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Rebalancing metal dyshomeostasis for Alzheimer’s disease therapy

  • Guan‐Jun Yang
  • Hao Liu
  • Dik-Lung MaEmail author
  • Chung-Hang LeungEmail author
Mini Review
Part of the following topical collections:
  1. Metal Ions and Degenerative Diseases

Abstract

Alzheimer’s disease (AD) is a type of neurodegenerative malady that is associated with the accumulation of amyloid plaques. Metal ions are critical for the development and upkeep of brain activity, but metal dyshomeostasis can contribute to the development of neurodegenerative diseases, including AD. This review highlights the association between metal dyshomeostasis and AD pathology, the feasibility of rebalancing metal homeostasis as a therapeutic strategy for AD, and a survey of current drugs that action via rebalancing metal homeostasis. Finally, we discuss the challenges that should be overcome by researchers in the future to enable the practical use of metal homeostasis rebalancing agents for clinical application.

Keywords

Metal dyshomeostasis Metal ions Alzheimer’s disease Metal chelators Aβ aggregation inhibitors Multifunctional agents 

Abbreviations

AD

Alzheimer’s disease

Amyloid-beta

BBB

Blood–brain barrier

CNS

Central nervous system

APP

Amyloid precursor protein

ROS

Reactive oxygen species

8HQ

8-Hydroxyquinoline

CQ

Clioquinol

DFP

Deferiprone

TETA

Trientine

DFO

Desferrioxamine

EGCG

(−)-Epigallocatechin-3-gallate

BACE1

β-Secretase

AChE

Acetylcholinesterase

NMDA

N-Methyl-d-aspartic acid

Notes

Acknowledgements

This work is supported by Hong Kong Baptist University (FRG2/17-18/003, China), the Health and Medical Research Fund (HMRF/14150561, China), the National Natural Science Foundation of China (21575121 and 21775131, China), the Hong Kong Baptist University Century Club Sponsorship Scheme 2018 (China), the Interdisciplinary Research Matching Scheme (RC-IRMS/16-17/03, China), Interdisciplinary Research Clusters Matching Scheme (RC-IRCs/17-18/03, China), Collaborative Research Fund (C5026-16G, China), SKLEBA and HKBU Strategic Development Fund (SKLP_1718_P04, China), the Funded by The Science and Technology Development Fund, Macau SAR (File no. 077/2016/A2 and SKL-QRCM-2017-2019) and the University of Macau (MYRG2016-00151-ICMS-QRCM and MYRG2018-00187-ICMS, China).

Compliance with ethical standards

Conflict of interest

Authors declare that there are no conflicts of interest.

