dopa on dopaminergic neurons is comparable to pramipexol in MPTP-treated animal model of Parkinson’s disease: a direct comparison study. J Neurochem 111:1042–1050
15. Tomás-Camardiel M, Rite I, Herrera AJ, de Pablos RM, Cano J, Machado A, Venero JL (2004) Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood–brain barrier, and damage in the nigral dopaminergic system. Neurobiol Dis 16:190–201
16. Ciesielska A, Mittermeyer G, Hadaczek P, Kells AP, Forsayeth J, Bankiewicz KS (2011) Anterograde axonal transport of AAV2-GDNF in rat basal ganglia. Mol Ther 19:922–927
17. Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic, Sydney, New York
18. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
19. Burté F, De Girolamo LA, Hargreaves AJ, Billett EE (2011) Alterations in the mitochondrial proteome of neuroblastoma cells in response to complex 1 inhibition. J Proteome Res 10:1974–1986
20. Morrison RS, Kinoshita Y, Johnson MD, Uo T, Ho JT, McBee JK, Conrads TP, Veenstra TD (2002) Proteomic analysis in the neurosciences. Mol Cell Proteomics 1:553–560
21. Song Z, Guo Q, Zhang J, Li M, Liu C, Zou W (2012) Proteomic analysis of PKCγ-related proteins in the spinal cord of morphine-tolerant rats. PLoS One 7:e42068
22. Grunert T, Leitner NR, Marchetti-Deschmann M, Miller I, Wallner B, Radwan M, Vogl C, Kolbe T, Kratky D, Gemeiner M, Allmaier G, Müller M, Strobl BA (2011) Comparative proteome analysis links tyrosine kinase 2 (Tyk2) to the regulation of cellular glucose and lipid metabolism in response to poly (I:C). J Proteomics 74:2866–2880
23. Hirano M, Rakwal R, Shibato J, Sawa H, Nagashima K, Ogawa Y, Yoshida Y, Iwahashi H, Niki E, Masuo Y (2008) Proteomics- and transcriptomics-based screening of differentially expressed proteins and genes in brain of Wig rat: a model for attention deficit hyperactivity disorder (ADHD) research. J Proteome Res 7:2471–2489
24. Lessner G, Schmitt O, Haas SJ, Mikkat S, Kreutzer M, Wree A, Glocker MO (2010) Differential proteome of the striatum from hemiparkinsonian rats displays vivid structural remodeling processes. J Proteome Res 9:4671–4687
25. Sinha A, Srivastava N, Singh S, Singh AK, Bhushan S, Shukla R, Singh MP (2009) Identification of differentially displayed proteins in cerebrospinal fluid of Parkinson’s disease patients: a proteomic approach. Clin Chim Acta 400:14–20
26. Shaw J, Rowlinson R, Nickson J, Stone T, Sweet A, Williams K, Tonge R (2003) Evaluation of saturation labelling two-dimensional difference gel electrophoresis fluorescent dyes. Proteomics 3:1181–1195
27. Banerjee K, Sinha M, Pham CL, Jana S, Chanda D, Cappai R, Chakrabarti S (2010) α-Synuclein induced membrane depolarization and loss of phosphorylation capacity of isolated rat brain mitochondria: implications in Parkinson’s disease. FEBS Lett 584:1571–1576
28. Krahenbuhl S, Chang M, Brass EP, Hoppel CL (1991) Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin [c-lactam]-induced methylmalonic aciduria. J Biol Chem 266:20998–21003
29. Shults CW, Nasirian F, Ward DM, Nakano K, Pay M, Hill LR, Haas RH (1995) Carbidopa/levodopa and selegiline do not affect platelet mitochondrial function in early Parkinsonism. Neurology 45:344–348
30. Srivastava G, Dixit A, Yadav S, Patel DK, Prakash O, Singh MP (2012) Resveratrol potentiates cytochrome P450 2 d22-mediated neuroprotection in maneb- and paraquat-induced parkinsonism in the mouse. Free Radic Biol Med 52:1294–1306
31. Tiwari MN, Singh AK, Agrawal S, Gupta SP, Jyoti A, Shanker R, Prakash O, Singh MP (2012) Cypermethrin alters the expression profile of mRNAs in the adult rat striatum: a putative mechanism of postnatal pre-exposure followed by adulthood re-exposure-enhanced neurodegeneration. Neurotox Res 22:321–334
32. Patel S, Singh K, Singh S, Singh MP (2008) Gene expression profiles of mouse striatum in control and maneb + paraquat-induced Parkinson’s disease phenotype: validation of differentially expressed energy metabolizing transcripts. Mol Biotechnol 40:59–68
