Neuroinflammation and copper in Alzheimer's disease

International Journal of Alzheimer's Disease

Volumn 2013, Issue , 2013, Pages

  Choo, Xin Yi ^a   Alukaidey, Lobna ^a   White, Anthony R ^a   Grubman, Alexandra ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; COPPER; TOLL LIKE RECEPTOR;

ALZHEIMER DISEASE; ANTIINFLAMMATORY ACTIVITY; ASTROCYTE; COPPER HOMEOSTASIS; HOMEOSTASIS; HUMAN; INFLAMMATION; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

EID: 84893674689     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.1155/2013/145345     Document Type: Review

References (145)

1. Newton K., Dixit V. M., Signaling in innate immunity and inflammation. Cold Spring Harbor Perspectives in Biology 2012 4 3 a006049
2. Murdoch J. R., Lloyd C. M., Chronic inflammation and asthma. Mutation Research 2010 690 1-2 24 39 2-s2.0-77955269402 10.1016/j.mrfmmm.2009.09.005
3. Xu H., Barnes G. T., Yang Q., Tan G., Yang D., Chou C. J., Sole J., Nichols A., Ross J. S., Tartaglia L. A., Chen H., Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. Journal of Clinical Investigation 2003 112 12 1821 1830 2-s2.0-9144223683 10.1172/JCI200319451
4. Danesh J., Whincup P., Walker M., Lennon L., Thomson A., Appleby P., Gallimore J. R., Pepys M. B., Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. British Medical Journal 2000 321 7255 199 204 2-s2.0-0034702485
5. Fillon M., Details linking chronic inflammation and cancer continue to emerge. Journal of the National Cancer Institute 2013 105 8 509 510 10.1093/jnci/djt087
6. Minghetti L., Role of inflammation in neurodegenerative diseases. Current Opinion in Neurology 2005 18 3 315 321 2-s2.0-20444466786
7. Wyss-Coray T., Mucke L., Inflammation in neurodegenerative disease-a double-edged sword. Neuron 2002 35 3 419 432 2-s2.0-0036685522 10.1016/S0896-6273(02)00794-8
8. Krishnaswamy J. K., Chu T., Eisenbarth S. C., Beyond pattern recognition: NOD-like receptors in dendritic cells. Trends in Immunology 2013 34 5 224 233 10.1016/j.it.2012.12.003
9. Takeda K., Akira S., TLR signaling pathways. Seminars in Immunology 2004 16 1 3 9 2-s2.0-0742324860 10.1016/j.smim.2003.10.003
10. O'Neill L. A., Bowie A. G., The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nature Reviews Immunology 2007 7 5 353 364 2-s2.0-34247566510 10.1038/nri2079
11. Medzhitov R., Toll-like receptors and innate immunity. Nature Reviews Immunology 2001 1 2 135 145 2-s2.0-0035524488
12. Mogensen T. H., Pathogen recognition and inflammatory signaling in innate immune defenses. Clinical Microbiology Reviews 2009 22 2 240 273 2-s2.0-66449088641 10.1128/CMR.00046-08
13. Becker C., O'Neill L. A. J., Inflammasomes in inflammatory disorders: the role of TLRs and their interactions with NLRs. Seminars in Immunopathology 2007 29 3 239 248 2-s2.0-34548670965 10.1007/s00281-007-0081-4
14. Tak P. P., Firestein G. S., NF- B: a key role in inflammatory diseases. Journal of Clinical Investigation 2001 107 1 7 11 2-s2.0-0034746919
15. Kelly R. J., Minogue A. M., Lyons A., Glial activation in AbetaPP/PS1 mice is associated with infiltration of IFNgamma-producing cells. Journal of Alzheimer's Disease 2013 37 1 63 75
16. Takeuchi O., Akira S., Pattern recognition receptors and inflammation. Cell 2010 140 6 805 820 2-s2.0-77950343791 10.1016/j.cell.2010.01.022
17. Proell M., Riedl S. J., Fritz J. H., Rojas A. M., Schwarzenbacher R., The Nod-Like Receptor (NLR) family: a tale of similarities and differences. PLoS ONE 2008 3 4 2-s2.0-44349171085 10.1371/journal.pone.0002119 e2119
18. Shaw P. J., Lamkanfi M., Kanneganti T., NOD-like receptor (NLR) signaling beyond the inflammasome. European Journal of Immunology 2010 40 3 624 627 2-s2.0-77749285687 10.1002/eji.200940211
19. Kufer T. A., Signal transduction pathways used by NLR-type innate immune receptors. Molecular BioSystems 2008 4 5 380 386 2-s2.0-42149148610 10.1039/b718948f
20. Duewell P., Kono H., Rayner K. J., Sirois C. M., Vladimer G., Bauernfeind F. G., Abela G. S., Franchi L., Nũez G., Schnurr M., Espevik T., Lien E., Fitzgerald K. A., Rock K. L., Moore K. J., Wright S. D., Hornung V., Latz E., NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010 464 7293 1357 1361 2-s2.0-77951800951 10.1038/nature08938
21. Eisenbarth S. C., Colegio O. R., O'Connor W. Jr., Sutterwala F. S., Flavell R. A., Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008 453 7198 1122 1126 2-s2.0-45749111446 10.1038/nature06939
