Mechanisms of enzymatic degradation of amyloid β microfibrils generating nanofilaments and nanospheres related to cytotoxicity

Biochemistry

Volumn 49, Issue 15, 2010, Pages 3254-3260

  Numata, Keiji ^a   Kaplan, David L ^a,b  

^a Tufts University   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMERS DISEASE; BRAIN TISSUE; DEGRADATION MECHANISM; DEGRADATION PRODUCTS; DEGRADING ENZYMES; ENZYMATIC DEGRADATION; ENZYMATIC DIGESTIONS; INSULIN-DEGRADING ENZYMES; LOOP REGIONS; MICRO-FIBRILS; NANOFILAMENTS; NEPRILYSIN; NEURONAL CELL; SECONDARY STRUCTURES; STRUCTURAL FEATURE;

CYTOTOXICITY; ENZYMES; GLYCOPROTEINS; NANOSPHERES;

DEGRADATION;

AMYLOID BETA PROTEIN; CHYMOTRYPSIN A; NANOSPHERE; PROTEINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; ENZYMATIC DEGRADATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; BRAIN; CIRCULAR DICHROISM; HUMANS; INSULYSIN; KINETICS; MICROFIBRILS; NEPRILYSIN; NEURONS; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77950924188     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902134p     Document Type: Article

References (49)