33. 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
34. Fontanesi F, Soto IC, Horn D, Barrientos A (2006) Assembly of mitochondrial cytochrome c-oxidase, a complicated and highly regulated cellular process. Am J Physiol Cell Physiol 291:C1129–C1147
35. Diedrich M, Mao L, Bernreuther C, Zabel C, Nebrich G, Kleene R, Klose J (2008) Proteome analysis of ventral midbrain in MPTP-treated normal and L1cam transgenic mice. Proteomics 8:1266–1275
36. Okado-Matsumoto A, Fridovich I (2001) Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem 276:38388–38393
37. Troy CM, Derossi D, Prochiantz A, Greene LA, Shelanski ML (1996) Downregulation of Cu/Zn superoxide dismutase leads to cell death via the nitric oxide-peroxynitrite pathway. J Neurosci 16:253–261
38. Krapfenbauer K, Engidawork E, Cairns N, Fountoulakis M, Lubec G (2003) Aberrant expression of peroxiredoxin subtypes in neurodegenerative disorders. Brain Res 967:152–160
39. Lee W, Choi KS, Riddell J, Ip C, Ghosh D, Park JH, Park YM (2007) Human peroxiredoxin 1 and 2 are not duplicate proteins: the unique presence of CYS83 in Prx1 underscores the structural and functional differences between Prx1 and Prx2. J Biol Chem 282:22011–22022
40. Palacino JJ, Sagi D, Goldberg MS, Krauss S, Motz C, Wacker M, Klose J, Shen J (2004) Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J Biol Chem 279:18614–18622
41. Garbis S, Lubec G, Fountoulakis M (2005) Limitations of current proteomics technologies. J Chromatogr A 1077:1–18
42. Knight M, Raghavan N, Goodall C, Cousin C, Ittiprasert W, Sayed A, Miller A, Williams DL, Bayne CJ (2009) Biomphalaria glabrata peroxiredoxin: effect of Schistosoma mansoni infection on differential gene regulation. Mol Biochem Parasitol 167:20–31
43. Ferrer I, Perez E, Dalfó E, Barrachina M (2007) Abnormal levels of prohibitin and ATP synthase in the substantia nigra and frontal cortex in Parkinson’s disease. Neurosci Lett 415:205–209
44. Park B, Yang J, Yun N, Choe KM, Jin BK, Oh YJ (2010) Proteomic analysis of expression and protein interactions in a 6-hydroxydopamine-induced rat brain lesion model. Neurochem Int 57:16–32
45. Periquet M, Corti O, Jacquier S, Brice A (2005) Proteomic analysis of parkin knockout mice: alterations in energy metabolism, protein handling and synaptic function. J Neurochem 95:1259–1276
46. Krishnan KS, Rikhy R, Rao S, Shivalkar M, Mosko M, Narayanan R, Etter P, Estes PS, Ramaswami M (2001) Nucleoside diphosphate kinase, a source of GTP, is required for dynamin-dependent synaptic vesicle recycling. Neuron 30:197–210
47. Carré M, André N, Carles G, Borghi H, Brichese L, Briand C, Braguer D (2002) Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem 277:33664–33669
48. Chaturvedi V, Jonnala KU, Cherukuvada VBS, Rangaraj N, Gunda S, Rathinam K, Singh S, Amere SS (2011) Repercussion of mitochondria deformity induced by anti-Hsp90 Drug 17AAG in human tumor cells. Drug Target Insights 5:11–32
49. Lopez-Campistrous A, Hao L, Xiang W, Ton D, Semchuk P, Sander J, Ellison MJ, Fernandez-Patron C (2008) Mitochondrial dysfunction in the hypertensive rat brain: respiratory complexes exhibit assembly defects in hypertension. Hypertension 51:412–419
50. Lubec G, Afjehi-Sadat L, Yang JW, John JP (2005) Searching for hypothetical proteins: theory and practice based upon original data and literature. Prog Neurobiol 77:90–127
51. Perrot A, Pionneau C, Azar N, Baillou C, Lemoine FM, Leblond V, Merle-Béral H, Béné MC, Herbrecht R, Bahram S, Vallat L (2012) Waldenström’s macroglobulinemia harbors a unique proteome where Ku70 is severely underexpressed as compared with other B-lymphoproliferative disorders. Blood Cancer J 2:e88
52. Paasch U, Heidenreich F, Pursche T, Kuhlisch E, Kettner K, Grunewald S, Kratzsch J, Dittmar G, Glander HJ, Hoflack B, Kriegel TM (2011) Identification of increased amounts of eppin protein complex components in sperm cells of diabetic and obese individuals by difference gel electrophoresis. Mol Cell Proteomics 10:M110.007187
