Advertisement

Metal Complexing Agents for the Treatment of Alzheimer's Disease

Chapter
Part of the Topics in Medicinal Chemistry book series (TMC, volume 2)

Abstract

Alzheimer's disease (AD) is a progressive neurodegenerative disorder characterized by neuronal dysfunction, reactive gliosis, and the formation of amyloid plaques and neurofibrillary tangles in the brain. There is a growing body of evidence to support a central role for biometals such as copper (Cu), zinc (Zn) and iron (Fe) in many critical aspects of AD and other neurodegenerative diseases. The amyloid beta (Aβ) peptide and its parental molecule, the amyloid precursor protein (APP) both modulate homeostasis of Cu and Zn in the brain. Perturbations to biometal metabolism in AD lead to fundamental changes in Aβ and APP expression as well as peptide aggregation and free radical production. These changes can subsequently promote neuronal oxidative stress and cell toxicity. Modulation of metal bioavailability in the brain has been proposed as a potential therapeutic strategy for treatment of AD patients. The lipid soluble metal ligand, clioquinol (CQ) has shown promising results in animal models and small clinical trials involving AD patients and a new generation of metal-ligand based therapeutics is currently under development. Further research will be necessary to fully understand the complex and interdependent pathways of biometal homeostasis and amyloid metabolism in AD. This information will be critical for developing efficacious metal-based pharmaceuticals for treatment of AD while limiting side-effects from disruption of normal metal-dependent metabolic activities.

Alzheimer's disease Amyloid Copper Clioquinol MPAC 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Cummings JL, Vinters HV, Cole GM, Khachaturian ZS (1998) Neurology 51:S2 Google Scholar
  2. 2.
    Glenner GG, Wong CW (1984) Biochem Biophys Res Commun 120:885 CrossRefGoogle Scholar
  3. 3.
    Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K (1985) Proc Natl Acad Sci USA 82:4245 CrossRefGoogle Scholar
  4. 4.
    Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Muller-Hill B (1987) Nature 325:733 CrossRefGoogle Scholar
  5. 5.
    Robakis NK, Wisniewski HM, Jenkins EC, Devine-Gage EA, Houck GE, Yao XL, Ramakrishna N, Wolfe G, Silverman WP, Brown WT (1987) Lancet 1(8529):384 CrossRefGoogle Scholar
  6. 6.
    Tanzi RE, Gusella JF, Watkins PC, Bruns GA, St George-Hyslop P, Van Keuren ML, Patterson D, Pagan S, Kurnit DM, Neve RL (1987) Science 235:880 CrossRefGoogle Scholar
  7. 7.
    Selkoe DJ (2001) Physiol Rev 81:741 Google Scholar
  8. 8.
    Prelli F, Castano EM, van Duinen SG, Bots GT, Luyendijk W, Frangione B (1988) Biochem Biophys Res Commun 151:1150 CrossRefGoogle Scholar
  9. 9.
    Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K (1995) Nature 375:754 CrossRefGoogle Scholar
  10. 10.
    Levy-Lahad E, Wijsman EM, Nemens E, Anderson L, Goddard KA, Weber JL, Bird TD, Schellenberg GD (1995) Science 269:970 CrossRefGoogle Scholar
  11. 11.
    Lemere CA, Blusztajn JK, Yamaguchi H, Wisniewski T, Saido TC, Selkoe DJ (1996) Neurobiol Dis 3:16 CrossRefGoogle Scholar
  12. 12.
    Barnham KJ, Haeffner F, Ciccotosto GD, Curtain CC, Tew D, Mavros C, Beyreuther K, Carrington D, Masters CL, Cherny RA, Cappai R, Bush AI (2004) FASEB J 18:1427 Google Scholar
  13. 13.
    Smith MA, Perry G, Richey PL, Sayre LM, Anderson VE, Beal MF, Kowall N (1996) Nature 382(6587):120 CrossRefGoogle Scholar
  14. 14.
    Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) J Neurochem 68:2092 CrossRefGoogle Scholar
  15. 15.
    Smith MA, Harris PL, Sayre LM, Perry G (1997) Proc Natl Acad Sci USA 94:9866 CrossRefGoogle Scholar
  16. 16.
    Sayre LM, Perry G, Harris PL, Liu Y, Schubert KA, Smith MA (2000) J Neurochem 74:270 CrossRefGoogle Scholar
  17. 17.
    Nunomura A, Perry G, Aliev G, Hirai K, Takeda A, Balraj EK, Jones PK, Ghanbari H, Wataya T, Shimohama S, Chiba S, Atwood CS, Petersen RB, Smith MA (2001) J Neuropathol Exp Neurol 60:759 Google Scholar
  18. 18.
