Aβ induces its own prion protein N-terminal fragment (PrPN1)-mediated neutralization in amorphous aggregates

Neurobiology of Aging

Volumn 35, Issue 7, 2014, Pages 1537-1548

  Béland, Maxime ^a   Bédard, Mikaël ^a   Tremblay, Guillaume ^a   Lavigne, Pierre ^a   Roucou, Xavier ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Cleavage; A ; Alzheimer; Amorphous aggregates; Diffuse plaques; Fibrillization; Neuroprotection; Prion; PrPN1

Indexed keywords

AMYLOID BETA PROTEIN; GUANIDINE; PRION PROTEIN;

AGED; ALZHEIMER DISEASE; AMYLOID PLAQUE; ARTICLE; AUTOPSY; CLINICAL ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; DISEASE DURATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VERY ELDERLY;

ALZHEIMER; AMORPHOUS AGGREGATES; AΒ; DIFFUSE PLAQUES; FIBRILLIZATION; NEUROPROTECTION; PRION; PRPN1; Α-CLEAVAGE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELLS, CULTURED; CRICETINAE; FEMALE; MICE; MOLECULAR TARGETED THERAPY; NEUROPROTECTIVE AGENTS; PRPC PROTEINS;

EID: 84903368117     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.02.001     Document Type: Article

References (59)

