Acute and chronic metal exposure impairs locomotion activity in Drosophila melanogaster: A model to study Parkinsonism

BioMetals

Volumn 24, Issue 6, 2011, Pages 1045-1057

  Bonilla Ramirez, Leonardo ^a   Jimenez Del Rio, Marlene ^a   Velez Pardo, Carlos ^a  

^a UNIVERSIDAD DE ANTIOQUIA   (Colombia)

Author keywords

Copper; Drosophila melanogaster; Iron; Manganese; Parkinson; Parkinsonism

Indexed keywords

COPPER; DEFEROXAMINE; EDETIC ACID; IRON; MANGANESE; PENICILLAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN LEVEL; CHELATION THERAPY; CLIMBING; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; DRUG EFFECT; ENVIRONMENTAL EXPOSURE; FEMALE; INTOXICATION; LIFESPAN; LOCOMOTION; LONG TERM EXPOSURE; MALE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PARKINSONISM;

ANIMALS; BRAIN; CHELATING AGENTS; COPPER; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; DROSOPHILA MELANOGASTER; FEMALE; IRON; LIFE EXPECTANCY; MANGANESE; MOTOR ACTIVITY; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; PARKINSONIAN DISORDERS;

DROSOPHILA MELANOGASTER;

EID: 83555172243     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-011-9463-0     Document Type: Article

References (68)

