Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally

Experimental Neurology

Volumn 190, Issue 2, 2004, Pages 373-383

  Ling, Zaodung ^a,b   Chang, Qin A ^a   Tong, Chong Wai ^a   Leurgans, Susan E ^a   Lipton, Jack W ^a   Carvey, Paul M ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b C   (United States)

Author keywords

Dopamine; Environment; Lewy body; LPS; Parkinson's diseases; Prenatal; Rotenone

Indexed keywords

DOPAMINE; EOSIN; LIPOPOLYSACCHARIDE; NEUROTOXIN; ROTENONE; SYNUCLEIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; IMMUNOCOMPETENT CELL; LEWY BODY; MICROGLIA; NONHUMAN; OXIDATION; PERINATAL PERIOD; PRENATAL PERIOD; PRIORITY JOURNAL; RAT;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; DOPAMINE; DRUG SYNERGISM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOHISTOCHEMISTRY; INSECTICIDES; LEWY BODIES; LIPOPOLYSACCHARIDES; MICROGLIA; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; ROTENONE; SYNUCLEINS; TYROSINE 3-MONOOXYGENASE;

EID: 8644287610     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.08.006     Document Type: Article

References (63)

1. J.D. Adams Jr, and I.N. Odunze Oxygen free radicals and Parkinson's disease Free Radical Biol. Med. 10 1991 161 169
2. R. Betarbet, T.B. Sherer, G. Mackenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre Chronic systemic pesticide exposure reproduces features of Parkinson's disease Nat. Neurosci. 3 2000 1301 1306
3. R. Betarbet, T.B. Sherer, D.A. Di Monte, and J.T. Greenamyre Mechanistic approaches to Parkinson's disease pathogenesis Brain Pathol. 12 2002 499 510
4. G. Boka, P. Anglade, D. Wallach, F. Javoy-Agid, Y. Agid, and E.C. Hirsch Immunocytochemical analysis of tumor necrosis factor and its receptors in Parkinson's disease Neurosci. Lett. 172 1994 151 154
5. D.B. Calne, and J.W. Langston Aetiology of Parkinson's disease Lancet 2 1983 1457 1459
6. D.B. Calne, R. Fuente-Fernandez, and A. Kishore Contributions of positron emission tomography to elucidating the pathogenesis of idiopathic parkinsonism and dopa responsive dystonia J. Neural Transm., Suppl. 50 1997 47 52
7. J. Casals, T.S. Elizan, and M.D. Yahr Postencephalitic parkinsonism-A review J. Neural Transm. 105 1998 645 676
8. G. Chapman, B.L. Beaman, D.A. Loeffler, D.M. Camp, E.F. Domino, D.W. Dickson, W.G. Ellis, I. Chen, S.E. Bachus, and P.A. Lewitt In situ hybridization for detection of nocardial 16S rRNA: reactivity within intracellular inclusions in experimentally infected cynomolgus monkeys-And in Lewy body-containing human brain specimens Exp. Neurol. 184 2003 715 725
9. K.K. Chung, V.L. Dawson, and T.M. Dawson New insights into Parkinson's disease J. Neurol. 250 Suppl. 3 2003 III15 III24
10. F.M. Corrigan, C.L. Wienburg, R.F. Shore, S.E. Daniel, and D. Mann Organochlorine insecticides in substantia nigra in Parkinson's disease J. Toxicol. Environ. Health, A 59 2000 229 234
11. O. Dammann, and A. Leviton Infection remote from the brain, neonatal white matter damage, and cerebral palsy in the preterm infant Semin. Pediatr. Neurol. 5 1998 190 201
12. R. Dawson Jr., M.F. Beal, S.C. Bondy, D.A. Di Monte, and G.E. Isom Excitotoxins, aging, and environmental neurotoxins: implications for understanding human neurodegenerative diseases Toxicol. Appl. Pharmacol. 134 1995 1 17
