Application of yeast to study the tau and amyloid-β abnormalities of Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 35, Issue 2, 2013, Pages 217-225

  Porzoor, Afsaneh ^a   Macreadie, Ian G ^a  

^a RMIT UNIVERSITY   (Australia)

Author keywords

Alzheimer's disease; amyloid ; Candida glabrata; Pichia pastoris; Saccharomyces cerevisiae; Schizosaccharomyces pombe; tau

Indexed keywords

AMYLOID BETA PROTEIN; CLIOQUINOL; CURCUMIN; DIMEBON; QUERCETIN; RESVERATROL; TAU PROTEIN;

ALZHEIMER DISEASE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; APOPTOSIS; BIOTECHNOLOGY; BLOOD BRAIN BARRIER; CANDIDA GLABRATA; CELL CYCLE; CELL DEATH; CELL DIVISION; DRUG SCREENING; GENE SEQUENCE; GENETIC ASSOCIATION; HEAT SHOCK RESPONSE; HIGH THROUGHPUT SCREENING; HUMAN; NONHUMAN; OLIGOMERIZATION; OXIDATIVE STRESS; PICHIA PASTORIS; PODOSPORA ANSERINA; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EID: 84877146722     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-122035     Document Type: Review

References (99)

1. World Health Organisation (2012) News Release: Dementia cases set to triple by 2050 but still largely ignored. WHO, Geneva, http://www.who.int/ mediacentre/news/releases/2012 /dementia 20120411/en/
2. Irie K, Murakami K, Masuda Y, Morimoto A, Ohigashi H, Ohashi R, Takegoshi K, Nagao M, Shimizu T, Shirasawa T (2005) Structure of-Amyloid fibrils and its relevance to their neurotoxicity: Implications for the pathogenesis of Alzheimer's disease. J Biosci Bioeng 99, 437-447
3. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R (2003) APP processing and synaptic function. Neuron 37, 925-937
4. Qu B, Boyer PJ, Johnston SA, Hynan LS, Rosenberg RN (2006) A 42 gene vaccination reduces brain amyloid plaque burden in transgenic mice. J Neurol Sci 244, 151-158
5. Solomon B, Frenkel D (2010) Immunotherapy for Alzheimer's disease. Neuropharmacology 59, 303-309
6. Berhanu WM, Masunov AE (2010) Natural polyphenols as inhibitors of amyloid aggregation. Molecular dynamics study of GNNQQNY heptapeptide decamer. Biophys Chem 149, 12-21
7. Misiti F, Sampaolese B, Mezzogori D, Orsini F, Pezzotti M, Giardina B, Clementi ME (2006) Protective effect of rhubarb derivatives on amyloid beta (1-42) peptide-induced apoptosis in IMR-32 cells: A case of nutrigenomic. Brain Res Bull 71, 29-36
8. Nakdook W, Khongsombat O, Taepavarapruk P, Taepavarapruk N, IngkaninanK(2010) The effects of Tabernaemontana divaricata root extract on amyloid-peptide 25-35 peptides induced cognitive deficits in mice. J Ethnopharmacol 130, 122-126
9. Wang H-Q, Sun X-B, Xu Y-X, Zhao H, Zhu Q-Y, Zhu C-Q (2010) Astaxanthin upregulates heme oxygenase-1 expression through ERK1/2 pathway and its protective effect against beta-Amyloid-induced cytotoxicity in SH-SY5Y cells. Brain Res 1360, 159-167
10. Selkoe DJ, Schenk D (2003) Alzheimer's disease: Molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545-584
11. Khurana V, Lindquist S (2010) Modelling neurodegeneration in Saccharomyces cerevisiae: Why cook with baker's yeast? Nat Rev Neurosci 11, 436-449
12. Pereira C, Bessa C, Soares J, Leao M, Saraiva L (2012) Contribution of yeast models to neurodegeneration research. J Biomed Biotechnol 2012, 941232
13. Vishnevskaia AB, Kushnirov VV, Ter-Avanesian MD (2007) Neurodegenerative amyloidoses: The yeast model. Mol Biol (Mosk) 41, 346-354
