Divalent metal transporter 1 is involved in amyloid precursor protein processing and Aβ generation

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4207-4217

  Zheng, Wei ^a   Xin, Na ^a   Chi, Zhi Hong ^a   Zhao, Bo Lu ^b   Zhang, Jie ^b   Li, Jia Yi ^c   Wang, Zhan You ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c LUND UNIVERSITY   (Sweden)

Author keywords

amyloid peptide; Alzheimer's disease; APP PS1 transgenic mouse; Divalent cation transporter 1; RNA interference

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ARTICLE; AUTOPSY; BRAIN; BRAIN CORTEX; CONTROLLED STUDY; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; ION TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SECRETION; RNA INTERFERENCE; TRANSGENIC MOUSE; WILD TYPE;

AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CATION TRANSPORT PROTEINS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; METALS; MICE; MICE, TRANSGENIC; MUTATION; NEURONS; PROTEIN ISOFORMS; RNA INTERFERENCE;

MUS MUSCULUS;

EID: 72749101173     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-135749     Document Type: Article

References (60)

1. Mattson, M. P. (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639 (Pubitemid 39061671)
2. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356 (Pubitemid 34790756)
3. Lovell, M. A., Robertson, J. D., Teesdale, W. J., Campbell, J. L., and Markesbery, W. R. (1998) Copper, iron and zinc in Alzheimer's disease senile plaques. J. Neurol. Sci. 158, 47-52
4. Finefrock, A. E., Bush, A. I., and Doraiswamy, P. M. (2003) Current status of metals as therapeutic targets in Alzheimer's disease. J. Am. Geriatr. Soc. 51, 1143-1148 (Pubitemid 36993474)
5. Miller, L. M., Wang, Q., Telivala, T. P., Smith, R. J., Lanzirotti, A., and 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 (Pubitemid 43867313)
6. Huang, X., Atwood, C. S., Moir, R. D., Hartshorn, M. A., Tanzi, R. E., and Bush, A. I. (2004) Trace metal contamination initiates the apparent auto-aggregation, amyloidosis, and oligomerization of Alzheimer's Aβ peptides. J. Biol. Inorg. Chem. 9, 954-960 (Pubitemid 40109902)
7. Atwood, C. S., Huang, X., Moir, R. D., Tanzi, R. E., and Bush, A. I. (1999) Role of free radicals and metal ions in the pathogenesis of Alzheimer's disease. Met. Ions Biol. Syst. 36, 309-364
8. Atwood, C. S., Scarpa, R. C., Huang, X., Moir, R. D., Jones, W. D., Fairlie, D. P., Tanzi, R. E., and Bush, A. I. (2000) Characterization of copper interactions with Alzheimer amyloid beta peptides: identification of an attomolar-affinity copper binding site on amyloid β1-42. J. Neurochem. 75, 1219-1233 (Pubitemid 30660512)
9. Opazo, C., Huang, X., Cherny, R. A., Moir, R. D., Roher, A. E., White, A. R., Cappai, R., Masters, C. L., Tanzi, R. E., Inestrosa, N. C., and Bush, A. I. (2002) Metalloenzyme-like activity of Alzheimer's disease beta-amyloid. Cu-dependent catalytic conversion of dopamine, cholesterol, and biological reducing agents to neurotoxic H(2)O(2). J. Biol. Chem. 277, 40302-40308 (Pubitemid 35215603)
10. Dong, J., Atwood, C. S., Anderson, V. E., Siedlak, S. L., Smith, M. A., Perry, G., and Carey, P. R. (2003) Metal binding and oxidation of amyloid-β within isolated senile plaque cores: Raman microscopic evidence. Biochemistry 42, 2768-2773 (Pubitemid 36331519)
11. Liu, G., Huang, W., Moir, R. D., Vanderburg, C. R., Lai, B., Peng, Z., Tanzi, R. E., Rogers, J. T., and Huang, X. (2006) Metal exposure and Alzheimer's pathogenesis. J. Struct. Biol. 155, 45-51
12. Rogers, J. T., Randall, J. D., Cahill, C. M., Eder, P. S., Huang, X., Gunshin, H., Leiter, L., McPhee, J., Sarang, S. S., Utsuki, T., Greig, N. H., Lahiri, D. K., Tanzi, R. E., Bush, A. I., Giordano, T., and Gullans, S. R. (2002) An iron-responsive element type II in the 5′-untranslated region of the Alzheimer's amyloid precursor protein transcript. J. Biol. Chem. 277, 45518-45528
