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).
Similar content being viewed by others
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
Halliwell B (2006) J Neurochem 97:1634–1658
Butterfield DA, Halliwell B (2019) Nat Rev Neurosci 20:148–160
Bush AI (2003) Trends Neurosci 26:207–214
Gaier ED, Eipper BA, Mains RE (2013) J Neurosci Res 91:2–19
Belaidi AA, Bush AI (2016) J Neurochem 139(Suppl 1):179–197
Opazo CM, Greenough MA, Bush AI (2014) Front Aging Neurosci 6:143
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
Angelova DF, Brown DR (2015) Metals 5:2070–2092
Choi BS, Zheng W (2009) Brain Res 1248:14–21
Meyer LA, Durley AP, Prohaska JR, Harris ZL (2001) J Biol Chem 276:36857–36861
Maryon EB, Molloy SA, Kaplan JH (2013) Am J Physiol Cell Physiol 304:C768–C779
Tapia L, Gonzalez-Aguero M, Cisternas MF, Suazo M, Cambiazo V, Uauy R, Gonzalez M (2004) Biochem J 378:617–624
La Fontaine S, Mercer JF (2007) Arch Biochem Biophys 463:149–167
Linz R, Lutsenko S (2007) J Bioenerg Biomembr 39:403–407
Greenough M, Pase L, Voskoboinik I, Petris MJ, O’Brien AW, Camakaris J (2004) Am J Physiol Cell Physiol 287:C1463–C1471
Pase L, Voskoboinik I, Greenough M, Camakaris J (2004) Biochem J 378:1031–1037
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
Moos T, Morgan EH (2004) J Neurochem 88:233–245
Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) Lancet Neurol 13:1045–1060
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
Wang CY, Jenkitkasemwong S, Duarte S, Sparkman BK, Shawki A, Mackenzie B, Knutson MD (2012) J Biol Chem 287:34032–34043
Zhao N, Gao J, Enns CA, Knutson MD (2010) J Biol Chem 285:32141–32150
Gunshin H, Mackenzie B, Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Nature 388:482–488
Ji C, Kosman DJ (2015) J Neurochem 133:668–683
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
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
Nandal A, Ruiz JC, Subramanian P, Ghimire-Rijal S, Sinnamon RA, Stemmler TL, Bruick RK, Philpott CC (2011) Cell Metab 14:647–657
Pantopoulos K (2004) Ann N Y Acad Sci 1012:1–13
Zhang DL, Ghosh MC, Rouault TA (2014) Front Pharmacol 5:124
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
Asano T, Komatsu M, Yamaguchi-Iwai Y, Ishikawa F, Mizushima N, Iwai K (2011) Mol Cell Biol 31:2040–2052
Nitti M, Piras S, Brondolo L, Marinari UM, Pronzato MA, Furfaro AL (2018) Int J Mol Sci 19:2260–2280
Zhang YW, Thompson R, Zhang H, Xu H (2011) Mol Brain 4:3
Unzeta M, Esteban G, Bolea I, Fogel WA, Ramsay RR, Youdim MB, Tipton KF, Marco-Contelles J (2016) Front Neurosci 10:205
Wimo A, Jonsson L, Bond J, Prince M, Winblad B, I. Alzheimer Disease (2013) Alzheimers Dement 9:1–11
Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR (2000) Brain Res Brain Res Rev 33:95–130
Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Proc Natl Acad Sci USA 82:4245–4249
Davies P, Maloney AJ (1976) Lancet 2:1403
Drachman DA, Leavitt J (1974) Arch Neurol 30:113–121
Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, Delon MR (1982) Science 215:1237–1239
Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR (1998) J Neurol Sci 158:47–52
Pithadia AS, Lim MH (2012) Curr Opin Chem Biol 16:67–73
Raven EP, Lu PH, Tishler TA, Heydari P, Bartzokis G (2013) J Alzheimers Dis 37:127–136
Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, Carey PR (2003) Biochemistry 42:2768–2773
