An N-heterocyclic amine chelate capable of antioxidant capacity and amyloid disaggregation

ACS Chemical Neuroscience

Volumn 3, Issue 11, 2012, Pages 919-927

  Lincoln, Kimberly M ^a   Richardson, Timothy E ^b   Rutter, Lauren ^a   Gonzalez, Paulina ^a   Simpkins, James W ^b   Green, Kayla N ^a  

^a TEXAS CHRISTIAN UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

aggregates; Alzheimers disease; Amyloid; chelate; copper; zinc

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; ANTIOXIDANT; CHELATE; COPPER ION; DICHLORODIHYDROFLUORESCEIN DIACETATE; PYCLEN; PYRIDINE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOASSAY; CELL DEATH; CONTROLLED STUDY; DENSITY FUNCTIONAL THEORY; NEUROFIBRILLARY TANGLE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; SCANNING ELECTRON MICROSCOPY; SPECTROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

AMINES; AMYLOID BETA-PEPTIDES; ANTIOXIDANTS; AZABICYCLO COMPOUNDS; CHELATING AGENTS; COPPER; HETEROCYCLIC COMPOUNDS; HUMANS; LIGANDS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; NEPHELOMETRY AND TURBIDIMETRY; OXIDATIVE STRESS; TRACE ELEMENTS; TYROSINE; ZINC;

EID: 84869768621     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn300060v     Document Type: Article

References (87)

1. (2011) Alzheimers Disease Facts and Figures, Alzheimers & Dementia, Alzheimers Association, p 7.
2. Wenk, G. L. (2003) Neuropathologic changes in Alzheimers disease J. Clin. Psychiatry 64, 7-10
3. Ono, M., Hayashi, S., Matsumura, K., Kimura, H., Okamoto, Y., Ihara, M., Takahashi, R., Mori, H., and Saji, H. (2011) Rhodanine and Thiohydantoin Derivatives for Detecting Tau Pathology in Alzheimers Brains ACS Chem. Neurosci. 2, 269-275
4. Wolk, D. A., Grachev, I. D., Buckley, C., Kazi, H., Grady, M. S., Trojanowski, J. Q., Hamilton, R. H., Sherwin, P., McLain, R., and Arnold., S. E. (2011) Association Between In Vivo Fluorine 18-Labeled Flutemetamol Amyloid Positron Emission Tomography Imaging and In Vivo Cerebral Cortical Histopathology Arch. Neurol. 68, 1398-1403
5. Fleisher, S., Chen, K., Liu, X., Roontiva, A., Thiyyagura, P., Ayutyanont, N., Joshi, A. D., Clark, C. M., Mintun, M. A., Pontecorvo, M. J., Doraiswamy, P. M., Johnson, K. A., Skovronsky, D. M., and Reiman, E. M. (2011) Using Positron Emission Tomography and Florbetapir F 18 to Image Cortical Amyloid in Patients With Mild Cognitive Impairment or Dementia Due to Alzheimer Disease Arch. Neurol. 68, 1461-1466
6. Rajendran, R., Minqin, R., Ynsa, M. D., Casadesus, G., Smith, M. A., Perry, G., Halliwell, B., and Watt, F. (2009) A novel approach to the identification and quantitative elemental analysis of amyloid deposits-Insights into the pathology of Alzheimers disease Biochem. Biophys. Res. Commun. 382, 91-95
7. Bush, A. I. (2003) The metallobiology of Alzheimers disease Trends Neurosci. 26, 207-214
8. Lovell, M. A., Robertson, J. D., and Teesdale, W. J. (1998) Copper, iron and zinc in AD senile plaques J. Neurol. Sci. 158, 47-52
9. Gaggelli, E., Kozlowski, H., Valensin, D., and Valensin, G. (2006) Copper homeostasis and neurodegenerative disorders (Alzheimers, prion, and Parkinsons diseases and amyotrophic lateral sclerosis) Chem. Rev. 106, 1995-2044
10. Mathis, C. A., Wang, Y., and Klunk, W. E. (2004) Imaging β-amyloid plaques and neurofibrillary tangles in the aging human brain Curr. Pharm. Des. 10, 1469-1492
11. Que, E. L., Domaille, D. W., and Chang, C. J. (2008) Metals in Neurobiology: Probing Their Chemistry and Biology with Molecular Imaging Chem. Rev. 108, 1517-1549
