Lipophilic adamantyl- or deferasirox-based conjugates of desferrioxamine B have enhanced neuroprotective capacity: Implications for Parkinson disease

Free Radical Biology and Medicine

Volumn 60, Issue , 2013, Pages 147-156

  Liddell, Jeffrey R ^a   Obando, Daniel ^b   Liu, Joe ^b   Ganio, George ^a   Volitakis, Irene ^a   Mok, Su San ^a   Crouch, Peter J ^a   White, Anthony R ^a   Codd, Rachel ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Chelator; DFOB; Free radicals; Hydrogen peroxide; Iron; Oxidative stress; Paraquat; Parkinson disease

Indexed keywords

ADAMANTANE; ALPHA SYNUCLEIN; CLIOQUINOL; DEFERASIROX; DEFEROXAMINE; GLUTATHIONE; HYDROGEN PEROXIDE; PHENANTHROLINE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CELL; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG BIOAVAILABILITY; DRUG CONJUGATION; MOUSE; NERVE CELL; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL;

ADAMANTANE; ANIMALS; ASTROCYTES; BENZOATES; CELLS, CULTURED; DEFEROXAMINE; DOPAMINERGIC NEURONS; HUMANS; HYDROGEN PEROXIDE; IRON CHELATING AGENTS; MICE; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PARKINSON DISEASE; PERMEABILITY; SUBSTANTIA NIGRA; TRIAZOLES;

ANIMALIA;

EID: 84875336179     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.01.027     Document Type: Article

References (81)

