Oral treatment with the d-enantiomeric peptide D3 improves the pathology and behavior of alzheimer's disease transgenic mice

ACS Chemical Neuroscience

Volumn 1, Issue 9, 2010, Pages 639-648

  Aileen Funke, Susanne ^a   Van Groen, Thomas ^b,c   Kadish, Inga ^b,c   Bartnik, Dirk ^d   Nagel Steger, Luitgard ^d   Brener, Oleksandr ^d   Sehl, Torsten ^d   Batra Safferling, Renu ^a   Moriscot, Christine ^e,f,g,h   Schoehn, Guy ^e,f,g,h   Horn, Anselm H C ⁱ   Müller Schiffmann, Andreas ^d   Korth, Carsten ^d   Sticht, Heinrich ⁱ   Willbold, Dieter ^a,d,e  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

^d HEINRICH HEINE UNIVERSITY   (Germany)

^e DIF   (France)

^f CNRS   (France)

^g UNIV GRENOBLE ALPES   (France)

^h Unit of Virus Host Cell Interactions   (France)

ⁱ UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Alzheimer's disease; D enantiomeric peptide; drugs; Mirror image phage display; oligomers

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; ARGINYLPROLYLARGINYLTHREONYLARGINYLLEUCYLHISTIDYLTHREONYLHISTIDYLARGINYLASPARAGINYLARGININE; NOOTROPIC AGENT; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; DISEASE COURSE; DRUG ACTIVITY; DRUG MECHANISM; ENANTIOMER; FEMALE; MOUSE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL;

ALZHEIMER'S DISEASE; D-ENANTIOMERIC PEPTIDE; DRUGS; MIRROR IMAGE PHAGE DISPLAY; OLIGOMERS;

ADMINISTRATION, ORAL; ALZHEIMER DISEASE; ANIMALS; COGNITION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MAZE LEARNING; MICE; MICE, TRANSGENIC; OLIGOPEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STEREOISOMERISM; TREATMENT OUTCOME;

MUS MUSCULUS;

EID: 77956686266     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn100057j     Document Type: Article

References (50)

