Susceptibility to rotenone is increased in neurons from parkin null mice and is reduced by minocycline

Journal of Neurochemistry

Volumn 97, Issue 4, 2006, Pages 934-946

  Casarejos, M J ^a   Menendez J ^a   Solano, R M ^a   Rodriguez Navarro J A ^a   Garcia De Yebenes J ^a   Mena, M A ^a  

^a HOSPITAL RAMÓN Y CAJAL   (Spain)

Author keywords

Dopamine neurons; Extracellular signal regulated kinase; Microglial cells; NADPH oxidase; Park 2 gene; Parkinson's disease

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CASPASE INHIBITOR; DOPAMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; INDOMETACIN; LACTATE DEHYDROGENASE; MICROTUBULE ASSOCIATED PROTEIN 2; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE INHIBITOR; PARKIN; PROSTAGLANDIN SYNTHASE INHIBITOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; TERT BUTOXYCARBONYLMETHOXYASPARTYL FLUOROMETHYL KETONE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN MITOCHONDRION; CELL LOSS; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; DOSE RESPONSE; EMBRYO; ENVIRONMENTAL FACTOR; ENZYME INHIBITION; FAMILIAL DISEASE; FAMILIAL PARKINSONISM; GENE; GENE ENVIRONMENT INTERACTION; GENE MUTATION; GENE REPRESSION; GENETICS; KNOCKOUT MOUSE; MACROGLIA; MEMBRANE POTENTIAL; MESENCEPHALON; MICROGLIA; MITOCHONDRIAL MEMBRANE; MOUSE; NERVE CELL CULTURE; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; NULL ALLELE; PARK 2 GENE; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, NATURAL; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROGLIA; MINOCYCLINE; NADPH OXIDASE; NEURONS; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; ROTENONE; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE; UBIQUITIN-PROTEIN LIGASES; UNCOUPLING AGENTS;

ANIMALIA;

EID: 33646114508     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03777.x     Document Type: Article

References (69)