References

  1. 1.
    Duce JA, Bush AI (2010) Prog Neurobiol 92:1–18CrossRefPubMedGoogle Scholar
  2. 2.
    Liu G, Huang W, Moir RD, Vanderburg CR, Lai B, Peng Z, Tanzi RE, Rogers JT, Huang X (2006) J Struct Biol 155:45–51CrossRefPubMedGoogle Scholar
  3. 3.
    Zatta P, Lucchini R, van Rensburg SJ, Taylor A (2003) Brain Res Bull 62:15–28CrossRefPubMedGoogle Scholar
  4. 4.
    Budimir A (2011) Acta Pharm 61:1–14CrossRefPubMedGoogle Scholar
  5. 5.
    Cristóvão JS, Santos R, Gomes CM (2016) Oxid Med Cell Longev 2016:9812178CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Zhu YP, Feng Y, Liu T, Wu YC (2015) Integr Med Int 2:63–72CrossRefGoogle Scholar
  7. 7.
    Squitti R, Salustri C (2011) Alzheimer's disease pathogenesis-core concepts, shifting paradigms and therapeutic targets. In: Monte SDL (ed) IntechOpen, Hampshire, pp 369–402Google Scholar
  8. 8.
    Rivera-Mancía S, Pérez-Neri I, Ríos C, Tristán-López L, Rivera-Espinosa L, Montes S (2010) Chem Biol Interact 186:184–199CrossRefPubMedGoogle Scholar
  9. 9.
    Savelieff MG, Lee S, Liu Y, Lim MH (2013) ACS Chem Biol 8:856–865CrossRefPubMedGoogle Scholar
  10. 10.
    Gupta UC, Gupta SC (2011) Curr Nutr Food Sci 7:221–231CrossRefGoogle Scholar
  11. 11.
    Adlard PA, Cherny RA, Finkelstein DI, Gautier E, Robb E, Cortes M, Volitakis I, Liu X, Smith JP, Perez K (2008) Neuron 59:43–55CrossRefPubMedGoogle Scholar
  12. 12.
    Choi JS, Braymer JJ, Nanga RP, Ramamoorthy A, Lim MH (2010) Proc Natl Acad Sci USA 107:21990–21995CrossRefPubMedGoogle Scholar
  13. 13.
    Chen YC, Chiu YJ, Lin CH, Hsu WC, Wu JL, Huang CH, Lin CW, Yao CF, Huang HJ, Lo YS, Chen CM, Wu YR, Chang KH, Lee-Chen GJ, Mei Hsieh-Li H (2019) J Alzheimers Dis 67:737–756PubMedGoogle Scholar
  14. 14.
    Xie Y, Liu Q, Zheng L, Wang B, Qu X, Ni J, Zhang Y, Du X (2018) Mol Nutr Food Res 62:1800107CrossRefGoogle Scholar
  15. 15.
    Kawada H, Blessing K, Kiyota T, Woolman T, Winchester L, Kador PF (2015) J Alzheimers Dis 44:297–307CrossRefPubMedGoogle Scholar
  16. 16.
    Kepp KP (2012) Chem Rev 112:5193–5239CrossRefPubMedGoogle Scholar
  17. 17.
    Gschwind A, Zwick E, Prenzel N, Leserer M, Ullrich A (2001) Oncogene 20:1594CrossRefPubMedGoogle Scholar
  18. 18.
    Zheng W, Monnot AD (2012) Pharmacol Ther 133:177–188CrossRefPubMedGoogle Scholar
  19. 19.
    Yokel RA (2006) J Alzheimers Dis 10:223–253CrossRefPubMedGoogle Scholar
  20. 20.
    Choi BS, Zheng W (2009) Brain Res 1248:14–21CrossRefPubMedGoogle Scholar
  21. 21.
    Ximenes-da-Silva A (2016) Front Neurosci 10:233CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Ergen K, Ince H, Düzova H, Karakoç Y, Emre MH (2013) Balkan Med J 30:105CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Scheiber IF, Mercer JF, Dringen R (2014) Prog Neurobiol 116:33–57CrossRefPubMedGoogle Scholar
  24. 24.
    Dringen R, Bishop GM, Koeppe M, Dang TN, Robinson SR (2007) Neurochem Res 32:1884–1890CrossRefPubMedGoogle Scholar
  25. 25.
    Tiffany-Castiglioni E, Hong S, Qian Y (2011) Int J Dev Neurosci 29:811–818CrossRefPubMedGoogle Scholar
