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Redox active metals in neurodegenerative diseases

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Abstract

Copper (Cu) and iron (Fe) are redox active metals essential for the regulation of cellular pathways that are fundamental for brain function, including neurotransmitter synthesis and release, neurotransmission, and protein turnover. Cu and Fe are tightly regulated by sophisticated homeostatic systems that tune the levels and localization of these redox active metals. The regulation of Cu and Fe necessitates their coordination to small organic molecules and metal chaperone proteins that restrict their reactions to specific protein centres, where Cu and Fe cycle between reduced (Fe2+, Cu+) and oxidised states (Fe3+, Cu2+). Perturbation of this regulation is evident in the brain affected by neurodegeneration. Here we review the evidence that links Cu and Fe dyshomeostasis to neurodegeneration as well as the promising preclinical and clinical studies reporting pharmacological intervention to remedy Cu and Fe abnormalities in the treatment of Alzheimer’s disease (AD), Parkinson’s disease (PD) and Amyotrophic lateral sclerosis (ALS).

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Abbreviations

AD:

Alzheimer’s disease

APP:

Amyloid precursor protein

ALS:

Amyotrophic lateral sclerosis

ATOX-1:

Antioxidant 1 copper chaperone 1

BBB:

Blood–brain-barrier

BCB:

Blood–cerebrospinal fluid barrier

BCECs:

Brain capillary endothelial cells

CNS:

Central nervous system

CSF:

Cerebrospinal fluid

CP:

Ceruloplasmin

CQ:

Clioquinol

CTR1:

Copper-transporter 1

CCS:

Copper chaperone for SOD1

COX17:

Cytochrome c oxidase copper chaperone

DMT1:

Divalent metal transporter 1

DFP:

Deferiprone

GSH:

Glutathione

6-OHDA:

6-Hydroxydopamine

IRE:

Iron-responsive element

IRPs:

Iron regulatory proteins

LB:

Lewy bodies

L-DOPA:

l-3,4-Dihydroxyphenylalanine

MRI:

Magnetic resonance image

NFTs:

Neurofibrillary tangles

PD:

Parkinson’s disease

ROS:

Reactive oxygen species

SNc:

Substantia nigra pars compacta

SOD1:

Superoxide dismutase 1

Tf:

Transferrin

TfR1:

Transferrin receptor 1

UTR:

Untranslated region

References

  1. Halliwell B (2006) J Neurochem 97:1634–1658

    Article  CAS  PubMed  Google Scholar 

  2. Butterfield DA, Halliwell B (2019) Nat Rev Neurosci 20:148–160

    Article  CAS  PubMed  Google Scholar 

  3. Bush AI (2003) Trends Neurosci 26:207–214

    Article  CAS  PubMed  Google Scholar 

  4. Gaier ED, Eipper BA, Mains RE (2013) J Neurosci Res 91:2–19

    CAS  PubMed  Google Scholar 

  5. Belaidi AA, Bush AI (2016) J Neurochem 139(Suppl 1):179–197

    Article  CAS  PubMed  Google Scholar 

  6. Opazo CM, Greenough MA, Bush AI (2014) Front Aging Neurosci 6:143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Stockwell BR, Friedmann Angeli JP, Bayir H, Bush AI, Conrad M, Dixon SJ, Fulda S, Gascon S, Hatzios SK, Kagan VE, Noel K, Jiang X, Linkermann A, Murphy ME, Overholtzer M, Oyagi A, Pagnussat GC, Park J, Ran Q, Rosenfeld CS, Salnikow K, Tang D, Torti FM, Torti SV, Toyokuni S, Woerpel KA (2017) Cell 171:273–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Angelova DF, Brown DR (2015) Metals 5:2070–2092

    Article  CAS  Google Scholar 

  9. Choi BS, Zheng W (2009) Brain Res 1248:14–21

    Article  CAS  PubMed  Google Scholar 

  10. Meyer LA, Durley AP, Prohaska JR, Harris ZL (2001) J Biol Chem 276:36857–36861

    Article  CAS  PubMed  Google Scholar 

  11. Maryon EB, Molloy SA, Kaplan JH (2013) Am J Physiol Cell Physiol 304:C768–C779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tapia L, Gonzalez-Aguero M, Cisternas MF, Suazo M, Cambiazo V, Uauy R, Gonzalez M (2004) Biochem J 378:617–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. La Fontaine S, Mercer JF (2007) Arch Biochem Biophys 463:149–167

    Article  PubMed  CAS  Google Scholar 

  14. Linz R, Lutsenko S (2007) J Bioenerg Biomembr 39:403–407

    Article  CAS  PubMed  Google Scholar 

  15. Greenough M, Pase L, Voskoboinik I, Petris MJ, O’Brien AW, Camakaris J (2004) Am J Physiol Cell Physiol 287:C1463–C1471

    Article  CAS  PubMed  Google Scholar 

  16. Pase L, Voskoboinik I, Greenough M, Camakaris J (2004) Biochem J 378:1031–1037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ohgami RS, Campagna DR, Greer EL, Antiochos B, McDonald A, Chen J, Sharp JJ, Fujiwara Y, Barker JE, Fleming MD (2005) Nat Genet 37:1264–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Moos T, Morgan EH (2004) J Neurochem 88:233–245

    Article  CAS  PubMed  Google Scholar 

  19. Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) Lancet Neurol 13:1045–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Pinilla-Tenas JJ, Sparkman BK, Shawki A, Illing AC, Mitchell CJ, Zhao N, Liuzzi JP, Cousins RJ, Knutson MD, Mackenzie B (2011) Am J Physiol Cell Physiol 301:C862–C871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wang CY, Jenkitkasemwong S, Duarte S, Sparkman BK, Shawki A, Mackenzie B, Knutson MD (2012) J Biol Chem 287:34032–34043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhao N, Gao J, Enns CA, Knutson MD (2010) J Biol Chem 285:32141–32150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Nature 388:482–488

    Article  CAS  PubMed  Google Scholar 

  24. Ji C, Kosman DJ (2015) J Neurochem 133:668–683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Frey AG, Nandal A, Park JH, Smith PM, Yabe T, Ryu MS, Ghosh MC, Lee J, Rouault TA, Park MH, Philpott CC (2014) Proc Natl Acad Sci USA 111:8031–8036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Leidgens S, Bullough KZ, Shi H, Li F, Shakoury-Elizeh M, Yabe T, Subramanian P, Hsu E, Natarajan N, Nandal A, Stemmler TL, Philpott CC (2013) J Biol Chem 288:17791–17802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nandal A, Ruiz JC, Subramanian P, Ghimire-Rijal S, Sinnamon RA, Stemmler TL, Bruick RK, Philpott CC (2011) Cell Metab 14:647–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Pantopoulos K (2004) Ann N Y Acad Sci 1012:1–13