1. K.A. Jellinger Neuropathology of sporadic Parkinson's disease: evaluation and changes of concepts Mov. Disord 27 2011 8 30
2. I. Ferrer Neuropathology and neurochemistry of nonmotor symptoms in Parkinson's disease Parkinsons Dis 2011 2011 708404
3. M.E. Gotz, K. Double, M. Gerlach, M.B. Youdim, and P. Riederer The relevance of iron in the pathogenesis of Parkinson's disease Ann. N. Y. Acad. Sci. 1012 2004 193 208
4. J. Sian-Hulsmann, S. Mandel, M.B. Youdim, and P. Riederer The relevance of iron in the pathogenesis of Parkinson's disease J. Neurochem. 118 2011 939 957
5. M. Arredondo, and M.T. Nunez Iron and copper metabolism Mol. Aspects Med. 26 2005 313 327
6. D.B. Kell Towards a unifying, systems biology understanding of large-scale cellular death and destruction caused by poorly liganded iron: Parkinson's, Huntington's, Alzheimer's, prions, bactericides, chemical toxicology and others as examples Arch. Toxicol 84 2010 825 889
7. M. Hashimoto, A. Takeda, L.J. Hsu, T. Takenouchi, and E. Masliah Role of cytochrome c as a stimulator of alpha-synuclein aggregation in Lewy body disease J. Biol. Chem. 274 1999 28849 28852
8. R.J. Castellani, S.L. Siedlak, G. Perry, and M.A. Smith Sequestration of iron by Lewy bodies in Parkinson's disease Acta Neuropathol. 100 2000 111 114
9. J. Sian, D.T. Dexter, A.J. Lees, S. Daniel, Y. Agid, F. Javoy-Agid, P. Jenner, and C.D. Marsden Alterations in glutathione levels in Parkinson's disease and other neurodegenerative disorders affecting basal ganglia Ann. Neurol. 36 1994 348 355
10. R.K. Pearce, A. Owen, S. Daniel, P. Jenner, and C.D. Marsden Alterations in the distribution of glutathione in the substantia nigra in Parkinson's disease J. Neural Transm. 104 1997 661 677
11. H.L. Martin, and P. Teismann Glutathione - a review on its role and significance in Parkinson's disease FASEB J 23 2009 3263 3272
12. M.B. Spina, and G. Cohen Dopamine turnover and glutathione oxidation: implications for Parkinson disease Proc. Natl. Acad. Sci. USA 86 1989 1398 1400
13. D.G. Graham Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones Mol. Pharmacol 14 1978 633 643
14. D.A. Drechsel, and M. Patel Role of reactive oxygen species in the neurotoxicity of environmental agents implicated in Parkinson's disease Free Radic. Biol. Med 44 2008 1873 1886
15. C. Henchcliffe, and M.F. Beal Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis Nat. Clin. Pract. Neurol. 4 2008 600 609
16. K. Kuter, P. Nowak, K. Golembiowska, and K. Ossowska Increased reactive oxygen species production in the brain after repeated low-dose pesticide paraquat exposure in rats: a comparison with peripheral tissues Neurochem. Res 35 2010 1121 1130
17. A.I. Brooks, C.A. Chadwick, H.A. Gelbard, D.A. Cory-Slechta, and H.J. Federoff Paraquat elicited neurobehavioral syndrome caused by dopaminergic neuron loss Brain Res. 823 1999 1 10
18. T.P. Brown, P.C. Rumsby, A.C. Capleton, L. Rushton, and L.S. Levy Pesticides and Parkinson's disease - is there a link? 114 2006 156 164
19. C.M. Tanner, F. Kamel, G.W. Ross, J.A. Hoppin, S.M. Goldman, M. Korell, C. Marras, G.S. Bhudhikanok, M. Kasten, A.R. Chade, K. Comyns, M.B. Richards, C. Meng, B. Priestley, H.H. Fernandez, F. Cambi, D.M. Umbach, A. Blair, D.P. Sandler, and J.W. Langston Rotenone, paraquat, and Parkinson's disease Environ. Health Perspect. 119 2011 866 872
20. J.S. Bus, and J.E. Gibson Paraquat: model for oxidant-initiated toxicity Environ. Health Perspect. 55 1984 37 46
21. S. Konetschny-Rapp, G. Jung, K.N. Raymond, J. Meiwes, and H. Zaehner Solution thermodynamics of the ferric complexes of new desferrioxamine siderophores obtained by directed fermentation J. Am. Chem. Soc. 114 1992 2224 2230
22. D. Ben-Shachar, G. Eshel, P. Riederer, and M.B. Youdim Role of iron and iron chelation in dopaminergic-induced neurodegeneration: implication for Parkinson's disease Ann. Neurol. 32 Suppl 1992 S105 110