1. HT Atasoy O Nuyan T Tunc M Yorubulut AE Unal LE Inan 2004 T2-weighted MRI in Parkinson's disease; substantia nigra pars compacta hypointensity correlates with the clinical scores Neurol India 52 3 332 337 15472421 (Pubitemid 39430186)
2. C Au A Benedetto M Aschner 2008 Manganese transport in eukaryotes: the role of DMT1 Neurotoxicology 29 4 569 576 18565586 10.1016/j.neuro.2008.04.022 1:CAS:528:DC%2BD1cXotlWqt7Y%3D
3. S Bahadorani P Bahadorani E Marcon DW Walker AJ Hilliker 2010 A Drosophila model of Menkes disease reveals a role for DmATP7 in copper absorption and neurodevelopment Dis Model Mech 3 1-2 84 891 20038716 10.1242/dmm.002642 1:CAS:528:DC%2BC3cXhsFyhtLbF
4. D Ben-Shachar MBH Youdim 1991 Intranigral iron injection induces behavioral and biochemical "Parkinsonism" in rats J Neurochem 57 2133 2135 1940919 10.1111/j.1471-4159.1991.tb06432.x 1:CAS:528:DyaK38Xks1Wq (Pubitemid 21922868)
5. D Berg 2006 In vivo detection of iron and neuromelanin by transcranial sonography-a new approach for early detection of substantia nigra damage J Neural Transm 113 6 775 780 16755382 10.1007/s00702-005-0447-5 1:CAS:528:DC%2BD28XltlGlt7c%3D (Pubitemid 43847171)
6. S Brar D Henderson J Schenck EA Zimmerman 2009 Iron accumulation in the substantia nigra of patients with Alzheimer disease and Parkinsonism Arch Neurol 66 3 371 374 19273756 10.1001/archneurol.2008.586
7. R Burke E Commons J Camakaris 2008 Expression and localisation of the essential copper transporter DmATP7 in Drosophila neuronal and intestinal tissues Int J Biochem Cell Biol 40 9 1850 1860 18321764 10.1016/j.biocel.2008. 01.021 1:CAS:528:DC%2BD1cXnsF2mtrY%3D
8. NC Burton TR Guilarte 2009 Manganese neurotoxicity: lessons learned from longitudinal studies in nonhuman primates Environ Health Perspect 117 3 325 332 19337503 10.1289/ehp.1173c25 1:CAS:528:DC%2BD1MXjvVWmur0%3D
9. WA Cass R Grondin AH Andersen Z Zhang PA Hardy LK Hussey-Andersen WS Rayens GA Gerhardt DM Gash 2007 Iron accumulation in the striatum predicts aging-related decline in motor function in rhesus monkeys Neurobiol Aging 28 2 258 271 16442671 10.1016/j.neurobiolaging.2005.12.010 1:CAS:528: DC%2BD28XhtlaktL%2FE (Pubitemid 44894635)
10. A Chaudhuri K Bowling C Funderburk H Lawal A Inamdar Z Wang JM O'Donnell 2007 Interaction of genetic and environmental factors in a Drosophila Parkinsonism model J Neurosci 27 10 2457 2467 17344383 10.1523/JNEUROSCI.4239- 06.2007 1:CAS:528:DC%2BD2sXjsVCrt7s%3D (Pubitemid 46393605)
11. DJ Costello SL Walsh HJ Harrington CH Walsh 2004 Concurrent hereditary haemochromatosis and idiopathic Parkinson's disease: a case report series J Neurol Neurosurg Psychiatry 75 4 631 633 15026513 10.1136/jnnp.2003.027441 1:STN:280:DC%2BD2c7jsVShsw%3D%3D (Pubitemid 38406666)
12. H Coulom S Birman 2004 Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster J Neurosci 24 48 10993 10998 15574749 10.1523/JNEUROSCI.2993-04.2004 1:CAS:528:DC%2BD2cXhtFShu77F (Pubitemid 39602410)
13. SK Das K Ray 2006 Wilson's disease: an update Nat Clin Pract Neurol 2 9 482 493 16932613 10.1038/ncpneuro0291 (Pubitemid 44275724)
14. DT Dexter P Jenner AH Schapira CD Marsden 1992 Alterations in levels of iron, ferritin, and other trace metals in neurodegenerative diseases affecting the basal ganglia. The Royal Kings and Queens Parkinson's Disease Research Group Ann Neurol 32 Suppl S94 S100 1510387 10.1002/ana.410320716 1:CAS:528: DyaK3sXltVSi