Miller LM, Wang Q, Telivala TP, Smith RJ, Lanzirotti A, Miklossy J (2006) J Struct Biol 155:30–37
Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, Smith MA (2000) J Neurochem 74:270–279
Smith MA, Harris PL, Sayre LM, Perry G (1997) Proc Natl Acad Sci USA 94:9866–9868
Deibel MA, Ehmann WD, Markesbery WR (1996) J Neurol Sci 143:137–142
Zatta P, Drago D, Bolognin S, Sensi SL (2009) Trends Pharmacol Sci 30:346–355
Bishop GM, Robinson SR, Liu Q, Perry G, Atwood CS, Smith MA (2002) Dev Neurosci 24:184–187
Roberts BR, Ryan TM, Bush AI, Masters CL, Duce JA (2012) J Neurochem 120(Suppl 1):149–166
Schrag M, Mueller C, Oyoyo U, Smith MA, Kirsch WM (2011) Prog Neurobiol 94:296–306
Schrag M, Mueller C, Zabel M, Crofton A, Kirsch WM, Ghribi O, Squitti R, Perry G (2013) Neurobiol Dis 59:100–110
Ayton S, James SA, Bush AI (2017) Cell Chem Biol 24:1192–1194
Hwang EJ, Kim HG, Kim D, Rhee HY, Ryu CW, Liu T, Wang Y, Jahng GH (2016) Med Phys 43:4718
Luo Z, Zhuang X, Kumar D, Wu X, Yue C, Han C, Lv J (2013) PLoS One 8:e76203
Connor JR, Menzies SL, St Martin SM, Mufson EJ (1992) J Neurosci Res 31:75–83
Meadowcroft MD, Connor JR, Smith MB, Yang QX (2009) J Magn Reson Imaging 29:997–1007
Valensin D, Migliorini C, Valensin G, Gaggelli E, La Penna G, Kozlowski H, Gabbiani C, Messori L (2011) Inorg Chem 50:6865–6867
Dikalov SI, Vitek MP, Mason RP (2004) Free Radic Biol Med 36:340–347
Guilloreau L, Combalbert S, Sournia-Saquet A, Mazarguil H, Faller P (2007) ChemBioChem 8:1317–1325
Nadal RC, Rigby SE, Viles JH (2008) Biochemistry 47:11653–11664
Nakamura M, Shishido N, Nunomura A, Smith MA, Perry G, Hayashi Y, Nakayama K, Hayashi T (2007) Biochemistry 46:12737–12743
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
Taniguchi A, Sasaki D, Shiohara A, Iwatsubo T, Tomita T, Sohma Y, Kanai M (2014) Angew Chem Int Ed Engl 53:1382–1385
Cheignon C, Faller P, Testemale D, Hureau C, Collin F (2016) Metallomics 8:1081–1089
Butterfield DA, Reed T, Newman SF, Sultana R (2007) Free Radic Biol Med 43:658–677
Selfridge JE, Lezi E, Lu J, Swerdlow RH (2013) Neurobiol Dis 51:3–12
Zhao Y, Zhao B (2013) Oxid Med Cell Longev 2013:316523
Gabbita SP, Lovell MA, Markesbery WR (1998) J Neurochem 71:2034–2040
Hardas SS, Sultana R, Clark AM, Beckett TL, Szweda LI, Murphy MP, Butterfield DA (2013) Redox Biol 1:80–85
Markesbery WR, Lovell MA (1998) Neurobiol Aging 19:33–36
Mecocci P, MacGarvey U, Beal MF (1994) Ann Neurol 36:747–751
Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) J Neurochem 68:2092–2097
Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI (2000) J Neurochem 75:1219–1233
Barritt JD, Viles JH (2015) J Biol Chem 290:27791–27802
Drew SC (2017) Front Neurosci 11:317
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
Sarell CJ, Syme CD, Rigby SE, Viles JH (2009) Biochemistry 48:4388–4402
Huang X, Atwood CS, Moir RD, Hartshorn MA, Tanzi RE, Bush AI (2004) J Biol Inorg Chem 9:954–960
Dai XL, Sun YX, Jiang ZF (2006) Acta Biochim Biophys Sin (Shanghai) 38:765–772
Sarell CJ, Wilkinson SR, Viles JH (2010) J Biol Chem 285:41533–41540
Greenough MA, Camakaris J, Bush AI (2013) Neurochem Int 62:540–555
Grundke-Iqbal I, Fleming J, Tung YC, Lassmann H, Iqbal K, Joshi JG (1990) Acta Neuropathol 81:105–110
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