    Halliwell B, Gutteridge JM (1984) Biochem J 219:1 Google Scholar
  19. 19.
    McCord JM, Fridovich I (1969) J Biol Chem 244:6049 Google Scholar
  20. 20.
    Eakin CM, Berman AJ, Miranker AD (2006) Nat Struct Mol Biol 13:202 CrossRefGoogle Scholar
  21. 21.
    Tarohda T, Yamamoto M, Amamo R (2004) Anal Bioanal Chem 380:240 CrossRefGoogle Scholar
  22. 22.
    Massie HR, Aiello VR, Iodice AA (1979) Mech Ageing Dev 10:93 CrossRefGoogle Scholar
  23. 23.
    Morita A, Kimura M, Itokawa Y (1994) Biol Trace Elem Res 42:165 CrossRefGoogle Scholar
  24. 24.
    Maynard CJ, Cappai R, Volitakis I, Cherny RA, White AR, Beyreuther K, Masters CL, Bush AI, Li QX (2002) J Biol Chem 277:44670 CrossRefGoogle Scholar
  25. 25.
    Benkovic SA, Connor JR (1993) J Comp Neurol 338:97 CrossRefGoogle Scholar
  26. 26.
    Martinez Lista E, Sole J, Arola L, Mas A (1993) Biol Neonate 64:47 CrossRefGoogle Scholar
  27. 27.
    Ahluwalia N, Gordon MA, Handte G, Mahlon M, Li NQ, Beard JL, Weinstock D, Ross AC (2000) J Nutr 130:2378 Google Scholar
  28. 28.
    Madaric A, Ginter E, Kadrabova J (1994) Physiol Res 43:107 Google Scholar
  29. 29.
    Ekmekcioglu C (2001) Nahrung 45:309 CrossRefGoogle Scholar
  30. 30.
    Iskra M, Patelski J, Majewski W (1993) J Trace Elem Electrolytes Health Dis 7:185 Google Scholar
  31. 31.
    McMaster D, McCrum E, Patterson CC, Kerr MM, O'Reilly D, Evans AE, Love AH (1992) Am J Clin Nutr 56:440 Google Scholar
  32. 32.
    Menditto A, Morisi G, Alimonti A, Caroli S, Petrucci F, Spagnolo A, Menotti A (1993) J Trace Elem Electrolytes Health Dis 7:251 Google Scholar
  33. 33.
    Milne DB, Johnson PE (1993) Clin Chem 39:883 Google Scholar
  34. 34.
    Prasad AS, Fitzgerald JT, Hess JW, Kaplan J, Pelen F, Dardenne M (1993) Nutrition 9:218 Google Scholar
  35. 35.
    Lindeman RD, Clark ML, Colmore JP (1971) J Gerontol 26:358 Google Scholar
  36. 36.
    Bunker VW, Hinks LJ, Stansfield MF, Lawson MS, Clayton BE (1987) Am J Clin Nutr 46:353 Google Scholar
  37. 37.
    Munro HN, Suter PM, Russell RM (1987) Annu Rev Nutr 7:23 CrossRefGoogle Scholar
  38. 38.
    Monget AL, Galan P, Preziosi P, Keller H, Bourgeois C, Arnaud J, Favier A, Hercberg S (1996) Int J Vitam Nutr Res 66:71 Google Scholar
  39. 39.
    Ravaglia G, Forti P, Maioli F, Nesi B, Pratelli L, Savarino L, Cucinotta D, Cavalli G (2000) J Clin Endocrinol Metab 85:2260 CrossRefGoogle Scholar
  40. 40.
    Connor JR, Tucker P, Johnson M, Snyder B (1993) Neurosci Lett 159:88 CrossRefGoogle Scholar
  41. 41.
    Wender M, Szczech J, Hoffmann S, Hilczer W (1992) Neuropatol Pol 30:65 Google Scholar
  42. 42.
    Martin WR, Ye FQ, Allen PS (1998) Mov Disord 13:281 CrossRefGoogle Scholar
  43. 43.
    Zecca L, Gallorini M, Schunemann V, Trautwein AX, Gerlach M, Riederer P, Vezzoni P, Tampellini D (2001) J Neurochem 76:1766 CrossRefGoogle Scholar
  44. 44.
    Zecca L, Youdim MB, Riederer P, Connor JR, Crichton RR (2004) Nat Rev Neurosci 5:863 CrossRefGoogle Scholar
  45. 45.
    Bartzokis G, Aravagiri M, Oldendorf WH, Mintz J, Marder SR (1993) Magn Reson Med 29:459 CrossRefGoogle Scholar
  46. 46.
    Bartzokis G, Mintz J, Sultzer D, Marx P, Herzberg JS, Phelan CK, Marder SR (1994) AJNR Am J Neuroradiol 15:1129 Google Scholar
  47. 47.
