Rotenone and paraquat perturb dopamine metabolism: A computational analysis of pesticide toxicity

Toxicology

Volumn 315, Issue 1, 2014, Pages 92-101

  Qi, Zhen ^a,b   Miller, Gary W ^a,c   Voit, Eberhard O ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

Dopamine; Mathematical model; Mode of action; Paraquat; Parkinson's disease; Rotenone

Indexed keywords

DOPAMINE; PARAQUAT; PESTICIDE; ROTENONE;

ARTICLE; DOPAMINE METABOLISM; DOPAMINERGIC NERVE CELL; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; MATHEMATICAL MODEL; MONTE CARLO METHOD; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA PARS COMPACTA; SYSTEMS BIOLOGY;

EID: 84891410329     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.11.003     Document Type: Article

References (52)

1. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nature Neuroscience 2000, 3:1301-1306.
2. Brooks A.I., Chadwick C.A., Gelbard H.A., Cory-Slechta D.A., Federoff H.J. Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss. Brain Research 1999, 823:1-10.
3. Brown T.P., Rumsby P.C., Capleton A.C., Rushton L., Levy L.S. Pesticides and Parkinson's disease - is there a link?. Environmental Health Perspectives 2006, 114:156-164.
4. Chaudhuri A., Bowling K., Funderburk C., Lawal H., Inamdar A., Wang Z., O'Donnell J.M. Interaction of genetic and environmental factors in a Drosophila parkinsonism model. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2007, 27:2457-2467.
5. Chiang A.S., Lin C.Y., Chuang C.C., Chang H.M., Hsieh C.H., Yeh C.W., Shih C.T., Wu J.J., Wang G.T., Chen Y.C., Wu C.C., Chen G.Y., Ching Y.T., Lee P.C., Lin C.Y., Lin H.H., Wu C.C., Hsu H.W., Huang Y.A., Chen J.Y., Chiang H.J., Lu C.F., Ni R.F., Yeh C.Y., Hwang J.K. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Current Biology 2011, 21:1-11.
6. Cocheme H.M., Murphy M.P. Complex I is the major site of mitochondrial superoxide production by paraquat. The Journal of Biological Chemistry 2008, 283:1786-1798.
7. Costello S., Cockburn M., Bronstein J., Zhang X., Ritz B. Parkinson's disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. American Journal of Epidemiology 2009, 169:919-926.
8. Giasson B.I., Lee V.M. A new link between pesticides and Parkinson's disease. Nature Neuroscience 2000, 3:1227-1228.
9. Gorell J.M., Johnson 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.
10. Greenamyre J.T., Betarbet R., Sherer T.B. The rotenone model of Parkinson's disease: genes, environment and mitochondria. Parkinsonism & Related Disorders 2003, 9(Suppl. 2):S59-S64.
11. Hirata Y., Nagatsu T. Rotenone and CCCP inhibit tyrosine hydroxylation in rat striatal tissue slices. Toxicology 2005, 216:9-14.
12. Hirata Y., Suzuno H., Tsuruta T., Oh-hashi K., Kiuchi K. The role of dopamine transporter in selective toxicity of manganese and rotenone. Toxicology 2008, 244:249-256.
13. Kang M.J., Gil S.J., Koh H.C. Paraquat induces alternation of the dopamine catabolic pathways and glutathione levels in the substantia nigra of mice. Toxicology Letters 2009, 188:148-152.
14. Kopin I.J. MPTP: an industrial chemical and contaminant of illicit narcotics stimulates a new era in research on Parkinson's disease. Environmental Health Perspectives 1987, 75:45-51.
15. Lawal H.O., Chang H.Y., Terrell A.N., Brooks E.S., Pulido D., Simon A.F., Krantz D.E. The Drosophila vesicular monoamine transporter reduces pesticide-induced loss of dopaminergic neurons. Neurobiology of Disease 2010, 40:102-112.