23. D. Ben-Shachar, G. Eshel, J.P. Finberg, and M.B. Youdim The iron chelator desferrioxamine (Desferal) retards 6-hydroxydopamine-induced degeneration of nigrostriatal dopamine neurons J. Neurochem. 56 1991 1441 1444
24. M. Santiago, E.R. Matarredona, L. Granero, J. Cano, and A. Machado Neuroprotective effect of the iron chelator desferrioxamine against MPP+ toxicity on striatal dopaminergic terminals J. Neurochem. 68 1997 732 738
25. J. Lan, and D.H. Jiang Desferrioxamine and vitamin E protect against iron and MPTP-induced neurodegeneration in mice J. Neural Transm 104 1997 469 481
26. Z. Zhang, K. Zhang, X. Du, and Y. Li Neuroprotection of desferrioxamine in lipopolysaccharide-induced nigrostriatal dopamine neuron degeneration Mol. Med. Report 5 2012 562 566
27. J.L. Kwiatkowski Real-world use of iron chelators Hematology Am. Soc. Hematol. Educ. Program 2011 2011 451 458
28. J.B. Porter Concepts and goals in the management of transfusional iron overload Am. J. Hematol. 82 2007 1136 1139
29. D.S. Kalinowski, and D.R. Richardson The evolution of iron chelators for the treatment of iron overload disease and cancer Pharmacol. Rev. 57 2005 547 583
30. D.R. Crapper McLachlan, A.J. Dalton, T.P. Kruck, M.Y. Bell, W.L. Smith, W. Kalow, and D.F. Andrews Intramuscular desferrioxamine in patients with Alzheimer's disease Lancet 337 1991 1304 1308
31. M.E. Percy, T.P. Kruck, A.I. Pogue, and W.J. Lukiw Towards the prevention of potential aluminum toxic effects and an effective treatment for Alzheimer's disease J. Inorg. Biochem. 105 2011 1505 1512
32. W. Zhu, W. Xie, T. Pan, P. Xu, M. Fridkin, H. Zheng, J. Jankovic, M.B. Youdim, and W. Le Prevention and restoration of lactacystin-induced nigrostriatal dopamine neuron degeneration by novel brain-permeable iron chelators FASEB J 21 2007 3835 3844
33. D. Kaur, F. Yantiri, S. Rajagopalan, J. Kumar, J.Q. Mo, R. Boonplueang, V. Viswanath, R. Jacobs, L. Yang, M.F. Beal, D. DiMonte, I. Volitaskis, L. Ellerby, R.A. Cherny, A.I. Bush, and J.K. Andersen Genetic or pharmacological iron chelation prevents MPTP-induced neurotoxicity in vivo: a novel therapy for Parkinson's disease Neuron 37 2003 899 909
34. O. Weinreb, T. Amit, S. Mandel, L. Kupershmidt, and M.B. Youdim Neuroprotective multifunctional iron chelators: from redox-sensitive process to novel therapeutic opportunities Antioxid. Redox Signaling 13 2010 919 949
35. L. Kupershmidt, O. Weinreb, T. Amit, S. Mandel, O. Bar-Am, and M.B. Youdim Novel molecular targets of the neuroprotective/neurorescue multimodal iron chelating drug M30 in the mouse brain Neuroscience 189 2011 345 358
36. M.B. Youdim M30, a brain permeable multi target neurorestorative drug in post nigrostriatal dopamine neuron lesion of parkinsonism animal models Parkinsonism Relat. Disord 18 Suppl. 1 2012 S151 154
37. J. Liu, D. Obando, L.G. Schipanski, L.K. Groebler, P.K. Witting, D.S. Kalinowski, D.R. Richardson, and R. Codd Conjugates of desferrioxamine B (DFOB) with derivatives of adamantane or with orally available chelators as potential agents for treating iron overload J. Med. Chem. 53 2010 1370 1382
38. M.J. Baptista, C. O'Farrell, S. Daya, R. Ahmad, D.W. Miller, J. Hardy, M.J. Farrer, and M.R. Cookson Co-ordinate transcriptional regulation of dopamine synthesis genes by alpha-synuclein in human neuroblastoma cell lines J. Neurochem. 85 2003 957 968
39. T. Du, G.D. Ciccotosto, G.A. Cranston, G. Kocak, C.L. Masters, P.J. Crouch, R. Cappai, and A.R. White Neurotoxicity from glutathione depletion is mediated by Cu-dependent p53 activation Free Radic. Biol. Med. 44 2008 44 55
40. J.R. Liddell, C. Zwingmann, M.M. Schmidt, A. Thiessen, D. Leibfritz, S.R. Robinson, and R. Dringen Sustained hydrogen peroxide stress decreases lactate production by cultured astrocytes J. Neurosci. Res. 87 2009 2696 2708
