Specific amyloid β clearance by a catalytic antibody

Journal of Biological Chemistry

Volumn 290, Issue 16, 2015, Pages 10229-10241

  Planque, Stephanie A ^a   Nishiyama, Yasuhiro ^a   Sonoda, Sari ^a   Lin, Yan ^b   Taguchi, Hiroaki ^a   Hara, Mariko ^a   Kolodziej, Steven ^a   Mitsuda, Yukie ^a   Gonzalez, Veronica ^b   Sait, Hameetha B R ^b   Fukuchi, Ken Ichiro ^c   Massey, Richard J ^d   Friedland, Robert P ^e   O'Nuallain, Brian ^f   Sigurdsson, Einar M ^a,b   Paul, Sudhir ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

^d Covalent Bioscience Inc ^*  (United States)

^e University of Louisville School of Medicine   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; GLYCOPROTEINS; HYDROLYSIS; PROTEINS;

ALZHEIMER DISEASE; AMYLOID BETAS; CATALYTIC ANTIBODIES; DI-PEPTIDES; INNATE IMMUNES; INNATE IMMUNITY; PRECURSOR PROTEINS; TRANSTHYRETIN;

ANTIBODIES;

AMYLOID BETA PROTEIN; CATALYTIC ANTIBODY; PEPTIDE FRAGMENT; RECOMBINANT PROTEIN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BINDING AFFINITY; CATALYSIS; CINGULATE GYRUS; CONTROLLED STUDY; DISSOLUTION; ELECTROPHORESIS; EXPRESSION VECTOR; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOBLOTTING; INNATE IMMUNITY; ION EXCHANGE CHROMATOGRAPHY; MOUSE; NEUROTRANSMISSION; NONHUMAN; OLIGOMERIZATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PURIFICATION; RADIOACTIVITY; TRANSMISSION ELECTRON MICROSCOPY; ALZHEIMER DISEASE; ANIMAL; BRAIN; CHEMISTRY; DISEASE MODEL; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PROTEIN ENGINEERING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANTIBODIES, CATALYTIC; BRAIN; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HEK293 CELLS; HUMANS; HYDROLYSIS; IMMUNITY, INNATE; MICE; PEPTIDE FRAGMENTS; PROTEIN ENGINEERING; PROTEOLYSIS; RECOMBINANT PROTEINS; SINGLE-CHAIN ANTIBODIES;

EID: 84927920291     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.641738     Document Type: Article

References (61)