1. Ahmadi F. A. Linseman D. A. Grammatopoulos T. N. Jones S. M. Bouchard R. J. Freed C. R. Heidenreich K. A. Zawada W. M. 2003 The pesticide rotenone induces caspase-3-mediated apoptosis in ventral mesencephalic dopaminergic neurons. J. Neurochem. 87 914 921.
2. Alam M. Schmidt W. J. 2002 Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats. Behav. Brain Res. 136 317 324.
3. Allam M. F. Del Castillo A. S. Navajas R. F. 2005 Parkinson's disease risk factors: genetic, environmental, or both? Neurol. Res. 27 206 208.
4. Ashwell K. 1991 The distribution of microglia and cell death in the fetal rat forebrain. Brain Res. Dev. Brain Res. 58 1 12.
5. Banati R. B. Gehrmann J. Schubert P. Kreutzberg G. W. 1993 Cytotoxicity of microglia. Glia 7 111 118.
6. Bantubungi K. Jacquard C. Greco A. et al. 2005 Minocycline in phenotypic models of Huntington's disease. Neurobiol. Dis. 18 206 217.
7. Bashkatova V. Alam M. Vanin A. Schmidt W. J. 2004 Chronic administration of rotenone increases levels of nitric oxide and lipid peroxidation products in rat brain. Exp. Neurol. 186 235 241.
8. Beal M. F. 2001 Experimental models of Parkinson's disease. Nat. Rev. Neurosci. 2 325 334.
9. de Bernardo S. Canals S. Casarejos M. J. Mena M. A. 2003 Glia-conditioned medium induces de novo synthesis of tyrosine hydroxylase and increases dopamine cell survival by differential signaling pathways. J. Neurosci. Res. 73 818 830.
10. Betarbet R. Sherer T. B. MacKenzie G. Garcia-Osuna M. Panov A. V. Greenamyre J. T. 2000 Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3 1301 1306.
11. Blum D. Chtarto A. Tenenbaum L. Brotchi J. Levivier M. 2004 Clinical potential of minocycline for neurodegenerative disorders. Neurobiol. Dis. 17 359 366.
12. Canals S. Casarejos M. J. Rodriguez-Martin E. de Bernardo S. Mena M. A. 2001 Neurotrophic and neurotoxic effects of nitric oxide on fetal midbrain cultures. J. Neurochem. 76 56 68.
13. Casarejos M. J. Solano R. M. Menendez J. Rodriguez-Navarro J. A. Correa C. Garcia de Yebenes J. Mena M. A. 2005 Differential effects of L-DOPA on monoamine metabolism, cell survival and glutathione production in midbrain neuronal-enriched cultures from parkin knockout and wild-type mice. J. Neurochem. 94 1005 1014.
14. Chen M. Ona V. O. Li M. et al. 2000 Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat. Med. 6 797 801.
15. Choi S. H. Joe E. H. Kim S. U. Jin B. K. 2003 Thrombin-induced microglial activation produces degeneration of nigral dopaminergic neurons in vivo. J. Neurosci. 23 5877 5886.
16. Coulom H. Birman S. 2004 Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J. Neurosci. 24 10 993 10 998.
17. Dauer W. Przedborski S. 2003 Parkinson's disease: mechanisms and models. Neuron 39 889 909.
18. Decker T. Lohmann-Matthes M. L. 1988 A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Meth. 115 61 69.
19. Diaz-Corrales F. J. Asanuma M. Miyazaki I. Miyoshi K. Ogawa N. 2005 Rotenone induces aggregation of gamma-tubulin protein and subsequent disorganization of the centrosome: relevance to formation of inclusion bodies and neurodegeneration. Neuroscience 133 117 135.
20. Di Monte D. A. 2003 The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol. 2 531 538.
21. Domercq M. Matute C. 2004 Neuroprotection by tetracyclines. Trends Pharmacol. Sci. 25 609 612.
22. Du Y. Ma Z. Lin S. et al. 2001 Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc. Natl Acad. Sci. USA 98 14 669 14 674.
23. Gao H. M. Liu B. Hong J. S. 2003 Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 23 6181 6187.
24. Gavrieli Y. Sherman Y. Ben-Sasson S. A. 1992 Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 493 501.
25. Hardy G. H. 2003 Mendelian proportions in a mixed population. 1908. Yale J. Biol. Med. 76 79 80.
26. Hilwig I. Gropp A. 1975 pH-dependent fluorescence of DNA and RNA in cytologic staining with '33258' Hoechst. Exp. Cell Res. 91 457 460.
27. Hirsch E. C. Hunot S. 2000 Nitric oxide, glial cells and neuronal degeneration in parkinsonism. Trends Pharmacol. Sci. 21 163 165.
28. Hoglinger G. U. Feger J. Prigent A. Michel P. P. Parain K. Champy P. Ruberg M. Oertel W. H. Hirsch E. C. 2003 Chronic systemic complex I inhibition induces a hypokinetic multisystem degeneration in rats. J. Neurochem. 84 491 502.
29. Hughes E. H. Schlichtenbrede F. C. Murphy C. C. Broderick C. van Rooijen N. Ali R. R. Dick A. D. 2004 Minocycline delays photoreceptor death in the rds mouse through a microglia-independent mechanism. Exp. Eye Res. 78 1077 1084.
30. Itier J. M. Ibañez P. Mena M. A. et al. 2003 Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum. Mol. Genet. 12 2277 2291.
31. Jenner P. 2003 Oxidative stress in Parkinson's disease. Ann. Neurol. 53 S26 S38.
32. Kerr J. F. Wyllie A. H. Currie A. R. 1972 Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 239 257.
33. Lapointe N. St-Hilaire M. Martinoli M. G. Blanchet J. Gould P. Rouillard C. Cicchetti F. 2004 Rotenone induces non-specific central nervous system and systemic toxicity. FASEB J. 18 717 719.
34. Lees A. J. 1992 When did Ray Kennedy's Parkinson's disease begin? Mov. Disord. 7 110 116.
35. Lin S. Zhang Y. Dodel R. Farlow M. R. Paul S. M. Du Y. 2001 Minocycline blocks nitric oxide-induced neurotoxicity by inhibition p38 MAP kinase in rat cerebellar granule neurons. Neurosci. Lett. 315 61 64.
36. Manning-Bog A. B. McCormack A. L. Li J. Uversky V. N. Fink A. L. Di Monte D. A. 2002 The herbicide paraquat causes up-regulation and aggregation of alpha-synuclein in mice: paraquat and alpha-synuclein. J. Biol. Chem. 277 1641 1644.
37. McGeer E. G. McGeer P. L. 2005 Pharmacologic approaches to the treatment of amyotrophic lateral sclerosis. Biodrugs 19 31 37.
