Transgenic models of Alzheimer's disease: Better utilization of existing models through viral transgenesis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 9, 2013, Pages 1437-1448

  Platt, Thomas L ^a   Reeves, Valerie L ^a   Murphy, M Paul ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Adeno associated virus; Alzheimer's disease; Lentivirus; Neurodegeneration; Transgenic mouse model

Indexed keywords

AMYLOID PROTEIN; TAU PROTEIN;

ADENO ASSOCIATED VIRUS; ALZHEIMER DISEASE; AMYLOID NEUROPATHY; HUMAN; LENTIVIRINAE; MEDICAL RESEARCH; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TAUOPATHY; TRANSGENIC ORGANISM; TRANSGENICS; VIRAL GENE THERAPY; ANIMAL; DISEASE MODEL; GENE TRANSFER; GENE VECTOR; GENETICS; MOUSE; PATHOLOGY; TRANSGENE; TRANSGENIC MOUSE; VIRUS;

ADENO-ASSOCIATED VIRUS; ANIMALIA; LENTIVIRUS; MUS MUSCULUS;

ALZHEIMER DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; MICE; MICE, TRANSGENIC; TRANSGENES; VIRUSES;

MLCS; MLOWN;

EID: 84881230059     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.04.017     Document Type: Review

References (196)

1. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
2. Forstl H., Kurz A. Clinical features of Alzheimer's disease. Eur. Arch. Psychiatry Clin. Neurosci. 1999, 249:288-290.
3. Hall A.M., Roberson E.D. Mouse models of Alzheimer's disease. Brain Res. Bull. 2012, 88:3-12.
4. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 1995, 373:523-527.
5. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
6. Duff K., Eckman C., Zehr C., Yu X., Prada C.M., Perez-tur J., Hutton M., Buee L., Harigaya Y., Yager D., Morgan D., Gordon M.N., Holcomb L., Refolo L., Zenk B., Hardy J., Younkin S. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1. Nature 1996, 383:710-713.
7. Goedert M., Spillantini M.G. A century of Alzheimer's disease. Science 2006, 314:777-781.
8. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., Copeland N.G., Lee M.K., Younkin L.H., Wagner S.L., Younkin S.G., Borchelt D.R. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 2004, 13:159-170.
9. Cho A., Haruyama N., Kulkarni A.B. Generation of transgenic mice. Curr. Protoc. Cell Biol. 2009, (Chapter 19, Unit 19 11).
10. Duff K., Suleman F. Transgenic mouse models of Alzheimer's disease: how useful have they been for therapeutic development?. Brief. Funct. Genomic. Proteomic. 2004, 3:47-59.
11. Sandbrink R., Masters C.L., Beyreuther K. APP gene family. Alternative splicing generates functionally related isoforms. Ann. N. Y. Acad. Sci. 1996, 777:281-287.
12. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 2001, 81:741-766.
13. Chen F., Hasegawa H., Schmitt-Ulms G., Kawarai T., Bohm C., Katayama T., Gu Y., Sanjo N., Glista M., Rogaeva E., Wakutani Y., Pardossi-Piquard R., Ruan X., Tandon A., Checler F., Marambaud P., Hansen K., Westaway D., St George-Hyslop P., Fraser P. TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature 2006, 440:1208-1212.
14. Tanzi R.E., Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 2005, 120:545-555.
15. Karran E., Mercken M., De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat. Rev. Drug Discov. 2011, 10:698-712.
16. Ohnishi S., Takano K. Amyloid fibrils from the viewpoint of protein folding. Cell. Mol. Life Sci. 2004, 61:511-524.
17. Robinson J.L., Geser F., Corrada M.M., Berlau D.J., Arnold S.E., Lee V.M., Kawas C.H., Trojanowski J.Q. Neocortical and hippocampal amyloid-beta and tau measures associate with dementia in the oldest-old. Brain 2011, 134:3708-3715.
18. Hu J., Van Eldik L.J. Glial-derived proteins activate cultured astrocytes and enhance beta amyloid-induced glial activation. Brain Res. 1999, 842:46-54.
19. Griffin W.S., Sheng J.G., Royston M.C., Gentleman S.M., McKenzie J.E., Graham D.I., Roberts G.W., Mrak R.E. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol. 1998, 8:65-72.
20. Meda L., Baron P., Scarlato G. Glial activation in Alzheimer's disease: the role of Abeta and its associated proteins. Neurobiol. Aging 2001, 22:885-893.
21. Glabe C.G. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging 2006, 27:570-575.
22. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 2005, 280:17294-17300.
23. Ahmed R.R., Holler C.J., Webb R.L., Li F., Beckett T.L., Murphy M.P. BACE1 and BACE2 enzymatic activities in Alzheimer's disease. J. Neurochem. 2010, 112:1045-1053.
24. Fukumoto H., Cheung B.S., Hyman B.T., Irizarry M.C. Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch. Neurol. 2002, 59:1381-1389.
25. Korade Z., Kenworthy A.K. Lipid rafts, cholesterol, and the brain. Neuropharmacology 2008, 55:1265-1273.
26. Kim S.I., Yi J.S., Ko Y.G. Amyloid beta oligomerization is induced by brain lipid rafts. J. Cell. Biochem. 2006, 99:878-889.
27. Rushworth J.V., Hooper N.M. Lipid rafts: linking Alzheimer's amyloid-beta production, aggregation, and toxicity at neuronal membranes. Int J Alzheimers Dis 2010, 2011:603052.
28. Holler C.J., Webb R.L., Laux A.L., Beckett T.L., Niedowicz D.M., Ahmed R.R., Liu Y., Simmons C.R., Dowling A.L., Spinelli A., Khurgel M., Estus S., Head E., Hersh L.B., Murphy M.P. BACE2 expression increases in human neurodegenerative disease. Am. J. Pathol. 2012, 180:337-350.
29. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923.
30. Sherrington R., Rogaev E.I., Liang Y., Rogaeva E.A., Levesque G., Ikeda M., Chi H., Lin C., Li G., Holman K., Tsuda T., Mar L., Foncin J.F., Bruni A.C., Montesi M.P., Sorbi S., Rainero I., Pinessi L., Nee L., Chumakov I., Pollen D., Brookes A., Sanseau P., Polinsky R.J., Wasco W., Da Silva H.A., Haines J.L., Perkicak-Vance M.A., Tanzi R.E., Roses A.D., Fraser P.E., Rommens J.M., St George-Hyslop P.H. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 1995, 375:754-760.
31. Tanzi R.E., Moir R.D., Wagner S.L. Clearance of Alzheimer's Abeta peptide: the many roads to perdition. Neuron 2004, 43:605-608.
32. Arriagada P.V., Marzloff K., Hyman B.T. Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 1992, 42:1681-1688.
33. Gomez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 1997, 41:17-24.
34. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
35. Gotz J., Chen F., van Dorpe J., Nitsch R.M. Formation of neurofibrillary tangles in P301l tau transgenic mice induced by Abeta 42 fibrils. Science 2001, 293:1491-1495.
36. Lewis J., Dickson D.W., Lin W.L., Chisholm L., Corral A., Jones G., Yen S.H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491.
37. Ittner L.M., Gotz J. Amyloid-beta and tau-a toxic pas de deux in Alzheimer's disease. Nat. Rev. Neurosci. 2011, 12:65-72.
38. Hardy J., Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 1991, 12:383-388.
39. Karran E., Mercken M., De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics, Nature reviews. Drug discovery 2011, 10:698-712.
40. Lambert J.C., Amouyel P. Genetics of Alzheimer's disease: new evidences for an old hypothesis?. Curr. Opin. Genet. Dev. 2011, 21:295-301.
41. Maas T., Eidenmuller J., Brandt R. Interaction of tau with the neural membrane cortex is regulated by phosphorylation at sites that are modified in paired helical filaments. J. Biol. Chem. 2000, 275:15733-15740.
42. Weingarten M.D., Lockwood A.H., Hwo S.Y., Kirschner M.W. A protein factor essential for microtubule assembly. Natl Acad Sci U S A. 1975, 72:1858-1862.
43. Duff K., Knight H., Refolo L.M., Sanders S., Yu X., Picciano M., Malester B., Hutton M., Adamson J., Goedert M., Burki K., Davies P. Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol. Dis. 2000, 7:87-98.
44. Mandelkow E.M., Schweers O., Drewes G., Biernat J., Gustke N., Trinczek B., Mandelkow E. Structure, microtubule interactions, and phosphorylation of tau protein. Ann. N. Y. Acad. Sci. 1996, 777:96-106.
45. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nature reviews. Neuroscience 2007, 8:663-672.
46. Deshpande A., Win K.M., Busciglio J. Tau isoform expression and regulation in human cortical neurons. FASEB J. 2008, 22:2357-2367.
47. Forman M.S., Lee V.M., Trojanowski J.Q. New insights into genetic and molecular mechanisms of brain degeneration in tauopathies. J. Chem. Neuroanat. 2000, 20:225-244.
48. Morris M., Maeda S., Vossel K., Mucke L. The many faces of tau. Neuron 2011, 70:410-426.
49. Watanabe A., Takio K., Ihara Y. Deamidation and isoaspartate formation in smeared tau in paired helical filaments. Unusual properties of the microtubule-binding domain of tau. J. Biol. Chem. 1999, 274:7368-7378.
50. Hasegawa M., Morishima-Kawashima M., Takio K., Suzuki M., Titani K., Ihara Y. Protein sequence and mass spectrometric analyses of tau in the Alzheimer's disease brain. J. Biol. Chem. 1992, 267:17047-17054.
51. Chau M.F., Radeke M.J., de Ines C., Barasoain I., Kohlstaedt L.A., Feinstein S.C. The microtubule-associated protein tau cross-links to two distinct sites on each alpha and beta tubulin monomer via separate domains. Biochemistry 1998, 37:17692-17703.
52. Robertson L.A., Moya K.L., Breen K.C. The potential role of tau protein O-glycosylation in Alzheimer's disease. J. Alzheimers Dis. 2004, 6:489-495.
53. Reynolds M.R., Reyes J.F., Fu Y., Bigio E.H., Guillozet-Bongaarts A.L., Berry R.W., Binder L.I. Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies. J. Neurosci. 2006, 26:10636-10645.
54. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Yoshida H., Titani K., Ihara Y. Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 1995, 270:823-829.
55. Michel G., Mercken M., Murayama M., Noguchi K., Ishiguro K., Imahori K., Takashima A. Characterization of tau phosphorylation in glycogen synthase kinase-3beta and cyclin dependent kinase-5 activator (p23) transfected cells. Biochim. Biophys. Acta 1998, 1380:177-182.
56. Ksiezak-Reding H., Pyo H.K., Feinstein B., Pasinetti G.M. Akt/PKB kinase phosphorylates separately Thr212 and Ser214 of tau protein in vitro. Biochim. Biophys. Acta 2003, 1639:159-168.
57. Lund E.T., McKenna R., Evans D.B., Sharma S.K., Mathews W.R. Characterization of the in vitro phosphorylation of human tau by tau protein kinase II (cdk5/p20) using mass spectrometry. J. Neurochem. 2001, 76:1221-1232.
58. Martin L., Latypova X., Wilson C.M., Magnaudeix A., Perrin M.L., Yardin C., Terro F. Tau protein kinases: involvement in Alzheimer's disease. Ageing Res. Rev. 2013, 12:289-309.