13. D.A. Di Monte The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol. 2 2003 531 538
14. G. Fishell, and K.D. Van Der Pattern formation in the striatum: developmental changes in the distribution of striatonigral projections Brain Res., Dev. Brain Res. 45 1989 239 255
15. G. Fiskum, A. Starkov, B.M. Polster, and C. Chinopoulos Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease Ann. N. Y. Acad. Sci. 991 2003 111 119
16. F. Fornai, P. Lenzi, M. Gesi, P. Soldani, M. Ferrucci, G. Lazzeri, L. Capobianco, G. Battaglia, A. De Blasi, F. Nicoletti, and A. Paparelli Methamphetamine produces neuronal inclusions in the nigrostriatal system and in PC12 cells J. Neurochem. 88 2004 114 123
17. L.S. Forno Neuropathology of Parkinson's disease J. Neuropathol. Exp. Neurol. 55 1996 259 272
18. H.M. Gao, J.S. Hong, W. Zhang, and B. Liu Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease J. Neurosci. 23 2003 1228 1236
19. H.M. Gao, B. Liu, W. Zhang, and J.S. Hong Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease FASEB J. 17 2003 1957 1959
20. D.A. Gayle, Z. Ling, C. Tong, T. Landers, J.W. Lipton, and P.M. Carvey Lipopolysaccharide (LPS)-induced dopamine cell loss in culture: roles of tumor necrosis factor-alpha, interleukin-1beta, and nitric oxide Brain Res., Dev. Brain Res. 133 2002 27 35
21. M. Gosalvez Carcinogenesis with the insecticide rotenone Life Sci. 32 1983 809 816
22. J.T. Greenamyre, R. Betarbet, and T.B. Sherer The rotenone model of Parkinson's disease: genes, environment and mitochondria Parkinsonism Relat. Disord. 9 Suppl. 2 2003 S59 S64
23. G. Hebert, J. Arsaut, R. Dantzer, and J. Demotes-Mainard Time-course of the expression of inflammatory cytokines and matrix metalloproteinases in the striatum and mesencephalon of mice injected with 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine, a dopaminergic neurotoxin Neurosci. Lett. 349 2003 191 195
24. O. Hornykiewicz, and S.J. Kish Biochemical pathophysiology of Parkinson's disease Adv. Neurol. 45 1987 19 34
25. F. Javoy-Agid, A. Ploska, and Y. Agid Microtopography of tyrosine hydroxylase, glutamic acid decarboxylase, and choline acetyltransferase in the substantia nigra and ventral tegmental area of control and Parkinsonian brains J. Neurochem. 37 1981 1218 1227
26. P. Jenner Oxidative stress in Parkinson's disease Ann. Neurol. 53 Suppl. 3 2003 S26 S36
27. P. Jenner, and C.W. Olanow Oxidative stress and the pathogenesis of Parkinson's disease Neurology 47 1996 S161 S170
28. A.N. Kalehua, D.D. Taub, P.V. Baskar, J. Hengemihle, J. Munoz, M. Trambadia, D.L. Speer, M.G. De Simoni, and D.K. Ingram Aged mice exhibit greater mortality concomitant to increased brain and plasma TNF-alpha levels following intracerebroventricular injection of lipopolysaccharide Gerontology 46 2000 115 128
29. T. Kielian, P. Mayes, and M. Kielian Characterization of microglial responses to Staphylococcus aureus: effects on cytokine, costimulatory molecule, and Toll-like receptor expression J. Neuroimmunol. 130 2002 86 99
30. W.G. Kim, R.P. Mohney, B. Wilson, G.H. Jeohn, B. Liu, and J.S. Hong Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia J. Neurosci. 20 2000 6309 6316