12. Fodero-Tavoletti, M. T., Villemagne, V. L., Rowe, C. C., Masters, C. L., Barnham, K. J., and Cappai, R. (2011) Amyloid-β: the seeds of darkness Int. J. Biochem. Cell Biol. 43, 1247-1251
13. Jakob-Roetne, R. and Jacobsen, H. (2009) Alzheimers disease: from pathology to therapeutic approaches Angew. Chem. 48, 3030-3059
14. Verdile, G., Fuller, S., Atwood, C. S., Laws, S. M., Gandy, S. E., and Martins, R. N. (2004) The role of beta amyloid in Alzheimers disease: still a cause of everything or the only one who got caught? Pharmacol. Res. 50, 397-409
15. Shankar, G. M., Li, S., and Mehta, T. H. (2008) Amyloid-β protein dimers isolated directly from Alzheimers brains impair synaptic plasticity and memory Nat. Med. 14, 837-842
16. Maynard, C. J., Bush, A. I., Masters, C. L., Cappai, R., and Li, Q. X. (2005) Metals and amyloid-beta in Alzheimers disease Int. J. Exp. Pathol. 86, 147-159
17. Rauk, A. (2009) The chemistry of Alzheimers disease Chem. Soc. Rev. 38, 2698-2715
18. Barnham, K. J. and Bush, A. I. (2008) Metals in Alzheimers and Parkinsons Diseases Curr. Opin. Chem. Biol. 12, 222-228
19. Duce, J. A. and Bush, A. I. (2010) Biological metals and Alzheimers disease: Implications for therapeutics and diagnostics Prog. Neurobiol. (Oxford, U.K.) 92, 1-18
20. Molina-Holgado, F., Hider, R. C., Gaeta, A., Williams, R., and Francis, P. (2007) Metals ions and neurodegeneration BioMetals 20, 639-654
21. Drew, S. C. and Barnham, K. J. (2011) The Heterogeneous Nature of Cu2+ Interactions with Alzheimers Amyloid-beta Peptide Acc. Chem. Res. 44, 1146-1155
22. Hyman, L. M. and Franz, K. J. (2012) Probing oxidative stress: Small molecule fluorescent sensors of metal ions, reactive oxygen species, and thiols Coord. Chem. Rev. 256, 2333-2356
23. Kraatz, H.-B. and Metlzer-Nolte, N. Concepts and Models in Bioinorganic Chemistry; 2006.
24. Barnham, K. J., Curtain, C. C., and Bush, A. I. (2007) Free radicals, metal ions, and Aβ aggregation and neurotoxicity Protein Rev. 6, 31-47
25. Barnham, K. J., Masters, C. L., and Bush, A. I. (2004) Neurodegenerative diseases and oxidative stress, Nature reviews Drug Discovery 3, 205-214
26. Smith, D. P., Ciccotosto, G. D., Tew, D. J., Fodero-Tavoletti, M. T., Johanssen, T., Masters, C. L., Barnham, K. J., and Cappai, R. (2007) Concentration Dependent Cu2+ Induced Aggregation and Dityrosine Formation of the Alzheimers Disease Amyloid-β Peptide Biochemistry 46, 2881-2891
27. Braymer, J. J., DeToma, A. S., Choi, J. S., Ko, K. S., and Lim, M.-H. (2011) Recent Development of Bifunctional Small Molecules to Study Metal-Amyloid -β-Species in Alzheimers Disease Int. J. Alzheimers Dis. 1-9
28. Crouch, P. J., Harding, S.-M. E., White, A. R., Camakaris, J., Bush, A. I., and Masters, C. L. (2008) Mechanisms of Aβ mediated neurodegeneration in Alzheimers disease Int. J. Biochem. Cell Biol. 40, 181-198
29. Adlard, P. A. and Bush, A. I. (2011) Zinc and Alzheimers disease Biomed. Health Res. 76, 417-431
30. Adlard, P. A., Cherny, R. A., Finkelstein, D. I., Gautier, E., Robb, E., Cortes, M., Volitakis, I., Liu, X., Smith, J. P., Perez, K., Laughton, K., Li, Q. X., Charman, S. A., Nicolazzo, J. A., Wilkins, S., Deleva, K., Lynch, T., Kok, G., Ritchie, C. W., Tanzi, R. E., Cappai, R., Masters, C. L., Barnham, K. J., and Bush, A. I. (2008) Rapid restoration of cognition in Alzheimers transgenic mice with 8-hydroxy quinoline analogs is associated with decreased interstitial Abeta Neuron 59, 43-55
31. Adlard, P. A., Parncutt, J. M., Finkelstein, D. I., and Bush, A. I. (2010) Cognitive Loss in Zinc Transporter-3 Knock-Out Mice: A Phenocopy for the Synaptic and Memory Deficits of Alzheimers Disease? J. Neurosci. 30, 1631-1636
