Cellular prion protein modulates β-amyloid deposition in aged APP/PS1 transgenic mice

Neurobiology of Aging

Volumn 34, Issue 12, 2013, Pages 2793-2804

  Ordóñez Gutiérrez, Lara ^a,b   Torres, Juan María ^c   Gavín, Rosalina ^b,d,e   Antón, Marta ^a,b   Arroba Espinosa, Ana Isabel ^c   Espinosa, Juan Carlos ^c   Vergara, Cristina ^b,d,e   del Río, José A ^b,d,e   Wandosell, Francisco ^a,b  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria   (Spain)

^d INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Aging; Amyloid; Neurodegeneration; Prion; Signaling

Indexed keywords

AMYLOID BETA PROTEIN; CELL PROTEIN; PRION PROTEIN; PROTEIN KINASE FYN; PROTEIN TGA20; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL LEVEL; CONTROLLED STUDY; CROSS BREEDING; ENZYME ACTIVATION; GENE; GENE DOSAGE; GENE EXPRESSION; IN VIVO STUDY; INFECTION; MOUSE; NONHUMAN; PARENCHYMA; PRION DISEASE; PRIORITY JOURNAL; PRNP GENE; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SENILE PLAQUE; TRANSGENIC MOUSE;

AGING; AMYLOID; NEURODEGENERATION; PRION; SIGNALING;

AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC; PRESENILIN-1; PRIONS; PRPC PROTEINS;

EID: 84884140563     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.05.019     Document Type: Article

References (64)