59. Drewes G., Trinczek B., Illenberger S., Biernat J., Schmitt-Ulms G., Meyer H.E., Mandelkow E.M., Mandelkow E. Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262. J. Biol. Chem. 1995, 270:7679-7688.
60. Geschwind D.H. Tau phosphorylation, tangles, and neurodegeneration: the chicken or the egg?. Neuron 2003, 40:457-460.
61. Hanger D.P., Anderton B.H., Noble W. Tau phosphorylation: the therapeutic challenge for neurodegenerative disease. Trends Mol. Med. 2009, 15:112-119.
62. Hernandez F., Avila J. Tauopathies. Cell. Mol. Life Sci. 2007, 64:2219-2233.
63. Alonso A., Zaidi T., Novak M., Grundke-Iqbal I., Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6923-6928.
64. Cuchillo-Ibanez I., Seereeram A., Byers H.L., Leung K.Y., Ward M.A., Anderton B.H., Hanger D.P. Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J. 2008, 22:3186-3195.
65. Iqbal K., Alonso Adel C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., Tanimukai H., Grundke-Iqbal I. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739:198-210.
66. Friedmann T., Roblin R. Gene therapy for human genetic disease?. Science 1972, 175:949-955.
67. Wilson J.M. Medicine. A history lesson for stem cells. Science 2009, 324:727-728.
68. Roth J.A., Cristiano R.J. Gene therapy for cancer: what have we done and where are we going?. J. Natl. Cancer Inst. 1997, 89:21-39.
69. Stephenson J. Studies illuminate cause of fatal reaction in gene-therapy trial. JAMA 2001, 285:2570.
70. Kibbe M.R., Murdock A., Wickham T., Lizonova A., Kovesdi I., Nie S., Shears L., Billiar T.R., Tzeng E. Optimizing cardiovascular gene therapy: increased vascular gene transfer with modified adenoviral vectors. Arch. Surg. 2000, 135:191-197.
71. Brody S.L., Crystal R.G. Adenovirus-mediated in vivo gene transfer. Ann. N. Y. Acad. Sci. 1994, 716:90-101. discussion 101-103.
72. Pfeifer A., Hofmann A. Lentiviral transgenesis. Methods Mol. Biol. 2009, 530:391-405.
73. Kay M.A., Glorioso J.C., Naldini L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat. Med. 2001, 7:33-40.
74. Deroose C.M., Reumers V., Gijsbers R., Bormans G., Debyser Z., Mortelmans L., Baekelandt V. Noninvasive monitoring of long-term lentiviral vector-mediated gene expression in rodent brain with bioluminescence imaging. Mol. Ther. 2006, 14:423-431.
75. Wang Y., Song Y.T., Liu Q., Liu C., Wang L.L., Liu Y., Zhou X.Y., Wu J., Wei H. Quantitative analysis of lentiviral transgene expression in mice over seven generations. Transgenic Res. 2010, 19:775-784.
76. Jahner D., Jaenisch R. Retrovirus-induced de novo methylation of flanking host sequences correlates with gene inactivity. Nature 1985, 315:594-597.
77. Park F., Kay M.A. Modified HIV-1 based lentiviral vectors have an effect on viral transduction efficiency and gene expression in vitro and in vivo. Mol. Ther. 2001, 4:164-173.
78. Zufferey R., Dull T., Mandel R.J., Bukovsky A., Quiroz D., Naldini L., Trono D. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 1998, 72:9873-9880.
79. Miyoshi H., Blomer U., Takahashi M., Gage F.H., Verma I.M. Development of a self-inactivating lentivirus vector. J. Virol. 1998, 72:8150-8157.
80. Cronin J., Zhang X.Y., Reiser J. Altering the tropism of lentiviral vectors through pseudotyping. Curr. Gene Ther. 2005, 5:387-398.
81. Park F. Lentiviral vectors: are they the future of animal transgenesis?. Physiol. Genomics 2007, 31:159-173.
82. Hacein-Bey-Abina S., von Kalle C., Schmidt M., Le Deist F., Wulffraat N., McIntyre E., Radford I., Villeval J.L., Fraser C.C., Cavazzana-Calvo M., Fischer A. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 2003, 348:255-256.
83. Hacein-Bey-Abina S., Von Kalle C., Schmidt M., McCormack M.P., Wulffraat N., Leboulch P., Lim A., Osborne C.S., Pawliuk R., Morillon E., Sorensen R., Forster A., Fraser P., Cohen J.I., de Saint Basile G., Alexander I., Wintergerst U., Frebourg T., Aurias A., Stoppa-Lyonnet D., Romana S., Radford-Weiss I., Gross F., Valensi F., Delabesse E., Macintyre E., Sigaux F., Soulier J., Leiva L.E., Wissler M., Prinz C., Rabbitts T.H., Le Deist F., Fischer A., Cavazzana-Calvo M. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 2003, 302:415-419.
84. Montini E., Cesana D., Schmidt M., Sanvito F., Ponzoni M., Bartholomae C., Sergi Sergi L., Benedicenti F., Ambrosi A., Di Serio C., Doglioni C., von Kalle C., Naldini L. Hematopoietic stem cell gene transfer in a tumor-prone mouse model uncovers low genotoxicity of lentiviral vector integration. Nat. Biotechnol. 2006, 24:687-696.
85. Pfeifer A., Ikawa M., Dayn Y., Verma I.M. Transgenesis by lentiviral vectors: lack of gene silencing in mammalian embryonic stem cells and preimplantation embryos. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:2140-2145.
86. Nakagawa T., Feliu-Mojer M.I., Wulf P., Lois C., Sheng M., Hoogenraad C.C. Generation of lentiviral transgenic rats expressing glutamate receptor interacting protein 1 (GRIP1) in brain, spinal cord and testis. J. Neurosci. Methods 2006, 152:1-9.
