The cellular prion protein mediates neurotoxic signalling of Î 2-sheet-rich conformers independent of prion replication

EMBO Journal

Volumn 30, Issue 10, 2011, Pages 2057-2070

  Resenberger, Ulrike K ^a   Harmeier, Anja ^b   Woerner, Andreas C ^c   Goodman, Jessica L ^d   Müller, Veronika ^a   Krishnan, Rajaraman ^d   Vabulas, R Martin ^c   Kretzschmar, Hans A ^a   Lindquist, Susan ^d   Hartl, F Ulrich ^c   Multhaup, Gerd ^b   Winklhofer, Konstanze F ^a   Tatzelt, Jörg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Alzheimer; intrinsically disordered; NMDA receptor; oligomer; prion

Indexed keywords

AMYLOID BETA PROTEIN; CELL PROTEIN; CELLULAR PRION PROTEIN; FUNGAL PROTEIN; PRION PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; DEGENERATIVE DISEASE; HUMAN; NEUROLOGIC DISEASE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

AMYLOID BETA-PEPTIDES; CELL DEATH; HUMANS; MEMBRANE PROTEINS; NEURONS; PRION DISEASES; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; PRPC PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS;

SCRAPIE PRION;

EID: 79956110918     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.86     Document Type: Article

References (59)

1. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y, Marino S, Weissmann C, Aguzzi A (1996) Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379: 339-343 (Pubitemid 26033075)
2. Büeler H, Aguzzi A, Sailer A, Greiner R-A, Autenried P, Aguet M, Weissmann C (1993) Mice devoid of PrP are resistant to scrapie. Cell 73: 1339-1347 (Pubitemid 23201147)
3. Büeler H, Fischer M, Lang Y, Bluethmann H, Lipp H-P, DeArmond SJ, Prusiner SB, Aguet M, Weissmann C (1992) Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356: 577-582
4. Caughey B, Baron GS (2006) Prions and their partners in crime. Nature 443: 803-810 (Pubitemid 44622685)
5. Chesebro B (2003) Introduction to the transmissible spongiform encephalopathies or prion diseases. Br Med Bull 66: 1-20 (Pubitemid 37173488)
6. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S, Caughey B, Masliah E, Oldstone M (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308: 1435-1439 (Pubitemid 40791292)
7. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84 (Pubitemid 41236735)
8. Collinge J (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 24: 519-550 (Pubitemid 32695238)
9. Collinge J, Clarke AR (2007) A general model of prion strains and their pathogenicity. Science 318: 930-936 (Pubitemid 350098981)
10. De Strooper B (2010) Proteases and proteolysis in Alzheimer disease: a multifactorial view on the disease process. Physiol Rev 90: 465-494
11. Ertmer A, Gilch S, Yun SW, Flechsig E, Klebl B, Stein-Gerlach M, Klein MA, Schatzl HM (2004) The tyrosine kinase inhibitor STI571 induces cellular clearance of PrPSc in prion-infected cells. J Biol Chem 279: 41918-41927 (Pubitemid 39313641)
12. Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Lauren J, Gimbel ZA, Strittmatter SM (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 30: 6367-6374
13. Glover JR, Kowal AS, Schirmer EC, Patino MM, Liu JJ, Lindquist S (1997) Self-seeded fibers formed by Sup35, the protein determinant of [PSI+], a heritable prion-like factor of S. cerevisiae. Cell 89: 811-819 (Pubitemid 27516184)
14. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurode-generation: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8: 101-112 (Pubitemid 46432529)
15. Harmeier A, Wozny C, Rost BR, Munter LM, Hua H, Georgiev O, Beyermann M, Hildebrand PW, Weise C, Schaffner W, Schmitz D, Multhaup G (2009) Role of amyloid-beta glycine 33 in oligomer-ization, toxicity, and neuronal plasticity. J Neurosci 29: 7582-7590
16. Heske J, Heller U, Winklhofer KF, Tatzelt J (2004) The C-terminal domain of the prion protein is necessary and sufficient for import into the endoplasmic reticulum. J Biol Chem 279: 5435-5443 (Pubitemid 38220567)
17. Ilieva H, Polymenidou M, Cleveland DW (2009) Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 187: 761-772
18. Kascsak RJ, Rubenstein R, Merz PA, Tonna-DeMasi M, Fersko R, Carp RI, Wisniewski HM, Diringer H (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61 : 3688-3693 (Pubitemid 18011463)
19. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489 (Pubitemid 36444329)
20. Khosravani H, Zhang Y, Tsutsui S, Hameed S, Altier C, Hamid J, Chen L, Villemaire M, Ali Z, Jirik FR, Zamponi GW (2008) Prion protein attenuates excitotoxicity by inhibiting NMDA receptors. J Cell Biol 181: 551-565
21. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, Lambert MP, Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 24: 10191-10200 (Pubitemid 39492046)
22. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95: 6448-6453
23. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457: 1128-1132
24. Li L, Lindquist S (2000) Creating a protein-based element of inheritance. Science 287: 661-664 (Pubitemid 30070915)
25. Mallucci G, Dickinson A, Linehan J, Klohn PC, Brandner S, Collinge J (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302: 871-874 (Pubitemid 37339628)
26. McLennan NF, Brennan PM, McNeill A, Davies I, Fotheringham A, Rennison KA, Ritchie D, Brannan F, Head MW, Ironside JW, Williams A, Bell JE (2004) Prion protein accumulation and neuroprotection in hypoxic brain damage. Am J Pathol 165: 227-235 (Pubitemid 38821830)
27. Miesbauer M, Pfeiffer NV, Rambold AS, Muller V, Kiachopoulos S, Winklhofer KF, Tatzelt J (2009) Alpha-helical domains promote translocation of intrinsically disordered polypeptides into the endoplasmic reticulum. J Biol Chem 284: 24384-24393
28. Mitteregger G, Vosko M, Krebs B, Xiang W, Kohlmannsperger V, Nolting S, Hamann GF, Kretzschmar HA (2007) The role of the octarepeat region in neuroprotective function of the cellular prion protein. Brain Pathol 17: 174-183 (Pubitemid 46466137)
29. Moore RA, Vorberg I, Priola SA (2005) Species barriers in prion diseases-brief review. Arch Virol Suppl 187-202
30. Muller WE, Ushijima H, Schroder HC, Forrest JM, Schatton WF, Rytik PG, Heffner-Lauc M (1993) Cytoprotective effect of NMDA receptor antagonists on prion protein (PrionSc)-induced toxicity in rat cortical cell cultures. Eur J Pharmacol 246: 261-267 (Pubitemid 23253684)
31. Munter LM, Botev A, Richter L, Hildebrand PW, Althoff V, Weise C, Kaden D, Multhaup G (2010) Aberrant amyloid precursor protein (APP) processing in hereditary forms of Alzheimer disease caused by APP familial Alzheimer disease mutations can be rescued by mutations in the APP GxxxG motif. J Biol Chem 285: 21636-21643