15. G Discalzi E Pira E Herrero Hernandez C Valentini M Turbiglio F Meliga 2000 Occupational Mn Parkinsonism: magnetic resonance imaging and clinical patterns following CaNa2-EDTA chelation Neurotoxicology 21 5 863 866 11130292 1:STN:280:DC%2BD3M7ivVyruw%3D%3D
16. U Dydak YM Jiang LL Long H Zhu J Chen WM Li RA Edden S Hu X Fu Z Long XA Mo D Meier J Harezlak M Aschner JB Murdoch W Zheng 2011 In vivo measurement of brain GABA concentrations by magnetic resonance spectroscopy in smelters occupationally exposed to manganese Environ Health Perspect 119 2 219 224 20876035 10.1289/ehp.1002192 1:CAS:528:DC%2BC3MXivVahu7k%3D
17. D Egli A Selvaraj H Yepiskoposyan B Zhang E Hafen O Georgiev W Schaffner 2003 Knockout of 'metal-responsive transcription factor' MTF-1 in Drosophila by homologous recombination reveals its central role in heavy metal homeostasis EMBO J 22 1 100 108 12505988 10.1093/emboj/cdg012 1:CAS:528: DC%2BD3sXovFartg%3D%3D (Pubitemid 36091273)
18. LS Forno 1996 Neuropathology of Parkinson's disease J Neuropathol Exp Neurol 55 259 272 8786384 10.1097/00005072-199603000-00001 1:STN:280: DyaK283gslyhsw%3D%3D (Pubitemid 26085575)
19. B Gallez C Baudelet J Adline M Geurts N Delzenne 1997 Accumulation of manganese in the brain of mice after intravenous injection of manganese-based contrast agents Chem Res Toxicol 10 4 360 363 9114970 10.1021/tx960194p 1:CAS:528:DyaK2sXivVKmu7o%3D (Pubitemid 27176295)
20. JM Graham MN Paley RA Grünewald N Hoggard PD Griffiths 2000 Brain iron deposition in Parkinson's disease imaged using the PRIME magnetic resonance sequence Brain 123 Pt 12 2423 2431 11099445 10.1093/brain/123.12.2423
21. TR Guilarte 2010 Manganese and Parkinson's disease: a critical review and new findings Environ Health Perspect 118 8 1071 1080 20403794 10.1289/ehp.0901748 1:CAS:528:DC%2BC3cXhtFSms7zJ
22. H Hua O Georgiev W Schaffner D Steiger 2010 Human copper transporter Ctr1 is functional in Drosophila, revealing a high degree of conservation between mammals and insects J Biol Inorg Chem 15 1 107 113 19856191 10.1007/s00775-009- 0599-0 1:CAS:528:DC%2BD1MXhtlSkurjN
23. D Huster 2010 Wilson disease Best Pract Res Clin Gastroenterol 24 5 531 539 20955957 10.1016/j.bpg.2010.07.014 1:CAS:528:DC%2BC3cXht12ksbjK
24. J Jankovic 2008 Parkinson's disease: clinical features and diagnosis J Neurol Neurosurg Psychiatry 79 4 368 376 18344392 10.1136/jnnp.2007.131045 1:STN:280:DC%2BD1c7oslamtA%3D%3D (Pubitemid 351441488)
25. M Jimenez-Del-Rio C Velez-Pardo 2004 The hydrogen peroxide and its importance in the Alzheimer's and Parkinson's disease Curr Med Chem Cent Nerv Syst Agents 4 279 285 10.2174/1568015043356896 (Pubitemid 39551304)
26. M Jimenez-Del-Rio C Velez-Pardo 2004 Transition metals-induced apoptosis in lymphocytes via hydroxyl radical generation, mitochondria dysfunction and caspase-3 activation: an in vitro model for neurodegeneration Arch Med Res 35 185 193 15163458 10.1016/j.arcmed.2004.01.001 1:CAS:528:DC%2BD2cXkt1SnsLo%3D (Pubitemid 38648986)
27. M Jimenez-Del-Rio C Guzman-Martinez C Velez-Pardo 2010 The effects of polyphenols on survival and locomotor activity in Drosophila melanogaster exposed to iron and paraquat Neurochem Res 35 227 238 19701790 10.1007/s11064-009-0046-1 1:CAS:528:DC%2BD1MXhtVaqt7zL
28. SG Kaler 2011 ATP7A-related copper transport diseases-emerging concepts and future trends Nat Rev Neurol 7 1 15 29 21221114 10.1038/nrneurol.2010.180 1:CAS:528:DC%2BC3MXjs1Omtw%3D%3D