    Article  CAS  PubMed  Google Scholar 

  29. Zhang DL, Ghosh MC, Rouault TA (2014) Front Pharmacol 5:124

    PubMed  PubMed Central  Google Scholar 

  30. Double KL, Gerlach M, Schunemann V, Trautwein AX, Zecca L, Gallorini M, Youdim MB, Riederer P, Ben-Shachar D (2003) Biochem Pharmacol 66:489–494

    Article  CAS  PubMed  Google Scholar 

  31. Asano T, Komatsu M, Yamaguchi-Iwai Y, Ishikawa F, Mizushima N, Iwai K (2011) Mol Cell Biol 31:2040–2052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Nitti M, Piras S, Brondolo L, Marinari UM, Pronzato MA, Furfaro AL (2018) Int J Mol Sci 19:2260–2280

    Article  PubMed Central  CAS  Google Scholar 

  33. Zhang YW, Thompson R, Zhang H, Xu H (2011) Mol Brain 4:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Unzeta M, Esteban G, Bolea I, Fogel WA, Ramsay RR, Youdim MB, Tipton KF, Marco-Contelles J (2016) Front Neurosci 10:205

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wimo A, Jonsson L, Bond J, Prince M, Winblad B, I. Alzheimer Disease (2013) Alzheimers Dement 9:1–11

    Article  PubMed  Google Scholar 

  36. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Brain Res Brain Res Rev 33:95–130

    Article  CAS  PubMed  Google Scholar 

  37. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Proc Natl Acad Sci USA 82:4245–4249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Davies P, Maloney AJ (1976) Lancet 2:1403

    Article  CAS  PubMed  Google Scholar 

  39. Drachman DA, Leavitt J (1974) Arch Neurol 30:113–121

    Article  CAS  PubMed  Google Scholar 

  40. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Science 215:1237–1239

    Article  CAS  PubMed  Google Scholar 

  41. Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR (1998) J Neurol Sci 158:47–52

    Article  CAS  PubMed  Google Scholar 

  42. Pithadia AS, Lim MH (2012) Curr Opin Chem Biol 16:67–73

    Article  CAS  PubMed  Google Scholar 

  43. Raven EP, Lu PH, Tishler TA, Heydari P, Bartzokis G (2013) J Alzheimers Dis 37:127–136

    Article  CAS  PubMed  Google Scholar 

  44. Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, Carey PR (2003) Biochemistry 42:2768–2773

    Article  CAS  PubMed  Google Scholar 

  45. Miller LM, Wang Q, Telivala TP, Smith RJ, Lanzirotti A, Miklossy J (2006) J Struct Biol 155:30–37

    Article  CAS  PubMed  Google Scholar 

  46. Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, Smith MA (2000) J Neurochem 74:270–279

    Article  CAS  PubMed  Google Scholar 

  47. Smith MA, Harris PL, Sayre LM, Perry G (1997) Proc Natl Acad Sci USA 94:9866–9868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Deibel MA, Ehmann WD, Markesbery WR (1996) J Neurol Sci 143:137–142

    Article  CAS  PubMed  Google Scholar 

  49. Zatta P, Drago D, Bolognin S, Sensi SL (2009) Trends Pharmacol Sci 30:346–355

    Article  CAS  PubMed  Google Scholar 

  50. Bishop GM, Robinson SR, Liu Q, Perry G, Atwood CS, Smith MA (2002) Dev Neurosci 24:184–187

    Article  CAS  PubMed  Google Scholar 

  51. Roberts BR, Ryan TM, Bush AI, Masters CL, Duce JA (2012) J Neurochem 120(Suppl 1):149–166

    Article  CAS  PubMed  Google Scholar 

  52. Schrag M, Mueller C, Oyoyo U, Smith MA, Kirsch WM (2011) Prog Neurobiol 94:296–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Schrag M, Mueller C, Zabel M, Crofton A, Kirsch WM, Ghribi O, Squitti R, Perry G (2013) Neurobiol Dis 59:100–110

    Article  CAS  PubMed  Google Scholar 

  54. Ayton S, James SA, Bush AI (2017) Cell Chem Biol 24:1192–1194

    Article  CAS  PubMed  Google Scholar 

  55. Hwang EJ, Kim HG, Kim D, Rhee HY, Ryu CW, Liu T, Wang Y, Jahng GH (2016) Med Phys 43:4718

    Article  PubMed  Google Scholar 

  56. Luo Z, Zhuang X, Kumar D, Wu X, Yue C, Han C, Lv J (2013) PLoS One 8:e76203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Connor JR, Menzies SL, St Martin SM, Mufson EJ (1992) J Neurosci Res 31:75–83

    Article  CAS  PubMed  Google Scholar 

  58. Meadowcroft MD, Connor JR, Smith MB, Yang QX (2009) J Magn Reson Imaging 29:997–1007

    Article  PubMed  PubMed Central  Google Scholar 

  59. Valensin D, Migliorini C, Valensin G, Gaggelli E, La Penna G, Kozlowski H, Gabbiani C, Messori L (2011) Inorg Chem 50:6865–6867

    Article  CAS  PubMed  Google Scholar 

  60. Dikalov SI, Vitek MP, Mason RP (2004) Free Radic Biol Med 36:340–347

    Article  CAS  PubMed  Google Scholar 

  61. Guilloreau L, Combalbert S, Sournia-Saquet A, Mazarguil H, Faller P (2007) ChemBioChem 8:1317–1325

    Article  CAS  PubMed  Google Scholar 

  62. Nadal RC, Rigby SE, Viles JH (2008) Biochemistry 47:11653–11664

    Article  CAS  PubMed  Google Scholar 

  63. Nakamura M, Shishido N, Nunomura A, Smith MA, Perry G, Hayashi Y, Nakayama K, Hayashi T (2007) Biochemistry 46:12737–12743

    Article  CAS  PubMed  Google Scholar 

  64. Reybier K, Ayala S, Alies B, Rodrigues JV, Bustos Rodriguez S, La Penna G, Collin F, Gomes CM, Hureau C, Faller P (2016) Angew Chem Int Ed Engl 55:1085–1089

    Article  CAS  PubMed  Google Scholar 

  65. Taniguchi A, Sasaki D, Shiohara A, Iwatsubo T, Tomita T, Sohma Y, Kanai M (2014) Angew Chem Int Ed Engl 53:1382–1385

    Article  CAS  PubMed  Google Scholar 

  66. Cheignon C, Faller P, Testemale D, Hureau C, Collin F (2016) Metallomics 8:1081–1089

    Article  CAS  PubMed  Google Scholar 

  67. Butterfield DA, Reed T, Newman SF, Sultana R (2007) Free Radic Biol Med 43:658–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Selfridge JE, Lezi E, Lu J, Swerdlow RH (2013) Neurobiol Dis 51:3–12