87. Flotte T.R., Trapnell B.C., Humphries M., Carey B., Calcedo R., Rouhani F., Campbell-Thompson M., Yachnis A.T., Sandhaus R.A., McElvaney N.G., Mueller C., Messina L.M., Wilson J.M., Brantly M., Knop D.R., Ye G.J., Chulay J.D. Phase 2 clinical trial of a recombinant adeno-associated viral vector expressing alpha1-antitrypsin: interim results. Hum. Gene Ther. 2011, 22:1239-1247.
88. Bowles D.E., McPhee S.W., Li C., Gray S.J., Samulski J.J., Camp A.S., Li J., Wang B., Monahan P.E., Rabinowitz J.E., Grieger J.C., Govindasamy L., Agbandje-McKenna M., Xiao X., Samulski R.J. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol. Ther. 2012, 20:443-455.
89. Mori S., Wang L., Takeuchi T., Kanda T. Two novel adeno-associated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 2004, 330:375-383.
90. Daya S., Berns K.I. Gene therapy using adeno-associated virus vectors. Clin. Microbiol. Rev. 2008, 21:583-593.
91. Atchison R.W., Casto B.C., Hammon W.M. Adenovirus-associated defective virus particles. Science 1965, 149:754-756.
92. Georg-Fries B., Biederlack S., Wolf J., zur Hausen H. Analysis of proteins, helper dependence, and seroepidemiology of a new human parvovirus. Virology 1984, 134:64-71.
93. Kotin R.M., Siniscalco M., Samulski R.J., Zhu X.D., Hunter L., Laughlin C.A., McLaughlin S., Muzyczka N., Rocchi M., Berns K.I. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:2211-2215.
94. Giraud C., Winocour E., Berns K.I. Site-specific integration by adeno-associated virus is directed by a cellular DNA sequence. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:10039-10043.
95. Huser D., Gogol-Doring A., Lutter T., Weger S., Winter K., Hammer E.M., Cathomen T., Reinert K., Heilbronn R. Integration preferences of wildtype AAV-2 for consensus rep-binding sites at numerous loci in the human genome. PLoS Pathog. 2010, 6:e1000985.
96. Zincarelli C., Soltys S., Rengo G., Rabinowitz J.E. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol. Ther. 2008, 16:1073-1080.
97. Cearley C.N., Wolfe J.H. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol. Ther. 2006, 13:528-537.
98. Chiorini J.A., Yang L., Liu Y., Safer B., Kotin R.M. Cloning of adeno-associated virus type 4 (AAV4) and generation of recombinant AAV4 particles. J. Virol. 1997, 71:6823-6833.
99. Rutledge E.A., Halbert C.L., Russell D.W. Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J. Virol. 1998, 72:309-319.
100. Burger C., Gorbatyuk O.S., Velardo M.J., Peden C.S., Williams P., Zolotukhin S., Reier P.J., Mandel R.J., Muzyczka N. Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol. Ther. 2004, 10:302-317.
101. Wang C., Wang C.M., Clark K.R., Sferra T.J. Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Ther. 2003, 10:1528-1534.
102. Harding T.C., Dickinson P.J., Roberts B.N., Yendluri S., Gonzalez-Edick M., Lecouteur R.A., Jooss K.U. Enhanced gene transfer efficiency in the murine striatum and an orthotopic glioblastoma tumor model, using AAV-7- and AAV-8-pseudotyped vectors. Hum. Gene Ther. 2006, 17:807-820.
103. Klein R.L., Dayton R.D., Leidenheimer N.J., Jansen K., Golde T.E., Zweig R.M. Efficient neuronal gene transfer with AAV8 leads to neurotoxic levels of tau or green fluorescent proteins. Mol. Ther. 2006, 13:517-527.
104. Klein R.L., Dayton R.D., Tatom J.B., Henderson K.M., Henning P.P. AAV8, 9, Rh10, Rh43 vector gene transfer in the rat brain: effects of serotype, promoter and purification method. Mol. Ther. 2008, 16:89-96.
105. Duque S., Joussemet B., Riviere C., Marais T., Dubreil L., Douar A.M., Fyfe J., Moullier P., Colle M.A., Barkats M. Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol. Ther. 2009, 17:1187-1196.
106. Foust K.D., Nurre E., Montgomery C.L., Hernandez A., Chan C.M., Kaspar B.K. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat. Biotechnol. 2009, 27:59-65.
107. Wu P., Phillips M.I., Bui J., Terwilliger E.F. Adeno-associated virus vector-mediated transgene integration into neurons and other nondividing cell targets. J. Virol. 1998, 72:5919-5926.
108. McCown T.J. Adeno-associated virus (AAV) vectors in the CNS. Curr. Gene Ther. 2005, 5:333-338.
109. Berns K.I., Pinkerton T.C., Thomas G.F., Hoggan M.D. Detection of adeno-associated virus (AAV)-specific nucleotide sequences in DNA isolated from latently infected Detroit 6 cells. Virology 1975, 68:556-560.
110. Muzyczka N. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 1992, 158:97-129.
111. Zaiss A.K., Liu Q., Bowen G.P., Wong N.C., Bartlett J.S., Muruve D.A. Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 2002, 76:4580-4590.
112. Samulski R.J., Chang L.S., Shenk T. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression. J. Virol. 1989, 63:3822-3828.
113. Xiao X., Li J., Samulski R.J. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 1998, 72:2224-2232.
114. Srivastava A., Lusby E.W., Berns K.I. Nucleotide sequence and organization of the adeno-associated virus 2 genome. J. Virol. 1983, 45:555-564.
115. Allocca M., Doria M., Petrillo M., Colella P., Garcia-Hoyos M., Gibbs D., Kim S.R., Maguire A., Rex T.S., Di Vicino U., Cutillo L., Sparrow J.R., Williams D.S., Bennett J., Auricchio A. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J. Clin. Invest. 2008, 118:1955-1964.