1. Alier K., Ma L., Yang J., Westaway D., Jhamandas J.H. Abeta inhibition of ionic conductance in mouse basal forebrain neurons is dependent upon the cellular prion protein PrPC. J.Neurosci. 2011, 31:16292-16297.
2. Altmeppen H.C., Prox J., Puig B., Dohler F., Falker C., Krasemann S., Glatzel M. Roles of endoproteolytic alpha-cleavage and shedding of the prion protein in neurodegeneration. FEBS J. 2013, 280:4338-4347.
3. Altmeppen H.C., Puig B., Dohler F., Thurm D.K., Falker C., Krasemann S., Glatzel M. Proteolytic processing of the prion protein in health and disease. Am. J. Neurodegener. Dis. 2012, 1:15-31.
4. 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.
5. Barry A.E., Klyubin I., Mc Donald J.M., Mably A.J., Farrell M.A., Scott M., Walsh D.M., Rowan M.J. Alzheimer's disease brain-derived amyloid-beta-mediated inhibition of LTP invivo is prevented by immunotargeting cellular prion protein. J.Neurosci. 2011, 31:7259-7263.
6. Bate C., Williams A. Amyloid-beta-induced synapse damage is mediated via cross-linkage of cellular prion proteins. J.Biol. Chem. 2011, 286:37955-37963.
7. Beland M., Motard J., Barbarin A., Roucou X. PrP(C) homodimerization stimulates the production of PrPC cleaved fragments PrPN1 and PrPC1. J.Neurosci. 2012, 32:13255-13263.
8. Beland M., Roucou X. Homodimerization as a molecular switch between low and high efficiency PrP C cell surface delivery and neuroprotective activity. Prion 2013, 7:170-174.
9. Biasini E., Turnbaugh J.A., Unterberger U., Harris D.A. Prion protein at the crossroads of physiology and disease. Trends Neurosci. 2012, 35:92-103.
10. 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.
11. Cerf E., Sarroukh R., Tamamizu-Kato S., Breydo L., Derclaye S., Dufrene Y.F., Narayanaswami V., Goormaghtigh E., Ruysschaert J.M., Raussens V. Antiparallel beta-sheet: a signature structure of the oligomeric amyloid beta-peptide. Biochem. J. 2009, 421:415-423.
12. Chen S., Yadav S.P., Surewicz W.K. Interaction between human prion protein and amyloid-beta (Abeta) oligomers: role OF N-terminal residues. J.Biol. Chem. 2010, 285:26377-26383.
13. Chen S.G., Teplow D.B., Parchi P., Teller J.K., Gambetti P., Autilio-Gambetti L. Truncated forms of the human prion protein in normal brain and in prion diseases. J.Biol. Chem. 1995, 270:19173-19180.
14. Cisse M., Sanchez P.E., Kim D.H., Ho K., Yu G.Q., Mucke L. Ablation of cellular prion protein does not ameliorate abnormal neural network activity or cognitive dysfunction in the J20 line of human amyloid precursor protein transgenic mice. J.Neurosci. 2011, 31:10427-10431.
15. Dickson D.W., Crystal H.A., Bevona C., Honer W., Vincent I., Davies P. Correlations of synaptic and pathological markers with cognition of the elderly. Neurobiol. Aging 1995, 16:285-298. discussion 298-304.
16. Ferrer I., Blanco R., Carmona M., Puig B., Ribera R., Rey M.J., Ribalta T. Prion protein expression in senile plaques in Alzheimer's disease. Acta Neuropathol. 2001, 101:49-56.
17. Fluharty B.R., Biasini E., Stravalaci M., Sclip A., Diomede L., Balducci C., La Vitola P., Messa M., Colombo L., Forloni G., Borsello T., Gobbi M., Harris D.A. An N-terminal fragment of the prion protein binds to amyloid-beta oligomers and inhibits their neurotoxicity invivo. J.Biol. Chem. 2013, 288:7857-7866.
18. Freir D.B., Nicoll A.J., Klyubin I., Panico S., Mc Donald J.M., Risse E., Asante E.A., Farrow M.A., Sessions R.B., Saibil H.R., Clarke A.R., Rowan M.J., Walsh D.M., Collinge J. Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites. Nat. Commun. 2011, 2:336.
19. Gagne D., Groulx J.F., Benoit Y.D., Basora N., Herring E., Vachon P.H., Beaulieu J.F. Integrin-linked kinase regulates migration and proliferation of human intestinal cells under a fibronectin-dependent mechanism. J.Cell. Physiol. 2010, 222:387-400.
20. 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.
21. Goggin K., Bissonnette C., Grenier C., Volkov L., Roucou X. Aggregation of cellular prion protein is initiated by proximity-induced dimerization. J.Neurochem. 2007, 102:1195-1205.
22. Guillot-Sestier M.V., Sunyach C., Ferreira S.T., Marzolo M.P., Bauer C., Thevenet A., Checler F. Alpha-secretase-derived fragment of cellular prion, N1, protects against monomeric and oligomeric amyloid beta (Abeta)-associated cell death. J.Biol. Chem. 2012, 287:5021-5032.
23. 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-E5.
24. Knopman D.S., Parisi J.E., Salviati A., Floriach-Robert M., Boeve B.F., Ivnik R.J., Smith G.E., Dickson D.W., Johnson K.A., Petersen L.E., McDonald W.C., Braak H., Petersen R.C. Neuropathology of cognitively normal elderly. J.Neuropathol. Exp. Neurol. 2003, 62:1087-1095.
25. Kudo W., Lee H.P., Zou W.Q., Wang X., Perry G., Zhu X., Smith M.A., Petersen R.B., Lee H.G. Cellular prion protein is essential for oligomeric amyloid-beta-induced neuronal cell death. Hum. Mol. Genet. 2012, 21:1138-1144.
26. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A 1998, 95:6448-6453.
27. 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.
28. Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. Aspecific amyloid-beta protein assembly in the brain impairs memory. Nature 2006, 440:352-357.
29. Liang J., Kong Q. alpha-Cleavage of cellular prion protein. Prion 2012, 6:453-460.
30. Mange A., Beranger F., Peoc'h K., Onodera T., Frobert Y., Lehmann S. Alpha- and beta- cleavages of the amino-terminus of the cellular prion protein. Biol. Cell 2004, 96:125-132.
31. Masters C.L., Simms G., Weinman N.A., Multhaup G., McDonald B.L., Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A 1985, 82:4245-4249.