14. Braun RJ,Büttner S, Ring J, Kroemer G, Madeo F (2010) Nervous yeast: Modeling neurotoxic cell death. Trends Biochem Sci 35, 135-144
15. Mager WH,Winderickx J (2005)Yeast as a model for medical and medicinal research. Trends Pharmacol Sci 26, 265-273
16. Wittenberg C, Reed SI (2005) Cell cycle-dependent transcription in yeast: Promoters, transcription factors, and transcriptomes. J Oncogene 24, 2746-2755
17. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274, 546, 563-547
18. Foury F (1997) Human genetic diseases:Across-Talk between man and yeast. Gene 195, 1-10
19. McGowan E, Pickford F, Kim J, Onstead L, Eriksen J, Yu C, Skipper L, Murphy MP, Beard J, Das P, Jansen K, DeLucia M, Lin W-L, Dolios G, Wang R, Eckman CB, Dickson DW, Hutton M, Hardy J, Golde T (2005) A 42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 47, 191-199
20. Saito T, Suemoto T, Brouwers N, Sleegers K, Funamoto S, Mihira N, Matsuba Y, Yamada K, Nilsson P, Takano J, Nishimura M, Iwata N,Van BroeckhovenC, IharaY, SaidoTC (2011) Potent amyloidogenicity and pathogenicity of A 43. Nat Neurosci 14, 1023-1032
21. Bharadwaj P,Waddington L,Varghese J, Macreadie IG (2008) A new method to measure cellular toxicity of non-fibrillar and fibrillar Alzheimer's A using yeast. J Alzheimers Dis 13, 147-150
22. Bagriantsev S, Liebman S (2006) Modulation of A 42 lown oligomerization using a novel yeast reporter system. BMC Biol 4, 32
23. Caine J, Sankovich S, Antony H, Waddington L, Macreadie P, Varghese J, Macreadie I (2007) Alzheimer's A fused to green fluorescent protein induces growth stress and a heat shock response. FEMS Yeast Res 7, 1230-1236
24. Macreadie I, Lotfi-Miri M, Mohotti S, Shapira D, Bennett L, Varghese J (2008) Validation of folate in a convenient yeast assay suited for identification of inhibitors of Alzheimer's A aggregation. J Alzheimers Dis 15, 391-396
25. Dubey AK, Bharadwaj PR, Varghese JN, Macreadie IG (2009) Alzheimer'sA rescues yeast from hydroxide toxicity. J Alzheimers Dis 18, 31-33
26. Park SK, Pegan SD, Mesecar AD, Jungbauer LM, LaDu MJ, Liebman SW (2011) Development and validation of a yeast high-Throughput screen for inhibitors of A 42 oligomerization. Dis Model Mech 4, 822-831
27. D'Angelo F, Vignaud H, Di Martino J, Salin B, Devin A, Cullin C, Marchal C (2013) A yeast model for amyloid-aggregation exemplifies the role of membrane trafficking and PICALM in cytotoxicity. Dis Model Mech 6, 206-216
28. Games D, Adams D, Alessandrini R, Barbour R, Borthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, Montoya-Zavala M, Mucke L, Paganini L, Penniman E, Power M, Schenk D, Seubert P, Snyder B, Soriano F, Tan H, Vitale J, Wadsworth S, Wolozin B, Zhao J (1995) Alzheimer-Type neuropathology in transgenic mice overexpressing V717F-Amyloid precursor protein. Nature 373, 523-527
29. Goate A, Chartier-Harlin M-C, Mullan M, Brown J, Crawford F, Fidani L, Giuffra L, Haynes A, Irving N, James L, Mant R, Newton P, Rooke K, Roques P, Talbot C, Pericak-Vance M, Roses A,Williamson R, Rossor M, Owen M, Hardy J (1991) Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 349, 704-706
30. Le Brocque D, Henry A, Cappai R, Li QX, Tanner JE, Galatis D, Gray C, Holmes S, Underwood JR, Beyreuther K, Masters CL, Evin G (1998) Processing of the Alzheimer's disease amyloid precursor protein in Pichia pastoris: Immunodetection of-secretase products. Biochemistry 37, 14958-14965
