Characterization of the role of the antioxidant proteins metallothioneins 1 and 2 in an animal model of Alzheimer's disease

Cellular and Molecular Life Sciences

Volumn 69, Issue 21, 2012, Pages 3665-3681

  Manso, Yasmina ^a,b   Carrasco, Javier ^a   Comes, Gemma ^b   Adlard, Paul A ^c   Bush, Ashley I ^c   Hidalgo, Juan ^a,b  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUT DE NEUROCIÈNCIES   (Spain)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Alzheimer' disease; Amyloid plaques; Behavior; Body weight; Gliosis; Metallothionein; Metals; Survival; Tg2576

Indexed keywords

AMYLOID PRECURSOR PROTEIN; METALLOTHIONEIN I; METALLOTHIONEIN II;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN CORTEX; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE MODEL; FEMALE; GENDER; HIPPOCAMPUS; MALE; MORTALITY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; WEIGHT CHANGE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; HUMANS; MALE; METALLOTHIONEIN; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; PEPTIDE FRAGMENTS;

ANIMALIA; MUS;

EID: 84867872169     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1045-y     Document Type: Article

References (83)

1. Andersen K, Launer LJ, Dewey ME, Letenneur L, Ott A, Copeland JR, Dartigues JF, Kragh-Sorensen P, Baldereschi M, Brayne C, Lobo A, Martinez-Lage JM, Stijnen T, Hofman A (1999) Gender differences in the incidence of AD and vascular dementia: the EURODEM Studies. EURODEM Incidence Research Group. Neurology 53:1992-1997
2. Andorn AC, Kalaria RN (2000) Factors affecting pro- and antioxidant properties of fragments of the b-protein precursor (bPP): implication for Alzheimer's disease. J Alzheimers Dis 2:69-78
3. Andrews GK (2000) Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 59:95-104
4. Armario A, Herna'ndez J, Bluethmann H, Hidalgo J (1998) IL-6 deficiency leads to increased emotionality in mice: evidence in transgenic mice carrying a null mutation for IL-6. J Neuroimmunol 92:160-169
5. Atwood CS, Obrenovich ME, Liu T, Chan H, Perry G, Smith MA, Martins RN (2003) Amyloid-beta: a chameleon walking in two worlds: a review of the trophic and toxic properties of amyloid-beta. Brain Res Brain Res Rev. 43:1-16
6. Barnes LL, Wilson RS, Bienias JL, Schneider JA, Evans DA, Bennett DA (2005) Sex differences in the clinical manifestations of Alzheimer disease pathology. Arch Gen Psychiatry 62:685-691
7. Barnham KJ, Masters CL, Bush AI (2004) Neurodegenerative diseases and oxidative stress. Nat Rev Drug Discov 3:205-214
8. Bayer TA, 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 (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
9. Beltramini M, Zambenedetti P, Wittkowski W, Zatta P (2004) Effects of steroid hormones on the Zn, Cu and MTI/II levels in the mouse brain. Brain Res 1013:134-141
10. Bertram L, Lill CM, Tanzi RE (2010) The genetics of Alzheimer disease: back to the future. Neuron 68:270-281
11. Biran Y, Masters CL, Barnham KJ, Bush AI, Adlard PA (2009) Pharmacotherapeutic targets in Alzheimer's disease. J Cell Mol Med 13:61-86
12. Bremner I, Williams RB, Young BW (1981) The effects of age, sex, and zinc status on the accumulation of (copper, zinc)- metallothionein in rat kidneys. J Inorg Biochem 14:135-146
13. Bush AI (2003) The metallobiology of Alzheimer's disease. Trends Neurosci 26:207-214
14. Bush AI, Moir RD, Rosenkrantz KM, Tanzi R (1995) Zinc and Alzheimer's disease-response. Science 268:1921-1923
15. Bush AI, Pettingell WH, Multhaup G, d Paradis M, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE (1994) Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 265:1464-1467
16. Cahill L (2006) Why sex matters for neuroscience. Nat Rev Neurosci 7:477-484
17. Callahan MJ, Lipinski WJ, Bian F, Durham RA, Pack A, Walker LC (2001) Augmented senile plaque load in aged female betaamyloid precursor protein-transgenic mice. Am J Pathol 158:1173-1177
18. Cano-Gauci DF, Sarkar B (1996) Reversible zinc exchange between metallothionein and the estrogen receptor zinc finger. FEBS Lett 386:1-4