1. Haass, C., and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112
2. Attems, J., Jellinger, K., Thal, D. R., and Van Nostrand, W. (2011) Review: sporadic cerebral amyloid angiopathy. Neuropathol. Appl. Neurobiol. 37, 75-93
3. Jellinger, K. A. (2002) Alzheimer disease and cerebrovascular pathology: an update. J. Neural Transm. 109, 813-836
4. 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
5. Adolfsson, O., Pihlgren, M., Toni, N., Varisco, Y., Buccarello, A. L., Antoniello, K., Lohmann, S., Piorkowska, K., Gafner, V., Atwal, J. K., Maloney, J., Chen, M., Gogineni, A., Weimer, R. M., Mortensen, D. L., Friesenhahn, M., Ho, C., Paul, R., Pfeifer, A., Muhs, A., and Watts, R. J. (2012) An effector-reduced anti-β-amyloid (Aβ) antibody with unique Aβ binding properties promotes neuroprotection and glial engulfment of Aβ. J. Neurosci. 32, 9677-9689
6. Zago, W., Schroeter, S., Guido, T., Khan, K., Seubert, P., Yednock, T., Schenk, D., Gregg, K. M., Games, D., Bard, F., and Kinney, G. G. (2013) Vascular alterations in PDAPP mice after anti-Aβ immunotherapy: implications for amyloid-related imaging abnormalities. Alzheimers Dement. 9, S105-S115
7. Sperling, R., Salloway, S., Brooks, D. J., Tampieri, D., Barakos, J., Fox, N. C., Raskind, M., Sabbagh, M., Honig, L. S., Porsteinsson, A. P., Lieberburg, I., Arrighi, H. M., Morris, K. A., Lu, Y., Liu, E., Gregg, K. M., Brashear, H. R., Kinney, G. G., Black, R., and Grundman, M. (2012) Amyloid-related imaging abnormalities in patients with Alzheimer's disease treated with bapineuzumab: a retrospective analysis. Lancet Neurol. 11, 241-249
8. Salloway, S., Sperling, R., Fox, N. C., Blennow, K., Klunk, W., Raskind, M., Sabbagh, M., Honig, L. S., Porsteinsson, A. P., Ferris, S., Reichert, M., Ketter, N., Nejadnik, B., Guenzler, V., Miloslavsky, M., Wang, D., Lu, Y., Lull, J., Tudor, I. C., Liu, E., Grundman, M., Yuen, E., Black, R., and Brashear, H. R. (2014) Two phase 3 trials of bapineuzumab in mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 370, 322-333
9. Morkuniene, R., Zvirbliene, A., Dalgediene, I., Cizas, P., Jankeviciute, S., Baliutyte, G., Jokubka, R., Jankunec, M., Valincius, G., and Borutaite, V. (2013) Antibodies bound to Aβ oligomers potentiate the neurotoxicity of Aβ by activating microglia. J. Neurochem. 126, 604-615
10. Lei, C., Lin, S., Tao, W., Hao, Z., Liu, M., and Wu, B. (2013) Association between cerebral microbleeds and cognitive function: a systematic review. J. Neurol. Neurosurg. Psychiatry 84, 693-697
11. Piazza, F., Greenberg, S. M., Savoiardo, M., Gardinetti, M., Chiapparini, L., Raicher, I., Nitrini, R., Sakaguchi, H., Brioschi, M., Billo, G., Colombo, A., Lanzani, F., Piscosquito, G., Carriero, M. R., Giaccone, G., Tagliavini, F., Ferrarese, C., and DiFrancesco, J. C. (2013) Anti-amyloid β autoantibodies in cerebral amyloid angiopathy-related inflammation: implications for amyloid-modifying therapies. Ann. Neurol. 73, 449-458
12. Paul, S., Planque, S. A., Nishiyama, Y., Hanson, C. V., and Massey, R. J. (2012) Nature and nurture of catalytic antibodies. Adv. Exp. Med. Biol. 750, 56-75
13. Shuster, A. M., Gololobov, G. V., Kvashuk, O. A., Bogomolova, A. E., Smirnov, I. V., and Gabibov, A. G. (1992) DNA hydrolyzing autoantibodies. Science 256, 665-667
14. Taguchi, H., Planque, S., Sapparapu, G., Boivin, S., Hara, M., Nishiyama, Y., and Paul, S. (2008) Exceptional amyloid β peptide hydrolyzing activity of nonphysiological immunoglobulin variable domain scaffolds. J. Biol. Chem. 283, 36724-36733