32. McDuff F.O., Naud J.F., Montagne M., Sauve S., Lavigne P. The Max homodimeric b-HLH-LZ significantly interferes with the specific heterodimerization between the c-Myc and Max b-HLH-LZ in absence of DNA: a quantitative analysis. J.Mol. Recognit. 2009, 22:261-269.
33. Mucke L., Selkoe D.J. Neurotoxicity of amyloid beta-protein: synaptic and network dysfunction. Cold Spring Harb. Perspect. Med. 2012, 2:a006338.
34. Nicoll A.J., Panico S., Freir D.B., Wright D., Terry C., Risse E., Herron C.E., O'Malley T., Wadsworth J.D., Farrow M.A., Walsh D.M., Saibil H.R., Collinge J. Amyloid-beta nanotubes are associated with prion protein-dependent synaptotoxicity. Nat. Commun. 2013, 4:2416.
35. Nieznanski K., Choi J.K., Chen S., Surewicz K., Surewicz W.K. Soluble prion protein inhibits amyloid-beta (Abeta) fibrillization and toxicity. J.Biol. Chem. 2012, 287:33104-33108.
36. Oliveira-Martins J.B., Yusa S., Calella A.M., Bridel C., Baumann F., Dametto P., Aguzzi A. Unexpected tolerance of alpha-cleavage of the prion protein to sequence variations. PLoS One 2010, 5:e9107.
37. Ostapchenko V.G., Beraldo F.H., Guimaraes A.L., Mishra S., Guzman M., Fan J., Martins V.R., Prado V.F., Prado M.A. Increased prion protein processing and expression of metabotropic glutamate receptor 1 in a mouse model of Alzheimer's disease. J.Neurochem 2013, 127:415-425.
38. Podlisny M.B., Ostaszewski B.L., Squazzo S.L., Koo E.H., Rydell R.E., Teplow D.B., Selkoe D.J. Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J.Biol. Chem. 1995, 270:9564-9570.
39. Privat N., Laffont-Proust I., Faucheux B.A., Sazdovitch V., Frobert Y., Laplanche J.L., Grassi J., Hauw J.J., Haik S. Human prion diseases: from antibody screening to a standardized fast immunodiagnosis using automation. Mod. Pathol. 2008, 21:140-149.
40. Resenberger U.K., Harmeier A., Woerner A.C., Goodman J.L., Muller V., Krishnan R., Vabulas R.M., Kretzschmar H.A., Lindquist S., Hartl F.U., Multhaup G., Winklhofer K.F., Tatzelt J. The cellular prion protein mediates neurotoxic signalling of beta-sheet-rich conformers independent of prion replication. EMBO J. 2011, 30:2057-2070.
41. Roostaee A., Cote S., Roucou X. Aggregation and amyloid fibril formation induced by chemical dimerization of recombinant prion protein in physiological-like conditions. J.Biol. Chem. 2009, 284:30907-30916.
42. Schmechel A., Zentgraf H., Scheuermann S., Fritz G., Pipkorn R., Reed J., Beyreuther K., Bayer T.A., Multhaup G. Alzheimer beta-amyloid homodimers facilitate A beta fibrillization and the generation of conformational antibodies. J.Biol. Chem. 2003, 278:35317-35324.
43. 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.
44. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
45. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 2008, 14:837-842.
46. Spencer D.M., Wandless T.J., Schreiber S.L., Crabtree G.R. Controlling signal transduction synthetic ligands. Science 1993, 262:1019-1024.
47. Stahl N., Baldwin M.A., Burlingame A.L., Prusiner S.B. Identification of glycoinositol phospholipid linked and truncated forms of the scrapie prion protein. Biochemistry 1990, 29:8879-8884.
48. Taylor D.R., Parkin E.T., Cocklin S.L., Ault J.R., Ashcroft A.E., Turner A.J., Hooper N.M. Role of ADAMs in the ectodomain shedding and conformational conversion of the prion protein. J.Biol. Chem. 2009, 284:22590-22600.
49. Um J.W., Kaufman A.C., Kostylev M., Heiss J.K., Stagi M., Takahashi H., Kerrisk M.E., Vortmeyer A., Wisniewski T., Koleske A.J., Gunther E.C., Nygaard H.B., Strittmatter S.M. Metabotropic glutamate receptor 5 is a coreceptor for Alzheimer abeta oligomer bound to cellular prion protein. Neuron. 2013, 79:887-902.
50. Um J.W., Nygaard H.B., Heiss J.K., Kostylev M.A., Stagi M., Vortmeyer A., Wisniewski T., Gunther E.C., Strittmatter S.M. Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat. Neurosci. 2012, 15:1227-1235.
51. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation invivo. Nature 2002, 416:535-539.
52. Whitehouse I.J., Jackson C., Turner A.J., Hooper N.M. Prion protein is reduced in aging and in sporadic but not in familial Alzheimer's disease. J.Alzheimers Dis. 2010, 22:1023-1031.
53. Whitehouse I.J., Miners J.S., Glennon E.B., Kehoe P.G., Love S., Kellett K.A., Hooper N.M. Prion protein is decreased in Alzheimer's brain and inversely correlates with BACE1 activity, amyloid-beta levels and Braak stage. PLoS One 2013, 8:e59554.
54. You H., Tsutsui S., Hameed S., Kannanayakal T.J., Chen L., Xia P., Engbers J.D., Lipton S.A., Stys P.K., Zamponi G.W. Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A 2012, 109:1737-1742.
55. Youmans K.L., Leung S., Zhang J., Maus E., Baysac K., Bu G., Vassar R., Yu C., LaDu M.J. Amyloid-beta42 alters apolipoprotein E solubility in brains of mice with five familial AD mutations. J.Neurosci. Methods 2011, 196:51-59.
56. Younan N.D., Sarell C.J., Davies P., Brown D.R., Viles J.H. The cellular prion protein traps Alzheimer's Abeta in an oligomeric form and disassembles amyloid fibers. FASEB J. 2013, 27:1847-1858.
57. Zahn R., Liu A., Luhrs T., Riek R., von Schroetter C., Lopez Garcia F., Billeter M., Calzolai L., Wider G., Wuthrich K. NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. U.S.A 2000, 97:145-150.
58. Zahn R., von Schroetter C., Wuthrich K. Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett. 1997, 417:400-404.
59. Zou W.Q., Xiao X., Yuan J., Puoti G., Fujioka H., Wang X., Richardson S., Zhou X., Zou R., Li S., Zhu X., McGeer P.L., McGeehan J., Kneale G., Rincon-Limas D.E., Fernandez-Funez P., Lee H.G., Smith M.A., Petersen R.B., Guo J.P. Amyloid-beta42 interacts mainly with insoluble prion protein in the Alzheimer brain. J.Biol. Chem. 2011, 286:15095-15105.