Altered microglial copper homeostasis in a mouse model of Alzheimer's disease

Journal of Neurochemistry

Volumn 114, Issue 6, 2010, Pages 1630-1638

  Zheng, Zhiqiang ^a   White, Carine ^a   Lee, Jaekwon ^b   Peterson, Troy S ^a   Bush, Ashley I ^c   Sun, Grace Y ^a,d   Weisman, Gary A ^a,d   Petris, Michael J ^a,d  

^a UNIVERSITY OF MISSOURI   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d University of Missouri   (United States)

Author keywords

Alzheimer's disease; ATP7A; copper homeostasis; inflammation; microglia

Indexed keywords

AMYLOID; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; GAMMA INTERFERON; INTERLEUKIN 1BETA; MENKES PROTEIN; TUMOR NECROSIS FACTOR ALPHA; ADENOSINE TRIPHOSPHATASE; ATP7A PROTEIN, MOUSE; CATION TRANSPORT PROTEIN; COPPER; CTR1 PROTEIN, MOUSE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINE; CONTROLLED STUDY; CYTOPLASM VESICLE; DISEASE ASSOCIATION; GOLGI COMPLEX; HEMOSTASIS; MICROGLIA; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; AMYLOID PLAQUE; ANIMAL; BIOSYNTHESIS; BRAIN; HOMEOSTASIS; METABOLISM; PATHOLOGY; PROTEIN TRANSPORT; TRANSGENIC MOUSE;

ADENOSINE TRIPHOSPHATASES; ALZHEIMER DISEASE; ANIMALS; BRAIN; CATION TRANSPORT PROTEINS; CELL LINE; COPPER; CYTOPLASMIC VESICLES; HOMEOSTASIS; INTERFERON-GAMMA; MICE; MICE, TRANSGENIC; MICROGLIA; PLAQUE, AMYLOID; PROTEIN TRANSPORT;

EID: 77956309944     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06888.x     Document Type: Article

References (61)