  26. 26.
    Brown DR (2004) Neurobiol Dis 15:534–543CrossRefPubMedGoogle Scholar
  27. 27.
    Hatori Y, Yan Y, Schmidt K, Furukawa E, Hasan NM, Yang N, Liu N, Sockanathan S, Lutsenko S (2016) Nat Commun 7:10640CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Mathie A, Sutton GL, Clarke CE, Veale EL (2006) Pharmacol Ther 111:567–583CrossRefPubMedGoogle Scholar
  29. 29.
    Opazo CM, Greenough MA, Bush AI (2014) Front Aging Neurosci 6:143CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Bush AI, Tanzi RE (2008) Neurotherapeutics 5:421–432CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Barnham KJ, McKinstry WJ, Multhaup G, Galatis D, Morton CJ, Curtain CC, Williamson NA, White AR, Hinds MG, Norton RS, Beyreuther K, Masters CL, Parker MW, Cappai R (2003) J Biol Chem 278:17401–17407CrossRefPubMedGoogle Scholar
  32. 32.
    Ciuculescu ED, Mekmouche Y, Faller P (2005) Chem Eur J 11:903–909CrossRefPubMedGoogle Scholar
  33. 33.
    Lee MC, Yu WC, Shih YH, Chen CY, Guo ZH, Huang SJ, Chan JC, Chen YR (2018) Sci Rep 8:4772CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Matheou CJ, Younan ND, Viles JH (2016) J Mol Biol 428:2832–2846CrossRefPubMedGoogle Scholar
  35. 35.
    Hsu HW, Bondy SC, Kitazawa M (2018) Toxicol Sci 163:338–345CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI (2000) J Neurochem 75:1219–1233CrossRefPubMedGoogle Scholar
  37. 37.
    Davenward S, Bentham P, Wright J, Crome P, Job D, Polwart A, Exley C (2013) J Alzheimers Dis 33:423–430CrossRefPubMedGoogle Scholar
  38. 38.
    McLachlan DR, Fraser PE, Dalton AJ (1992) Ciba Found Symp 169:87–89PubMedGoogle Scholar
  39. 39.
    Loy R, Tariot PN (2002) J Mol Neurosci 19:301–307CrossRefGoogle Scholar
  40. 40.
    Bush AI (2008) J Alzheimers Dis 15:223–240CrossRefPubMedGoogle Scholar
  41. 41.
    Bush AI (2013) J Alzheimers Dis 33:S277–S281CrossRefPubMedGoogle Scholar
  42. 42.
    Kepp KP (2017) Coord Chem Rev 351:127–159CrossRefGoogle Scholar
  43. 43.
    Palanimuthu D, Poon R, Sahni S, Anjum R, Hibbs D, Lin HY, Bernhardt PV, Kalinowski DS, Richardson DR (2017) Eur J Med Chem 139:612–632CrossRefPubMedGoogle Scholar
  44. 44.
    Reitz C (2012) Int J Alzheimers Dis 2012:369808PubMedPubMedCentralGoogle Scholar
  45. 45.
    Postina R (2012) J Neurochem 120:46–54CrossRefPubMedGoogle Scholar
  46. 46.
    Polanco JC, Li C, Bodea LG, Martinez-Marmol R, Meunier FA, Götz J (2018) Nat Rev Neurol 14:22CrossRefPubMedGoogle Scholar
  47. 47.
    Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wölfing H, Chieng BC, Christie MJ, Napier IA, Eckert A, Staufenbiel M, Hardeman E, Götz J (2010) Cell 142:387–397CrossRefPubMedGoogle Scholar
  48. 48.
    Hölscher C (2019) EBioMedicine 39:17–18CrossRefPubMedGoogle Scholar
  49. 49.
    Giuffrida ML, Caraci F, Pignataro B, Cataldo S, De Bona P, Bruno V, Molinaro G, Pappalardo G, Messina A, Palmigiano A (2009) J Neurochem 29:10582–10587Google Scholar
  50. 50.