53. Person MD, Shen J, Traner A, Hensley SC, Lo HH, Abbruzzese LJ, Li D (2006) Protein fragment domains identified using 2D Gel electrophoresis/MALDI-TOF. J Biomol Tech 17:145–156
54. Baldwin MA (2004) Protein identification by mass spectrometry: issues to be considered. Mol Cell Proteomics 3:1–9
55. Rinalducci S, Murgiano L, Zolla L (2008) Redox proteomics: basic principles and future perspectives for the detection of protein oxidation in plants. J Exp Bot 59:3781–3801
56. Spencer JP, Jenner A, Butler J, Aruoma OI, Dexter DT, Jenner P, Halliwell B (1996) Evaluation of the pro-oxidant and antioxidant actions of L-DOPA and dopamine in vitro: implications for Parkinson’s disease. Free Radic Res 24:95–105
57. O’Sullivan SS, Johnson M, Williams DR, Revesz T, Holton JL, Lees AJ, Perry EK (2011) The effect of drug treatment on neurogenesis in Parkinson’s disease. Mov Disord 26:45–50
58. Good CH, Hoffman AF, Hoffer BJ, Chefer VI, Shippenberg TS, Bäckman CM, Larsson NG, Olson L, Gellhaar S, Galter D, Lupica CR (2011) Impaired nigrostriatal function precedes behavioral deficits in a genetic mitochondrial model of Parkinson’s disease. FASEB J 25:1333–1344
59. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O (2003) Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632–13637
60. Noble W, Garwood CJ, Hanger DP (2009) Minocycline as a potential therapeutic agent in neurodegenerative disorders characterised by protein misfolding. Prion 3:78–83
61. Gassner B, Wüthrich A, Scholtysik G, Solioz M (1997) The pyrethroids permethrin and cyhalothrin are potent inhibitors of the mitochondrial complex I. J Pharmacol Exp Ther 281:855–860
62. Bagh MB, Thakurta IG, Biswas M, Behera P, Chakrabarti S (2011) Age-related oxidative decline of mitochondrial functions in rat brain is prevented by long term oral antioxidant supplementation. Biogerontology 12:119–131
63. Nakai M, Mori A, Watanabe A, Mitsumoto Y (2003) 1-methyl-4-phenylpyridinium (MPP+) decreases mitochondrial oxidation-reduction (REDOX) activity and membrane potential (Deltapsi(m)) in rat striatum. Exp Neurol 179:103–110
64. Gevaerd MS, Miyoshi E, Silveira R, Canteras NS, Takahashi RN, Da Cunha C (2001) L-Dopa restores striatal dopamine level but fails to reverse MPTP-induced memory deficits in rats. Int J Neuropsychopharmacol 4:361–370
65. Won H, Lim S, Jang M, Kim Y, Rashid MA, Jyothi KR, Dashdorj A, Kang I, Ha J, Kim SS (2012) Peroxiredoxin-2 upregulated by NF-κB attenuates oxidative stress during the differentiation of muscle-derived C2C12 cells. Antioxid Redox Signal 16:245–261
66. Burgula S, Medisetty R, Jammulamadaka N, Musturi S, Ilavazhagan G, Singh SS (2010) Downregulation of PEBP1 in rat brain cortex in hypoxia. J Mol Neurosci 41:36–47
67. Zhou P, Qian L, D’Aurelio M, Cho S, Wang G, Manfredi G, Pickel V, Iadecola C (2012) Prohibitin reduces mitochondrial free radical production and protects brain cells from different injury modalities. J Neurosci 32:583–592
68. Cox AG, Brown KK, Arner ES, Hampton MB (2008) The thioredoxin reductase inhibitor auranofin triggers apoptosis through a Bax/Bak-dependent process that involves peroxiredoxin 3 oxidation. Biochem Pharmacol 76:1097–1109
69. Zhao C, Ling Z, Newman MB, Bhatia A, Carvey PM (2007) TNF-alpha knockout and minocycline treatment attenuates blood–brain barrier leakage in MPTP-treated mice. Neurobiol Dis 26:36–46
70. Bessler H, Djaldetti R, Salman H, Bergman M, Djaldetti M (1999) IL-1 beta, IL-2, IL-6 and TNF-alpha production by peripheral blood mononuclear cells from patients with Parkinson’s disease. Biomed Pharmacother 53:141–145
71. Eberhardt O, Schulz JB (2003) Apoptotic mechanisms and antiapoptotic therapy in the MPTP model of Parkinson’s disease. Toxicol Lett 139:135–151
72. Singh AK, Tiwari MN, Prakash O, Singh MP (2012) A current review of cypermethrin-induced neurotoxicity and nigrostriatal dopaminergic neurodegeneration. Curr Neuropharmacol 10:64–71