Investigating Interventions in Alzheimer's Disease with Computer Simulation Models

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Proctor, Carole J ^a   Boche, Delphine ^b   Gray, Douglas A ^c,d   Nicoll, James A R ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

ACTIVE IMMUNIZATION; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; COGNITIVE DEFECT; COMPUTER SIMULATION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE CONTROL; IMMUNOTHERAPY; INTERVENTION STUDY; MATHEMATICAL MODEL; MEDICAL RESEARCH; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PASSIVE IMMUNIZATION; PROCESS DEVELOPMENT; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STOCHASTIC MODEL; TREATMENT OUTCOME;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANTIBODIES, MONOCLONAL; COMPUTER SIMULATION; DRUG EVALUATION, PRECLINICAL; HUMANS; IMMUNIZATION; IMMUNOTHERAPY; MODELS, BIOLOGICAL; SYSTEMS BIOLOGY; TAU PROTEINS;

EID: 84884198965     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073631     Document Type: Article

References (89)

1. Crews L, Masliah E, (2010) Molecular mechanisms of neurodegeneration in Alzheimer's disease. Hum Mol Genet 19: R12-R20.
2. Lannfelt L, Blennow K, Zetterberg H, Batsman S, Ames D, et al. (2008) Safety, efficacy, and biomarker findings of PBT2 in targeting Aβ as a modifying therapy for Alzheimer's disease: a phase IIa, double-blind, randomised, placebo-controlled trial. Lancet Neurol 7: 779-786.
3. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, et al. (1999) Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400: 173-177.
4. Salloway S, Sperling R, Gilman S, Fox NC, Blennow K, et al. (2009) A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer disease. Neurology 73: 2061-2070.
5. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, et al. (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38: 547-554.
6. Bayer AJ, Bullock R, Jones RW, Wilkinson D, Paterson KR, et al. (2005) Evaluation of the safety and immunogenicity of synthetic Abeta42 (AN1792) in patients with AD. Neurology 64: 94-101.
7. Orgogozo JM, Gilman S, Dartigues JF, Laurent B, Puel M, et al. (2003) Subacute meningoencephalitis in a subset of patients with AD after Abeta42 immunization. Neurology 61: 46-54.
8. Sperling RA, Jack CR Jr, Black SE, Frosch MP, Greenberg SM, et al. (2011) Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: recommendations from the Alzheimer's Association Research Roundtable Workgroup. Alzheimers Dement 7: 367-385.
9. Jucker M, (2010) The benefits and limitations of animal models for translational research in neurodegenerative diseases. Nat Med 16: 1210-1214.
10. Boche D, Denham N, Holmes C, Nicoll JA, (2010) Neuropathology after active Abeta42 immunotherapy: implications for Alzheimer's disease pathogenesis. Acta Neuropathol (Berl) 120: 369-384.
11. Holmes C, Boche D, Wilkinson D, Yadegarfar G, Hopkins V, et al. (2008) Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 372: 216-223.
12. Nicoll JA, Barton E, Boche D, Neal JW, Ferrer I, et al. (2006) Abeta species removal after Abeta42 immunization. J Neuropathol Exp Neurol 65: 1040-1048.
13. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, et al. (2003) Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 9: 448-452.
14. Rinne JO, Brooks DJ, Rossor MN, Fox NC, Bullock R, et al. (2010) 11C-PiB PET assessment of change in fibrillar amyloid-beta load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double-blind, placebo-controlled, ascending-dose study. Lancet Neurol 9: 363-372.
15. Zotova E, Holmes C, Johnston D, Neal JW, Nicoll JA, et al. (2011) Microglial alterations in human Alzheimer's disease following Abeta42 immunisation. Neuropathol Appl Neurobiol.
16. Maarouf C, Daugs I, Kokjohn T, Kalback W, Patton RL, et al. (2010) The biochemical aftermath of anti-amyloid immunotherapy. Mol Neurodegener 5: 39.
17. Boche D, Donald J, Love S, Harris S, Neal JW, et al. (2010) Reduction of aggregated Tau in neuronal processes but not in the cell bodies after Abeta42 immunisation in Alzheimer's disease. Acta Neuropathol (Berl) 120: 13-20.