29. P Kosta MI Argyropoulou S Markoula S Konitsiotis 2006 MRI evaluation of the basal ganglia size and iron content in patients with Parkinson's disease J Neurol 253 1 26 32 15981079 10.1007/s00415-005-0914-9 (Pubitemid 43157384)
30. DW Lee JK Andersen 2010 Iron elevations in the aging Parkinsonian brain: a consequence of impaired iron homeostasis? J Neurochem 112 2 332 339 20085612 10.1111/j.1471-4159.2009.06470.x 1:CAS:528:DC%2BC3cXhtVGjurY%3D
31. Z Mao RL Davis 2009 Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity Front Neural Circuits 3 5 19597562 10.3389/neuro.04.005.2009
32. WR Martin M Wieler M Gee 2008 Midbrain iron content in early Parkinson disease: a potential biomarker of disease status Neurology 70 16 Pt 2 1411 14117 18172063 10.1212/01.wnl.0000286384.31050.b5 1:CAS:528:DC%2BD1cXksFantr8%3D (Pubitemid 351521933)
33. S Meenakshi-Sundaram A Mahadevan AB Taly GR Arunodaya HS Swamy SK Shankar 2008 Wilson's disease: a clinico-neuropathological autopsy study J Clin Neurosci 15 4 409 417 18242093 10.1016/j.jocn.2006.07.017 1:STN:280: DC%2BD1c7lt1eqtA%3D%3D
34. F Missirlis S Holmberg T Georgieva BC Dunkov TA Rouault JH Law 2006 Characterization of mitochondrial ferritin in Drosophila Proc Natl Acad Sci USA 103 15 5893 5898 16571656 10.1073/pnas.0601471103 1:CAS:528:DC%2BD28XktFait7c%3D
35. M Morello P Zatta P Zambenedetti A Martorana V D'Angelo G Melchiorri G Bernardi G Sancesario 2007 Manganese intoxication decreases the expression of manganoproteins in the rat basal ganglia: an immunohistochemical study Brain Res Bull 74 6 406 415 17920449 10.1016/j.brainresbull.2007.07.011 1:CAS:528:DC%2BD2sXhtFeiurvI (Pubitemid 47505280)
36. M Muckenthaler N Gunkel D Frishman A Cyrklaff P Tomancak MW Hentze 1998 Iron-regulatory protein-1 (IRP-1) is highly conserved in two invertebrate species-characterization of IRP-1 homologues in Drosophila melanogaster and Caenorhabditis elegans Eur J Biochem 254 2 230 237 9660175 10.1046/j.1432-1327. 1998.2540230.x 1:CAS:528:DyaK1cXjvFeiu7k%3D (Pubitemid 28289375)
37. I Nakatsuka S Maeda T Andoh Y Hayashi R Mizuno H Higuchi T Miyawaki 2009 Oxidative changes in the rat brain by intraperitoneal injection of ferric nitrilotriacetate Redox Rep 14 3 109 114 19490752 10.1179/135100009X392575 1:CAS:528:DC%2BD1MXhsFKrs7nI
38. AE Oakley JF Collingwood J Dobson G Love HR Perrott JA Edwardson M Elstner CM Morris 2007 Individual dopaminergic neurons show raised iron levels in Parkinson disease Neurology 68 21 1820 1825 17515544 10.1212/01.wnl. 0000262033.01945.9a 1:STN:280:DC%2BD2szgsVynuw%3D%3D (Pubitemid 46791395)
39. CW Olanow PF Good H Shinotoh KA Hewitt F Vingerhoets BJ Snow MF Beal DB Calne DP Perl 1996 Manganese intoxication in the rhesus monkey: a clinical, imaging, pathologic, and biochemical study Neurology 46 2 492 498 8614520 1:STN:280:DyaK287otF2rsA%3D%3D (Pubitemid 26081339)
40. JL Ordoñez-Librado V Anaya-Martínez AL Gutierrez-Valdez L Colín-Barenque E Montiel-Flores MR Avila-Costa 2010 Manganese inhalation as a Parkinson disease model Parkinsons Dis 2011 612989 21209715
41. D Ozcelik H Uzun 2009 Copper intoxication; antioxidant defenses and oxidative damage in rat brain Biol Trace Elem Res 127 1 45 52 18784908 10.1007/s12011-008-8219-3 1:CAS:528:DC%2BD1cXhsFartr%2FK