    Atwood CS, Huang X, Moir RD, Tanzi RE, Bush AI (2018) In metal ions in biological systems. Routledge, Abingdon, pp 309–364CrossRefGoogle Scholar
  51. 51.
    Kim AC, Lim S, Kim YK (2018) Int J Mol Sci 19:128CrossRefPubMedCentralGoogle Scholar
  52. 52.
    Garza-Lombó C, Posadas Y, Quintanar L, Gonsebatt ME, Franco R (2018) Antioxid Redox Signal 28:1669–1703CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Nam E, Derrick JS, Lee S, Kang J, Han J, Lee SJC, Chung SW, Lim MH (2018) ACS Chem Neurosci 9:2655–2666CrossRefPubMedGoogle Scholar
  54. 54.
    Pohanka M (2018) Bratisl Lek Listy 119:535–543PubMedGoogle Scholar
  55. 55.
    Grasso G, Santoro AM, Lanza V, Sbardella D, Tundo GR, Ciaccio C, Marini S, Coletta M, Milardi D (2017) Coord Chem Rev 347:1–22CrossRefGoogle Scholar
  56. 56.
    Santoro AM, Monaco I, Attanasio F, Lanza V, Pappalardo G, Tomasello MF, Cunsolo A, Rizzarelli E, De Luigi A, Salmona M, Milardi D (2016) Sci Rep 6:33444CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Arena G, Bellia F, Frasca G, Grasso G, Lanza V, Rizzarelli E, Tabbì G, Zito V, Milardi D (2013) Inorg Chem 52:9567–9573CrossRefPubMedGoogle Scholar
  58. 58.
    Pellacani C, Costa L (2018) Environ Pollut 235:791–805CrossRefPubMedGoogle Scholar
  59. 59.
    Alsousi AA, Igwe OJ (2019) Exp Cell Res 374:19–28CrossRefPubMedGoogle Scholar
  60. 60.
    Song GL, Chen C, Wu QY, Zhang ZH, Zheng R, Chen Y, Jia SZ, Ni JZ (2018) Metallomics 10:1107–1115CrossRefPubMedGoogle Scholar
  61. 61.
    Guo C, Liu JL, Fan YG, Yang ZS, Wang ZY (2018) Front Neurosci 12:632CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Cao J, Hou J, Ping J, Cai D (2018) Mol Neurodegener 13:64CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Grubman A, White AR, Liddell JR (2014) Mitochondrial metals as a potential therapeutic target in neurodegeneration. Br J Pharmacol 171:2159–2173CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Nam E, Han J, Suh JM, Yi Y, Lim MH (2018) Curr Opin Chem Biol 43:8–14CrossRefPubMedGoogle Scholar
  65. 65.
    Koh JY, Kim HN, Hwang JJ, Kim YH, Park SE (2019) Mol Brain 12:18CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Boland B, Yu WH, Corti O, Mollereau B, Henriques A, Bezard E, Pastores GM, Rubinsztein DC, Nixon RA, Duchen MR, Mallucci GR, Kroemer G, Levine B, Eskelinen EL, Mochel F, Spedding M, Louis C, Martin OR, Millan MJ (2018) Nat Rev Drug Discov 17:660CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Chen LL, Huang YJ, Cui JT, Song N, Xie J (2019) ACS Chem Neurosci 10(2):863–871CrossRefPubMedGoogle Scholar
  68. 68.
    White AR, Kanninen K, Crouch P (2015) Front Aging Neurosci 7:127CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Crouch PJ, Savva MS, Hung LW, Donnelly PS, Mot AI, Parker SJ, Greenough MA, Volitakis I, Adlard PA, Cherny RA (2011) J Neurochem 119:220–230CrossRefPubMedGoogle Scholar
  70. 70.
    Prasanthi JRP, Schrag M, Dasari B, Marwarha G, Dickson A, Kirsch WM, Ghribi O (2012) J Alzheimer’s Dis 30:167–182CrossRefGoogle Scholar
  71. 71.