19. Carlson GA, Borchelt DR, Dake A, Turner S, Danielson V, Coffin JD, Eckman C, Meiners J, Nilsen SP, Younkin SG, Hsiao KK (1997) Genetic modification of the phenotypes produced by amyloid precursor protein overexpression in transgenic mice. Hum Mol Genet 6:1951-1959
20. Carlson MC, Zandi PP, Plassman BL, Tschanz JT, Welsh-Bohmer KA, Steffens DC, Bastian LA, Mehta KM, Breitner JC, Group CCS (2001) Hormone replacement therapy and reduced cognitive decline in older women: the Cache County Study. Neurology 57:2210-2216
21. Carrasco J, Adlard P, Cotman C, Quintana A, Penkowa M, Xu F, Van Nostrand WE, Hidalgo J (2006) Metallothionein-I and -III expression in animal models of Alzheimer disease. Neuroscience 143:911-922
22. Carroll JC, Rosario ER, Chang L, Stanczyk FZ, Oddo S, LaFerla FM, Pike CJ (2007) Progesterone and estrogen regulate Alzheimer- like neuropathology in female 3xTg-AD mice. J Neurosci 27:13357-13365
23. Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, Oddo S, McGaugh JL, LaFerla FM (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis 28:76-82
24. Crouch PJ, Hung LW, Adlard PA, Cortes M, Lal V, Filiz G, Perez KA, Nurjono M, Caragounis A, Du T, Laughton K, Volitakis I, Bush AI, Li QX, Masters CL, Cappai R, Cherny RA, Donnelly PS, White AR, Barnham KJ (2009) Increasing Cu bioavailability inhibits Abeta oligomers and tau phosphorylation. Proc Natl Acad Sci USA 106:381-386
25. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2:271-276
26. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim Y, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, Tanzi RE, Masters CL, Bush AI (2001) Treatment with a copper- zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30:665-676
27. Chiaverini N, De Ley M (2010) Protective effect of metallothionein on oxidative stress-induced DNA damage. Free Radic Res 44:605-613
28. Chung RS, Howells C, Eaton ED, Shabala L, Zovo K, Palumaa P, Sillard R, Woodhouse A, Bennett WR, Ray S, Vickers JC, West AK (2010) The native copper- and zinc-binding protein metallothionein blocks copper-mediated Abeta aggregation and toxicity in rat cortical neurons. PLoS One 5:e12030
29. Deng Y, Tarassishin L, Kallhoff V, Peethumnongsin E, Wu L, Li YM, Zheng H (2006) Deletion of presenilin 1 hydrophilic loop sequence leads to impaired gamma-secretase activity and exacerbated amyloid pathology. J Neurosci 26:3845-3854
30. Durnam DM, Palmiter RD (1981) Transcriptional regulation of the mouse metallothionein-I gene by heavy metals. J Biol Chem 256:5712-5716
31. Egli D, Yepiskoposyan H, Selvaraj A, Balamurugan K, Rajaram R, Simons A, Multhaup G, Mettler S, Vardanyan A, Georgiev O, Schaffner W (2006) A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol Cell Biol 26:2286-2296
32. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13:432-438
33. Espeland MA, Rapp SR, Shumaker SA, Brunner R, Manson JE, Sherwin BB, Hsia J, Margolis KL, Hogan PE, Wallace R, Dailey M, Freeman R, Hays J, Study WsHIM (2004) Conjugated equine estrogens and global cognitive function in postmenopausal women: Women's Health Initiative Memory Study. JAMA 291:2959-2968
34. File SE (2001) Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125:151-157
35. Guglielmotto M, Giliberto L, Tamagno E, Tabaton M (2010) Oxidative stress mediates the pathogenic effect of different Alzheimer's disease risk factors. Front Aging Neurosci 2:3
36. Günther V, Lindert U, Schaffner W (2012) The taste of heavy metals: gene regulation by MTF-1. Biochim Biophys Acta (in press)
37. Heneka MT, O'Banion MK, Terwel D, Kummer MP (2010) Neuroinflammatory processes in Alzheimer's disease. J. Neural Transm 117:919-947
38. Hidalgo J, Aschner M, Zatta P, Vasa'k M (2001) Roles of the metallothionein family of proteins in the central nervous system. Brain Res Bull 55:133-145
39. Hidalgo J, Giralt M, Garvey JS, Armario A (1987) Sex and restraint stress differences in rat metallothionein and Zn levels. Rev Esp Fisiol 43:427-431
40. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4:97-100
41. Holcomb LA, Gordon MN, Jantzen P, Hsiao K, Duff K, Morgan D (1999) Behavioral changes in transgenic mice expressing both amyloid precursor protein and presenilin-1 mutations: lack of association with amyloid deposits. Behav Genet 29:177-185
42. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102
43. Hua H, Münter L, Harmeier A, Georgiev O, Multhaup G, Schaffner W (2011) Toxicity of Alzheimer's disease-associated Ab peptide is ameliorated in a Drosophila model by tight control of zinc and copper availability. Biol Chem 392:919-926
44. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, Carlson GA (1999) SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neurosci 2:157-161
45. Irie Y, Keung WM (2003) Anti-amyloid beta activity of metallothionein- III is different from its neuronal growth inhibitory activity: structure-activity studies. Brain Res 960:228-234
46. Ittner LM, Götz J (2011) Amyloid-b and tau - a toxic pas de deux in Alzheimer's disease. Nat Rev Neurosci 12:65-72
47. Kim J, Onstead L, Randle S, Price R, Smithson L, Zwizinski C, Dickson DW, Golde T, McGowan E (2007) Abeta40 inhibits amyloid deposition in vivo. J Neurosci 27:627-633
48. Kim JH, Nam YP, Jeon SM, Han HS, Suk K (2012) Amyloid neurotoxicity is attenuated by metallothionein: dual mechanisms at work. J Neurochem 121:751-762
49. King DL, Arendash GW (2002) Behavioral characterization of the Tg2576 transgenic model of Alzheimer's disease through 19 months. Physiol Behav 75:627-642
50. King DL, Arendash GW, Crawford F, Sterk T, Menendez J, Mullan MJ (1999) Progressive and gender-dependent cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer's disease. Behav Brain Res 103:145-162
51. Kovacs EJ, Messingham KA, Gregory MS (2002) Estrogen regulation of immune responses after injury. Mol Cell Endocrinol 193:129-135
52. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, Debulpaep M, Vandersteen A, Segers-Nolten I, Van Der Werf K, Subramaniam V, Braeken D, Callewaert G, Bartic C, D'Hooge R, Martins IC, Rousseau F, Schymkowitz J, De Strooper B (2010) Neurotoxicity of Alzheimer's disease Ab peptides is induced by small changes in the Ab42 to Ab40 ratio. EMBO J 29:3408-3420
53. Lee DK, Carrasco J, Hidalgo J, Andrews GK (1999) Identification of a signal transducer and activator of transcription (STAT) binding site in the mouse metallothionein-I promoter involved in interleukin-6-induced gene expression. Biochem J 337:59-65
54. Lee JY, Cole TB, Palmiter RD, Suh SW, Koh JY (2002) Contribution by synaptic zinc to the gender-disparate plaque formation in human Swedish mutant APP transgenic mice. Proc Natl Acad Sci USA 99:7705-7710
55. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357
56. Lindeque JZ, Levanets O, Louw R, van der Westhuizen FH (2010) The involvement of metallothioneins in mitochondrial function and disease. Curr Protein Pept Sci 11:292-309
57. Manso Y, Adlard PA, Carrasco J, Vasa'k M, Hidalgo J (2011) Metallothionein and brain inflammation. J Biol Inorg Chem 16:1103-1113
58. Manso Y, Serra M, Comes G, Giralt M, Carrasco J, Cols N, Vasa'k M, Gonza'lez-Duarte P, Hidalgo J (2010) The comparison of mouse full metallothionein-1 versus alpha and beta domains and metallothionein-1-to-3 mutation following traumatic brain injury reveals different biological motifs. J Neurosci Res 88:1708-1718
59. Martinho A, Gonçalves I, Cardoso I, Almeida MR, Quintela T, Saraiva MJ, Santos CR (2010) Human metallothioneins 2 and 3 differentially affect amyloid-beta binding by transthyretin. FEBS J 277:3427-3436
60. Masters BA, Kelly EJ, Quaife CJ, Brinster RL, Palmiter RD (1994) Targeted disruption of metallothionein I and II genes increases sensitivity to cadmium. Proc Natl Acad Sci USA 91:584-588
61. Ono S, Koropatnick DJ, Cherian MG (1997) Regional brain distribution of metallothionein, zinc and copper in toxic milk mutant and transgenic mice. Toxicology 124:1-10