    Article  CAS  PubMed  Google Scholar 

  69. Zhao Y, Zhao B (2013) Oxid Med Cell Longev 2013:316523

    PubMed  PubMed Central  Google Scholar 

  70. Gabbita SP, Lovell MA, Markesbery WR (1998) J Neurochem 71:2034–2040

    Article  CAS  PubMed  Google Scholar 

  71. Hardas SS, Sultana R, Clark AM, Beckett TL, Szweda LI, Murphy MP, Butterfield DA (2013) Redox Biol 1:80–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Markesbery WR, Lovell MA (1998) Neurobiol Aging 19:33–36

    Article  CAS  PubMed  Google Scholar 

  73. Mecocci P, MacGarvey U, Beal MF (1994) Ann Neurol 36:747–751

    Article  CAS  PubMed  Google Scholar 

  74. Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) J Neurochem 68:2092–2097

    Article  CAS  PubMed  Google Scholar 

  75. Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI (2000) J Neurochem 75:1219–1233

    Article  CAS  PubMed  Google Scholar 

  76. Barritt JD, Viles JH (2015) J Biol Chem 290:27791–27802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Drew SC (2017) Front Neurosci 11:317

    Article  PubMed  PubMed Central  Google Scholar 

  78. Mital M, Wezynfeld NE, Fraczyk T, Wiloch MZ, Wawrzyniak UE, Bonna A, Tumpach C, Barnham KJ, Haigh CL, Bal W, Drew SC (2015) Angew Chem Int Ed Engl 54:10460–10464

    Article  CAS  PubMed  Google Scholar 

  79. Sarell CJ, Syme CD, Rigby SE, Viles JH (2009) Biochemistry 48:4388–4402

    Article  CAS  PubMed  Google Scholar 

  80. Huang X, Atwood CS, Moir RD, Hartshorn MA, Tanzi RE, Bush AI (2004) J Biol Inorg Chem 9:954–960

    Article  CAS  PubMed  Google Scholar 

  81. Dai XL, Sun YX, Jiang ZF (2006) Acta Biochim Biophys Sin (Shanghai) 38:765–772

    Article  CAS  Google Scholar 

  82. Sarell CJ, Wilkinson SR, Viles JH (2010) J Biol Chem 285:41533–41540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Greenough MA, Camakaris J, Bush AI (2013) Neurochem Int 62:540–555

    Article  CAS  PubMed  Google Scholar 

  84. Grundke-Iqbal I, Fleming J, Tung YC, Lassmann H, Iqbal K, Joshi JG (1990) Acta Neuropathol 81:105–110

    Article  CAS  PubMed  Google Scholar 

  85. Quintana C, Bellefqih S, Laval JY, Guerquin-Kern JL, Wu TD, Avila J, Ferrer I, Arranz R, Patino C (2006) J Struct Biol 153:42–54

    Article  CAS  PubMed  Google Scholar 

  86. Bolognin S, Messori L, Drago D, Gabbiani C, Cendron L, Zatta P (2011) Int J Biochem Cell Biol 43:877–885

    Article  CAS  PubMed  Google Scholar 

  87. Liu B, Moloney A, Meehan S, Morris K, Thomas SE, Serpell LC, Hider R, Marciniak SJ, Lomas DA, Crowther DC (2011) J Biol Chem 286:4248–4256

    Article  CAS  PubMed  Google Scholar 

  88. Ma Q, Li Y, Du J, Liu H, Kanazawa K, Nemoto T, Nakanishi H, Zhao Y (2006) Peptides 27:841–849

    Article  CAS  PubMed  Google Scholar 

  89. Ma QF, Li YM, Du JT, Kanazawa K, Nemoto T, Nakanishi H, Zhao YF (2005) Biopolymers 79:74–85

    Article  CAS  PubMed  Google Scholar 

  90. Martic S, Rains MK, Kraatz HB (2013) Anal Biochem 442:130–137

    Article  CAS  PubMed  Google Scholar 

  91. Soragni A, Zambelli B, Mukrasch MD, Biernat J, Jeganathan S, Griesinger C, Ciurli S, Mandelkow E, Zweckstetter M (2008) Biochemistry 47:10841–10851

    Article  CAS  PubMed  Google Scholar 

  92. Kitazawa M, Cheng D, Laferla FM (2009) J Neurochem 108:1550–1560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Voss K, Harris C, Ralle M, Duffy M, Murchison C, Quinn JF (2014) Transl Neurodegener 3:24

    Article  PubMed  PubMed Central  Google Scholar 

  94. Faller P, Hureau C (2009) Dalton Trans. https://doi.org/10.1039/b813398k:1080-1094

    Article  PubMed  Google Scholar 

  95. Hesse L, Beher D, Masters CL, Multhaup G (1994) FEBS Lett 349:109–116

    Article  CAS  PubMed  Google Scholar 

  96. Bush AI, Multhaup G, Moir RD, Williamson TG, Small DH, Rumble B, Pollwein P, Beyreuther K, Masters CL (1993) J Biol Chem 268:16109–16112

    CAS  PubMed  Google Scholar 

  97. Miller Y, Ma B, Nussinov R (2010) Proc Natl Acad Sci USA 107:9490–9495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Treiber C, Simons A, Strauss M, Hafner M, Cappai R, Bayer TA, Multhaup G (2004) J Biol Chem 279:51958–51964

    Article  CAS  PubMed  Google Scholar 

  99. Maynard CJ, Cappai R, Volitakis I, Cherny RA, White AR, Beyreuther K, Masters CL, Bush AI, Li QX (2002) J Biol Chem 277:44670–44676

    Article  CAS  PubMed  Google Scholar 

  100. Bellingham SA, Ciccotosto GD, Needham BE, Fodero LR, White AR, Masters CL, Cappai R, Camakaris J (2004) J Neurochem 91:423–428

    Article  CAS  PubMed  Google Scholar 

  101. Duce JA, Tsatsanis A, Cater MA, James SA, Robb E, Wikhe K, Leong SL, Perez K, Johanssen T, Greenough MA, Cho HH, Galatis D, Moir RD, Masters CL, McLean C, Tanzi RE, Cappai R, Barnham KJ, Ciccotosto GD, Rogers JT, Bush AI (2010) Cell 142:857–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wong BX, Tsatsanis A, Lim LQ, Adlard PA, Bush AI, Duce JA (2014) PLoS One 9:e114174

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Cho HH, Cahill CM, Vanderburg CR, Scherzer CR, Wang B, Huang X, Rogers JT (2010) J Biol Chem 285:31217–31232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Rogers JT, Randall JD, Cahill CM, Eder PS, Huang X, Gunshin H, Leiter L, McPhee J, Sarang SS, Utsuki T, Greig NH, Lahiri DK, Tanzi RE, Bush AI, Giordano T, Gullans SR (2002) J Biol Chem 277:45518–45528