16. Le Couteur D.G., McLean A.J., Taylor M.C., Woodham B.L., Board P.G. Pesticides and Parkinson's disease. Biomedicine & Pharmacotherapy 1999, 53:122-130.
17. Lee Y., Chen P.-W., Voit E.O. Analysis of operating principles with S-system models. Mathematical Biosciences 2011, 231:49-60.
18. Manly B.F.J. Randomization, Bootstrap and Monte Carlo Methods in Biology 2006, Chapman and Hall/CRC, Boca Raton, Fl, USA. third ed.
19. McCormack A.L., Thiruchelvam M., Manning-Bog A.B., Thiffault C., Langston J.W., Cory-Slechta D.A., Di Monte D.A. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiology of Disease 2002, 10:119-127.
20. Priyadarshi A., Khuder S.A., Schaub E.A., Shrivastava S. A meta-analysis of Parkinson's disease and exposure to pesticides. Neurotoxicology 2000, 21:435-440.
21. Qi Z., Fieni D., Tretter F., Voit E.O. The neurochemical mobile with non-linear interaction matrix: an exploratory computational model. Pharmacopsychiatry 2013, 46(Suppl. 1):S53-S63.
22. Qi Z., Kikuchi S., Tretter F., Voit E.O. Effects of dopamine and glutamate on synaptic plasticity: a computational modeling approach for drug abuse as comorbidity in mood disorders. Pharmacopsychiatry 2011, 44(Suppl. 1):S62-S75.
23. Qi Z., Miller G.M., Voit E.O. Mathematical models in schizophrenia. Handbook of Schizophrenia Spectrum Disorders 2011, vol. I. Springer Verlag, New York.
24. Qi Z., Miller G.M., Voit E.O. Mathematical models of dopamine metabolism in Parkinson's disease. Systems Biology of Parkinson's Disease 2012, Springer Science+Business Media, LLC, New York. P. Wellstead, M. Cloutier (Eds.).
25. Qi Z., Miller G.W., Voit E.O. Computational systems analysis of dopamine metabolism. PLoS ONE 2008, 3:e2444.
26. Qi Z., Miller G.W., Voit E.O. Computational analysis of determinants of dopamine (DA) dysfunction in DA nerve terminals. Synapse 2009, 63:1133-1142.
27. Qi Z., Miller G.W., Voit E.O. Computational modeling of synaptic neurotransmission as a tool for assessing dopamine hypotheses of schizophrenia. Pharmacopsychiatry 2010, 43(Suppl. 1):S50-S60.
28. Qi Z., Miller G.W., Voit E.O. The internal state of medium spiny neurons varies in response to different input signals. BMC Systems Biology 2010, 4:26.
29. Ramachandiran S., Hansen J.M., Jones D.P., Richardson J.R., Miller G.W. Divergent mechanisms of paraquat, MPP+, and rotenone toxicity: oxidation of thioredoxin and caspase-3 activation. Toxicological Sciences: An Official Journal of the Society of Toxicology 2007, 95:163-171.
30. Rappold P.M., Cui M., Chesser A.S., Tibbett J., Grima J.C., Duan L., Sen N., Javitch J.A., Tieu K. Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:20766-20771.
31. Ren J.P., Zhao Y.W., Sun X.J. Toxic influence of chronic oral administration of paraquat on nigrostriatal dopaminergic neurons in C57BL/6 mice. Chinese Medical Journal (English) 2009, 122:2366-2371.
32. Richardson J.R., Quan Y., Sherer T.B., Greenamyre J.T., Miller G.W. Paraquat neurotoxicity is distinct from that of MPTP and rotenone. Toxicological Sciences: An Official Journal of the Society of Toxicology 2005, 88:193-201.
33. Rowlands J.C., Casida J.E. NADH: ubiquinone oxidoreductase inhibitors block induction of ornithine decarboxylase activity in MCF-7 human breast cancer cells. Pharmacology & Toxicology 1998, 83:214-219.
