Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Pan Montojo, Francisco ^a,c   Anichtchik, Oleg ^b   Dening, Yanina ^a   Knels, Lilla ^a   Pursche, Stefan ^a   Jung, Roland ^a   Jackson, Sandra ^a   Gille, Gabriele ^a   Spillantini, Maria Grazia ^b   Reichmann, Heinz ^a   Funk, Richard H W ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; PESTICIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE COURSE; ENVIRONMENTAL FACTOR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INFLAMMATION; INTESTINE INNERVATION; MOTONEURON NUCLEUS; MOTOR DYSFUNCTION; MOUSE; NERVOUS SYSTEM FUNCTION; NEUROANATOMY; NEUROCHEMISTRY; NONHUMAN; PARKINSON DISEASE; PROTEIN PHOSPHORYLATION; RESPIRATORY CHAIN; VAGUS NERVE NUCLEUS; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; DRUG EFFECT; PATHOLOGY; STOMACH;

DASHEEN MOSAIC VIRUS; MUS;

ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; ENTERIC NERVOUS SYSTEM; MICE; MICE, INBRED BALB C; PARKINSON DISEASE; ROTENONE; STOMACH;

EID: 77649284470     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008762     Document Type: Article

References (60)

1. de Rijk MC, Launer LJ, Berger K, Breteler MM, Dartigues JF, et al. (2000) Prevalence of Parkinson's disease in Europe: A collaborative study of population-based cohorts. Neurologic Diseases in the Elderly Research Group. Neurology 54: S21-23.
2. Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, et al. (2003) Movement Disorders Society Scientific Issues Committee report: SIC Task Force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18: 467-486.
3. Crossman AR (1989) Neural mechanisms in disorders of movement. Comp Biochem Physiol A Comp Physiol 93: 141-149.
4. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375.
5. Lang AE, Obeso JA (2004) Time to move beyond nigrostriatal dopamine deficiency in Parkinson's disease. Ann Neurol 55: 761-765.
6. Chaudhuri KR, Martinez-Martin P (2008) Quantitation of non-motor symptoms in Parkinson's disease. Eur J Neurol 15 Suppl 2: 2-7.
7. Adler CH, Thorpy MJ (2005) Sleep issues in Parkinson's disease. Neurology 64: S12-20.
8. Abbott RD, Petrovitch H, White LR, Masaki KH, Tanner CM, et al. (2001) Frequency of bowel movements and the future risk of Parkinson's disease. Neurology 57: 456-462.
9. Ross GW, Abbott RD, Petrovitch H, Tanner CM, Davis DG, et al. (2006) Association of olfactory dysfunction with incidental Lewy bodies. Mov Disord 21: 2062-2067.
10. Ponsen MM, Stoffers D, Booij J, van Eck-Smit BL, Wolters E, et al. (2004) Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Ann Neurol 56: 173-181.
11. Hawkes CH, Shephard BC, Daniel SE (1999) Is Parkinson's disease a primary olfactory disorder? Qjm 92: 473-480.
12. Pfeiffer RF (2003) Gastrointestinal dysfunction in Parkinson's disease. Lancet Neurol 2: 107-116.
13. Goldstein DS (2006) Orthostatic hypotension as an early finding in Parkinson's disease. Clin Auton Res 16: 46-54.
14. Goetz CG, Tanner CM, Levy M, Wilson RS, Garron DC (1986) Pain in Parkinson's disease. Mov Disord 1: 45-49.
15. Buzas B, Max MB (2004) Pain in Parkinson disease. Neurology 62: 2156-2157.
16. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840.
17. Duda JE, Lee VM, Trojanowski JQ (2000) Neuropathology of synuclein aggregates. J Neurosci Res 61: 121-127.
18. Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60: 337-341.
19. Wakabayashi K, Takahashi H, Ohama E, Ikuta F (1990) Parkinson's disease: an immunohistochemical study of Lewy body-containing neurons in the enteric nervous system. Acta Neuropathol 79: 581-583.
20. Forno LS (1996) Neuropathology of Parkinson's disease. J Neuropathol Exp Neurol 55: 259-272.
21. Braak H, de Vos RA, Bohl J, Del Tredici K (2006) Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 396: 67-72.
22. McGeer PL, McGeer EG (2008) The alpha-synuclein burden hypothesis of Parkinson disease and its relationship to Alzheimer disease. Exp Neurol 212: 235-238.
23. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, et al. (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4: 160-164.
24. Paisan-Ruiz C, Jain S, Evans EW, Gilks WP, Simon J, et al. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44: 595-600.
25. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, et al. (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608.
26. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
27. Schapira AH (2004) Disease modification in Parkinson's disease. Lancet Neurol 3: 362-368.
28. Jenner P (2003) Oxidative stress in Parkinson's disease. Ann Neurol 53 Suppl 3: S26-36; discussion S36-28.
29. McGeer PL, McGeer EG (2004) Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat Disord 10 Suppl 1: S3-7.