    Article  CAS  PubMed  Google Scholar 

  105. Acevedo KM, Hung YH, Dalziel AH, Li QX, Laughton K, Wikhe K, Rembach A, Roberts B, Masters CL, Bush AI, Camakaris J (2011) J Biol Chem 286:8252–8262

    Article  CAS  PubMed  Google Scholar 

  106. Hou P, Liu G, Zhao Y, Shi Z, Zheng Q, Bu G, Xu H, Zhang YW (2015) Neurobiol Aging 36:1310–1315

    Article  CAS  PubMed  Google Scholar 

  107. Noda Y, Asada M, Kubota M, Maesako M, Watanabe K, Uemura M, Kihara T, Shimohama S, Takahashi R, Kinoshita A, Uemura K (2013) Neurosci Lett 547:10–15

    Article  CAS  PubMed  Google Scholar 

  108. Gerber H, Wu F, Dimitrov M, Osuna GM, Fraering PC (2017) J Biol Chem 292:3751–3767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G (1999) Biochem J 344(Pt 2):461–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Bayer TA, Schafer S, Simons A, Kemmling A, Kamer T, Tepest R, Eckert A, Schussel K, Eikenberg O, Sturchler-Pierrat C, Abramowski D, Staufenbiel M, Multhaup G (2003) Proc Natl Acad Sci USA 100:14187–14192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Hardy JA, Higgins GA (1992) Science 256:184–185

    Article  CAS  PubMed  Google Scholar 

  112. Masaldan S, Belaidi AA, Ayton S, Bush AI (2019) Pharmaceuticals (Basel) 12:93

    Article  Google Scholar 

  113. Nikseresht S, Bush AI, Ayton S (2019) Br J Pharmacol 176:3622–3635

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Li C, Wang J, Zhou B (2010) J Alzheimers Dis 21:1249–1262

    Article  CAS  PubMed  Google Scholar 

  115. 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) Neuron 30:665–676

    Article  CAS  PubMed  Google Scholar 

  116. Grossi C, Francese S, Casini A, Rosi MC, Luccarini I, Fiorentini A, Gabbiani C, Messori L, Moneti G, Casamenti F (2009) J Alzheimers Dis 17:423–440

    Article  CAS  PubMed  Google Scholar 

  117. LeVine H 3rd, Ding Q, Walker JA, Voss RS, Augelli-Szafran CE (2009) Neurosci Lett 465:99–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Mancino AM, Hindo SS, Kochi A, Lim MH (2009) Inorg Chem 48:9596–9598

    Article  CAS  PubMed  Google Scholar 

  119. Ritchie CW, Bush AI, Mackinnon A, Macfarlane S, Mastwyk M, MacGregor L, Kiers L, Cherny R, Li QX, Tammer A, Carrington D, Mavros C, Volitakis I, Xilinas M, Ames D, Davis S, Beyreuther K, Tanzi RE, Masters CL (2003) Arch Neurol 60:1685–1691

    Article  PubMed  Google Scholar 

  120. Adlard PA, Cherny RA, Finkelstein DI, Gautier E, Robb E, Cortes M, Volitakis I, Liu X, Smith JP, Perez K, Laughton K, Li QX, Charman SA, Nicolazzo JA, Wilkins S, Deleva K, Lynch T, Kok G, Ritchie CW, Tanzi RE, Cappai R, Masters CL, Barnham KJ, Bush AI (2008) Neuron 59:43–55

    Article  CAS  PubMed  Google Scholar 

  121. Faux NG, Ritchie CW, Gunn A, Rembach A, Tsatsanis A, Bedo J, Harrison J, Lannfelt L, Blennow K, Zetterberg H, Ingelsson M, Masters CL, Tanzi RE, Cummings JL, Herd CM, Bush AI (2010) J Alzheimers Dis 20:509–516

    Article  CAS  PubMed  Google Scholar 

  122. Lannfelt L, Blennow K, Zetterberg H, Batsman S, Ames D, Harrison J, Masters CL, Targum S, Bush AI, Murdoch R, Wilson J, Ritchie CW, PES Group (2008) Lancet Neurol 7:779–786

    Article  CAS  PubMed  Google Scholar 

  123. Villemagne VL, Rowe CC, Barnham KJ, Cherny R, Woodward M, Bozinosvski S, Salvado O, Bourgeat P, Perez K, Fowler C, Rembach A, Maruff P, Ritchie C, Tanzi R, Masters CL (2017) Alzheimers Dement (N Y) 3:622–635

    Google Scholar 

  124. Bica L, Liddell JR, Donnelly PS, Duncan C, Caragounis A, Volitakis I, Paterson BM, Cappai R, Grubman A, Camakaris J, Crouch PJ, White AR (2014) PLoS One 9:e90070

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  125. 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) Proc Natl Acad Sci USA 106:381–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Donnelly PS, Caragounis A, Du T, Laughton KM, Volitakis I, Cherny RA, Sharples RA, Hill AF, Li QX, Masters CL, Barnham KJ, White AR (2008) J Biol Chem 283:4568–4577

    Article  CAS  PubMed  Google Scholar 

  127. Crapper McLachlan DR, Dalton AJ, Kruck TP, Bell MY, Smith WL, Kalow W, Andrews DF (1991) Lancet 337:1304–1308

    Article  CAS  PubMed  Google Scholar 

  128. Hanson LR, Fine JM, Renner DB, Svitak AL, Burns RB, Nguyen TM, Tuttle NJ, Marti DL, Panter SS, Frey WH 2nd (2012) Drug Deliv Transl Res 2:160–168

    Article  CAS  PubMed  Google Scholar 

  129. Guo C, Wang P, Zhong ML, Wang T, Huang XS, Li JY, Wang ZY (2013) Neurochem Int 62:165–172

    Article  CAS  PubMed  Google Scholar 

  130. Banerjee P, Sahoo A, Anand S, Bir A, Chakrabarti S (2016) J Alzheimers Dis 49:681–693

    Article  CAS  PubMed  Google Scholar 

  131. Kupershmidt L, Amit T, Bar-Am O, Youdim MB, Weinreb O (2012) Antioxid Redox Signal 17:860–877

    Article  CAS  PubMed  Google Scholar 

  132. Molina-Holgado F, Gaeta A, Francis PT, Williams RJ, Hider RC (2008) J Neurochem 105:2466–2476

    Article  CAS  PubMed  Google Scholar 

  133. Prasanthi JR, Schrag M, Dasari B, Marwarha G, Dickson A, Kirsch WM, Ghribi O (2012) J Alzheimers Dis 30:167–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Lang AE, Lozano AM (1998) N Engl J Med 339:1130–1143