13. Bush, A. I. (2003) The metallobiology of Alzheimer's disease. Trends. Neurosci. 26, 207-214
14. Maynard, C. J., Cappai, R., Volitakis, I., Cherny, R. A., White, A. R., Beyreuther, K., Masters, C. L., Bush, A. I., and Li, Q. X. (2002) Overexpression of Alzheimer's disease amyloid-β opposes the age-dependent elevations of brain copper and iron. J. Biol. Chem. 277, 44670-44676 (Pubitemid 36159056)
15. Colangelo, V., Schurr, J., Ball, M. J., Pelaez, R. P., Bazan, N. G., and Lukiw, W. J. (2002) Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: transcription and neurotrophic factor down-regulation and up-regulation of apoptotic and pro-inflammatory signaling. J. Neurosci. Res. 70, 462-473 (Pubitemid 35222383)
16. Zhang, L. H., Wang, X., Stoltenberg, M., Danscher, G., Huang, L., and Wang, Z. Y. (2008) Abundant expression of zinc transporters in the amyloid plaques of Alzheimer's disease brain. Brain Res. Bull. 77, 55-60
17. Zhang, L. H., Wang, X., Zheng, Z. H., Ren, H., Stoltenberg, M., Danscher, G., Huang, L., Rong, M., and Wang, Z. Y. (2008) Altered expression and distribution of zinc transporters in APP/PS1 transgenic mouse brain. Neurobiol Aging doi:10.1016/j.neurobiolaging. 2008.02.018
18. Ke, Y., and Qian, Z. M. (2007) Brain iron metabolism: neurobiology and neurochemistry. Prog. Neurobiol. 83, 149-173 (Pubitemid 47484044)
19. Phinney, A. L., Drisaldi, B., Schmidt, S. D., Lugowski, S., Coronado, V., Liang, Y., Horne, P., Yang, J., Sekoulidis, J., Coomaraswamy, J., Chishti, M. A., Cox, D. W., Mathews, P. M., Nixon, R. A., Carlson, G. A., St. George-Hyslop, P., and Westaway, D. (2003) In vivo reduction of amyloid-beta by a mutant copper transporter. Proc. Natl. Acad. Sci. U. S. A. 100, 14193-14198
20. Devirgiliis, C., Zalewski, P. D., Perozzi, G., and Murgia, C. (2007) Zinc fluxes and zinc transporter genes in chronic diseases. Mutat. Res. 622, 84-93 (Pubitemid 47211172)
21. Macreadie, I. G. (2008) Copper transport and Alzheimer's disease. Eur. Biophys. J. 37, 295-300
22. Fleming, M. D., Trenor, C. C., 3rd, Su, M. A., Foernzler, D., Beier, D. R., Dietrich, W. F., and Andrews, N. C. (1997) Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat. Genet. 16, 383-386
23. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., and Hediger, M. A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388, 482-488 (Pubitemid 27328927)
24. Li, H., Li, F., Sun, H., and Qian, Z. M. (2003) Membrane-inserted conformation of transmembrane domain 4 of divalent-metal transporter. Biochem. J. 372, 757-766 (Pubitemid 36760389)
25. Tandy, S., Williams, M., Leggett, A., Lopez-Jimenez, M., Dedes, M., Ramesh, B., Srai, S. K., and Sharp, P. (2000) Nramp2 expression is associated with pH-dependent iron uptake across the apical membrane of human intestinal Caco-2 cells. J. Biol. Chem. 275, 1023-1029 (Pubitemid 30051149)
26. Erikson, K. M., and Aschner, M. (2006) Increased manganese uptake by primary astrocyte cultures with altered iron status is mediated primarily by divalent metal transporter. Neurotoxicology 27, 125-130
27. Nevo, Y., and Nelson, N. (2004) The mutation F227I increases the coupling of metal ion transport in DCT1. J. Biol. Chem. 279, 53056-53061 (Pubitemid 40051805)
28. Lee, P. L., Gelbart, T., West, C., Halloran, C., and Beutler, E. (1998) The human Nramp2 gene: characterization of the gene structure, alternative splicing, promoter region and polymorphisms. Blood Cells Mol. Dis. 24, 199-215 (Pubitemid 28365738)
