An update on the rotenone models of Parkinson's disease: Their ability to reproduce the features of clinical disease and model gene-environment interactions

NeuroToxicology

Volumn 46, Issue , 2015, Pages 101-116

  Johnson, Michaela E ^a   Bobrovskaya, Larisa ^a  

^a UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

Animal model; Gene environment interactions; Non motor symptoms; Parkinson's disease; Rotenone

Indexed keywords

ALPHA SYNUCLEIN; BACOPA MONNIERI EXTRACT; IBUPROFEN; LYCOPENE; MELATONIN; NEUROPROTECTIVE AGENT; PLANT EXTRACT; ROTENONE; TESTOSTERONE; TOMATO EXTRACT; UNCLASSIFIED DRUG; INSECTICIDE;

ANXIETY; CAENORHABDITIS ELEGANS; CIRCADIAN RHYTHM; CLINICAL FEATURE; COGNITIVE DEFECT; DEPRESSION; DIGESTIVE SYSTEM FUNCTION DISORDER; DOPAMINERGIC SYSTEM; DROSOPHILA; GENETIC ASSOCIATION; GENETIC MODEL; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HYPOSMIA; LYMNAEA STAGNALIS; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; REVIEW; RODENT MODEL; SLEEP DISORDER; STRIATONIGRAL DEGENERATION; ZEBRA FISH; ANIMAL; DISEASE MODEL; GENETICS;

ANIMALIA; PARKINSONIA;

ANIMALS; DISEASE MODELS, ANIMAL; GENE-ENVIRONMENT INTERACTION; HUMANS; INSECTICIDES; PARKINSON DISEASE; ROTENONE;

EID: 84920184454     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2014.12.002     Document Type: Review

References (192)

1. Abeliovich A., Schmitz Y., Fariñas I., Choi-Lundberg D., Ho W.-H., Castillo P.E., et al. Mice lacking α-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 2000, 25:239-252.
2. Ahn T.-B., Kim S., Kim J., Park S.-S., Lee D., Min H., et al. α-Synuclein gene duplication is present in sporadic Parkinson disease. Neurology 2008, 70:43-49.
3. Alam M., Mayerhofer A., Schmidt W.J. The neurobehavioral changes induced by bilateral rotenone lesion in medial forebrain bundle of rats are reversed by l-DOPA. Behav Brain Res 2004, 151:117-124.
4. Alam M., Schmidt W.J. Rotenone destroys dopaminergic neurons and induces Parkinsonian symptoms in rats. Behav Brain Res 2002, 136:317-324.
5. Alam M., Schmidt W.J. Mitochondrial complex I inhibition depletes plasma testosterone in the rotenone model of Parkinson's disease. Physiol Behav 2004, 83:395-400.
6. Anichtchik O., Diekmann H., Fleming A., Roach A., Goldsmith P., Rubinsztein D.C. Loss of PINK1 function affects development and results in neurodegeneration in zebrafish. J Neurosci 2008, 28:8199-8207.
7. Antolin I., Mayo J.C., Sainz R.M., del Brio Mde L., Herrera F., Martin V., et al. Protective effect of melatonin in a chronic experimental model of Parkinson's disease. Brain Res 2002, 943:163-173.
8. Bai Q., Mullett S.J., Garver J.A., Hinkle D.A., Burton E.A. Zebrafish DJ-1 is evolutionarily conserved and expressed in dopaminergic neurons. Brain Res 2006, 1113:33-44.
9. Bardien S., Lesage S., Brice A., Carr J. Genetic characteristics of leucine-rich repeat kinase 2 (LRRK2) associated Parkinson's disease. Parkinsonism Relat Disord 2011, 17:501-508.
10. Bassani T.B., Gradowski R.W., Zaminelli T., Barbiero J.K., Santiago R.M., Boschen S.L., et al. Neuroprotective and antidepressant-like effects of melatonin in a rotenone-induced Parkinson's disease model in rats. Brain Res 2014, [Epub ahead of print]. 10.1016/j.brainres.2014.09.068.
11. Betarbet R., Canet-Aviles R.M., Sherer T.B., Mastroberardino P.G., McLendon C., Kim J.H., et al. Intersecting pathways to neurodegeneration in Parkinson's disease: effects of the pesticide rotenone on DJ-1, α-synuclein, and the ubiquitin-proteasome system. Neurobiol Dis 2006, 22:404-420.
12. Betarbet R., Sherer T.B., Greenamyre J.T. Animal models of Parkinson's disease. Bioessays 2002, 24:308-318.
13. 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. Nat Neurosci 2000, 3:1301-1306.
14. Bonifati V., Rizzu P., van Baren M.J., Schaap O., Breedveld G.J., Krieger E., et al. Mutations in the DJ-1 gene associated with autosomal recessive early-onset Parkinsonism. Science 2003, 299:256-259.
15. Bonifati V., Rohe C., Breedveld G., Fabrizio E., De Mari M., Tassorelli C., et al. Early-onset Parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology 2005, 65:87-95.
16. Braak H., Braak E., Yilmazer D., Schultz C., de Vos R.A., Jansen E.N. Nigral and extranigral pathology in Parkinson's disease. J Neural Transm Suppl 1995, 46:15-31.
