A universal method for detection of amyloidogenic misfolded proteins

Biochemistry

Volumn 50, Issue 20, 2011, Pages 4322-4329

  Yam, Alice Y ^a   Wang, Xuemei ^a   Gao, Carol Man ^b   Connolly, Michael D ^b   Zuckermann, Ronald N ^d   Bleu, Thieu ^d   Hall, John ^d   Fedynyshyn, Joseph P ^d   Allauzen, Sophie ^d   Peretz, David ^c   Salisbury, Cleo M ^a  

^a Novartis Vaccines and Diagnostics Inc   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c Tethys Bioscience   (United States)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMERS DISEASE; BIOLOGICAL MATRIXES; CELLULAR DAMAGE; EARLY DETECTION; MISFOLDED PROTEINS; MISFOLDING; PATHOPHYSIOLOGY; PROTEIN AGGREGATES; RESEARCH TOOLS; SUPRAMOLECULAR FEATURES; TYPE II; UNIVERSAL METHOD;

AGGREGATES; BIOLOGY; CELL DEATH; DAMAGE DETECTION; OLIGOMERS;

PROTEINS;

ALPHA SYNUCLEIN; AMYLIN; AMYLOID BETA PROTEIN; OLIGOMER; SERINE PROTEINASE INHIBITOR; SERPIN A1; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOIDOGENIC MISFOLDED PROTEIN; ARTICLE; BRAIN HOMOGENATE; BRAIN SPONGIOSIS; CELL DEATH; CHEMICAL STRUCTURE; HUMAN; HUMAN TISSUE; IMMUNOASSAY; IN VITRO STUDY; NEUROLOGIC DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; PARKINSON DISEASE; PATHOPHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PREECLAMPSIA; PRION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN DEFECT; SYNUCLEINOPATHY; TAUOPATHY; VASCULAR AMYLOIDOSIS;

AMYLOID; EARLY DIAGNOSIS; HUMANS; INDICATORS AND REAGENTS; MOLECULAR WEIGHT; PEPTOIDS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEOSTASIS DEFICIENCIES;

EID: 79956193967     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200215j     Document Type: Article

References (55)