    Wang CY, Xie JW, Xu Y, Wang T, Cai JH, Wang X, Zhao BL, An L, Wang ZY (2013) Antioxid Redox Signal 19:2024–2039CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Weiss K, Manolaki N, Zuin M, Kruse C, Dhawan A (2018) J Hepatol 68:S106–S107CrossRefGoogle Scholar
  73. 73.
    Litwin T, Członkowska A, Socha P (2019) Clinical and translational perspectives on WILSON DISEASE. Academic Press, Cambridge, pp 357–364CrossRefGoogle Scholar
  74. 74.
    Smolen JS, Aletaha D (2015) Nat Rev Rheumatol 11:276CrossRefPubMedGoogle Scholar
  75. 75.
    Squitti R, Rossini PM, Cassetta E, Moffa F, Pasqualetti P, Cortesi M, Colloca A, Rossi L, Finazzi-Agro’ A (2002) Eur J Clin Investig 32:51–59CrossRefGoogle Scholar
  76. 76.
    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 277:45518–45528CrossRefPubMedGoogle Scholar
  77. 77.
    Lee JY, Friedman JE, Angel I, Kozak A, Koh JY (2004) Neurobiol Aging 25:1315–1321CrossRefPubMedGoogle Scholar
  78. 78.
    Lanza V, Milardi D, Di Natale G, Pappalardo G (2018) Curr Med Chem 25:525–539CrossRefPubMedGoogle Scholar
  79. 79.
    Palumbo CS, Schilsky ML (2019) Ann Transl Med 7(Suppl 2):S65CrossRefGoogle Scholar
  80. 80.
    Gracia RC, Snodgrass WR (2007) Am J Health Syst Pharm 64(1):45–53CrossRefPubMedGoogle Scholar
  81. 81.
    Hane F, Leonenko Z (2014) Biomolecules 4:101–116CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Yang GJ, Lei PM, Wong SY, Ma DL, Leung CH (2018) Molecules 23:3194CrossRefPubMedCentralGoogle Scholar
  83. 83.
    Yang GJ, Ko CN, Zhong HJ, Leung CH, Ma DL (2019) Cancers 11:92CrossRefPubMedCentralGoogle Scholar
  84. 84.
    Goozee KG, Shah TM, Sohrabi HR, Rainey-Smith SR, Brown B, Verdile G, Martins RN (2016) Br J Nutr 115:449–465CrossRefPubMedGoogle Scholar
  85. 85.
    Tang M, Taghibiglou C (2017) J Alzheimers Dis 58:1003–1016CrossRefPubMedGoogle Scholar
  86. 86.
    Dey A, Bhattacharya R, Mukherjee A, Pandey DK (2017) Biotechnol Adv 35:178–216CrossRefPubMedGoogle Scholar
  87. 87.
    Mori T, Koyama N, Tan J, Segawa T, Maeda M, Town T (2019) J Biol Chem 294:2714–2731CrossRefPubMedGoogle Scholar
  88. 88.
    Xicota L, Rodriguez-Morato J, Dierssen M, de la Torre R (2017) Curr Drug Targets 18:174–195CrossRefPubMedGoogle Scholar
  89. 89.
    Chang X, Rong C, Chen Y, Yang C, Hu Q, Mo Y, Zhang C, Gu X, Zhang L, He W, Cheng S, Hou X, Su R, Liu S, Dun W, Wang Q, Fang S (2015) Exp Cell Res 334:136–145CrossRefPubMedGoogle Scholar
  90. 90.
    Rojas C, Rojas-Castaneda J, Rojas P (2016) Curr Top Nutraceutical Res 14(1):1–16Google Scholar
  91. 91.
    Jiang M, Li J, Peng Q, Liu Y, Liu W, Luo C, Peng J, Li J, Yung KK, Mo Z (2014) J Neuroinflammation 11:167CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Kuo LC, Song YQ, Yao CA, Cheng IH, Chien CT, Lee GC, Yang WC, Lin Y (2018) J Agric Food Chem 67:81–89CrossRefPubMedGoogle Scholar
  93. 93.
    Bate C, Tayebi M, Williams A (2008) Mol Neurodegener 3:1CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Gill I, Kaur S, Kaur N, Dhiman M, Mantha AK (2017) J Alzheimers Dis 60:S25–S40CrossRefPubMedGoogle Scholar