18. Serrano-Pozo A, William CM, Ferrer I, Uro-Coste E, Delisle M-B, et al. (2010) Beneficial effect of human anti-amyloid-beta active immunization on neurite morphology and tau pathology. Brain 133: 1312-1327.
19. Baker AM, Holmes C, Love S, Nicoll JAR, Boche D, (2011) Lower glycogen synthase kinase-3beta load in Alzheimer's disease after Abeta42 immunization. Neuropathol Appl Neurobiol 37: 22-42.
20. Proctor C, Gray D, (2010) GSK3 and p53- is there a link in Alzheimer's disease? Mol Neurodegener 5: 7.
21. Giovanna C, Cecchi C, Pensalfini A, Bonini S, Ferrari-Toninelli G, et al. (2010) Generation of reactive oxygen species by beta amyloid fibrils and oligomers involves different intra/extracellular pathways. Amino Acids 38: 1101-1106.
22. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, et al. (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 304: 448-452.
23. Ohyagi Y, Asahara H, Chui D-H, Tsuruta Y, Sakae N, et al. (2004) Intracellular Abeta42 activates p53 promoter: a pathway to neurodegeneration in Alzheimer's disease. FASEB J pp. 04-2637fje.
24. Tseng BP, Green KN, Chan JL, Blurton-Jones M, LaFerla FM, (2008) Aβ inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol Aging 29: 1607-1618.
25. Kim JR, Muresan A, Lee KYC, Murphy RM, (2004) Urea modulation of beta-amyloid fibril growth: Experimental studies and kinetic models. Protein Sci 13: 2888-2898.
26. Pallitto MM, Murphy RM, (2001) A mathematical model of the kinetics of beta-amyloid fibril growth from the denatured state. Biophys J 81: 1805-1822.
27. Craft DL, Wein LM, Selkoe DJ, (2002) A mathematical model of the impact of novel Treatments on the Abeta burden in the Alzheimers brain, CSF and plasma. Bull Math Biol 64: 1011-1031.
28. Morris JC, McKeel DW Jr, Storandt M, Rubin EH, Price JL, et al. (1991) Very mild Alzheimer's disease: informant-based clinical, psychometric, and pathologic distinction from normal aging. Neurology 41: 469-478.
29. Nagy Z, Esiri MM, Jobst KA, Morris JH, King EM, et al. (1995) Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria. Dementia 6: 21-31.
30. Nelson PT, Abner EL, Schmitt FA, Kryscio RJ, Jicha GA, et al. (2009) Brains with medial temporal lobe neurofibrillary tangles but no neuritic amyloid plaques are a diagnostic dilemma but may have pathogenetic aspects distinct from Alzheimer disease. J Neuropathol Exp Neurol 68: 774-784.
31. Wilcock GK, Esiri MM, (1982) Plaques, tangles and dementia. A quantitative study. J Neurol Sci 56: 343-356.
32. Small SA, Duff K, (2008) Linking Abeta and tau in late-onset Alzheimer's disease: a dual pathway hypothesis. Neuron 60: 534-542.
33. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, et al. (2010) Dendritic function of tau mediates amyloid-β toxicity in Alzheimer's disease mouse models. Cell 142: 387-397.
34. Rapoport M, Dawson HN, Binder LI, Vitek MP, Ferreira A, (2002) Tau is essential to beta-amyloid-induced neurotoxicity. Proc Natl Acad Sci USA 99: 6364-6369.
35. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, et al. (2007) Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
36. Hucka M, Finney A, Sauro HM, Bolouri H, Doyle JC, et al. (2003) The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models. Bioinformatics 19: 524-531.
37. The Systems Biology Markup Language www.sbml.org. Accessed 2013 Aug 1.
38. Hu X, Crick SL, Bu G, Frieden C, Pappu RV, et al. (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci U S A 106: 20324-20329.
39. Mawuenyega KG, Sigurdson W, Ovod V, Munsell L, Kasten T, et al. (2010) Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 330: 1774.
40. Alzheimer Research Forum http://www.alzforum.org/new/detail.asp?id=3268. Accessed 2013 Aug 1.
41. Proctor CJ, Pienaar IS, Elson JL, Kirkwood TB, (2012) Aggregation, impaired degradation and immunization targeting of amyloid-beta dimers in Alzheimer's disease: a stochastic modelling approach. Mol Neurodegener 7: 32.