15. Fukuchi, K., Tahara, K., Kim, H. D., Maxwell, J. A., Lewis, T. L., Accavitti-Loper, M. A., Kim, H., Ponnazhagan, S., and Lalonde, R. (2006) Anti-Aßsingle-chain antibody delivery via adeno-associated virus for treatment of Alzheimer's disease. Neurobiol. Dis. 23, 502-511
16. Sapparapu, G., Planque, S. A., Nishiyama, Y., Foung, S. K., and Paul, S. (2009) Antigen-specific proteolysis by hybrid antibodies containing promiscuous proteolytic light chains paired with an antigen-binding heavy chain. J. Biol. Chem. 284, 24622-24633
17. Zhang, J., Liu, X., Bell, A., To, R., Baral, T. N., Azizi, A., Li, J., Cass, B., and Durocher, Y. (2009) Transient expression and purification of chimeric heavy chain antibodies. Protein Expr. Purif. 65, 77-82
18. Nishiyama, Y., Taguchi, H., Hara, M., Planque, S. A., Mitsuda, Y., and Paul, S. (2014) Metal-dependent amyloid β-degrading catalytic antibody construct. J. Biotechnol. 180, 17-22
19. Planque, S. A., Nishiyama, Y., Hara, M., Sonoda, S., Murphy, S. K., Watanabe, K., Mitsuda, Y., Brown, E. L., Massey, R. J., Primmer, S. R., O'Nuallain, B., and Paul, S. (2014) Physiological IgM class catalytic antibodies selective for transthyretin amyloid. J. Biol. Chem. 289, 13243-13258
20. Nishiyama, Y., Karle, S., Mitsuda, Y., Taguchi, H., Planque, S., Salas, M., Hanson, C., and Paul, S. (2006) Towards irreversible HIV inactivation: stable gp120 binding by nucleophilic antibodies. J. Mol. Recognit. 19, 423-431
21. Dahlgren, K. N., Manelli, A. M., Stine, W. B., Jr., Baker, L. K., Krafft, G. A., and LaDu, M. J. (2002) Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046-32053
22. Paul, S., Planque, S., Zhou, Y. X., Taguchi, H., Bhatia, G., Karle, S., Hanson, C., and Nishiyama, Y. (2003) Specific HIV gp120-cleaving antibodies induced by covalently reactive analog of gp120. J. Biol. Chem. 278, 20429-20435
23. Oakley, H., Cole, S. L., Logan, S., Maus, E., Shao, P., Craft, J., Guillozet-Bongaarts, A., Ohno, M., Disterhoft, J., Van Eldik, L., Berry, R., and Vassar, R. (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140
24. Asuni, A. A., Boutajangout, A., Scholtzova, H., Knudsen, E., Li, Y. S., Quartermain, D., Frangione, B., Wisniewski, T., and Sigurdsson, E. M. (2006) Vaccination of Alzheimer's model mice with Aβ derivative in alum adjuvant reduces Aβ burden without microhemorrhages. Eur. J. Neurosci. 24, 2530-2542
25. Davis, J., Xu, F., Deane, R., Romanov, G., Previti, M. L., Zeigler, K., Zlokovic, B. V., and Van Nostrand, W. E. (2004) Early-onset and robust cerebral microvascular accumulation of amyloid β-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid β-protein precursor. J. Biol. Chem. 279, 20296-20306
26. Miao, J., Xu, F., Davis, J., Otte-Höller, I., Verbeek, M. M., and Van Nostrand, W. E. (2005) Cerebral microvascular amyloid β protein deposition induces vascular degeneration and neuroinflammation in transgenic mice expressing human vasculotropic mutant amyloid β precursor protein. Am. J. Pathol. 167, 505-515
27. Li, L., Sun, M., Gao, Q. S., and Paul, S. (1996) Low level formation of potent catalytic IgG fragments mediated by disulfide bond instability. Mol. Immunol. 33, 593-600
28. Sumitomo, M., Shen, R., and Nanus, D. M. (2005) Involvement of neutral endopeptidase in neoplastic progression. Biochim. Biophys. Acta 1751, 52-59
29. Radisky, E. S., Lee, J. M., Lu, C. J., and Koshland, D. E., Jr. (2006) Insights into the serine protease mechanism from atomic resolution structures of trypsin reaction intermediates. Proc. Natl. Acad. Sci. U.S.A. 103, 6835-6840