17. Braak H., de Vos R.A., Bohl J., Del Tredici K. Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 2006, 396:67-72.
18. Braak H., Del Tredici K. Invited article: nervous system pathology in sporadic Parkinson disease. Neurology 2008, 70:1916-1925.
19. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003, 24:197-211.
20. Bretaud S., Lee S., Guo S. Sensitivity of zebrafish to environmental toxins implicated in Parkinson's disease. Neurotoxicol Teratol 2004, 26:857-864.
21. Burn D.J. Beyond the iron mask: towards better recognition and treatment of depression associated with Parkinson's disease. Mov Disord 2002, 17:445-454.
22. Cannon J.R., Geghman K.D., Tapias V., Sew T., Dail M.K., Li C., et al. Expression of human E46K-mutated alpha-synuclein in BAC-transgenic rats replicates early-stage Parkinson's disease features and enhances vulnerability to mitochondrial impairment. Exp Neurol 2013, 240:44-56.
23. Cannon J.R., Tapias V., Na H.M., Honick A.S., Drolet R.E., Greenamyre J.T. A highly reproducible rotenone model of Parkinson's disease. Neurobiol Dis 2009, 34:279-290.
24. Carriere C.H., Kang N.H., Niles L.P. Neuroprotection by valproic acid in an intrastriatal rotenone model of Parkinson's disease. Neuroscience 2014, 267:114-121.
25. Cersosimo M.G., Benarroch E.E. Neural control of the gastrointestinal tract: implications for Parkinson disease. Mov Disord 2008, 23:1065-1075.
26. Cersosimo M.G., Raina G.B., Pecci C., Pellene A., Calandra C.R., Gutierrez C., et al. Gastrointestinal manifestations in Parkinson's disease: prevalence and occurrence before motor symptoms. J Neurol 2013, 260:1332-1338.
27. Chandran G. Neuroprotective effect of aqueous extract of Selaginella delicatula as evidenced by abrogation of rotenone-induced motor deficits, oxidative dysfunctions, and neurotoxicity in mice. Cell Mol Neurobiol 2013, 33:929-942.
28. Chase R. Behavior and its neural control in gastropod molluscs 2002, Oxford University Press, New York.
29. Cheng H.C., Ulane C.M., Burke R.E. Clinical progression in Parkinson disease and the neurobiology of axons. Ann Neurol 2010, 67:715-725.
30. Choi J., Sullards M.C., Olzmann J.A., Rees H.D., Weintraub S.T., Bostwick D.E., et al. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J Biol Chem 2006, 281:10816-10824.
31. Cicchetti F., Drouin-Ouellet J., Gross R.E. Environmental toxins and Parkinson's disease: what have we learned from pesticide-induced animal models. Trends Pharmacol Sci 2009, 30:475-483.
32. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 2006, 441:1162-1166.
33. Coulom H., Birman S. Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J Neurosci 2004, 24:10993-10998.
34. de Rijk M.C., Launer L.J., Berger K., Breteler M.M., Dartigues J.F., Baldereschi M., et al. Prevalence of Parkinson's disease in Europe: a collaborative study of population-based cohorts. Neurologic Diseases in the Elderly Research Group. Neurology 2000, 54:S21-S23.
35. Dickson D.W., Fujishiro H., Orr C., DelleDonne A., Josephs K.A., Frigerio R., et al. Neuropathology of non-motor features of Parkinson disease. Parkinsonism Relat Disord 2009, 15(Suppl. 3):S1-S5.
36. Dos Santos A.C., Castro M.A., Jose E.A., Delattre A.M., Dombrowski P.A., Da Cunha C., et al. REM sleep deprivation generates cognitive and neurochemical disruptions in the intranigral rotenone model of Parkinson's disease. J Neurosci Res 2013, 91:1508-1516.
37. Doty R.L. Olfaction in Parkinson's disease and related disorders. Neurobiol Dis 2012, 46:527-552.
38. Drolet R.E., Cannon J.R., Montero L., Greenamyre J.T. Chronic rotenone exposure reproduces Parkinson's disease gastrointestinal neuropathology. Neurobiol Dis 2009, 36:96-102.
39. Duty S., Jenner P. Animal models of Parkinson's disease: a source of novel treatments and clues to the cause of the disease. Br J Pharmacol 2011, 164:1357-1391.
40. Edwards L.L., Pfeiffer R.F., Quigley E.M.M., Hofman R., Balluff M. Gastrointestinal symptoms in Parkinson's disease. Mov Disord 1991, 6:151-156.
41. Eng L.F., Ghirnikar R.S. GFAP and astrogliosis. Brain Pathol 1994, 4:229-237.
42. Exner N., Treske B., Paquet D., Holmström K., Schiesling C., Gispert S., et al. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci 2007, 27:12413-12418.
43. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
44. Feany M.B., Pallanck L.J. Parkin: a multipurpose neuroprotective agent. Neuron 2003, 38:13-16.
45. Fernandez M., Barcia E., Fernandez-Carballido A., Garcia L., Slowing K., Negro S. Controlled release of rasagiline mesylate promotes neuroprotection in a rotenone-induced advanced model of Parkinson's disease. Int J Pharm 2012, 438:266-278.
46. Fernandez M., Negro S., Slowing K., Fernandez-Carballido A., Barcia E. An effective novel delivery strategy of rasagiline for Parkinson's disease. Int J Pharm 2011, 419:271-280.
