Peripheral administration of a humanized anti-PrP antibody blocks Alzheimer's disease Aβ synaptotoxicity

Journal of Neuroscience

Volumn 34, Issue 18, 2014, Pages 6140-6145

  Klyubin, Igor ^a   Nicoll, Andrew J ^b   Khalili Shirazi, Azadeh ^b   Farmer, Michael ^b   Canning, Stephanie ^b   Mably, Alexandra ^c   Linehan, Jacqueline ^b   Brown, Alexander ^d   Wakeling, Madeleine ^b   Brandner, Sebastian ^b   Walsh, Dominic M ^c   Rowan, Michael J ^a   Collinge, John ^b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Alzheimer's; Drug discovery; Immunotherapy; Long term potentiation; Prion

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN EXTRACT; PRION PROTEIN ANTIBODY; PRN 100; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY AFFINITY; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOLOGY; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; SYNAPTOTOXICITY; WESTERN BLOTTING;

ALZHEIMER'S; DRUG DISCOVERY; IMMUNOTHERAPY; LONG-TERM POTENTIATION; PRION;

AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, MONOCLONAL; BIOPHYSICS; CA1 REGION, HIPPOCAMPAL; DRUG ADMINISTRATION ROUTES; ELECTRIC STIMULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; LONG-TERM POTENTIATION; MALE; PEPTIDE FRAGMENTS; PRIONS; RATS; RATS, WISTAR; TEMPORAL LOBE;

EID: 84899637070     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3526-13.2014     Document Type: Article

References (28)