32. Munter LM, Voigt P, Harmeier A, Kaden D, Gottschalk KE, Weise C, Pipkorn R, Schaefer M, Langosch D, Multhaup G (2007) GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Abeta42. EMBO J 26: 1702-1712 (Pubitemid 46480941)
33. Ondrejcak T, Klyubin I, Hu NW, Barry AE, Cullen WK, Rowan MJ (2010) Alzheimer's disease amyloid beta-protein and synaptic function. Neuromolecular Med 12: 13-26
34. Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 13: 812-818
35. Podlisny MB, Ostaszewski BL, Squazzo SL, Koo EH, Rydell RE, Teplow DB, Selkoe DJ (1995) Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J Biol Chem 270: 9564-9570
36. Prusiner SB, Scott M, Foster D, Pan K-M, Groth D, Mirenda C, Torchia M, Yang S-L, Serban D, Carlson GA, Hoppe PC, Westaway D, DeArmond SJ (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63: 673-686 (Pubitemid 120035041)
37. Prusiner SB, Scott MR, DeArmond SJ, Cohen FE (1998) Prion protein biology. Cell 93: 337-348 (Pubitemid 28232079)
38. Rambold AS, Müller V, Ron U, Ben-Tal N, Winklhofer KF, Tatzelt J (2008) Stress-protective activity of prion protein is corrupted by scrapie-prions. EMBO J 27: 1974-1984
39. Scheibel T, Kowal AS, Bloom JD, Lindquist SL (2001) Bidirectional amyloid fiber growth for a yeast prion determinant. Curr Biol 11 : 366-369 (Pubitemid 32200741)
40. Scott M, Foster D, Mirenda C, Serban D, Coufal F, Walchli M, Torchia M, Groth D, Carlson G, DeArmond SJ, Westaway D, Prusiner SB (1989) Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 59: 847-857 (Pubitemid 20022375)
41. Scott MR, Safar J, Telling G, Nguyen O, Groth D, Torchia M, Koehler R, Tremblay P, Walther D, Cohen FE, DeArmond SJ, Prusiner SB (1997) Identification of a prion protein epitope modulating transmission of bovine spongiform encepha-lopathy prions to transgenic mice. Proc Natl Acad Sci USA 94: 14279-14284 (Pubitemid 28041364)
42. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27: 2866-2875 (Pubitemid 46438992)
43. Shirotani K, Tomioka M, Kremmer E, Haass C, Steiner H (2007) Pathological activity of familial Alzheimer's disease-associated mutant presenilin can be executed by six different gamma-secretase complexes. Neurobiol Dis 27: 102-107 (Pubitemid 46921480)
44. Shorter J, Lindquist S (2005) Prions as adaptive conduits of memory and inheritance. Nat Rev Genet 6: 435-450 (Pubitemid 40733889)
45. Shyu WC, Lin SZ, Chiang MF, Ding DC, Li KW, Chen SF, Yang HI, Li H (2005) Overexpression of PrPC by adenovirus-mediated gene targeting reduces ischemic injury in a stroke rat model. J Neurosci 25: 8967-8977 (Pubitemid 41384465)
46. Spudich A, Frigg R, Kilic E, Kilic U, Oesch B, Raeber A, Bassetti CL, Hermann DM (2005) Aggravation of ischemic brain injury by prion protein deficiency: role of ERK-1/-2 and STAT-1. Neurobiol Dis 20: 442-449 (Pubitemid 41476270)
47. Tatzelt J, Prusiner SB, Welch WJ (1996) Chemical chaperones interfere with the formation of scrapie prion protein. EMBO J 15: 6363-6373 (Pubitemid 26413769)
48. Tompa P, Fuxreiter M, Oldfield CJ, Simon I, Dunker AK, Uversky VN (2009) Close encounters of the third kind: disordered domains and the interactions of proteins. Bioessays 31: 328-335
49. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid b protein potently inhibit hippocampal long-term poten-tiation in vivo. Nature 416: 535-539 (Pubitemid 34288854)
50. Wei Y, Liu T, Sazinsky SL, Moffet DA, Pelczer I, Hecht MH (2003) Stably folded de novo proteins from a designed combinatorial library. Protein Sci 12: 92-102 (Pubitemid 36020138)
51. Weise J, Sandau R, Schwarting S, Crome O, Wrede A, Schulz-Schaeffer W, Zerr I, Bahr M (2006) Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury. Stroke 37: 1296-1300 (Pubitemid 43731879)
52. Weissmann C, Fischer M, Raeber A, Büeler H, Sailer A, Shmerling D, Rülicke T, Brandner S, Aguzzi A (1996) The role of PrP in pathogenesis of experimental scrapie. Cold Spring Harb Symp Quant Biol 61: 511-522 (Pubitemid 27257997)
53. West MW, Wang W, Patterson J, Mancias JD, Beasley JR, Hecht MH (1999) De novo amyloid proteins from designed combinatorial libraries. Proc Natl Acad Sci USA 96: 11211-11216 (Pubitemid 29487360)
54. Wickner RB (1994) [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae [see comments]. Science 264: 566-569 (Pubitemid 24185861)
55. Winklhofer KF, Heller U, Reintjes A, Tatzelt J (2003a) Inhibition of complex glycosylation increases formation of PrPSc. Traffic 4: 313-322 (Pubitemid 36582633)
56. Winklhofer KF, Heske J, Heller U, Reintjes A, Muranji W, Moarefi I, Tatzelt J (2003b) Determinants of the in vivo-folding of the prion protein: a bipartite function of helix 1 in folding and aggregation. J Biol Chem 278: 14961-14970 (Pubitemid 36799827)
57. Winklhofer KF, Tatzelt J (2000) Cationic lipopolyamines induce degradation of PrPSc in scrapie-infected mouse neuroblastoma cells. Biol Chem 381: 463-469 (Pubitemid 30453825)
58. Winklhofer KF, Tatzelt J, Haass C (2008) The two faces of protein misfolding: gain and loss of function in neurodegenerative diseases. EMBO J 27: 336-349 (Pubitemid 351161650)
59. Yamasaki A, Eimer S, Okochi M, Smialowska A, Kaether C, Baumeister R, Haass C, Steiner H (2006) The GxGD motif of presenilin contributes to catalytic function and substrate identification of gamma-secretase. J Neurosci 26: 3821-3828