Amyloid-β peptide-specific darpins as a novel class of potential therapeutics for alzheimer disease

Journal of Biological Chemistry

Volumn 289, Issue 39, 2014, Pages 27080-27089

  Hanenberg, Michael ^a   McAfoose, Jordan ^a   Kulic, Luka ^a,b   Welt, Tobias ^a   Wirth, Fabian ^a   Parizek, Petra ^c   Strobel, Lisa ^a   Cattepoel, Susann ^a   Späni, Claudia ^b   Derungs, Rebecca ^a   Maier, Marcel ^b   Plückthun, Andreas ^c   Nitsch, Roger M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c Neurimmune Holding AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE;

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; CENTRAL NERVOUS SYSTEM AGENTS; D23 PEPTIDE; E2 5 PEPTIDE; NEUROPROTECTIVE AGENT; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; ANKYRIN; APP PROTEIN, HUMAN; RECOMBINANT PROTEIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DRUG MECHANISM; DRUG PROTEIN BINDING; EPITOPE MAPPING; IN VITRO STUDY; MENTAL PERFORMANCE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN CONFORMATION; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANKYRIN REPEAT; HUMANS; MICE; MICE, TRANSGENIC; RECOMBINANT PROTEINS;

EID: 84907478708     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.564013     Document Type: Article

References (47)