29. Hubert, N., and Hentze, M. W. (2002) Previously uncharacterized isoforms of divalent metal transporter (DMT)-1: implications for regulation and cellular function. Proc. Natl. Acad. Sci. U. S. A. 99, 12345-12350
30. Mackenzie, B., Takanaga, H., Hubert, N., Rolfs, A., and Hediger, M. A. (2007) Functional properties of multiple isoforms of human divalent metal-ion transporter 1 (DMT1). Biochem. J. 403, 59-69 (Pubitemid 46569867)
31. Ke, Y., Chang, Y. Z., Duan, X. L., Du, J. R., Zhu, L., Wang, K., Yang, X. D., Ho, K. P., and Qian, Z. M. (2005) Age-dependent and iron-independent expression of two mRNA isoforms of divalent metal transporter 1 in rat brain. Neurobiol. Aging 26, 739-748 (Pubitemid 40233011)
32. Paradkar, P. N., and Roth, J. A. (2006) Nitric oxide transcriptionally down-regulates specific isoforms of divalent metal transporter (DMT1) via NF-κB. J. Neurochem. 96, 1768-1777
33. Wang, X., Garrick, M. D., Yang, F., Dailey, L. A., Piantadosi, C. A., and Ghio, A. J. (2005) TNF, IFN-γ, and endotoxin increase expression of DMT1 in bronchial epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L24-L33 (Pubitemid 40863551)
34. Wardrop, S. L., and Richardson, D. R. (2000) Interferon- and lipopolysaccharide regulate the expression of Nramp2 and increase the uptake of iron from low relative molecular mass complexes by macrophages. Eur. J. Biochem. 267, 6586-6593
35. Salazar, J., Mena, N., Hunot, S., Prigent, A., Alvarez-Fischer, D., Arredondo, M., Duyckaerts, C., Sazdovitch, V., Zhao, L., Garrick, L. M., Nunez, M. T., Garrick, M. D., Raisman-Vozari, R., and Hirsch, E. C. (2008) Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 105, 18578-18583
36. Jankowsky, J. L., Slunt, H. H., Ratovitski, T., Jenkins, N. A., Copeland, N. G., and Borchelt, D. R. (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 17, 157-165 (Pubitemid 32409891)
37. Zhang, J., Liu, Q., Chen, Q., Liu, N. Q., Li, F. L., Lu, Z. B., Qin, C., Zhu, H., Huang, Y. Y., He, W., and Zhao, B. L. (2006) Nicotine attenuates beta-amyloid-induced neurotoxicity by regulating metal homeostasis. FASEB J. 20, 1212-1214
38. Zhang, J., Mori, A., Chen, Q., and Zhao, B. (2006) Fermented papaya preparation attenuates β-amyloid precursor protein: β-amyloid-mediated copper neurotoxicity in beta-amyloid precursor protein and beta-amyloid precursor protein Swedish mutation overexpressing SH-SY5Y cells. Neuroscience 143, 63-72 (Pubitemid 44667306)
39. Denizot, F., and Lang, R. (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods 89, 271-277 (Pubitemid 16080782)
40. 2+ regulates the cellular iron uptake in K562 cells. Cell Calcium 33, 257-266
41. Burdo, J. R., Martin, J., Menzies, S. L., Dolan, K. G., Romano, M. A., Fletcher, R. J., Garrick, M. D., Garrick, L. M., and Connor, J. R. (1999) Cellular distribution of iron in the brain of the Belgrade rat. Neuroscience 93, 1189-1196 (Pubitemid 29341666)
42. Burdo, J. R., Simpson, I. A., Menzies, S., Beard, J., and Connor, J. R. (2004) Regulation of the profile of iron-management proteins in brain microvasculature. J. Cereb. Blood Flow Metab. 24, 67-74 (Pubitemid 38021270)
43. Burdo, J. R., Menzies, S. L., Simpson, I. A., Garrick, L. M., Garrick, M. D., Dolan, K. G., Haile, D. J., Beard, J. L., and Connor, J. R. (2001) Distribution of divalent metal transporter 1 and metal transport protein 1 in the normal and Belgrade rat. J. Neurosci. Res. 66, 1198-1207
44. Knutson, M., Menzies, S., Connor, J., and Wessling-Resnick, M. (2004) Developmental, regional, and cellular expression of SFT/UbcH5A and DMT1 mRNA in brain. J. Neurosci. Res. 76, 633-641 (Pubitemid 38696916)
45. Huang, E., Ong, W. Y., Go, M. L., and Connor, J. R. (2006) Upregulation of iron regulatory proteins and divalent metal transporter-1 isoforms in the rat hippocampus after kainate induced neuronal injury. Exp. Brain Res. 170, 376-386