Bolognin S, Messori L, Drago D, Gabbiani C, Cendron L, Zatta P (2011) Int J Biochem Cell Biol 43:877–885
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
Ma Q, Li Y, Du J, Liu H, Kanazawa K, Nemoto T, Nakanishi H, Zhao Y (2006) Peptides 27:841–849
Ma QF, Li YM, Du JT, Kanazawa K, Nemoto T, Nakanishi H, Zhao YF (2005) Biopolymers 79:74–85
Martic S, Rains MK, Kraatz HB (2013) Anal Biochem 442:130–137
Soragni A, Zambelli B, Mukrasch MD, Biernat J, Jeganathan S, Griesinger C, Ciurli S, Mandelkow E, Zweckstetter M (2008) Biochemistry 47:10841–10851
Kitazawa M, Cheng D, Laferla FM (2009) J Neurochem 108:1550–1560
Voss K, Harris C, Ralle M, Duffy M, Murchison C, Quinn JF (2014) Transl Neurodegener 3:24
Faller P, Hureau C (2009) Dalton Trans. https://doi.org/10.1039/b813398k:1080-1094
Hesse L, Beher D, Masters CL, Multhaup G (1994) FEBS Lett 349:109–116
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
Miller Y, Ma B, Nussinov R (2010) Proc Natl Acad Sci USA 107:9490–9495
Treiber C, Simons A, Strauss M, Hafner M, Cappai R, Bayer TA, Multhaup G (2004) J Biol Chem 279:51958–51964
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
Bellingham SA, Ciccotosto GD, Needham BE, Fodero LR, White AR, Masters CL, Cappai R, Camakaris J (2004) J Neurochem 91:423–428
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
Wong BX, Tsatsanis A, Lim LQ, Adlard PA, Bush AI, Duce JA (2014) PLoS One 9:e114174
Cho HH, Cahill CM, Vanderburg CR, Scherzer CR, Wang B, Huang X, Rogers JT (2010) J Biol Chem 285:31217–31232
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
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
Hou P, Liu G, Zhao Y, Shi Z, Zheng Q, Bu G, Xu H, Zhang YW (2015) Neurobiol Aging 36:1310–1315
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
Gerber H, Wu F, Dimitrov M, Osuna GM, Fraering PC (2017) J Biol Chem 292:3751–3767
Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G (1999) Biochem J 344(Pt 2):461–467
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
Hardy JA, Higgins GA (1992) Science 256:184–185
Masaldan S, Belaidi AA, Ayton S, Bush AI (2019) Pharmaceuticals (Basel) 12:93
Nikseresht S, Bush AI, Ayton S (2019) Br J Pharmacol 176:3622–3635
Li C, Wang J, Zhou B (2010) J Alzheimers Dis 21:1249–1262
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
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
LeVine H 3rd, Ding Q, Walker JA, Voss RS, Augelli-Szafran CE (2009) Neurosci Lett 465:99–103
Mancino AM, Hindo SS, Kochi A, Lim MH (2009) Inorg Chem 48:9596–9598
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
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
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
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
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
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
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
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
Crapper McLachlan DR, Dalton AJ, Kruck TP, Bell MY, Smith WL, Kalow W, Andrews DF (1991) Lancet 337:1304–1308
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
Guo C, Wang P, Zhong ML, Wang T, Huang XS, Li JY, Wang ZY (2013) Neurochem Int 62:165–172
Banerjee P, Sahoo A, Anand S, Bir A, Chakrabarti S (2016) J Alzheimers Dis 49:681–693
