Low levels of copper disrupt brain amyloid-β homeostasis by altering its production and clearance

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 36, 2013, Pages 14771-14776

  Singh, Itender ^a   Sagare, Abhay P ^a   Coma, Mireia ^a   Perlmutter, David ^a   Gelein, Robert ^a   Bell, Robert D ^a   Deane, Richard J ^a   Zhong, Elaine ^a   Parisi, Margaret ^a   Ciszewski, Joseph ^a   Kasper, R Tristan ^a   Deane, Rashid ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

BACE1; BBB; Cerebrovascular; Environmental; Toxicity

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; COPPER; DRINKING WATER; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PRION PROTEIN; CD31 ANTIGEN; LOW DENSITY LIPOPROTEIN RECEPTOR; LRP1 PROTEIN, MOUSE; RADIOACTIVE IODINE; TUMOR SUPPRESSOR PROTEIN;

AGED; AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BRAIN; BRAIN CAPILLARY; BRAIN CELL; BRAIN MATURATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE OVEREXPRESSION; HOMEOSTASIS; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NITROTYROSINATION; NONHUMAN; OXIDATIVE STRESS; PARENCHYMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REPRODUCIBILITY; TRANSGENIC MOUSE; AGE; ANIMAL; BLOOD BRAIN BARRIER; C57BL MOUSE; CAPILLARY; CELL CULTURE; CELL SURVIVAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLIC CLEARANCE RATE; METABOLISM; TIME; VASCULARIZATION; WESTERN BLOTTING;

ANIMALIA; MUS; MUS MUSCULUS;

AGE FACTORS; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIGENS, CD31; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; CAPILLARIES; CELL SURVIVAL; CELLS, CULTURED; COPPER; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; HOMEOSTASIS; HUMANS; IODINE RADIOISOTOPES; METABOLIC CLEARANCE RATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, LDL; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84883356543     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1302212110     Document Type: Article

References (64)