1. Angal S, King DJ, Bodmer MW, Turner A, Lawson AD, Roberts G, Pedley B, Adair JR (1993) A single amino-acid substitution abolishes the heterogeneity of chimeric mouse/human (Igg4) antibody. Mol Immunol 30: 105-108. CrossRef Medline
2. Antonyuk SV, Trevitt CR, Strange RW, Jackson GS, Sangar D, Batchelor M, Cooper S, Fraser C, Jones S, Georgiou T, Khalili-Shirazi A, Clarke AR, Hasnain SS, Collinge J (2009) Crystal structure of human prion protein bound to a therapeutic antibody. Proc Natl Acad Sci U S A 106:2554-2558. CrossRef Medline
3. Barry AE, Klyubin I, Mc Donald JM, Mably AJ, Farrell MA, Scott M, Walsh DM, Rowan MJ (2011) Alzheimer's disease brain-derived amyloid-β-mediated inhibition of LTP in vivo Is prevented by immunotargeting cellular prion protein. J Neurosci 31:7259-7263. CrossRef Medline
4. Bate C, Williams A (2011) Amyloid-β-induced synapse damage is mediated via cross-linkage of cellular prion proteins. J Biol Chem 286:37955-37963. CrossRef Medline
5. Béland M, Roucou X (2012) The prion protein unstructured N-terminal region is a broad-spectrum molecular sensor with diverse and contrasting potential functions. J Neurochem 120:853-868. CrossRef Medline
6. Benilova I, Karran E, De Strooper B (2012) The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 15:349-357. CrossRef Medline
7. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline
8. Chung E, Ji Y, Sun Y, Kascsak RJ, Kascsak RB, Mehta PD, Strittmatter SM, Wisniewski T (2010) Anti-PrP C monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neurosci 11:130. CrossRef Medline
9. Collinge J (2001) Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 24:519-550. CrossRef Medline
10. Freir DB, Nicoll AJ, Klyubin I, Panico S, Mc Donald JM, Risse E, Asante EA, Farrow MA, Sessions RB, Saibil HR, Clarke AR, Rowan MJ, Walsh DM, Collinge J (2011) Interaction between prion protein and toxic amyloid-β assemblies can be therapeutically targeted at multiple sites. Nat Commun 2:336. CrossRef Medline
11. Jackson GS, Hill AF, Joseph C, Hosszu L, Power A, Waltho JP, Clarke AR, Collinge J. (1999) Multiple folding pathways for heterologously expressed human prion protein. Biochim Biophys Acta 1431:1-13. CrossRef Medline
12. Jones PT, Dear PH, Foote J, Neuberger MS, Winter G (1986) Replacing the complementarity-determining regions in a human-antibody with those from a mouse. Nature 321:522-525. CrossRef Medline
13. Khalili-Shirazi A, Summers L, Linehan J, Mallinson G, Anstee D, Hawke S, Jackson GS, Collinge J (2005) PrP glycoforms are associated in a strainspecific ratio in native PrP Sc. J Gen Virol 86:2635-2644. CrossRef Medline
14. Klöhn PC, Farmer M, Linehan JM, O'Malley C, Fernandez de Marco M, Taylor W, Farrow M, Khalili-Shirazi A, Brandner S, Collinge J (2012) PrP antibodies do not trigger mouse hippocampal neuron apoptosis. Science 335:52. CrossRef Medline
15. Klyubin I, Betts V, Welzel AT, Blennow K, Zetterberg H, Wallin A, Lemere CA, Cullen WK, Peng Y, Wisniewski T, Selkoe DJ, Anwyl R, Walsh DM, Rowan MJ (2008) Amyloid-β protein dimer-containing human CSF disrupts synaptic plasticity: prevention by systemic passive immunization. J Neurosci 28:4231-4237. CrossRef Medline
16. Kozler P, Pokorný J (2003) Altered blood-brain barrier permeability and its effect on the distribution of Evans blue and sodium fluorescein in the rat brain applied by intracarotid injection. Physiol Res 52:607-614. Medline
17. Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers. Nature 457:1128-1132. CrossRef Medline
18. Linden R, Martins VR, Prado MA, Cammarota M, Izquierdo I, Brentani RR (2008) Physiology of the prion protein. Physiol Rev 88:673-728. CrossRef Medline
19. Nicoll AJ, Collinge J (2009) Preventing prion pathogenicity by targeting the cellular prion protein. Infect Disord Drug Targets 9:48-57. CrossRef Medline
20. Ohsawa N, Song CH, Suzuki A, Furuoka H, Hasebe R, Horiuchi M (2013) Therapeutic effect of peripheral administration of an anti-prion protein antibody on mice infected with prions. Microbiol Immunol 57:288-297. CrossRef Medline
21. Polymenidou M, Moos R, Scott M, Sigurdson C, Shi YZ, Yajima B, Hafner-Bratkovic I, Jerala R, Hornemann S, Wuthrich K, Bellon A, Vey M, Garen G, James MN, Kav N, Aguzzi A (2008) The POM monoclonals: A comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS One 3:e3872. CrossRef Medline
22. Roettger Y, Du Y, Bacher M, Zerr I, Dodel R, Bach JP (2013) Immunotherapy in prion disease. Nat Rev Neurol 9:98-105. CrossRef Medline
23. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-842. CrossRef Medline
24. Solforosi L, Criado JR, McGavern DB, Wirz S, Sánchez-Alavez M, Sugama S, DeGiorgio LA, Volpe BT, Wiseman E, Abalos G, Masliah E, Gilden D, Oldstone MB, Conti B, Williamson RA (2004) Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303:1514-1516. CrossRef Medline
25. Sonati T, Reimann RR, Falsig J, Baral PK, O'Connor T, Hornemann S, Yaganoglu S, Li B, Herrmann US, Wieland B, Swayampakula M, Rahman MH, Das D, Kav N, Riek R, Liberski PP, James MN, AguzziA (2013) The toxicity of antiprion antibodies is mediated by the flexible tail of the prion protein. Nature 501:102-106. CrossRef Medline
26. White AR, Enever P, Tayebi M, Mushens R, Linehan J, Brandner S, Anstee D, Collinge J, Hawke S (2003) Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature 422:80-83. CrossRef Medline
27. Williams DG, Matthews DJ, Jones T (2010) Humanising antibodies byCDR grafting. In: Antibody engineering (Roland Kontermann SD, ed), pp 319-339. Berlin: Springer-Verlag.
28. Zahn R, von Schroetter C, Wüthrich K (1997) Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett 417:400-404. CrossRef Medline