Kupershmidt L, Amit T, Bar-Am O, Youdim MB, Weinreb O (2012) Antioxid Redox Signal 17:860–877
Molina-Holgado F, Gaeta A, Francis PT, Williams RJ, Hider RC (2008) J Neurochem 105:2466–2476
Prasanthi JR, Schrag M, Dasari B, Marwarha G, Dickson A, Kirsch WM, Ghribi O (2012) J Alzheimers Dis 30:167–182
Lang AE, Lozano AM (1998) N Engl J Med 339:1130–1143
Jankovic J (2008) J Neurol Neurosurg Psychiatry 79:368–376
Schulz JB (2008) J Neurol 255(Suppl 5):3–7
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
Pall HS, Williams AC, Blake DR, Lunec J, Gutteridge JM, Hall M, Taylor A (1987) Lancet 2:238–241
Arnal N, Cristalli DO, de Alaniz MJ, Marra CA (2010) Brain Res 1319:118–130
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
Torsdottir G, Kristinsson J, Sveinbjornsdottir S, Snaedal J, Johannesson T (1999) Pharmacol Toxicol 85:239–243
Davies KM, Mercer JF, Chen N, Double KL (2016) Clin Sci (Lond) 130:565–574
Montes S, Rivera-Mancia S, Diaz-Ruiz A, Tristan-Lopez L, Rios C (2014) Oxid Med Cell Longev 2014:147251
Howells C, West AK, Chung RS (2010) FEBS J 277:2931–2939
Dexter DT, Wells FR, Agid F, Agid Y, Lees AJ, Jenner P, Marsden CD (1987) Lancet 2:1219–1220
Dexter DT, Wells FR, Lees AJ, Agid F, Agid Y, Jenner P, Marsden CD (1989) J Neurochem 52:1830–1836
Hirsch EC, Brandel JP, Galle P, Javoy-Agid F, Agid Y (1991) J Neurochem 56:446–451
Riederer P, Sofic E, Rausch WD, Schmidt B, Reynolds GP, Jellinger K, Youdim MB (1989) J Neurochem 52:515–520
Double KL, Reyes S, Werry EL, Halliday GM (2010) Prog Neurobiol 92:316–329
Frank-Cannon TC, Alto LT, McAlpine FE, Tansey MG (2009) Mol Neurodegener 4:47
Gerlach M, Double KL, Youdim MB, Riederer P (2006) J Neural Transm Suppl 70:133–142
Mills E, Dong XP, Wang F, Xu H (2010) Future Med Chem 2:51–64
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
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
Conway KA, Harper JD, Lansbury PT (1998) Nat Med 4:1318–1320
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
Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, Lee VM (2002) Neuron 34:521–533
Yu Z, Xu X, Xiang Z, Zhou J, Zhang Z, Hu C, He C (2010) PLoS One 5:e9956
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
Abeyawardhane DL, Heitger DR, Fernandez RD, Forney AK, Lucas HR (2019) ACS Chem Neurosci 10:1402–1410
Paik SR, Shin HJ, Lee JH, Chang CS, Kim J (1999) Biochem J 340(Pt 3):821–828
Uversky VN, Li J, Fink AL (2001) J Biol Chem 276:44284–44296
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
Mason RJ, Paskins AR, Dalton CF, Smith DP (2016) Biochemistry 55:4737–4741
Lu Y, Prudent M, Fauvet B, Lashuel HA, Girault HH (2011) ACS Chem Neurosci 2:667–675
Wang C, Liu L, Zhang L, Peng Y, Zhou F (2010) Biochemistry 49:8134–8142
Abeyawardhane DL, Fernandez RD, Heitger DR, Crozier MK, Wolver JC, Lucas HR (2018) J Am Chem Soc 140:17086–17094
Peng Y, Wang C, Xu HH, Liu YN, Zhou F (2010) J Inorg Biochem 104:365–370
Chen B, Wen X, Jiang H, Wang J, Song N, Xie J (2019) Free Radic Biol Med 141:253–260
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
Cobley JN, Fiorello ML, Bailey DM (2018) Redox Biol 15:490–503
Munoz P, Cardenas S, Huenchuguala S, Briceno A, Couve E, Paris I, Segura-Aguilar J (2015) Toxicol Sci 145:37–47
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
Maker HS, Weiss C, Silides DJ, Cohen G (1981) J Neurochem 36:589–593