38. Mena M. A. Casarejos M. J. Carazo A. Paino C. García de Yebenes J. 1997 Glia protect fetal midbrain dopamine neurons in culture from L-DOPA toxicity through multiple mechanisms. J. Neural Transm. 104 317 328.
39. Mena M. A. de Bernardo S. Casarejos M. J. Canals S. Rodriguez-Martin E. 2002 The role of astroglia on the survival of dopamine neurons. Mol. Neurobiol. 25 245 263.
40. Moon Y. Lee K. H. Park J. H. Geum D. Kim K. 2005 Mitochondrial membrane depolarization and the selective death of dopaminergic neurons by rotenone: protective effect of coenzyme Q10. J. Neurochem. 93 1199 1208.
41. Nicklas W. J. Vyas I. Heikkila R. E. 1985 Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci. 36 2503 2508.
42. Olanow C. W. Tatton W. G. 1999 Etiology and pathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 22 123 144.
43. Palacino J. J. Sagi D. Goldberg M. S. Krauss S. Motz C. Wacker M. Klose J. Shen J. 2004 Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J. Biol. Chem. 279 18 614 18 622.
44. Pardo B. Paino C. L. Casarejos M. J. Mena M. A. 1997 Neuronal-enriched cultures from embryonic rat ventral mesencephalon for pharmacological studies of dopamine neurons. Brain Res. Brain Res. Protoc. 1 127 132.
45. Periquet M. Corti O. Jacquier S. Brice A. 2005 Proteomic analysis of parkin knockout mice: alterations in energy metabolism, protein handling and synaptic function. J. Neurochem. 95 1259 1276.
46. Pi R. Li W. Lee N. T. Chan H. H. Pu Y. Chan L. N. Sucher N. J. Chang D. C. Li M. Han Y. 2004 Minocycline prevents glutamate-induced apoptosis of cerebellar granule neurons by differential regulation of p38 and Akt pathways. J. Neurochem. 91 1219 1230.
47. Pyo H. Joe E. Jung S. Lee S. H. Jou I. 1999 Gangliosides activate cultured rat brain microglia. J. Biol. Chem. 274 34 584 34 589.
48. Ramsay R. R. Salach J. I. Singer T. P. 1986a Uptake of the neurotoxin 1-methyl-4-phenylpyridine (MPP+) by mitochondria and its relation to the inhibition of the mitochondrial oxidation of NAD+-linked substrates by MPP+. Biochem. Biophys. Res. Commun. 134 743 748.
49. Ramsay R. R. Salach J. I. Dadgar J. Singer T. P. 1986b Inhibition of mitochondrial NADH dehydrogenase by pyridine derivatives and its possible relation to experimental and idiopathic parkinsonism. Biochem. Biophys. Res. Commun. 135 269 275.
50. Rodriguez-Martin E. Casarejos M. J. Bazan E. Canals S. Herranz A. S. Mena M. A. 2000 Nitric oxide induces differentiation in the NB69 human catecholamine-rich cell line. Neuropharmacology 39 2090 2100.
51. Ryu E. J. Harding H. P. Angelastro J. M. Vitolo O. V. Ron D. Greene L. A. 2002 Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22 10 690 10 698.
52. Schapira A. H. Cooper J. M. Dexter D. Clark J. B. Jenner P. Marsden C. D. 1990 Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54 823 827.
53. Serrano A. Menendez J. Casarejos M. J. Solano R. M. Gallego E. Sanchez M. Mena M. A. Garcia de Yebenes J. 2005 Effects of cinnarizine, a calcium antagonist that produces human parkinsonism, in parkin knock out mice. Neuropharmacology 49 208 219.
54. Sherer T. B. Betarbet R. Stout A. K. Lund S. Baptista M. Panov A. V. Cookson M. R. Greenamyre J. T. 2002 An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J. Neurosci. 22 7006 7015.
55. Sherer T. B. Betarbet R. Kim J. H. Greenamyre J. T. 2003a Selective microglial activation in the rat rotenone model of Parkinson's disease. Neurosci. Lett. 341 87 90.
56. Sherer T. B. Betarbet R. Testa C. M. Seo B. B. Richardson J. R. Kim J. H. Miller G. W. Yagi T. Matsuno-Yagi A. Greenamyre J. T. 2003b Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23 10 756 10 764.
57. Sherer T. B. Kim J. H. Betarbet R. Greenamyre J. T. 2003c Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp. Neurol. 179 9 16.
58. Streit W. J. Kreutzberg G. W. 1987 Lectin binding by resting and reactive microglia. J. Neurocytol. 16 249 260.
59. Tada-Oikawa S. Hiraku Y. Kawanishi M. Kawanishi S. 2003 Mechanism for generation of hydrogen peroxide and change of mitochondrial membrane potential during rotenone-induced apoptosis. Life Sci. 73 3277 3288.
60. Thomas M. Le W. D. 2004 Minocycline: neuroprotective mechanisms in Parkinson's disease. Curr. Pharma. Des. 10 679 686.
61. Tikka T. M. Koistinaho J. E. 2001 Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 166 7527 7533.
62. Tikka T. Fiebich B. L. Goldsteins G. Keinanen R. Koistinaho J. 2001 Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21 2580 2588.
63. Uversky V. N. Li J. Fink A. L. 2001 Pesticides directly accelerate the rate of alpha-synuclein fibril formation: a possible factor in Parkinson's disease. FEBS Lett. 500 105 108.
64. Vila M. Jackson-Lewis V. Guegan C. Wu D. C. Teismann P. Choi D. K. Tieu K. Przedborski S. 2001 The role of glial cells in Parkinson's disease. Curr. Opin. Neurol. 14 483 489.
65. Wu D. C. Jackson-Lewis V. Vila M. Tieu K. Teismann P. Vadseth C. Choi D. K. Ischiropoulos H. Przedborski S. 2002 Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22 1763 1771.
66. Yrjanheikki J. Keinanen R. Pellikka M. Hokfelt T. Koistinaho J. 1998 Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl Acad. Sci. USA 95 15 769 15 774.
67. Zhang W. Narayanan M. Friedlander R. M. 2003 Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann. Neurol. 53 267 270.
68. Zhu S. Stavrovskaya I. G. Drozda M. et al. 2002 Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417 74 78.
69. 2 release at mitochondrial complex I: stimulation by rotenone, control by Ca(2+), and relevance to Parkinson disease. J. Biol. Chem. 280 15 587 15 594.