Effects of Neonatal Iron Feeding and Chronic Clioquinol Administration on the Parkinsonian Human A53T Transgenic Mouse

ACS Chemical Neuroscience

Volumn 7, Issue 3, 2016, Pages 360-366

  Billings, Jessica L ^a   Hare, Dominic J ^a,b   Nurjono, Milawaty ^a   Volitakis, Irene ^a   Cherny, Robert A ^a   Bush, Ashley I ^a   Adlard, Paul A ^a   Finkelstein, David I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

alpha synuclein; dietary iron; iron accumulation; Parkinson's disease; risk factor

Indexed keywords

ALPHA SYNUCLEIN; CLIOQUINOL; IRON; IRON CHELATING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DAMAGE; CELL LOSS; CONTROLLED STUDY; DENERVATION; DRUG TARGETING; FEEDING; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; IRON INTAKE; IRON THERAPY; LOCOMOTION; MOUSE; NEWBORN; NONHUMAN; PARKINSONISM; PHENOTYPE; PRIORITY JOURNAL; RISK FACTOR; TREATMENT DURATION; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; MOTOR ACTIVITY; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; CLIOQUINOL; DISEASE MODELS, ANIMAL; HUMANS; IRON; IRON CHELATING AGENTS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; PARKINSONIAN DISORDERS; PHENOTYPE;

EID: 84962288899     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.5b00305     Document Type: Article

References (34)