42. Patton RL, Kalback WM, Esh CL, Kokjohn TA, Van Vickle GD, et al. (2006) Amyloid-beta peptide remnants in AN-1792-immunized Alzheimer's disease patients: a biochemical analysis. Am J Pathol 169: 1048-1063.
43. Watcharasit P, Bijur GN, Zmijewski JW, Song L, Zmijewska A, et al. (2002) Direct, activating interaction between glycogen synthase kinase-3beta and p53 after DNA damage. Proc Natl Acad Sci USA 99: 7951-7955.
44. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, et al. (2006) COPASI-a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.
45. Hardy J, Allsop D, (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12: 383-388.
46. Selkoe DJ, (1991) The molecular pathology of Alzheimer's disease. Neuron 6: 487-498.
47. Chaves RS, Melo TQ, Martins SA, Ferrari MF, (2010) Protein aggregation containing beta-amyloid, alpha-synuclein and hyperphosphorylated tau in cultured cells of hippocampus, substantia nigra and locus coeruleus after rotenone exposure. BMC Neurosci 11: 144.
48. Proctor CJ, Gray DA, (2012) A unifying hypothesis for familial and sporadic Alzheimer's disease. Int J Alzheimers Dis 2012.
49. Gendron T, Petrucelli L, (2009) The role of tau in neurodegeneration. Mol Neurodegener 4: 13.
50. Hooper C, Killick R, Lovestone S, (2008) The GSK3 hypothesis of Alzheimer's disease. J Neurochem 104: 1433-1439.
51. Hooper C, Meimaridou E, Tavassoli M, Melino G, Lovestone S, et al. (2007) p53 is upregulated in Alzheimer's disease and induces tau phosphorylation in HEK293a cells. Neurosci Lett 418: 34-37.
52. Dolan PJ, Johnson GV, (2010) The role of tau kinases in Alzheimer's disease. Curr Opin Drug Discov Devel 13: 595-603.
53. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
54. Hepler RW, Grimm KM, Nahas DD, Breese R, Dodson EC, et al. (2006) Solution State Characterization of Amyloid β-Derived Diffusible Ligands. Biochemistry (Mosc) 45: 15157-15167.
55. Cirrito JR, Kang J-E, Lee J, Stewart FR, Verges DK, et al. (2008) Endocytosis is required for synaptic activity-dependent release of amyloid-β in vivo. Neuron 58: 42-51.
56. Parihar MS, Brewer GJ, (2010) Amyloid-beta as a modulator of synaptic plasticity. J Alzheimer's Dis 22: 741-763.
57. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421.
58. Oddo S, Billings L, Kesslak JP, Cribbs DH, LaFerla FM, (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43: 321-332.
59. Bales KR, (2012) The value and limitations of transgenic mouse models used in drug discovery for Alzheimer's disease: an update. Expert Opin Drug Discov 7: 281-297.
60. Ardiles AO, Tapia-Rojas CC, Mandal M, Alexandre F, Kirkwood A, et al. (2012) Postsynaptic dysfunction is associated with spatial and object recognition memory loss in a natural model of Alzheimer's disease. Proc Natl Acad Sci U S A 109: 13835-13840.
61. Rockenstein E, Torrance M, Adame A, Mante M, Bar-on P, et al. (2007) Neuroprotective effects of regulators of the glycogen synthase kinase-3beta signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation. J Neurosci 27: 1981-1991.
62. Gomez-Sintes R, Lucas JJ, (2010) NFAT/Fas signaling mediates the neuronal apoptosis and motor side effects of GSK-3 inhibition in a mouse model of lithium therapy. J Clin Invest 120: 2432-2445.
63. Huang TC, Lu KT, Wo YY, Wu YJ, Yang YL, (2011) Resveratrol protects rats from Abeta-induced neurotoxicity by the reduction of iNOS expression and lipid peroxidation. PLoS ONE 6: e29102.
64. Haupt Y, Maya R, Kazaz A, Oren M, (1997) Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299.
65. Watcharasit P, Bijur GN, Song L, Zhu J, Chen X, et al. (2003) Glycogen synthase kinase-3beta (GSK3beta) binds to and promotes the actions of p53. J Biol Chem 278: 48872-48879.
66. Alvarez G, Munoz-Montano JR, Satrustegui J, Avila J, Bogonez E, et al. (1999) Lithium protects cultured neurons against beta-amyloid-induced neurodegeneration. FEBS Lett 453: 260-264.