    Bartzokis G, Sultzer D, Mintz J, Holt LE, Marx P, Phelan CK, Marder SR (1994) Biol Psychiatry 35:480 CrossRefGoogle Scholar
  48. 48.
    Bartzokis G, Marder SR (1995) Biol Psychiatry 38:133 CrossRefGoogle Scholar
  49. 49.
    Bartzokis G, Beckson M, Hance DB, Marx P, Foster JA, Marder SR (1997) Magn Reson Imaging 15:29 CrossRefGoogle Scholar
  50. 50.
    Bartzokis G, Cummings JL, Markham CH, Marmarelis PZ, Treciokas LJ, Tishler TA, Marder SR, Mintz J (1999) Magn Reson Imaging 17:213 CrossRefGoogle Scholar
  51. 51.
    Bartzokis G, Sultzer D, Cummings J, Holt LE, Hance DB, Henderson VW, Mintz J (2000) Arch Gen Psychiatry 57:47 CrossRefGoogle Scholar
  52. 52.
    Bartzokis G, Tishler TA (2000) Cell Mol Biol (Noisy-le-grand) 46:821 Google Scholar
  53. 53.
    Bartzokis G, Tishler TA, Shin IS, Lu PH, Cummings JL (2004) Ann NY Acad Sci 1012:224 CrossRefGoogle Scholar
  54. 54.
    Musci G, Bonaccorsi di Patti MC, Fagiolo U, Calabrese L (1993) J Biol Chem 268:13388 Google Scholar
  55. 55.
    Freedman JH, Ciriolo MR, Peisach J (1989) J Biol Chem 264:5598 Google Scholar
  56. 56.
    Owen AD, Schapira AH, Jenner P, Marsden CD (1997) J Neural Transm Suppl 51:167 Google Scholar
  57. 57.
    Lovell MA, Robertson JD, Teesdale WJ, Campbell JL, Markesbery WR (1998) J Neurol Sci 158:47 CrossRefGoogle Scholar
  58. 58.
    Schlief ML, Craig AM, Gitlin JD (2005) J Neurosci 25:239 CrossRefGoogle Scholar
  59. 59.
    Deibel MA, Ehmann WD, Markesbery WR (1996) J Neurol Sci 143:137 CrossRefGoogle Scholar
  60. 60.
    Cuajungco MP, Lees GJ (1997) Neurobiol Dis 4:137 CrossRefGoogle Scholar
  61. 61.
    Atwood CS, Huang X, Moir RD, Tanzi RE, Bush AI (1999) Met Ions Biol Syst 36:309 Google Scholar
  62. 62.
    Loeffler DA, DeMaggio AJ, Juneau PL, Brickman CM, Mashour GA, Finkelman JH, Pomara N, LeWitt PA (1994) Alzheimer Dis Assoc Disord 8:190 CrossRefGoogle Scholar
  63. 63.
    Maynard CJ, Bush AI, Masters CL, Cappai R, Li QX (2005) Int J Exp Pathol 86:147 CrossRefGoogle Scholar
  64. 64.
    Wand GS, May C, May V, Whitehouse PJ, Rapoport SI, Eipper BA (1987) Neurology 37:1057 Google Scholar
  65. 65.
    Maurer I, Zierz S, Moller HJ (2000) Neurobiol Aging 21:455 CrossRefGoogle Scholar
  66. 66.
    Cottrell DA, Blakely EL, Johnson MA, Ince PG, Turnbull DM (2001) Neurology 57:260 Google Scholar
  67. 67.
    Duara R, Grady C, Haxby J, Sundaram M, Cutler NR, Heston L, Moore A, Schlageter N, Larson S, Rapoport SI (1986) Neurology 36:879 Google Scholar
  68. 68.
    McGeer EG, McGeer PL, Harrop R, Akiyama H, Kamo H (1990) J Neurosci Res 27:612 CrossRefGoogle Scholar
  69. 69.
    Omar RA, Chyan YJ, Andorn AC, Poeggeler B, Robakis NK, Pappolla MA (1999) J Alzheimers Dis 1:139 Google Scholar
  70. 70.
    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 CrossRefGoogle Scholar
  71. 71.
    Valko M, Morris H, Cronin MT (2005) Curr Med Chem 12:1161 CrossRefGoogle Scholar
  72. 72.
    Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV (1999) Science 284:805 CrossRefGoogle Scholar
  73. 73.
    Mecocci P, MacGarvey U, Beal MF (1994) Ann Neurol 36:747 CrossRefGoogle Scholar
  74. 74.
    Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, Aksenova M, Gabbita SP, Wu JF, Carney JM, et al. (1995) J Neurochem 65:2146 CrossRefGoogle Scholar
  75. 75.