31. Ding XL, Husseman J, Tomashevski A, Nochlin D, Jin LW, Vincent I (2000) The cell cycle Cdc25A tyrosine phosphatase is activated in degenerating postmitotic neurons in Alzheimer's disease. Am J Pathol 157, 1983-1990
32. Mosch B, Morawski M, Mittag A, Lenz D, Tarnok A, Arendt T (2007) Aneuploidy and DNA replication in the normal human brain and Alzheimer's disease. J Neurosci 27, 6859-6867
33. Thirumalai D, Reddy G, Straub JE (2012) Role of water in protein aggregation and amyloid polymorphism. Acc Chem Res 45, 83-92
34. Heo C, Chang KA, Choi HS, Kim HS, Kim S, Liew H, Kim JA, Yu E, Ma J, Suh YH (2007) Effects of the monomeric, oligomeric, and fibrillar A 42 peptides on the proliferation and differentiation of adult neural stem cells from subventricular zone. J Neurochem 102, 493-500
35. Weingarten MD, Lockwood AH, Hwo SY, Kirschner MW (1975) A protein factor essential for microtubule assembly. Proc Natl Acad Sci U S A 72, 1858-1862
36. Le Corre S, KlafkiHW, Plesnila N, Hubinger G, Obermeier A, Sahagun H, Monse B, Seneci P, Lewis J, Eriksen J, Zehr C, Yue M, McGowan E, Dickson DW, Hutton M, Roder HM (2006) An inhibitor of tau hyperphosphorylation prevents severe motor impairments in tau transgenic mice. Proc Natl Acad Sci U S A 103, 9673-9678
37. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A (2002) Tau is essential to-Amyloid-induced neurotoxicity. Proc Natl Acad Sci U S A 99, 6364-6369
38. Zabrocki P, Pellens K,Vanhelmont T,Vandebroek T, Griffioen G,Wera S, Van Leuven F,Winderickx J (2005) Characterization of-synuclein aggregation and synergistic toxicity with protein tau in yeast. FEBS J 272, 1386-1400
39. Vega IE, Traverso EE, Ferrer-Acosta Y, Matos E, Colon M, Gonzalez J, Dickson D, Hutton M, Lewis J, Yen SH (2008) A novel calcium-binding protein is associated with tau proteins in tauopathy. J Neurochem 106, 96-106
40. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM (2004) A immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43, 321-332
41. David DC, Layfield R, Serpell L, Narain Y, Goedert M, SpillantiniMG(2002) Proteasomal degradation of tau protein. J Neurochem 83, 176-185
42. Goldbaum O, Oppermann M, Handschuh M, Dabir D, Zhang B, Forman MS, Trojanowski JQ, Lee VM, Richter-Landsberg C (2003) Proteasome inhibition stabilizes tau inclusions in oligodendroglial cells that occur after treatment with okadaic acid. J Neurosci 23, 8872-8880
43. Poppek D, Keck S, Ermak G, Jung T, Stolzing A, Ullrich O, Davies KJ, Grune T (2006) Phosphorylation inhibits turnover of the tau protein by the proteasome: Influence of RCAN1 and oxidative stress. Biochem J 400, 511-520
44. LoPresti P, Konat GW (2001) Hydrogen peroxide induces transient dephosphorylation of tau protein in cultured rat oligodendrocytes. Neurosci Lett 311, 142-144
45. Galas MC, Dourlen P, Begard S, Ando K, Blum D, Hamdane M, Buee L (2006) The peptidylprolyl cis/trans-isomerase Pin1 modulates stress-induced dephosphorylation of tau in neurons. Implication in a pathological mechanism related to Alzheimer disease. J Biol Chem 281, 19296-19304
46. Zambrano CA, Egana JT, Nunez MT, Maccioni RB, Gonzalez-Billault C (2004) Oxidative stress promotes tau dephosphorylation in neuronal cells: The roles of cdk5 and PP1. Free Radic Biol Med 36, 1393-1402
