Inhibition of human high-affinity copper importer Ctr1 orthologous in the nervous system of Drosophila ameliorates Aβ42-induced Alzheimer's disease-like symptoms

Neurobiology of Aging

Volumn 34, Issue 11, 2013, Pages 2604-2612

  Lang, Minglin ^a,b,d   Fan, Qiangwang ^a   Wang, Lei ^a,c   Zheng, Yajun ^b   Xiao, Guiran ^a   Wang, Xiaoxi ^a   Wang, Wei ^e   Zhong, Yi ^a,c   Zhou, Bing ^a  

^a TSINGHUA UNIVERSITY   (China)

^b AGRICULTURAL UNIVERSITY OF HEBEI   (China)

^c BEIJING UNIVERSITY OF CHEMICAL TECHNOLOGY   (China)

^d KANSAS STATE UNIVERSITY   (United States)

^e EDITH COWAN UNIVERSITY   (Australia)

Author keywords

Alzheimer's disease; Amyloid ; Copper; Ctr1; DmATP7; Drosophila; High affinity copper importer; Neurodegeneration

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN PROTEIN; CATION TRANSPORT PROTEIN; COPPER ION; CTR1 PROTEIN; CTR1B PROTEIN; CTR1C PROTEIN; DMATP7 PROTEIN; IDE PROTEIN; ISOPROTEIN; NEP1 PROTEIN; NEP2 PROTEIN; NEP3 PROTEIN; PROTEINASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BRAIN METABOLISM; CATION TRANSPORT; CLIMBING; CONTROLLED STUDY; COPPER BRAIN ACCUMULATION; COPPER METABOLISM; CTR1C GENE; DISEASE ASSOCIATION; DISEASE MODEL; DROSOPHILA; GENE; LIFE EXTENSION; MOLECULAR WEIGHT; MOTOR PERFORMANCE; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA INTERFERENCE; SEQUENCE HOMOLOGY;

ALZHEIMER'S DISEASE; AMYLOID-Β; COPPER; CTR1; DMATP7; DROSOPHILA; HIGH-AFFINITY COPPER IMPORTER; NEURODEGENERATION;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CATION TRANSPORT PROTEINS; CELL COUNT; CHELATING AGENTS; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; HUMANS; LOCOMOTION; LONGEVITY; MALE; MEMORY DISORDERS; NERVE DEGENERATION; NERVOUS SYSTEM; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHENANTHROLINES; RNA INTERFERENCE; TIME FACTORS;

EID: 84881555354     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.05.029     Document Type: Article

References (59)