1. Prohaska JR (2008) Role of copper transporters in copper homeostasis. Am J Clin Nutr 88(3):826S-829S.
2. Lutsenko S, Bhattacharjee A, Hubbard AL (2010) Copper handling machinery of the brain. Metallomics 2(9):596-608.
3. Chutkow JG (1978) Evidence for uptake of nonceruloplasminic copper in the brain: Effect of ionic copper and amino acids. Proc Soc Exp Biol Med. 158(1):113-116.
4. Harris ED (2000) Cellular copper transport and metabolism. Annu Rev Nutr 20:291-310.
5. Brewer GJ (2012) Copper excess, zinc deficiency, and cognition loss in Alzheimer's disease. Biofactors 38(2):107-113.
6. Squitti R (2012) Copper dysfunction in Alzheimer's disease: From meta-analysis of biochemical studies to new insight into genetics. J Trace Elem Med Biol 26(2-3):93-96.
7. Bush AI, Tanzi RE (2008) Therapeutics for Alzheimer's disease based on the metal hypothesis. Neurotherapeutics 5(3):421-432. (Pubitemid 351952485)
8. Rose F, Hodak M, Bernholc J (2011) Mechanism of copper(II)-induced misfolding of Parkinson's disease protein. Sci Rep 1:11.
9. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR (1998) Copper, iron and zinc in Alzheimer's disease senile plaques. J Neurol Sci 158(1):47-52. (Pubitemid 28277534)
10. Squitti R, et al. (2002) Elevation of serum copper levels in Alzheimer' s disease. Neurology 59(8):1153-1161. (Pubitemid 35192384)
11. Squitti R, et al. (2006) Excess of nonceruloplasmin serum copper in AD correlates with MMSE, CSF [beta]-amyloid, and h-tau. Neurology 67(1):76-82. (Pubitemid 44305465)
12. James SA, et al. (2012) Elevated labile Cu is associated with oxidative pathology in Alzheimer disease. Free Radic Biol Med 52(2):298-302.
13. Faux NG, et al. (2010) PBT2 rapidly improves cognition in Alzheimer's Disease: Additional phase II analyses. J Alzheimers Dis 20(2):509-516.
14. Sparks DL, Schreurs BG (2003) Trace amounts of copper in water induce beta-amyloid plaques and learning deficits in a rabbit model of Alzheimer's disease. Proc Natl Acad Sci USA 100(19):11065-11069. (Pubitemid 37140153)
15. Sparks DL, et al. (2006) Trace copper levels in the drinking water, but not zinc or aluminum influence CNS Alzheimer-like pathology. J Nutr Health Aging 10(4): 247-254. (Pubitemid 44351819)
16. Bayer TA, 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(24):14187-14192. (Pubitemid 37499212)
17. Phinney AL, et al. (2003) In vivo reduction of amyloid-beta by a mutant copper transporter. Proc Natl Acad Sci USA 100(24):14193-14198. (Pubitemid 37499213)
18. Maynard CJ, et al. (2002) Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J Biol Chem 277(47):44670-44676. (Pubitemid 36159056)
19. Bayer TA, Multhaup G (2005) Involvement of amyloid beta precursor protein (AbetaPP) modulated copper homeostasis in Alzheimer's disease. J Alzheimers Dis 8(2):201-206; discussion 209-215.
20. Borchardt T, et al. (1999) Copper inhibits beta-amyloid production and stimulates the non-amyloidogenic pathway of amyloid-precursor-protein secretion. Biochem J 344(Pt 2):461-467. (Pubitemid 30011603)
21. Selkoe DJ (2001) Clearing the brain's amyloid cobwebs. Neuron 32(2):177-180.
22. Deane R, Zlokovic BV (2007) Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 4(2):191-197. (Pubitemid 46562394)
23. Iwata N, Higuchi M, Saido TC (2005) Metabolism of amyloid-beta peptide and Alzheimer's disease. Pharmacol Ther 108(2):129-148. (Pubitemid 41527082)
24. Iliff JJ, et al. (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta. Sci Trans Med 4(147):147ra111.
25. Deane R, et al. (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms. Neuron 43(3):333-344. (Pubitemid 39061126)
26. Donahue JE, et al. (2006) RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol 112(4):405-415. (Pubitemid 44469161)
27. Deane R, et al. (2008) apoE isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118(12):4002-4013.
28. Stöckel J, Safar J, Wallace AC, Cohen FE, Prusiner SB (1998) Prion protein selectively binds copper(II) ions. Biochemistry 37(20):7185-7193. (Pubitemid 28235199)
29. Taylor DR, Hooper NM (2007) The low-density lipoprotein receptor-related protein 1 (LRP1) mediates the endocytosis of the cellular prion protein. Biochem J 402(1):17-23.
30. Ruiz FH, González M, Bodini M, Opazo C, Inestrosa NC (1999) Cysteine 144 is a key residue in the copper reduction by the beta-amyloid precursor protein. J Neurochem 73(3):1288-1292. (Pubitemid 29395490)
31. Terwel D, et al. (2011) Neuroinflammatory and behavioural changes in the Atp7B mutant mouse model of Wilson's disease. J Neurochem 118(1):105-112.
32. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57(2):178-201.
33. Deane R, BradburyMW(1990) Transport of lead-203 at the blood-brain barrier during short cerebrovascular perfusion with saline in the rat. J Neurochem 54(3):905-914.
34. Deane R, Zheng W, Zlokovic BV (2004) Brain capillary endothelium and choroid plexus epithelium regulate transport of transferrin-bound and free iron into the rat brain. J Neurochem 88(4):813-820. (Pubitemid 38199301)