47. De Vos A, Anandhakumar J, Van den Brande J, Verduyckt M, Franssens V, Winderickx J, Swinnen E (2011) Yeast as a model system to study tau biology. Int J Alzheimers Dis 2011, 428970
48. Vandebroek T, Terwel D, Vanhelmont T, Gysemans M, Van Haesendonck C, Engelborghs Y, Winderickx J, Van Leuven F (2006) Microtubule binding and clustering of human Tau-4R and Tau-P301L proteins isolated from yeast deficient in orthologues of glycogen synthase kinase-3- or cdk5. J Biol Chem 281, 25388-25397
49. Vanhelmont T, Vandebroek T, De Vos A, Terwel D, Lemaire K, Anandhakumar J, Franssens V, Swinnen E, Van Leuven F, Winderickx J (2010) Serine-409 phosphorylation and oxidative damage define aggregation of human protein tau in yeast. FEMS Yeast Res 10, 992-1005
50. Bretteville A, Planel E (2008) Tau aggregates: Toxic, inert, or protective species? J Alzheimers Dis 14, 431-436
51. Timmers AC, Niebel A, Balague C, Dagkesamanskaya A (2002) Differential localisation of GFP fusions to cytoskeleton-binding proteins in animal, plant, and yeast cells. Protoplasma 220, 69-78
52. Vandebroek T, Vanhelmont T, Terwel D, Borghgraef P, Lemaire K, Snauwaert J, Wera S, Van Leuven F, Winderickx J (2005) Identification and isolation of a hyperphosphorylated, conformationally changed intermediate of human protein tau expressed in yeast. Biochemistry 44, 11466-11475
53. Wen Y, Planel E, Herman M, Figueroa HY, Wang L, Liu L, Lau LF, Yu WH, Duff KE (2008) Interplay between cyclindependent kinase 5 and glycogen synthase kinase 3-mediated by neuregulin signaling leads to differential effects on tau phosphorylation and amyloid precursor protein processing. J Neurosci 28, 2624-2632
54. Nemavarkar P, Chourasia BK, Pasupathy K (2004) Evaluation of radioprotective action of compounds using Saccharomyces cerevisiae. J Environ Pathol Toxicol Oncol 23, 145-151
55. Nemavarkar PS, Chourasia BK, Pasupathy K (2004) Detection of gamma-irradiation induced DNA damage and radioprotection of compounds in yeast using comet assay. J Radiat Res 45, 169-174
56. Wurth C, Guimard NK, Hecht MH (2002) Mutations that reduce aggregation of the Alzheimer's A 42 peptide: An unbiased search for the sequence determinants of A amyloidogenesis. J Mol Biol 319, 1279-1290
57. Treusch S, Hamamichi S, Goodman JL, Matlack KE, Chung CY, Baru V, Shulman JM, Parrado A, Bevis BJ, Valastyan JS, Han H, Lindhagen-Persson M, Reiman EM, Evans DA, Bennett DA, Olofsson A, DeJager PL, Tanzi RE, Caldwell KA, Caldwell GA, Lindquist S (2011) Functional links between A toxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 334, 1241-1245
58. Lopez LC, Dos-Reis S, Espargaro A, Carrodeguas JA, Maddelein ML, Ventura S, Sancho J (2012) Discovery of novel inhibitors of amyloid-peptide 1-42 aggregation. J Med Chem 55, 9521-9530
59. Middendorp O, Ortler C, Neumann U, Paganetti P, Luthi U, Barberis A (2004) Yeast growth selection system for the identification of cell-Active inhibitors of-secretase. Biochim Biophys Acta 1674, 29-39
60. Middendorp O, Luthi U, Hausch F, Barberis A (2004) Searching for the most effective screening system to identify cell-Active inhibitors of-secretase. Biol Chem 385, 481-485
61. Fabrizio P, Longo VD (2008) Chronological aging-induced apoptosis in yeast. Biochim Biophys Acta 1783, 1280-1285