Wada K, Fujibayashi Y, Tajima N, Yokoyama A (1994) Biol Pharm Bull 17:701–704
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
Dearling JL, Packard AB (2010) Nucl Med Biol 37:237–243
Fujibayashi Y, Taniuchi H, Yonekura Y, Ohtani H, Konishi J, Yokoyama A (1997) J Nucl Med 38:1155–1160
Vavere AL, Lewis JS (2007) Dalton Trans. https://doi.org/10.1039/b705989b:4893-4902
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
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
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
Cohen AR, Galanello R, Piga A, De Sanctis V, Tricta F (2003) Blood 102:1583–1587
Galanello R, Campus S (2009) Acta Haematol 122:155–164
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
Glickstein H, El RB, Shvartsman M, Cabantchik ZI (2005) Blood 106:3242–3250
Sohn YS, Mitterstiller AM, Breuer W, Weiss G, Cabantchik ZI (2011) Br J Pharmacol 164:406–418
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
Saberi S, Stauffer JE, Schulte DJ, Ravits J (2015) Neurol Clin 33:855–876
Pratt AJ, Getzoff ED, Perry JJ (2012) Degener Neurol Neuromuscul Dis 2:1–14
Bensimon G, Lacomblez L, Meininger V (1994) N Engl J Med 330:585–591
Sreedharan J, Brown RH Jr (2013) Ann Neurol 74:309–316
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
Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK (2008) Neurobiol Dis 30:400–407
Barber SC, Shaw PJ (2010) Free Radic Biol Med 48:629–641
Rothstein JD (2009) Ann Neurol 65(Suppl 1):S3–S9
Banci L, Bertini I, Boca M, Girotto S, Martinelli M, Valentine JS, Vieru M (2008) PLoS One 3:e1677
Culotta VC, Yang M, O’Halloran TV (2006) Biochim Biophys Acta 1763:747–758
Valentine JS, Doucette PA, Zittin Potter S (2005) Annu Rev Biochem 74:563–593
Beckman JS, Carson M, Smith CD, Koppenol WH (1993) Nature 364:584
Leal SS, Cristovao JS, Biesemeier A, Cardoso I, Gomes CM (2015) Metallomics 7:333–346
Tokuda E, Okawa E, Ono S (2009) J Neurochem 111:181–191
Tokuda E, Okawa E, Watanabe S, Ono S, Marklund SL (2013) Neurobiol Dis 54:308–319
Gong YH, Elliott JL (2000) Exp Neurol 162:27–36
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
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
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
Morimoto S, Kuzuhara S, Kokubo Y (2009) Mov Disord 24:123–126
Nakagomi S, Barsoum MJ, Bossy-Wetzel E, Sutterlin C, Malhotra V, Lipton SA (2008) Neurobiol Dis 29:221–231
Smith RG, Henry YK, Mattson MP, Appel SH (1998) Ann Neurol 44:696–699
Cheung G, Gawel MJ, Cooper PW, Farb RI, Ang LC, Gawal MJ (1995) Radiology 194:263–270
Hecht MJ, Fellner F, Fellner C, Hilz MJ, Neundorfer B, Heuss D (2002) J Neurol Sci 199:59–65
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
Yasui M, Ota K, Garruto RM (1993) Neurotoxicology 14:445–450
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
Ignjatovic A, Stevic Z, Lavrnic D, Nikolic-Kokic A, Blagojevic D, Spasic M, Spasojevic I (2012) Amyotroph Lateral Scler 13:357–362
Jeong SY, Rathore KI, Schulz K, Ponka P, Arosio P, David S (2009) J Neurosci 29:610–619
Wang Q, Zhang X, Chen S, Zhang X, Zhang S, Youdium M, Le W (2011) Neurodegener Dis 8:310–321
Goodall EF, Haque MS, Morrison KE (2008) J Neurol 255:1652–1656
Qureshi M, Brown RH Jr, Rogers JT, Cudkowicz ME (2008) Open Neurol J 2:51–54
Yu J, Wang N, Qi F, Wang X, Zhu Q, Lu Y, Zhang H, Che F, Li W (2018) Biomed Rep 9:333–338