1. Selkoe, D. J. (2011) Resolving controversies on the path to Alzheimer's therapeutics. Nat. Med. 17, 1060-1065
2. Citron, M. (2010) Alzheimer's disease: strategies for disease modification. Nat. Rev. Drug Discov. 9, 387-398
3. Karran, E., Mercken, M., and De Strooper, B. (2011) The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat. Rev. Drug. Discov. 10, 698-712
4. Schenk, D., Barbour, R., Dunn, W., Gordon, G., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., Khan, K., Kholodenko, D., Lee, M., Liao, Z., Lieberburg, I., Motter, R., Mutter, L., Soriano, F., Shopp, G., Vasquez, N., Vandevert, C., Walker, S., Wogulis, M., Yednock, T., Games, D., and Seubert, P. (1999) Immunization with amyloid-β attenuates Alzheimerdisease-like pathology in the PDAPP mouse. Nature 400, 173-177
5. Morgan, D., Diamond, D. M., Gottschall, P. E., Ugen, K. E., Dickey, C., Hardy, J., Duff, K., Jantzen, P., DiCarlo, G., Wilcock, D., Connor, K., Hatcher, J., Hope, C., Gordon, M., and Arendash, G. W. (2000)Aβ peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408, 982-985
6. Rinne, J. O., Brooks, D. J., Rossor, M. N., Fox, N. C., Bullock, R., Klunk, W. E., Mathis, C. A., Blennow, K., Barakos, J., Okello, A. A., Rodriguez Martinez de Liano S., Liu, E., Koller, M., Gregg, K. M., Schenk, D., Black, R., and Grundman, M. (2010) 11C-PiB PET assessment of change in fibrillar amyloid-β load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double-blind, placebo-controlled, ascendingdose study. Lancet Neurol. 9, 363-372
7. Siemers, E. R., Friedrich, S., Dean, R. A., Gonzales, C. R., Farlow, M. R., Paul, S. M., and Demattos, R. B. (2010) Safety and changes in plasma and cerebrospinal fluid amyloidβ after a single administration of an amyloidβ monoclonal antibody in subjects with Alzheimer disease. Clin. Neuropharmacol. 33, 67-73
8. Relkin, N. R., Szabo, P., Adamiak, B., Burgut, T., Monthe, C., Lent, R. W., Younkin, S., Younkin, L., Schiff, R., and Weksler, M. E. (2009) 18-Month study of intravenous immunoglobulin for treatment of mild Alzheimer disease. Neurobiol. Aging 30, 1728-1736
9. Delrieu, J., Ousset, P. J., Caillaud, C., and Vellas, B. (2012) "Clinical trials in Alzheimer's disease": immunotherapy approaches. J. Neurochem. 120, 186-193
10. Boersma, Y. L., and Plückthun, A. (2011) DARPins and other repeat protein scaffolds: advances in engineering and applications. Curr. Opin. Biotechnol. 22, 849-857
11. Binz, H. K., Stumpp, M. T., Forrer, P., Amstutz, P., and Plückthun, A. (2003) Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J. Mol. Biol. 332, 489-503
12. Binz, H. K., Amstutz, P., Kohl, A., Stumpp, M. T., Briand, C., Forrer, P., Grütter, M. G., and Plückthun, A. (2004) High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 22, 575-582
13. Amstutz, P., Binz, H. K., Parizek, P., Stumpp, M. T., Kohl, A., Grütter, M. G., Forrer, P., and Plückthun, A. (2005) Intracellular kinase inhibitors selected from combinatorial libraries of designed ankyrin repeat proteins. J. Biol. Chem. 280, 24715-24722
14. Kohl, A., Amstutz, P., Parizek, P., Binz, H. K., Briand, C., Capitani, G., Forrer, P., Plückthun, A., and Grütter, M. G. (2005) Allosteric inhibition of aminoglycoside phosphotransferase by a designed ankyrin repeat protein. Structure 13, 1131-1141
15. Zahnd, C., Kawe, M., Stumpp, M. T., de Pasquale, C., Tamaskovic, R., Nagy-Davidescu, G., Dreier, B., Schibli, R., Binz, H. K., Waibel, R., and Plückthun, A. (2010) Efficient tumor targeting with high affinity designed ankyrin repeat proteins: effects of affinity and molecular size. Cancer Res. 70, 1595-1605
16. Banks, W. A., Terrell, B., Farr, S. A., Robinson, S. M., Nonaka, N., and Morley, J. E. (2002) Passage of amyloid β protein antibody across the blood-brain barrier in a mouse model of Alzheimer's disease. Peptides 23, 2223-2226
17. Bard, F., Cannon, C., Barbour, R., Burke, R. L., Games, D., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., Khan, K., Kholodenko, D., Lee, M., Lieberburg, I., Motter, R., Nguyen, M., Soriano, F., Vasquez, N., Weiss, K., Welch, B., Seubert, P., Schenk, D., and Yednock, T. (2000) Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 6, 916-919
18. Levites, Y., Smithson, L. A., Price, R. W., Dakin, R. S., Yuan, B., Sierks, M. R., Kim, J., McGowan, E., Reed, D. K., Rosenberry, T. L., Das, P., and Golde, T. E. (2006) Insights into the mechanisms of action of anti-Aβ antibodies in Alzheimer's disease mouse models. FASEB J. 20, 2576-2578
19. Stumpp, M. T., Binz, H. K., and Amstutz, P. (2008) DARPins: a new generation of protein therapeutics. Drug Discov. Today 13, 695-701
20. Cattepoel, S., Hanenberg, M., Kulic, L., and Nitsch, R. M. (2011) Chronic intranasal treatment with an anti-Aβ30-42 scFv antibody ameliorates amyloid pathology in a transgenic mouse model of Alzheimer's disease. PLoS ONE 6, e18296
21. Zahnd, C., Amstutz, P., and Plückthun, A. (2007) Ribosome display: selecting and evolving proteins in vitro that specifically bind to a target. Nat. Methods 4, 269-279
22. Wetzel, S. K., Settanni, G., Kenig, M., Binz, H. K., and Plückthun, A. (2008) Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 376, 241-257
23. Finder, V. H., Vodopivec, I., Nitsch, R. M., and Glockshuber, R. (2010) The recombinant amyloid-β peptide Aβ 1-42 aggregates faster and is more neurotoxic than synthetic Aβ 1-42. J. Mol. Biol. 396, 9-18
24. Hsiao, K., Chapman, P., Nilsen, S., Eckman, C., Harigaya, Y., Younkin, S., Yang, F., and Cole, G. (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274, 99-102
25. Biscaro, B., Lindvall, O., Hock, C., Ekdahl, C. T., and Nitsch, R. M. (2009) Aβ immunotherapy protects morphology and survival of adult-born neurons in doubly transgenic APP/PS1 mice. J. Neurosci. 29, 14108-14119