    Article  CAS  PubMed  Google Scholar 

  135. Jankovic J (2008) J Neurol Neurosurg Psychiatry 79:368–376

    Article  CAS  PubMed  Google Scholar 

  136. Schulz JB (2008) J Neurol 255(Suppl 5):3–7

    Article  CAS  PubMed  Google Scholar 

  137. Hozumi I, Hasegawa T, Honda A, Ozawa K, Hayashi Y, Hashimoto K, Yamada M, Koumura A, Sakurai T, Kimura A, Tanaka Y, Satoh M, Inuzuka T (2011) J Neurol Sci 303:95–99

    Article  CAS  PubMed  Google Scholar 

  138. Pall HS, Williams AC, Blake DR, Lunec J, Gutteridge JM, Hall M, Taylor A (1987) Lancet 2:238–241

    Article  CAS  PubMed  Google Scholar 

  139. Arnal N, Cristalli DO, de Alaniz MJ, Marra CA (2010) Brain Res 1319:118–130

    Article  CAS  PubMed  Google Scholar 

  140. Davies KM, Bohic S, Carmona A, Ortega R, Cottam V, Hare DJ, Finberg JP, Reyes S, Halliday GM, Mercer JF, Double KL (2014) Neurobiol Aging 35:858–866

    Article  CAS  PubMed  Google Scholar 

  141. Torsdottir G, Kristinsson J, Sveinbjornsdottir S, Snaedal J, Johannesson T (1999) Pharmacol Toxicol 85:239–243

    Article  CAS  PubMed  Google Scholar 

  142. Davies KM, Mercer JF, Chen N, Double KL (2016) Clin Sci (Lond) 130:565–574

    Article  Google Scholar 

  143. Montes S, Rivera-Mancia S, Diaz-Ruiz A, Tristan-Lopez L, Rios C (2014) Oxid Med Cell Longev 2014:147251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  144. Howells C, West AK, Chung RS (2010) FEBS J 277:2931–2939

    Article  CAS  PubMed  Google Scholar 

  145. Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, Jenner P, Marsden CD (1987) Lancet 2:1219–1220

    Article  CAS  PubMed  Google Scholar 

  146. Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P, Marsden CD (1989) J Neurochem 52:1830–1836

    Article  CAS  PubMed  Google Scholar 

  147. Hirsch EC, Brandel JP, Galle P, Javoy-Agid F, Agid Y (1991) J Neurochem 56:446–451

    Article  CAS  PubMed  Google Scholar 

  148. Riederer P, Sofic E, Rausch WD, Schmidt B, Reynolds GP, Jellinger K, Youdim MB (1989) J Neurochem 52:515–520

    Article  CAS  PubMed  Google Scholar 

  149. Double KL, Reyes S, Werry EL, Halliday GM (2010) Prog Neurobiol 92:316–329

    Article  CAS  PubMed  Google Scholar 

  150. Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG (2009) Mol Neurodegener 4:47

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  151. Gerlach M, Double KL, Youdim MB, Riederer P (2006) J Neural Transm Suppl 70:133–142

    CAS  Google Scholar 

  152. Mills E, Dong XP, Wang F, Xu H (2010) Future Med Chem 2:51–64

    Article  CAS  PubMed  Google Scholar 

  153. Ward RJ, Colivicchi MA, Allen R, Schol F, Lallemand F, de Witte P, Ballini C, Corte LD, Dexter D (2009) J Neurochem 111:1119–1128

    Article  CAS  PubMed  Google Scholar 

  154. Dexter DT, Carayon A, Javoy-Agid F, Agid Y, Wells FR, Daniel SE, Lees AJ, Jenner P, Marsden CD (1991) Brain 114(Pt 4):1953–1975

    Article  PubMed  Google Scholar 

  155. Conway KA, Harper JD, Lansbury PT (1998) Nat Med 4:1318–1320

    Article  CAS  PubMed  Google Scholar 

  156. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Science 276:2045–2047

    Article  CAS  PubMed  Google Scholar 

  157. Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, Lee VM (2002) Neuron 34:521–533

    Article  CAS  PubMed  Google Scholar 

  158. Yu Z, Xu X, Xiang Z, Zhou J, Zhang Z, Hu C, He C (2010) PLoS One 5:e9956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  159. Duda JE, Giasson BI, Chen Q, Gur TL, Hurtig HI, Stern MB, Gollomp SM, Ischiropoulos H, Lee VM, Trojanowski JQ (2000) Am J Pathol 157:1439–1445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Abeyawardhane DL, Heitger DR, Fernandez RD, Forney AK, Lucas HR (2019) ACS Chem Neurosci 10:1402–1410

    Article  CAS  PubMed  Google Scholar 

  161. Paik SR, Shin HJ, Lee JH, Chang CS, Kim J (1999) Biochem J 340(Pt 3):821–828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Uversky VN, Li J, Fink AL (2001) J Biol Chem 276:44284–44296

    Article  CAS  PubMed  Google Scholar 

  163. Rasia RM, Bertoncini CW, Marsh D, Hoyer W, Cherny D, Zweckstetter M, Griesinger C, Jovin TM, Fernandez CO (2005) Proc Natl Acad Sci USA 102:4294–4299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Mason RJ, Paskins AR, Dalton CF, Smith DP (2016) Biochemistry 55:4737–4741

    Article  CAS  PubMed  Google Scholar 

  165. Lu Y, Prudent M, Fauvet B, Lashuel HA, Girault HH (2011) ACS Chem Neurosci 2:667–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Wang C, Liu L, Zhang L, Peng Y, Zhou F (2010) Biochemistry 49:8134–8142

    Article  CAS  PubMed  Google Scholar 

  167. Abeyawardhane DL, Fernandez RD, Heitger DR, Crozier MK, Wolver JC, Lucas HR (2018) J Am Chem Soc 140:17086–17094

    Article  CAS  PubMed  Google Scholar 

  168. Peng Y, Wang C, Xu HH, Liu YN, Zhou F (2010) J Inorg Biochem 104:365–370

    Article  CAS  PubMed  Google Scholar 

  169. Chen B, Wen X, Jiang H, Wang J, Song N, Xie J (2019) Free Radic Biol Med 141:253–260

    Article  CAS  PubMed  Google Scholar 

  170. Zecca L, Stroppolo A, Gatti A, Tampellini D, Toscani M, Gallorini M, Giaveri G, Arosio P, Santambrogio P, Fariello RG, Karatekin E, Kleinman MH, Turro N, Hornykiewicz O, Zucca FA (2004) Proc Natl Acad Sci USA 101:9843–9848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Cobley JN, Fiorello ML, Bailey DM (2018) Redox Biol 15:490–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Munoz P, Cardenas S, Huenchuguala S, Briceno A, Couve E, Paris I, Segura-Aguilar J (2015) Toxicol Sci 145:37–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Zucca FA, Segura-Aguilar J, Ferrari E, Munoz P, Paris I, Sulzer D, Sarna T, Casella L, Zecca L (2017) Prog Neurobiol 155:96–119