1. Abbas N., Bednar I., Mix E., Marie S., Paterson D., Ljungberg A., Morris C., Winblad B., Nordberg A. Zhu J. (2002) Up-regulation of the inflammatory cytokines IFN-gamma and IL-12 and down-regulation of IL-4 in cerebral cortex regions of APP(SWE) transgenic mice. J. Neuroimmunol. 126, 50 57.
2. Adlard P. A., Cherny R. A., Finkelstein D. I. et al. (2008) Rapid restoration of cognition in Alzheimer's transgenic mice with 8-hydroxy quinoline analogs is associated with decreased interstitial Abeta. Neuron 59, 43 55.
3. Atwood C. S., Moir R. D., Huang X., Scarpa R. C., Bacarra N. M., Romano D. M., Hartshorn M. A., Tanzi R. E. Bush A. I. (1998) Dramatic aggregation of Alzheimer abeta by Cu(II) is induced by conditions representing physiological acidosis. J. Biol. Chem. 273, 12817 12826.
4. Atwood C. S., Scarpa R. C., Huang X., Moir R. D., Jones W. D., Fairlie D. P., Tanzi R. E. Bush A. I. (2000) Characterization of copper interactions with alzheimer amyloid beta peptides: identification of an attomolar-affinity copper binding site on amyloid beta1-42. J. Neurochem. 75, 1219 1233.
5. Barnham K. J., Haeffner F., Ciccotosto G. D. et al. (2004) Tyrosine gated electron transfer is key to the toxic mechanism of Alzheimer's disease beta-amyloid. FASEB J. 18, 1427 1429.
6. Bate C., Kempster S., Last V. Williams A. (2006) Interferon-gamma increases neuronal death in response to amyloid-beta1-42. J. Neuroinflammation 3, 7.
7. Bayer T. A., Schafer S., Simons A. et al. (2003) Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Abeta production in APP23 transgenic mice. Proc. Natl Acad. Sci. USA 100, 14187 14192.
8. Blasko I., Marx F., Steiner E., Hartmann T. Grubeck-Loebenstein B. (1999) TNFalpha plus IFNgamma induce the production of Alzheimer beta-amyloid peptides and decrease the secretion of APPs. FASEB J. 13, 63 68.
9. Bocchini V., Mazzolla R., Barluzzi R., Blasi E., Sick P. Kettenmann H. (1992) An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res. 31, 616 621.
10. Bush A. I. (2008) Drug development based on the metals hypothesis of Alzheimer's disease. J. Alzheimers Dis. 15, 223 240.
11. Cagnin A., Brooks D. J., Kennedy A. M., Gunn R. N., Myers R., Turkheimer F. E., Jones T. Banati R. B. (2001) In-vivo measurement of activated microglia in dementia. Lancet 358, 461 467.
12. Cherny R. A., Legg J. T., McLean C. A., Fairlie D. P., Huang X., Atwood C. S., Beyreuther K., Tanzi R. E., Masters C. L. Bush A. I. (1999) Aqueous dissolution of Alzheimer's disease Abeta amyloid deposits by biometal depletion. J. Biol. Chem. 274, 23223 23228.
13. Cherny R. A., Atwood C. S., Xilinas M. E. et al. (2001) Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30, 665 676.
14. Chishti M. A., Yang D. S., Janus C. et al. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 276, 21562 21570.
15. Chohan M. O. Iqbal K. (2006) From tau to toxicity: emerging roles of NMDA receptor in Alzheimer's disease. J. Alzheimers Dis. 10, 81 87.
16. Crouch P. J., Blake R., Duce J. A. et al. (2005) Copper-dependent inhibition of human cytochrome c oxidase by a dimeric conformer of amyloid-beta1-42. J. Neurosci. 25, 672 679.
17. 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. (2001) Alzheimer's disease amyloid-beta binds copper and zinc to generate an allosterically ordered membrane-penetrating structure containing superoxide dismutase-like subunits. J. Biol. Chem. 276, 20466 20473.
18. Curtain C. C., Ali F. E., Smith D. G., Bush A. I., Masters C. L. Barnham K. J. (2003) Metal ions, pH, and cholesterol regulate the interactions of Alzheimer's disease amyloid-beta peptide with membrane lipid. J. Biol. Chem. 278, 2977 2982.
19. Das P., Howard V., Loosbrock N., Dickson D., Murphy M. P. Golde T. E. (2003) Amyloid-beta immunization effectively reduces amyloid deposition in FcRgamma-/- knock-out mice. J. Neurosci. 23, 8532 8538.
20. Di Bona D., Plaia A., Vasto S. et al. (2008) Association between the interleukin-1beta polymorphisms and Alzheimer's disease: a systematic review and meta-analysis. Brain Res. Rev. 59, 155 163.
