Specific pesticide-dependent increases in α-synuclein levels in human neuroblastoma (SH-SY5Y) and melanoma (SK-MEL-2) cell lines

Toxicological Sciences

Volumn 133, Issue 2, 2013, Pages 289-297

  Chorfa, Areski ^a   Bétemps, Dominique ^a   Morignat, Eric ^a   Lazizzera, Corinne ^a   Hogeveen, Kevin ^a   Andrieu, Thibault ^b   Baron, Thierry ^a  

^a Lyon Laboratory   (France)

^b INSERM   (France)

Author keywords

synuclein; Malignant melanona; Neuroblastoma; Parkinson's disease; Pesticides

Indexed keywords

ALPHA SYNUCLEIN; MANEB; PARAQUAT; PESTICIDE; ROTENONE; SUGAR PHOSPHATE;

ADENOVIRUS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MELANOMA CELL; NEUROBLASTOMA CELL; PROTEIN EXPRESSION; WESTERN BLOTTING;

Α-SYNUCLEIN; MALIGNANT MELANONA.; NEUROBLASTOMA; PARKINSON'S DISEASE; PESTICIDES;

ALPHA-SYNUCLEIN; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; GLYCINE; HUMANS; INSECTICIDES; MANEB; MELANOMA; NEUROBLASTOMA; PARAQUAT; PARKINSON DISEASE; ROTENONE; TRANSDUCTION, GENETIC;

ADENOVIRIDAE;

EID: 84878495489     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft076     Document Type: Article

References (38)