116. Wisniewski H.M., Ghetti B., Terry R.D. Neuritic (senile) plaques and filamentous changes in aged rhesus monkeys. J. Neuropathol. Exp. Neurol. 1973, 32:566-584.
117. Kanemaru K., Iwatsubo T., Ihara Y. Comparable amyloid beta-protein (A beta) 42(43) and A beta 40 deposition in the aged monkey brain. Neurosci. Lett. 1996, 214:196-198.
118. Schultz C., Dehghani F., Hubbard G.B., Thal D.R., Struckhoff G., Braak E., Braak H. Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons. J. Neuropathol. Exp. Neurol. 2000, 59:39-52.
119. Schultz C., Hubbard G.B., Rub U., Braak E., Braak H. Age-related progression of tau pathology in brains of baboons. Neurobiol. Aging 2000, 21:905-912.
120. Kiatipattanasakul W., Nakayama H., Yongsiri S., Chotiapisitkul S., Nakamura S., Kojima H., Doi K. Abnormal neuronal and glial argyrophilic fibrillary structures in the brain of an aged albino cynomolgus monkey (Macaca fascicularis). Acta Neuropathol. 2000, 100:580-586.
121. Head E. Neurobiology of the aging dog. Age (Dordr.) 2011, 33:485-496.
122. Head E., McCleary R., Hahn F.F., Milgram N.W., Cotman C.W. Region-specific age at onset of beta-amyloid in dogs. Neurobiol. Aging 2000, 21:89-96.
123. Pugliese M., Mascort J., Mahy N., Ferrer I. Diffuse beta-amyloid plaques and hyperphosphorylated tau are unrelated processes in aged dogs with behavioral deficits. Acta Neuropathol. 2006, 112:175-183.
124. Martin L.J., Sisodia S.S., Koo E.H., Cork L.C., Dellovade T.L., Weidemann A., Beyreuther K., Masters C., Price D.L. Amyloid precursor protein in aged nonhuman primates. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:1461-1465.
125. Struble R.G., Price D.L., Cork L.C., Price D.L. Senile plaques in cortex of aged normal monkeys. Brain Res. 1985, 361:267-275.
126. Radde R., Duma C., Goedert M., Jucker M. The value of incomplete mouse models of Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 2008, 35(Suppl. 1):S70-S74.
127. Conn P.M. Handbook of Models for Human Aging 2006, Elsevier Academic Press, Amsterdam.
128. Richardson J.A., Burns D.K. Mouse models of Alzheimer's disease: a quest for plaques and tangles. ILAR J. 2002, 43:89-99.
129. Torres-Aleman I. Mouse models of Alzheimer's dementia: current concepts and new trends. Endocrinology 2008, 149:5952-5957.
130. Braidy N., Munoz P., Palacios A.G., Castellano-Gonzalez G., Inestrosa N.C., Chung R.S., Sachdev P., Guillemin G.J. Recent rodent models for Alzheimer's disease: clinical implications and basic research. J. Neural Transm. 2012, 119:173-195.
131. Matsui T., Ingelsson M., Fukumoto H., Ramasamy K., Kowa H., Frosch M.P., Irizarry M.C., Hyman B.T. Expression of APP pathway mRNAs and proteins in Alzheimer's disease. Brain Res. 2007, 1161:116-123.
132. Spilman P., Podlutskaya N., Hart M.J., Debnath J., Gorostiza O., Bredesen D., Richardson A., Strong R., Galvan V. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 2010, 5:e9979.
133. German D.C., Nelson O., Liang F., Liang C.L., Games D. The PDAPP mouse model of Alzheimer's disease: locus coeruleus neuronal shrinkage. J. Comp. Neurol. 2005, 492:469-476.
134. Schenk D., Barbour R., Dunn W., Gordon G., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Liao Z., Lieberburg I., Motter R., Mutter L., Soriano F., Shopp G., Vasquez N., Vandevert C., Walker S., Wogulis M., Yednock T., Games D., Seubert P. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999, 400:173-177.
135. Bard F., Cannon C., Barbour R., Burke R.L., Games D., Grajeda H., Guido T., Hu K., Huang J., Johnson-Wood K., Khan K., Kholodenko D., Lee M., Lieberburg I., Motter R., Nguyen M., Soriano F., Vasquez N., Weiss K., Welch B., Seubert P., Schenk D., Yednock T. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 2000, 6:916-919.
136. Bacskai B.J., Kajdasz S.T., Christie R.H., Carter C., Games D., Seubert P., Schenk D., Hyman B.T. Imaging of amyloid-beta deposits in brains of living mice permits direct observation of clearance of plaques with immunotherapy. Nat. Med. 2001, 7:369-372.
137. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 2001, 21:372-381.
138. Irizarry M.C., McNamara M., Fedorchak K., Hsiao K., Hyman B.T. APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J. Neuropathol. Exp. Neurol. 1997, 56:965-973.
139. Seo J.S., Leem Y.H., Lee K.W., Kim S.W., Lee J.K., Han P.L. Severe motor neuron degeneration in the spinal cord of the Tg2576 mouse model of Alzheimer disease. J. Alzheimers Dis. 2010, 21:263-276.
140. Boutajangout A., Goni F., Knudsen E., Schreiber F., Asuni A., Quartermain D., Frangione B., Chabalgoity A., Wisniewski T., Sigurdsson E.M. Diminished amyloid-beta burden in Tg2576 mice following a prophylactic oral immunization with a salmonella-based amyloid-beta derivative vaccine. J. Alzheimers Dis. 2009, 18:961-972.
141. Rakover I., Arbel M., Solomon B. Immunotherapy against APP beta-secretase cleavage site improves cognitive function and reduces neuroinflammation in Tg2576 mice without a significant effect on brain abeta levels. Neurodegener Dis 2007, 4:392-402.