22. Martinon F., Pétrilli V., Mayor A., Tardivel A., Tschopp J., Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006 440 7081 237 241 2-s2.0-32944468985 10.1038/nature04516
23. Masters S. L., O'Neill L. A. J., Disease-associated amyloid and misfolded protein aggregates activate the inflammasome. Trends in Molecular Medicine 2011 17 5 276 282 2-s2.0-79955156438 10.1016/j.molmed.2011.01.005
24. Griffin W. S., Sheng J. G., Royston M. C., Gentleman S. M., McKenzie J. E., Graham D. I., Roberts G. W., Mrak R. E., Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathology 1998 8 1 65 72 2-s2.0-0031983986
25. Ogura H., Murakami M., Okuyama Y., Tsuruoka M., Kitabayashi C., Kanamoto M., Nishihara M., Iwakura Y., Hirano T., Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction. Immunity 2008 29 4 628 636 2-s2.0-55049118394 10.1016/j.immuni.2008.07.018
26. Hanada T., Yoshimura A., Regulation of cytokine signaling and inflammation. Cytokine and Growth Factor Reviews 2002 13 4-5 413 421 2-s2.0-0036694663 10.1016/S1359-6101(02)00026-6
27. Zheng Z., White C., Lee J., Peterson T. S., Bush A. I., Sun G. Y., Weisman G. A., Petris M. J., Altered microglial copper homeostasis in a mouse model of Alzheimer's disease. Journal of Neurochemistry 2010 114 6 1630 1638 2-s2.0-77956309944 10.1111/j.1471-4159.2010.06888.x
28. Lee K. H., Yun S., Nam K. N., Gho Y. S., Lee E. H., Activation of microglial cells by ceruloplasmin. Brain Research 2007 1171 1 1 8 2-s2.0-34548623301 10.1016/j.brainres.2007.07.053
29. Becaria A., Lahiri D. K., Bondy S. C., Chen D., Hamadeh A., Li H., Taylor R., Campbell A., Aluminum and copper in drinking water enhance inflammatory or oxidative events specifically in the brain. Journal of Neuroimmunology 2006 176 1-2 16 23 2-s2.0-33746034583 10.1016/j.jneuroim.2006.03.025
30. Lu J., Wu D., Zheng Y., Sun D., Hu B., Shan Q., Zhang Z., Fan S., Trace amounts of copper exacerbate beta amyloid-induced neurotoxicity in the cholesterol-fed mice through TNF-mediated inflammatory pathway. Brain, Behavior, and Immunity 2009 23 2 193 203 2-s2.0-58549116872 10.1016/j.bbi.2008.09.003
31. Rossi-George A., Guo C.-J., Oakes B. L., Gow A. J., Copper modulates the phenotypic response of activated BV2 microglia through the release of nitric oxide. Nitric Oxide 2012 27 4 201 209 10.1016/j.niox.2012.07.002
32. Maynard C. J., Cappai R., Volitakis I., Cherny R. A., White A. R., Beyreuther K., Masters C. L., Bush A. I., Li Q., Overexpression of Alzheimer's disease amyloid- β opposes the age-dependent elevations of brain copper and iron. Journal of Biological Chemistry 2002 277 47 44670 44676 2-s2.0-0037160028 10.1074/jbc.M204379200
33. Bellingham S. A., Lahiri D. K., Maloney B., La Fontaine S., Multhaup G., Camakaris J., Copper depletion down-regulates expression of the Alzheimer's disease amyloid- β precursor protein gene. Journal of Biological Chemistry 2004 279 19 20378 20386 2-s2.0-2442586535 10.1074/jbc.M400805200
34. Bailey S. L., Carpentier P. A., McMahon E. J., Begolka W. S., Miller S. D., Innate and adaptive immune responses of the central nervous system. Critical Reviews Immunology 2006 26 2 149 188 10.1615/CritRevImmunol.v26.i2.40
35. Bajramovic J. J., Regulation of innate immune responses in the central nervous system. CNS & Neurological Disorders Drug Targets 2011 10 1 4 24 2-s2.0-79960973055
36. Weller R. O., Djuanda E., Yow H., Carare R. O., Lymphatic drainage of the brain and the pathophysiology of neurological disease. Acta Neuropathologica 2009 117 1 1 14 2-s2.0-57049154546 10.1007/s00401-008-0457-0
37. Xiao B.-G., Link H., Immune regulation within the central nervous system. Journal of the Neurological Sciences 1998 157 1 1 12 2-s2.0-0032522507 10.1016/S0022-510X(98)00049-5
38. Kivisäkk P., Mahad D. J., Callahan M. K., Trebst C., Tucky B., Wei T., Wu L., Baekkevold E. S., Lassmann H., Staugaitis S. M., Campbell J. J., Ransohoff R. M., Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proceedings of the National Academy of Sciences of the United States of America 2003 100 14 8389 8394 2-s2.0-0037816192 10.1073/pnas.1433000100
39. Kida S., Weller R. O., Zhang E.-T., Phillips M. J., Iannotti F., Anatomical pathways for lymphatic drainage of the brain and their pathological significance. Neuropathology and Applied Neurobiology 1995 21 3 181 184 2-s2.0-0028997951