31. J.H. Kordower Functional fetal nigral grafts in a patient with Parkinson's disease: chemoanatomic, ultrastructural, and metabolic studies J.M. Rosenstein T.J. Collier M.A. Burke Y.E.L.J.M. Chen L. Martel A.E Levey E.J. Mufso T.B Freeman W. Olanow The Journal of Comparative Neurology vol. 370 1996 203 230
32. S. Kyrkanides, M.K. O'banion, P.E. Whiteley, J.C. Daeschner, and J.A. Olschowka Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury J. Neuroimmunol. 119 2001 269 277
33. D.G. Le Couteur, M. Muller, M.C. Yang, G.D. Mellick, and A.J. Mclean Age-environment and gene-environment interactions in the pathogenesis of Parkinson's disease Rev. Environ. Health 17 2002 51 64
34. S. Li, S.D. Hursting, B.J. Davis, J.A. Mclachlan, and J.C. Barrett Environmental exposure, DNA methylation, and gene regulation: lessons from diethylstilbestrol-induced cancers Ann. N. Y. Acad. Sci. 983 2003 161 169
35. Z.D. Ling, T.J. Collier, C.E. Sortwell, J.W. Lipton, T.Q. Vu, H.C. Robie, and P.M. Carvey Striatal trophic activity is reduced in the aged rat brain Brain Res. 856 2000 301 309
36. Z. Ling, D.A. Gayle, S.Y. Ma, J.W. Lipton, C.W. Tong, J.S. Hong, and P.M. Carvey In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain Mov. Disord. 17 2002 116 124
37. Z.D. Ling, D.A. Gayle, J.W. Lipton, and P.M. Carvey Prenatal lipopolysaccharide alters postnatal dopamine in the laboratory rat T. Nagatsu T. Nabeshima R. McCarty D. Goldstein Catecholamine Research: From Molecular Insights to Clinical Medicine 2002 Kluwer Academic/Plenum Publishers New York 209 212
38. Z.D. Ling, Q. Chang, J.W. Lipton, C.W. Tong, T.M. Landers, and P.M. Carvey Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain Neuroscience 124 2004 619 628
39. J.W. Lipton, T.Q. Vu, Z. Ling, S. Gyawali, J.R. Mayer, and P.M. Carvey Prenatal cocaine exposure induces an attenuation of uterine blood flow in the rat Neurotoxicol. Teratol. 24 2002 143 148
40. S.Y. Ma, M. Roytta, J.O. Rinne, Y. Collan, and U.K. Rinne Correlation between neuromorphometry in the substantia nigra and clinical features in Parkinson's disease using dissector counts J. Neurol. Sci. 151 1997 83 87
41. S.Y. Ma, M. Roytt, Y. Collan, and J.O. Rinne Unbiased morphometrical measurements show loss of pigmented nigral neurones with ageing Neuropathol. Appl. Neurobiol. 25 1999 394 399
42. S.O. McGuire, P.M. Carvey, and Z.D. Ling Tumor necrosis factor is toxic to mesencephalic dopamine neurons Exp. Neurol. 169 2001 219 230
43. M. Mogi, A. Togari, T. Kondo, Y. Mizuno, O. Komure, S. Kuno, H. Ichinose, and T. Nagatsu Caspase activities and tumor necrosis factor receptor R1 (p55) level are elevated in the substantia nigra from parkinsonian brain J. Neural Transm. 107 2000 335 341
44. M. Mogi, A. Togari, K. Tanaka, N. Ogawa, H. Ichinose, and T. Nagatsu Increase in level of tumor necrosis factor-alpha in 6-hydroxydopamine-lesioned striatum in rats is suppressed by immunosuppressant FK506 Neurosci. Lett. 2000 165 168
45. P.K. Morrish, J.S. Rakshi, D.L. Bailey, G.V. Sawle, and D.J. Brooks Measuring the rate of progression and estimating the preclinical period of Parkinson's disease with [18F]dopa PET J. Neurol., Neurosurg., Psychiatry 64 1998 314 319
46. T. Nagatsu, M. Mogi, H. Ichinose, and A. Togari Changes in cytokines and neurotrophins in Parkinson's disease J. Neural Transm., Suppl. 2000 277 290
47. Y.K. Ng, and E.A. Ling Induction of major histocompatibility class II antigen on microglial cells in postnatal and adult rats following intraperitoneal injections of lipopolysaccharide Neurosci. Res. 28 1997 111 118