1. Selkoe, D. J. (2003) Folding proteins in fatal ways Nature 426, 900 - 904
2. Ross, C. A. and Poirier, M. A. (2005) Opinion: What is the role of protein aggregation in neurodegeneration? Nat. Rev. Mol. Cell Biol. 6, 891 - 898
3. Sipe, J. D. and Cohen, A. S. (2000) History of the amyloid fibril J. Struct. Biol. 130, 88 - 98
4. Nagai, Y., Inui, T., Popiel, H. A., Fujikake, N., Hasegawa, K., Urade, Y., Goto, Y., Naiki, H., and Toda, T. (2007) A toxic monomeric conformer of the polyglutamine protein Nat. Struct. Mol. Biol. 14, 332 - 340
5. Chimon, S., Shaibat, M. A., Jones, C. R., Calero, D. C., Aizezi, B., and Ishii, Y. (2007) Evidence of fibril-like β-sheet structures in a neurotoxic amyloid intermediate of Alzheimer's β-amyloid Nat. Struct. Mol. Biol. 14, 1157 - 1164
6. Jarrett, J. T., Berger, E. P., and Lansbury, P. T., Jr. (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease Biochemistry 32, 4693 - 4697
7. Fradinger, E. A., Monien, B. H., Urbanc, B., Lomakin, A., Tan, M., Li, H., Spring, S. M., Condron, M. M., Cruz, L., Xie, C. W., Benedek, G. B., and Bitan, G. (2008) C-Terminal peptides coassemble into Aβ42 oligomers and protect neurons against Aβ42-induced neurotoxicity Proc. Natl. Acad. Sci. U.S.A. 105, 14175 - 14180
8. Yatin, S. M., Varadarajan, S., Link, C. D., and Butterfield, D. A. (1999) In vitro and in vivo oxidative stress associated with Alzheimer's amyloid β-peptide (1-42) Neurobiol. Aging 20, 325 - 330
9. Drake, J., Link, C. D., and Butterfield, D. A. (2003) Oxidative stress precedes fibrillar deposition of Alzheimer's disease amyloid β-peptide (1-42) in a transgenic Caenorhabditis elegans model Neurobiol. Aging 24, 415 - 420
10. Citron, M. (2004) Strategies for disease modification in Alzheimer's disease Nat. Rev. Neurosci. 5, 677 - 685
11. Masliah, E., Hansen, L., Adame, A., Crews, L., Bard, F., Lee, C., Seubert, P., Games, D., Kirby, L., and Schenk, D. (2005) Aβ vaccination effects on plaque pathology in the absence of encephalitis in Alzheimer's disease Neurology 64, 129 - 131
12. 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 Alzheimer-disease-like pathology in the PDAPP mouse Nature 400, 173 - 177
13. Iwata, N., Tsubuki, S., Takaki, Y., Watanabe, K., Sekiguchi, M., Hosoki, E., Kawashima-Morishima, M., Lee, H. J., Hama, E., Sekine-Aizawa, Y., and Saido, T. C. (2000) Identification of the major Aβ1-42-degrading catabolic pathway in brain parenchyma: Suppression leads to biochemical and pathological deposition Nat. Med. 6, 143 - 150
14. Madani, R., Poirier, R., Wolfer, D. P., Welzl, H., Groscurth, P., Lipp, H. P., Lu, B., El Mouedden, M., Mercken, M., Nitsch, R. M., and Mohajeri, M. H. (2006) Lack of neprilysin suffices to generate murine amyloid-like deposits in the brain and behavioral deficit in vivo J. Neurosci. Res. 84, 1871 - 1878
15. Authier, F., Posner, B. I., and Bergeron, J. J. (1996) Insulin-degrading enzyme Clin. Invest. Med. 19, 149 - 160
16. Duckworth, W. C., Bennett, R. G., and Hamel, F. G. (1998) Insulin degradation: Progress and potential Endocr. Rev. 19, 608 - 624
17. Pardossi-Piquard, R., Dunys, J., Yu, G., St George-Hyslop, P., Alves da Costa, C., and Checler, F. (2006) Neprilysin activity and expression are controlled by nicastrin J. Neurochem. 97, 1052 - 1056
18. Leissring, M. A., Farris, W., Wu, X., Christodoulou, D. C., Haigis, M. C., Guarente, L., and Selkoe, D. J. (2004) Alternative translation initiation generates a novel isoform of insulin-degrading enzyme targeted to mitochondria Biochem. J. 383, 439 - 446
19. Ciaccio, C., Tundo, G. R., Grasso, G., Spoto, G., Marasco, D., Ruvo, M., Gioia, M., Rizzarelli, E., and Coletta, M. (2009) Somatostatin: A novel substrate and a modulator of insulin-degrading enzyme activity J. Mol. Biol. 385, 1556 - 1567
20. Song, E. S., Juliano, M. A., Juliano, L., and Hersh, L. B. (2003) Substrate activation of insulin-degrading enzyme (insulysin). A potential target for drug development J. Biol. Chem. 278, 49789 - 49794
21. Arai, T., Freddi, G., Innocenti, R., and Tsukada, M. (2004) Biodegradation of Bombyx mori silk fibroin fibers and films J. Appl. Polym. Sci. 91, 2383 - 2390
22. Lotz, B., Gonthier-Vassal, A., Brack, A., and Magoshi, J. (1982) Twisted single crystals of Bombyx mori silk fibroin and related model polypeptides with β structure. A correlation with the twist of the β sheets in globular proteins J. Mol. Biol. 156, 345 - 357
23. Li, M., Ogiso, M., and Minoura, N. (2003) Enzymatic degradation behavior of porous silk fibroin sheets Biomaterials 24, 357 - 365
24. Numata, K., Cebe, P., and Kaplan, D. L. (2010) Mechanism of enzymatic degradation of β-sheet crystals Biomaterials 31, 2926 - 2933
25. Horan, R. L., Antle, K., Collette, A. L., Wang, Y., Huang, J., Moreau, J. E., Volloch, V., Kaplan, D. L., and Altman, G. H. (2005) In vitro degradation of silk fibroin Biomaterials 26, 3385 - 3393