  95. 95.
    Vitolo O, Gong B, Cao Z, Ishii H, Jaracz S, Nakanishi K, Arancio O, Dzyuba SV, Lefort R, Shelanski M (2009) Neurobiol Aging 30:257–265CrossRefPubMedGoogle Scholar
  96. 96.
    Goyal D, Shuaib S, Mann S, Goyal B (2017) ACS Comb Sci 19:55–80CrossRefPubMedGoogle Scholar
  97. 97.
    Dułak D, Banach M, Gadzała M, Konieczny L, Roterman I (2018) Acta Biochim Pol 65:595–604PubMedGoogle Scholar
  98. 98.
    Pizzi A, Dichiarante V, Terraneo G, Metrangolo P (2018) Pept Sci 110(5):e23088CrossRefGoogle Scholar
  99. 99.
    Villari V, Tosto R, Di Natale G, Sinopoli A, Tomasello MF, Lazzaro S, MicaliN Pappalardo G (2017) ChemistrySelect 2:9122–9129CrossRefGoogle Scholar
  100. 100.
    Shiryaev N, Jouroukhin Y, Giladi E, Polyzoidou E, Grigoriadis NC, Rosenmann H, Gozes I (2009) Neurobiol Dis 34:381–388CrossRefPubMedGoogle Scholar
  101. 101.
    Wang F, Zhou X-L, Yang Q-G, Xu W-H, Wang F, Chen Y-P, Chen G-H (2011) PLoS One 6:e27649CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Corona C, Frazzini V, Silvestri E, Lattanzio R, La Sorda VR, Piantelli M, Canzoniero LM, Ciavardelli D, Rizzarelli E, Sensi SL (2011) PLoS One 6:e17971CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Attanasio F, Convertino M, Magno A, Caflisch A, Corazza A, Haridas H, Esposito G, Cataldo S, Pignataro B, Milardi D, Rizzarelli E (2013) ChemBioChem 14:583–592CrossRefPubMedGoogle Scholar
  104. 104.
    Amijee H, Bate C, Williams A, Virdee J, Jeggo R, Spanswick D, Scopes DI, Treherne JM, Mazzitelli S, Chawner R (2012) Biochemistry 51:8338–8352CrossRefPubMedGoogle Scholar
  105. 105.
    Singh A, Hasan A, Tiwari S, Pandey LM (2018) CNS Neurol Disord Drug Targets 17:571–589CrossRefPubMedGoogle Scholar
  106. 106.
    Hamada Y, Miyamoto N, Kiso Y (2015) Bioorg Med Chem Lett 25:1572–1576CrossRefPubMedGoogle Scholar
  107. 107.
    Man BYW, Chan HM, Leung CH, Chan DSH, Bai LP, Jiang ZH, Li HW, Ma DL (2011) Chem Sci 2:917–921CrossRefGoogle Scholar
  108. 108.
    Lu L, Zhong HJ, Wang M, Ho SL, Li HW, Leung CH, Ma DL (2015) Sci Rep 5:14619CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Valensin D, Gabbiani C, Messori L (2012) Coord Chem Rev 256:2357–2366CrossRefGoogle Scholar
  110. 110.
    Barnham KJ, Kenche VB, Ciccotosto GD, Smith DP, Tew DJ, Liu X, Perez K, Cranston GA, Johanssen TJ, Volitakis I, Bush AI, Masters CL, White AR, Smith JP, Cherny RA, Cappai R (2008) Proc Natl Acad Sci USA 105:6813–6818CrossRefPubMedGoogle Scholar
  111. 111.
    Sasaki I, Bijani C, Ladeira S, Bourdon V, Faller P, Hureau C (2012) Dalton Trans 41:6404–6407CrossRefPubMedGoogle Scholar
  112. 112.
    Valensin D, Anzini P, Gaggelli E, Gaggelli N, Tamasi G, Cini R, Gabbiani C, Michelucci E, Messori L, Kozlowski H, Valensin G (2010) Inorg Chem 49:4720–4722CrossRefPubMedGoogle Scholar
  113. 113.
    Kumar A, Moody L, Olaivar JF, Lewis NA, Khade RL, Holder AA, Zhang Y, Rangachari V (2010) ACS Chem Neurosci 1:691–701CrossRefPubMedCentralGoogle Scholar