    Article  CAS  PubMed  Google Scholar 

  174. Maker HS, Weiss C, Silides DJ, Cohen G (1981) J Neurochem 36:589–593

    Article  CAS  PubMed  Google Scholar 

  175. Wada K, Fujibayashi Y, Tajima N, Yokoyama A (1994) Biol Pharm Bull 17:701–704

    Article  CAS  PubMed  Google Scholar 

  176. Fodero-Tavoletti MT, Villemagne VL, Paterson BM, White AR, Li QX, Camakaris J, O’Keefe G, Cappai R, Barnham KJ, Donnelly PS (2010) J Alzheimers Dis 20:49–55

    Article  CAS  PubMed  Google Scholar 

  177. Dearling JL, Packard AB (2010) Nucl Med Biol 37:237–243

    Article  CAS  PubMed  Google Scholar 

  178. Fujibayashi Y, Taniuchi H, Yonekura Y, Ohtani H, Konishi J, Yokoyama A (1997) J Nucl Med 38:1155–1160

    CAS  PubMed  Google Scholar 

  179. Vavere AL, Lewis JS (2007) Dalton Trans. https://doi.org/10.1039/b705989b:4893-4902

    Article  PubMed  Google Scholar 

  180. Ikawa M, Okazawa H, Tsujikawa T, Matsunaga A, Yamamura O, Mori T, Hamano T, Kiyono Y, Nakamoto Y, Yoneda M (2015) Neurology 84:2033–2039

    Article  CAS  PubMed  Google Scholar 

  181. Hung LW, Villemagne VL, Cheng L, Sherratt NA, Ayton S, White AR, Crouch PJ, Lim S, Leong SL, Wilkins S, George J, Roberts BR, Pham CL, Liu X, Chiu FC, Shackleford DM, Powell AK, Masters CL, Bush AI, O’Keefe G, Culvenor JG, Cappai R, Cherny RA, Donnelly PS, Hill AF, Finkelstein DI, Barnham KJ (2012) J Exp Med 209:837–854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Dexter DT, Statton SA, Whitmore C, Freinbichler W, Weinberger P, Tipton KF, Della Corte L, Ward RJ, Crichton RR (2011) J Neural Transm (Vienna) 118:223–231

    Article  CAS  Google Scholar 

  183. Cohen AR, Galanello R, Piga A, De Sanctis V, Tricta F (2003) Blood 102:1583–1587

    Article  CAS  PubMed  Google Scholar 

  184. Galanello R, Campus S (2009) Acta Haematol 122:155–164

    Article  CAS  PubMed  Google Scholar 

  185. Devos D, Moreau C, Devedjian JC, Kluza J, Petrault M, Laloux C, Jonneaux A, Ryckewaert G, Garcon G, Rouaix N, Duhamel A, Jissendi P, Dujardin K, Auger F, Ravasi L, Hopes L, Grolez G, Firdaus W, Sablonniere B, Strubi-Vuillaume I, Zahr N, Destee A, Corvol JC, Poltl D, Leist M, Rose C, Defebvre L, Marchetti P, Cabantchik ZI, Bordet R (2014) Antioxid Redox Signal 21:195–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Glickstein H, El RB, Shvartsman M, Cabantchik ZI (2005) Blood 106:3242–3250

    Article  CAS  PubMed  Google Scholar 

  187. Sohn YS, Mitterstiller AM, Breuer W, Weiss G, Cabantchik ZI (2011) Br J Pharmacol 164:406–418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Martin-Bastida A, Lao-Kaim NP, Loane C, Politis M, Roussakis AA, Valle-Guzman N, Kefalopoulou Z, Paul-Visse G, Widner H, Xing Y, Schwarz ST, Auer DP, Foltynie T, Barker RA, Piccini P (2017) Eur J Neurol 24:357–365

    Article  CAS  PubMed  Google Scholar 

  189. Saberi S, Stauffer JE, Schulte DJ, Ravits J (2015) Neurol Clin 33:855–876

    Article  PubMed  PubMed Central  Google Scholar 

  190. Pratt AJ, Getzoff ED, Perry JJ (2012) Degener Neurol Neuromuscul Dis 2:1–14

    PubMed Central  Google Scholar 

  191. Bensimon G, Lacomblez L, Meininger V (1994) N Engl J Med 330:585–591

    Article  CAS  PubMed  Google Scholar 

  192. Sreedharan J, Brown RH Jr (2013) Ann Neurol 74:309–316

    Article  CAS  PubMed  Google Scholar 

  193. Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, Oda T (2006) Biochem Biophys Res Commun 351:602–611

    Article  CAS  PubMed  Google Scholar 

  194. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK (2008) Neurobiol Dis 30:400–407

    Article  CAS  PubMed  Google Scholar 

  195. Barber SC, Shaw PJ (2010) Free Radic Biol Med 48:629–641

    Article  CAS  PubMed  Google Scholar 

  196. Rothstein JD (2009) Ann Neurol 65(Suppl 1):S3–S9

    Article  CAS  PubMed  Google Scholar 

  197. Banci L, Bertini I, Boca M, Girotto S, Martinelli M, Valentine JS, Vieru M (2008) PLoS One 3:e1677

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  198. Culotta VC, Yang M, O’Halloran TV (2006) Biochim Biophys Acta 1763:747–758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Valentine JS, Doucette PA, Zittin Potter S (2005) Annu Rev Biochem 74:563–593

    Article  CAS  PubMed  Google Scholar 

  200. Beckman JS, Carson M, Smith CD, Koppenol WH (1993) Nature 364:584

    Article  CAS  PubMed  Google Scholar 

  201. Leal SS, Cristovao JS, Biesemeier A, Cardoso I, Gomes CM (2015) Metallomics 7:333–346

    Article  CAS  PubMed  Google Scholar 

  202. Tokuda E, Okawa E, Ono S (2009) J Neurochem 111:181–191

    Article  CAS  PubMed  Google Scholar 

  203. Tokuda E, Okawa E, Watanabe S, Ono S, Marklund SL (2013) Neurobiol Dis 54:308–319

    Article  CAS  PubMed  Google Scholar 

  204. Gong YH, Elliott JL (2000) Exp Neurol 162:27–36

    Article  CAS  PubMed  Google Scholar 

  205. Roberts BR, Lim NK, McAllum EJ, Donnelly PS, Hare DJ, Doble PA, Turner BJ, Price KA, Lim SC, Paterson BM, Hickey JL, Rhoads TW, Williams JR, Kanninen KM, Hung LW, Liddell JR, Grubman A, Monty JF, Llanos RM, Kramer DR, Mercer JF, Bush AI, Masters CL, Duce JA, Li QX, Beckman JS, Barnham KJ, White AR, Crouch PJ (2014) J Neurosci 34:8021–8031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Ferrante RJ, Browne SE, Shinobu LA, Bowling AC, Baik MJ, MacGarvey U, Kowall NW, Brown RH Jr, Beal MF (1997) J Neurochem 69:2064–2074