26. Bauer, C. A., Thompson, R. C., and Blout, E. R. (1976) The active centers of Streptomyces griseus protease 3 and α-chymotrypsin: Enzyme-substrate interactions remote from the scissile bond Biochemistry 15, 1291 - 1295
27. Bauer, C. A., Thompson, R. C., and Blout, E. R. (1976) The active centers of Streptomyces griseus protease 3, α-chymotrypsin, and elastase: Enzyme-substrate interactions close to the scissile bond Biochemistry 15, 1296 - 1299
28. Bauer, C. A. (1978) Active centers of Streptomyces griseus protease 1, Streptomyces griseus protease 3, and α-chymotrypsin: Enzyme-substrate interactions Biochemistry 17, 375 - 380
29. Stine, W. B., Jr., Dahlgren, K. N., Krafft, G. A., and LaDu, M. J. (2003) In vitro characterization of conditions for amyloid-β peptide oligomerization and fibrillogenesis J. Biol. Chem. 278, 11612 - 11622
30. Numata, K., Hirota, T., Kikkawa, Y., Tsuge, T., Iwata, T., Abe, H., and Doi, Y. (2004) Enzymatic degradation processes of lamellar crystals in thin films for poly[(R)-3-hydroxybutyric acid] and its copolymers revealed by real-time atomic force microscopy Biomacromolecules 5, 2186 - 2194
31. Kanemitsu, H., Tomiyama, T., and Mori, H. (2003) Human neprilysin is capable of degrading amyloid β peptide not only in the monomeric form but also the pathological oligomeric form Neurosci. Lett. 350, 113 - 116
32. Sreerama, N. and Woody, R. W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism Anal. Biochem. 209, 32 - 44
33. Riss, T. L. and Moravec, R. A. (1992) Comparison of MTT, XTT, and a novel tetrazolium compound for MTS for in vitro proliferation and chemosensitivity assays Mol. Biol. Cell 3, 184a
34. Cheatum, C. M., Tokmakoff, A., and Knoester, J. (2004) Signatures of β-sheet secondary structures in linear and two-dimensional infrared spectroscopy J. Chem. Phys. 120, 8201 - 8215
35. Rak, M., Del Bigio, M. R., Mai, S., Westaway, D., and Gough, K. (2007) Dense-core and diffuse Aβ plaques in TgCRND8 mice studied with synchrotron FTIR microspectroscopy Biopolymers 87, 207 - 217
36. 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 Aβ1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U.S.A. 95, 6448 - 6453
37. Hoshi, M., Sato, M., Matsumoto, S., Noguchi, A., Yasutake, K., Yoshida, N., and Sato, K. (2003) Spherical aggregates of β-amyloid (amylospheroid) show high neurotoxicity and activate tau protein kinase I/glycogen synthase kinase-3β Proc. Natl. Acad. Sci. U.S.A. 100, 6370 - 6375
38. Kirschner, D. A., Abraham, C., and Selkoe, D. J. (1986) X-ray diffraction from intraneuronal paired helical filaments and extraneuronal amyloid fibers in Alzheimer disease indicates cross-β conformation Proc. Natl. Acad. Sci. U.S.A. 83, 503 - 507
39. 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
40. Luìhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Döbeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer's amyloid-β(1-42) fibrils Proc. Natl. Acad. Sci. U.S.A. 102, 17342 - 17347
41. Morelli, L., Llovera, R., Gonzalez, S. A., Affranchino, J. L., Prelli, F., Frangione, B., Ghiso, J., and Castano, E. M. (2003) Differential degradation of amyloid β genetic variants associated with hereditary dementia or stroke by insulin-degrading enzyme J. Biol. Chem. 278, 23221 - 23226
42. Morelli, L., Llovera, R. E., Alonso, L. G., Frangione, B., de Prat-Gay, G., Ghiso, J., and Castanìo, E. M. (2005) Insulin-degrading enzyme degrades amyloid peptides associated with British and Danish familial dementia Biochem. Biophys. Res. Commun. 332, 808 - 816
43. Zhao, J., Li, L., and Leissring, M. A. (2009) Insulin-degrading enzyme is exported via an unconventional protein secretion pathway Mol. Neurodegener. 4, 4
44. 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 (Part 2) 509 - 516
45. 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
46. Inouye, H., Fraser, P. E., and Kirschner, D. A. (1993) Structure of β-crystallite assemblies formed by Alzheimer β-amyloid protein analogues: Analysis by X-ray diffraction Biophys. J. 64, 502 - 519
47. Malinchik, S. B., Inouye, H., Szumowski, K. E., and Kirschner, D. A. (1998) Structural analysis of Alzheimer's β(1-40) amyloid: Protofilament assembly of tubular fibrils Biophys. J. 74, 537 - 545
48. Tucker, H. M., Kihiko, M., Caldwell, J. N., Wright, S., Kawarabayashi, T., Price, D., Walker, D., Scheff, S., McGillis, J. P., Rydel, R. E., and Estus, S. (2000) The plasmin system is induced by and degrades amyloid-β aggregates J. Neurosci. 20, 3937 - 3946
49. Jacobsen, J. S., Comery, T. A., Martone, R. L., Elokdah, H., Crandall, D. L., Oganesian, A., Aschmies, S., Kirksey, Y., Gonzales, C., Xu, J., Zhou, H., Atchison, K., Wagner, E., Zaleska, M. M., Das, I., Arias, R. L., Bard, J., Riddell, D., Gardell, S. J., Abou-Gharbia, M., Robichaud, A., Magolda, R., Vlasuk, G. P., Bjornsson, T., Reinhart, P. H., and Pangalos, M. N. (2008) Enhanced clearance of Aβ in brain by sustaining the plasmin proteolysis cascade Proc. Natl. Acad. Sci. U.S.A. 105, 8754 - 8759