1. Hare, D. J., Ayton, S., Bush, A., and Lei, P. (2013) A delicate balance: Iron metabolism and diseases of the brain Front. Aging Neurosci. 5, 34 10.3389/fnagi.2013.00034
2. Ward, R. R., Zucca, F. A., Duyn, J. H., Crichton, R. R., and Zecca, L. (2014) The role of iron in brain ageing and neurodegenerative disorders Lancet Neurol. 13, 1045-1060 10.1016/S1474-4422(14)70117-6
3. Zecca, L., Stroppolo, A., Gatti, A., Tampellini, D., Toscani, M., Gallorini, M., Giaveri, G., Arosio, P., Santambrogio, P., and Fariello, R. G. et al. 2004, The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging Proc. Natl. Acad. Sci. U. S. A. 101, 9843 10.1073/pnas.0403495101
4. Li, J., Uversky, V. N., and Fink, A. L. (2001) Effect of Familial Parkinson's Disease Point Mutations A30P and A53T on the Structural Properties, Aggregation, and Fibrillation of Human α-Synuclein Biochemistry 40, 11604-11613 10.1021/bi010616g
5. Ostrerova-Golts, N., Petrucelli, L., Hardy, J., Lee, J. M., Farer, M., and Wolozin, B. (2000) The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity J. Neurosci. 20, 6048-6054
6. Hare, D. J., Lei, P., Ayton, S., Roberts, B. R., Grimm, R., George, J. L., Bishop, D. P., Beavis, A. D., Donovan, S. J., McColl, G., Volitakis, I., Masters, C. L., Adlard, P. A., Cherny, R. A., Bush, A. I., Finkelstein, D. I., and Doble, P. A. (2014) An iron-dopamine index predicts risk of parkinsonian neurodegeneration in the substantia nigra pars compacta Chem. Sci. 5, 2160-2169 10.1039/C3SC53461H
7. Finkelstein, D. I., Hare, D. J., Billings, J. L., Sedjahtera, A., Nurjono, M., Arthofer, E., George, S., Culvenor, J. G., Bush, A. I., and Adlard, P. A. (2015) Clioquinol Improves Cognitive, Motor Function, and Microanatomy of the Alpha-Synuclein hA53T Transgenic Mice ACS Chem. Neurosci. 10.1021/acschemneuro.5b00253
8. Bareggi, S. R. and Cornelli, U. (2012) Clioquinol: Review of its mechanisms of action and clinical uses in neurodegenerative disorders CNS Neurosci. Ther. 18, 41-46 10.1111/j.1755-5949.2010.00231.x
9. Kaur, D., Yantiri, F., Rajagopalan, S., Kumar, J., Mo, J. Q., Boonplueang, R., Viswanath, V., Jacobs, R., Yang, L., Beal, M. F., DiMonte, D., Volitakis, I., Ellerby, L., Cherny, R. A., Bush, A. I., and Andersen, J. K. (2003) Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: A novel therapy for Parkinson's disease Neuron 37, 899-909 10.1016/S0896-6273(03)00126-0
10. Hare, D. J., Adlard, P. A., Doble, P. A., and Finkelstein, D. I. (2013) Metallobiology of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity Metallomics 5, 91-109 10.1039/c2mt20164j
11. Hare, D. J., Arora, M., Jenkins, N. L., Finkelstein, D. I., Doble, P. A., and Bush, A. I. (2015) Is early-life iron exposure critical in neurodegeneration? Nat. Rev. Neurol. 11, 536-544 10.1038/nrneurol.2015.100
12. Kaur, D., Rajagopalan, S., Cherny, R. A., and Andersen, J. K. (2007) Increased murine neonatal iron intake results in Parkinson-like neurodegeneration with age Neurobiol. Aging 28, 907-913 10.1016/j.neurobiolaging.2006.04.003
13. Fredriksson, A., Schröder, N., Eriksson, P., Izquierdo, I., and Archer, T. (1999) Neonatal Iron Exposure Induces Neurobehavioural Dysfunctions in Adult Mice Toxicol. Appl. Pharmacol. 159, 25-30 10.1006/taap.1999.8711
14. Fredriksson, A., Schröder, N., Eriksson, P., Izquierdo, I., and Archer, T. (2001) Neonatal iron potentiates adult MPTP-induced neurodegenerative and functional deficits Parkinsonism Relat. Disord. 7, 97-105 10.1016/S1353-8020(00)00028-6
15. Ayton, S. and Lei, P. (2014) Nigral Iron Elevation Is an Invariable Feature of Parkinson's Disease and Is a Sufficient Cause of Neurodegeneration BioMed Res. Int. 2014, 1-9 10.1155/2014/581256
16. Giasson, B. I., Duda, J. E., Quinn, S. M., Zhang, B., Trojanowski, J. Q., and Lee, V. M. Y. (2002) Neuronal α-Synucleinopathy with Severe Movement Disorder in Mice Expressing A53T Human α-Synuclein Neuron 34, 521-533 10.1016/S0896-6273(02)00682-7
17. Hare, D. J., Lee, J. K., Beavis, A. D., van Gramberg, A., George, J., Adlard, P. A., Finkelstein, D. I., and Doble, P. A. (2012) Three-dimensional atlas of iron, copper, and zinc in the mouse cerebrum and brainstem Anal. Chem. 84, 3990-3997 10.1021/ac300374x
18. Bacopoulos, N. G. and Bhatnagar, R. K. (1977) Correlation between tyrosine hydroxylase activity and catecholamine concentration or turnover in brain regions J. Neurochem. 29, 639-643 10.1111/j.1471-4159.1977.tb07780.x