    Ceballos-Picot I, Merad-Boudia M, Nicole A, Thevenin M, Hellier G, Legrain S, Berr C (1996) Free Radic Biol Med 20:579 CrossRefGoogle Scholar
  76. 76.
    Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G (1997) J Neurosci 17:2653 Google Scholar
  77. 77.
    Smith MA, Richey PL, Taneda S, Kutty RK, Sayre LM, Monnier VM, Perry G (1994) Ann NY Acad Sci 738:447 CrossRefGoogle Scholar
  78. 78.
    Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, Markesbery WR (1991) Proc Natl Acad Sci USA 88:10540 CrossRefGoogle Scholar
  79. 79.
    Perry G, Taddeo MA, Petersen RB, Castellani RJ, Harris PL, Siedlak SL, Cash AD, Liu Q, Nunomura A, Atwood CS, Smith MA (2003) Biometals 16:77 CrossRefGoogle Scholar
  80. 80.
    Pappolla MA, Omar RA, Kim KS, Robakis NK (1992) Am J Pathol 140:621 Google Scholar
  81. 81.
    Furuta A, Price DL, Pardo CA, Troncoso JC, Xu ZS, Taniguchi N, Martin LJ (1995) Am J Pathol 146:357 Google Scholar
  82. 82.
    Smith MA, Kutty RK, Richey PL, Yan SD, Stern D, Chader GJ, Wiggert B, Petersen RB, Perry G (1994) Am J Pathol 145:42 Google Scholar
  83. 83.
    Curtain CC, Ali F, Volitakis I, Cherny RA, Norton RS, Beyreuther K, Barrow CJ, Masters CL, Bush AI, Barnham KJ (2001) J Biol Chem 276:20466 CrossRefGoogle Scholar
  84. 84.
    Atwood CS, Moir RD, Huang X, Scarpa RC, Bacarra NM, Romano DM, Hartshorn MA, Tanzi RE, Bush AI (1998) J Biol Chem 273:12817 CrossRefGoogle Scholar
  85. 85.
    Atwood CS, Scarpa RC, Huang X, Moir RD, Jones WD, Fairlie DP, Tanzi RE, Bush AI (2000) J Neurochem 75:1219 CrossRefGoogle Scholar
  86. 86.
    Cuajungco MP, Faget KY, Huang X, Tanzi RE, Bush AI (2000) Ann NY Acad Sci 920:292 CrossRefGoogle Scholar
  87. 87.
    Dong J, Atwood CS, Anderson VE, Siedlak SL, Smith MA, Perry G, Carey PR (2003) Biochemistry 42:2768 CrossRefGoogle Scholar
  88. 88.
    Behl C, Davis JB, Lesley R, Schubert D (1994) Cell 77:817 CrossRefGoogle Scholar
  89. 89.
    Huang X, Atwood CS, Hartshorn MA, Multhaup G, Goldstein LE, Scarpa RC, Cuajungco MP, Gray DN, Lim J, Moir RD, Tanzi RE, Bush AI (1999) Biochemistry 38:7609 CrossRefGoogle Scholar
  90. 90.
    Galeazzi L, Ronchi P, Franceschi C, Giunta S (1999) Amyloid 6:7 Google Scholar
  91. 91.
    Atwood CS, Perry G, Zeng H, Kato Y, Jones WD, Ling KQ, Huang X, Moir RD, Wang D, Sayre LM, Smith MA, Chen SG, Bush AI (2004) Biochemistry 43:560 CrossRefGoogle Scholar
  92. 92.
    Perry G, Cash AD, Smith MA (2002) J Biomed Biotechnol 2:120 CrossRefGoogle Scholar
  93. 93.
    Stadtman ER, Oliver CN (1991) J Biol Chem 266:2005 Google Scholar
  94. 94.
    Kuo YM, Webster S, Emmerling MR, De Lima N, Roher AE (1998) Biochim Biophys Acta 1406:291 Google Scholar
  95. 95.
    Barnham KJ, Ciccotosto GD, Tickler AK, Ali FE, Smith DG, Williamson NA, Lam YH, Carrington D, Tew D, Kocak G, Volitakis I, Separovic F, Barrow CJ, Wade JD, Masters CL, Cherny RA, Curtain CC, Bush AI, Cappai R (2003) J Biol Chem 278:42959 CrossRefGoogle Scholar
  96. 96.
    Tickler AK, Smith DG, Ciccotosto GD, Tew DJ, Curtain CC, Carrington D, Masters CL, Bush AI, Cherny RA, Cappai R, Wade JD, Barnham KJ (2005) J Biol Chem 280:13355 CrossRefGoogle Scholar
  97. 97.