32. Crouch, P. J., Hung, L. W., Adlard, P. A., Cortes, M., Lal, V., Filiz, G., Perez, K. A., Nurjono, M., Caragounis, A., Du, T., Laughton, K., Volitakis, I., Bush, A. I., Li, Q. X., Masters, C. L., Cappai, R., Cherny, R. A., Donnelly, P. S., White, A. R., and Barnham, K. J. (2009) Increasing Cu bioavailability inhibits Abeta oligomers and tau phosphorylation Proc. Natl. Acad. Sci. U.S.A. 106, 381-386
33. Crouch, P. J., Savva, M. S., Hung, L. W., Donnelly, P. S., Mot, A. I., Parker, S. J., Greenough, M. A., Volitakis, I., Adlard, P. A., Cherny, R. A., Masters, C. L., Bush, A. I., Barnham, K. J., and White, A. R. (2011) The Alzheimers therapeutic PBT2 promotes amyloid-β degradation and GSK3 phosphorylation via a metal chaperone activity J. Neurochem. 119, 220-230
34. James, S. A., Volitakis, I., Adlard, P. A., Duce, J. A., Masters, C. L., Cherny, R. A., and Bush, A. I. (2012) Elevated labile Cu is associated with oxidative pathology in Alzheimer disease Free Radical Biol. Med. 52, 298-302
35. Manso, Y., Comes, G., Hidalgo, J., Bush, A. I., and Adlard, P. A. (2011) Copper modulation as a therapy for Alzheimers disease? Int. J. Alzheimers Dis. 370345, 370345
36. Miu, A. C., Benga, O., Adlard, P. A., and Bush, A. I. (2006) Metals and Alzheimers disease J. Alzheimers Dis. 10, 145-163
37. Strozyk, D., Launer, L. J., Adlard, P. A., Cherny, R. A., Tsatsanis, A., Volitakis, I., Blennow, K., Petrovitch, H., White, L. R., and Bush, A. I. (2009) Zinc and copper modulate Alzheimer Aβ levels in human cerebrospinal fluid Neurobiol. Aging 30, 1069-1077
38. Faller, P. (2009) Copper and zinc binding to amyloid-β: coordination, dynamics, aggregation, reactivity and metal-ion transfer ChemBioChem 10, 2837-2845
39. Casadesus, G., Smith, M. A., Zhu, X. W., Aliev, G., Cash, A. D., Honda, K., Petersen, R. B., and Perry, G. (2004) Alzheimer disease: Evidence for a central pathogenic role of iron-mediated reactive oxygen species J. Alzheimers Dis. 6, 165-169
40. Castellani, R. J., Honda, K., Zhu, X. W., Cash, A. D., Nunomura, A., Perry, G., and Smith, M. A. (2004) Contribution of redox-active iron and copper to oxidative damage in Alzheimer disease Ageing Res. Rev. 3, 319-326
41. Wilkins, S., Masters, C. L., Bush, A. I., Cherny, R. A., and Finkelstein, D. I. (2009) Clioquinol protects against cell death in parkinsons disease models in vivo and in vitro Adv. Behav. Biol. 58, 431-442
42. Berk, M., Copolov, D. L., Dean, O., Lu, K., Jeavons, S., Schapkaitz, I., Anderson-Hunt, M., and Bush, A. I. (2008) N-Acetyl Cysteine for Depressive Symptoms in Bipolar Disorder-A Double-Blind Randomized Placebo-Controlled Trial Biol. Psychiatry 64, 468-475
43. Greenough, M. A., Volitakis, I., Li, Q.-X., Laughton, K., Evin, G., Ho, M., Dalziel, A. H., Camakaris, J., and Bush, A. I. (2011) Presenilins promote the cellular uptake of copper and zinc and maintain copper chaperone of SOD1-dependent copper/zinc superoxide dismutase activity J. Biol. Chem. 286, 9776-9786
44. Hung, Y. H., Robb, E. L., Volitakis, I., Ho, M., Evin, G., Li, Q.-X., Culvenor, J. G., Masters, C. L., Cherny, R. A., and Bush, A. I. (2009) Paradoxical condensation of copper with elevated β-amyloid in lipid rafts under cellular copper deficiency conditions: Implications for Alzheimer disease J. Biol. Chem. 284, 21899-21907
45. Melov, S., Adlard, P. A., Morten, K., Johnson, F., Golden, T. R., Hinerfeld, D., Schilling, B., Mavros, C., Masters, C. L., Volitakis, I., Li, Q.-X., Laughton, K., Hubbard, A., Cherny, R. A., Gibson, B., and Bush, A. I. (2007) Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS One 2, e536.
