N-Terminal pyroglutamate formation of Aβ38 and Aβ40 enforces oligomer formation and potency to disrupt hippocampal long-term potentiation

Journal of Neurochemistry

Volumn 121, Issue 5, 2012, Pages 774-784

  Schlenzig, Dagmar ^a   Rönicke, Raik ^b   Cynis, Holger ^a   Ludwig, Hans Henning ^a   Scheel, Eike ^a   Reymann, Klaus ^b   Saido, Takaomi ^c   Hause, Gerd ^d   Schilling, Stephan ^a   Demuth, Hans Ulrich ^a  

^a PROBIODRUG AG   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

A ; ABri; ADan; Alzheimer's disease; amyloid; pyroglutamate

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN 37; AMYLOID BETA PROTEIN 38; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; OLIGOMER; PYROGLUTAMIC ACID; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; AMYLOIDOSIS; CONTROLLED STUDY; CROSS LINKING; HIPPOCAMPUS; HUMAN; HUMAN CELL; HYDROPHOBICITY; IN VITRO STUDY; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROPATHOLOGY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN SECRETION; REVIEW;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HEK293 CELLS; HIPPOCAMPUS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE FRAGMENTS; PYRROLIDONECARBOXYLIC ACID;

EID: 84860519322     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07707.x     Document Type: Review

References (37)