    Ciccotosto GD, Tew D, Curtain CC, Smith D, Carrington D, Masters CL, Bush AI, Cherny RA, Cappai R, Barnham KJ (2004) J Biol Chem 279:42528 CrossRefGoogle Scholar
  98. 98.
    Opazo C, Huang X, Cherny RA, Moir RD, Roher AE, White AR, Cappai R, Masters CL, Tanzi RE, Inestrosa NC, Bush AI (2002) J Biol Chem 277:40302 CrossRefGoogle Scholar
  99. 99.
    Crouch PJ, Blake R, Duce JA, Ciccotosto GD, Li QX, Barnham KJ, Curtain CC, Cherny RA, Cappai R, Dyrks T, Masters CL, Trounce IA (2005) J Neurosci 25:672 CrossRefGoogle Scholar
  100. 100.
    White AR, Bush AI, Beyreuther K, Masters CL, Cappai R (1999) J Neurochem 72:2092 CrossRefGoogle Scholar
  101. 101.
    Irizarry MC, Gurol ME, Raju S, Diaz-Arrastia R, Locascio JJ, Tennis M, Hyman BT, Growdon JH, Greenberg SM, Bottiglieri T (2005) Neurology 65:1402 CrossRefGoogle Scholar
  102. 102.
    Miller JW (1999) Nutr Rev 57:126 Google Scholar
  103. 103.
    Seshadri S (2006) J Alzheimer's Dis 9:393 Google Scholar
  104. 104.
    Pacheco-Quinto J, Rodriguez de Turco EB, DeRosa S, Howard A, Cruz-Sanchez F, Sambamurti K, Refolo L, Petanceska S, Pappolla MA (2006) Neurobiol Dis 22:651 CrossRefGoogle Scholar
  105. 105.
    White AR, Huang X, Jobling MF, Barrow CJ, Beyreuther K, Masters CL, Bush AI, Cappai R (2001) J Neurochem 76:1509 CrossRefGoogle Scholar
  106. 106.
    Nelson TJ, Alkon DL (2005) J Biol Chem 280:7377 CrossRefGoogle Scholar
  107. 107.
    Puglielli L, Friedlich AL, Setchell KD, Nagano S, Opazo C, Cherny RA, Barnham KJ, Wade JD, Melov S, Kovacs DM, Bush AI (2005) J Clin Invest 115:2556 CrossRefGoogle Scholar
  108. 108.
    Dikalov SI, Vitek MP, Mason RP (2004) Free Radic Biol Med 36:340 CrossRefGoogle Scholar
  109. 109.
    Murray IV, Sindoni ME, Axelsen PH (2005) Biochemistry 44:12606 CrossRefGoogle Scholar
  110. 110.
    Wasco W, Bupp K, Magendantz M, Gusella JF, Tanzi RE, Solomon F (1992) Proc Natl Acad Sci USA 89:10758 CrossRefGoogle Scholar
  111. 111.
    Sprecher CA, Grant FJ, Grimm G, O'Hara PJ, Norris F, Norris K, Foster DC (1993) Biochemistry 32:4481 CrossRefGoogle Scholar
  112. 112.
    Slunt HH, Thinakaran G, Von Koch C, Lo AC, Tanzi RE, Sisodia SS (1994) J Biol Chem 269:2637 Google Scholar
  113. 113.
    Bayer TA, Cappai R, Masters CL, Beyreuther K, Multhaup G (1999) Mol Psychiatry 4:524 CrossRefGoogle Scholar
  114. 114.
    Okado H, Okamoto H (1995) Gerontology 41 Suppl 1:7 Google Scholar
  115. 115.
    Torroja L, Luo L, White K (1996) J Neurosci 16:4638 Google Scholar
  116. 116.
    Iijima K, Lee DS, Okutsu J, Tomita S, Hirashima N, Kirino Y, Suzuki T (1998) Biochem J 330:29 Google Scholar
  117. 117.
    Villard L, Tassone F, Crnogorac-Jurcevic T, Clancy K, Gardiner K (1998) Gene 210:17 CrossRefGoogle Scholar
  118. 118.
    White AR, Multhaup G, Galatis D, McKinstry WJ, Parker MW, Pipkorn R, Beyreuther K, Masters CL, Cappai R (2002) J Neurosci 22:365 Google Scholar
  119. 119.
    Hesse L, Beher D, Masters CL, Multhaup G (1994) FEBS Lett 349:109 CrossRefGoogle Scholar
  120. 120.
    Valensin D, Mancini FM, Luczkowski M, Janicka A, Wisniewska K, Gaggelli E, Valensin G, Lankiewicz L, Kozlowski H (2004) Dalton Trans 16 Google Scholar
  121. 121.
    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 CrossRefGoogle Scholar
  122. 122.