1. Adlard P.A., Bush A.I. Metals and Alzheimer's disease. J.Alzheimers Dis. 2006, 10:145-163.
2. Arking R., Buck S., Berrios A., Dwyer S., Baker G.T. Elevated paraquat resistance can be used as a bioassay for longevity in a genetically based long-lived strain of Drosophila. Dev. Genet. 1991, 12:362-370.
3. Atwood C.S., Moir R.D., Huang X.D., Scarpa R.C., Bacarra N.M.E., Romano D.M., Hartshorn M.K., Tanzi R.E., Bush A.I. Dramatic aggregation of Alzheimer A beta by Cu(II) is induced by conditions representing physiological acidosis. J.Biol. Chem. 1998, 273:12817-12826.
4. Barnham K.J., Bush A.I. Metals in Alzheimer's and Parkinson's diseases. Curr. Opin. Chem. Biol. 2008, 12:222-228.
5. Bharathi, Indi S.S., Rao K.S.J. Copper- and iron-induced differential fibril formation in alpha-synuclein: TEM study. Neurosci. Lett. 2007, 424:78-82.
6. Bieler S., Soto C. beta-Sheet breakers for Alzheimer's disease therapy. Curr. Drug. Targets 2004, 5:553-558.
7. Bitan G., Kirkitadze M.D., Lomakin A., Vollers S.S., Benedek G.B., Teplow D.B. Amyloid beta-protein (A beta) assembly: a beta 40 and A beta 42 oligomerize through distinct pathways. Proc. Natl. Acad. Sci. U.S.A 2003, 100:330-335.
8. Bleackley M.R., MacGillivray R.T.A. Transition metal homeostasis: from yeast to human disease. Biometals 2011, 24:785-809.
9. Brewer G.J. Copper excess, zinc deficiency, and cognition loss in Alzheimer's disease. Biofactors 2012, 38:107-113.
10. Bush A.I., Pettingell W.H., Multhaup G., Paradis M.D., Vonsattel J.P., Gusella J.F., Beyreuther K., Masters C.L., Tanzi R.E. Rapid induction of Alzheimer a-beta amyloid formation by zinc. Science 1994, 265:1464-1467.
11. Butterfield D.A., Howard B., Yatin S., Koppal T., Drake J., Hensley K., Aksenov M., Aksenova M., Subramaniam R., Varadarajan S., Harris-White M.E., Pedigo N.W., Carney J.M. Elevated oxidative stress in models of normal brain aging and Alzheimer's disease. Life Sci. 1999, 65:1883-1892.
12. Carty N., Nash K.R., Brownlow M., Cruite D., Wilcock D., Selenica M.L., Lee D.C., Gordon M.N., Morgan D. Intracranial injection of AAV expressing NEP but not IDE reduces amyloid pathology in APP+PS1 transgenic mice. PloS One 2013, 8:e59626.
13. Cherny R.A., Legg J.T., McLean C.A., Fairlie D.P., Huang X.D., Atwood C.S., Beyreuther K., Tanzi R.E., Masters C.L., Bush A.I. Aqueous dissolution of Alzheimer's disease A beta amyloid deposits by biometal depletion. J.Biol. Chem. 1999, 274:23223-23228.
14. Chiang H.C., Wang L., Xie Z.L., Yau A., Zhong Y. PI3 kinase signaling is involved in A beta-induced memory loss in Drosophila. Proc. Natl. Acad. Sci. U.S.A 2010, 107:7060-7065.
15. Dias-Santagata D., Fulga T.A., Duttaroy A., Feany M.B. Oxidative stress mediates tau-induced neurodegeneration in Drosophila. J.Clin. Invest. 2007, 117:236-245.
16. Dong J., Atwood C.S., Anderson V.E., Siedlak S.L., Smith M.A., Perry G., Carey P.R. Metal binding and oxidation of amyloid-beta within isolated senile plaque cores: raman microscopic evidence. Biochem.-US 2003, 42:2768-2773.
17. Duce J.A., Bush A.I. Biological metals and Alzheimer's disease: implications for therapeutics and diagnostics. Prog. Neurobiol. 2010, 92:1-18.
18. Farris W., Mansourian S., Chang Y., Lindsley L., Eckman E.A., Frosch M.P., Eckman C.B., Tanzi R.E., Selkoe D.J., Guenette S. Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain invivo. Proc. Natl. Acad. Sci. U.S.A 2003, 100:4162-4167.
19. Finelli A., Kelkar A., Song H.J., Yang H.D., Konsolaki M. Amodel for studying Alzheimer's A beta 42-induced toxicity in Drosophila melanogaster. Mol. Cell. Neurosci. 2004, 26:365-375.
20. Geng J., Li M., Wu L., Ren J., Qu X. Liberation of copper from amyloid plaques: making a risk factor useful for Alzheimer's disease treatment. J.Med. Chem. 2012, 55:9146-9155.
21. Golde T.E., Dickson D., Hutton M. Filling the gaps in the abeta cascade hypothesis of Alzheimer's disease. Curr. Alzheimer Res. 2006, 3:421-430.
22. Haass C., Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nature Rev. Mol. Cell. Biol. 2007, 8:101-112.