30. Randall, A. D., Witton, J., Booth, C., Hynes-Allen, A., and Brown, J. T. (2010) The functional neurophysiology of the amyloid precursor protein (APP) processing pathway. Neuropharmacology 59, 243-267
31. Kasturirangan, S., Boddapati, S., and Sierks, M. R. (2010) Engineered proteolytic nanobodies reduce Aβ burden and ameliorate Aβ-induced cytotoxicity. Biochemistry 49, 4501-4508
32. Efthimiopoulos, S., Vassilacopoulou, D., Ripellino, J. A., Tezapsidis, N., and Robakis, N. K. (1996) Cholinergic agonists stimulate secretion of soluble full-length amyloid precursor protein in neuroendocrine cells. Proc. Natl. Acad. Sci. U.S.A. 93, 8046-8050
33. Kitazume, S., Yoshihisa, A., Yamaki, T., Oikawa, M., Tachida, Y., Ogawa, K., Imamaki, R., Hagiwara, Y., Kinoshita, N., Takeishi, Y., Furukawa, K., Tomita, N., Arai, H., Iwata, N., Saido, T., Yamamoto, N., and Taniguchi, N. (2012) Soluble amyloid precursor protein 770 is released from inflamed endothelial cells and activated platelets: a novel biomarker for acute coronary syndrome. J. Biol. Chem. 287, 40817-40825
34. Barrett, P. J., Song, Y., Van Horn, W. D., Hustedt, E. J., Schafer, J. M., Hadziselimovic, A., Beel, A. J., and Sanders, C. R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336, 1168-1171
35. Mukherjee, A., Song, E., Kihiko-Ehmann, M., Goodman, J. P., Jr., Pyrek, J. S., Estus, S., and Hersh, L. B. (2000) Insulysin hydrolyzes amyloid β peptides to products that are neither neurotoxic nor deposit on amyloid plaques. J. Neurosci. 20, 8745-8749
36. Fukumoto, H., Tokuda, T., Kasai, T., Ishigami, N., Hidaka, H., Kondo, M., Allsop, D., and Nakagawa, M. (2010) High-molecular-weight β-amyloid oligomers are elevated in cerebrospinal fluid of Alzheimer patients. FASEB J. 24, 2716-2726
37. Chesneau, V., Vekrellis, K., Rosner, M. R., and Selkoe, D. J. (2000) Purified recombinant insulin-degrading enzyme degrades amyloid β-protein but does not promote its oligomerization. Biochem. J. 351, 509-516
38. Purushothuman, S., Marotte, L., Stowe, S., Johnstone, D. M., and Stone, J. (2013) The response of cerebral cortex to haemorrhagic damage: experimental evidence from a penetrating injury model. PLoS One 8, e59740
39. 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
40. Banks, W. A., Farr, S. A., Morley, J. E., Wolf, K. M., Geylis, V., and Steinitz, M. (2007) Anti-amyloid β protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of Alzheimer's disease: an age-related selective uptake with reversal of learning impairment. Exp. Neurol. 206, 248-256
41. Salloway, S., Sperling, R., Gilman, S., Fox, N. C., Blennow, K., Raskind, M., Sabbagh, M., Honig, L. S., Doody, R., van Dyck, C. H., Mulnard, R., Barakos, J., Gregg, K. M., Liu, E., Lieberburg, I., Schenk, D., Black, R., Grundman, M., and Bapineuzumab 201 Clinical Trial, I. (2009) A phase 2 multiple ascending dose trial of bapineuzumab in mild to moderate Alzheimer disease. Neurology 73, 2061-2070
42. Vasilevko, V., Xu, F., Previti, M. L., Van Nostrand, W. E., and Cribbs, D. H. (2007) Experimental investigation of antibody-mediated clearance mechanisms of amyloid-β in CNS of Tg-SwDI transgenic mice. J. Neurosci. 27, 13376-13383
43. Doody, R. S., Thomas, R. G., Farlow, M., Iwatsubo, T., Vellas, B., Joffe, S., Kieburtz, K., Raman, R., Sun, X., Aisen, P. S., Siemers, E., Liu-Seifert, H., and Mohs, R. (2014) Phase 3 trials of solanezumab for mild-to-moderate Alzheimer's disease. N. Engl. J. Med. 370, 311-321