46. +)-induced apoptosis in MES23.5 cells. Neurobiol. Aging 32, S12
47. Xu, H. M., Jiang, H., Wang, J., Luo, B., and Xie, J. X. (2008) Over-expressed human divalent metal transporter 1 is involved in iron accumulation in MES23.5 cells. Neurochem. Int. 52, 1044-1051
48. Falangola, M. F., Lee, S. P., Nixon, R. A., Duff, K., and Helpern, J. A. (2005) Histological co-localization of iron in Abeta plaques of PS/APP transgenic mice. Neurochem. Res. 30, 201-205 (Pubitemid 40569203)
49. Jamieson, S. E., White, J. K., Howson, J. M., Pask, R., Smith, A. N., Brayne, C., Evans, J. G., Xuereb, J., Cairns, N. J., Rubinsztein, D. C., and Blackwell, J. M. (2005) Candidate gene association study of solute carrier family 11a members 1 (SLC11A1) and 2 (SLC11A2) genes in Alzheimer's disease. Neurosci. Lett. 374, 124-128 (Pubitemid 40092209)
50. Saavedra, L., Mohamed, A., Ma, V., Kar, S., and de Chaves, E. P. (2007) Internalization of β-amyloid peptide by primary neurons in the absence of apolipoprotein E. J. Biol. Chem. 282, 35722-35732 (Pubitemid 350277136)
51. Rogers, J. T., Bush, A. I., Cho, H. H., Smith, D. H., Thomson, A. M., Friedlich, A. L., Lahiri, D. K., Leedman, P. J., Huang, X., and Cahill, C. M. (2008) Iron and the translation of the amyloid precursor protein (APP) and ferritin mRNAs: riboregulation against neural oxidative damage in Alzheimer's disease. Biochem. Soc. Trans. 36, 1282-1287
52. Bandyopadhyay, S., Hartley, D. M., Cahill, C. M., Lahiri, D. K., Chattopadhyay, N., and Rogers, J. T. (2006) Interleukin-1 stimulates non-amyloidogenic pathway by alpha-secretase (ADAM-10 and ADAM-17) cleavage of APP in human astrocytic cells involving p38 MAP kinase. J. Neurosci. Res. 84, 106-118 (Pubitemid 44023067)
53. Bandyopadhyay, S., Huang, X., Cho, H., Greig, N. H., Youdim, M. B., and Rogers, J. T. (2006) Metal specificity of an ironresponsive element in Alzheimer's APP mRNA 5′untranslated region, tolerance of SH-SY5Y and H4 neural cells to desferrioxamine, clioquinol, VK-28, and a piperazine chelator. J. Neural Transm. Suppl. 71, 237-247
54. Venti, A., Giordano, T., Eder, P., Bush, A. I., Lahiri, D. K., Greig, N. H., and Rogers, J. T. (2004) The integrated role of desferrioxamine and phenserine targeted to an iron-responsive element in the APP-mRNA 5′-untranslated region. Ann. N. Y. Acad. Sci. 1035, 34-48 (Pubitemid 40362325)
55. Andrews, N. C. (1999) The iron transporter DMT1. Int. J. Biochem. Cell Biol. 31, 991-994
56. Conrad, M. E., Umbreit, J. N., Moore, E. G., Hainsworth, L. N., Porubcin, M., Simovich, M. J., Nakada, M. T., Dolan, K., and Garrick, M. D. (2000) Separate pathways for cellular uptake of ferric and ferrous iron. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G767-G774 (Pubitemid 30953716)
57. Bellingham, S. A., Lahiri, D. K., Maloney, B., La Fontaine, S., Multhaup, G., and Camakaris, J. (2004) Copper depletion down-regulates expression of the Alzheimer's disease amyloidbeta precursor protein gene. J. Biol. Chem. 279, 20378-20386 (Pubitemid 38623484)
58. Aracena, P., Aguirre, P., Munoz, P., and Nunez, M. T. (2006) Iron and glutathione at the crossroad of redox metabolism in neurons. Biol. Res. 39, 157-165 (Pubitemid 44027656)
59. Tabner, B. J., El-Agnaf, O. M., Turnbull, S., German, M. J., Paleologou, K. E., Hayashi, Y., Cooper, L. J., Fullwood, N. J., and Allsop, D. (2005) Hydrogen peroxide is generated during the very early stages of aggregation of the amyloid peptides implicated in Alzheimer disease and familial British dementia. J. Biol. Chem. 280, 35789-35792 (Pubitemid 41633844)
60. Lee, J. Y., Friedman, J. E., Angel, I., Kozak, A., and 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 (Pubitemid 39299169)