47. Ferris C.F., Marella M., Smerkers B., Barchet T.M., Gershman B., Matsuno-Yagi A., et al. A phenotypic model recapitulating the neuropathology of Parkinson's disease. Brain Behav 2013, 3:351-366.
48. Finlayson B., Schnick R., Skaar D., Anderson J., Demong L., Duffield D., et al. Rotenone use in fish management and Parkinson's disease: another look. Fisheries 2012, 37:471-474.
49. Fleming S.M., Zhu C., Fernagut P.O., Mehta A., DiCarlo C.D., Seaman R.L., et al. Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone. Exp Neurol 2004, 187:418-429.
50. Flinn L., Bretaud S., Lo C., Ingham P.W., Bandmann O. Zebrafish as a new animal model for movement disorders. J Neurochem 2008, 106:1991-1997.
51. Flinn L., Mortiboys H., Volkmann K., Koster R.W., Ingham P.W., Bandmann O. Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio). Brain 2009, 132:1613-1623.
52. Forsyth C.B., Shannon K.M., Kordower J.H., Voigt R.M., Shaikh M., Jaglin J.A., et al. Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS ONE 2011, 6:e28032.
53. Frisina P.G., Haroutunian V., Libow L.S. The neuropathological basis for depression in Parkinson's disease. Parkinsonism Relat Disord 2009, 15:144-148.
54. Garcia-Garcia F., Ponce S., Brown R., Cussen V., Krueger J.M. Sleep disturbances in the rotenone animal model of Parkinson disease. Brain Res 2005, 1042:160-168.
55. Gasser T. Genetics of Parkinson's disease. J Neurol 2001, 248:833-840.
56. George S., San Mok S., Nurjono M., Ayton S., Finkelstein D.I., Masters C.L., et al. α-Synuclein transgenic mice reveal compensatory increases in Parkinson's disease-associated proteins DJ-1 and parkin and have enhanced α-synuclein and PINK1 levels after rotenone treatment. J Mol Neurosci 2010, 42:243-254.
57. Girish C., Muralidhara Propensity of Selaginella delicatula aqueous extract to offset rotenone-induced oxidative dysfunctions and neurotoxicity in Drosophila melanogaster: implications for Parkinson's disease. Neurotoxicology 2012, 33:444-456.
58. Gispert S., Ricciardi F., Kurz A., Azizov M., Hoepken H.-H., Becker D., et al. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS ONE 2009, 4:e5777.
59. Gokul K. Oral supplements of aqueous extract of tomato seeds alleviate motor abnormality, oxidative impairments and neurotoxicity induced by rotenone in mice: relevance to Parkinson's disease. Neurochem Res 2014, 39:1382-1394.
60. Greenamyre J.T., Cannon J.R., Drolet R., Mastroberardino P.G. Lessons from the rotenone model of Parkinson's disease. Trends Pharmacol Sci 2010, 31:141-142.
61. Greene J.G., Noorian A.R., Srinivasan S. Delayed gastric emptying and enteric nervous system dysfunction in the rotenone model of Parkinson's disease. Exp Neurol 2009, 218:154-161.
62. Halliday G., Lees A., Stern M. Milestones in Parkinson's disease - clinical and pathologic features. Mov Disord 2011, 26:1015-1021.
63. Harding A.J., Stimson E., Henderson J.M., Halliday G.M. Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. Brain 2002, 125:2431-2445.
64. Hatano Y., Li Y., Sato K., Asakawa S., Yamamura Y., Tomiyama H., et al. Novel PINK1 mutations in early-onset Parkinsonism. Ann Neurol 2004, 56:424-427.
65. Hawkes C.H., Del Tredici K., Braak H. Parkinson's disease: a dual-hit hypothesis. Neuropathol Appl Neurobiol 2007, 33:599-614.
66. He Y., Imam S.Z., Dong Z., Jankovic J., Ali S.F., Appel S.H., et al. Role of nitric oxide in rotenone-induced nigrostriatal injury. J Neurochem 2003, 86:1338-1345.
67. Hedrich K., Djarmati A., Schäfer N., Hering R., Wellenbrock C., Weiss P., et al. DJ-1 (PARK7) mutations are less frequent than Parkin (PARK2) mutations in early-onset Parkinson disease. Neurology 2004, 62:389-394.
68. Heikkila R., Nicklas W., Vyas I., Duvoisin R. Dopaminergic toxicity of rotenone and the 1-methyl-4-phenylpyridinium ion after their stereotaxic administration to rats: implication for the mechanism of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. Neurosci Lett 1985, 62:389-394.
69. Hien P., Gortnizka H., Kraemer R. Rotenone-potential and prospect for sustainable agriculture. Omonrice 2003, 11:83-92.
70. Hoglinger G.U., Feger J., Prigent A., Michel P.P., Parain K., Champy P., et al. Chronic systemic complex I inhibition induces a hypokinetic multisystem degeneration in rats. J Neurochem 2003, 84:491-502.
71. Hoglinger G.U., Lannuzel A., Khondiker M.E., Michel P.P., Duyckaerts C., Feger J., et al. The mitochondrial complex I inhibitor rotenone triggers a cerebral tauopathy. J Neurochem 2005, 95:930-939.
72. Hoglinger G.U., Oertel W.H., Hirsch E.C. The rotenone model of Parkinsonism - the five years inspection. J Neural Transm Suppl 2006, 70:269-272.