41. K.A. Price, P.J. Crouch, S. Lim, B.M. Paterson, J.R. Liddell, P.S. Donnelly, and A.R. White Subcellular localization of a fluorescent derivative of CuII(atsm) offers insight into the neuroprotective action of CuII(atsm) Metallomics 3 2011 1280 1290
42. J.G. Culvenor, C.A. McLean, S. Cutt, B.C. Campbell, F. Maher, P. Jakala, T. Hartmann, K. Beyreuther, C.L. Masters, and Q.X. Li Non-Abeta component of Alzheimer's disease amyloid (NAC) revisited: NAC and alpha-synuclein are not associated with Abeta amyloid Am. J. Pathol. 155 1999 1173 1181
43. R.M. Pielak, and J.J. Chou Flu channel drug resistance: a tale of two sites Protein Cell 1 2010 246 258
44. O. Rascol, A. Lozano, M. Stern, and W. Poewe Milestones in Parkinson's disease therapeutics Mov. Disord 26 2011 1072 1082
45. J. Liu, D. Obando, V. Liao, T. Lifa, and R. Codd The many faces of the adamantyl group in drug design Eur. J. Med. Chem. 46 2011 1949 1963
46. S. Salomone, F. Caraci, G.M. Leggio, J. Fedotova, and F. Drago New pharmacological strategies for treatment of Alzheimer's disease: focus on disease modifying drugs Br. J. Clin. Pharmacol. 73 2012 504 517
47. J.B. Porter Deferasirox: an update Hemoglobin 33 Suppl. 1 2009 S70 75
48. H. Nick, A. Wong, P. Acklin, B. Faller, Y. Jin, R. Lattmann, T. Sergejew, S. Hauffe, H. Thomas, and H.P. Schnebli ICL670A: preclinical profile Adv. Exp. Med. Biol. 509 2002 185 203
49. J.B. Galey Potential use of iron chelators against oxidative damage Adv. Pharmacol. 38 1997 167 203
50. C.W. Ritchie, A.I. Bush, A. Mackinnon, S. Macfarlane, M. Mastwyk, L. MacGregor, L. Kiers, R. Cherny, Q.X. Li, A. Tammer, D. Carrington, C. Mavros, I. Volitakis, M. Xilinas, D. Ames, S. Davis, K. Beyreuther, R.E. Tanzi, and C.L. Masters Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Abeta amyloid deposition and toxicity in Alzheimer disease: a pilot phase 2 clinical trial Arch. Neurol. 60 2003 1685 1691
51. G. Liu, L. Aliaga, and H. Cai alpha-Synuclein, LRRK2 and their interplay in Parkinson's disease Future Neurol 7 2012 145 153
52. G.M. Bishop, T.N. Dang, R. Dringen, and S.R. Robinson Accumulation of non-transferrin-bound iron by neurons, astrocytes, and microglia Neurotox. Res. 19 2011 443 451
53. C.M. Morris, and J.A. Edwardson Iron histochemistry of the substantia nigra in Parkinson's disease Neurodegeneration 3 1994 277 282
54. J. Sian, D.T. Dexter, A.J. Lees, S. Daniel, P. Jenner, and C.D. Marsden Glutathione-related enzymes in brain in Parkinson's disease Ann. Neurol. 36 1994 356 361
55. J.R. Liddell, H.H. Hoepken, P.J. Crack, S.R. Robinson, and R. Dringen Glutathione peroxidase 1 and glutathione are required to protect mouse astrocytes from iron-mediated hydrogen peroxide toxicity J. Neurosci. Res. 84 2006 578 586
56. M.R. Summers, A. Jacobs, D. Tudway, P. Perera, and C. Ricketts Studies in desferrioxamine and ferrioxamine metabolism in normal and iron-loaded subjects Br. J. Haematol. 42 1979 547 555
57. J.B. Porter, R. Rafique, S. Srichairatanakool, B.A. Davis, F.T. Shah, T. Hair, and P. Evans Recent insights into interactions of deferoxamine with cellular and plasma iron pools: implications for clinical use Ann. N. Y. Acad. Sci. 1054 2005 155 168
58. H.S. Chun, G.E. Gibson, L.A. DeGiorgio, H. Zhang, V.J. Kidd, and J.H. Son Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism J. Neurochem. 76 2001 1010 1021
59. S. Ramachandiran, J.M. Hansen, D.P. Jones, J.R. Richardson, and G.W. Miller Divergent mechanisms of paraquat, MPP+, and rotenone toxicity: oxidation of thioredoxin and caspase-3 activation Toxicol. Sci. 95 2007 163 171
60. W. Ying, S.K. Han, J.W. Miller, and R.A. Swanson Acidosis potentiates oxidative neuronal death by multiple mechanisms J. Neurochem. 73 1999 1549 1556
61. T. Jayasena, R.S. Grant, N. Keerthisinghe, I. Solaja, and G.A. Smythe Membrane permeability of redox active metal chelators: an important element in reducing hydroxyl radical induced NAD+ depletion in neuronal cells Neurosci. Res. 57 2007 454 461