Ikeda K, Hirayama T, Takazawa T, Kawabe K, Iwasaki Y (2012) Intern Med 51:1501–1508
Nadjar Y, Gordon P, Corcia P, Bensimon G, Pieroni L, Meininger V, Salachas F (2012) PLoS One 7:e45034
Mitchell RM, Simmons Z, Beard JL, Stephens HE, Connor JR (2010) Muscle Nerve 42:95–103
McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG (1993) Glia 7:84–92
Kang SH, Li Y, Fukaya M, Lorenzini I, Cleveland DW, Ostrow LW, Rothstein JD, Bergles DE (2013) Nat Neurosci 16:571–579
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
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
McAllum EJ, Roberts BR, Hickey JL, Dang TN, Grubman A, Donnelly PS, Liddell JR, White AR, Crouch PJ (2015) Neurobiol Dis 81:20–24
Vieira FG, Hatzipetros T, Thompson K, Moreno AJ, Kidd JD, Tassinari VR, Levine B, Perrin S, Gill A (2017) IBRO Rep 2:47–53
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
Son M, Elliott JL (2014) J Neurol Sci 336:1–7
Son M, Leary SC, Romain N, Pierrel F, Winge DR, Haller RG, Elliott JL (2008) J Biol Chem 283:12267–12275
Avramovich-Tirosh Y, Bar-Am O, Amit T, Youdim MB, Weinreb O (2010) Curr Alzheimer Res 7:300–306
Kupershmidt L, Weinreb O, Amit T, Mandel S, Carri MT, Youdim MB (2009) FASEB J 23:3766–3779
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
Wang Y, Mao XO, Xie L, Banwait S, Marti HH, Greenberg DA, Jin K (2007) J Neurosci 27:304–307
Lysogorskaia EV, Abramycheva N, Zakharova MN, Illarioshkin SN (2012) Zh Nevrol Psikhiatr Im S S Korsakova 112:42–45
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
Beerepoot LV, Shima DT, Kuroki M, Yeo KT, Voest EE (1996) Cancer Res 56:3747–3751
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
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
Conrad M, Angeli JP, Vandenabeele P, Stockwell BR (2016) Nat Rev Drug Discov 15:348–366
Masaldan S, Bush AI, Devos D, Rolland AS, Moreau C (2019) Free Radic Biol Med 133:221–233
Ursini F, Maiorino M, Valente M, Ferri L, Gregolin C (1982) Biochim Biophys Acta 710:197–211
Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR (2016) Proc Natl Acad Sci USA 113:E4966–E4975
Shah R, Shchepinov MS, Pratt DA (2018) ACS Cent Sci 4:387–396
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
Reed JC, Pellecchia M (2012) Cell 149:963–965
Yang WS, Stockwell BR (2008) Chem Biol 15:234–245
Mancias JD, Wang X, Gygi SP, Harper JW, Kimmelman AC (2014) Nature 509:105–109
Pratico D, Sung S (2004) J Alzheimers Dis 6:171–175
Reed TT, Pierce WM, Markesbery WR, Butterfield DA (2009) Brain Res 1274:66–76
Mandal PK, Saharan S, Tripathi M, Murari G (2015) Biol Psychiatry 78:702–710
Raefsky SM, Furman R, Milne G, Pollock E, Axelsen P, Mattson MP, Shchepinov MS (2018) Neurobiol Aging 66:165–176
Hambright WS, Fonseca RS, Chen L, Na R, Ran Q (2017) Redox Biol 12:8–17
Weinreb O, Mandel S, Youdim MBH, Amit T (2013) Free Radic Biol Med 62:52–64
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
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
Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH (2004) Neurology 62:1758–1765
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
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
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
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.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00775-019-01731-9