42. P Péran A Cherubini F Assogna F Piras C Quattrocchi A Peppe P Celsis O Rascol JF Démonet A Stefani M Pierantozzi FE Pontieri C Caltagirone G Spalletta U Sabatini 2010 Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature Brain 133 11 3423 3433 20736190 10.1093/brain/awq212
43. DP Perl CW Olanow 2007 The neuropathology of manganese-induced Parkinsonism J Neuropathol Exp Neurol 66 8 675 682 17882011 10.1097/nen. 0b013e31812503cf 1:CAS:528:DC%2BD2sXhtVWqsbfO (Pubitemid 47344246)
44. IS Pienaar J Götz MB Feany 2010 Parkinson's disease: insights from non-traditional model organisms Prog Neurobiol 92 4 558 571 20851733 10.1016/j.pneurobio.2010.09.001 1:CAS:528:DC%2BC3cXhsVGntrvJ
45. K Prabhakaran D Ghosh GD Chapman PG Gunasekar 2008 Molecular mechanism of manganese exposure-induced dopaminergic toxicity Brain Res Bull 76 4 361 367 18502311 10.1016/j.brainresbull.2008.03.004 1:CAS:528:DC%2BD1cXmtlWht7Y%3D
46. KV Rao MD Norenberg 2004 Manganese induces the mitochondrial permeability transition in cultured astrocytes J Biol Chem 279 31 32333 32338 15173181 10.1074/jbc.M402096200 1:CAS:528:DC%2BD2cXmtVChsL8%3D (Pubitemid 39014685)
47. PV Reddy KV Rao MD Norenberg 2008 The mitochondrial permeability transition, and oxidative and nitrosative stress in the mechanism of copper toxicity in cultured neurons and astrocytes Lab Invest 88 8 816 830 18591939 10.1038/labinvest.2008.49 1:CAS:528:DC%2BD1cXovV2lt7o%3D
48. J Salazar N Mena S Hunot A Prigent D Alvarez-Fischer M Arredondo C Duyckaerts V Sazdovitch L Zhao LM Garrick MT Nuñez MD Garrick R Raisman-Vozari EC Hirsch 2008 Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease Proc Natl Acad Sci USA 105 47 18578 18583 19011085 10.1073/pnas.0804373105 1:CAS:528: DC%2BD1cXhsVOltLzN
49. GA Salvador RM Uranga NM Giusto 2010 Iron and mechanisms of neurotoxicity Int J Alzheimers Dis 2011 720658 21234369
50. GJ Sengstock CW Olanow RA Menzies AJ Dunn GW Arendash 1993 Infusion of iron into the rat substantia nigra: nigral pathology and dose-dependent loss of striatal dopaminergic markers J Neurosci Res 35 1 67 82 7685399 10.1002/jnr.490350109 1:CAS:528:DyaK3sXksVKrsro%3D (Pubitemid 23143633)
51. GJ Sengstock CW Olanow AJ Dunn S Barone Jr GW Arendash 1994 Progressive changes in striatal dopaminergic markers, nigral volume, and rotational behavior following iron infusion into the rat substantia nigra Exp Neurol 130 1 82 94 7529713 10.1006/exnr.1994.1187 1:CAS:528:DyaK2MXjvVKkurk%3D
52. H Shinotoh BJ Snow KA Hewitt BD Pate D Doudet R Nugent DP Perl W Olanow DB Calne 1995 MRI and PET studies of manganese-intoxicated monkeys Neurology 45 6 1199 1204 7783889 1:STN:280:DyaK2MzgtlartQ%3D%3D
53. AM Snyder JR Connor 2009 Iron, the substantia nigra and related neurological disorders Biochim Biophys Acta 1790 7 606 614 18778755 10.1016/j.bbagen.2008.08.005 1:CAS:528:DC%2BD1MXnt1yjtLg%3D
54. A Southon A Farlow M Norgate R Burke J Camakaris 2008 Malvolio is a copper transporter in Drosophila melanogaster J Exp Biol 211 Pt 5 709 716 18281333 10.1242/jeb.014159 1:CAS:528:DC%2BD1cXls1Cqs70%3D (Pubitemid 351542830)
55. A Southon N Palstra N Veldhuis A Gaeth C Robin R Burke J Camakaris 2010 Conservation of copper-transporting P(IB)-type ATPase function Biometals 23 4 681 694 20372979 10.1007/s10534-010-9332-2 1:CAS:528:DC%2BC3cXoslWqtLo%3D
56. F Spadoni A Stefani M Morello F Lavaroni P Giacomini G Sancesario 2000 Selective vulnerability of pallidal neurons in the early phases of manganese intoxication Exp Brain Res 135 4 544 551 11156318 10.1007/s002210000554 1:CAS:528:DC%2BD3cXosVOltLw%3D