    Article  CAS  PubMed  Google Scholar 

  207. Ilieva EV, Ayala V, Jove M, Dalfo E, Cacabelos D, Povedano M, Bellmunt MJ, Ferrer I, Pamplona R, Portero-Otin M (2007) Brain 130:3111–3123

    Article  PubMed  Google Scholar 

  208. Morimoto S, Kuzuhara S, Kokubo Y (2009) Mov Disord 24:123–126

    Article  PubMed  Google Scholar 

  209. Nakagomi S, Barsoum MJ, Bossy-Wetzel E, Sutterlin C, Malhotra V, Lipton SA (2008) Neurobiol Dis 29:221–231

    Article  CAS  PubMed  Google Scholar 

  210. Smith RG, Henry YK, Mattson MP, Appel SH (1998) Ann Neurol 44:696–699

    Article  CAS  PubMed  Google Scholar 

  211. Cheung G, Gawel MJ, Cooper PW, Farb RI, Ang LC, Gawal MJ (1995) Radiology 194:263–270

    Article  CAS  PubMed  Google Scholar 

  212. Hecht MJ, Fellner F, Fellner C, Hilz MJ, Neundorfer B, Heuss D (2002) J Neurol Sci 199:59–65

    Article  PubMed  Google Scholar 

  213. Santillo AF, Skoglund L, Lindau M, Eeg-Olofsson KE, Tovi M, Engler H, Brundin RM, Ingvast S, Lannfelt L, Glaser A, Kilander L (2009) Alzheimer Dis Assoc Disord 23:298–300

    Article  PubMed  Google Scholar 

  214. Yasui M, Ota K, Garruto RM (1993) Neurotoxicology 14:445–450

    CAS  PubMed  Google Scholar 

  215. Kwan JY, Jeong SY, Van Gelderen P, Deng HX, Quezado MM, Danielian LE, Butman JA, Chen L, Bayat E, Russell J, Siddique T, Duyn JH, Rouault TA, Floeter MK (2012) PLoS One 7:e35241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Ignjatovic A, Stevic Z, Lavrnic D, Nikolic-Kokic A, Blagojevic D, Spasic M, Spasojevic I (2012) Amyotroph Lateral Scler 13:357–362

    Article  CAS  PubMed  Google Scholar 

  217. Jeong SY, Rathore KI, Schulz K, Ponka P, Arosio P, David S (2009) J Neurosci 29:610–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Wang Q, Zhang X, Chen S, Zhang X, Zhang S, Youdium M, Le W (2011) Neurodegener Dis 8:310–321

    Article  CAS  PubMed  Google Scholar 

  219. Goodall EF, Haque MS, Morrison KE (2008) J Neurol 255:1652–1656

    Article  CAS  PubMed  Google Scholar 

  220. Qureshi M, Brown RH Jr, Rogers JT, Cudkowicz ME (2008) Open Neurol J 2:51–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  221. Yu J, Wang N, Qi F, Wang X, Zhu Q, Lu Y, Zhang H, Che F, Li W (2018) Biomed Rep 9:333–338

    CAS  PubMed  PubMed Central  Google Scholar 

  222. Ikeda K, Hirayama T, Takazawa T, Kawabe K, Iwasaki Y (2012) Intern Med 51:1501–1508

    Article  CAS  PubMed  Google Scholar 

  223. Nadjar Y, Gordon P, Corcia P, Bensimon G, Pieroni L, Meininger V, Salachas F (2012) PLoS One 7:e45034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Mitchell RM, Simmons Z, Beard JL, Stephens HE, Connor JR (2010) Muscle Nerve 42:95–103

    Article  CAS  PubMed  Google Scholar 

  225. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG (1993) Glia 7:84–92

    Article  CAS  PubMed  Google Scholar 

  226. Kang SH, Li Y, Fukaya M, Lorenzini I, Cleveland DW, Ostrow LW, Rothstein JD, Bergles DE (2013) Nat Neurosci 16:571–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Soon CP, Donnelly PS, Turner BJ, Hung LW, Crouch PJ, Sherratt NA, Tan JL, Lim NK, Lam L, Bica L, Lim S, Hickey JL, Morizzi J, Powell A, Finkelstein DI, Culvenor JG, Masters CL, Duce J, White AR, Barnham KJ, Li QX (2011) J Biol Chem 286:44035–44044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Hilton JB, Mercer SW, Lim NK, Faux NG, Buncic G, Beckman JS, Roberts BR, Donnelly PS, White AR, Crouch PJ (2017) Sci Rep 7:42292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  229. McAllum EJ, Roberts BR, Hickey JL, Dang TN, Grubman A, Donnelly PS, Liddell JR, White AR, Crouch PJ (2015) Neurobiol Dis 81:20–24

    Article  CAS  PubMed  Google Scholar 

  230. Vieira FG, Hatzipetros T, Thompson K, Moreno AJ, Kidd JD, Tassinari VR, Levine B, Perrin S, Gill A (2017) IBRO Rep 2:47–53

    Article  PubMed  PubMed Central  Google Scholar 

  231. Williams JR, Trias E, Beilby PR, Lopez NI, Labut EM, Bradford CS, Roberts BR, McAllum EJ, Crouch PJ, Rhoads TW, Pereira C, Son M, Elliott JL, Franco MC, Estevez AG, Barbeito L, Beckman JS (2016) Neurobiol Dis 89:1–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Son M, Elliott JL (2014) J Neurol Sci 336:1–7

    Article  CAS  PubMed  Google Scholar 

  233. Son M, Leary SC, Romain N, Pierrel F, Winge DR, Haller RG, Elliott JL (2008) J Biol Chem 283:12267–12275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Avramovich-Tirosh Y, Bar-Am O, Amit T, Youdim MB, Weinreb O (2010) Curr Alzheimer Res 7:300–306

    Article  CAS  PubMed  Google Scholar 

  235. Kupershmidt L, Weinreb O, Amit T, Mandel S, Carri MT, Youdim MB (2009) FASEB J 23:3766–3779

    Article  CAS  PubMed  Google Scholar 

  236. Storkebaum E, Lambrechts D, Dewerchin M, Moreno-Murciano MP, Appelmans S, Oh H, Van Damme P, Rutten B, Man WY, De Mol M, Wyns S, Manka D, Vermeulen K, Van Den Bosch L, Mertens N, Schmitz C, Robberecht W, Conway EM, Collen D, Moons L, Carmeliet P (2005) Nat Neurosci 8:85–92