1. Abramowski D., Rabe S., Upadhaya A.R., Reichwald J., Danner S., Staab D., Capetillo-Zarate E., Yamaguchi H., Saido T.C., Wiederhold K.H., Thal D.R., Staufenbiel M. Transgenic expression of intraneuronal Abeta42 but not Abeta40 leads to cellular Abeta lesions, degeneration, and functional impairment without typical Alzheimer's disease pathology. J Neurosci 2012, 32:1273-1283.
2. Baier M., Apelt J., Riemer C., Gultner S., Schwarz A., Bamme T., Burwinkel M., Schliebs R. Prion infection of mice transgenic for human APPSwe: increased accumulation of cortical formic acid extractable Abeta(1-42) and rapid scrapie disease development. Int J Dev Neurosci 2008, 26:821-824.
3. Balducci C., Beeg M., Stravalaci M., Bastone A., Sclip A., Biasini E., Tapella L., Colombo L., Manzoni C., Borsello T., Chiesa R., Gobbi M., Salmona M., Forloni G. Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc Natl Acad Sci U S A 2010, 107:2295-2300.
4. Bendheim P.E., Brown H.R., Rudelli R.D., Scala L.J., Goller N.L., Wen G.Y., Kascsak R.J., Cashman N.R., Bolton D.C. Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology 1992, 42:149-156.
5. Bhaskar K., Hobbs G.A., Yen S.H., Lee G. Tyrosine phosphorylation of tau accompanies disease progression in transgenic mouse models of tauopathy. Neuropathol Appl Neurobiol 2010, 36:462-477.
6. Boland B., Smith D.A., Mooney D., Jung S.S., Walsh D.M., Platt F.M. Macroautophagy is not directly involved in the metabolism of amyloid precursor protein. J Biol Chem 2010, 285:37415-37426.
7. Borchelt D.R., Ratovitski T., van Lare J., Lee M.K., Gonzales V., Jenkins N.A., Copeland N.G., Price D.L., Sisodia S.S. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997, 19:939-945.
8. Brown D.R., Hafiz F., Glasssmith L.L., Wong B.S., Jones I.M., Clive C., Haswell S.J. Consequences of manganese replacement of copper for prion protein function and proteinase resistance. Embo J 2000, 19:1180-1186.
9. Bueler H., Fischer M., Lang Y., Bluethmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., Weissmann C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 1992, 356:577-582.
10. Cai Y., Zhang X.M., Macklin L.N., Cai H., Luo X.G., Oddo S., Laferla F.M., Struble R.G., Rose G.M., Patrylo P.R., Yan X.X. BACE1 Elevation is Involved in Amyloid Plaque Development in the Triple Transgenic Model of Alzheimer's Disease: Differential Abeta Antibody Labeling of Early-Onset Axon Terminal Pathology. Neurotox Res 2011, 21:160-174.
11. Calella A.M., Farinelli M., Nuvolone M., Mirante O., Moos R., Falsig J., Mansuy I.M., Aguzzi A. Prion protein and Abeta-related synaptic toxicity impairment. EMBO Mol Med 2010, 2:306-314.
12. Capetillo-Zarate E., Gracia L., Tampellini D., Gouras G.K. Intraneuronal Abeta accumulation, amyloid plaques, and synapse pathology in Alzheimer's disease. Neurodegener Dis 2012, 10:56-59.
13. Cashman N.R., Loertscher R., Nalbantoglu J., Shaw I., Kascsak R.J., Bolton D.C., Bendheim P.E. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 1990, 61:185-192.
14. Castilla J., Gutierrez Adan A., Brun A., Pintado B., Ramirez M.A., Parra B., Doyle D., Rogers M., Salguero F.J., Sanchez C., Sanchez-Vizcaino J.M., Torres J.M. Early detection of PrPres in BSE-infected bovine PrP transgenic mice. Arch Virol 2003, 148:677-691.
15. Cataldo A.M., Barnett J.L., Mann D.M., Nixon R.A. Colocalization of lysosomal hydrolase and beta-amyloid in diffuse plaques of the cerebellum and striatum in Alzheimer's disease and Down's syndrome. J Neuropathol Exp Neurol 1996, 55:704-715.
16. Chin J., Palop J.J., Puolivali J., Massaro C., Bien-Ly N., Gerstein H., Scearce-Levie K., Masliah E., Mucke L. Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J Neurosci 2005, 25:9694-9703.
17. Chung E., Ji Y., Sun Y., Kascsak R.J., Kascsak R.B., Mehta P.D., Strittmatter S.M., Wisniewski T. Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neurosci 2010, 11:130-140.
18. Curtis J., Errington M., Bliss T., Voss K., MacLeod N. Age-dependent loss of PTP and LTP in the hippocampus of PrP-null mice. Neurobiol Dis 2003, 13:55-62.
19. DeKosky S.T., Scheff S.W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990, 27:457-464.
20. Dodelet V.C., Cashman N.R. Prion protein expression in human leukocyte differentiation. Blood 1998, 91:1556-1561.
21. Feraudet C., Morel N., Simon S., Volland H., Frobert Y., Creminon C., Vilette D., Lehmann S., Grassi J. Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem 2005, 280:11247-11258.
22. Fischer M., Rulicke T., Raeber A., Sailer A., Moser M., Oesch B., Brandner S., Aguzzi A., Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. Embo J 1996, 15:1255-1264.
23. Freir D.B., Fedriani R., Scully D., Smith I.M., Selkoe D.J., Walsh D.M., Regan C.M. Abeta oligomers inhibit synapse remodelling necessary for memory consolidation. Neurobiol Aging 2011, 32:2211-2218.
24. Gimbel D.A., Nygaard H.B., Coffey E.E., Gunther E.C., Lauren J., Gimbel Z.A., Strittmatter S.M. Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 2010, 30:6367-6374.
25. Griffiths H.H., Whitehouse I.J., Baybutt H., Brown D., Kellett K.A., Jackson C.D., Turner A.J., Piccardo P., Manson J.C., Hooper N.M. Prion protein interacts with BACE1 protein and differentially regulates its activity toward wild type and Swedish mutant amyloid precursor protein. J Biol Chem 2011, 286:33489-33500.
26. Haig D.A., Clarke M.C. Multiplication of the scrapie agent. Nature 1971, 234:106-107.
27. Halford R., Russell D. Reduction of cholesterol synthesis in the mouse brain does not affect amyloid formation in Alzheimer'sdisease, but does extend lifespan. Proc Natl Acad Sci U S A 2009, 106:3502-3506.
28. Ho G.J., Hashimoto M., Adame A., Izu M., Alford M.F., Thal L.J., Hansen L.A., Masliah E. Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: implications for its functional role. Neurobiol Aging 2005, 26:625-635.
29. Hsia A.Y., Masliah E., McConlogue L., Yu G.Q., Tatsuno G., Hu K., Kholodenko D., Malenka R.C., Nicoll R.A., Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci U S A 1999, 96:3228-3233.