21. Dong J., Atwood C. S., Anderson V. E., Siedlak S. L., Smith M. A., Perry G. Carey P. R. (2003) Metal binding and oxidation of amyloid-beta within isolated senile plaque cores: Raman microscopic evidence. Biochemistry (Mosc) 42, 2768 2773.
22. Dong J., Canfield J. M., Mehta A. K. et al. (2007) Engineering metal ion coordination to regulate amyloid fibril assembly and toxicity. Proc. Natl Acad. Sci. USA 104, 13313 13318.
23. Giuffrida M. L., Grasso G., Ruvo M., Pedone C., Saporito A., Marasco D., Pignataro B., Cascio C., Copani A. Rizzarelli E. (2007) Abeta(25-35) and its C- and/or N-blocked derivatives: copper driven structural features and neurotoxicity. J. Neurosci. Res. 85, 623 633.
24. Greenough M., Pase L., Voskoboinik I., Petris M. J., O'Brien A. W. Camakaris J. (2004) Signals regulating trafficking of Menkes (MNK; ATP7A) copper-translocating P-type ATPase in polarized MDCK cells. Am. J. Physiol. Cell Physiol. 287, C1463 C1471.
25. Harris J. R. (2002) In vitro fibrillogenesis of the amyloid beta 1-42 peptide: cholesterol potentiation and aspirin inhibition. Micron 33, 609 626.
26. Huang X., Atwood C. S., Hartshorn M. A. et al. (1999a) The A beta peptide of Alzheimer's disease directly produces hydrogen peroxide through metal ion reduction. Biochemistry (Mosc) 38, 7609 7616.
27. Huang X., Cuajungco M. P., Atwood C. S. et al. (1999b) Cu(II) potentiation of alzheimer abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J. Biol. Chem. 274, 37111 37116.
28. Huang X., Atwood C. S., Moir R. D., Hartshorn M. A., Tanzi R. E. Bush A. I. (2004) Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's Abeta peptides. J. Biol. Inorg. Chem. 9, 954 960.
29. Ida N., Hartmann T., Pantel J., Schroder J., Zerfass R., Forstl H., Sandbrink R., Masters C. L. Beyreuther K. (1996) Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J. Biol. Chem. 271, 22908 22914.
30. Janus C., Pearson J., McLaurin J. et al. (2000) A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408, 979 982.
31. La Fontaine S. L., Firth S. D., Camakaris J. et al. (1998) Correction of the copper transport defect of Menkes patient fibroblasts by expression of the Menkes and Wilson ATPases. J. Biol. Chem. 273, 31375 31380.
32. Lannfelt L., Blennow K., Zetterberg H. et al. (2008) Safety, efficacy, and biomarker findings of PBT2 in targeting Abeta as a modifying therapy for Alzheimer's disease: a phase IIa, double-blind, randomised, placebo-controlled trial. Lancet Neurol. 7, 779 786.
33. Lee J. Y., Mook-Jung I. Koh J. Y. (1999) Histochemically reactive zinc in plaques of the Swedish mutant beta-amyloid precursor protein transgenic mice. J. Neurosci. 19, RC10.
34. Lee J. Y., Friedman J. E., Angel I., Kozak A. Koh J. Y. (2004) The lipophilic metal chelator DP-109 reduces amyloid pathology in brains of human beta-amyloid precursor protein transgenic mice. Neurobiol. Aging 25, 1315 1321.
35. Lombardo J. A., Stern E. A., McLellan M. E., Kajdasz S. T., Hickey G. A., Bacskai B. J. Hyman B. T. (2003) Amyloid-beta antibody treatment leads to rapid normalization of plaque-induced neuritic alterations. J. Neurosci. 23, 10879 10883.
36. Lovell M. A., Robertson J. D., Teesdale W. J., Campbell J. L. Markesbery W. R. (1998) Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 158, 47 52.
37. Magaki S., Raghavan R., Mueller C., Oberg K. C., Vinters H. V. Kirsch W. M. (2007) Iron, copper, and iron regulatory protein 2 in Alzheimer's disease and related dementias. Neurosci. Lett. 418, 72 76.
38. Mao X., Kim B. E., Wang F., Eide D. J. Petris M. J. (2007) A histidine-rich cluster mediates the ubiquitination and degradation of the human zinc transporter, hZIP4, and protects against zinc cytotoxicity. J. Biol. Chem. 282, 6992 7000.
39. Mattson M. P., Tomaselli K. J. Rydel R. E. (1993) Calcium-destabilizing and neurodegenerative effects of aggregated beta-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35 49.
40. Maynard C. J., Cappai R., Volitakis I., Cherny R. A., White A. R., Beyreuther K., Masters C. L., Bush A. I. Li Q. X. (2002) Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J. Biol. Chem. 277, 44670 44676.
41. McGeer P. L., Itagaki S., Tago H. McGeer E. G. (1987) Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci. Lett. 79, 195 200.