73. Hosamani R., Muralidhara Neuroprotective efficacy of Bacopa monnieri against rotenone induced oxidative stress and neurotoxicity in Drosophila melanogaster. Neurotoxicology 2009, 30:977-985.
74. Hosamani R., Ramesh S.R., Muralidhara Attenuation of rotenone-induced mitochondrial oxidative damage and neurotoxicity in Drosophila melanogaster supplemented with creatine. Neurochem Res 2010, 35:1402-1412.
75. Huang J., Liu H., Gu W., Yan Z., Xu Z., Yang Y., et al. A delivery strategy for rotenone microspheres in an animal model of Parkinson's disease. Biomaterials 2006, 27:937-946.
76. Huisman E., Uylings H.B., Hoogland P.V. Gender-related changes in increase of dopaminergic neurons in the olfactory bulb of Parkinson's disease patients. Mov Disord 2008, 23:1407-1413.
77. Huisman E., Uylings H.B.M., Hoogland P.V. A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson's disease. Mov Disord 2004, 19:687-692.
78. Hwang R.D., Wiemerslage L., LaBreck C.J., Khan M., Kannan K., Wang X., et al. The neuroprotective effect of human uncoupling protein 2 (hUCP2) requires cAMP-dependent protein kinase in a toxin model of Parkinson's disease. Neurobiol Dis 2014, 69:180-191.
79. Imai Y., Soda M., Takahashi R. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J Biol Chem 2000, 275:35661-35664.
80. Inden M., Kitamura Y., Abe M., Tamaki A., Takata K., Taniguchi T. Parkinsonian rotenone mouse model: reevaluation of long-term administration of rotenone in C57BL/6 mice. Biol Pharm Bull 2011, 34:92-96.
81. Inden M., Kitamura Y., Takeuchi H., Yanagida T., Takata K., Kobayashi Y., et al. Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J Neurochem 2007, 101:1491-1504.
82. Islam R., Yang L., Sah M., Kannan K., Anamani D., Vijayan C., et al. A neuroprotective role of the human uncoupling protein 2 (hUCP2) in a Drosophila Parkinson's disease model. Neurobiol Dis 2012, 46:137-146.
83. Jayanth A., Talkad M.S. Neuroprotective activity of Stachytrapheta indica on rotenone induced Parkinson's disease in zebrafish. World J Pharm Pharm Sci 2014, 3:940-955.
84. Jellinger K.A. Synuclein deposition and non-motor symptoms in Parkinson disease. J Neurol Sci 2011, 310:107-111.
85. Jia F., Song N., Zhao C., Xie J., Jiang H. Unexpected improvements of spatial learning and memory abilities in chronic rotenone intoxicated mice. PLOS ONE 2014, 9:e91641.
86. Kano O., Ikeda K., Cridebring D., Takazawa T., Yoshii Y., Iwasaki Y. Neurobiology of depression and anxiety in Parkinson's disease. Parkinson's Dis 2011, 2011:143547.
87. Karuppagounder S.S., Madathil S.K., Pandey M., Haobam R., Rajamma U., Mohanakumar K.P. Quercetin up-regulates mitochondrial complex-I activity to protect against programmed cell death in rotenone model of Parkinson's disease in rats. Neuroscience 2013, 236:136-148.
88. Kaur H., Chauhan S., Sandhir R. Protective effect of lycopene on oxidative stress and cognitive decline in rotenone induced model of Parkinson's disease. Neurochem Res 2011, 36:1435-1443.
89. Kim R.H., Smith P.D., Aleyasin H., Hayley S., Mount M.P., Pownall S., et al. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc Natl Acad Sci USA 2005, 102:5215-5220.
90. Lapointe N., St-Hilaire M., Martinoli M.G., Blanchet J., Gould P., Rouillard C., et al. Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J 2004, 18:717-719.
91. Lawal H.O., Chang H.Y., Terrell A.N., Brooks E.S., Pulido D., Simon A.F., et al. The Drosophila vesicular monoamine transporter reduces pesticide-induced loss of dopaminergic neurons. Neurobiol Dis 2010, 40:102-112.
92. Lax P., Esquiva G., Esteve-Rudd J., Otalora B.B., Madrid J.A., Cuenca N. Circadian dysfunction in a rotenone-induced parkinsonian rodent model. Chronobiol Int 2012, 29:147-156.
93. Lebouvier T., Chaumette T., Damier P., Coron E., Touchefeu Y., Vrignaud S., et al. Pathological lesions in colonic biopsies during Parkinson's disease. Gut 2008, 57:1741-1743.
94. Lesage S., Brice A. Role of Mendelian genes in sporadic Parkinson's disease. Parkinsonism Relat Disord 2012, 18(Suppl. 1):S66-S70.
95. Lewy F.H. Paralysis agitans: I. Pathologische anatomie. Handbuch der neurologie 1912, Springer-Verlag, Berlin.
96. Lima M.M. Sleep disturbances in Parkinson's disease: the contribution of dopamine in REM sleep regulation. Sleep Med Rev 2013, 17:367-375.
97. Lin C.H., Huang J.Y., Ching C.H., Chuang J.I. Melatonin reduces the neuronal loss, downregulation of dopamine transporter, and upregulation of D2 receptor in rotenone-induced parkinsonian rats. J Pineal Res 2008, 44:205-213.