34. Sai Y., Wu Q., Le W., Ye F., Li Y., Dong Z. Rotenone-induced PC12 cell toxicity is caused by oxidative stress resulting from altered dopamine metabolism. Toxicology In Vitro: An International Journal Published in Association with BIBRA 2008, 22:1461-1468.
35. Sakka N., Sawada H., Izumi Y., Kume T., Katsuki H., Kaneko S., Shimohama S., Akaike A. Dopamine is involved in selectivity of dopaminergic neuronal death by rotenone. NeuroReport 2003, 14:2425-2428.
36. Savageau M.A. Biochemical systems analysis. II. The steady-state solutions for an n-pool system using a power-law approximation. Journal of Theoretical Biology 1969, 25:370-379.
37. Semchuk K.M., Love E.J., Lee R.G. Parkinson's disease and exposure to agricultural work and pesticide chemicals. Neurology 1992, 42:1328-1335.
38. Sherer T.B., Betarbet R., Greenamyre J.T. Pesticides and Parkinson's disease. The Scientific World Journal 2001, 1:207-208.
39. Sherer T.B., Kim J.H., Betarbet R., Greenamyre J.T. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Experimental Neurology 2003, 179:9-16.
40. Shimizu K., Matsubara K., Ohtaki K., Fujimaru S., Saito O., Shiono H. Paraquat induces long-lasting dopamine overflow through the excitotoxic pathway in the striatum of freely moving rats. Brain Research 2003, 976:243-252.
41. Stathakis D.G., Burton D.Y., McIvor W.E., Krishnakumar S., Wright T.R., O'Donnell J.M. The catecholamines up (Catsup) protein of Drosophila melanogaster functions as a negative regulator of tyrosine hydroxylase activity. Genetics 1999, 153:361-382.
42. Tanner C.M., Goldman S.M. Epidemiology of Parkinson's disease. Neurologic Clinics 1996, 14:317-335.
43. Tanner C.M., Langston J.W. Do environmental toxins cause Parkinson's disease? A critical review. Neurology 1990, 40(Suppl.):17-30. (discussion 30-31).
44. Voit E.O. Computational Analysis of Biochemical Systems: A Practical Guide for Biochemists and Molecular Biologists 2000, Cambridge University Press, Cambridge, UK.
45. Voit E.O. A systems-theoretical framework for health and disease: inflammation and preconditioning from an abstract modeling point of view. Mathematical Biosciences 2009, 217:11-18.
46. Voit E.O. Biochemical Systems Theory: A Review. Int. Scholarly Research Network (ISRN-Biomathematics) 2013, 1-53.
47. Voit E.O., Qi Z., Kikuchi S. Mesoscopic models of neurotransmission as intermediates between disease simulators and tools for discovering design principles. Pharmacopsychiatry 2012, 45(Suppl. 1):S22-S30.
48. Voit E.O., Qi Z., Miller G.W. Steps of modeling complex biological systems. Pharmacopsychiatry 2008, 41(Suppl. 1):S78-S84.
49. Wang A., Costello S., Cockburn M., Zhang X., Bronstein J., Ritz B. Parkinson's disease risk from ambient exposure to pesticides. European Journal of Epidemiology 2011, 26:547-555.
50. Watabe M., Nakaki T. Mitochondrial complex I inhibitor rotenone-elicited dopamine redistribution from vesicles to cytosol in human dopaminergic SH-SY5Y cells. The Journal of Pharmacology and Experimental Therapeutics 2007, 323:499-507.
51. Watabe M., Nakaki T. Mitochondrial complex I inhibitor rotenone inhibits and redistributes vesicular monoamine transporter 2 via nitration in human dopaminergic SH-SY5Y cells. Molecular Pharmacology 2008, 74:933-940.
52. Wu J., Qi Z., Voit E.O. Impact of delays and noise on dopamine signal transduction. Studies in Health Technology and Informatics 2011, 162:222-235.