46. Watanabe, S., Nagano, S., Duce, J., Kiaei, M., Li, Q.-X., Tucker, S. M., Tiwari, A., Brown, R. H., Beal, M. F., Hayward, L. J., Culotta, V. C., Yoshihara, S., Sakoda, S., and Bush, A. I. (2007) Increased affinity for copper mediated by cysteine 111 in forms of mutant superoxide dismutase 1 linked to amyotrophic lateral sclerosis Free Radical Biol. Med. 42, 1534-1542
47. Crichton, R. R., Dexter, D. T., and Ward, R. J. (2008) Metal based neurodegenerative diseases-From molecular mechanisms to therapeutic strategies Coord. Chem Rev 252, 1189-1199
48. Adlard, P. A., Bica, L., White, A. R., Nurjono, M., Filiz, G., Crouch, P. J., Donnelly, P. S., Cappai, R., Finkelstein, D. I., and Bush, A. I. (2011) Metal ionophore treatment restores dendritic spine density and synaptic protein levels in a mouse model of Alzheimers disease PLoS One 6, e17669
49. Adlard, P. A., Parncutt, J. M., Finkelstein, D. I., and Bush, A. I. (2010) Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimers disease? J. Neurosci. 30, 1631-1636
50. Hardeland, R. (2005) Antioxidative protection by melatonin-Multiplicity of mechanisms from radical detoxification to radical avoidance Endocrine 27, 119-130
51. Lynch, M. A. (2004) Long-term potentiation and memory Physiol. Rev. 84, 87-136
52. Khan, A., Ashcroft, A. E., Korchazhkina, O. V., and Exley, C. (2004) Metal-mediated formation of fibrillar ABri amyloid J. Inorg. Biochem. 98, 2006-2010
53. Zatta, P., Drago, D., Zambenedetti, P., Bolognin, S., Nogara, E., Peruffo, A., and Cozzi, B. (2008) Accumulation of copper and other metal ions, and metallothionein I/II expression in the bovine brain as a function of aging J. Chem. Neuroanat. 36, 1-5
54. Sayre, L. M., Smith, M. A., and Perry, G. (2001) Chemistry and biochemistry of oxidative stress in neurodegenerative disease Curr. Med. Chem. 8, 721-738
55. Zambenedetti, P., Schmitt, H. P., and Zatta, P. (2002) Metallothionein I-II immunocytochemical reactivity in Binswangers encephalopathy J. Alzheimers Dis. 4, 459-466
56. Zatta, P., Raso, M., Zambenedetti, P., Wittkowski, W., Messori, L., Piccioli, F., Mauri, P. L., and Beltramini, M. (2005) Copper and zinc dismetabolism in the mouse brain upon chronic cuprizone treatment Cell. Mol. Life Sci. 62, 1502-1513
57. Lannfelt, L., Blennow, K., Zetterberg, H., Batsman, S., Ames, D., Harrison, J., Maters, C. L., Targum, S., Bush, A. I., Murdoch, R., Wilson, J., and Ritchie, C. W. (2008) Safety, efficacy, and biomarker findings of PBT2 in targeting Aβ as a modifying therapy for Alzheimers disease: a phase IIa, double-blind, randomized, placebo-controlled trial Lancet Neurol. 7, 779-786
58. Bush, A. I. and Tanzi, R. E. (2008) Therapeutics for Alzheimers disease based on the metal hypothesis Neurotherapeutics 5, 421-432