40. Glass C. K., Saijo K., Winner B., Marchetto M. C., Gage F. H., Mechanisms underlying inflammation in neurodegeneration. Cell 2010 140 6 918 934 2-s2.0-77950363010 10.1016/j.cell.2010.02.016
41. Streit W. J., Mrak R. E., Griffin W. S. T., Microglia and neuroinflammation: a pathological perspective. Journal of Neuroinflammation 2004 1 1 14 2-s2.0-7744224673 10.1186/1742-2094-1-14
42. Alexianu M. E., Kozovska M., Appel S. H., Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 2001 57 7 1282 1289 2-s2.0-0035833937
43. Autti T., Raininko R., Santavuori P., Vanhanen S. L., Poutanen V. P., Haltia M., MRI of neuronal ceroid lipofuscinosis. II. Postmortem MRI and histopathological study of the brain in 16 cases of neuronal ceroid lipofuscinosis of juvenile or late infantile type. Neuroradiology 1997 39 5 371 377 2-s2.0-0030962978 10.1007/s002340050427
44. Bamberger M. E., Harris M. E., McDonald D. R., Husemann J., Landreth G. E., A cell surface receptor complex for fibrillar β -amyloid mediates microglial activation. Journal of Neuroscience 2003 23 7 2665 2674 2-s2.0-0037387147
45. Damier P., Hirsch E. C., Zhang P., Agid Y., Javoy-Agid F., Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience 1993 52 1 1 6 2-s2.0-0027434596 10.1016/0306-4522(93)90175-F
46. Ingelsson M., Fukumoto H., Newell K. L., Growdon J. H., Hedley-Whyte E. T., Frosch M. P., Albert M. S., Hyman B. T., Irizarry M. C., Early A β accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004 62 6 925 931 2-s2.0-1842510004
47. Kamo H., Haebara H., Akiguchi I., A distinctive distribution of reactive astroglia in the precentral cortex in amyotrophic lateral sclerosis. Acta Neuropathologica 1987 74 1 33 38 2-s2.0-0023258156
48. Thellung S., Florio T., Corsaro A., Arena S., Merlino M., Salmona M., Tagliavini F., Bugiani O., Forloni G., Schettini G., Intracellular mechanisms mediating the neuronal death and astrogliosis induced by the prion protein fragment 106-126. International Journal of Developmental Neuroscience 2000 18 4-5 481 492 2-s2.0-0034237389 10.1016/S0736-5748(00)00005-8
49. Dickson D. W., Farlo J., Davies P., Crystal H., Fuld P., Yen S.-H. C., Alzheimer's disease. A double-labeling immunohistochemical study of senile plaques. American Journal of Pathology 1988 132 1 86 101 2-s2.0-0023809230
50. McGeer P. L., Akiyama H., Itagaki S., McGeer E. G., Immune system response in Alzheimer's disease. Canadian Journal of Neurological Sciences 1989 16 supplement 4 516 527 2-s2.0-0024442083
51. Rozemuller J. M., Eikelenboom P., Pals S. T., Stam F. C., Microglial cells around amyloid plaques in Alzheimer's disease express leucocyte adhesion molecules of the LFA-1 family. Neuroscience Letters 1989 101 3 288 292 2-s2.0-0024394987
52. Jomova K., Vondrakova D., Lawson M., Valko M., Metals, oxidative stress and neurodegenerative disorders. Molecular and Cellular Biochemistry 2010 345 1-2 91 104 2-s2.0-78449282609 10.1007/s11010-010-0563-x
53. Valko M., Morris H., Cronin M. T. D., Metals, toxicity and oxidative stress. Current Medicinal Chemistry 2005 12 10 1161 1208 2-s2.0-18544371009 10.2174/0929867053764635
54. Akama K. T., Albanese C., Pestell R. G., Van Eldik L. J., Amyloid β -peptide stimulates nitric oxide production in astrocytes through an NF b-dependent mechanism. Proceedings of the National Academy of Sciences of the United States of America 1998 95 10 5795 5800 2-s2.0-0032510692 10.1073/pnas.95.10.5795
55. Flanders K. C., Lippa C. F., Smith T. W., Pollen D. A., Sporn M. B., Altered expression of transforming growth factor- β in Alzheimer's disease. Neurology 1995 45 8 1561 1569 2-s2.0-0029046504
56. Grammas P., Ovase R., Inflammatory factors are elevated in brain microvessels in Alzheimer's disease. Neurobiology of Aging 2001 22 6 837 842 2-s2.0-0035690770 10.1016/S0197-4580(01)00276-7
57. Lue L. F., Rydel R., Brigham E. F., Yang L., Hampel H., Murphy G. M. Jr., Brachova L., Yan S., Walker D. G., Shen Y., Rogers J., Inflammatory repertoire of Alzheimer's disease and nondemented elderly microglia in vitro. Glia 2001 35 1 72 79 2-s2.0-0034948192 10.1002/glia.1072
58. Akiyama H., Streit W., Strohmeyer R., Inflammation and Alzheimer's disease. Neurobiology of Aging 2000 21 3 383 421 10.1016/S0197-4580(00)00124-X
59. Salminen A., Ojala J., Kauppinen A., Kaarniranta K., Suuronen T., Inflammation in Alzheimer's disease: amyloid- β oligomers trigger innate immunity defence via pattern recognition receptors. Progress in Neurobiology 2009 87 3 181 194 2-s2.0-61349088546 10.1016/j.pneurobio.2009.01.001
60. Mocchegiani E., Costarelli L., Giacconi R., Piacenza F., Basso A., Malavolta M., Micronutrient (Zn, Cu, Fe)-gene interactions in ageing and inflammatory age-related diseases: implications for treatments. Ageing Research Reviews 2012 11 2 297 319 2-s2.0-84857020239 10.1016/j.arr.2012.01.004
61. Madaric A., Ginter E., Kadrabova J., Serum copper, zinc and copper/zinc ratio in males: influence of aging. Physiological Research 1994 43 2 107 111 2-s2.0-0027974414
62. Lawson L. J., Perry V. H., Dri P., Gordon S., Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 1990 39 1 151 170 2-s2.0-0025220976 10.1016/0306-4522(90)90229-W
63. Mittelbronn M., Dietz K., Schluesener H. J., Meyermann R., Local distribution of microglia in the normal adult human central nervous system differs by up to one order of magnitude. Acta Neuropathologica 2001 101 3 249 255 2-s2.0-0035105538
64. Olah M., Amor S., Brouwer N., Vinet J., Eggen B., Biber K., Boddeke H. W. G. M., Identification of a microglia phenotype supportive of remyelination. Glia 2012 60 2 306 321 2-s2.0-83055184202 10.1002/glia.21266
65. DeWitt D. A., Perry G., Cohen M., Doller C., Silver J., Astrocytes regulate microglial phagocytosis of senile plaque cores of Alzheimer's disease. Experimental Neurology 1998 149 2 329 340 2-s2.0-18144453796 10.1006/exnr.1997.6738
66. Shaffer L. M., Dority M. D., Gupta-Bansal R., Frederickson R. C. A., Younkin S. G., Brunden K. R., Amyloid β precursor protein (A β) removal by neuroglial cells in culture. Neurobiology of Aging 1995 16 5 737 745 2-s2.0-0028849635 10.1016/0197-4580(95)00055-J
67. Meda L., Baron P., Prat E., Scarpini E., Scarlato G., Cassatella M. A., Rossi F., Proinflammatory profile of cytokine production by human monocytes and murine microglia stimulated with β -amyloid[25-35]. Journal of Neuroimmunology 1999 93 1-2 45 52 2-s2.0-0032891880 10.1016/S0165-5728(98)00188- X
68. Remarque E. J., Bollen E. L. E. M., Weverling-Rijnsburger A. W. E., Laterveer J. C., Blauw G. J., Westendorp R. G. J., Patients with Alzheimer's disease display a pro-inflammatory phenotype. Experimental Gerontology 2001 36 1 171 176 2-s2.0-0035201651 10.1016/S0531-5565(00)00176-5
69. Colton C. A., Gilbert D. L., Production of superoxide anions by a CNS macrophage, the microglia. FEBS Letters 1987 223 2 284 288 2-s2.0-0023642584
70. Colton C. A., Heterogeneity of microglial activation in the innate immune response in the brain. Journal of Neuroimmune Pharmacology 2009 4 4 399 418 2-s2.0-70449526190 10.1007/s11481-009-9164-4
71. Jimenez S., Baglietto-Vargas D., Caballero C., Moreno-Gonzalez I., Torres M., Sanchez-Varo R., Ruano D., Vizuete M., Gutierrez A., Vitorica J., Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic. Journal of Neuroscience 2008 28 45 11650 11661 2-s2.0-58149216131 10.1523/JNEUROSCI.3024-08.2008
72. Kimelberg H., Primary astrocyte cultures-a key to astrocyte function. Cellular and Molecular Neurobiology 1983 3 1 1 16 2-s2.0-0020728439 10.1007/BF00734994
73. Farina C., Aloisi F., Meinl E., Astrocytes are active players in cerebral innate immunity. Trends in Immunology 2007 28 3 138 145 2-s2.0-33847099936 10.1016/j.it.2007.01.005
74. Mrak R. E., Sheng J. G., Griffin W. S. T., Correlation of astrocytic S100 β expression with dystrophie neurites in amyloid plaques of Alzheimer's disease. Journal of Neuropathology and Experimental Neurology 1996 55 3 273 279 2-s2.0-0029670066
75. Pike C. J., Cummings B. J., Monzavi R., Cotman C. W., β -Amyloid-induced changes in cultured astrocytes parallel reactive astrocytosis associated with senile plaques in Alzeimer's disease. Neuroscience 1994 63 2 517 531 2-s2.0-0028172346 10.1016/0306-4522(94)90547-9
76. Wyss-Coray T., Loike J. D., Brionne T. C., Lu E., Anankov R., Yan F., Silverstein S. C., Husemann J., Adult mouse astrocytes degrade amyloid- β in vitro and in situ. Nature Medicine 2003 9 4 453 457 2-s2.0-0037394788 10.1038/nm838
77. Del Bo R., Angeretti N., Lucca E., De Simoni M. G., Forloni G., Reciprocal control of inflammatory cytokines, IL-1 and IL-6, β -amyloid production in cultures. Neuroscience Letters 1995 188 1 70 74 2-s2.0-0028946146 10.1016/0304-3940(95)11384-9