62. Palmiter RD, Findley SD, Whitmore TE, Durnam DM (1992) MT-III, a brain-specific member of the metallothionein gene family. Proc Natl Acad Sci USA 89:6333-6337
63. Penkowa M, Carrasco J, Giralt M, Moos T, Hidalgo J (1999) CNS wound healing is severely depressed in metallothionein I- and II-deficient mice. J Neurosci 19:2535-2545
64. Penkowa M, Moos T, Carrasco J, Hadberg H, Molinero A, Bluethmann H, Hidalgo J (1999) Strongly compromised inflammatory response to brain injury in interleukin-6-deficient mice. Glia 25:343-357
65. Phinney AL, Drisaldi B, Schmidt SD, Lugowski S, Coronado V, Liang Y, Horne P, Yang J, Sekoulidis J, Coomaraswamy J, Chishti MA, Cox DW, Mathews PM, Nixon RA, Carlson GA, St George-Hyslop P, Westaway D (2003) In vivo reduction of amyloid-beta by a mutant copper transporter. Proc Natl Acad Sci USA 100:14193-14198
66. Pugh PL, Richardson JC, Bate ST, Upton N, Sunter D (2007) Non-cognitive behaviours in an APP/PS1 transgenic model of Alzheimer's disease. Behav Brain Res 178:18-28
67. Quaife CJ, Findley SD, Erickson JC, Froelick GJ, Kelly EJ, Zambrowicz BP, Palmiter RD (1994) Induction of a new metallothionein isoform (MT-IV) occurs during differentiation of stratified squamous epithelia. Biochemistry 33:7250-7259
68. Rosario ER, Carroll J, Pike CJ (2010) Testosterone regulation of Alzheimer-like neuropathology in male 3xTg-AD mice involves both estrogen and androgen pathways. Brain Res 1359:281-290
69. Sato M, Bremner I (1993) Oxygen free radicals and metallothionein. Free Rad Biol Med 14:325-337
70. Schäfer S, Pajonk FG, Multhaup G, Bayer TA (2007) Copper and clioquinol treatment in young APP transgenic and wild-type mice: effects on life expectancy, body weight, and metal-ion levels. J Mol Med (Berl) 85:405-413
71. Schwarzman AL, Gregori L, Vitek MP, Lyubski S, Strittmatter WJ, Enghilde JJ, Bhasin R, Silverman J, Weisgraber KH, Coyle PK, Zagorski MG, Talafous J, Eisenberg M, Saunders AM, Roses AD, Goldgaber D (1994) Transthyretin sequesters amyloid beta protein and prevents amyloid formation. Proc Natl Acad Sci USA 91:8368-8372
72. Sinforiani E, Citterio A, Zucchella C, Bono G, Corbetta S, Merlo P, Mauri M (2010) Impact of gender differences on the outcome of Alzheimer's disease. Dement Geriatr Cogn Disord 30:147-154
73. Sultana R, Butterfield DA (2010) Role of oxidative stress in the progression of Alzheimer's disease. J Alzheimers Dis 19:341-353
74. Toda T, Noda Y, Ito G, Maeda M, Shimizu T (2011) Presenilin-2 mutation causes early amyloid accumulation and memory impairment in a transgenic mouse model of Alzheimer's disease. J Biomed Biotechnol 2011:617974
75. Vasa'k M, Meloni G (2011) Chemistry and biology of mammalian metallothioneins. J Biol Inorg Chem 16:1067-1078
76. Vest RS, Pike CJ (2012) Gender, sex steroid hormones, and Alzheimer's disease. Horm Behav (in press)
77. Waelput W, Broekaert D, Vandekerckhove J, Brouckaert P, Tavernier J, Libert C (2001) A mediator role for metallothionein in tumor necrosis factor-induced lethal shock. J Exp Med 194:1617-1624
78. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-539
79. West AK, Hidalgo J, Eddins D, Levin ED, Aschner M (2008) Metallothionein in the central nervous system: roles in protection, regeneration and cognition. Neurotoxicology 29:489-503
80. West AK, Leung JY, Chung RS (2011) Neuroprotection and regeneration by extracellular metallothionein via lipoprotein- receptor-related proteins. J Biol Inorg Chem 1115-1122
81. Widyarini S, Domanski D, Painter N, Reeve VE (2006) Estrogen receptor signaling protects against immune suppression by UV radiation exposure. Proc Natl Acad Sci USA 103:12837-12842
82. Yang X, Doser TA, Fang CX, Nunn JM, Janardhanan R, Zhu M, Sreejayan N, Quinn MT, Ren J (2006) Metallothionein prolongs survival and antagonizes senescence-associated cardiomyocyte diastolic dysfunction: role of oxidative stress. FASEB J 20:1024-1026
83. Zeitoun-Ghandour S, Leszczyszyn OI, Blindauer CA, Geier FM, Bundy JG, Stu;rzenbaum SR (2011) C. elegans metallothioneins: response to and defence against ROS toxicity. Mol Biosyst 7:2397-2406