26. Kim, K. S., Miller, D. L., Sapienza, V. J., Chen, C. M., Bai, C., Gundke-Iqbal, I., Currie, J. R., and Wisniewski, H. M. (1988) Production and characterization of monoclonal antibodies reactive to synthetic cerebrovascular amyloid peptide. Neurosci. Res. Commun. 2, 121-130
27. Mohajeri, M. H., Saini, K., Schultz, J. G., Wollmer, M. A., Hock, C., and Nitsch, R. M. (2002) Passive immunization againstβ-amyloid peptide protects central nervous system (CNS) neurons from increased vulnerability associated with an Alzheimer's disease-causing mutation. J. Biol. Chem. 277, 33012-33017
28. Arendash, G. W., Gordon, M. N., Diamond, D. M., Austin, L. A., Hatcher, J. M., Jantzen, P., DiCarlo, G., Wilcock, D., and Morgan, D. (2001) Behavioral assessment of Alzheimer's transgenic mice following long-term Aβ vaccination: task specificity and correlations between Aβ deposition and spatial memory. DNA Cell Biol. 20, 737-744
29. Wilcock, D. M., Rojiani, A., Rosenthal, A., Levkowitz, G., Subbarao, S., Alamed, J., Wilson, D., Wilson, N., Freeman, M. J., Gordon, M. N., and Morgan, D. (2004) Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J. Neurosci. 24, 6144-6151
30. DeMattos, R. B., Bales, K. R., Cummins, D. J., Dodart, J.-C., Paul, S. M., and Holtzman, D. M. (2001) Peripheral anti-Aβ antibody alters CNS and plasma Aβ clearance and decreases brain Aβ burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 98, 8850-8855
31. 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
32. O'Nuallain, B., and Wetzel, R. (2002) Conformational Abs recognizing a generic amyloid fibril epitope. Proc. Natl. Acad. Sci. U.S.A. 99, 1485-1490
33. Ramakrishnan, M., Kandimalla, K. K., Wengenack, T. M., Howell, K. G., and Poduslo, J. F. (2009) Surface plasmon resonance binding kinetics of Alzheimer's disease amyloid β peptide-capturing and plaque-binding monoclonal antibodies. Biochemistry 48, 10405-10415
34. Schweizer, A., Roschitzki-Voser, H., Amstutz, P., Briand, C., Gulotti-Georgieva, M., Prenosil, E., Binz, H. K., Capitani, G., Baici, A., Plückthun, A., and Grütter, M. G. (2007) Inhibition of caspase-2 by a designed ankyrin repeat protein: specificity, structure, and inhibition mechanism. Structure 15, 625-636
35. Vitalis, A., and Caflisch, A. (2010) Micelle-like architecture of the monomer ensemble of Alzheimer's amyloid-β peptide in aqueous solution and its implications for Aβ aggregation. J. Mol. Biol. 403, 148-165
36. Tampellini, D., Magrané, J., Takahashi, R. H., Li, F., Lin, M. T., Almeida, C. G., and Gouras, G. K. (2007) Internalized antibodies to the Aβ domain of APP reduce neuronal Aβ and protect against synaptic alterations. J. Biol. Chem. 282, 18895-18906
37. Colcher, D., Pavlinkova, G., Beresford, G., Booth, B. J., Choudhury, A., and Batra, S. K. (1998) Pharmacokinetics and biodistribution of geneticallyengineered antibodies. Q. J. Nucl. Med. 42, 225-241
38. Koenigsknecht-Talboo, J., Meyer-Luehmann, M., Parsadanian, M., Garcia-Alloza, M., Finn, M. B., Hyman, B. T., Bacskai, B. J., and Holtzman, D. M. (2008) Rapid microglial response around amyloid pathology after systemic anti-Aβ antibody administration in PDAPP mice. J. Neurosci. 28, 14156-14164
39. Wang, A., Das, P., Switzer, R. C.,Golde, T. E., and Jankowsky, J. L. (2011) Robust amyloid clearance in a mouse model of Alzheimer's disease provides novel insights into the mechanism of amyloid-β immunotherapy. J. Neurosci. 31, 4124-4136
40. Racke, M. M., Boone, L. I., Hepburn, D. L., Parsadainian, M., Bryan, M. T., Ness, D. K., Piroozi, K. S., Jordan, W. H., Brown, D. D., Hoffman, W. P., Holtzman, D. M., Bales, K. R., Gitter, B. D., May, P. C., Paul, S. M., and DeMattos, R. B. (2005) Exacerbation of cerebral amyloid angiopathy-associated microhemorrhage in amyloid precursor protein transgenic mice by immunotherapy is dependent on antibody recognition of deposited forms of amyloid β. J. Neurosci. 25, 629-636
41. Pfeifer, M., Boncristiano, S., Bondolfi, L., Stalder, A., Deller, T., Staufenbiel, M., Mathews, P. M., and Jucker, M. (2002) Cerebral hemorrhage after passive anti-Aβ immunotherapy. Science 298, 1379
42. Bacskai, B. J., Kajdasz, S. T., McLellan, M. E., Games, D., Seubert, P., Schenk, D., and Hyman, B. T. (2002) Non-Fc-mediated mechanisms are involved in clearance of amyloid-β in vivo by immunotherapy. J. Neurosci. 22, 7873-7878
43. Wilcock, D. M., DiCarlo, G., Henderson, D., Jackson, J., Clarke, K., Ugen, K. E., Gordon, M. N., and Morgan, D. (2003) Intracranially administered anti-Aβ antibodies reduce β-amyloid deposition by mechanisms both independent of and associated with microglial activation. J. Neurosci. 23, 3745-3751
44. Wilcock, D. M., Alamed, J., Gottschall, P. E., Grimm, J., Rosenthal, A., Pons, J., Ronan, V., Symmonds, K., Gordon, M. N., and Morgan, D. (2006) Deglycosylated anti-amyloid-β antibodies eliminate cognitive deficits and reduce parenchymal amyloid with minimal vascular consequences in aged amyloid precursor protein transgenic mice. J. Neurosci. 26, 5340-5346
45. Shibata, M., Yamada, S., Kumar, S. R., Calero, M., Bading, J., Frangione, B., Holtzman, D. M., Miller, C. A., Strickland, D. K., Ghiso, J., and Zlokovic, B. V. (2000) Clearance of Alzheimer's amyloid-β1-40 peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J. Clin. Invest. 106, 1489-1499
46. Dennis, M. S., Zhang, M., Meng, Y. G., Kadkhodayan, M., Kirchhofer, D., Combs, D., and Damico, L. A. (2002) Albumin binding as a general strategy for improving the pharmacokinetics of proteins. J. Biol. Chem. 277, 35035-35043
47. Nguyen, A., Reyes, A. E.,Zhang, M., McDonald, P., Wong, W. L., Damico, L. A., and Dennis, M. S. (2006) The pharmacokinetics of an albumin-binding Fab (AB. Fab) can be modulated as a function of affinity for albumin. Protein Eng. Des. Sel. 19, 291-297.