98. Linhart R., Wong S.A., Cao J., Tran M., Huynh A., Ardrey C., et al. Vacuolar protein sorting 35 (Vps35) rescues locomotor deficits and shortened lifespan in Drosophila expressing a Parkinson's disease mutant of Leucine-Rich Repeat Kinase 2 (LRRK2). Mol Neurodegener 2014, 9:23. 10.1186/1750-1326-9-23.
99. Liu S., Ninan I., Antonova I., Battaglia F., Trinchese F., Narasanna A., et al. alpha-Synuclein produces a long-lasting increase in neurotransmitter release. EMBO J 2004, 23:4506-4516.
100. Lücking C.B., Dürr A., Bonifati V., Vaughan J., De Michele G., Gasser T., et al. Association between early-onset Parkinson's disease and mutations in the parkin gene. N Engl J Med 2000, 342:1560-1567.
101. Madathil S.K., Karuppagounder S.S., Mohanakumar K.P. Sodium salicylate protects against rotenone-induced Parkinsonism in rats. Synapse 2013, 67:502-514.
102. Marella M., Seo B.B., Nakamaru-Ogiso E., Greenamyre J.T., Matsuno-Yagi A., Yagi T. Protection by the NDI1 gene against neurodegeneration in a rotenone rat model of Parkinson's disease. PLoS ONE 2008, 3:e1433.
103. Marsh J.L., Thompson L.M. Drosophila in the study of neurodegenerative disease. Neuron 2006, 52:169-178.
104. Martinez T.N., Greenamyre J.T. Toxin models of mitochondrial dysfunction in Parkinson's disease. Antioxid Redox Signal 2012, 16:920-934.
105. Martinez-Martin P. The importance of non-motor disturbances to quality of life in Parkinson's disease. J Neurol Sci 2011, 310:12-16.
106. Meulener M., Whitworth A.J., Armstrong-Gold C.E., Rizzu P., Heutink P., Wes P.D., et al. Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr Biol 2005, 15:1572-1577.
107. Mizuta I., Satake W., Nakabayashi Y., Ito C., Suzuki S., Momose Y., et al. Multiple candidate gene analysis identifies α-synuclein as a susceptibility gene for sporadic Parkinson's disease. Hum Mol Genet 2006, 15:1151-1158.
108. Mocko J.B., Kern A., Moosmann B., Behl C., Hajieva P. Phenothiazines interfere with dopaminergic neurodegeneration in Caenorhabditis elegans models of Parkinson's disease. Neurobiol Dis 2010, 40:120-129.
109. Morais L.H., Lima M.M.S., Martynhak B.J., Santiago R., Takahashi T.T., Ariza D., et al. Characterization of motor, depressive-like and neurochemical alterations induced by a short-term rotenone administration. Pharmacol Rep 2012, 64:1081-1090.
110. Morgan W.W., Nelson J.F. Chronic administration of pharmacological levels of melatonin does not ameliorate the MPTP-induced degeneration of the nigrostriatal pathway. Brain Res 2001, 921:115-121.
111. Mulcahy P., O'Doherty A., Paucard A., O'Brien T., Kirik D., Dowd E. Development and characterisation of a novel rat model of Parkinson's disease induced by sequential intranigral administration of AAV-α-synuclein and the pesticide, rotenone. Neuroscience 2012, 203:170-179.
112. Mulcahy P., O'Doherty A., Paucard A., O'Brien T., Kirik D., Dowd E. The behavioural and neuropathological impact of intranigral AAV-α-synuclein is exacerbated by systemic infusion of the Parkinson's disease-associated pesticide, rotenone, in rats. Behav Brain Res 2013, 243:6-15.
113. Mulcahy P., Walsh S., Paucard A., Rea K., Dowd E. Characterisation of a novel model of Parkinson's disease by intra-striatal infusion of the pesticide rotenone. Neuroscience 2011, 181:234-242.
114. Mundinano I.C., Caballero M.C., Ordonez C., Hernandez M., DiCaudo C., Marcilla I., et al. Increased dopaminergic cells and protein aggregates in the olfactory bulb of patients with neurodegenerative disorders. Acta Neuropathol 2011, 122:61-74.
115. Murakami S., Miyazaki I., Sogawa N., Miyoshi K., Asanuma M. Neuroprotective effects of metallothionein against rotenone-induced myenteric neurodegeneration in Parkinsonian mice. Neurotox Res 2014, 26:285-298.
116. Natale G., Kastsiushenka O., Fulceri F., Ruggieri S., Paparelli A., Fornai F. MPTP-induced Parkinsonism extends to a subclass of TH-positive neurons in the gut. Brain Res 2010, 1355:195-206.
117. Navarro J.A., Hessner S., Yenisetti S.C., Bayersdorfer F., Zhang L., Voigt A., et al. Analysis of dopaminergic neuronal dysfunction in genetic and toxin-induced models of Parkinson's disease in Drosophila. J Neurochem 2014, 131:369-382.
118. Ng C.H., Mok S.Z., Koh C., Ouyang X., Fivaz M.L., Tan E.K., et al. Parkin protects against LRRK2 G2019S mutant-induced dopaminergic neurodegeneration in Drosophila. J Neurosci 2009, 29:11257-11262.
119. Nishioka K., Ross O.A., Ishii K., Kachergus J.M., Ishiwata K., Kitagawa M., et al. Expanding the clinical phenotype of SNCA duplication carriers. Mov Disord 2009, 24:1811-1819.