42. Miller L. M., Wang Q., Telivala T. P., Smith R. J., Lanzirotti A. Miklossy J. (2006) Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with beta-amyloid deposits in Alzheimer's disease. J. Struct. Biol. 155, 30 37.
43. Monsonego A., Imitola J., Petrovic S., Zota V., Nemirovsky A., Baron R., Fisher Y., Owens T. Weiner H. L. (2006) Abeta-induced meningoencephalitis is IFN-gamma-dependent and is associated with T cell-dependent clearance of Abeta in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA 103, 5048 5053.
44. Petris M. J., Mercer J. F., Culvenor J. G., Lockhart P., Gleeson P. A. Camakaris J. (1996) Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J. 15, 6084 6095.
45. Petris M. J., Voskoboinik I., Cater M., Smith K., Kim B. E., Llanos R. M., Strausak D., Camakaris J. Mercer J. F. (2002) Copper-regulated trafficking of the Menkes disease copper ATPase is associated with formation of a phosphorylated catalytic intermediate. J. Biol. Chem. 277, 46736 46742.
46. Phinney A. L., Drisaldi B., Schmidt S. D. et al. (2003) In vivo reduction of amyloid-beta by a mutant copper transporter. Proc. Natl Acad. Sci. USA 100, 14193 14198.
47. Pike C. J., Burdick D., Walencewicz A. J., Glabe C. G. Cotman C. W. (1993) Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676 1687.
48. Regland B., Lehmann W., Abedini I., Blennow K., Jonsson M., Karlsson I., Sjogren M., Wallin A., Xilinas M. Gottfries C. G. (2001) Treatment of Alzheimer's disease with clioquinol. Dement. Geriatr. Cogn. Disord. 12, 408 414.
49. Ritchie C. W., Bush A. I., Mackinnon A. et al. (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.
50. Sasaki A., Yamaguchi H., Ogawa A., Sugihara S. Nakazato Y. (1997) Microglial activation in early stages of amyloid beta protein deposition. Acta Neuropathol. 94, 316 322.
51. Schlief M. L., Craig A. M. Gitlin J. D. (2005) NMDA receptor activation mediates copper homeostasis in hippocampal neurons. J. Neurosci. 25, 239 246.
52. Schlief M. L., West T., Craig A. M., Holtzman D. M. Gitlin J. D. (2006) Role of the Menkes copper-transporting ATPase in NMDA receptor-mediated neuronal toxicity. Proc. Natl Acad. Sci. USA 103, 14919 14924.
53. Simonyi A., He Y., Sheng W., Sun A. Y., Wood W. G., Weisman G. A. Sun G. Y. (2010) Targeting NADPH oxidase and phospholipases A2 in Alzheimer's disease. Mol. Neurobiol. 41, 73 86.
54. Suh S. W., Jensen K. B., Jensen M. S., Silva D. S., Kesslak P. J., Danscher G. Frederickson C. J. (2000) Histochemically-reactive zinc in amyloid plaques, angiopathy, and degenerating neurons of Alzheimer's diseased brains. Brain Res. 852, 274 278.
55. Tweedie D., Sambamurti K. Greig N. H. (2007) TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr. Alzheimer Res. 4, 378 385.
56. White C., Lee J., Kambe T., Fritsche K. Petris M. J. (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949 33956.
57. Wilcock D. M., DiCarlo G., Henderson D., Jackson J., Clarke K., Ugen K. E., Gordon M. N. Morgan D. (2003) Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J. Neurosci. 23, 3745 3751.
58. Yamaguchi Y., Heiny M. E., Suzuki M. Gitlin J. D. (1996) Biochemical characterization and intracellular localization of the Menkes disease protein. Proc. Natl Acad. Sci. USA 93, 14030 14035.
59. Yamamoto M., Kiyota T., Horiba M., Buescher J. L., Walsh S. M., Gendelman H. E. Ikezu T. (2007) Interferon-gamma and tumor necrosis factor-alpha regulate amyloid-beta plaque deposition and beta-secretase expression in Swedish mutant APP transgenic mice. Am. J. Pathol. 170, 680 692.
60. Yoburn J. C., Tian W., Brower J. O., Nowick J. S., Glabe C. G. Van Vranken D. L. (2003) Dityrosine cross-linked Abeta peptides: fibrillar beta-structure in Abeta(1-40) is conducive to formation of dityrosine cross-links but a dityrosine cross-link in Abeta(8-14) does not induce beta-structure. Chem. Res. Toxicol. 16, 531 535.
61. Yoshiike Y., Tanemura K., Murayama O., Akagi T., Murayama M., Sato S., Sun X., Tanaka N. Takashima A. (2001) New insights on how metals disrupt amyloid beta-aggregation and their effects on amyloid-beta cytotoxicity. J. Biol. Chem. 276, 32293 32299.