1. Leliveld, S. R. and Korth, C. (2007) The use of conformation-specific ligands and assays to dissect the molecular mechanisms of neurodegenerative diseases J. Neurosci. Res. 85, 2285-2297 (Pubitemid 47204744)
2. Lansbury, P. T. and Lashuel, H. A. (2006) A century-old debate on protein aggregation and neurodegeneration enters the clinic Nature 443, 774-779 (Pubitemid 44622681)
3. 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 (Pubitemid 46432529)
4. Haataja, L., Gurlo, T., Huang, C. J., and Butler, P. C. (2008) Islet amyloid in type 2 diabetes, and the toxic oligomer hypothesis Endocr. Rev. 29, 303-316 (Pubitemid 351679701)
5. Klyubin, I., Betts, V., Welzel, A. T., Blennow, K., Zetterberg, H., Wallin, A., Lemere, C. A., Cullen, W. K., Peng, Y., Wisniewski, T., Selkoe, D. J., Anwyl, R., Walsh, D. M., and Rowan, M. J. (2008) Amyloid beta protein dimer-containing human CSF disrupts synaptic plasticity: prevention by systemic passive immunization J. Neurosci. 28, 4231-4237
6. Konarkowska, B., Aitken, J. F., Kistler, J., Zhang, S., and Cooper, G. J. (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells FEBS J. 273, 3614-3624 (Pubitemid 44086959)
7. Lacor, P. N., Buniel, M. C., Chang, L., Fernandez, S. J., Gong, Y., Viola, K. L., Lambert, M. P., Velasco, P. T., Bigio, E. H., Finch, C. E., Krafft, G. A., and Klein, W. L. (2004) Synaptic targeting by Alzheimer's-related amyloid beta oligomers J. Neurosci. 24, 10191-10200 (Pubitemid 39492046)
8. Lacor, P. N., Buniel, M. C., Furlow, P. W., Clemente, A. S., Velasco, P. T., Wood, M., Viola, K. L., and Klein, W. L. (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease J. Neurosci. 27, 796-807 (Pubitemid 46174498)
9. 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
10. Lin, H., Bhatia, R., and Lal, R. (2001) Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology FASEB J. 15, 2433-2444 (Pubitemid 33063171)
11. Karpinar, D. P., Balija, M. B., Kugler, S., Opazo, F., Rezaei-Ghaleh, N., Wender, N., Kim, H. Y., Taschenberger, G., Falkenburger, B. H., Heise, H., Kumar, A., Riedel, D., Fichtner, L., Voigt, A., Braus, G. H., Giller, K., Becker, S., Herzig, A., Baldus, M., Jackle, H., Eimer, S., Schulz, J. B., Griesinger, C., and Zweckstetter, M. (2009) Pre-fibrillar alpha-synuclein variants with impaired beta-structure increase neurotoxicity in Parkinson's disease models EMBO J. 28, 3256-3268
12. Hartley, D. M., Walsh, D. M., Ye, C. P., Diehl, T., Vasquez, S., Vassilev, P. M., Teplow, D. B., and Selkoe, D. J. (1999) Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons J. Neurosci. 19, 8876-8884 (Pubitemid 30226709)
13. Anguiano, M., Nowak, R. J., and Lansbury, P. T., Jr. (2002) Protofibrillar islet amyloid polypeptide permeabilizes synthetic vesicles by a pore-like mechanism that may be relevant to type II diabetes Biochemistry 41, 11338-11343
14. Uversky, V. N. (2010) Mysterious oligomerization of the amyloidogenic proteins FEBS J. 277, 2940-2953
15. El-Agnaf, O. M. A., Salem, S. A., Paleologou, K. E., Curran, M. D., Gibson, M. J., Court, J. A., Schlossmacher, M. G., and Allsop, D. (2006) Detection of oligomeric forms of alpha-synuclein protein in human plasma as a potential biomarker for Parkinson's disease FASEB J. 20, 419-425 (Pubitemid 44933318)
16. Georganopoulou, D. G., Chang, L., Nam, J. M., Thaxton, C. S., Mufson, E. J., Klein, W. L., and Mirkin, C. A. (2005) Nanoparticle-based detection in cerebral spinal fluid of a soluble pathogenic biomarker for Alzheimer's disease Proc. Natl. Acad. Sci. U.S.A. 102, 2273-2276 (Pubitemid 40279365)
17. Xia, W., Yang, T., Shankar, G., Smith, I. M., Shen, Y., Walsh, D. M., and Selkoe, D. J. (2009) A specific enzyme-linked immunosorbent assay for measuring beta-amyloid protein oligomers in human plasma and brain tissue of patients with Alzheimer disease Arch. Neurol. 66, 190-199
18. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., Regan, C. M., Walsh, D. M., Sabatini, B. L., and Selkoe, D. J. (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nature Med. 14, 837-842
19. Pitschke, M., Prior, R., Haupt, M., and Riesner, D. (1998) Detection of single amyloid beta-protein aggregates in the cerebrospinal fluid of Alzheimer's patients by fluorescence correlation spectroscopy Nature Med. 4, 832-834 (Pubitemid 28331026)
20. Tomic, J. L., Pensalfini, A., Head, E., and Glabe, C. G. (2009) Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction Neurobiol. Dis. 35, 352-358
21. Du, D., Murray, A. N., Cohen, E., Kim, H. E., Simkovsky, R., Dillin, A., and Kelly, J. W. A Kinetic Aggregation Assay Allowing Selective and Sensitive Amyloid-beta Quantification in Cells and Tissues. Biochemistry.
22. Lau, A. L., Yam, A. Y., Michelitsch, M. M., Wang, X., Gao, C., Goodson, R. J., Shimizu, R., Timoteo, G., Hall, J., Medina-Selby, A., Coit, D., McCoin, C., Phelps, B., Wu, P., Hu, C., Chien, D., and Peretz, D. (2007) Characterization of prion protein (PrP)-derived peptides that discriminate full-length PrPSc from PrPC Proc. Natl. Acad. Sci. U.S.A. 104, 11551-11556 (Pubitemid 47175050)
23. Gao, C. M., Yam, A. Y., Wang, X., Magdangal, E., Salisbury, C. M., Peretz, D., Zuckermann, R. N., Connolly, M. D., Hansson, O., Minthon, L., Zetterberg, H., Blennow, K., Fedynyshyn, J. P., and Allauzen, S. (2010) Aβ40 oligomers identified as a potential biomarker for the diagnosis of Alzheimer's Disease PLoS One 5, e15725
24. Greenwald, J. and Riek, R. (2010) Biology of amyloid: structure, function, and regulation Structure 18, 1244-1260
25. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. O., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers Nature 447, 453-457 (Pubitemid 46816731)
26. Culf, A. S. and Ouellette, R. J. Solid-phase synthesis of N-substituted glycine oligomers (alpha-peptoids) and derivatives. Molecules 15, 5282-5335.
27. Figliozzi, G. M., Goldsmith, R., Ng, S. C., Banville, S. C., and Zuckermann, R. N. (1996) Synthesis of N-substituted glycine peptoid libraries Methods Enzymol. 267, 437-447 (Pubitemid 26159237)
28. Stine, W. B., Jr., Dahlgren, K. N., Krafft, G. A., and LaDu, M. J. (2003) In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis J. Biol. Chem. 278, 11612-11622 (Pubitemid 36792723)
29. Barghorn, S., Nimmrich, V., Striebinger, A., Krantz, C., Keller, P., Janson, B., Bahr, M., Schmidt, M., Bitner, R. S., Harlan, J., Barlow, E., Ebert, U., and Hillen, H. (2005) Globular amyloid beta-peptide oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease J. Neurochem. 95, 834-847 (Pubitemid 41567174)
30. Yu, L., Edalji, R., Harlan, J. E., Holzman, T. F., Lopez, A. P., Labkovsky, B., Hillen, H., Barghorn, S., Ebert, U., Richardson, P. L., Miesbauer, L., Solomon, L., Bartley, D., Walter, K., Johnson, R. W., Hajduk, P. J., and Olejniczak, E. T. (2009) Structural characterization of a soluble amyloid beta-peptide oligomer Biochemistry 48, 1870-1877
31. Hepler, R. W., Grimm, K. M., Nahas, D. D., Breese, R., Dodson, E. C., Acton, P., Keller, P. M., Yeager, M., Wang, H., Shughrue, P., Kinney, G., and Joyce, J. G. (2006) Solution state characterization of amyloid beta-derived diffusible ligands Biochemistry 45, 15157-15167 (Pubitemid 46032442)
32. Noguchi, A., Matsumura, S., Dezawa, M., Tada, M., Yanazawa, M., