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JBIC Journal of Biological Inorganic Chemistry

, Volume 24, Issue 8, pp 1141–1157 | Cite as

Redox active metals in neurodegenerative diseases

  • Karla Acevedo
  • Shashank Masaldan
  • Carlos M. OpazoEmail author
  • Ashley I. BushEmail author
Mini Review
Part of the following topical collections:
  1. Metal Ions and Degenerative Diseases

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).

Keywords

Copper Iron Neurodegeneration 

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

Notes

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.

Compliance with ethical standards

Conflict of interest

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.

References

  1. 1.
    Halliwell B (2006) J Neurochem 97:1634–1658PubMedCrossRefGoogle Scholar
  2. 2.
    Butterfield DA, Halliwell B (2019) Nat Rev Neurosci 20:148–160PubMedCrossRefGoogle Scholar
  3. 3.
    Bush AI (2003) Trends Neurosci 26:207–214PubMedCrossRefGoogle Scholar
  4. 4.
    Gaier ED, Eipper BA, Mains RE (2013) J Neurosci Res 91:2–19PubMedGoogle Scholar
  5. 5.
    Belaidi AA, Bush AI (2016) J Neurochem 139(Suppl 1):179–197PubMedCrossRefGoogle Scholar
  6. 6.
    Opazo CM, Greenough MA, Bush AI (2014) Front Aging Neurosci 6:143PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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 171:273–285PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Angelova DF, Brown DR (2015) Metals 5:2070–2092CrossRefGoogle Scholar
  9. 9.
    Choi BS, Zheng W (2009) Brain Res 1248:14–21PubMedCrossRefGoogle Scholar
  10. 10.
    Meyer LA, Durley AP, Prohaska JR, Harris ZL (2001) J Biol Chem 276:36857–36861PubMedCrossRefGoogle Scholar
  11. 11.
    Maryon EB, Molloy SA, Kaplan JH (2013) Am J Physiol Cell Physiol 304:C768–C779PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Tapia L, Gonzalez-Aguero M, Cisternas MF, Suazo M, Cambiazo V, Uauy R, Gonzalez M (2004) Biochem J 378:617–624PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    La Fontaine S, Mercer JF (2007) Arch Biochem Biophys 463:149–167PubMedCrossRefGoogle Scholar
  14. 14.
    Linz R, Lutsenko S (2007) J Bioenerg Biomembr 39:403–407PubMedCrossRefGoogle Scholar
  15. 15.
    Greenough M, Pase L, Voskoboinik I, Petris MJ, O’Brien AW, Camakaris J (2004) Am J Physiol Cell Physiol 287:C1463–C1471PubMedCrossRefGoogle Scholar
  16. 16.
    Pase L, Voskoboinik I, Greenough M, Camakaris J (2004) Biochem J 378:1031–1037PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Ohgami RS, Campagna DR, Greer EL, Antiochos B, McDonald A, Chen J, Sharp JJ, Fujiwara Y, Barker JE, Fleming MD (2005) Nat Genet 37:1264–1269PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Moos T, Morgan EH (2004) J Neurochem 88:233–245PubMedCrossRefGoogle Scholar
  19. 19.
    Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) Lancet Neurol 13:1045–1060PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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–C871PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Wang CY, Jenkitkasemwong S, Duarte S, Sparkman BK, Shawki A, Mackenzie B, Knutson MD (2012) J Biol Chem 287:34032–34043PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Zhao N, Gao J, Enns CA, Knutson MD (2010) J Biol Chem 285:32141–32150PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Nature 388:482–488PubMedCrossRefGoogle Scholar
  24. 24.
    Ji C, Kosman DJ (2015) J Neurochem 133:668–683PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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 111:8031–8036PubMedCrossRefGoogle Scholar
  26. 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 288:17791–17802PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Nandal A, Ruiz JC, Subramanian P, Ghimire-Rijal S, Sinnamon RA, Stemmler TL, Bruick RK, Philpott CC (2011) Cell Metab 14:647–657PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Pantopoulos K (2004) Ann N Y Acad Sci 1012:1–13PubMedCrossRefGoogle Scholar
  29. 29.
    Zhang DL, Ghosh MC, Rouault TA (2014) Front Pharmacol 5:124PubMedPubMedCentralGoogle Scholar
  30. 30.
    Double KL, Gerlach M, Schunemann V, Trautwein AX, Zecca L, Gallorini M, Youdim MB, Riederer P, Ben-Shachar D (2003) Biochem Pharmacol 66:489–494PubMedCrossRefGoogle Scholar
  31. 31.
    Asano T, Komatsu M, Yamaguchi-Iwai Y, Ishikawa F, Mizushima N, Iwai K (2011) Mol Cell Biol 31:2040–2052PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Nitti M, Piras S, Brondolo L, Marinari UM, Pronzato MA, Furfaro AL (2018) Int J Mol Sci 19:2260–2280PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Zhang YW, Thompson R, Zhang H, Xu H (2011) Mol Brain 4:3PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Unzeta M, Esteban G, Bolea I, Fogel WA, Ramsay RR, Youdim MB, Tipton KF, Marco-Contelles J (2016) Front Neurosci 10:205PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Wimo A, Jonsson L, Bond J, Prince M, Winblad B, I. Alzheimer Disease (2013) Alzheimers Dement 9:1–11PubMedCrossRefGoogle Scholar
  36. 36.
    Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Brain Res Brain Res Rev 33:95–130PubMedCrossRefGoogle Scholar
  37. 37.
    Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Proc Natl Acad Sci USA 82:4245–4249PubMedCrossRefGoogle Scholar
  38. 38.
    Davies P, Maloney AJ (1976) Lancet 2:1403PubMedCrossRefGoogle Scholar
  39. 39.
    Drachman DA, Leavitt J (1974) Arch Neurol 30:113–121PubMedCrossRefGoogle Scholar
  40. 40.
    Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Science 215:1237–1239PubMedCrossRefGoogle Scholar
  41. 41.
    Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR (1998) J Neurol Sci 158:47–52PubMedCrossRefGoogle Scholar
  42. 42.
    Pithadia AS, Lim MH (2012) Curr Opin Chem Biol 16:67–73PubMedCrossRefGoogle Scholar
  43. 43.
    Raven EP, Lu PH, Tishler TA, Heydari P, Bartzokis G (2013) J Alzheimers Dis 37:127–136PubMedCrossRefGoogle Scholar
  44. 44.
    Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, Carey PR (2003) Biochemistry 42:2768–2773PubMedCrossRefGoogle Scholar
  45. 45.
    Miller LM, Wang Q, Telivala TP, Smith RJ, Lanzirotti A, Miklossy J (2006) J Struct Biol 155:30–37PubMedCrossRefGoogle Scholar
  46. 46.
    Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, Smith MA (2000) J Neurochem 74:270–279PubMedCrossRefGoogle Scholar
  47. 47.
    Smith MA, Harris PL, Sayre LM, Perry G (1997) Proc Natl Acad Sci USA 94:9866–9868PubMedCrossRefGoogle Scholar
  48. 48.
    Deibel MA, Ehmann WD, Markesbery WR (1996) J Neurol Sci 143:137–142PubMedCrossRefGoogle Scholar
  49. 49.
    Zatta P, Drago D, Bolognin S, Sensi SL (2009) Trends Pharmacol Sci 30:346–355PubMedCrossRefGoogle Scholar
  50. 50.
    Bishop GM, Robinson SR, Liu Q, Perry G, Atwood CS, Smith MA (2002) Dev Neurosci 24:184–187PubMedCrossRefGoogle Scholar
  51. 51.
    Roberts BR, Ryan TM, Bush AI, Masters CL, Duce JA (2012) J Neurochem 120(Suppl 1):149–166PubMedCrossRefGoogle Scholar
  52. 52.
    Schrag M, Mueller C, Oyoyo U, Smith MA, Kirsch WM (2011) Prog Neurobiol 94:296–306PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Schrag M, Mueller C, Zabel M, Crofton A, Kirsch WM, Ghribi O, Squitti R, Perry G (2013) Neurobiol Dis 59:100–110PubMedCrossRefGoogle Scholar
  54. 54.
    Ayton S, James SA, Bush AI (2017) Cell Chem Biol 24:1192–1194PubMedCrossRefGoogle Scholar
  55. 55.
    Hwang EJ, Kim HG, Kim D, Rhee HY, Ryu CW, Liu T, Wang Y, Jahng GH (2016) Med Phys 43:4718PubMedCrossRefGoogle Scholar
  56. 56.
    Luo Z, Zhuang X, Kumar D, Wu X, Yue C, Han C, Lv J (2013) PLoS One 8:e76203PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Connor JR, Menzies SL, St Martin SM, Mufson EJ (1992) J Neurosci Res 31:75–83PubMedCrossRefGoogle Scholar
  58. 58.
    Meadowcroft MD, Connor JR, Smith MB, Yang QX (2009) J Magn Reson Imaging 29:997–1007PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Valensin D, Migliorini C, Valensin G, Gaggelli E, La Penna G, Kozlowski H, Gabbiani C, Messori L (2011) Inorg Chem 50:6865–6867PubMedCrossRefGoogle Scholar
  60. 60.
    Dikalov SI, Vitek MP, Mason RP (2004) Free Radic Biol Med 36:340–347PubMedCrossRefGoogle Scholar
  61. 61.
    Guilloreau L, Combalbert S, Sournia-Saquet A, Mazarguil H, Faller P (2007) ChemBioChem 8:1317–1325PubMedCrossRefGoogle Scholar
  62. 62.
    Nadal RC, Rigby SE, Viles JH (2008) Biochemistry 47:11653–11664PubMedCrossRefGoogle Scholar
  63. 63.
    Nakamura M, Shishido N, Nunomura A, Smith MA, Perry G, Hayashi Y, Nakayama K, Hayashi T (2007) Biochemistry 46:12737–12743PubMedCrossRefGoogle Scholar
  64. 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 55:1085–1089PubMedCrossRefGoogle Scholar
  65. 65.
    Taniguchi A, Sasaki D, Shiohara A, Iwatsubo T, Tomita T, Sohma Y, Kanai M (2014) Angew Chem Int Ed Engl 53:1382–1385PubMedCrossRefGoogle Scholar
  66. 66.
    Cheignon C, Faller P, Testemale D, Hureau C, Collin F (2016) Metallomics 8:1081–1089PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Butterfield DA, Reed T, Newman SF, Sultana R (2007) Free Radic Biol Med 43:658–677PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Selfridge JE, Lezi E, Lu J, Swerdlow RH (2013) Neurobiol Dis 51:3–12PubMedCrossRefGoogle Scholar
  69. 69.
    Zhao Y, Zhao B (2013) Oxid Med Cell Longev 2013:316523PubMedPubMedCentralGoogle Scholar
  70. 70.
    Gabbita SP, Lovell MA, Markesbery WR (1998) J Neurochem 71:2034–2040PubMedCrossRefGoogle Scholar
  71. 71.
    Hardas SS, Sultana R, Clark AM, Beckett TL, Szweda LI, Murphy MP, Butterfield DA (2013) Redox Biol 1:80–85PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Markesbery WR, Lovell MA (1998) Neurobiol Aging 19:33–36PubMedCrossRefGoogle Scholar
  73. 73.
    Mecocci P, MacGarvey U, Beal MF (1994) Ann Neurol 36:747–751PubMedCrossRefGoogle Scholar
  74. 74.
    Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) J Neurochem 68:2092–2097PubMedCrossRefGoogle Scholar
  75. 75.
    Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI (2000) J Neurochem 75:1219–1233PubMedCrossRefGoogle Scholar
  76. 76.
    Barritt JD, Viles JH (2015) J Biol Chem 290:27791–27802PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Drew SC (2017) Front Neurosci 11:317PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 54:10460–10464PubMedCrossRefGoogle Scholar
  79. 79.
    Sarell CJ, Syme CD, Rigby SE, Viles JH (2009) Biochemistry 48:4388–4402PubMedCrossRefGoogle Scholar
  80. 80.
    Huang X, Atwood CS, Moir RD, Hartshorn MA, Tanzi RE, Bush AI (2004) J Biol Inorg Chem 9:954–960PubMedCrossRefGoogle Scholar
  81. 81.
    Dai XL, Sun YX, Jiang ZF (2006) Acta Biochim Biophys Sin (Shanghai) 38:765–772CrossRefGoogle Scholar
  82. 82.
    Sarell CJ, Wilkinson SR, Viles JH (2010) J Biol Chem 285:41533–41540PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Greenough MA, Camakaris J, Bush AI (2013) Neurochem Int 62:540–555PubMedCrossRefGoogle Scholar
  84. 84.
    Grundke-Iqbal I, Fleming J, Tung YC, Lassmann H, Iqbal K, Joshi JG (1990) Acta Neuropathol 81:105–110PubMedCrossRefGoogle Scholar
  85. 85.
    Quintana C, Bellefqih S, Laval JY, Guerquin-Kern JL, Wu TD, Avila J, Ferrer I, Arranz R, Patino C (2006) J Struct Biol 153:42–54PubMedCrossRefGoogle Scholar
  86. 86.
    Bolognin S, Messori L, Drago D, Gabbiani C, Cendron L, Zatta P (2011) Int J Biochem Cell Biol 43:877–885PubMedCrossRefGoogle Scholar
  87. 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 286:4248–4256PubMedCrossRefGoogle Scholar
  88. 88.
    Ma Q, Li Y, Du J, Liu H, Kanazawa K, Nemoto T, Nakanishi H, Zhao Y (2006) Peptides 27:841–849PubMedCrossRefGoogle Scholar
  89. 89.
    Ma QF, Li YM, Du JT, Kanazawa K, Nemoto T, Nakanishi H, Zhao YF (2005) Biopolymers 79:74–85PubMedCrossRefGoogle Scholar
  90. 90.
    Martic S, Rains MK, Kraatz HB (2013) Anal Biochem 442:130–137PubMedCrossRefGoogle Scholar
  91. 91.
    Soragni A, Zambelli B, Mukrasch MD, Biernat J, Jeganathan S, Griesinger C, Ciurli S, Mandelkow E, Zweckstetter M (2008) Biochemistry 47:10841–10851PubMedCrossRefGoogle Scholar
  92. 92.
    Kitazawa M, Cheng D, Laferla FM (2009) J Neurochem 108:1550–1560PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Voss K, Harris C, Ralle M, Duffy M, Murchison C, Quinn JF (2014) Transl Neurodegener 3:24PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
  95. 95.
    Hesse L, Beher D, Masters CL, Multhaup G (1994) FEBS Lett 349:109–116PubMedCrossRefGoogle Scholar
  96. 96.
    Bush AI, Multhaup G, Moir RD, Williamson TG, Small DH, Rumble B, Pollwein P, Beyreuther K, Masters CL (1993) J Biol Chem 268:16109–16112PubMedGoogle Scholar
  97. 97.
    Miller Y, Ma B, Nussinov R (2010) Proc Natl Acad Sci USA 107:9490–9495PubMedCrossRefGoogle Scholar
  98. 98.
    Treiber C, Simons A, Strauss M, Hafner M, Cappai R, Bayer TA, Multhaup G (2004) J Biol Chem 279:51958–51964PubMedCrossRefGoogle Scholar
  99. 99.
    Maynard CJ, Cappai R, Volitakis I, Cherny RA, White AR, Beyreuther K, Masters CL, Bush AI, Li QX (2002) J Biol Chem 277:44670–44676PubMedCrossRefGoogle Scholar
  100. 100.
    Bellingham SA, Ciccotosto GD, Needham BE, Fodero LR, White AR, Masters CL, Cappai R, Camakaris J (2004) J Neurochem 91:423–428PubMedCrossRefGoogle Scholar
  101. 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 142:857–867PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Wong BX, Tsatsanis A, Lim LQ, Adlard PA, Bush AI, Duce JA (2014) PLoS One 9:e114174PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Cho HH, Cahill CM, Vanderburg CR, Scherzer CR, Wang B, Huang X, Rogers JT (2010) J Biol Chem 285:31217–31232PubMedPubMedCentralCrossRefGoogle Scholar
  104. 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 277:45518–45528PubMedCrossRefGoogle Scholar
  105. 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 286:8252–8262PubMedCrossRefGoogle Scholar
  106. 106.
    Hou P, Liu G, Zhao Y, Shi Z, Zheng Q, Bu G, Xu H, Zhang YW (2015) Neurobiol Aging 36:1310–1315PubMedCrossRefGoogle Scholar
  107. 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 547:10–15PubMedCrossRefGoogle Scholar
  108. 108.
    Gerber H, Wu F, Dimitrov M, Osuna GM, Fraering PC (2017) J Biol Chem 292:3751–3767PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G (1999) Biochem J 344(Pt 2):461–467PubMedPubMedCentralCrossRefGoogle Scholar
  110. 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 100:14187–14192PubMedCrossRefGoogle Scholar
  111. 111.
    Hardy JA, Higgins GA (1992) Science 256:184–185PubMedCrossRefGoogle Scholar
  112. 112.
    Masaldan S, Belaidi AA, Ayton S, Bush AI (2019) Pharmaceuticals (Basel) 12:93CrossRefGoogle Scholar
  113. 113.
    Nikseresht S, Bush AI, Ayton S (2019) Br J Pharmacol 176:3622–3635PubMedCrossRefGoogle Scholar
  114. 114.
    Li C, Wang J, Zhou B (2010) J Alzheimers Dis 21:1249–1262PubMedCrossRefGoogle Scholar
  115. 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 30:665–676PubMedCrossRefGoogle Scholar
  116. 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 17:423–440PubMedCrossRefGoogle Scholar
  117. 117.
    LeVine H 3rd, Ding Q, Walker JA, Voss RS, Augelli-Szafran CE (2009) Neurosci Lett 465:99–103PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Mancino AM, Hindo SS, Kochi A, Lim MH (2009) Inorg Chem 48:9596–9598PubMedCrossRefGoogle Scholar
  119. 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 60:1685–1691PubMedCrossRefGoogle Scholar
  120. 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 59:43–55PubMedCrossRefGoogle Scholar
  121. 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 20:509–516PubMedCrossRefGoogle Scholar
  122. 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 7:779–786PubMedCrossRefGoogle Scholar
  123. 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) 3:622–635Google Scholar
  124. 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:e90070PubMedPubMedCentralCrossRefGoogle Scholar
  125. 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 106:381–386PubMedCrossRefGoogle Scholar
  126. 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 283:4568–4577PubMedCrossRefGoogle Scholar
  127. 127.
    Crapper McLachlan DR, Dalton AJ, Kruck TP, Bell MY, Smith WL, Kalow W, Andrews DF (1991) Lancet 337:1304–1308PubMedCrossRefGoogle Scholar
  128. 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 2:160–168PubMedCrossRefGoogle Scholar
  129. 129.
    Guo C, Wang P, Zhong ML, Wang T, Huang XS, Li JY, Wang ZY (2013) Neurochem Int 62:165–172PubMedCrossRefGoogle Scholar
  130. 130.
    Banerjee P, Sahoo A, Anand S, Bir A, Chakrabarti S (2016) J Alzheimers Dis 49:681–693PubMedCrossRefGoogle Scholar
  131. 131.
    Kupershmidt L, Amit T, Bar-Am O, Youdim MB, Weinreb O (2012) Antioxid Redox Signal 17:860–877PubMedCrossRefGoogle Scholar
  132. 132.
    Molina-Holgado F, Gaeta A, Francis PT, Williams RJ, Hider RC (2008) J Neurochem 105:2466–2476PubMedCrossRefGoogle Scholar
  133. 133.
    Prasanthi JR, Schrag M, Dasari B, Marwarha G, Dickson A, Kirsch WM, Ghribi O (2012) J Alzheimers Dis 30:167–182PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Lang AE, Lozano AM (1998) N Engl J Med 339:1130–1143PubMedCrossRefGoogle Scholar
  135. 135.
    Jankovic J (2008) J Neurol Neurosurg Psychiatry 79:368–376PubMedCrossRefGoogle Scholar
  136. 136.
    Schulz JB (2008) J Neurol 255(Suppl 5):3–7PubMedCrossRefGoogle Scholar
  137. 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 303:95–99PubMedCrossRefGoogle Scholar
  138. 138.
    Pall HS, Williams AC, Blake DR, Lunec J, Gutteridge JM, Hall M, Taylor A (1987) Lancet 2:238–241PubMedCrossRefGoogle Scholar
  139. 139.
    Arnal N, Cristalli DO, de Alaniz MJ, Marra CA (2010) Brain Res 1319:118–130PubMedCrossRefGoogle Scholar
  140. 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 35:858–866PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Torsdottir G, Kristinsson J, Sveinbjornsdottir S, Snaedal J, Johannesson T (1999) Pharmacol Toxicol 85:239–243PubMedCrossRefGoogle Scholar
  142. 142.
    Davies KM, Mercer JF, Chen N, Double KL (2016) Clin Sci (Lond) 130:565–574CrossRefGoogle Scholar
  143. 143.
    Montes S, Rivera-Mancia S, Diaz-Ruiz A, Tristan-Lopez L, Rios C (2014) Oxid Med Cell Longev 2014:147251PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Howells C, West AK, Chung RS (2010) FEBS J 277:2931–2939PubMedCrossRefGoogle Scholar
  145. 145.
    Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, Jenner P, Marsden CD (1987) Lancet 2:1219–1220PubMedCrossRefGoogle Scholar
  146. 146.
    Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P, Marsden CD (1989) J Neurochem 52:1830–1836PubMedCrossRefGoogle Scholar
  147. 147.
    Hirsch EC, Brandel JP, Galle P, Javoy-Agid F, Agid Y (1991) J Neurochem 56:446–451PubMedCrossRefGoogle Scholar
  148. 148.
    Riederer P, Sofic E, Rausch WD, Schmidt B, Reynolds GP, Jellinger K, Youdim MB (1989) J Neurochem 52:515–520PubMedCrossRefGoogle Scholar
  149. 149.
    Double KL, Reyes S, Werry EL, Halliday GM (2010) Prog Neurobiol 92:316–329PubMedCrossRefGoogle Scholar
  150. 150.
    Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG (2009) Mol Neurodegener 4:47PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Gerlach M, Double KL, Youdim MB, Riederer P (2006) J Neural Transm Suppl 70:133–142Google Scholar
  152. 152.
    Mills E, Dong XP, Wang F, Xu H (2010) Future Med Chem 2:51–64PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Ward RJ, Colivicchi MA, Allen R, Schol F, Lallemand F, de Witte P, Ballini C, Corte LD, Dexter D (2009) J Neurochem 111:1119–1128PubMedCrossRefGoogle Scholar
  154. 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):1953–1975PubMedCrossRefGoogle Scholar
  155. 155.
    Conway KA, Harper JD, Lansbury PT (1998) Nat Med 4:1318–1320PubMedCrossRefGoogle Scholar
  156. 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 276:2045–2047PubMedCrossRefGoogle Scholar
  157. 157.
    Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, Lee VM (2002) Neuron 34:521–533PubMedCrossRefGoogle Scholar
  158. 158.
    Yu Z, Xu X, Xiang Z, Zhou J, Zhang Z, Hu C, He C (2010) PLoS One 5:e9956PubMedPubMedCentralCrossRefGoogle Scholar
  159. 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 157:1439–1445PubMedPubMedCentralCrossRefGoogle Scholar
  160. 160.
    Abeyawardhane DL, Heitger DR, Fernandez RD, Forney AK, Lucas HR (2019) ACS Chem Neurosci 10:1402–1410PubMedCrossRefPubMedCentralGoogle Scholar
  161. 161.
    Paik SR, Shin HJ, Lee JH, Chang CS, Kim J (1999) Biochem J 340(Pt 3):821–828PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Uversky VN, Li J, Fink AL (2001) J Biol Chem 276:44284–44296PubMedCrossRefPubMedCentralGoogle Scholar
  163. 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 102:4294–4299PubMedCrossRefGoogle Scholar
  164. 164.
    Mason RJ, Paskins AR, Dalton CF, Smith DP (2016) Biochemistry 55:4737–4741PubMedCrossRefGoogle Scholar
  165. 165.
    Lu Y, Prudent M, Fauvet B, Lashuel HA, Girault HH (2011) ACS Chem Neurosci 2:667–675PubMedPubMedCentralCrossRefGoogle Scholar
  166. 166.
    Wang C, Liu L, Zhang L, Peng Y, Zhou F (2010) Biochemistry 49:8134–8142PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Abeyawardhane DL, Fernandez RD, Heitger DR, Crozier MK, Wolver JC, Lucas HR (2018) J Am Chem Soc 140:17086–17094PubMedCrossRefPubMedCentralGoogle Scholar
  168. 168.
    Peng Y, Wang C, Xu HH, Liu YN, Zhou F (2010) J Inorg Biochem 104:365–370PubMedCrossRefPubMedCentralGoogle Scholar
  169. 169.
    Chen B, Wen X, Jiang H, Wang J, Song N, Xie J (2019) Free Radic Biol Med 141:253–260PubMedCrossRefGoogle Scholar
  170. 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 101:9843–9848PubMedCrossRefGoogle Scholar
  171. 171.
    Cobley JN, Fiorello ML, Bailey DM (2018) Redox Biol 15:490–503PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Munoz P, Cardenas S, Huenchuguala S, Briceno A, Couve E, Paris I, Segura-Aguilar J (2015) Toxicol Sci 145:37–47PubMedPubMedCentralCrossRefGoogle Scholar
  173. 173.
    Zucca FA, Segura-Aguilar J, Ferrari E, Munoz P, Paris I, Sulzer D, Sarna T, Casella L, Zecca L (2017) Prog Neurobiol 155:96–119PubMedCrossRefGoogle Scholar
  174. 174.
    Maker HS, Weiss C, Silides DJ, Cohen G (1981) J Neurochem 36:589–593PubMedCrossRefGoogle Scholar
  175. 175.
    Wada K, Fujibayashi Y, Tajima N, Yokoyama A (1994) Biol Pharm Bull 17:701–704PubMedCrossRefGoogle Scholar
  176. 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 20:49–55PubMedCrossRefGoogle Scholar
  177. 177.
    Dearling JL, Packard AB (2010) Nucl Med Biol 37:237–243PubMedCrossRefGoogle Scholar
  178. 178.
    Fujibayashi Y, Taniuchi H, Yonekura Y, Ohtani H, Konishi J, Yokoyama A (1997) J Nucl Med 38:1155–1160PubMedGoogle Scholar
  179. 179.
  180. 180.
    Ikawa M, Okazawa H, Tsujikawa T, Matsunaga A, Yamamura O, Mori T, Hamano T, Kiyono Y, Nakamoto Y, Yoneda M (2015) Neurology 84:2033–2039PubMedCrossRefGoogle Scholar
  181. 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 209:837–854PubMedPubMedCentralCrossRefGoogle Scholar
  182. 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) 118:223–231CrossRefGoogle Scholar
  183. 183.
    Cohen AR, Galanello R, Piga A, De Sanctis V, Tricta F (2003) Blood 102:1583–1587PubMedCrossRefGoogle Scholar
  184. 184.
    Galanello R, Campus S (2009) Acta Haematol 122:155–164PubMedCrossRefGoogle Scholar
  185. 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 21:195–210PubMedPubMedCentralCrossRefGoogle Scholar
  186. 186.
    Glickstein H, El RB, Shvartsman M, Cabantchik ZI (2005) Blood 106:3242–3250PubMedCrossRefGoogle Scholar
  187. 187.
    Sohn YS, Mitterstiller AM, Breuer W, Weiss G, Cabantchik ZI (2011) Br J Pharmacol 164:406–418PubMedPubMedCentralCrossRefGoogle Scholar
  188. 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 24:357–365PubMedCrossRefGoogle Scholar
  189. 189.
    Saberi S, Stauffer JE, Schulte DJ, Ravits J (2015) Neurol Clin 33:855–876PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Pratt AJ, Getzoff ED, Perry JJ (2012) Degener Neurol Neuromuscul Dis 2:1–14PubMedCentralPubMedGoogle Scholar
  191. 191.
    Bensimon G, Lacomblez L, Meininger V (1994) N Engl J Med 330:585–591PubMedCrossRefGoogle Scholar
  192. 192.
    Sreedharan J, Brown RH Jr (2013) Ann Neurol 74:309–316PubMedCrossRefGoogle Scholar
  193. 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 351:602–611PubMedCrossRefGoogle Scholar
  194. 194.
    Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK (2008) Neurobiol Dis 30:400–407PubMedCrossRefGoogle Scholar
  195. 195.
    Barber SC, Shaw PJ (2010) Free Radic Biol Med 48:629–641PubMedCrossRefGoogle Scholar
  196. 196.
    Rothstein JD (2009) Ann Neurol 65(Suppl 1):S3–S9PubMedCrossRefGoogle Scholar
  197. 197.
    Banci L, Bertini I, Boca M, Girotto S, Martinelli M, Valentine JS, Vieru M (2008) PLoS One 3:e1677PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Culotta VC, Yang M, O’Halloran TV (2006) Biochim Biophys Acta 1763:747–758PubMedPubMedCentralCrossRefGoogle Scholar
  199. 199.
    Valentine JS, Doucette PA, Zittin Potter S (2005) Annu Rev Biochem 74:563–593PubMedCrossRefGoogle Scholar
  200. 200.
    Beckman JS, Carson M, Smith CD, Koppenol WH (1993) Nature 364:584PubMedCrossRefGoogle Scholar
  201. 201.
    Leal SS, Cristovao JS, Biesemeier A, Cardoso I, Gomes CM (2015) Metallomics 7:333–346PubMedCrossRefGoogle Scholar
  202. 202.
    Tokuda E, Okawa E, Ono S (2009) J Neurochem 111:181–191PubMedCrossRefGoogle Scholar
  203. 203.
    Tokuda E, Okawa E, Watanabe S, Ono S, Marklund SL (2013) Neurobiol Dis 54:308–319PubMedCrossRefGoogle Scholar
  204. 204.
    Gong YH, Elliott JL (2000) Exp Neurol 162:27–36PubMedCrossRefGoogle Scholar
  205. 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 34:8021–8031PubMedPubMedCentralCrossRefGoogle Scholar
  206. 206.
    Ferrante RJ, Browne SE, Shinobu LA, Bowling AC, Baik MJ, MacGarvey U, Kowall NW, Brown RH Jr, Beal MF (1997) J Neurochem 69:2064–2074PubMedCrossRefGoogle Scholar
  207. 207.
    Ilieva EV, Ayala V, Jove M, Dalfo E, Cacabelos D, Povedano M, Bellmunt MJ, Ferrer I, Pamplona R, Portero-Otin M (2007) Brain 130:3111–3123PubMedCrossRefGoogle Scholar
  208. 208.
    Morimoto S, Kuzuhara S, Kokubo Y (2009) Mov Disord 24:123–126PubMedCrossRefGoogle Scholar
  209. 209.
    Nakagomi S, Barsoum MJ, Bossy-Wetzel E, Sutterlin C, Malhotra V, Lipton SA (2008) Neurobiol Dis 29:221–231PubMedCrossRefGoogle Scholar
  210. 210.
    Smith RG, Henry YK, Mattson MP, Appel SH (1998) Ann Neurol 44:696–699PubMedCrossRefGoogle Scholar
  211. 211.
    Cheung G, Gawel MJ, Cooper PW, Farb RI, Ang LC, Gawal MJ (1995) Radiology 194:263–270PubMedCrossRefGoogle Scholar
  212. 212.
    Hecht MJ, Fellner F, Fellner C, Hilz MJ, Neundorfer B, Heuss D (2002) J Neurol Sci 199:59–65PubMedCrossRefGoogle Scholar
  213. 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 23:298–300PubMedCrossRefGoogle Scholar
  214. 214.
    Yasui M, Ota K, Garruto RM (1993) Neurotoxicology 14:445–450PubMedGoogle Scholar
  215. 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:e35241PubMedPubMedCentralCrossRefGoogle Scholar
  216. 216.
    Ignjatovic A, Stevic Z, Lavrnic D, Nikolic-Kokic A, Blagojevic D, Spasic M, Spasojevic I (2012) Amyotroph Lateral Scler 13:357–362PubMedCrossRefGoogle Scholar
  217. 217.
    Jeong SY, Rathore KI, Schulz K, Ponka P, Arosio P, David S (2009) J Neurosci 29:610–619PubMedPubMedCentralCrossRefGoogle Scholar
  218. 218.
    Wang Q, Zhang X, Chen S, Zhang X, Zhang S, Youdium M, Le W (2011) Neurodegener Dis 8:310–321PubMedCrossRefGoogle Scholar
  219. 219.
    Goodall EF, Haque MS, Morrison KE (2008) J Neurol 255:1652–1656PubMedCrossRefGoogle Scholar
  220. 220.
    Qureshi M, Brown RH Jr, Rogers JT, Cudkowicz ME (2008) Open Neurol J 2:51–54PubMedPubMedCentralCrossRefGoogle Scholar
  221. 221.
    Yu J, Wang N, Qi F, Wang X, Zhu Q, Lu Y, Zhang H, Che F, Li W (2018) Biomed Rep 9:333–338PubMedPubMedCentralGoogle Scholar
  222. 222.
    Ikeda K, Hirayama T, Takazawa T, Kawabe K, Iwasaki Y (2012) Intern Med 51:1501–1508PubMedCrossRefGoogle Scholar
  223. 223.
    Nadjar Y, Gordon P, Corcia P, Bensimon G, Pieroni L, Meininger V, Salachas F (2012) PLoS One 7:e45034PubMedPubMedCentralCrossRefGoogle Scholar
  224. 224.
    Mitchell RM, Simmons Z, Beard JL, Stephens HE, Connor JR (2010) Muscle Nerve 42:95–103PubMedCrossRefGoogle Scholar
  225. 225.
    McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG (1993) Glia 7:84–92PubMedCrossRefGoogle Scholar
  226. 226.
    Kang SH, Li Y, Fukaya M, Lorenzini I, Cleveland DW, Ostrow LW, Rothstein JD, Bergles DE (2013) Nat Neurosci 16:571–579PubMedPubMedCentralCrossRefGoogle Scholar
  227. 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 286:44035–44044PubMedPubMedCentralCrossRefGoogle Scholar
  228. 228.
    Hilton JB, Mercer SW, Lim NK, Faux NG, Buncic G, Beckman JS, Roberts BR, Donnelly PS, White AR, Crouch PJ (2017) Sci Rep 7:42292PubMedPubMedCentralCrossRefGoogle Scholar
  229. 229.
    McAllum EJ, Roberts BR, Hickey JL, Dang TN, Grubman A, Donnelly PS, Liddell JR, White AR, Crouch PJ (2015) Neurobiol Dis 81:20–24PubMedCrossRefGoogle Scholar
  230. 230.
    Vieira FG, Hatzipetros T, Thompson K, Moreno AJ, Kidd JD, Tassinari VR, Levine B, Perrin S, Gill A (2017) IBRO Rep 2:47–53PubMedPubMedCentralCrossRefGoogle Scholar
  231. 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 89:1–9PubMedPubMedCentralCrossRefGoogle Scholar
  232. 232.
    Son M, Elliott JL (2014) J Neurol Sci 336:1–7PubMedCrossRefGoogle Scholar
  233. 233.
    Son M, Leary SC, Romain N, Pierrel F, Winge DR, Haller RG, Elliott JL (2008) J Biol Chem 283:12267–12275PubMedPubMedCentralCrossRefGoogle Scholar
  234. 234.
    Avramovich-Tirosh Y, Bar-Am O, Amit T, Youdim MB, Weinreb O (2010) Curr Alzheimer Res 7:300–306PubMedCrossRefGoogle Scholar
  235. 235.
    Kupershmidt L, Weinreb O, Amit T, Mandel S, Carri MT, Youdim MB (2009) FASEB J 23:3766–3779PubMedCrossRefGoogle Scholar
  236. 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 8:85–92PubMedCrossRefGoogle Scholar
  237. 237.
    Wang Y, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA, Jin K (2007) J Neurosci 27:304–307PubMedPubMedCentralCrossRefGoogle Scholar
  238. 238.
    Lysogorskaia EV, Abramycheva N, Zakharova MN, Illarioshkin SN (2012) Zh Nevrol Psikhiatr Im S S Korsakova 112:42–45PubMedGoogle Scholar
  239. 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 9:173–182PubMedCrossRefGoogle Scholar
  240. 240.
    Beerepoot LV, Shima DT, Kuroki M, Yeo KT, Voest EE (1996) Cancer Res 56:3747–3751PubMedGoogle Scholar
  241. 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 29:742–748PubMedPubMedCentralCrossRefGoogle Scholar
  242. 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 149:1060–1072PubMedPubMedCentralCrossRefGoogle Scholar
  243. 243.
    Conrad M, Angeli JP, Vandenabeele P, Stockwell BR (2016) Nat Rev Drug Discov 15:348–366PubMedPubMedCentralCrossRefGoogle Scholar
  244. 244.
    Masaldan S, Bush AI, Devos D, Rolland AS, Moreau C (2019) Free Radic Biol Med 133:221–233PubMedCrossRefGoogle Scholar
  245. 245.
    Ursini F, Maiorino M, Valente M, Ferri L, Gregolin C (1982) Biochim Biophys Acta 710:197–211PubMedCrossRefGoogle Scholar
  246. 246.
    Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR (2016) Proc Natl Acad Sci USA 113:E4966–E4975PubMedCrossRefGoogle Scholar
  247. 247.
    Shah R, Shchepinov MS, Pratt DA (2018) ACS Cent Sci 4:387–396PubMedPubMedCentralCrossRefGoogle Scholar
  248. 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 13:91–98PubMedCrossRefGoogle Scholar
  249. 249.
    Reed JC, Pellecchia M (2012) Cell 149:963–965PubMedCrossRefGoogle Scholar
  250. 250.
    Yang WS, Stockwell BR (2008) Chem Biol 15:234–245PubMedPubMedCentralCrossRefGoogle Scholar
  251. 251.
    Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC (2014) Nature 509:105–109PubMedPubMedCentralCrossRefGoogle Scholar
  252. 252.
    Pratico D, Sung S (2004) J Alzheimers Dis 6:171–175PubMedCrossRefGoogle Scholar
  253. 253.
    Reed TT, Pierce WM, Markesbery WR, Butterfield DA (2009) Brain Res 1274:66–76PubMedCrossRefGoogle Scholar
  254. 254.
    Mandal PK, Saharan S, Tripathi M, Murari G (2015) Biol Psychiatry 78:702–710PubMedCrossRefGoogle Scholar
  255. 255.
    Raefsky SM, Furman R, Milne G, Pollock E, Axelsen P, Mattson MP, Shchepinov MS (2018) Neurobiol Aging 66:165–176PubMedPubMedCentralCrossRefGoogle Scholar
  256. 256.
    Hambright WS, Fonseca RS, Chen L, Na R, Ran Q (2017) Redox Biol 12:8–17PubMedPubMedCentralCrossRefGoogle Scholar
  257. 257.
    Weinreb O, Mandel S, Youdim MBH, Amit T (2013) Free Radic Biol Med 62:52–64PubMedCrossRefGoogle Scholar
  258. 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:e0157602PubMedPubMedCentralCrossRefGoogle Scholar
  259. 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 94:169–178CrossRefGoogle Scholar
  260. 260.
    Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH (2004) Neurology 62:1758–1765PubMedCrossRefGoogle Scholar
  261. 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 9:2918PubMedPubMedCentralCrossRefGoogle Scholar
  262. 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 15:681–689PubMedCrossRefGoogle Scholar

Copyright information

© Society for Biological Inorganic Chemistry (SBIC) 2019

Authors and Affiliations

  1. 1.Melbourne Dementia Research Centre, The Florey Institute of Neuroscience and Mental HealthThe University of MelbourneParkvilleAustralia

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