Apolipoprotein E-mimetics inhibit neurodegeneration and restore cognitive functions in a transgenic drosophila model of Alzheimer's disease

PLoS ONE

Volumn 4, Issue 12, 2009, Pages

  Sarantseva, Svetlana ^a   Timoshenko, Svetlana ^a   Bolshakova, Olga ^a   Karaseva, Eugenia ^a   Rodin, Dmitry ^a   Schwarzman, Alexander L ^a,b   Vitek, Michael P ^c,d  

^a PETERSBURG NUCLEAR PHYSICS INSTITUTE   (Russian Federation)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Russian Federation)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d Optimal Screening Vehicles Division   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; COG 112; COG 133; GREEN FLUORESCENT PROTEIN; NEUROPROTECTIVE AGENT; SYNAPTOBREVIN; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; DRUG EFFICACY; GENE OVEREXPRESSION; LEARNING; MEMORY; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN AGGREGATION; PROTEIN SECRETION; SYNAPTIC TRANSMISSION;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOLIPOPROTEINS E; BRAIN; COGNITION; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; GREEN FLUORESCENT PROTEINS; HUMANS; MEMORY; NERVE DEGENERATION; PEPTIDES; R-SNARE PROTEINS;

DROSOPHILA MELANOGASTER;

EID: 77949510114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008191     Document Type: Article

References (56)