62. Buttner S, Bitto A, Ring J, Augsten M, Zabrocki P, Eisenberg T, Jungwirth H, Hutter S, Carmona-Gutierrez D, Kroemer G, Winderickx J, Madeo F (2008) Functional mitochondria are required for-synuclein toxicity in aging yeast. J Biol Chem 283, 7554-7560
63. McMurray MA, Gottschling DE (2004) Aging and genetic instability in yeast. Curr Opin Microbiol 7, 673-679
64. Fabrizio P, Longo VD (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2, 73-81
65. Fabrizio P, Pozza F, Pletcher SD, Gendron CM, Longo VD (2001) Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288-290
66. Sikora E, Arendt T, Bennett M, Narita M (2011) Impact of cellular senescence signature on ageing research. Ageing Res Rev 10, 146-152
67. Churcher C, Bowman S, Badcock K, Bankier A, Brown D, Chillingworth T, Connor R, Devlin K, Gentles S, Hamlin N, Harris D, Horsnell T, Hunt S, Jagels K, Jones M, Lye G, Moule S, Odell C, Pearson D, Rajandream M, Rice P, Rowley N, Skelton J, Smith V, Barrell B, et al. (1997) The nucleotide sequence of Saccharomyces cerevisiae chromosome IX. Nature 387, 84-87
68. Bach S,Talarek N, AndrieuT,Vierfond J-M,MetteyY, Galons H, Dormont D, Meijer L, Cullin C, BlondelM(2003) Isolation of drugs active against mammalian prions using a yeast-based screening assay. Nat Biotechnol 21, 1075-1081
69. Pimentel C, Batista-Nascimento L, Rodrigues-Pousada C, Menezes RA (2012) Oxidative stress in Alzheimer's and Parkinson's diseases: Insights from the yeast Saccharomyces cerevisiae. Oxid Med Cell Longev 2012, 132146
70. Vidan S, Snyder M (2001) Large-scale mutagenesis: Yeast genetics in the genome era. Curr Opin Biotechnol 12, 28-34
71. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, Robinson M, Raghibizadeh S, Hogue CW, Bussey H, Andrews B, Tyers M, Boone C (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368
72. Fields S, Song O (1989) A novel genetic system to detect protein-protein interactions. Nature 340, 245-246
73. SenGupta DJ, Zhang B, Kraemer B, Pochart P, Fields S, Wickens M (1996) A three-hybrid system to detect RNAprotein interactions in vivo. Proc Natl Acad Sci USA 93, 8496-8501
74. Culotti J, Hartwell LH (1971) Genetic control of the cell division cycle in yeast: III. Seven genes controlling nuclear division. Exp Cell Res 67, 389-401
75. Emili A, Schieltz DM, Yates Iii JR, Hartwell LH (2001) Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol Cell 7, 13-20
76. Hartwell L (1992) Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71, 543-546
77. Hartwell LH (1971) Genetic control of the cell division cycle in yeast: IV. Genes controlling bud emergence and cytokinesis. Exp Cell Res 69, 265-276
78. Müller B, Grossniklaus U (2010) Model organisms-A historical perspective. J Proteomic 73, 2054-2063
79. Paulovich AG, Toczyski DP, Hartwell LH (1997) When checkpoints fail. Cell 88, 315-321
80. Simon JA, Bedalov A (2004) Yeast as a model system for anticancer drug discovery. Nat Rev Cancer 4, 481-487
81. Hughes SR, Goyal S, Sun JE, Gonzalez-DeWhitt P, Fortes MA, Riedel NG, Sahasrabudhe SR (1996) Two-hybrid system as a model to study the interaction of beta-Amyloid peptide monomers. Proc Natl Acad Sci U S A 93, 2065-2070
82. von der Haar T, Josse L, Wright P, Zenthon J, Tuite MF (2007) Development of a novel yeast cell-based system for studying the aggregation of Alzheimer's disease-Associated A peptides in vivo. Neurodegener Dis 4, 136-147