1. Alexandru A., Jagla W., Graubner S., et al. (2011) Neurotoxicity and lethal phenotype of pE3-Aβ expression in a transgenic mouse model-pE3-Aβ formation and neuronal loss in TBA2.1 mice. J. Neurosci. 31, 12790-12801.
2. Bitan G., Kirkitadze M. D., Lomakin A., Vollers S. S., Benedek G. B., and, Teplow D. B., (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc. Natl Acad. Sci. USA 100, 330-335. (Pubitemid 36078074)
3. Bolognesi B., Kumita J. R., Barros T. P., Esbjorner E. K., Luheshi L. M., Crowther D. C., Wilson M. R., Dobson C. M., Favrin G., and, Yerbury J. J., (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem. Biol. 5, 735-740.
4. Campioni S., Mannini B., Zampagni M., et al. (2010) A causative link between the structure of aberrant protein oligomers and their toxicity. Nat. Chem. Biol. 6, 140-147.
5. Cardamone M., and, Puri N. K., (1992) Spectrofluorimetric assessment of the surface hydrophobicity of proteins. Biochem. J., 282 (Pt 2), 589-593.
6. Cleary J. P., Walsh D. M., Hofmeister J. J., Shankar G. M., Kuskowski M. A., Selkoe D. J., and, Ashe K. H., (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 8, 79-84. (Pubitemid 41236735)
7. Cynis H., Scheel E., Saido T. C., Schilling S., and, Demuth H. U., (2008) Amyloidogenic processing of amyloid precursor protein: evidence of a pivotal role of glutaminyl cyclase in generation of pyroglutamate-modified amyloid-beta. Biochemistry 47, 7405-7413. (Pubitemid 351991019)
8. D'Arrigo C., Tabaton M., and, Perico A., (2009) N-terminal truncated pyroglutamyl beta amyloid peptide Abetapy3-42 shows a faster aggregation kinetics than the full-length Abeta1-42. Biopolymers 91, 861-873.
9. Ellis K. J., and, Morrison J. F., (1982) Buffers of constant ionic strength for studying pH-dependent processes. Methods Enzymol. 87, 405-426.
10. Ghiso J., Revesz T., Holton J., et al. (2001) Chromosome 13 dementia syndromes as models of neurodegeneration. Amyloid 8, 277-284. (Pubitemid 34042998)
11. Güntert A., Dobeli H., and, Bohrmann B., (2006) High sensitivity analysis of amyloid-beta peptide composition in amyloid deposits from human and PS2APP mouse brain. Neuroscience 143, 461-475. (Pubitemid 44716598)
12. He W., and, Barrow C. J., (1999) The A beta 3-pyroglutamyl and 11-pyroglutamyl peptides found in senile plaque have greater beta-sheet forming and aggregation propensities in vitro than full-length A beta. Biochemistry 38, 10871-10877.
13. Hsieh H., Boehm J., Sato C., Iwatsubo T., Tomita T., Sisodia S., and, Malinow R., (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831-843. (Pubitemid 44828454)
14. Irie K., Murakami K., Masuda Y., Morimoto A., Ohigashi H., Ohashi R., Takegoshi K., Nagao M., Shimizu T., and, Shirasawa T., (2005) Structure of beta-amyloid fibrils and its relevance to their neurotoxicity: implications for the pathogenesis of Alzheimer's disease. J. Biosci. Bioeng. 99, 437-447. (Pubitemid 40874521)
15. Iwatsubo T., Odaka A., Suzuki N., Mizusawa H., Nukina N., and, Ihara Y., (1994) Visualization of A beta 42(43) and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42(43). Neuron, 13, 45-53.
16. Jarrett J. T., Berger E. P., and, Lansbury Jr P. T., (1993) The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32, 4693-4697. (Pubitemid 23162022)
17. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W., and, Glabe C. G., (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489. (Pubitemid 36444329)
18. Klafki H. W., Wiltfang J., and, Staufenbiel M., (1996) Electrophoretic separation of betaA4 peptides (1-40) and (1-42). Anal. Biochem. 237, 24-29. (Pubitemid 26155625)
19. Lambert M. P., Barlow A. K., Chromy B. A., et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453.
20. Lemere C. A., Blusztajn J. K., Yamaguchi H., Wisniewski T., Saido T. C., and, Selkoe D. J., (1996) Sequence of deposition of heterogeneous amyloid beta-peptides and APO E in Down syndrome: implications for initial events in amyloid plaque formation. Neurobiol. Dis. 3, 16-32.
21. Lesne S., Koh M. T., Kotilinek L., Kayed R., Glabe C. G., Yang A., Gallagher M., and, Ashe K. H., (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357.
22. Miravalle L., Calero M., Takao M., Roher A. E., Ghetti B., and, Vidal R., (2005) Amino-terminally truncated Abeta peptide species are the main component of cotton wool plaques. Biochemistry 44, 10810-10821. (Pubitemid 41153641)
23. Murakami K., Irie K., Morimoto A., Ohigashi H., Shindo M., Nagao M., Shimizu T., and, Shirasawa T., (2003) Neurotoxicity and physicochemical properties of Abeta mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer's disease. J. Biol. Chem. 278, 46179-46187. (Pubitemid 37432769)
24. Nimmrich V., Grimm C., Draguhn A., Barghorn S., Lehmann A., Schoemaker H., Hillen H., Gross G., Ebert U., and, Bruehl C., (2008) Amyloid beta oligomers (A beta(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J. Neurosci. 28, 788-797. (Pubitemid 351159014)
25. Piccini A., Russo C., Gliozzi A., et al. (2005) {beta}-amyloid is different in normal aging and in Alzheimer disease. J. Biol. Chem. 280, 34186-34192. (Pubitemid 41443143)
26. Rönicke R., Schroder U. H., Bohm K., and, Reymann K. G., (2009) The Na+/H+ exchanger modulates long-term potentiation in rat hippocampal slices. Naunyn. Schmiedebergs. Arch. Pharmacol. 379, 233-239.
27. Rönicke R., Mikhaylova M., Ronicke S., Meinhardt J., Schroder U. H., Fandrich M., Reiser G., Kreutz M. R., and, Reymann K. G., (2011) Early neuronal dysfunction by amyloid beta oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol. Aging 32, 2219-2228.
28. Russo C., Schettini G., Saido T. C., Hulette C., Lippa C., Lannfelt L., Ghetti B., Gambetti P., Tabaton M., and, Teller J. K., (2000) Presenilin-1 mutations in Alzheimer's disease. Nature 405, 531-532. (Pubitemid 30367716)
29. Schilling S., Lauber T., Schaupp M., Manhart S., Scheel E., Bohm G., and, Demuth H. U., (2006) On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45, 12393-12399. (Pubitemid 44583682)
30. Schilling S., Zeitschel U., Hoffmann T., et al. (2008) Glutaminyl cyclase inhibition attenuates pyroglutamate Abeta and Alzheimer's disease-like pathology. Nat. Med. 14, 1106-1111.
31. Schlenzig D., Manhart S., Cinar Y., Kleinschmidt M., Hause G., Willbold D., Funke S. A., Schilling S., and, Demuth H. U., (2009) Pyroglutamate formation influences solubility and amyloidogenicity of amyloid peptides. Biochemistry 48, 7072-7078.
32. Shankar G. M., Li S., Mehta T. H., et al. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842.
33. Shirotani K., Tsubuki S., Lee H. J., Maruyama K., and, Saido T. C., (2002) Generation of amyloid beta peptide with pyroglutamate at position 3 in primary cortical neurons. Neurosci. Lett. 327, 25-28. (Pubitemid 34722435)
34. Townsend M., Shankar G. M., Mehta T., Walsh D. M., and, Selkoe D. J., (2006) Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J. Physiol. 572, 477-492.
35. Walsh D. M., and, Selkoe D. J., (2004) Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44, 181-193. (Pubitemid 39348839)
36. Walsh D. M., Hartley D. M., Condron M. M., Selkoe D. J., and, Teplow D. B., (2001) In vitro studies of amyloid beta-protein fibril assembly and toxicity provide clues to the aetiology of Flemish variant (Ala692 - >Gly) Alzheimer's disease. Biochem. J. 355, 869-877. (Pubitemid 32434107)
37. Walsh D. M., Townsend M., Podlisny M. B., Shankar G. M., Fadeeva J. V., Agnaf O. E., Hartley D. M., and, Selkoe D. J., (2005) Certain inhibitors of synthetic amyloid beta-peptide (Abeta) fibrillogenesis block oligomerization of natural Abeta and thereby rescue long-term potentiation. J. Neurosci. 25, 2455-2462. (Pubitemid 40365155)