1. Davis KL, Samuels SC (1998) Dementia and delerium. In: Enna SJ, Coyle JT, eds. Pharmacological Management of Neurological and Psychiatric Disorders. New York: McGraw-Hill. pp 267-316.
2. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, et al. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlateof cognitiveimpairment. Ann Neurol 30: 572-580.
3. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298: 789-791.
4. Walsh DM, Selkoe DJ (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44: 181-193.
5. Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer's disease. Neurobiol Aging 24: 1023-1027.
6. Isacson O (2004) Problems and solutions for circuits and synapses in Parkinson's disease. Neuron 43: 165-168.
7. Li J-Y, Plomann M, Brundin P (2003) Huntington's Disease: a synaptopathy? Trends Mol Med 9: 414-420.
8. Wishart TM, Parson SH, Gillingwater TH (2006) Synaptic vulnerability in neurodegenerative disease. J Neuropathol Exp Neurol 65: 733-739
9. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, et al. (2003) Tripletransgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421.
10. Day M, Wang Z, Ding J, An X, Ingham CA, et al. (2006) Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9(2): 251-9.
11. Lee WC, Yoshihara M, Lttleton JT (2004) Cytoplasmic aggregates trap polyglutaminecontaining proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc Natl Acad Sci USA 101: 3224-3229
12. Cunningham C, Deacon R, Wells H, Boche D, Waters S, et al. (2003) Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 17(10): 2147-55.
13. Hardy J (1997) Amyloid, the presenilins and Alzheimer_s disease. Trends Neurosci 20: 154-159.
14. De Strooper B, Annaert W (2002) Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci 113: 1857-70
15. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. An updated summary of the amyloid hypothesis. Science 297: 353-356.
16. De Strooper B (2003) Aph-1, Pen-2, and Nicastrin with Presenilin generate an active _-secretase complex. Neuron 38: 9-12.
17. Torroja L, Packard M, Gorczyca M, White K, Budnik V (1999) The Drosophila b-Amyloid Precursor Protein homolog promotes synapse differentiation at the neuromuscular junction. J Neurosci 15: 7793-7803.
18. Luo L, Martin-Morri LE, White K (1990) Identification, secretion, and neural expression of APPL Drosophila protein similar to human amyloid protein precursor. J Neurosci 10: 3849-3861.
19. Fossgreen A, Bruckner B, Czech C, Masters CL, Beyreuther K, et al. (1998) Transgenic Drosophila expressing human amyloid precursor protein show gamma-secretase activity and a blistered-wing phenotype. Proc Natl Acad Sci U S A 95(23): 13703-8.
20. Greeve I, Kretzschmar D, Tschape J-A, Beyn A, Brellinger C, et al. (2004) Agedependent neurodegeneration and Alzheimer-amyloid plaque formation in transgenic Drosophila. J Neurisci 24: 3899-3906.
21. Laskowitz DT, Fillit H, Yeung N, Toku K, Vitek MP (2006) Apolipoprotein E- derived peptides reduce CNS inflammation: implications for therapy of neurological disease. Acta Neurol Scand S185: 15-20.
22. Laskowitz DT, Vitek MP (2007) Apolipoprotein E and neurological disease: therapeutic potential and pharmacogenomic interactions. Pharmacogenomics 8: 959-969.
23. Wang H, Durham L, Dawson H, Song P, Warner DS, et al. (2007) An apolipoprotein ebased therapeutic improves outcome and reduce Alzheimer's disease pathology following closed head injury: evidence of pharmacogenomic interaction. Neuroscience 144: 1324-33.
24. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415
25. Luo L, Liao YJ, Jan LY, Jan YN (1994) Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev 8: 1787-1802.
26. Merdes G, Soba P, Loewer F, Bilic MV, Beyreuther K, et al. (2004) Interference of human and Drosophila APP and APP-like proteins with PNS development in Drosophila. EMBO J 23: 4082-4095.
27. Tienari PJ, De Strooper B, Ikonen E, et al. (1996) The Beta-amyloid domain is Essential for axonal sorting of amyloid precursor pProtein. EMBO J 15: 5218-5229.
28. Goldstein LS (2003) Do disorders of movement cause movement disorders and dementia? Neuron 40(2): 415-25.
29. Muqit MM, Feany MB (2002) Modelling neurodegenerative diseases in Drosophila: a fruitful approach? Nat Rev Neurosci 3: 237-243
30. Tully T, Quinn W (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol 157: 263-277
31. Rousselle C, Clair P, Lefauconnier JM, Kaczorek M, Scherrmann JM, et al. (2000) New advances in the transport of doxorubicin through the blood - brain barrier by a peptide vectormediated strategy. Mol Pharmacol 57: 679-686
32. Li F-Q, Sempowski GD, McKenna SE, Laskowitz DT, Colton CA, et al. (2006) Apolipoprotein E-derived peptides ameliorate clinical disability and inflammatory infiltrates into the spinal cord in a murine model of multiple sclerosis. J Pharmacol Exp Ther 318: 956-965.