  114. 114.
    Price KA, Crouch PJ, Lim S, Paterson BM, Liddell JR, Donnelly PS, White AR (2011) Metallomics 3:1280–1290CrossRefPubMedGoogle Scholar
  115. 115.
    Lanza V, D’Agata R, Iacono G, Bellia F, Spoto G, Vecchio G (2015) J Inorg Biochem 153:377–382CrossRefPubMedGoogle Scholar
  116. 116.
    Zhang HY (2005) FEBS Lett 579:5260–5264CrossRefPubMedGoogle Scholar
  117. 117.
    Shimmyo Y, Kihara T, Akaike A, Niidome T, Sugimoto H (2008) J Neurosci Res 86:368–377CrossRefPubMedGoogle Scholar
  118. 118.
    Meunier J, Ieni J, Maurice T (2006) Br J Pharmacol 149:998–1012CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Dubois B, Tolosa E, Katzenschlager R, Emre M, Lees AJ, Schumann G, Pourcher E, Gray J, Thomas G, Swartz J, Hsu T, Moline ML (2012) Mov Disord 27(10):1230–1238CrossRefPubMedGoogle Scholar
  120. 120.
    Montero-Odasso M, Speechley M, Chertkow H, Sarquis-Adamson Y, Wells J, Borrie M, Vanderhaeghe L, Zou GY, Fraser S, Bherer L, Muir-Hunter SW (2019) Eur J Neurol 26(4):651–659CrossRefPubMedGoogle Scholar
  121. 121.
    Jiang N, Huang Q, Liu J, Liang N, Li Q, Li Q, Xie SS (2018) Eur J Med Chem 146:287–298CrossRefPubMedGoogle Scholar
  122. 122.
    Rodda J, Carter J (2012) BMJ 344:e2986CrossRefPubMedGoogle Scholar
  123. 123.
    Panek D, Więckowska A, Jończyk J, Godyń J, Bajda M, Wichur T, Pasieka A, Knez D, Pišlar A, Korabecny J, Soukup O, Sepsova V, Sabaté R, Kos J, Gobec S, Malawska B (2018) ACS Chem Neurosci 9:1074–1094CrossRefPubMedGoogle Scholar
  124. 124.
    Kumar S, Chowdhury S, Kumar S (2017) BMC Neurosci 18(1):76CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Dong X (2018) Theranostics 8:1481CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Hsu D (2017) A Marshall G. Curr Alzheimer Res 14:426–440PubMedPubMedCentralGoogle Scholar
  127. 127.
    Panza F, Solfrizzi V, Imbimbo BP, Logroscino G (2014) Expert Opin Biol Ther 14:1465–1476CrossRefPubMedGoogle Scholar
  128. 128.
    Sharma A, Pachauri V, Flora SJS (2018) Front Pharmacol 9:1247CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Savelieff MG, Nam G, Kang J, Lee HJ, Lee M, Lim MH (2018) Chem Rev 119:1221–1322CrossRefPubMedGoogle Scholar
  130. 130.
    Kenche VB, Barnham KJ (2011) Br J Pharmacol 163:211–219CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Konttinen H, Lejavová K, Malm T, Kanninen KM (2017) Biometals in neurodegenerative diseases. Elsevier, Amsterdam, pp 195–215CrossRefGoogle Scholar
  132. 132.
    Wang X, Wang X, Guo Z (2018) Coord Chem Rev 362:72–84CrossRefGoogle Scholar
  133. 133.
    Lee HJ, Savelieff MG, Kang J, Brophy MB, Nakashige TG, Lee SJC, Nolan EM, Lim MH (2018) Metallomics 10:1116–1127CrossRefPubMedGoogle Scholar

Copyright information

© Society for Biological Inorganic Chemistry (SBIC) 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical SciencesUniversity of MacauTaipaChina
  2. 2.Department of ChemistryHong Kong Baptist UniversityKowloonChina

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