78. Johnstone M., Gearing A. J. H., Miller K. M., A central role for astrocytes in the inflammatory response to β-amyloid; chemokines, cytokines and reactive oxygen species are produced. Journal of Neuroimmunology 1999 93 1-2 182 193 2-s2.0-0032891616 10.1016/S0165-5728(98)00226-4
79. Forloni G., Mangiarotti F., Angeretti N., Lucca E., De Simoni M. G., β -amyloid fragment potentiates IL-6 and TNF- α secretion by LPS in astrocytes but not in microglia. Cytokine 1997 9 10 759 762 2-s2.0-0031258670 10.1006/cyto.1997.0232
80. Hu J., Akama K. T., Krafft G. A., Chromy B. A., Van Eldik L. J., Amyloid- β peptide activates cultured astrocytes: morphological alterations, cytokine induction and nitric oxide release. Brain Research 1998 785 2 195 206 2-s2.0-0032473596 10.1016/S0006-8993(97)01318-8
81. Haass C., Selkoe D. J., Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β -peptide. Nature Reviews Molecular Cell Biology 2007 8 2 101 112 2-s2.0-33847662852 10.1038/nrm2101
82. Walsh D. M., Selkoe D. J., A β oligomers-a decade of discovery. Journal of Neurochemistry 2007 101 5 1172 1184 2-s2.0-34248190279 10.1111/j.1471-4159.2006.04426.x
83. Harris M. E., Hensley K., Butterfield D. A., Leedle R. A., Carney J. M., Direct evidence of oxidative injury produced by the Alzheimer's β -amyloid peptide (1-40) in cultured hippocampal neurons. Experimental Neurology 1995 131 2 193 202 2-s2.0-0028908516
84. Walter S., Letiembre M., Liu Y., Heine H., Penke B., Hao W., Bode B., Manietta N., Walter J., Schulz-Schüffer W., Faßbender K., Role of the toll-like receptor 4 in neuroinflammation in Alzheimer's disease. Cellular Physiology and Biochemistry 2007 20 6 947 956 2-s2.0-35848963223 10.1159/000110455
85. Jana M., Palencia C. A., Pahan K., Fibrillar amyloid- β peptides activate microglia via TLR2: implications for Alzheimer's disease. Journal of Immunology 2008 181 10 7254 7262 2-s2.0-58149181978
86. Chaney M. O., Stine W. B., Kokjohn T. A., Kuo Y., Esh C., Rahman A., Luehrs D. C., Schmidt A. M., Stern D., Yan S. D., Roher A. E., RAGE and amyloid beta interactions: atomic force microscopy and molecular modeling. Biochimica et Biophysica Acta 2005 1741 1-2 199 205 2-s2.0-20444462454 10.1016/j.bbadis.2005. 03.014
87. Lue L. F., Walker D. G., Brachova L., Beach T. G., Rogers J., Schmidt A. M., Stern D. M., Yan S. D., Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Experimental Neurology 2001 171 1 29 45 2-s2.0-0034840664 10.1006/exnr.2001.7732
88. Salminen A., Ojala J., Suuronen T., Kaarniranta K., Kauppinen A., Amyloid- β oligomers set fire to inflammasomes and induce Alzheimer's pathology: Alzheimer Review Series. Journal of Cellular and Molecular Medicine 2008 12 6 2255 2262 2-s2.0-57149123424 10.1111/j.1582-4934.2008.00496.x
89. Jack C. S., Arbour N., Manusow J., Montgrain V., Blain M., McCrea E., Shapiro A., Antel J. P., TLR signaling tailors innate immune responses in human microglia and astrocytes. Journal of Immunology 2005 175 7 4320 4330 2-s2.0-25444498280
90. Kielian T., Toll-like receptors in central nervous system glial inflammation and homeostasis. Journal of Neuroscience Research 2006 83 5 711 730 2-s2.0-33645322938 10.1002/jnr.20767
91. Song M., Jin J., Lim J., Kou J., Pattanayak A., Rehman J. A., Kim H., Tahara K., Lalonde R., Fukuchi K., TLR4 mutation reduces microglial activation, increases A β deposits and exacerbates cognitive deficits in a mouse model of Alzheimer's disease. Journal of Neuroinflammation 2011 8 92 1 14 2-s2.0-79961134149 10.1186/1742-2094-8-92
92. Richard K. L., Filali M., Préfontaine P., Rivest S., Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid β 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. Journal of Neuroscience 2008 28 22 5784 5793 2-s2.0-45949106077 10.1523/JNEUROSCI.1146-08.2008
93. Tahara K., Kim H., Jin J., Maxwell J. A., Li L., Fukuchi K., Role of toll-like receptor signalling in A β uptake and clearance. Brain 2006 129 11 3006 3019 2-s2.0-33750576993 10.1093/brain/awl249
94. Stewart C. R., Stuart L. M., Wilkinson K., Van Gils J. M., Deng J., Halle A., Rayner K. J., Boyer L., Zhong R., Frazier W. A., Lacy-Hulbert A., Khoury J. E., Golenbock D. T., Moore K. J., CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nature Immunology 2010 11 2 155 161 2-s2.0-75649087741 10.1038/ni.1836
95. Zhang W., Wang L., Yu J., Chi Z., Tan L., Increased expressions of TLR2 and TLR4 on peripheral blood mononuclear cells from patients with Alzheimer's disease. Journal of the Neurological Sciences 2012 315 1-2 67 71 2-s2.0-84858001196 10.1016/j.jns.2011.11.032