142. Lanz T.A., Hosley J.D., Adams W.J., Merchant K.M. Studies of Abeta pharmacodynamics in the brain, cerebrospinal fluid, and plasma in young (plaque-free) Tg2576 mice using the gamma-secretase inhibitor N2-[(2S)-2-(3,5-difluorophenyl)-2-hydroxyethanoyl]-N1-[(7S)-5-methyl-6-oxo-6,7-di hydro-5H-dibenzo[b,d]azepin-7-yl]-l-alaninamide (LY-411575). J. Pharmacol. Exp. Ther. 2004, 309:49-55.
143. Bacskai B.J., Kajdasz S.T., McLellan M.E., Games D., Seubert P., Schenk D., Hyman B.T. Non-Fc-mediated mechanisms are involved in clearance of amyloid-beta in vivo by immunotherapy. J. Neurosci. 2002, 22:7873-7878.
144. Sung S., Yao Y., Uryu K., Yang H., Lee V.M., Trojanowski J.Q., Pratico D. Early vitamin E supplementation in young but not aged mice reduces Abeta levels and amyloid deposition in a transgenic model of Alzheimer's disease. FASEB J. 2004, 18:323-325.
145. Pratico D., Uryu K., Leight S., Trojanoswki J.Q., Lee V.M. Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J. Neurosci. 2001, 21:4183-4187.
146. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K.H., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P.A., Waridel C., Calhoun M.E., Jucker M., Probst A., Staufenbiel M., Sommer B. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13287-13292.
147. Beckmann N., Schuler A., Mueggler T., Meyer E.P., Wiederhold K.H., Staufenbiel M., Krucker T. Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease. J. Neurosci. 2003, 23:8453-8459.
148. Winkler D.T., Bondolfi L., Herzig M.C., Jann L., Calhoun M.E., Wiederhold K.H., Tolnay M., Staufenbiel M., Jucker M. Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J. Neurosci. 2001, 21:1619-1627.
149. Van Dam D., D'Hooge R., Staufenbiel M., Van Ginneken C., Van Meir F., De Deyn P.P. Age-dependent cognitive decline in the APP23 model precedes amyloid deposition. Eur. J. Neurosci. 2003, 17:388-396.
150. Calhoun M.E., Wiederhold K.H., Abramowski D., Phinney A.L., Probst A., Sturchler-Pierrat C., Staufenbiel M., Sommer B., Jucker M. Neuron loss in APP transgenic mice. Nature 1998, 395:755-756.
151. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 2001, 276:21562-21570.
152. Hanna A., Iremonger K., Das P., Dickson D., Golde T., Janus C. Age-related increase in amyloid plaque burden is associated with impairment in conditioned fear memory in CRND8 mouse model of amyloidosis. Alzheimers Res. Ther. 2012, 4:21.
153. Holcomb L., Gordon M.N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D., Sanders S., Zehr C., O'Campo K., Hardy J., Prada C.M., Eckman C., Younkin S., Hsiao K., Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 1998, 4:97-100.
154. Kumar-Singh S., Pirici D., McGowan E., Serneels S., Ceuterick C., Hardy J., Duff K., Dickson D., Van Broeckhoven C. Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am. J. Pathol. 2005, 167:527-543.
155. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 2001, 17:157-165.
156. Gureviciene I., Ikonen S., Gurevicius K., Sarkaki A., van Groen T., Pussinen R., Ylinen A., Tanila H. Normal induction but accelerated decay of LTP in APP+PS1 transgenic mice. Neurobiol. Dis. 2004, 15:188-195.
157. Reiserer R.S., Harrison F.E., Syverud D.C., McDonald M.P. Impaired spatial learning in the APPSwe+PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav. 2007, 6:54-65.
158. Siman R., Reaume A.G., Savage M.J., Trusko S., Lin Y.G., Scott R.W., Flood D.G. Presenilin-1 P264L knock-in mutation: differential effects on abeta production, amyloid deposition, and neuronal vulnerability. J. Neurosci. 2000, 20:8717-8726.
159. Flood D.G., Reaume A.G., Dorfman K.S., Lin Y.G., Lang D.M., Trusko S.P., Savage M.J., Annaert W.G., De Strooper B., Siman R., Scott R.W. FAD mutant PS-1 gene-targeted mice: increased A beta 42 and A beta deposition without APP overproduction. Neurobiol. Aging 2002, 23:335-348.
160. Reaume A.G., Howland D.S., Trusko S.P., Savage M.J., Lang D.M., Greenberg B.D., Siman R., Scott R.W. Enhanced amyloidogenic processing of the beta-amyloid precursor protein in gene-targeted mice bearing the Swedish familial Alzheimer's disease mutations and a "humanized" Abeta sequence. J. Biol. Chem. 1996, 271:23380-23388.
161. Murphy M.P., Beckett T.L., Ding Q., Patel E., Markesbery W.R., St Clair D.K., LeVine H., Keller J.N. Abeta solubility and deposition during AD progression and in APPxPS-1 knock-in mice. Neurobiol. Dis. 2007, 27:301-311.
162. Oakley H., Cole S.L., Logan S., Maus E., Shao P., Craft J., Guillozet-Bongaarts A., Ohno M., Disterhoft J., Van Eldik L., Berry R., Vassar R. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 2006, 26:10129-10140.
163. Ohno M., Cole S.L., Yasvoina M., Zhao J., Citron M., Berry R., Disterhoft J.F., Vassar R. BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice. Neurobiol. Dis. 2007, 26:134-145.
164. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., Hackett J., Adamson J., Lincoln S., Dickson D., Davies P., Petersen R.C., Stevens M., de Graaff E., Wauters E., van Baren J., Hillebrand M., Joosse M., Kwon J.M., Nowotny P., Che L.K., Norton J., Morris J.C., Reed L.A., Trojanowski J., Basun H., Lannfelt L., Neystat M., Fahn S., Dark F., Tannenberg T., Dodd P.R., Hayward N., Kwok J.B., Schofield P.R., Andreadis A., Snowden J., Craufurd D., Neary D., Owen F., Oostra B.A., Hardy J., Goate A., van Swieten J., Mann D., Lynch T., Heutink P. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705.
165. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Paul Murphy M., Baker M., Yu X., Duff K., Hardy J., Corral A., Lin W.L., Yen S.H., Dickson D.W., Davies P., Hutton M. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 2000, 25:402-405.
166. Nasreddine Z.S., Loginov M., Clark L.N., Lamarche J., Miller B.L., Lamontagne A., Zhukareva V., Lee V.M., Wilhelmsen K.C., Geschwind D.H. From genotype to phenotype: a clinical pathological, and biochemical investigation of frontotemporal dementia and parkinsonism (FTDP-17) caused by the P301L tau mutation. Ann. Neurol. 1999, 45:704-715.
167. Andorfer C., Kress Y., Espinoza M., de Silva R., Tucker K.L., Barde Y.A., Duff K., Davies P. Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem. 2003, 86:582-590.
168. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
169. Polydoro M., Acker C.M., Duff K., Castillo P.E., Davies P. Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. J. Neurosci. 2009, 29:10741-10749.
170. Sterniczuk R., Dyck R.H., Laferla F.M., Antle M.C. Characterization of the 3xTg-AD mouse model of Alzheimer's disease: part 1. Circadian changes. Brain Res 2010, 1348:139-148.
171. Gimenez-Llort L., Blazquez G., Canete T., Johansson B., Oddo S., Tobena A., LaFerla F.M., Fernandez-Teruel A. Modeling behavioral and neuronal symptoms of Alzheimer's disease in mice: a role for intraneuronal amyloid. Neurosci. Biobehav. Rev. 2007, 31:125-147.
172. Mastrangelo M.A., Bowers W.J. Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice. BMC Neurosci. 2008, 9:81.
173. Sterniczuk R., Antle M.C., Laferla F.M., Dyck R.H. Characterization of the 3xTg-AD mouse model of Alzheimer's disease: part 2. Behavioral and cognitive changes. Brain Res 2010, 1348:149-155.
174. Oddo S., Billings L., Kesslak J.P., Cribbs D.H., LaFerla F.M. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 2004, 43:321-332.
175. Oddo S., Caccamo A., Smith I.F., Green K.N., LaFerla F.M. A dynamic relationship between intracellular and extracellular pools of Abeta. Am. J. Pathol. 2006, 168:184-194.
176. Winton M.J., Lee E.B., Sun E., Wong M.M., Leight S., Zhang B., Trojanowski J.Q., Lee V.M. Intraneuronal APP, not free Abeta peptides in 3xTg-AD mice: implications for tau versus Abeta-mediated Alzheimer neurodegeneration. J. Neurosci. 2011, 31:7691-7699.
177. Takeda S., Sato N., Uchio-Yamada K., Sawada K., Kunieda T., Takeuchi D., Kurinami H., Shinohara M., Rakugi H., Morishita R. Diabetes-accelerated memory dysfunction via cerebrovascular inflammation and Abeta deposition in an Alzheimer mouse model with diabetes. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7036-7041.
178. Naldini L., Blomer U., Gage F.H., Trono D., Verma I.M. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11382-11388.
179. Kordower J.H., Bloch J., Ma S.Y., Chu Y., Palfi S., Roitberg B.Z., Emborg M., Hantraye P., Deglon N., Aebischer P. Lentiviral gene transfer to the nonhuman primate brain. Exp. Neurol. 1999, 160:1-16.
180. Khandelwal P.J., Dumanis S.B., Herman A.M., Rebeck G.W., Moussa C.E. Wild type and P301L mutant tau promote neuro-inflammation and alpha-synuclein accumulation in lentiviral gene delivery models. Mol. Cell. Neurosci. 2012, 49:44-53.
181. Kanninen K., Heikkinen R., Malm T., Rolova T., Kuhmonen S., Leinonen H., Yla-Herttuala S., Tanila H., Levonen A.L., Koistinaho M., Koistinaho J. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:16505-16510.
182. Singer O., Marr R.A., Rockenstein E., Crews L., Coufal N.G., Gage F.H., Verma I.M., Masliah E. Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat. Neurosci. 2005, 8:1343-1349.
183. Peng K.A., Masliah E. Lentivirus-expressed siRNA vectors against Alzheimer disease. Methods Mol. Biol. 2010, 614:215-224.
184. Zhao X., Wen L., Li G., Ba Q., Cui Y., Han Z., Jia Y., Xu Y. Lentivirus-mediated APP695-RNAi reduces apoptosis in APP transgenic mouse neurons. Neuroreport 2011, 22:804-808.
185. Jaworski T., Dewachter I., Lechat B., Croes S., Termont A., Demedts D., Borghgraef P., Devijver H., Filipkowski R.K., Kaczmarek L., Kugler S., Van Leuven F. AAV-tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice. PLoS One 2009, 4:e7280.
186. Klein R.L., Dayton R.D., Tatom J.B., Diaczynsky C.G., Salvatore M.F. Tau expression levels from various adeno-associated virus vector serotypes produce graded neurodegenerative disease states. Eur. J. Neurosci. 2008, 27:1615-1625.
187. Xu Q., Chou B., Fitzsimmons B., Miyanohara A., Shubayev V., Santucci C., Hefferan M., Marsala M., Hua X.Y. In vivo gene knockdown in rat dorsal root ganglia mediated by self-complementary adeno-associated virus serotype 5 following intrathecal delivery. PLoS One 2012, 7:e32581.