44. Kou, J., Yang, J., Lim, J. E., Pattanayak, A., Song, M., Planque, S., Paul, S., and Fukuchi, K. (2015) Catalytic immunoglobulin gene delivery in a mouse model of Alzheimer's disease: prophylactic and therapeutic applications. Mol. Neurobiol. 51, 43-56
45. Colcher, D., Pavlinkova, G., Beresford, G., Booth, B. J., Choudhury, A., and Batra, S. K. (1998) Pharmacokinetics and biodistribution of genetically-engineered antibodies. Q. J. Nucl. Med. 42, 225-241
46. Robert, R., and Wark, K. L. (2012) Engineered antibody approaches for Alzheimer's disease immunotherapy. Arch. Biochem. Biophys. 526, 132-138
47. Berger, V., Richter, F., Zettlitz, K., Unverdorben, F., Scheurich, P., Herrmann, A., Pfizenmaier, K., and Kontermann, R. E. (2013) An anti-TNFR1 scFv-HSA fusion protein as selective antagonist of TNF action. Protein Eng. Des. Sel. 26, 581-587
48. Spencer, B. J., and Verma, I. M. (2007) Targeted delivery of proteins across the blood-brain barrier. Proc. Natl. Acad. Sci. U.S.A. 104, 7594-7599
49. Thomas, F. C., Taskar, K., Rudraraju, V., Goda, S., Thorsheim, H. R., Gaasch, J. A., Mittapalli, R. K., Palmieri, D., Steeg, P. S., Lockman, P. R., and Smith, Q. R. (2009) Uptake of ANG1005, a novel paclitaxel derivative, through the blood-brain barrier into brain and experimental brain metastases of breast cancer. Pharm. Res. 26, 2486-2494
50. Schurr, J. M., and McLaren, A. D. (1966) Enzyme action: comparison on soluble and insoluble substrate. Science 152, 1064-1066
51. Cruys-Bagger, N., Elmerdahl, J., Praestgaard, E., Borch, K., and Westh, P. (2013) A steady-state theory for processive cellulases. FEBS J. 280, 3952-3961
52. Barrow, C. J., Yasuda, A., Kenny, P. T., and Zagorski, M. G. (1992) Solution conformations and aggregational properties of synthetic amyloid β-peptides of Alzheimer's disease: analysis of circular dichroism spectra. J. Mol. Biol. 225, 1075-1093
53. Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747
54. Kuroda, D., Shirai, H., Jacobson, M. P., and Nakamura, H. (2012) Computer-aided antibody design. Protein Eng. Des. Sel. 25, 507-521
55. Yoshihara, T., Takiguchi, S., Kyuno, A., Tanaka, K., Kuba, S., Hashiguchi, S., Ito, Y., Hashimoto, T., Iwatsubo, T., Tsuyama, S., Nakashima, T., and Sugimura, K. (2008) Immunoreactivity of phage library-derived human single-chain antibodies to amyloid β conformers in vitro. J. Biochem. 143, 475-486
56. Pollack, S. J., Hsiun, P., and Schultz, P. G. (1989) Stereospecific hydrolysis of alkyl esters by antibodies. J. Am. Chem. Soc. 111, 5961-5962
57. Goodyear, C. S., and Silverman, G. J. (2005) B cell superantigens: a microbe's answer to innate-like B cells and natural antibodies. Springer Semin. Immunopathol. 26, 463-484
58. Lesné, S. E., Sherman, M. A., Grant, M., Kuskowski, M., Schneider, J. A., Bennett, D. A., and Ashe, K. H. (2013) Brain amyloid-β oligomers in ageing and Alzheimer's disease. Brain 136, 1383-1398
59. Kalinin, S., Willard, S. L., Shively, C. A., Kaplan, J. R., Register, T. C., Jorgensen, M. J., Polak, P. E., Rubinstein, I., and Feinstein, D. L. (2013) Development of amyloid burden in African Green monkeys. Neurobiol. Aging 34, 2361-2369
60. Greenberg, A. S., Avila, D., Hughes, M., Hughes, A., McKinney, E. C., and Flajnik, M. F. (1995) A new antigen receptor gene family that undergoes rearrangement and extensive somatic diversification in sharks. Nature 374, 168-173
61. Tucker, H. M., Kihiko-Ehmann, M., and Estus, S. (2002) Urokinase-type plasminogen activator inhibits amyloid-β neurotoxicity and fibrillogenesis via plasminogen. J. Neurosci. Res. 70, 249-255