96. Bierhaus A., Stern D. M., Nawroth P. P., RAGE in inflammation: a new therapeutic target? Current Opinion in Investigational Drugs 2006 7 11 985 991 2-s2.0-33751026851
97. Deane R., Wu Z., Zlokovic B. V., RAGE (Yin) versus LRP (Yang) balance regulates Alzheimer amyloid β -peptide clearance through transport across the blood-brain barrier. Stroke 2004 35 11, supplement 1 2628 2631 2-s2.0-7644225312 10.1161/01.STR.0000143452.85382.d1
98. Donahue J. E., Flaherty S. L., Johanson C. E., Duncan J. A. III, Silverberg G. D., Miller M. C., Tavares R., Yang W., Wu Q., Sabo E., Hovanesian V., Stopa E. G., RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathologica 2006 112 4 405 415 2-s2.0-33749157416 10.1007/s00401-006- 0115-3
99. Arancio O., Zhang H. P., Chen X., Lin C., Trinchese F., Puzzo D., Liu S., Hegde A., Yan S. F., Stern A., Luddy J. S., Lue L., Walker D. G., Roher A., Buttini M., Mucke L., Li W., Schmidt A. M., Kindy M., Hyslop P. A., Stern D. M., Yan S. S. D., RAGE potentiates A β -induced perturbation of neuronal function in transgenic mice. EMBO Journal 2004 23 20 4096 4105 2-s2.0-8144223671 10.1038/sj.emboj.7600415
100. Zuliani G., Ranzini M., Guerra G., Rossi L., Munari M. R., Zurlo A., Volpato S., Atti A. R., Blè A., Fellin R., Plasma cytokines profile in older subjects with late onset Alzheimer's disease or vascular dementia. Journal of Psychiatric Research 2007 41 8 686 693 2-s2.0-33947709910 10.1016/j.jpsychires.2006.02.008
101. Ojala J., Alafuzoff I., Herukka S., van Groen T., Tanila H., Pirttilä T., Expression of interleukin-18 is increased in the brains of Alzheimer's disease patients. Neurobiology of Aging 2009 30 2 198 209 2-s2.0-57849144282 10.1016/j.neurobiolaging.2007.06.006
102. Apelt J., Schliebs R., β -amyloid-induced glial expression of both pro- and anti-inflammatory cytokines in cerebral cortex of aged transgenic Tg2576 mice with Alzheimer plaque pathology. Brain Research 2001 894 1 21 30 2-s2.0-0035831189 10.1016/S0006-8993(00)03176-0
103. Pétrilli V., Dostert C., Muruve D. A., Tschopp J., The inflammasome: a danger sensing complex triggering innate immunity. Current Opinion in Immunology 2007 19 6 615 622 2-s2.0-36849045915 10.1016/j.coi.2007. 09.002
104. Furukawa K., Barger S. W., Blalock E. M., Mattson M. P., Activation of K+ channels and suppression of neuronal activity by secreted β -amyloid-precursor protein. Nature 1996 379 6560 74 78 2-s2.0-0030068094 10.1038/379074a0
105. Yu S. P., Farhangrazi Z. S., Ying H. S., Yeh C., Choi D. W., Enhancement of outward potassium current may participate in β -amyloid peptide-induced cortical neuronal death. Neurobiology of Disease 1998 5 2 81 88 2-s2.0-0004491134 10.1006/nbdi.1998.0186
106. Halle A., Hornung V., Petzold G. C., Stewart C. R., Monks B. G., Reinheckel T., Fitzgerald K. A., Latz E., Moore K. J., Golenbock D. T., The NALP3 inflammasome is involved in the innate immune response to amyloid- β Nature Immunology 2008 9 8 857 865 2-s2.0-47849085872 10.1038/ni.1636
107. Bush A. I., Metals and neuroscience. Current Opinion in Chemical Biology 2000 4 2 184 191 10.1016/S1367-5931(99)00073-3
108. Linder M. C., Hazegh-Azam M., Copper biochemistry and molecular biology. American Journal of Clinical Nutrition 1996 63 supplement 5 797S 811S 2-s2.0-0029883795
109. Bayer T. A., Schäfer S., Simons A., Kemmling A., Kamer T., Tepest R., Eckert A., Schüssel K., Eikenberg O., Sturchler-Pierrat C., Abramowski D., Staufenbiel M., Multhaup G., Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid A β production in APP23 transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 2003 100 2 14187 14192 2-s2.0-10744226316 10.1073/pnas.2332818100
110. Lovell M. A., Robertson J. D., Teesdale W. J., Campbell J. L., Markesbery W. R., Copper, iron and zinc in Alzheimer's disease senile plaques. Journal of the Neurological Sciences 1998 158 1 47 52 2-s2.0-0032507975 10.1016/S0022-510X(98)00092-6
111. Schrag M., Crofton A., Zabel M., Jiffry A., Kirsch D., Dickson A., Mao X. W., Vinters H. V., Domaille D. W., Chang C. J., Kirsch W., Effect of cerebral amyloid angiopathy on brain iron, copper, and zinc in alzheimer's disease. Journal of Alzheimer's Disease 2011 24 1 137 149 2-s2.0-79955650486 10.3233/JAD-2010-101503
112. Noy D., Solomonov I., Sinkevich O., Arad T., Kjaer K., Sagi I., Zinc-amyloid β interactions on a millisecond time-scale stabilize non-fibrillar Alzheimer-related species. Journal of the American Chemical Society 2008 130 4 1376 1383 2-s2.0-38649112930 10.1021/ja076282l
113. Smith M. A., Harris P. L. R., Sayre L. M., Perry G., Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proceedings of the National Academy of Sciences of the United States of America 1997 94 18 9866 9868 2-s2.0-0030885482 10.1073/pnas.94.18.9866
114. Atwood C. S., Moir R. D., Huang X., Scarpa R. C., Bacarra N. M. E., Romano D. M., Hartshorn M. A., Tanzi R. E., Bush A. I., Dramatic aggregation of alzheimer by Cu(II) is induced by conditions representing physiological acidosis. Journal of Biological Chemistry 1998 273 21 12817 12826 2-s2.0-0032557425 10.1074/jbc.273.21.12817
115. Atwood C. S., Scarpa R. C., Huang X., Moir R. D., Jones W. D., Fairlie D. P., Tanzi R. E., Bush A. I., Characterization of copper interactions with Alzheimer amyloid β peptides: identification of an attomolar-affinity copper binding site on amyloid β 1-42. Journal of Neurochemistry 2000 75 3 1219 1233 2-s2.0-0033844944 10.1046/j.1471-4159.2000.0751219.x
116. Curtain C. C., Ali F., Volitakis I., Cherny R. A., Norton R. S., Beyreuther K., Barrow C. J., Masters C. L., Bush A. I., Barnham K. J., Alzheimer's disease amyloid- β binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. Journal of Biological Chemistry 2001 276 23 20466 20473 2-s2.0-0035827681 10.1074/jbc.M100175200
117. Huang X., Atwood C. S., Moir R. D., Hartshorn M. A., Tanzi R. E., Bush A. I., Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's A β peptides. Journal of Biological Inorganic Chemistry 2004 9 8 954 960 2-s2.0-12144282992 10.1007/s00775-004-0602-8
118. Barnham K. J., Haeffner F., Ciccotosto G. D., Curtain C. C., Tew D., Mavros C., Beyreuther K., Carrington D., Masters C. L., Cherny R. A., Cappai R., Bush A. I., Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease β -amyloid. FASEB Journal 2004 18 12 1427 1429 2-s2.0-9444284334 10.1096/fj.04-1890fje
119. White C., Lee J., Kambe T., Fritsche K., Petris M. J., A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. Journal of Biological Chemistry 2009 284 49 33949 33956 2-s2.0-71749115454 10.1074/jbc.M109.070201
120. Multhaup G., Schlicksupp A., Hesse L., Beher D., Ruppert T., Masters C. L., Beyreuther K., The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 1996 271 5254 1406 1409 2-s2.0-0029935396
121. Schmalz G., Schuster U., Schweikl H., Influence of metals on IL-6 release in vitro. Biomaterials 1998 19 18 1689 1694 2-s2.0-0032170249 10.1016/S0142-9612(98)00075-1
122. Suska F., Esposito M., Gretzer C., Källtorp M., Tengvall P., Thomsen P., IL-1 α IL-1 β and TNF- α secretion during in vivo/ex vivo cellular interactions with titanium and copper. Biomaterials 2003 24 3 461 468 2-s2.0-0037290141 10.1016/S0142-9612(02)00359-9
123. Suska F., Gretzer C., Esposito M., Emanuelsson L., Wennerberg A., Tengvall P., Thomsen P., In vivo cytokine secretion and NF- B activation around titanium and copper implants. Biomaterials 2005 26 5 519 527 2-s2.0-3242792640 10.1016/j.biomaterials.2004.02.066
124. Kennedy T. P., Ghio A. J., Reed W., Samet J., Zagorski J., Quay J., Carter J., Dailey L., Hoidal J. R., Devlin R. B., Copper-dependent inflammation and nuclear factor- b activation by particulate air pollution. American Journal of Respiratory Cell and Molecular Biology 1998 19 3 366 378 2-s2.0-0032161565
125. Rice T. M., Clarke R. W., Godleski J. J., Al-Mutairi E., Jiang N., Hauser R., Paulauskis J. D., Differential ability of transition metals to induce pulmonary inflammation. Toxicology and Applied Pharmacology 2001 177 1 46 53 2-s2.0-0035891487 10.1006/taap.2001.9287
126. Bar-Or D., Thomas G. W., Yukl R. L., Rael L. T., Shimonkevitz R. P., Curtis C. G., Winkler J. V., Copper stimulates the synthesis and release of interleukin-8 in human endothelial cells: a possible early role in systemic inflammatory responses. Shock 2003 20 2 154 158 2-s2.0-1542541530
127. Hung Y. H., Bush A. I., La Fontaine S., Links between copper and cholesterol in Alzheimer's disease. Frontiers in Physiology 2013 4 111 1 18
128. Terwel D., Löschmann Y., Schmidt H. H.-J., Schöler H. R., Cantz T., Heneka M. T., Neuroinflammatory and behavioural changes in the Atp7B mutant mouse model of Wilson's disease. Journal of Neurochemistry 2011 118 1 105 112 2-s2.0-79958856274 10.1111/j.1471-4159.2011.07278.x