30. Greenamyre JT, Betarbet R, Sherer TB (2003) The rotenone model of Parkinson's disease: genes, environment and mitochondria. Parkinsonism Relat Disord 9 Suppl 2: S59-64.
31. Gorell JM, Johnson CC, Rybicki BA, Peterson EL, Richardson RJ (1998) The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living. Neurology 50: 1346-1350.
32. Bove J, Prou D, Perier C, Przedborski S (2005) Toxin-induced models of Parkinson's disease. NeuroRx 2: 484-494.
33. Richter F, Hamann M, Richter A (2007) Chronic rotenone treatment induces behavioral effects but no pathological signs of parkinsonism in mice. J Neurosci Res 85: 681-691.
34. Lee HJ, Suk JE, Bae EJ, Lee JH, Paik SR, et al. (2008) Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 40: 1835-1849.
35. Liu H, Zhang JP, Shi M, Quinn T, Bradner J, et al. (2009) Rab11a and HSP90 regulate recycling of extracellular alpha-synuclein. J Neurosci 29: 1480-1485.
36. Desplats P, Lee HJ, Bae EJ, Patrick C, Rockenstein E, et al. (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci U S A 106: 13010-13015.
37. Monville C, Torres EM, Dunnett SB (2006) Comparison of incremental and accelerating protocols of the rotarod test for the assessment of motor deficits in the 6-OHDA model. J Neurosci Methods 158: 219-223.
38. Porta EA (2002) Pigments in aging: an overview. Ann N Y Acad Sci 959: 57-65.
39. Braak H, Sastre M, Bohl JR, de Vos RA, Del Tredici K (2007) Parkinson's disease: lesions in dorsal horn layer I, involvement of parasympathetic and sympathetic pre- and postganglionic neurons. Acta Neuropathol 113: 421-429.
40. Braak H, Rub U, Gai WP, Del Tredici K (2003) Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110: 517-536.
41. Rojo AI, Cavada C, de Sagarra MR, Cuadrado A (2007) Chronic inhalation of rotenone or paraquat does not induce Parkinson's disease symptoms in mice or rats. Exp Neurol 208: 120-126.
42. Inden M, Kitamura Y, Takeuchi H, Yanagida T, Takata K, et al. (2007) Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J Neurochem 101: 1491-1504.
43. Li JY, Englund E, Holton JL, Soulet D, Hagell P, et al. (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14: 501-503.
44. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14: 504-506.
45. Mendez I, Vinuela A, Astradsson A, Mukhida K, Hallett P, et al. (2008) Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat Med 14: 507-509.
46. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, et al. (2008) Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451: 720-724.
47. Brundin P, Li JY, Holton JL, Lindvall O, Revesz T (2008) Research in motion: the enigma of Parkinson's disease pathology spread. Nat Rev Neurosci 9: 741-745.
48. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, et al. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 3: 1301-1306.
49. Seehafer SS, Pearce DA (2006) You say lipofuscin, we say ceroid: defining autofluorescent storage material. Neurobiol Aging 27: 576-588.
50. Sherer TB, Betarbet R, Testa CM, Seo BB, Richardson JR, et al. (2003) Mechanism of toxicity in rotenone models of Parkinson's disease. J Neurosci 23: 10756-10764.
51. Hoglinger GU, Lannuzel A, Khondiker ME, Michel PP, Duyckaerts C, et al. (2005) The mitochondrial complex I inhibitor rotenone triggers a cerebral tauopathy. J Neurochem 95: 930-939.
52. Drolet RE, Cannon JR, Montero L, Greenamyre JT (2009) Chronic rotenone exposure reproduces Parkinson's disease gastrointestinal neuropathology. Neurobiol Dis 36: 96-102.
53. Phillips RJ, Walter GC, Wilder SL, Baronowsky EA, Powley TL (2008) Alpha-synuclein-immunopositive myenteric neurons and vagal preganglionic terminals: autonomic pathway implicated in Parkinson's disease? Neuroscience 153: 733-750.
54. Huang J, Liu H, Gu W, Yan Z, Xu Z, et al. (2006) A delivery strategy for rotenone microspheres in an animal model of Parkinson's disease. Biomaterials 27: 937-946.
55. Birch-Machin MA, Jackson S, Kler RS, Turnbull DM (1993a) Study of skeletal muscle mitochondrial dysfunction; LHL J, editor. San Diego, CA: Academic Press Inc. pp 58-59.
56. Shepherd D, Garland PB (1969) The kinetic properties of citrate synthase from rat liver mitochondria. Biochem J 114: 597-610.
57. Tofaris GK, Garcia Reitbock P, Humby T, Lambourne SL, O'Connell M, et al. (2006) Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alpha-synuclein(1- 120): implications for Lewy body disorders. J Neurosci 26: 3942-3950.
58. Kadar A, Wittmann G, Liposits Z, Fekete C (2009) Improved method for combination of immunocytochemistry and Nissl staining. J Neurosci Methods 184: 115-118.
59. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, et al. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96: 379-394.
60. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.