1. Brookmeyer, R., Johnson, E., Ziegler-Graham, K., and Arrighi, H. M. (2007) Forecasting the global burden of Alzheimer's disease Alzheimer's Dementia 3, 186-191
2. Haass, C. and Selkoe, D. J. (1993) Cellular processing of beta-amyloid precursor protein and the genesis of amyloid beta-peptide Cell 75, 1039-1042
3. Kang, J., Lemaire, H. G., Unterbeck, A., Salbaum, J. M., Masters, C. L., Grzeschik, K. H., Multhaup, G., Beyreuther, K., and Muller-Hill, B. (1987) The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor Nature 325, 733-736
4. Weidemann, A., Konig, G., Bunke, D., Fischer, P., Salbaum, J. M., Masters, C. L., and Beyreuther, K. (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein Cell 57, 115-126
5. Hardy, J. A. and Higgins, G. A. (1992) Alzheimer's disease: the amyloid cascade hypothesis Science 256, 184-185
6. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease Neuron 6, 487-498
7. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112
8. 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., and Klein, W. L. (1998) Diffusible, nonfibrillar ligands derived from Abeta1?42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
9. Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., and Sabatini, B. L. (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
10. Walsh, D. M. and Selkoe, D. J. (2007) A beta oligomers: a decade of discovery J. Neurochem. 101, 1172-1184
11. Blennow, K., de Leon, M. J., and Zetterberg, H. (2006) Alzheimer's disease Lancet 368, 387-403
12. Roberson, E. D. and Mucke, L. (2006) 100 years and counting: prospects for defeating Alzheimer's disease Science 314, 781-784
13. Jakob-Roetne, R. and Jacobsen, H. (2009) Alzheimer's disease: from pathology to therapeutic approaches Angew. Chem., Int. Ed. 48, 3030-3059
14. Nerelius, C., Johansson, J., and Sandegren, A. (2009) Amyloid beta-peptide aggregation. What does it result in and how can it be prevented? Front. Biosci. 14, 1716-1729
15. Podlisny, M. B., Walsh, D. M., Amarante, P., Ostaszewski, B. L., Stimson, E. R., Maggio, J. E., Teplow, D. B., and Selkoe, D. J. (1998) Oligomerization of endogenous and synthetic amyloid beta-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red Biochemistry 37, 3602-3611
16. McLaurin, J., Golomb, R., Jurewicz, A., Antel, J. P., and Fraser, P. E. (2000) Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid beta peptide and inhibit abeta -induced toxicity J. Biol. Chem. 275, 18495-18502
17. Townsend, M., Cleary, J. P., Mehta, T., Hofmeister, J., Lesne, S., O'Hare, E., Walsh, D. M., and Selkoe, D. J. (2006) Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers Ann. Neurol. 60, 668-676
18. Gervais, F., Paquette, J., Morissette, C., Krzywkowski, P., Yu, M., Azzi, M., Lacombe, D., Kong, X., Aman, A., Laurin, J., Szarek, W. A., and Tremblay, P. (2007) Targeting soluble Abeta peptide with Tramiprosate for the treatment of brain amyloidosis Neurobiol. Aging 28, 537-547
19. Cherny, R. A., Atwood, C. S., Xilinas, M. E., Gray, D. N., Jones, W. D., McLean, C. A., Barnham, K. J., Volitakis, I., Fraser, F. W., Kim, Y., Huang, X., Goldstein, L. E., Moir, R. D., Lim, J. T., Beyreuther, K., Zheng, H., Tanzi, R. E., Masters, C. L., and Bush, A. I. (2001) Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice Neuron 30, 665-676
20. Price, K. A., Crouch, P. J., and White, A. R. (2007) Therapeutic treatment of Alzheimer's disease using metal complexing agents Recent Pat. CNS Drug Discovery 2, 180-187
21. Necula, M., Breydo, L., Milton, S., Kayed, R., van der Veer, W. E., Tone, P., and Glabe, C. G. (2007) Methylene blue inhibits amyloid Abeta oligomerization by promoting fibrillization Biochemistry 46, 8850-8860
22. Bieschke, J., Russ, J., Friedrich, R. P., Ehrnhoefer, D. E., Wobst, H., Neugebauer, K., and Wanker, E. E. EGCG remodels mature {alpha}-synuclein and amyloid-{beta} fibrils and reduces cellular toxicity, Proc. Natl. Acad. Sci. U.S.A.
23. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., Engemann, S., Pastore, A., and Wanker, E. E. (2008) EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers Nat. Struct. Mol. Biol. 15, 558-566
24. Nagel-Steger, L., Demeler, B., Meyer-Zaika, W., Hochdorffer, K., Schrader, T., and Willbold, D. (2010) Modulation of aggregate size- and shape-distributions of the amyloid-beta peptide by a designed beta-sheet breaker Eur. Biophys. J. 39, 15-22
25. Rzepecki, P., Nagel-Steger, L., Feuerstein, S., Linne, U., Molt, O., Zadmard, R., Aschermann, K., Wehner, M., Schrader, T., and Riesner, D. (2004) Prevention of Alzheimer's disease-associated Abeta aggregation by rationally designed nonpeptidic beta-sheet ligands J. Biol. Chem. 279, 47497-47505
26. Juhasz, G., Marki, A., Vass, G., Fulop, L., Budai, D., Penke, B., Falkay, G., and Szegedi, V. (2009) An intraperitoneally administered pentapeptide protects against Abeta (1?42) induced neuronal excitation in vivo J. Alzheimer's Dis. 16, 189-196
27. Poduslo, J. F., Curran, G. L., Kumar, A., Frangione, B., and Soto, C. (1999) Beta-sheet breaker peptide inhibitor of Alzheimer's amyloidogenesis with increased blood-brain barrier permeability and resistance to proteolytic degradation in plasma J. Neurobiol. 39, 371-382