35. Tayarani I, Cloëz I, Clément M, Bourre JM (1989) Antioxidant enzymes and related trace elements in aging brain capillaries and choroid plexus. J Neurochem 53(3):817-824.
36. Wapnir RA (1998) Copper absorption and bioavailability. Am J Clin Nutr 67(5, Suppl):1054S-1060S.
37. Weiss KC, Linder MC (1985) Copper transport in rats involving a new plasma protein. Am J Physiol 249(1 Pt 1):E77-E88. (Pubitemid 15031734)
38. Wirth PL, Linder MC (1985) Distribution of copper among components of human serum. J Natl Cancer Inst 75(2):277-284. (Pubitemid 15229333)
39. Brewer GJ (2009) The risks of copper toxicity contributing to cognitive decline in the aging population and to Alzheimer's disease. J Am Coll Nutr 28(3):238-242.
40. Hill GM, Brewer GJ, Juni JE, Prasad AS, Dick RD (1986) Treatment of Wilson's disease with zinc. II. Validation of oral 64copper with copper balance. Am J Med Sci 292(6):344-349. (Pubitemid 17040561)
41. Choi BS, ZhengW(2009) Copper transport to the brain by the blood-brain barrier and blood-CSF barrier. Brain Res 1248:14-21.
42. Qian Y, Tiffany-Castiglioni E, Welsh J, Harris ED (1998) Copper efflux from murine microvascular cells requires expression of the menkes disease Cu-ATPase. J Nutr 128(8):1276-1282. (Pubitemid 28361417)
43. Greenough MA, et al. (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(11):9776-9786.
44. Hu GF (1998) Copper stimulates proliferation of human endothelial cells under culture. J Cell Biochem 69(3):326-335.
45. Smith MA, et al. (1994) Advanced Maillard reaction end products, free radicals, and protein oxidation in Alzheimer's disease. Ann N Y Acad Sci 738:447-454.
46. Huang X, et al. (1999) Cu(II) potentiation of alzheimer abeta neurotoxicity. Correlation with cell-free hydrogen peroxide production and metal reduction. J Biol Chem 274(52):37111-37116.
47. Butterfield DA, Lauderback CM (2002) Lipid peroxidation and protein oxidation in Alzheimer's disease brain: Potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med 32(11):1050-1060. (Pubitemid 34603342)
48. Kong GK, et al. (2008) Copper binding to the Alzheimer's disease amyloid precursor protein. Eur Biophys J 37(3):269-279.
49. Li Y, Cam J, Bu G (2001) Low-density lipoprotein receptor family: Endocytosis and signal transduction. Mol Neurobiol 23(1):53-67. (Pubitemid 32948272)
50. Syme CD, Nadal RC, Rigby SE, Viles JH (2004) Copper binding to the amyloid-beta (Abeta) peptide associated with Alzheimer's disease: Folding, coordination geometry, pH dependence, stoichiometry, and affinity of Abeta-(1-28): Insights from a range of complementary spectroscopic techniques. J Biol Chem 279(18):18169-18177. (Pubitemid 38623229)
51. Atwood CS, et al. (2004) Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43(2):560-568. (Pubitemid 38082580)
52. Guix FX, Uribesalgo I, Coma M, Muñoz FJ (2005) The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol 76(2):126-152. (Pubitemid 41242885)
53. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G (1997) Widespread per-oxynitrite-mediated damage in Alzheimer's disease. J Neurosci 17(8):2653-2657. (Pubitemid 27154998)
54. Sultana R, et al. (2006) Identification of nitrated proteins in Alzheimer's disease brain using a redox proteomics approach. Neurobiol Dis 22(1):76-87.
55. Coma M, et al. (2005) Lack of oestrogen protection in amyloid-mediated endothelial damage due to protein nitrotyrosination. Brain 128(Pt 7):1613-1621. (Pubitemid 41373680)
56. Yoburn JC, et al. (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(4):531-535. (Pubitemid 36514511)
57. House E, et al. (2004) Aluminium, iron, zinc and copper influence the in vitro formation of amyloid fibrils of Abeta42 in a manner which may have consequences for metal chelation therapy in Alzheimer's disease. J Alzheimers Dis 6(3):291-301.
58. Hung YH, et al. (2009) Paradoxical condensation of copper with elevated beta-amyloid in lipid rafts under cellular copper deficiency conditions: Implications for Alzheimer disease. J Biol Chem 284(33):21899-21907.
59. You H, et al. (2012) Aβ neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 109(5):1737-1742.
60. Deane R, et al. (2012) A multimodal RAGE-specific inhibitor reduces amyloid β-mediated brain disorder in a mouse model of Alzheimer disease. J Clin Invest 122(4):1377-1392.
61. Lannfelt L, et al.; PBT2-201-EURO study group (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(9):779-786.
62. Crouch PJ, et al. (2011) The Alzheimer's therapeutic PBT2 promotes amyloid-β degradation and GSK3 phosphorylation via a metal chaperone activity. J Neurochem 119(1):220-230.
63. Deane R, Bell RD, Sagare A, Zlokovic BV (2009) Clearance of amyloid-beta peptide across the blood-brain barrier: Implication for therapies in Alzheimer's disease. CNS Neurol Disord Drug Targets 8(1):16-30.
64. Wu Z, et al. (2005) Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease. Nat Med 11(9):959-965. (Pubitemid 41294441)