120. Nuytemans K., Theuns J., Cruts M., Van Broeckhoven C. Genetic etiology of Parkinson disease associated with mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 genes: a mutation update. Hum Mutat 2010, 31:763-780.
121. Okun M.S., DeLong M.R., Hanfelt J., Gearing M., Levey A. Plasma testosterone levels in Alzheimer and Parkinson diseases. Neurology 2004, 62:411-413.
122. Okun M.S., McDonald W.M., DeLong M.R. Refractory non-motor symptoms in male patients with Parkinson disease due to testosterone deficiency: a common unrecognized comorbidity. Arch Neurol 2002, 59:807-811.
123. Olanow C.W., Tatton W.G. Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 1999, 22:123-144.
124. Pan-Montojo F., Anichtchik O., Dening Y., Knels L., Pursche S., Jung R., et al. Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE 2010, 5:e8762.
125. Pandi-Perumal S.R., BaHammam A.S., Brown G.M., Spence D.W., Bharti V.K., Kaur C., et al. Melatonin antioxidative defense: therapeutical implications for aging and neurodegenerative processes. Neurotox Res 2013, 23:267-300.
126. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 2006, 441:1157-1161.
127. Perez F.A., Curtis W.R., Palmiter R.D. Parkin-deficient mice are not more sensitive to 6-hydroxydopamine or methamphetamine neurotoxicity. BMC Neurosci 2005, 6:71.
128. Pfeiffer R.F. Gastrointestinal dysfunction in Parkinson's disease. Parkinsonism Relat Disord 2011, 17:10-15.
129. Piccoli G., Condliffe S.B., Bauer M., Giesert F., Boldt K., De Astis S., et al. LRRK2 controls synaptic vesicle storage and mobilization within the recycling pool. J Neurosci 2011, 31:2225-2237.
130. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997, 276:2045-2047.
131. Prediger R.D., Aguiar A.S., Matheus F.C., Walz R., Antoury L., Raisman-Vozari R., et al. Intranasal administration of neurotoxicants in animals: support for the olfactory vector hypothesis of Parkinson's disease. Neurotox Res 2012, 21:90-116.
132. Ravenstijn P.G.M., Merlini M., Hameetman M., Murray T.K., Ward M.A., Lewis H., et al. The exploration of rotenone as a toxin for inducing Parkinson's disease in rats, for application in BBB transport and PK-PD experiments. J Pharmacol Toxicol Methods 2008, 57:114-130.
133. Ray A., Martinez B., Berkowitz L., Caldwell G., Caldwell K. Mitochondrial dysfunction, oxidative stress, and neurodegeneration elicited by a bacterial metabolite in a C. elegans Parkinson's model. Cell Death Dis 2014, 5:e984.
134. Rodrigues L.S., Targa A., Noseda A.C.D., Aurich M.F., Da Cunha C., Lima M. Olfactory impairment in the rotenone model of Parkinson's disease is associated with bulbar dopaminergic D2 activity after REM sleep deprivation. Front Cell Neurosci 2014, 8:383.
135. Rohé C.F., Montagna P., Breedveld G., Cortelli P., Oostra B.A., Bonifati V. Homozygous PINK1 C-terminus mutation causing early-onset Parkinsonism. Ann Neurol 2004, 56:427-431.
136. Rojas J.C., Simola N., Kermath B.A., Kane J.R., Schallert T., Gonzalez-Lima F. Striatal neuroprotection with methylene blue. Neuroscience 2009, 163:877-889.
137. Rojo A., Cavada C., Rosa de Sagarra M., Cuadrado A. Chronic inhalation of rotenone or paraquat does not induce Parkinson's disease symptoms in mice or rats. Exp Neurol 2007, 208:120-126.
138. Ross O.A., Wu Y.R., Lee M.C., Funayama M., Chen M.L., Soto A.I., et al. Analysis of Lrrk2 R1628P as a risk factor for Parkinson's disease. Ann Neurol 2008, 64:88-92.
139. Sager J.J., Bai Q., Burton E.A. Transgenic zebrafish models of neurodegenerative diseases. Brain Struct Funct 2010, 214:285-302.
140. Saha S., Guillily M.D., Ferree A., Lanceta J., Chan D., Ghosh J., et al. LRRK2 modulates vulnerability to mitochondrial dysfunction in Caenorhabditis elegans. J Neurosci 2009, 29:9210-9218.
141. Salam S., Ansari A., Amon S., Rezai P., Selvaganapathy P.R., Mishra R.K., et al. A microfluidic phenotype analysis system reveals function of sensory and dopaminergic neuron signaling in C. elegans electrotactic swimming behavior. Worm 2013, 2:e24558.
142. Salama M., Ellaithy A., Helmy B., El-Gamal M., Tantawy D., Mohamed M., et al. Colchicine protects dopaminergic neurons in a rat model of Parkinson's disease. CNS Neurol Disord Drug Targets 2012, 11:836-843.
143. Santiago R.M., Barbieiro J., Lima M.M., Dombrowski P.A., Andreatini R., Vital M.A. Depressive-like behaviors alterations induced by intranigral MPTP, 6-OHDA, LPS and rotenone models of Parkinson's disease are predominantly associated with serotonin and dopamine. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:1104-1114.