28. Soto, C., Sigurdsson, E. M., Morelli, L., Kumar, R. A., Castano, E. M., and Frangione, B. (1998) Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy Nat. Med. 4, 822-826
29. Tjernberg, L. O., Naslund, J., Lindqvist, F., Johansson, J., Karlstrom, A. R., Thyberg, J., Terenius, L., and Nordstedt, C. (1996) Arrest of beta-amyloid fibril formation by a pentapeptide ligand J. Biol. Chem. 271, 8545-8548
30. Frydman-Marom, A., Rechter, M., Shefler, I., Bram, Y., Shalev, D. E., and Gazit, E. (2009) Cognitive-performance recovery of Alzheimer's disease model mice by modulation of early soluble amyloidal assemblies Angew. Chem., Int. Ed. 48, 1981-1986
31. van Groen, T., Kadish, I., Wiesehan, K., Funke, S. A., and Willbold, D. (2009) In vitro and in vivo staining characteristics of small, fluorescent, Abeta42-binding D-enantiomeric peptides in transgenic AD mouse models ChemMedChem 4, 276-282
32. van Groen, T., Wiesehan, K., Funke, S. A., Kadish, I., Nagel-Steger, L., and Willbold, D. (2008) Reduction of Alzheimer's disease amyloid plaque load in transgenic mice by D3, a D-enantiomeric peptide identified by mirror image phage display ChemMedChem 3, 1848-1852
33. Wiesehan, K., Buder, K., Linke, R. P., Patt, S., Stoldt, M., Unger, E., Schmitt, B., Bucci, E., and Willbold, D. (2003) Selection of D-amino-acid peptides that bind to Alzheimer's disease amyloid peptide abeta1?42 by mirror image phage display ChemBioChem 4, 748-753
34. Wiesehan, K., Stohr, J., Nagel-Steger, L., van Groen, T., Riesner, D., and Willbold, D. (2008) Inhibition of cytotoxicity and amyloid fibril formation by a D-amino acid peptide that specifically binds to Alzheimer's disease amyloid peptide Protein Eng., Des. Sel. 21, 241-246
35. Schumacher, T. N., Mayr, L. M., Minor, D. L., Jr., Milhollen, M. A., Burgess, M. W., and Kim, P. S. (1996) Identification of d -peptide ligands through mirror-image phage display Science 271, 1854-1857
36. Van Regenmortel, M. H. and Muller, S. (1998) d -peptides as immunogens and diagnostic reagents Curr. Opin. Biotechnol. 9, 377-382
37. Jankowsky, J. L., Slunt, H. H., Ratovitski, T., Jenkins, N. A., Copeland, N. G., and Borchelt, D. R. (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies Biomol. Eng. 17, 157-165
38. Lafaye, P., Achour, I., England, P., Duyckaerts, C., and Rougeon, F. (2009) Single-domain antibodies recognize selectively small oligomeric forms of amyloid beta, prevent Abeta-induced neurotoxicity and inhibit fibril formation Mol. Immunol. 46, 695-704
39. Eisele, Y. S., Bolmont, T., Heikenwalder, M., Langer, F., Jacobson, L. H., Yan, Z. X., Roth, K., Aguzzi, A., Staufenbiel, M., Walker, L. C., and Jucker, M. (2009) Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation Proc. Natl. Acad. Sci. U.S.A. 106, 12926-12931
40. Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-beta(1?42) fibrils Proc. Natl. Acad. Sci. U.S.A. 102, 17342-17347
41. Liu, H., Funke, S. A., and Willbold, D. (2010) Transport of alzheimer disease amyloid-beta-binding d-amino acid peptides across an in vitro blood-brain barrier model, Rejuvenation Res. 13, 210 ? 213.
42. Rapoport, M. and Lorberboum-Galski, H. (2010) TAT-based drug delivery system: new directions in protein delivery for new hopes? Expert Opin. Drug Delivery 6, 453-463
43. Klunk, W. E., Jacob, R. F., and Mason, R. P. (1999) Quantifying amyloid by congo red spectral shift assay Methods Enzymol. 309, 285-305
44. Klunk, W. E., Jacob, R. F., and Mason, R. P. (1999) Quantifying amyloid beta-peptide (Abeta) aggregation using the Congo red-Abeta (CR-abeta) spectrophotometric assay Anal. Biochem. 266, 66-76
45. Kassler, K., Horn, A. H., and Sticht, H. (2010) Effect of pathogenic mutations on the structure and dynamics of Alzheimer's Abeta(42)-amyloid oligomers, J. Mol. Model. 16, 1011 ? 1020.
46. Zheng, J., Jang, H., Ma, B., Tsai, C. J., and Nussinov, R. (2007) Modeling the Alzheimer Abeta17?42 fibril architecture: tight intermolecular sheet-sheet association and intramolecular hydrated cavities Biophys. J. 93, 3046-3057
47. Handattu, S. P., Garber, D. W., Monroe, C. E., van Groen, T., Kadish, I., Nayyar, G., Cao, D., Palgunachari, M. N., Li, L., and Anantharamaiah, G. M. (2009) Oral apolipoprotein A-I mimetic peptide improves cognitive function and reduces amyloid burden in a mouse model of Alzheimer's disease Neurobiol. Dis. 34, 525-534
48. van Groen, T., Kiliaan, A. J., and Kadish, I. (2006) Deposition of mouse amyloid beta in human APP/PS1 double and single AD model transgenic mice Neurobiol. Dis. 23, 653-662
49. Ida, N., Hartmann, T., Pantel, J., Schroder, J., Zerfass, R., Forstl, H., Sandbrink, R., Masters, C. L., and Beyreuther, K. (1996) Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay J. Biol. Chem. 271, 22908-22914
50. Kadish, I., Pradier, L., and van Groen, T. (2002) Transgenic mice expressing the human presenilin 1 gene demonstrate enhanced hippocampal reorganization following entorhinal cortex lesions Brain Res. Bull. 57, 587-594