    White AR, Multhaup G, Maher F, Bellingham S, Camakaris J, Zheng H, Bush AI, Beyreuther K, Masters CL, Cappai R (1999) J Neurosci 19:9170 Google Scholar
  123. 123.
    White AR, Reyes R, Mercer JF, Camakaris J, Zheng H, Bush AI, Multhaup G, Beyreuther K, Masters CL, Cappai R (1999) Brain Res 842:439 CrossRefGoogle Scholar
  124. 124.
    Ruiz FH, Gonzalez M, Bodini M, Opazo C, Inestrosa NC (1999) J Neurochem 73:1288 CrossRefGoogle Scholar
  125. 125.
    Cerpa WF, Barria MI, Chacon MA, Suazo M, Gonzalez M, Opazo C, Bush AI, Inestrosa NC (2004) FASEB J 18:1701 Google Scholar
  126. 126.
    Bellingham SA, Ciccotosto GD, Needham BE, Fodero LR, White AR, Masters CL, Cappai R, Camakaris J (2004) J Neurochem 91:423 CrossRefGoogle Scholar
  127. 127.
    Hassett R, Kosman DJ (1995) J Biol Chem 270:128 CrossRefGoogle Scholar
  128. 128.
    Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G (1999) Biochem J 344 Pt 2:461 Google Scholar
  129. 129.
    Phinney AL, Drisaldi B, Schmidt SD, Lugowski S, Coronado V, Liang Y, Horne P, Yang J, Sekoulidis J, Coomaraswamy J, Chishti MA, Cox DW, Mathews PM, Nixon RA, Carlson GA, St George-Hyslop P, Westaway D (2003) Proc Natl Acad Sci USA 100:14193 CrossRefGoogle Scholar
  130. 130.
    Takeda A (2000) Brain Res Brain Res Rev 34:137 CrossRefGoogle Scholar
  131. 131.
    Weiss JH, Sensi SL, Koh JY (2000) Trends Pharmacol Sci 21:395 CrossRefGoogle Scholar
  132. 132.
    Danscher G, Stoltenberg M (2005) J Histochem Cytochem 53:141 CrossRefGoogle Scholar
  133. 133.
    Frederickson CJ, Koh JY, Bush AI (2005) Nat Rev Neurosci 6:449 CrossRefGoogle Scholar
  134. 134.
    Suh SW, Jensen KB, Jensen MS, Silva DS, Kesslak PJ, Danscher G, Frederickson CJ (2000) Brain Res 852:274 CrossRefGoogle Scholar
  135. 135.
    Lee JY, Mook-Jung I, Koh JY (1999) J Neurosci 19:RC10 Google Scholar
  136. 136.
    Frederickson CJ, Suh SW, Silva D, Frederickson CJ, Thompson RB (2000) J Nutr 130:1471S Google Scholar
  137. 137.
    Bush AI (2003) Trends Neurosci 26:207 CrossRefGoogle Scholar
  138. 138.
    Zuchner T, Schliebe N, Schliebs R (2006) Int J Dev Neurosci 24:23 CrossRefGoogle Scholar
  139. 139.
    Religa D, Strozyk D, Cherny RA, Volitakis I, Haroutunian V, Winblad B, Naslund J, Bush AI (2006) Neurology 67:69 CrossRefGoogle Scholar
  140. 140.
    Smith JL, Xiong S, Lovell MA (2006) Neurotoxicology 27:1 CrossRefGoogle Scholar
  141. 141.
    Bush AI, Pettingell WH, Multhaup G, d Paradis M, Vonsattel JP, Gusella JF, Beyreuther K, Masters CL, Tanzi RE (1994) Science 265:1464 CrossRefGoogle Scholar
  142. 142.
    Liu ST, Howlett G, Barrow CJ (1999) Biochemistry 38:9373 CrossRefGoogle Scholar
  143. 143.
    Huang X, Atwood CS, Moir RD, Hartshorn MA, Vonsattel JP, Tanzi RE, Bush AI (1997) J Biol Chem 272:26464 CrossRefGoogle Scholar
  144. 144.
    Lee JY, Cole TB, Palmiter RD, Suh SW, Koh JY (2002) Proc Natl Acad Sci USA 99:7705 CrossRefGoogle Scholar
  145. 145.
    Friedlich AL, Lee JY, van Groen T, Cherny RA, Volitakis I, Cole TB, Palmiter RD, Koh JY, Bush AI (2004) J Neurosci 24:3453 CrossRefGoogle Scholar
  146. 146.
    Lovell MA, Xie C, Markesbery WR (1999) Brain Res 823:88 CrossRefGoogle Scholar
  147. 147.
    McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Ann Neurol 46:860 CrossRefGoogle Scholar
  148. 148.