67. Gong CX, Grundke-Iqbal I, Iqbal K, (1994) Dephosphorylation of Alzheimer's disease abnormally phosphorylated tau by protein phosphatase-2A. Neuroscience 61: 765-772.
68. Jope RS, Yuskaitis CJ, Beurel E, (2007) Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem Res 32: 577-595.
69. Le Novere N, Bornstein B, Broicher A, Courtot M, Donizelli M, et al. (2006) BioModels Database: a free, centralized database of curated, published, quantitative kinetic models of biochemical and cellular systems. Nucleic Acids Res 34: D689-691.
70. Wilcock DM, DiCarlo G, Henderson D, Jackson J, Clarke K, et al. (2003) Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J Neurosci 23: 3745-3751.
71. Perlmutter LS, Barron E, Chui HC, (1990) Morphologic association between microglia and senile plaque amyloid in Alzheimer's disease. Neurosci Lett 119: 32-36.
72. Bard F, Cannon C, Barbour R, Burke RL, Games D, et al. (2000) Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6: 916-919.
73. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A, (2011) Physiology of microglia. Physiol Rev 91: 461-553.
74. McDonald DR, Brunden KR, Landreth GE, (1997) Amyloid fibrils activate tyrosine kinase-dependent signaling and superoxide production in microglia. J Neurosci 17: 2284-2294.
75. Solomon B, Koppel R, Frankel D, Hanan-Aharon E, (1997) Disaggregation of Alzheimer β-amyloid by site-directed mAb. Proceedings of the National Academy of Sciences 94: 4109-4112.
76. Dodel RC, Hampel H, Du Y, (2003) Immunotherapy for Alzheimer's disease. Lancet Neurol 2: 215-220.
77. Boche D, Perry VH, Nicoll JAR, (2013) Review: Activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol 39: 3-18.
78. Esler WP, Stimson ER, Ghilardi JR, Vinters HV, Lee JP, et al. (1996) In vitro growth of Alzheimer's disease β-amyloid plaques displays first-order kinetics. Biochemistry (Mosc) 35: 749-757.
79. Tseng BP, Esler WP, Clish CB, Stimson ER, Ghilardi JR, et al. (1999) Deposition of monomeric, not oligomeric, Aβ mediates growth of Alzheimer's disease amyloid plaques in human brain preparations. Biochemistry (Mosc) 38: 10424-10431.
80. Hyman BT, Marzloff K, Arriagada PV, (1993) The lack of accumulation of senile plaques or amyloid burden in Alzheimer's disease suggests a dynamic balance between amyloid deposition and resolution. J Neuropathol Exp Neurol 52: 594-600.
81. Maggio JE, Stimson ER, Ghilardi JR, Allen CJ, Dahl CE, et al. (1992) Reversible in vitro growth of Alzheimer disease beta-amyloid plaques by deposition of labeled amyloid peptide. Proc Natl Acad Sci U S A 89: 5462-5466.
82. Cruz L, Urbanc B, Buldyrev SV, Christie R, Gómez-Isla T, et al. (1997) Aggregation and disaggregation of senile plaques in Alzheimer disease. Proc Natl Acad Sci U S A 94: 7612-7616.
83. Tang X, Milyavsky M, Goldfinger N, Rotter V, (2007) Amyloid-[beta] precursor-like protein APLP1 is a novel p53 transcriptional target gene that augments neuroblastoma cell death upon genotoxic stress. Oncogene 26: 7302-7312.
84. Sato K, Tanabe C, Yonemura Y, Watahiki H, Zhao Y, et al. (2012) Localization of mature neprilysin in lipid rafts. J Neurosci Res 90: 870-877.
85. Miners JS, Barua N, Kehoe PG, Gill S, Love S, (2011) Abeta-degrading enzymes: potential for treatment of Alzheimer disease. J Neuropathol Exp Neurol 70: 944-959.
86. Hoops S, Sahle S, Gauges R, Lee C, Pahle Jr, et al. (2006) COPASI- a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.
87. Wilkinson DJ (2006) Stochastic Modelling for Systems Biology: Chapman & Hall/CRC Press.
88. Gillespie DT, (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem 31: 2340-2361.
89. Wickham H (2009) ggplot2: elegant graphics for data analysis.: Springer New York.