1. Aguzzi, A. (2009). Cell biology: Beyond the prion principle. Nature 459 924-925.
2. Angot, E., Steiner, J. A., Lema Tomé, C. M., Ekström, P., Mattsson, B.,Björklund, A., and Brundin, P. (2012). Alphαsynuclein cell-to-cell transferand seeding in grafted dopaminergic neurons in vivo. PLoS ONE 7,e39465.
3. Barbosa, E. R., Leiros da Costa, M. D., Bacheschi, L. A., Scaff, M., and Leite,C. C. (2001). Parkinsonism after glycine-derivate exposure. Mov. Disord.16, 565-568.
4. Braak, H., de Vos, R. A., Bohl, J., and Del Tredici, K. (2006). Gastric alphasynuclein immunoreactive inclusions in Meissner,s and Auerbach,s plexusesin cases staged for Parkinson,s disease-related brain pathology. Neurosci.Lett. 396, 67-72.
5. Burns, R. S., Chiueh, C. C., Markey, S. P., Ebert, M. H., Jacobowitz, D. M., and Kopin, I. J. (1983). A primate model of parkinsonism: Selective destruction of dopaminergic neurons in the pars compacta of the substantia nigraN-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc. Natl. Acad. Sci. U.S.A. 80, 4546-4550.
6. Chartier-Harlin, M. C., Kachergus, J., Roumier, C., Mouroux, V., Douay, X., Lincoln, S., Levecque, C., Larvor, L., Andrieux, J., Hulihan, M., et al. (2004). Alphαsynuclein locus duplication as a cause of familial Parkinson,s disease. Lancet 364, 1167-1169.
7. Denizot, F., and Lang, R. (1986). Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89, 271-277.
8. Dennis, L. K., Lynch, C. F., Sandler, D. P., and Alavanja, M. C. (2010).Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ. Health Perspect. 118, 812-817.
9. Farrer, M., Kachergus, J., Forno, L., Lincoln, S., Wang, D. S., Hulihan, M., Maraganore, D., Gwinn-Hardy, K., Wszolek, Z., Dickson, D., et al. (2004). Comparison of kindreds with parkinsonism and alphαsynuclein genomic multiplications. Ann. Neurol. 55, 174-179.
10. Fuchs, J., Nilsson, C., Kachergus, J., Munz, M., Larsson, E. M., SchÜle, B., Langston, J. W., Middleton, F. A., Ross, O. A., Hulihan, M., et al. (2007). Phenotypic variation in a large Swedish pedigree due to SNCA duplication and triplication. Neurology 68, 916-922.
11. Gómez-Santos, C., Ferrer, I., Reiriz, J., Viñals, F., Barrachina, M., and Ambrosio, S. (2002). MPP+ increases alphαsynuclein expression and ERK/ MAP-kinase phosphorylation in human neuroblastoma SH-SY5Y cells.Brain Res. 935, 32-39.
12. Gr̈ndemann, J., Schlaudraff, F., Haeckel, O., and Liss, B. (2008). Elevated alphαsynuclein mRNA levels in individual UV-laser-microdissected dopaminergic substantia nigra neurons in idiopathic Parkinson,s disease. Nucleic Acids Res. 36, e38.
13. Hawkes, C. H., Del Tredici, K., and Braak, H. (2009). Parkinson,s disease: The dual hit theory revisited. Ann. N. Y. Acad. Sci. 1170, 615-622.
14. Ibáñez, P., Bonnet, A. M., Débarges, B., Lohmann, E., Tison, F., Pollak, P., Agid, Y., DÜrr, A., and Brice, A. (2004). Causal relation between alphasynuclein gene duplication and familial Parkinson,s disease. Lancet 364, 1169-1171.
15. Israeli, E., Yakunin, E., Zarbiv, Y., Hacohen-Solovich, A., Kisos, H., Loeb, V., Lichtenstein, M., Ben-Gedalya, T., Sabag, O., Pikarsky, E., et al. (2011). α-Synuclein expression selectively affects tumorigenesis in mice modeling Parkinson,s disease. PLoS ONE 6, e19622.
16. Jowaed, A., Schmitt, I., Kaut, O., and WÜllner, U. (2010). Methylation regulates alphαsynuclein expression and is decreased in Parkinson,s disease patients, brains. J. Neurosci. 30, 6355-6359.
17. Kisos, H., Pukaβ, K., Ben-Hur, T., Richter-Landsberg, C., and Sharon, R.(2012). Increased neuronal αsynuclein pathology associates with its accumulation in oligodendrocytes in mice modeling αsynucleinopathies. PLoS ONE 7, e46817.
18. Kovacs, G. G., Botond, G., and Budka, H. (2010). Protein coding of neurodegenerative dementias: The neuropathological basis of biomarker diagnostics. Acta Neuropathol. 119, 389-408.
19. Langston, J. W., Ballard, P., Tetrud, J. W., and Irwin, I. (1983). Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979-980.
20. Lee, B. R., and Kamitani, T. (2011). Improved immunodetection of endogenous αsynuclein. PLoS ONE 6, e23939.
21. Lee, S. J., Desplats, P., Sigurdson, C., Tsigelny, I., and Masliah, E. (2010). Cell-tocell transmission of non-prion protein aggregates. Nat. Rev. Neurol. 6, 702-706.
22. Matsumoto, L., Takuma, H., Tamaoka, A., Kurisaki, H., Date, H., Tsuji, S., and Iwata, A. (2010). CpG demethylation enhances alphαsynuclein expression and affects the pathogenesis of Parkinson,s disease. PLoS ONE 5, e15522.
23. Matsuo, Y., and Kamitani, T. (2010). Parkinson,s disease-related protein, alphasynuclein, in malignant melanoma. PLoS ONE 5, e10481.
24. Mink, P. J., Mandel, J. S., Lundin, J. I., and Sceurman, B. K. (2011). Epidemiologic studies of glyphosate and non-cancer health outcomes: A review. Regul. Toxicol. Pharmacol. 61, 172-184.
25. Mizuta, I., Satake, W., Nakabayashi, Y., Ito, C., Suzuki, S., Momose, Y., Nagai, Y., Oka, A., Inoko, H., Fukae, J., et al. (2006). Multiple candidate gene analysis identifies alphαsynuclein as a susceptibility gene for sporadic Parkinson,s disease. Hum. Mol. Genet. 15, 1151-1158.
26. Moretto, A., and Colosio, C. (2011). Biochemical and toxicological evidence of neurological effects of pesticides: The example of Parkinson,s disease. Neurotoxicology 32, 383-391.
27. Mougenot, A. L., Bétemps, D., Hogeveen, K. N., Kovacs, G. G., Chouaf- Lakhdar, L., Milhavet, O., Lehmann, S., Legastelois, S., Pin, J. J., and Baron, T. G. (2010). Production of a monoclonal antibody, against human αsynuclein, in a subpopulation of C57BL/6J mice, presenting a deletion of the αsynuclein locus. J. Neurosci. Methods 192, 268-276.
28. Mougenot, A. L., Nicot, S., Bencsik, A., Morignat, E., Verchère, J., Lakhdar, L., Legastelois, S., and Baron, T. (2012). Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol. Aging 33, 2225-2228.
29. Norris, E. H., Uryu, K., Leight, S., Giasson, B. I., Trojanowski, J. Q., and Lee, V. M. (2007). Pesticide exposure exacerbates alphαsynucleinopathy in an A53T transgenic mouse model. Am. J. Pathol. 170, 658-666.
30. Pan, T., Li, X., and Jankovic, J. (2011). The association between Parkinson,s disease and melanoma. Int. J. Cancer 128, 2251-2260.
31. Pan, T., Zhu, J., Hwu, W. J., and Jankovic, J. (2012). The role of alphasynuclein in melanin synthesis in melanoma and dopaminergic neuronal cells. PLoS ONE 7, e45183.
32. Pan-Montojo, F., Anichtchik, O., Dening, Y., Knels, L., Pursche, S., Jung, R., Jackson, S., Gille, G., Spillantini, M. G., Reichmann, H., et al. (2010). Progression of Parkinson,s disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE 5, e8762.
33. Pan-Montojo, F., Schwarz, M., Winkler, C., Arnhold, M., O'Sullivan, G. A., Pal, A., Said, J., Marsico, G., Verbavatz, J. M., Rodrigo-Angulo, M., et al. (2012). Environmental toxins trigger PD-like progression via increased alphαsynuclein release from enteric neurons in mice. Sci. Rep. 2, 898.
34. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., et al. (2003). alpha-Synuclein locus triplication causes Parkinson,s disease. Science 302, 841.
35. Sung, Y. H., and Eliezer, D. (2007). Residual structure, backbone dynamics, and interactions within the synuclein family. J. Mol. Biol. 372, 689-707.
36. Tanner, C. M., Kamel, F., Ross, G. W., Hoppin, J. A., Goldman, S. M., Korell, M., Marras, C., Bhudhikanok, G. S., Kasten, M., Chade, A. R., et al. (2011). Rotenone, paraquat, and Parkinson,s disease. Environ. Health Perspect. 119, 866-872.
37. Ulusoy, A., and Di Monte, D. A. (2013). α-Synuclein elevation in human neurodegenerative diseases: Experimental, pathogenetic, and therapeutic implications. Mol. Neurobiol. 47, 484-494.
38. Wills, J., Credle, J., Oaks, A. W., Duka, V., Lee, J. H., Jones, J., and Sidhu, A. (2012). Paraquat, but not maneb, induces synucleinopathy and tauopathy in striata of mice through inhibition of proteasomal and autophagic pathways. PLoS ONE 7, e30745