    Walsh DM, Klyubin I, Shankar GM, Townsend M, Fadeeva JV, Betts V, Podlisny MB, Cleary JP, Ashe KH, Rowan MJ, Selkoe DJ (2005) Biochem Soc Trans 33:1087 CrossRefGoogle Scholar
  149. 149.
    Bush AI, Multhaup G, Moir RD, Williamson TG, Small DH, Rumble B, Pollwein P, Beyreuther K, Masters CL (1993) J Biol Chem 268:16109 Google Scholar
  150. 150.
    Sottrup-Jensen L, Sand O, Kristensen L, Fey GH (1989) J Biol Chem 264:15781 Google Scholar
  151. 151.
    Du Y, Bales KR, Dodel RC, Liu X, Glinn MA, Horn JW, Little SP, Paul SM (1998) J Neurochem 70:1182 CrossRefGoogle Scholar
  152. 152.
    Du Y, Ni B, Glinn M, Dodel RC, Bales KR, Zhang Z, Hyslop PA, Paul SM (1997) J Neurochem 69:299 CrossRefGoogle Scholar
  153. 153.
    Yu WH, Lukiw WJ, Bergeron C, Niznik HB, Fraser PE (2001) Brain Res 894:37 CrossRefGoogle Scholar
  154. 154.
    Uchida Y, Takio K, Titani K, Ihara Y, Tomonaga M (1991) Neuron 7:337 CrossRefGoogle Scholar
  155. 155.
    Zambenedetti P, Giordano R, Zatta P (1998) J Chem Neuroanat 15:21 CrossRefGoogle Scholar
  156. 156.
    Carson JA, Turner AJ (2002) J Neurochem 81:1 CrossRefGoogle Scholar
  157. 157.
    Das S, Mandal M, Chakraborti T, Mandal A, Chakraborti S (2003) Mol Cell Biochem 253:31 CrossRefGoogle Scholar
  158. 158.
    White AR, Du T, Laughton KM, Volitakis I, Sharples RA, Xilinas ME, Hoke DE, Holsinger RM, Evin G, Cherny RA, Hill AF, Barnham KJ, Li QX, Bush AI, Masters CL (2006) J Biol Chem 281:17670 CrossRefGoogle Scholar
  159. 159.
    Eisenstein RS (2000) Annu Rev Nutr 20:627 CrossRefGoogle Scholar
  160. 160.
    Lieu PT, Heiskala M, Peterson PA, Yang Y (2001) Mol Aspects Med 22:1 CrossRefGoogle Scholar
  161. 161.
    Rouault TA (2001) Pediatr Neurol 25:130 CrossRefGoogle Scholar
  162. 162.
    Sipe JC, Lee P, Beutler E (2002) Dev Neurosci 24:188 CrossRefGoogle Scholar
  163. 163.
    Connor JR, Menzies SL, Burdo JR, Boyer PJ (2001) Pediatr Neurol 25:118 CrossRefGoogle Scholar
  164. 164.
    Beard JL, Connor JR, Jones BC (1993) Nutr Rev 51:157 CrossRefGoogle Scholar
  165. 165.
    Jeong SY, David S (2006) J Neurosci 26:9810 CrossRefGoogle Scholar
  166. 166.
    Schipper HM (2000) Exp Gerontol 35:821 CrossRefGoogle Scholar
  167. 167.
    Connor JR, Menzies SL, St Martin SM, Mufson EJ (1992) J Neurosci Res 31:75 CrossRefGoogle Scholar
  168. 168.
    Dobson J (2001) Cell Mol Biol (Noisy-le-grand) 47 Online Pub:OL49 Google Scholar
  169. 169.
    Kuroda Y, Kawahara M (1994) Tohoku J Exp Med 174:263 CrossRefGoogle Scholar
  170. 170.
    Rottkamp CA, Raina AK, Zhu X, Gaier E, Bush AI, Atwood CS, Chevion M, Perry G, Smith MA (2001) Free Radic Biol Med 30:447 CrossRefGoogle Scholar
  171. 171.
    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 CrossRefGoogle Scholar
  172. 172.
    Hoke DE, Tan JL, Ilaya NT, Culvenor JG, Smith SJ, White AR, Masters CL, Evin GM (2005) FEBS J 272:5544 CrossRefGoogle Scholar
  173. 173.
    McLoughlin DM, Standen CL, Lau KF, Ackerley S, Bartnikas TP, Gitlin JD, Miller CC (2001) J Biol Chem 276:9303 CrossRefGoogle Scholar
  174. 174.
    Angeletti B, Waldron KJ, Freeman KB, Bawagan H, Hussain I, Miller CC, Lau KF, Tennant ME, Dennison C, Robinson NJ, Dingwall C (2005) J Biol Chem 280:17930 CrossRefGoogle Scholar
  175. 175.