129. Liu H. P., Lin W. Y., Wang W. F., Genetic variability in copper-transporting P-type adenosine triphosphatase (ATP7B) is associated with Alzheimer's disease in a Chinese population. Journal of Biological Regulators and Homeostatic Agents 2013 27 2 319 327
130. Squitti R., Polimanti R., Copper hypothesis in the missing hereditability of sporadic alzheimer's disease: ATP7B gene as potential harbor of rare variants. Journal of Alzheimer's Disease 2012 29 3 493 501 2-s2.0-84859395496 10.3233/JAD-2011-111991
131. Solerte S. B., Cravello L., Ferrari E., Fioravanti M., Overproduction of IFN- γ and TNF- α from natural killer (NK) cells is associated with abnormal NK reactivity and cognitive derangement in Alzheimer's disease. Annals of the New York Academy of Sciences 2000 917 331 340 2-s2.0-0033664955
132. Baron R., Nemirovsky A., Harpaz I., Cohen H., Owens T., Monsonego A.,
133. Mastrangelo M. A., Sudol K. L., Narrow W. C., Bowers W. J., Interferon- γ differentially affects Alzheimer's disease pathologies and induces neurogenesis in triple transgenic-AD mice. American Journal of Pathology 2009 175 5 2076 2088 2-s2.0-73649129558 10.2353/ajpath.2009.090059
134. Connor J. R., Tucker P., Johnson M., Snyder B., Ceruloplasmin levels in the human superior temporal gyrus in aging and Alzheimer's disease. Neuroscience Letters 1993 159 1-2 88 90 2-s2.0-0027327899
135. Loeffler D. A., LeWitt P. A., Juneau P. L., Sima A. A. F., Nguyen H.-U., DeMaggio A. J., Brickman C. M., Brewer G. J., Dick R. D., Troyer M. D., Kanaley L., Increased regional brain concentrations of ceruloplasmin in neurodegenerative disorders. Brain Research 1996 738 2 265 274 2-s2.0-0030569306 10.1016/S0006-8993(96)00782-2
136. Osaki S., Johnson D. A., Mobilization of liver iron by ferroxidase (ceruloplasmin). Journal of Biological Chemistry 1969 244 20 5757 5758 2-s2.0-0014691028
137. Nemeth E., Tuttle M. S., Powelson J., Vaughn M. D., Donovan A., Ward D. M., Ganz T., Kaplan J., Hepcidin regulates cellular iron efflux by binding to ferroportin and inducing its internalization. Science 2004 306 5704 2090 2093 2-s2.0-10844258104 10.1126/science.1104742
138. Venti A., Giordano T., Eder P., Bush A. I., Lahiri D. K., Greig N. H., Rogers J. T., Integrated role of desferrioxamine and phenserine targeted to an iron-responsive element in the APP-mRNA 5′-untranslated region. Annals of the New York Academy of Sciences 2004 1035 34 48 2-s2.0-14944344156 10.1196/annals.1332.003
139. Myhre O., Utkilen H., Duale N., Brunborg G., Hofer T., Metal dyshomeostasis and inflammation in Alzheimer's and Parkinson's diseases: possible impact of environmental exposures. Oxidative Medicine and Cellular Longevity 2013 2013 19 726954 10.1155/2013/726954
140. Acevedo K. M., Hung Y. H., Dalziel A. H., Copper promotes the trafficking of the amyloid precursor protein. Journal of Biological Chemistry 2011 286 10 8252 8262 10.1074/jbc.M110.128512
141. Zucconi G. G., Cipriani S., Scattoni R., Balgkouranidou I., Hawkins D. P., Ragnarsdottir K. V., Copper deficiency elicits glial and neuronal response typical of neurodegenerative disorders. Neuropathology and Applied Neurobiology 2007 33 2 212 225 2-s2.0-33847759150 10.1111/j.1365-2990.2006.00793.x
142. Liang W. S., Dunckley T., Beach T. G., Grover A., Mastroeni D., Walker D. G., Caselli R. J., Kukull W. A., McKeel D., Morris J. C., Hulette C., Schmechel D., Alexander G. E., Reiman E. M., Rogers J., Stephan D. A., Gene expression profiles in anatomically and functionally distinct regions of the normal aged human brain. Physiological Genomics 2007 28 3 311 322 2-s2.0-34247202571 10.1152/physiolgenomics.00208.2006
143. Liang W. S., Reiman E. M., Valla J., Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proceedings of the National Academy of Sciences of the United States of America 2008 105 11 4441 4446 10.1073/pnas.0709259105
144. Agullo L., Garcia A., Hidalgo J., Metallothionein-I+II induction by zinc and copper in primary cultures of rat microglia. Neurochemistry International 1998 33 3 237 242 2-s2.0-0032167397 10.1016/S0197-0186(98)00022-9
145. Crouch P.J., Hung L.W., Adlard P.A. Increasing Cu bioavailability inhibits A β oligomers and tau phosphorylation, Proceedings of the National Academy of Sciences 2009 106 2 381-386 10.1073/pnas.0809057106