    Article  CAS  PubMed  Google Scholar 

  237. Wang Y, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA, Jin K (2007) J Neurosci 27:304–307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  238. Lysogorskaia EV, Abramycheva N, Zakharova MN, Illarioshkin SN (2012) Zh Nevrol Psikhiatr Im S S Korsakova 112:42–45

    CAS  PubMed  Google Scholar 

  239. Stalmans I, Lambrechts D, De Smet F, Jansen S, Wang J, Maity S, Kneer P, von der Ohe M, Swillen A, Maes C, Gewillig M, Molin DG, Hellings P, Boetel T, Haardt M, Compernolle V, Dewerchin M, Plaisance S, Vlietinck R, Emanuel B, de Gittenberger Groot AC, Scambler P, Morrow B, Driscol DA, Moons L, Esguerra CV, Carmeliet G, Behn-Krappa A, Devriendt K, Collen D, Conway SJ, Carmeliet P (2003) Nat Med 9:173–182

    Article  CAS  PubMed  Google Scholar 

  240. Beerepoot LV, Shima DT, Kuroki M, Yeo KT, Voest EE (1996) Cancer Res 56:3747–3751

    CAS  PubMed  Google Scholar 

  241. Moreau C, Danel V, Devedjian JC, Grolez G, Timmerman K, Laloux C, Petrault M, Gouel F, Jonneaux A, Dutheil M, Lachaud C, Lopes R, Kuchcinski G, Auger F, Kyheng M, Duhamel A, Perez T, Pradat PF, Blasco H, Veyrat-Durebex C, Corcia P, Oeckl P, Otto M, Dupuis L, Garcon G, Defebvre L, Cabantchik ZI, Duce J, Bordet R, Devos D (2018) Antioxid Redox Signal 29:742–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B 3rd, Stockwell BR (2012) Cell 149:1060–1072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Conrad M, Angeli JP, Vandenabeele P, Stockwell BR (2016) Nat Rev Drug Discov 15:348–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Masaldan S, Bush AI, Devos D, Rolland AS, Moreau C (2019) Free Radic Biol Med 133:221–233

    Article  CAS  PubMed  Google Scholar 

  245. Ursini F, Maiorino M, Valente M, Ferri L, Gregolin C (1982) Biochim Biophys Acta 710:197–211

    Article  CAS  PubMed  Google Scholar 

  246. Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR (2016) Proc Natl Acad Sci USA 113:E4966–E4975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Shah R, Shchepinov MS, Pratt DA (2018) ACS Cent Sci 4:387–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Doll S, Proneth B, Tyurina YY, Panzilius E, Kobayashi S, Ingold I, Irmler M, Beckers J, Aichler M, Walch A, Prokisch H, Trumbach D, Mao G, Qu F, Bayir H, Fullekrug J, Scheel CH, Wurst W, Schick JA, Kagan VE, Angeli JP, Conrad M (2017) Nat Chem Biol 13:91–98

    Article  CAS  PubMed  Google Scholar 

  249. Reed JC, Pellecchia M (2012) Cell 149:963–965

    Article  CAS  PubMed  Google Scholar 

  250. Yang WS, Stockwell BR (2008) Chem Biol 15:234–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC (2014) Nature 509:105–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. Pratico D, Sung S (2004) J Alzheimers Dis 6:171–175

    Article  CAS  PubMed  Google Scholar 

  253. Reed TT, Pierce WM, Markesbery WR, Butterfield DA (2009) Brain Res 1274:66–76

    Article  CAS  PubMed  Google Scholar 

  254. Mandal PK, Saharan S, Tripathi M, Murari G (2015) Biol Psychiatry 78:702–710

    Article  CAS  PubMed  Google Scholar 

  255. Raefsky SM, Furman R, Milne G, Pollock E, Axelsen P, Mattson MP, Shchepinov MS (2018) Neurobiol Aging 66:165–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Hambright WS, Fonseca RS, Chen L, Na R, Ran Q (2017) Redox Biol 12:8–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Weinreb O, Mandel S, Youdim MBH, Amit T (2013) Free Radic Biol Med 62:52–64

    Article  CAS  PubMed  Google Scholar 

  258. Monti DA, Zabrecky G, Kremens D, Liang TW, Wintering NA, Cai J, Wei X, Bazzan AJ, Zhong L, Bowen B, Intenzo CM, Iacovitti L, Newberg AB (2016) PLoS One 11:e0157602

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  259. Van Do B, Gouel F, Jonneaux A, Timmerman K, Gele P, Petrault M, Bastide M, Laloux C, Moreau C, Bordet R, Devos D, Devedjian JC (2016) Neurobiol Dis 94:169–178

    Article  CAS  Google Scholar 

  260. Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH (2004) Neurology 62:1758–1765

    Article  CAS  PubMed  Google Scholar 

  261. Devos D, Moreau C, Kyheng M, Garcon G, Rolland AS, Blasco H, Gele P, Timothee Lenglet T, Veyrat-Durebex C, Corcia P, Dutheil M, Bede P, Jeromin A, Oeckl P, Otto M, Meninger V, Danel-Brunaud V, Devedjian JC, Duce JA, Pradat PF (2019) Sci Rep 9:2918

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  262. Tsvetkov P, Detappe A, Cai K, Keys HR, Brune Z, Ying W, Thiru P, Reidy M, Kugener G, Rossen J, Kocak M, Kory N, Tsherniak A, Santagata S, Whitesell L, Ghobrial IM, Markley JL, Lindquist S, Golub TR (2019) Nat Chem Biol 15:681–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The Florey Institute of Neuroscience and Mental Health acknowledges the strong support from the Victorian Government and in particular the funding from the Operational Infrastructure Support Grant. This work was supported by the Australian Research Council (AIB, CO), the National Health and Medical Research Council and the CRC for Mental Health (AIB). Figures 1 and 2 were compiled using images from Servier Medical art.

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Correspondence to Carlos M. Opazo or Ashley I. Bush.

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Prof. Bush is a shareholder in Prana Biotechnology Ltd, Cogstate Ltd, Brighton Biotech LLC, Grunbiotics Pty Ltd, Eucalyptus Pty Ltd, and Mesoblast Ltd. He is a paid consultant for, and has a profit share interest in, Collaborative Medicinal Development Pty Ltd.

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Acevedo, K., Masaldan, S., Opazo, C.M. et al. Redox active metals in neurodegenerative diseases. J Biol Inorg Chem 24, 1141–1157 (2019). https://doi.org/10.1007/s00775-019-01731-9

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  • DOI: https://doi.org/10.1007/s00775-019-01731-9

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