188. Piedrahita D., Hernandez I., Lopez-Tobon A., Fedorov D., Obara B., Manjunath B.S., Boudreau R.L., Davidson B., Laferla F., Gallego-Gomez J.C., Kosik K.S., Cardona-Gomez G.P. Silencing of CDK5 reduces neurofibrillary tangles in transgenic Alzheimer's mice. J. Neurosci. 2010, 30:13966-13976.
189. Dassie E., Andrews M.R., Bensadoun J.C., Cacquevel M., Schneider B.L., Aebischer P., Wouters F.S., Richardson J.C., Hussain I., Howlett D.R., Spillantini M.G., Fawcett J.W. Focal expression of adeno-associated viral-mutant tau induces widespread impairment in an APP mouse model. Neurobiol. Aging 2013, 34:1355-1368.
190. Lambert J.C., Heath S., Even G., Campion D., Sleegers K., Hiltunen M., Combarros O., Zelenika D., Bullido M.J., Tavernier B., Letenneur L., Bettens K., Berr C., Pasquier F., Fievet N., Barberger-Gateau P., Engelborghs S., De Deyn P., Mateo I., Franck A., Helisalmi S., Porcellini E., Hanon O., de Pancorbo M.M., Lendon C., Dufouil C., Jaillard C., Leveillard T., Alvarez V., Bosco P., Mancuso M., Panza F., Nacmias B., Bossu P., Piccardi P., Annoni G., Seripa D., Galimberti D., Hannequin D., Licastro F., Soininen H., Ritchie K., Blanche H., Dartigues J.F., Tzourio C., Gut I., Van Broeckhoven C., Alperovitch A., Lathrop M., Amouyel P. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat. Genet. 2009, 41:1094-1099.
191. Harold D., Abraham R., Hollingworth P., Sims R., Gerrish A., Hamshere M.L., Pahwa J.S., Moskvina V., Dowzell K., Williams A., Jones N., Thomas C., Stretton A., Morgan A.R., Lovestone S., Powell J., Proitsi P., Lupton M.K., Brayne C., Rubinsztein D.C., Gill M., Lawlor B., Lynch A., Morgan K., Brown K.S., Passmore P.A., Craig D., McGuinness B., Todd S., Holmes C., Mann D., Smith A.D., Love S., Kehoe P.G., Hardy J., Mead S., Fox N., Rossor M., Collinge J., Maier W., Jessen F., Schurmann B., van den Bussche H., Heuser I., Kornhuber J., Wiltfang J., Dichgans M., Frolich L., Hampel H., Hull M., Rujescu D., Goate A.M., Kauwe J.S., Cruchaga C., Nowotny P., Morris J.C., Mayo K., Sleegers K., Bettens K., Engelborghs S., De Deyn P.P., Van Broeckhoven C., Livingston G., Bass N.J., Gurling H., McQuillin A., Gwilliam R., Deloukas P., Al-Chalabi A., Shaw C.E., Tsolaki M., Singleton A.B., Guerreiro R., Muhleisen T.W., Nothen M.M., Moebus S., Jockel K.H., Klopp N., Wichmann H.E., Carrasquillo M.M., Pankratz V.S., Younkin S.G., Holmans P.A., O'Donovan M., Owen M.J., Williams J. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat. Genet. 2009, 41:1088-1093.
192. Chapuis J., Hansmannel F., Gistelinck M., Mounier A., Van Cauwenberghe C., Kolen K.V., Geller F., Sottejeau Y., Harold D., Dourlen P., Grenier-Boley B., Kamatani Y., Delepine B., Demiautte F., Zelenika D., Zommer N., Hamdane M., Bellenguez C., Dartigues J.F., Hauw J.J., Letronne F., Ayral A.M., Sleegers K., Schellens A., Broeck L.V., Engelborghs S., De Deyn P.P., Vandenberghe R., O'Donovan M., Owen M., Epelbaum J., Mercken M., Karran E., Bantscheff M., Drewes G., Joberty G., Campion D., Octave J.N., Berr C., Lathrop M., Callaerts P., Mann D., Williams J., Buee L., Dewachter I., Van Broeckhoven C., Amouyel P., Moechars D., Dermaut B., Lambert J.C. Increased expression of BIN1 mediates Alzheimer genetic risk by modulating tau pathology. Mol Psychiatry 2013.
193. Muller A.J., Baker J.F., DuHadaway J.B., Ge K., Farmer G., Donover P.S., Meade R., Reid C., Grzanna R., Roach A.H., Shah N., Soler A.P., Prendergast G.C. Targeted disruption of the murine Bin1/Amphiphysin II gene does not disable endocytosis but results in embryonic cardiomyopathy with aberrant myofibril formation. Mol. Cell. Biol. 2003, 23:4295-4306.
194. Fugier C., Klein A.F., Hammer C., Vassilopoulos S., Ivarsson Y., Toussaint A., Tosch V., Vignaud A., Ferry A., Messaddeq N., Kokunai Y., Tsuburaya R., de la Grange P., Dembele D., Francois V., Precigout G., Boulade-Ladame C., Hummel M.C., Lopez de Munain A., Sergeant N., Laquerriere A., Thibault C., Deryckere F., Auboeuf D., Garcia L., Zimmermann P., Udd B., Schoser B., Takahashi M.P., Nishino I., Bassez G., Laporte J., Furling D., Charlet-Berguerand N. Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy. Nat. Med. 2011, 17:720-725.
195. Ren G., Vajjhala P., Lee J.S., Winsor B., Munn A.L. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 2006, 70:37-120.
196. Kar A., Kuo D., He R., Zhou J., Wu J.Y. Tau alternative splicing and frontotemporal dementia. Alzheimer Dis. Assoc. Disord. 2005, 19(Suppl. 1):S29-S36.