    Miyazaki K, Hasegawa M, Funahashi K, Umeda M (1993) Nature 362:839 CrossRefGoogle Scholar
  176. 176.
    Ma Q, Li Y, Du J, Liu H, Kanazawa K, Nemoto T, Nakanishi H, Zhao Y (2006) Peptides 27:841 CrossRefGoogle Scholar
  177. 177.
    Bjorkdahl C, Sjogren MJ, Winblad B, Pei JJ (2005) Neuroreport 16:591 CrossRefGoogle Scholar
  178. 178.
    Yamamoto A, Shin RW, Hasegawa K, Naiki H, Sato H, Yoshimasu F, Kitamoto T (2002) J Neurochem 82:1137 CrossRefGoogle Scholar
  179. 179.
    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 CrossRefGoogle Scholar
  180. 180.
    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 CrossRefGoogle Scholar
  181. 181.
    Ritchie CW, Bush AI, Masters CL (2004) Expert Opin Investig Drugs 13:1585 CrossRefGoogle Scholar
  182. 182.
    Gaeta A, Hider RC (2005) Br J Pharmacol 146:1041 CrossRefGoogle Scholar
  183. 183.
    Cherny RA, Legg JT, McLean CA, Fairlie DP, Huang X, Atwood CS, Beyreuther K, Tanzi RE, Masters CL, Bush AI (1999) J Biol Chem 274:23223 CrossRefGoogle Scholar
  184. 184.
    Di Vaira M, Bazzicalupi C, Orioli P, Messori L, Bruni B, Zatta P (2004) Inorg Chem 43:3795 CrossRefGoogle Scholar
  185. 185.
    Lau TL, Ambroggio EE, Tew DJ, Cappai R, Masters CL, Fidelio GD, Barnham KJ, Separovic F (2006) J Mol Biol 356:759 CrossRefGoogle Scholar
  186. 186.
    Abramov AY, Canevari L, Duchen MR (2003) J Neurosci 23:5088 Google Scholar
  187. 187.
    Lee JY, Friedman JE, Angel I, Kozak A, Koh JY (2004) Neurobiol Aging 25:1315 CrossRefGoogle Scholar
  188. 188.
    McLaurin J, Kierstead ME, Brown ME, Hawkes CA, Lambermon MH, Phinney AL, Darabie AA, Cousins JE, French JE, Lan MF, Chen F, Wong SS, Mount HT, Fraser PE, Westaway D, St George-Hyslop P (2006) Nat Med 12:801 CrossRefGoogle Scholar
  189. 189.
    Martin CJ (1995) J Inorg Biochem 58:89 CrossRefGoogle Scholar
  190. 190.
    Regland B, Lehmann W, Abedini I, Blennow K, Jonsson M, Karlsson I, Sjogren M, Wallin A, Xilinas M, Gottfries CG (2001) Dement Geriatr Cogn Disord 12:408 CrossRefGoogle Scholar
  191. 191.
    Ibach B, Haen E, Marienhagen J, Hajak G (2005) Pharmacopsychiatry 38:178 CrossRefGoogle Scholar
  192. 192.
    Crapper McLachlan DR, Dalton AJ, Kruck TP, Bell MY, Smith WL, Kalow W, Andrews DF (1991) Lancet 337:1304 CrossRefGoogle Scholar
  193. 193.
    Flaten TP (2001) Brain Res Bull 55:187 CrossRefGoogle Scholar
  194. 194.
    Squitti R, Rossini PM, Cassetta E, Moffa F, Pasqualetti P, Cortesi M, Colloca A, Rossi L, Finazzi-Agro A (2002) Eur J Clin Invest 32:51 CrossRefGoogle Scholar
  195. 195.
    Liu G, Garrett MR, Men P, Zhu X, Perry G, Smith MA (2005) Biochim Biophys Acta 1741:246 Google Scholar
  196. 196.
    Cui Z, Lockman PR, Atwood CS, Hsu CH, Gupte A, Allen DD, Mumper RJ (2005) Eur J Pharm Biopharm 59:263 CrossRefGoogle Scholar
  197. 197.
    Huang X, Cuajungco MP, Atwood CS, Hartshorn MA, Tyndall JD, Hanson GR, Stokes KC, Leopold M, Multhaup G, Goldstein LE, Scarpa RC, Saunders AJ, Lim J, Moir RD, Glabe C, Bowden EF, Masters CL, Fairlie DP, Tanzi RE, Bush AI (1999) J Biol Chem 274:37111 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2007

Authors and Affiliations

  1. 1.Department of PathologyThe University of MelbourneVictoriaAustralia
  2. 2.The Mental Health Research InstituteParkville, VictoriaAustralia

Personalised recommendations