62. R. Kruger, W. Kuhn, T. Muller, D. Woitalla, M. Graeber, S. Kosel, H. Przuntek, J.T. Epplen, L. Schols, and O. Riess Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease Nat. Genet. 18 1998 106 108
63. N. Ostrerova-Golts, L. Petrucelli, J. Hardy, J.M. Lee, M. Farer, and B. Wolozin The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity J. Neurosci. 20 2000 6048 6054
64. 2 in a human neuroblastoma divided cell line transfected with α-synuclein and its familial Parkinson's disease-linked mutants 342 2003 124 128
65. F.L. Martin, S.J.M. Williamson, K.E. Paleologou, R. Hewitt, O.M.A. El-Agnaf, and D. Allsop Fe(II)-induced DNA damage in α-synuclein- transfected human dopaminergic BE(2)-M17 neuroblastoma cells: detection by the comet assay 87 2003 620 630
66. E. Junn, and M.M. Mouradian Human alpha-synuclein over-expression increases intracellular reactive oxygen species levels and susceptibility to dopamine Neurosci. Lett 320 2002 146 150
67. 2- and Sin-1-induced cell death Neurobiol. Aging 28 2007 1709 1717
68. C.E. Moussa, C. Wersinger, Y. Tomita, and A. Sidhu Differential cytotoxicity of human wild type and mutant alpha-synuclein in human neuroblastoma SH-SY5Y cells in the presence of dopamine Biochemistry 43 2004 5539 5550
69. W. Xie, O.W. Wan, and K.K. Chung New insights into the role of mitochondrial dysfunction and protein aggregation in Parkinson's disease Biochim. Biophys. Acta 1802 2010 935 941
70. M. Fontecave, and J.L. Pierre Activation and toxicity of oxygen. 2. Iron and hydrogen peroxide: biochemical aspects Bull. Soc. Chim. Fr 130 1993 77 85
71. I. Spasojevic, S.K. Armstrong, T.J. Brickman, and A.L. Crumbliss Electrochemical behavior of the Fe(III) complexes of the cyclic hydroxamate siderophores alcaligin and desferrioxamine E Inorg. Chem. 38 1999 449 454
72. J.C. Tomkinson, and R.J.P. Williams Oxidation-reduction potentials of complex ions J. Chem. Soc. 1958 2010 2018
73. B. Halliwell, and J.M. Gutteridge Free Radicals in Biology and Medicine 2007 Oxford Univ. Press Oxford
74. A. Caragounis, T. Du, G. Filiz, K.M. Laughton, I. Volitakis, R.A. Sharples, R.A. Cherny, C.L. Masters, S.C. Drew, A.F. Hill, Q.X. Li, P.J. Crouch, K.J. Barnham, and A.R. White Differential modulation of Alzheimer's disease amyloid beta-peptide accumulation by diverse classes of metal ligands Biochem. J. 407 2007 435 450
75. A. Takeda, A. Devenyi, and J.R. Connor Evidence for non-transferrin- mediated uptake and release of iron and manganese in glial cell cultures from hypotransferrinemic mice J. Neurosci. Res 51 1998 454 462
76. S.E. Hamrick, P.S. McQuillen, X. Jiang, D. Mu, A. Madan, and D.M. Ferriero A role for hypoxia-inducible factor-1alpha in desferoxamine neuroprotection Neurosci. Lett. 379 2005 96 100
77. Y. Avramovich-Tirosh, O. Bar-Am, T. Amit, M.B. Youdim, and O. Weinreb Up-regulation of hypoxia-inducible factor (HIF)-1alpha and HIF-target genes in cortical neurons by the novel multifunctional iron chelator anti-Alzheimer drug, M30 Curr. Alzheimer Res 7 2010 300 306
78. D.W. Lee, S. Rajagopalan, A. Siddiq, R. Gwiazda, L. Yang, M.F. Beal, R.R. Ratan, and J.K. Andersen Inhibition of prolyl hydroxylase protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity: model for the potential involvement of the hypoxia-inducible factor pathway in Parkinson disease J. Biol. Chem. 284 2009 29065 29076
79. L.K. Groebler, J. Liu, A. Shanu, R. Codd, and P.K Witting Comparing the potential renal protective activity of desferrioxamine B and the novel chelator desferrioxamine B-N-(3-hydroxyadamant-1-yl)carboxamide in a cell model of myoglobinuria Biochem. J. 435 2011 669 677
80. B.J. Reeder, and M.T. Wilson Desferrioxamine inhibits production of cytotoxic heme to protein cross-linked myoglobin: a mechanism to protect against oxidative stress without iron chelation Chem. Res. Toxicol 18 2005 1004 1011
81. S.A. Hitchcock, and L.D. Pennington Structure-brain exposure relationships J. Med. Chem. 49 2006 7559 7583