48. E. Nurmi, H.M. Ruottinen, V. Kaasinen, J. Bergman, M. Haaparanta, O. Solin, and J.O. Rinne Progression in Parkinson's disease: a positron emission tomography study with a dopamine transporter ligand [18F]CFT Ann. Neurol. 47 2000 804 808
49. D.M. Paige, M. Augustyn, W.K. Adih, F. Witter, and J. Chang Bacterial vaginosis and preterm birth: a comprehensive review of the literature J. Nurse-Midwifery 43 1998 83 89
50. S.R. Paludan Synergistic action of pro-inflammatory agents: cellular and molecular aspects J. Leukocyte Biol. 67 2000 18 25
51. T.B. Sherer, R. Betarbet, C.M. Testa, B.B. Seo, J.R. Richardson, J.H. Kim, G.W. Miller, T. Yagi, A. Matsuno-Yagi, and J.T. Greenamyre Mechanism of toxicity in rotenone models of Parkinson's disease J. Neurosci. 23 2003 10756 10764
52. K. Shigematsu, P.L. Mcgeer, D.G. Walker, T. Ishii, and E.G. Mcgeer Reactive microglia/macrophages phagocytose amyloid precursor protein produced by neurons following neural damage J. Neurosci. Res. 31 1992 443 453
53. S.B. Soloway Naturally occurring insecticides Environ. Health Perspect. 14 1976 109 117
54. D.D. Song, C.W. Shults, A. Sisk, E. Rockenstein, and E. Masliah Enhanced substantia nigra mitochondrial pathology in human alpha-Synuclein transgenic mice after treatment with MPTP Exp. Neurol. 186 2004 158 172
55. M.B. Spina, and G. Cohen Exposure of striatal [corrected] synaptosomes to L-dopa increases levels of oxidized glutathione [published erratum appears in J Pharmacol Exp Ther 1989 (Jan);248(1):478]. J. Pharmacol. Exp. Ther. 247 1988 502 507
56. J.E. Sutherland, and M. Costa Epigenetics and the environment Ann. N. Y. Acad. Sci. 983 2003 151 160
57. A. Terao, A. Apte-Deshpande, L. Dousman, S. Morairty, B.P. Eynon, T.S. Kilduff, and Y.R. Freund Immune response gene expression increases in the aging murine hippocampus J. Neuroimmunol. 132 2002 99 112
58. M. Thiruchelvam, E.K. Richfield, R.B. Baggs, A.W. Tank, and D.A. Cory-Slechta The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease J. Neurosci. 20 2000 9207 9214
59. M. Thiruchelvam, E.K. Richfield, B.M. Goodman, R.B. Baggs, and D.A. Cory-Slechta Developmental exposure to the pesticides paraquat and maneb and the Parkinson's disease phenotype Neurotoxicology 23 2002 621 633
60. M. Thiruchelvam, A. Mccormack, E.K. Richfield, R.B. Baggs, A.W. Tank, D.A. Di Monte, and D.A. Cory-Slechta Age-related irreversible progressive nigrostriatal dopaminergic neurotoxicity in the paraquat and maneb model of the Parkinson's disease phenotype Eur. J. Neurosci. 18 2003 589 600
61. P. Thorsen, I.P. Jensen, B. Jeune, N. Ebbesen, M. Arpi, A. Bremmelgaard, and B.R. Moller Few microorganisms associated with bacterial vaginosis may constitute the pathologic core: a population-based microbiologic study among 3596 pregnant women Am. J. Obstet. Gynecol. 178 1998 580 587
62. T.Q. Vu, Z.D. Ling, S.Y. Ma, H.C. Robie, C.W. Tong, E.Y. Chen, J.W. Lipton, and P.M. Carvey Pramipexole attenuates the dopaminergic cell loss induced by intraventricular 6-hydroxydopamine J. Neural Transm. 107 2000 159 176
63. W. Zheng, S. Ren, and J.H. Graziano Manganese inhibits mitochondrial aconitase: a mechanism of manganese neurotoxicity Brain Res. 799 1998 334 342