57. K Sriram GX Lin AM Jefferson JR Roberts RS Chapman BT Chen JM Soukup AJ Ghio JM Antonini 2010 Dopaminergic neurotoxicity following pulmonary exposure to manganese-containing welding fumes Arch Toxicol 84 7 521 540 20224926 10.1007/s00204-010-0525-9 1:CAS:528:DC%2BC3cXjtFWltLk%3D
58. M Südmeyer A Saleh L Wojtecki M Cohnen J Gross M Ploner H Hefter L Timmermann A Schnitzler 2006 Wilson's disease tremor is associated with magnetic resonance imaging lesions in basal ganglia structures Mov Disord 21 12 2134 2139 17044091 10.1002/mds.21136 (Pubitemid 46140425)
59. M Takanashi H Mochizuki K Yokomizo N Hattori H Mori Y Yamamura Y Mizuno 2001 Iron accumulation in the substantia nigra of autosomal recessive juvenile Parkinsonism (ARJP) Parkinsonism Relat Disord 7 4 311 314 11344015 10.1016/S1353-8020(00)00050-X (Pubitemid 32409973)
60. RM Taylor Y Chen A Dhawan EuroWilson Consortium 2009 Triethylene tetramine dihydrochloride (trientine) in children with Wilson disease: experience at King's College Hospital and review of the literature Eur J Pediatr 168 9 1061 1068 19066958 10.1007/s00431-008-0886-8
61. K Tiklová KA Senti S Wang A Gräslund C Samakovlis 2010 Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila Nat Cell Biol 12 11 1071 1077 20935638 10.1038/ncb2111
62. LI Wallis MN Paley JM Graham RA Grünewald EL Wignall HM Joy PD Griffiths 2008 MRI assessment of basal ganglia iron deposition in Parkinson's disease J Magn Reson Imaging 28 5 1061 1067 18972346 10.1002/jmri.21563
63. T Yoshiga T Georgieva BC Dunkov N Harizanova K Ralchev JH Law 1999 Drosophila melanogaster transferrin. Cloning, deduced protein sequence, expression during the life cycle, gene localization and up-regulation on bacterial infection Eur J Biochem 260 2 414 420 10095776 10.1046/j.1432-1327. 1999.00173.x 1:CAS:528:DyaK1MXitVSls7c%3D (Pubitemid 29122537)
64. MB Youdim M Fridkin H Zheng 2004 Novel bifunctional drugs targeting monoamine oxidase inhibition and iron chelation as an approach to neuroprotection in Parkinson's disease and other neurodegenerative diseases J Neural Transm 111 10-11 1455 1471 15480846 10.1007/s00702-004-0143-x 1:CAS:528:DC%2BD2cXotFCrtbY%3D (Pubitemid 39468399)
65. WR Yu H Jiang J Wang JX Xie 2008 Copper (Cu2+) induces degeneration of dopaminergic neurons in the nigrostriatal system of rats Neurosci Bull 24 2 73 78 18369385 10.1007/s12264-008-0073-y 1:CAS:528:DC%2BD1MXlt12gtrk%3D (Pubitemid 351738281)
66. L Zecca A Stroppolo A Gatti D Tampellini M Toscani M Gallorini G Giaveri P Arosio P Santambrogio RG Fariello E Karatekin MH Kleinman N Turro O Hornykiewicz FA Zucca 2004 The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging Proc Natl Acad Sci USA 101 26 9843 9848 15210960 10.1073/pnas.0403495101 1:CAS:528:DC%2BD2cXlvVahtLY%3D (Pubitemid 38869324)
67. L Zecca D Berg T Arzberger P Ruprecht WD Rausch M Musicco D Tampellini P Riederer M Gerlach G Becker 2005 In vivo detection of iron and neuromelanin by transcranial sonography: a new approach for early detection of substantia nigra damage Mov Disord 20 10 1278 1285 15986424 10.1002/mds.20550 (Pubitemid 41645902)
68. J Zhang Y Zhang J Wang P Cai C Luo Z Qian Y Dai H Feng 2010 Characterizing iron deposition in Parkinson's disease using susceptibility- weighted imaging: an in vivo MR study Brain Res 1330 124 130 20303339 10.1016/j.brainres.2010.03.036 1:CAS:528:DC%2BC3cXltF2jtLg%3D