23. Halliwell B., Gutteridge J.M.C. Role of free-radicals and catalytic metal-ions in human-disease-an overview. Methods Enzymol. 1990, 186:1-85.
24. Horikoshi Y., Mori T., Maeda M., Kinoshita N., Sato K., Yamaguchi H. Abeta N-terminal-end specific antibody reduced beta-amyloid in Alzheimer-model mice. Biochem. Biophys. Res. Commun. 2004, 325:384-387.
25. Huang X.D., Cuajungco M.P., Atwood C.S., Hartshorn M.A., Tyndall J.D.A., Hanson G.R., Stokes K.C., Leopold M., Multhaup G., Goldstein L.E., Scarpa R.C., Saunders A.J., Lim J., Moir R.D., Glabe C., Bowden E.F., Masters C.L., Fairlie D.P., Tanzi R.E., Bush A.I. Cu(II) potentiation of Alzheimer A beta neurotoxicity-correlation with cell-free hydrogen peroxide production and metal reduction. J.Biol. Chem. 1999, 274:37111-37116.
26. Iijima K., Chiang H.C., Hearn S.A., Hakker I., Gatt A., Shenton C., Granger L., Leung A., Iijima-Ando K., Zhong Y. Abeta 42 mutants with different aggregation profiles induce distinct pathologies in Drosophila. PLoS One 2008, 3. : e1703.
27. Iijima K., Liu H.P., Chiang A.S., Hearn S.A., Konsolaki M., Zhong Y. Dissecting the pathological effects of human A beta 40 and A beta 42 in Drosophila: a potential model for Alzheimer's disease. Proc Natl Acad Sci U.S.A 2004, 101:6623-6628.
28. Iwata N., Tsubuki S., Takaki Y., Watanabe K., Sekiguchi M., Hosoki E., Kawashima-Morishima M., Lee H.J., Hama E., Sekine-Aizawa Y., Saido T.C. Identification of the major A beta(1-42)-degrading catabolic pathway in brain parenchyma: suppression leads to biochemical and pathological deposition. Nat. Med. 2000, 6:143-150.
29. James S.A., Volitakis I., Adlard P.A., Duce J.A., Masters C.L., Cherny R.A., Bush A.I. Elevated labile Cu is associated with oxidative pathology in Alzheimer disease. Free Radic. Biol. Med. 2012, 52:298-302.
30. Jones C.E., Abdelraheim S.R., Brown D.R., Viles J.H. Preferential Cu2+ coordination by His(96) and His(111) induces beta-sheet formation in the unstructured amyloidogenic region of the prion protein. J.Biol. Chem. 2004, 279:32018-32027.
31. Keller J.N., Schmitt F.A., Scheff S.W., Ding Q., Chen Q., Butterfield D.A., Markesbery W.R. Evidence of increased oxidative damage in subjects with mild cognitive impairment. Neurology 2005, 64:1152-1156.
32. Kessler H., Bayer T.A., Bach D., Schneider-Axmann T., Supprian T., Herrmann W., Haber M., Multhaup G., Falkai P., Pajonk F.G. Intake of copper has no effect on cognition in patients with mild Alzheimer's disease: a pilot phase 2 clinical trial. J.Neural Transm. 2008, 115:1181-1187.
33. Lang M.L., Wang L., Fan Q.W., Xiao G.R., Wang X.X., Zhong Y., Zhou B. Genetic inhibition of solute-linked carrier 39 family transporter 1 ameliorates A beta pathology in a Drosophila model of Alzheimer's disease. PLoS Genet. 2012, 8:623-639.
34. 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. J.Neurol. Sci. 1998, 158:47-52.
35. Lutsenko S., Petris N.J. Function and regulation of the mammalian copper-transporting ATPases: insights from biochemical and cell biological approaches. J.Membrane Biol. 2003, 191:1-12.
36. Maynard C.J., Cappai R., Volitakis I., Cherny R.A., White A.R., Beyreuther K., Masters C.L., Bush A.I., Li Q.X. Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J.Biol. Chem. 2002, 277:44670-44676.
37. Miller L.M., Wang Q., Telivala T.P., Smith R.J., Lanzirotti A., Miklossy J. 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. 2006, 155:30-37.
38. Muqit M.M.K., Feany M.B. Modelling neurodegenerative diseases in Drosophila: a fruitful approach?. Nat. Rev. Neurosci. 2002, 3:237-243.
39. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E.K., Jones P.K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C.S., Petersen R.B., Smith M.A. Oxidative damage is the earliest event in Alzheimer disease. J.Neuropathol. Exp. Neurol. 2001, 60:759-767.
40. Reddy P.H. Amyloid precursor protein-mediated free radicals and oxidative damage: implications for the development and progression of Alzheimer's disease. J.Neurochem. 2006, 96:1-13.