144. Saravanan K.S., Sindhu K.M., Mohanakumar K.P. Acute intranigral infusion of rotenone in rats causes progressive biochemical lesions in the striatum similar to Parkinson's disease. Brain Res 2005, 1049:147-155.
145. Savitt J.M., Dawson V.L., Dawson T.M. Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Invest 2006, 116:1744-1754.
146. Sharma N., Nehru B. Beneficial effect of vitamin E in rotenone induced model of PD: behavioural, neurochemical and biochemical study. Exp Neurobiol 2013, 22:214-223.
147. Sharma R., McMillan C.R., Tenn C.C., Niles L.P. Physiological neuroprotection by melatonin in a 6-hydroxydopamine model of Parkinson's disease. Brain Res 2006, 1068:230-236.
148. Sherer T.B., Betarbet R., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., et al. Mechanism of toxicity in rotenone models of Parkinson's disease. J Neurosci 2003, 23:10756-10764.
149. Sherer T.B., Kim J.H., Betarbet R., Greenamyre J.T. Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol 2003, 179:9-16.
150. Shimura H., Hattori N., Kubo S-i Mizuno Y., Asakawa S., Minoshima S., et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 2000, 25:302-305.
151. Shulman J.M., De Jager P.L., Feany M.B. Parkinson's disease: genetics and pathogenesis. Annu Rev Pathol Mech Dis 2011, 6:193-222.
152. Silvestri L., Caputo V., Bellacchio E., Atorino L., Dallapiccola B., Valente E.M., et al. Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive Parkinsonism. Hum Mol Genet 2005, 14:3477-3492.
153. Sindhu K.M., Saravanan K.S., Mohanakumar K.P. Behavioral differences in a rotenone-induced hemi-Parkinsonian rat model developed following intranigral or median forebrain bundle infusion. Brain Res 2005, 1051:25-34.
154. Singaram C., Ashraf W., Gaumnitz E.A., Torbey C., Sengupta A., Pfeiffer R., et al. Dopaminergic defect of enteric nervous system in Parkinson's disease patients with chronic constipation. Lancet 1995, 346:861-864.
155. Soloway S.B. Naturally occurring insecticides. Environ Health Perspect 1976, 14:109-117.
156. Sonia Angeline M., Chaterjee P., Anand K., Ambasta R.K., Kumar P. Rotenone-induced Parkinsonism elicits behavioral impairments and differential expression of parkin, heat shock proteins and caspases in the rat. Neuroscience 2012, 220:291-301.
157. Sonia Angeline M., Sarkar A., Anand K., Ambasta R.K., Kumar P. Sesamol and naringenin reverse the effect of rotenone-induced PD rat model. Neuroscience 2013, 254:379-394.
158. St Laurent R., O'Brien L.M., Ahmad S.T. Sodium butyrate improves locomotor impairment and early mortality in a rotenone-induced Drosophila model of Parkinson's disease. Neuroscience 2013, 246:382-390.
159. Subramanian P., Prasanna V., Jayapalan J.J., Abdul Rahman P.S., Hashim O.H. Role of Bacopa monnieri in the temporal regulation of oxidative stress in clock mutant (cryb) of Drosophila melanogaster. J Insect Physiol 2014, 65:37-44.
160. Sudati J.H., Vieira F.A., Pavin S.S., Dias G.R., Seeger R.L., Golombieski R., et al. Valeriana officinalis attenuates the rotenone-induced toxicity in Drosophila melanogaster. Neurotoxicology 2013, 37:118-126.
161. Suetomi K., Mereiter S., Mori C., Takanami T., Higashitani A. Caenorhabditis elegans ATR checkpoint kinase ATL-1 influences life span through mitochondrial maintenance. Mitochondrion 2013, 13:729-735.
162. Tan E., Tan L.C., Lim H., Li R., Tang M., Yih Y., et al. LRRK2 R1628P increases risk of Parkinson's disease: replication evidence. Hum Genet 2008, 124:287-288.
163. Tan E.K., Yew K., Chua E., Puvan K., Shen H., Lee E., et al. PINK1 mutations in sporadic early-onset Parkinson's disease. Mov Disord 2006, 21:789-793.
164. Tanner C.M., Kamel F., Ross G.W., Hoppin J.A., Goldman S.M., Korell M., et al. Rotenone, paraquat and Parkinson's disease. Environ Health Perspect 2011, 119:866-872.
165. Tapias V., Cannon J.R., Greenamyre J.T. Melatonin treatment potentiates neurodegeneration in a rat rotenone Parkinson's disease model. J Neurosci Res 2010, 88:420-427.
166. Tapias V., Cannon J.R., Greenamyre J.T. Pomegranate juice exacerbates oxidative stress and nigrostriatal degeneration in Parkinson's disease. Neurobiol Aging 2014, 35:1162-1176.
167. Tasselli M., Chaumette T., Paillusson S., Monnet Y., Lafoux A., Huchet-Cadiou C., et al. Effects of oral administration of rotenone on gastrointestinal functions in mice. Neurogastroenterol Motil 2013, 25:e183-e193.
168. Thakur P., Nehru B. Anti-inflammatory properties rather than anti-oxidant capability is the major mechanism of neuroprotection by sodium salicylate in a chronic rotenone model of Parkinson's disease. Neuroscience 2013, 231:420-431.
169. Thomas K.J., McCoy M.K., Blackinton J., Beilina A., van der Brug M., Sandebring A., et al. DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum Mol Genet 2010, 20:40-50.