83. SimakovaO, Arispe NJ (2006) Early and late cytotoxic effects of external application of the Alzheimer's A result from the initial formation and function of A ion channels. Biochemistry 45, 5907-5915
84. LaFerla FM, Green KN, Oddo S (2007) Intracellular A in Alzheimer's disease. Nat Rev Neurosci 8, 499-509
85. Zhang W, Espinoza D, Hines V, Innis M, Mehta P, Miller DL (1997) Characterization of-Amyloid peptide precursor processing by the yeast Yap3 and Mkc7 proteases. Biochim Biophys Acta 1359, 110-122
86. Gunyuzlu PL, White WH, Davis GL, Hollis GF, Toyn JH (2000) A yeast genetic assay for caspase cleavage of the A precursor protein. Mol Biotechnol 15, 29-37
87. Lüthi U, Schaerer-Brodbeck C, Tanner S, Middendorp O, Edler K, Barberis A (2003) Human-secretase activity in yeast detected by a novel cellular growth selection system. Biochim Biophys Acta 1620, 167-178
88. Lüthi U, Schaerer-Brodbeck C, Tanner S, Middendorp O, Edler K, Barberis A (2003) Human-secretase activity in yeast detected by a novel cellular growth selection system. Biochim Biophys Acta 1620, 167-178
89. Edbauer D,Winkler E, Regula JT, Pesold B, Steiner H, Haass C (2003) Reconstitution of-secretase activity. Nat Cell Biol 5, 486-488
90. Vandebroek T, Terwel D, Vanhelmont T, Winderickx J, Van Leuven F (2005) Phosphorylation and aggregation of protein tau in humanized yeast cells and in transgenic mouse brain. In New Trends in Alzheimer and Parkinson Related Disorders: ADPD. Medimond, pp. 15-19, http://med. kuleuven.be/legtegg/ Publications/pub0101/pdf0101.pdf
91. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425, 191-196
92. Belinha I, Amorim MA, Rodrigues P, de Freitas V, Moradas-Ferreira P, Mateus N, Costa V (2007) Quercetin increases oxidative stress resistance and longevity in Saccharomyces cerevisiae. J Agric Food Chem 55, 2446-2451
93. Li C, Wang J, Zhou B (2010) The metal chelating and chaperoning effects of clioquinol: Insights from yeast studies. J Alzheimers Dis 21, 1249-1262
94. Minear S, O'Donnell AF, Ballew A, Giaever G, Nislow C, Stearns T, Cyert MS (2011) Curcumin inhibits growth of Saccharomyces cerevisiae through iron chelation. Eukaryot Cell 10, 1574-1581
95. Bharadwaj PR, Verdile G, Barr RK, Gupta V, Steele JW, Lachenmayer ML, Yue Z, Ehrlich ME, Petsko G, Ju S, Ringe D, Sankovich SE, Caine JM, Macreadie IG, Gandy S, Martins RN (2012) Latrepirdine (Dimebon) enhances autophagy and reduces intracellular GFP-A 42 levels in yeast. J Alzheimers Dis 32, 949-967
96. Hendriks L, van Duijn CM, Cras P, Cruts M, Van HulW, van Harskamp F,Warren A, McInnis MG, Antonarakis SE, Martin JJ, et al. (1992) Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the-Amyloid precursor protein gene. Nat Genet 1, 218-221
97. Levy E, Carman MD, Fernandez-Madrid IJ, Power MD, Lieberburg I, van Duinen SG, Bots GT, Luyendijk W, Frangione B (1990) Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. Science 248, 1124-1126
98. Grabowski TJ, Cho HS, Vonsattel JP, Rebeck GW, Greenberg SM(2001) Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy. Ann Neurol 49, 697-705
99. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, Forsell C, Stenh C, Luthman J, Teplow DB, Younkin SG, Naslund J, Lannfelt L (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced A protofibril formation. Nat Neurosci 4, 887-893