41. Rival T., Page R.M., Chandraratna D.S., Sendall T.J., Ryder E., Liu B., Lewis H., Rosahl T., Hider R., Camargo L.M., Shearman M.S., Crowther D.C., Lomas D.A. Fenton chemistry and oxidative stress mediate the toxicity of the beta-amyloid peptide in a Drosophila model of Alzheimer's disease. Eur. J. Neurosci. 2009, 29:1335-1347.
42. Saini N., Oelhafen S., Hua H.Q., Georgiev O., Schaffner W., Bueler H. Extended lifespan of Drosophila parkin mutants through sequestration of redox-active metals and enhancement of anti-oxidative pathways. Neurobiol. Dis. 2010, 40:82-92.
43. Sharma A.K., Pavlova S.T., Kim J., Finkelstein D., Hawco N.J., Rath N.P., Mirica L.M. Bifunctional compounds for controlling metal-mediated aggregation of the abeta42 peptide. J.Am. Chem. Soc. 2012, 134:6625-6636.
44. Sgourakis N.G., Yan Y.L., McCallum S.A., Wang C.Y., Garcia A.E. The Alzheimer's peptides A beta 40 and 42 adopt distinct conformations in water: a combined MD/NMR study. J.Mol. Biol. 2007, 368:1448-1457.
45. Southon A., Palstra N., Veldhuis N., Gaeth A., Robin C., Burke R., Camakaris J. Conservation of copper-transporting P(IB)-type ATPase function. Biometals 2010, 23:681-694.
46. Steiger D., Fetchko M., Vardanyan A., Atanesyan L., Steiner K., Turski M.L., Thiele D.J., Georgiev O., Schaffner W. The Drosophila copper transporter Ctr1C functions in male fertility. J.Biol. Chem. 2010, 285:17089-17097.
47. Strozyk D., Launer L.J., Adlard P.A., Cherny R.A., Tsatsanis A., Volitakis I., Blennow K., Petrovitch H., White L.R., Bush A.I. Zinc and copper modulate Alzheimer A beta levels in human cerebrospinal fluid. Neurobiol. Aging 2009, 30:1069-1077.
48. Sudoh S., Frosch M.P., Wolf B.A. Differential effects of proteases involved in intracellular degradation of amyloid beta-protein between detergent-soluble and -insoluble pools in CHO-695 cells. Biochemistry 2002, 41:1091-1099.
49. Syme C.D., Nadal R.C., Rigby S.E.J., Viles J.H. Copper binding to the amyloid-beta (A beta) peptide associated with Alzheimer's disease-folding, coordination geometry, pH dependence, stoichiometry, and affinity of A beta-(1-28): insights from a range of complementary spectroscopic techniques. J.Biol. Chem. 2004, 279:18169-18177.
50. Tougu V., Tiiman A., Palumaa P. Interactions of Zn(II) and Cu(II) ions with Alzheimer's amyloid-beta peptide. metal ion binding, contribution to fibrillization and toxicity. Metallomics 2011, 3:250-261.
51. Tully T., Cambiazo V., Kruse L. Memory through metamorphosis in normal and mutant Drosophila. J.Neurosci. 1994, 14:68-74.
52. Tully T., Quinn W.G. Classical-conditioning and retention in normal and mutant Drosophila-melanogaster. J.Comp. Physiol. A. 1985, 157:263-277.
53. Turski M.L., Thiele D.J. Drosophila Ctr1A functions as a copper transporter essential for development. J.Biol. Chem 2007, 282:24017-24026.
54. White A.R., Multhaup G., Maher F., Bellingham S., Camakaris J., Zheng H., Bush A.I., Beyreuther K., Masters C.L., Cappai R. The Alzheimer's disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures. J.Neurosci. 1999, 19:9170-9179.
55. Xing Y.M., Higuchi K. Amyloid fibril proteins. Mech. Ageing Dev. 2002, 123:1625-1636.
56. Yamamoto N., Arima H., Naruse K., Kasahara R., Taniura H., Hirate H., Sugiura T., Suzuki K., Sobue K. Ketamine reduces amyloid beta-protein degradation by suppressing neprilysin expression in primarycultured astrocytes. Neurosci. Lett. 2013, 545, 54-58.
57. Yatin S.M., Varadarajan S., Link C.D., Butterfield D.A. Invitro and invivo oxidative stress associated with Alzheimer's amyloid beta-peptide (1-42). Neurobiol. Aging 1999, 20:325-330.
58. Yin H., Barnet R.C., Miller R.R. 2nd-Order conditioning and Pavlovian conditioned inhibition-operational similarities and differences. J.Exp. Psychol. Anim. B. 1994, 20:419-428.
59. Zhou H., Cadigan K.M., Thiele D.J. Acopper-regulated transporter required for copper acquisition, pigmentation, and specific stages of development in Drosophila melanogaster. J.Biol. Chem. 2003, 278:48210-48218.