19. Oaks, A. W., Frankfurt, M., Finkelstein, D. I., and Sidhu, A. (2013) Age-Dependent Effects of A53T Alpha-Synuclein on Behavior and Dopaminergic Function PLoS One 8, e60378 10.1371/journal.pone.0060378
20. Hung, L. W., Villemagne, V. L., Cheng, L., Sherratt, N. A., Ayton, S., White, A. R., Crouch, P. J., Lim, S., Leong, S. L., and Wilkins, S. (2012) The hypoxia imaging agent CuII (atsm) is neuroprotective and improves motor and cognitive functions in multiple animal models of Parkinson's disease J. Exp. Med. 209, 837-854
21. Ryan, T. M., Roberts, B. R., McColl, G., Hare, D. J., Doble, P. A., Li, Q.-X., Lind, M., Roberts, A. M., Mertens, H. D. T., Kirby, N., Pham, C. L. L., Hinds, M. G., Adlard, P. A., Barnham, K. J., Curtain, C. C., and Masters, C. L. (2015) Stabilization of nontoxic Aβ-oligomers: Insights into the mechanism of action of hydroxyquinolines in Alzheimer's disease J. Neurosci. 35, 2871-2884 10.1523/JNEUROSCI.2912-14.2015
22. Devos, D., Moreau, C., Devedjian, J. C., Kluza, J., Petrault, M., Laloux, C., Jonneaux, A., Ryckewaert, G., Garçon, G., Rouaix, N., Duhamel, A., Jissendi, P., Dujardin, K., Auger, F., Ravasi, L., Hopes, L., Grolez, G., Firdaus, W., Sablonnière, B., Strubi-Vuillaume, I., Zahr, N., Destée, A., Corvol, J.-C., Pöltl, D., Leist, M., Rose, C., Defebvre, L., Marchetti, P., Cabantchik, Z. I., and Bordet, R. (2014) Targeting chelatable iron as a therapeutic modality in Parkinson's disease Antioxid. Redox Signaling 21, 195-210 10.1089/ars.2013.5593
23. Fredriksson, A., Schröder, N., Eriksson, P., Izquierdo, I., and Archer, T. (2000) Maze learning and motor activity deficits in adult mice induced by iron exposure during a critical postnatal period Dev. Brain Res. 119, 65-74 10.1016/S0165-3806(99)00160-1
24. Olivares, D., Huang, X., Branden, L., Greig, N., and Rogers, J. (2009) Physiological and Pathological Role of Alpha-synuclein in Parkinson's Disease Through Iron Mediated Oxidative Stress; The Role of a Putative Iron-responsive Element Int. J. Mol. Sci. 10, 1226-1260 10.3390/ijms10031226
25. Ortega, R., Carmona, A., Roudeau, S., Perrin, L., Dučić, T., Carboni, E., Bohic, S., Cloetens, P., and Lingor, P. (2015) α-Synuclein Over-Expression Induces Increased Iron Accumulation and Redistribution in Iron-Exposed Neurons Mol. Neurobiol. 10.1007/s12035-015-9146-x
26. Kelly, L. P., Carvey, P. M., Keshavarzian, A., Shannon, K. M., Shaikh, M., Bakay, R. A. E., and Kordower, J. H. (2014) Progression of intestinal permeability changes and alpha-synuclein expression in a mouse model of Parkinson's disease Mov. Disord. 29, 999-1009 10.1002/mds.25736
27. Taylor, E. M., Crowe, A., and Morgan, E. H. (1991) Transferrin and Iron Uptake by the Brain: Effects of Altered Iron Status J. Neurochem. 57, 1584-1592 10.1111/j.1471-4159.1991.tb06355.x
28. Barnham, K. J. and Bush, A. I. (2014) Biological metals and metal-targeting compounds in major neurodegenerative diseases Chem. Soc. Rev. 43, 6727-6749 10.1039/C4CS00138A
29. Deas, E., Cremades, N., Angelova, P. R., Ludtmann, M., Yao, Z., Chen, S., Horrocks, M., Banushi, B., Little, D., Devine, M., Gissen, P., Klenerman, D., Dobson, C., Wood, N., Gandhi, S., and Abramov, A. Y. (2015) Alpha-synuclein oligomers interact with metal ions to induce oxidative stress and neuronal death in Parkinson's disease Antioxid. Redox Signaling 10.1089/ars.2015.6343
30. Sacks, P. V. and Houchin, D. N. (1978) Comparative bioavailability of elemental iron powders for repair of iron deficiency anemia in rats. Studies of efficacy and toxicity of carbonyl iron Am. J. Clin. Nutr. 31, 566-571
31. Finkelstein, D. I., Stanic, D., Parish, C. L., Tomas, D., Dickson, K., and Horne, M. K. (2000) Axonal sprouting following lesions of the rat substantia nigra Neuroscience 97, 99-112 10.1016/S0306-4522(00)00009-9
32. Ayton, S., Lei, P., Duce, J. A., Wong, B. X. W., Sedjahtera, A., Adlard, P. A., Bush, A. I., and Finkelstein, D. I. (2013) Ceruloplasmin dysfunction and therapeutic potential for Parkinson disease Ann. Neurol. 73, 554-559 10.1002/ana.23817
33. Gundersen, H. J., Bagger, P., Bendtsen, T. F., Evans, S. M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J. R., Pakkenberg, B., Sørensen, F. B., Vesterby, A., and West, M. J. (1988) The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis APMIS 96, 857-881 10.1111/j.1699-0463.1988.tb00954.x
34. Parish, C. L., Stanic, D., Drago, J., Borrelli, E., Finkelstein, D. I., and Horne, M. K. (2002) Effects of long-term treatment with dopamine receptor agonists and antagonists on terminal arbor size Eur. J. Neurosci. 16, 787-794 10.1046/j.1460-9568.2002.02132.x