59. Crabb, E. and Moore, E. A. (2009) Metals and Life, Chelation Therapy, Springer.
60. Hegde, M. L., Bharathi, P., Suram, A., Venugopal, C., Jagannathan, R., Poddar, P., Srinivas, P., Sambamurti, K., Rao, K. J., Scancar, J., Messori, L., Zecca, L., and Zatta, P. (2009) Challenges associated with metal chelation therapy in Alzheimers disease J. Alzheimers Dis. 17, 457-468
61. Ritchie, C. W., Bush, A. I., Mackinnon, A., Macfarlane, S., Mastwyk, M., MacGregor, L., Kiers, L., Cherny, R., Li, Q. X., Tammer, A., Carrington, D., Mavros, C., Volitakis, I., Xilinas, M., Ames, D., Davis, S., Beyreuther, K., Tanzi, R. E., and Masters, C. L. (2003) Metal-protein attenuation with iodochlorhydroxyquin (clioquinol) targeting Abeta amyloid deposition and toxicity in Alzheimer disease: a pilot phase 2 clinical trial Arch. Neurol. 60, 1685-1691
62. Faux, N. G., Ritchie, C. W., Gunn, A., Rembach, A., Tsatsanis, A., Bedo, J., Harrison, J., Lannfelt, L., Blennow, K., Zetterberg, H., Ingelsson, M., Masters, C. L., Tanzi, R. E., Cummings, J. L., Herd, C. M., and Bush, A. I. (2010) PBT2 Rapidly Improves Cognition in Alzheimers Disease: Additional Phase II Analyses J. Alzheimers Dis. 20, 509-516
63. Izatt, R. M., Pawlak, K., Bradshaw, J. S., and Bruening, R. L. (1991) Thermodynamic and kinetic data for macrocycle interactions with cations and anions Chem. Rev. 91, 1721-1785
64. Rojas-Quijano, F. A., Kovacs, Z., and Sherry, A. D. (2006) INOR 282-Synthesis and evaluation of PCTA derivatives as luminescent-CEST active molecular probes for soft tissue imaging. Abstr. Pap. Am. Chem. Soc. 232.
65. Rojas-Quijano, F. A., Benyo, E. T., Tircso, G., Kalman, F. K., Baranyai, Z., Aime, S., Sherry, A. D., and Kovacs, Z. (2009) Lanthanide(III) Complexes of Tris(amide) PCTA Derivatives as Potential Bimodal Magnetic Resonance and Optical Imaging Agents Chem. - Eur. J. 15, 13188-13200
66. Viswanathan, S., Kovacs, Z., Green, K. N., Ratnakar, S. J., and Sherry, A. D. (2010) Alternatives to Gadolinium-Based Metal Chelates for Magnetic Resonance Imaging Chem. Rev. 110, 2960-3018
67. Scott, L. E. and Orvig, C. (2009) Medicinal Inorganic Chemistry Approaches to Passivation and Removal of Aberrant Metal Ions in Disease Chem. Rev. 109, 4885-4910
68. Schugar, H., Green, D. E., Bowen, M. L., Scott, L. E., Storr, T., Bohmerle, K., Thomas, F., Allen, D. D., Lockman, P. R., Merkel, M., Thompson, K. H., and Orvig, C. (2007) Combating Alzheimers disease with multifunctional molecules designed for metal passivation Angew. Chem., Int. Ed. 46, 1716-1718
69. Scott, L. E., Page, B. D. G., Patrick, B. O., and Orvig, C. (2008) Altering pyridinone N-substituents to optimize activity as potential prodrugs for Alzheimers disease Dalton Trans. 6364-6367
70. Chen, T. W., X., He, Y., Zhang, C., Wu, Z., Liao, K., Wang, J., and Guo, Z.. (2009) Effects of Cyclen and Cyclam on Zinc(II)- and Copper(II)-Induced Amyloid β-Peptide Aggregation and Neurotoxicity Inorg. Chem. 48, 5801-5809
71. Hindo, S. S., Mancino, A. M., Braymer, J. J., Liu, Y. H., Vivekanandan, S., Ramamoorthy, A., and Lim, M. H. (2009) Small Molecule Modulators of Copper-Induced A beta Aggregation J. Am. Chem. Soc. 131, 16663-16665
72. Rolinski, O. J., Amaro, M., and Birch, D. J. S. (2010) Early detection of amyloid aggregation using intrinsic fluorescence Biosens. Bioelectron. 25, 2249-2252