33. Peng T, Liu Y-H, Yang C-L, Wan C-M, Wang Y-Q, et al. (2004) A new peptide with membrane-permeable function derived from human circadian proteins. Acta Biochimica et Biophysica Sinica 36: 629-636.
34. Schwarzman AL, Tsiper M, Gregori L, Goldgaber D, Fracowiak J, et al. (2005) Selection of peptides binding to the amyloid _-protein reveals potential inhibitors of amyloid formation. Amyloid: J Protein Folding Disord 12: 1-11
35. Irvine GB, El-Agnaf OM, ShankarGM, Walsh DM (2008) Protein aggregation in the brain: the molecular basis for Alzheimer's and Parkinson's diseases. Mol Med 14: 451-464.
36. Saura CA, Choi S.-Y, Beglopoulos V, Malkani S, Zhang D, et al. (2004) Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42: 23-36
37. Shen J, Kelleher RJ (2007) The presenilin hypothesis of Alzheimer's disease: Evidence for a loss-of-function pathogenic mechanism. Proc Natl Acad Sci USA 104: 403-409.
38. Seabrook GR, Smith DW, Bowery BJ, Easter A, Reynolds T, et al. (1999) Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein. Neuropharmacology 38: 349-359
39. Senechal Y, Larmet Y, Dev KK (2006) Unraveling in vivo functions of amyloid precursor protein: Insights from knockout and knockdown studies Neurodegenerative Dis 3: 134-147.
40. Iijima K, Liu H-P, Chiang A-S, Hearn SA, Konsolaki M, et al. (2004) Dissecting the pathological effects of human A_ 40 and A _42 in Drosophila: A potential model for Alzheimer's disease. Proc Nat Acad Sci USA 101: 6623-6628
41. Crowther DC, Kinghorn KJ, Miranda AE, Page R, Curry JA, et al. (2005) Intraneuronal A_, non-amyloid aggregates and neurodefeneration in Drosophila model of Alzheimer's disease. Neuroscience 132: 123-135.
42. Iijima K, Chiang HC, Hearn S A, Hakker I, Gatt A, et al. (2008) Abeta42 mutants with different aggregation profiles induce distinct pathologies in Drosophila. PLoS ONE 3: e1703: 1-9.
43. Chiang H-C, Iijima K, Hakker I, Zhong Y (2009) Distinctive roles of different _-amyloid 1-42 aggregates in modulation of synaptic functions. FASEB J 23(6): 1969-77.
44. Carmine-Simmen K, Prostor T, Tschape J, Poeck B, Triphan T, et al. (2008) Neurotoxic effects induced by the Drosophila amyloid-beta peptide suggest a conserved toxic functions. Neurobiol Dis 33: 274-28.
45. Sarantseva SV, Bol shakova OI, Timoshenko SI, Rodin DI, Vitek MP, et al. (2009) Studying the pathogenesis of Alzheimer's disease in a Drosophila melanogaster model: Human APP overexpression in the brain of transgenic flies leads to deficit of the synaptic protein synaptotagmin. Genetika Jan;45(1): 119-26.
46. Gunawardena S, Goldstein LS (2001) Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32: 389-401.
47. Ashe KH (2000) Synaptic structure and function in transgenic APP mice. Ann NY Acad Sci 924: 39-41.
48. Lu B, Vogel H (2009) Drosophila models of neurodegenerative diseases. Annu Rev Pathol Mech Dis 4: 315-342.
49. Bolton SJ, Jones DN, Darker JG, Eggleston DS, Hunter AJ, et al. (2000) Cellular uptake and spread of the cell-permeable peptide penetratin in adult rat brain. Eur J Neurosci 12: 2847-2855.
50. Sarantseva SV, Bolshakova OI, Timoshenko SI, Kolobov AA, Vitek MP, et al. (2009) Protein transduction domain peptides mediates delivery to the brain via the blood-brain barrier in Drosophila melanogaster. Biochemistry (Moscow) Supplement Series B: Biomedical Chemistry 3: 149-155.
51. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, et al. (2006) Ubiquitin hydrolase Uch-L1 rescues b-amyloid-induced decreases in synaptic function and contextual memory. Cell 126: 775-88.
52. Caccamo A, Oddo S, Billings L, Green K, Martinez-Coria H, et al. (2006) M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49: 671-682.
53. Adlard PA, Cherny RA, Finkelstein DI, Gautier E, Robb E, et al. (2008) Rapid restoration of cognition in Alzheimer's transgenic mice with 8-Hydroxy Quinoline analogs is associated with decreased interstitial Ab Neuron 59: 43-55.
54. Sheng Z, Prorok M, Brown BE, Castellino FJ (2008) N-methyl-D-aspartate receptor inhibition by an apolipoprotein E-derived peptide relies on low-density lipoprotein receptor-associated protein. Neuropharmacology 55: 204-214
55. Singh K, Chaturvedi R, Asim M, Barry DP, Lewis ND, et al. (2008) The apolipoprotein Emimetic peptide COG112 inhibits the inflammatory response to Citrobacter rodentium in colonic epithelial cells by preventing NF_B activation. J Biol Chem 283: 16752-16761.
56. Tan L, Schedl1 P, Song H-J, Garza D, Konsolaki M (2008) The Toll_NF_B signaling pathway mediates the neuropathological effects of the human Alzheimer's Ab42 polypeptide in Drosophila. PLoS ONE 3(12): e3966: 1-10.