30. Ilaria, L., Cristina G., Chiara T., Anna F., Teresa E.D., Fiorella C. "Abeta plaque-associated glial reaction as a determinant of apoptotic neuronal death and cortical gliogenesis: A study in APP mutant mice.". Neurosci Lett 2011, 506:94-99.
31. Jaeger P.A., Pickford F., Sun C.H., Lucin K.M., Masliah E., Wyss-Coray T. Regulation of amyloid precursor protein processing by the Beclin 1 complex. PLoS One 2010, 5:e11102.
32. 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.
33. Johnson-Wood K., Lee M., Motter R., Hu K., Gordon G., Barbour R., Khan K., Gordon M., Tan H., Games D., Lieberburg I., Schenk D., Seubert P., McConlogue L. Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease. Proc Natl Acad Sci U S A 1997, 94:1550-1555.
34. Kaiser D.M., Acharya M., Leighton P.L., Wang H., Daude N., Wohlgemuth S., Shi B., Allison W.T. Amyloid beta precursor protein and prion protein have a conserved interaction affecting cell adhesion and CNS development. PLoS One 2012, 7:e51305.
35. Kane M.D., Lipinski W.J., Callahan M.J., Bian F., Durham R.A., Schwarz R.D., Roher A.E., Walker L.C. Evidence for seeding of beta -amyloid by intracerebral infusion of Alzheimer brain extracts in beta -amyloid precursor protein-transgenic mice. J Neurosci 2000, 20:3606-3611.
36. 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.
37. Kellett K.A., Hooper N.M. Prion protein and Alzheimer disease. Prion 2009, 3:190-194.
38. Kessels H.W., Nguyen L.N., Nabavi S., Malinow R. The prion protein as a receptor for amyloid-beta. Nature 2010, 466:E3-E4. discussion E4-5.
39. Kurt M.A., Davies D.C., Kidd M., Duff K., Howlett D.R. Hyperphosphorylated tau and paired helical filament-like structures in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Neurobiol Dis 2003, 14:89-97.
40. Langer F., Eisele Y.S., Fritschi S.K., Staufenbiel M., Walker L.C., Jucker M. Soluble Abeta seeds are potent inducers of cerebral beta-amyloid deposition. J Neurosci 2011, 31:14488-14495.
41. Lauren J., Gimbel D.A., Nygaard H.B., Gilbert J.W., Strittmatter S.M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 2009, 457:1128-1132.
42. Lee G., Thangavel R., Sharma V.M., Litersky J.M., Bhaskar K., Fang S.M., Do L.H., Andreadis A., Van Hoesen G., Ksiezak-Reding H. Phosphorylation of tau by fyn: implications for Alzheimer's disease. J Neurosci 2004, 24:2304-2312.
43. Manson J.C., Clarke A.R., Hooper M.L., Aitchison L., McConnell I., Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 1994, 8:121-127.
44. McKee A.C., Carreras I., Hossain L., Ryu H., Klein W.L., Oddo S., LaFerla F.M., Jenkins B.G., Kowall N.W., Dedeoglu A. Ibuprofen reduces Abeta, hyperphosphorylated tau and memory deficits in Alzheimer mice. Brain Res 2008, 1207:225-236.
45. Morales R., Duran-Aniotz C., Castilla J., Estrada L.D., Soto C. De novo induction of amyloid-beta deposition in vivo. Mol Psychiatry 2011, 17:1347-1353.
46. Morales R., Estrada L.D., Diaz-Espinoza R., Morales-Scheihing D., Jara M.C., Castilla J., Soto C. Molecular cross talk between misfolded proteins in animal models of Alzheimer's and prion diseases. J Neurosci 2010, 30:4528-4535.
47. Mouillet-Richard S., Schneider B., Pradines E., Pietri M., Ermonval M., Grassi J., Richards J.G., Mutel V., Launay J.M., Kellermann O. Cellular prion protein signaling in serotonergic neuronal cells. Ann N Y Acad Sci 2007, 1096:106-119.
48. Mucke L. Neuroscience: Alzheimer's disease. Nature 2009, 461:895-897.
49. Nixon R.A., Wegiel J., Kumar A., Yu W.H., Peterhoff C., Cataldo A., Cuervo A.M. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 2005, 64:113-122.
50. Oddo S., Caccamo A., Kitazawa M., Tseng B.P., LaFerla F.M. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 2003, 24:1063-1070.
51. Padilla D., Beringue V., Espinosa J.C., Andreoletti O., Jaumain E., Reine F., Herzog L., Gutierrez-Adan A., Pintado B., Laude H., Torres J.M. Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog 2011, 7:e1001319.
52. Pammer J., Weninger W., Tschachler E. Human keratinocytes express cellular prion-related protein in vitro and during inflammatory skin diseases. Am J Pathol 1998, 153:1353-1358.
53. Parkin E.T., Watt N.T., Hussain I., Eckman E.A., Eckman C.B., Manson J.C., Baybutt H.N., Turner A.J., Hooper N.M. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc Natl Acad Sci U S A 2007, 104:11062-11067.
54. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N Engl J Med 2010, 362:329-344.
55. Rangel A., Madronal N., Gruart A., Gavin R., Llorens F., Sumoy L., Torres J.M., Delgado-Garcia J.M., Del Rio J.A. Regulation of GABA(A) and glutamate receptor expression, synaptic facilitation and long-term potentiation in the hippocampus of prion mutant mice. PLoS One 2009, 4:e7592.
56. Reilly C.E. Nonpathogenic prion protein (PrPc) acts as a cell-surface signal transducer. J Neurol 2000, 247:819-820.
57. 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.
58. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T.D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D., Younkin S. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 1996, 2:864-870.
59. Schwarze-Eicker K., Keyvani K., Gortz N., Westaway D., Sachser N., Paulus W. Prion protein (PrPc) promotes beta-amyloid plaque formation. Neurobiol Aging 2005, 26:1177-1182.
60. Selkoe D.J. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 2001, 3:75-80.
61. 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.
62. Stahl N., Borchelt D.R., Hsiao K., Prusiner S.B. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 1987, 51:229-240.
63. Takahashi R.H., Tobiume M., Sato Y., Sata T., Gouras G.K., Takahashi H. Accumulation of cellular prion protein within dystrophic neurites of amyloid plaques in the Alzheimer's disease brain. Neuropathology 2011, 31:208-214.
64. Tasdemir E., Galluzzi L., Maiuri M.C., Criollo A., Vitale I., Hangen E., Modjtahedi N., Kroemer G. Methods for assessing autophagy and autophagic cell death. Methods Mol Biol 2008, 445:29-76.