73. Amaro, M., Birch, D. J. S., and Rolinski, O. J. (2011) Beta-amyloid oligomerisation monitored by intrinsic tyrosine fluorescence Phys. Chem. Chem. Phys. 13, 6434-6441
74. Maji, S. K., Amsden, J. J., Rothschild, K. J., Condron, M. M., and Teplow, D. B. (2005) Conformational dynamics of amyloid beta-protein assembly probed using intrinsic fluorescence Biochemistry 44, 13365-13376
75. Yang, C.-A., Chen, Y.-H., Ke, S.-C., Chen, Y.-R., Huang, H.-B., Lin, T.-H., and Chen, Y.-C. (2011) Correlation of Copper Interaction, Copper-Driven Aggregation, and Copper-Driven H2O2 Formation with Aβ40 Conformation. Int. J. Alzheimers Dis. Vol. 2011, Article ID 607861, 7 pages. 10.4061/2011/607861
76. Guilloreau, L., Combalbert, S., Sournia-Saquet, A., Mazarguil, H., and Faller, P. (2007) Redox Chemistry of Copper-Amyloid-β: The Generation of Hydroxyl Radical in the Presence of Ascorbate is Linked to Redox-Potentials and Aggregation State ChemBioChem 8, 1317-1325
77. Richardson, T. E., Yang, S. H., Wen, Y., and Simpkins, J. W. (2011) Estrogen protection in Friedreichs ataxia skin fibroblasts Endocrinology 152, 2742-2749
78. Albrecht, P., Lewerenz, J., Dittmer, S., Noack, R., Maher, P., and Methner, A. (2010) Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system xc- as a neuroprotective drug target CNS Neurol. Disord.: Drug Targets 9, 373-382
79. Lipinski, C. A., Lombardo, F., Dominy, B. W., and Feeney, P. J. (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Delivery Rev. 46, 3-26
80. Scarborough, C. C., Sproules, S., Weyhermuller, T., DeBeer, S., and Wieghardt, K. (2011) Electronic and Molecular Structures of the Members of the Electron Transfer Series [Cr((t)bpy)(3)](n) (n = 3+, 2+, 1+, 0): An X-ray Absorption Spectroscopic and Density Functional Theoretical Study Inorg. Chem. 50, 12446-12462
81. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H. C., M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Keith, T., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, J. M., Klene, M., Knox, J. E., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, O., Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2010) Gaussian 09, Revision B.01, Gaussian, Inc., Wallingford, CT.
82. Steenken, S. and Oneill, P. (1979) Reaction of Oh Radicals with 2-Pyridones and 4-Pyridones in Aqueous-Solution-Electron-Spin Resonance and Pulse-Radiolysis Study J. Phys. Chem. 83, 2407-2412
83. Murakami, K. U., T, Morikawa, R., Ito, Masai, Haneda, M., and Yoshino, M. (1998) Antioxidant effect of dipicolinic acid on the metal-catalyzed lipid peroxidation and enzyme inactivation Biomed. Res. 19, 205-208
84. Murakami, K., Tanemura, Y., and Yoshino, M. (2003) Dipicolinic acid prevents the copper-dependent oxidation of low density lipoprotein J. Nutr. Biochem. 14, 99-103
85. Aitken, R. A., Fodi, B., Palmer, M. H., Slawin, A. M. Z., and Yang, J. (2012) Experimental and theoretical molecular and electronic structures of the N-oxides of pyridazine, pyrimidine and pyrazine Tetrahedron 68, 5845-5851
86. Green, K. N., Brothers, S. M., Lee, B., Darensbourg, M. Y., and Rockcliffe, D. A. (2009) Chemical Issues Addressing the Construction of the Distal Ni[Cysteine-Glycine-Cysteine]2- Site of Acetyl CoA Synthase: Why Not Copper? Inorg. Chem. 48, 2780-2792
87. Hureau, C. and Faller, P. (2009) Abeta-mediated ROS production by Cu ions: structural insights, mechanisms and relevance to Alzheimers disease Biochimie 91, 1212-1217