170. Tong Y., Yamaguchi H., Giaime E., Boyle S., Kopan R., Kelleher R.J., et al. Loss of leucine-rich repeat kinase 2 causes impairment of protein degradation pathways, accumulation of alpha-synuclein, and apoptotic cell death in aged mice. Proc Natl Acad Sci USA 2010, 107:9879-9884.
171. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004, 304:1158-1160.
172. Valente E.M., Salvi S., Ialongo T., Marongiu R., Elia A.E., Caputo V., et al. PINK1 mutations are associated with sporadic early-onset Parkinsonism. Ann Neurol 2004, 56:336-341.
173. Ved R., Saha S., Westlund B., Perier C., Burnam L., Sluder A., et al. Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. J Biol Chem 2005, 280:42655-42668.
174. Vehovszky A., Szabo H., Hiripi L., Elliott C.J., Hernadi L. Behavioural and neural deficits induced by rotenone in the pond snail Lymnaea stagnalis: a possible model for Parkinson's disease in an invertebrate. Eur J Neurosci 2007, 25:2123-2130.
175. Venderova K., Kabbach G., Abdel-Messih E., Zhang Y., Parks R.J., Imai Y., et al. Leucine-rich repeat kinase 2 interacts with Parkin, DJ-1 and PINK-1 in a Drosophila melanogaster model of Parkinson's disease. Hum Mol Genet 2009, 18:4390-4404.
176. Wakabayashi K., Takahashi H., Takeda S., Ohama E., Ikuta F. Parkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses. Acta Neuropathol 1988, 76:217-221.
177. Wang C., Lu R., Ouyang X., Ho M.W., Chia W., Yu F., et al. Drosophila overexpressing parkin R275W mutant exhibits dopaminergic neuron degeneration and mitochondrial abnormalities. J Neurosci 2007, 27:8563-8570.
178. Wang D., Tang B., Zhao G., Pan Q., Xia K., Bodmer R., et al. Dispensable role of Drosophila ortholog of LRRK2 kinase activity in survival of dopaminergic neurons. Mol Neurodegener 2008, 3:3. 10.1186/1750-1326-3-3.
179. Webber P.J., West A.B. LRRK2 in Parkinson's disease: function in cells and neurodegeneration. FEBS J 2009, 276:6436-6444.
180. Wolozin B., Saha S., Guillily M., Ferree A., Riley M. Investigating convergent actions of genes linked to familial Parkinson's disease. Neurodegener Dis 2008, 5:182-185.
181. Wood W.B. The nematode Caenorhabditis elegans 1987, Cold Spring Harbour Laboratory, New York.
182. Wu L., Tian Y.-Y., Shi J.-P., Xie W., Shi J.-Q., Lu J., et al. Inhibition of endoplasmic reticulum stress is involved in the neuroprotective effects of candesartan cilexitil in the rotenone rat model of Parkinson's disease. Neurosci Lett 2013, 548:50-55.
183. Xiong N., Huang J., Zhang Z., Zhang Z., Xiong J., Liu X., et al. Stereotaxical infusion of rotenone: a reliable rodent model for Parkinson's disease. PLoS ONE 2009, 4:e7878.
184. Xiong N., Long X., Xiong J., Jia M., Chen C., Huang J., et al. Mitochondrial complex I inhibitor rotenone-induced toxicity and its potential mechanisms in Parkinson's disease models. Crit Rev Toxicol 2012, 42:613-632.
185. Xiong Y., Coombes C.E., Kilaru A., Li X., Gitler A.D., Bowers W.J., et al. GTPase activity plays a key role in the pathobiology of LRRK2. PLoS Genet 2010, 6:e1000902.
186. Yacoubian T.A., Slone S.R., Harrington A.J., Hamamichi S., Schieltz J.M., Caldwell K.A., et al. Differential neuroprotective effects of 14-3-3 proteins in models of Parkinson's disease. Cell Death Dis 2010, 1:e2.
187. Yi P.L., Tsai C.H., Lu M.K., Liu H.J., Chen Y.C., Chang F.C. Interleukin-1beta mediates sleep alteration in rats with rotenone-induced Parkinsonism. Sleep 2007, 30:413-425.
188. Zaminelli T., Gradowski R.W., Bassani T.B., Barbiero J.K., Santiago R.M., Maria-Ferreira D., et al. Antidepressant and antioxidative effect of ibuprofen in the rotenone model of Parkinson's disease. Neurotox Res 2014, 26:351-362.
189. Zhang Y., Gao J., Chung K.K., Huang H., Dawson V.L., Dawson T.M. Parkin functions as an E2-dependent ubiquitin-protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci USA 2000, 97:13354-13359.
190. Zhang Z., Burgunder J.M., An X., Wu Y., Chen W., Zhang J., et al. LRRK2 R1628P variant is a risk factor of Parkinson's disease among Han-Chinese from mainland China. Mov Disord 2009, 24:1902-1905.
191. Zhou S., Wang Z., Klaunig J.E. Caenorhabditis elegans neuron degeneration and mitochondrial suppression caused by selected environmental chemicals. Int J Biochem Mol Biol 2013, 4:191-200.
192. Zimprich A., Benet-Pages A., Struhal W., Graf E., Eck S.H., Offman M.N., et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am J Hum Genet 2011, 89:168-175.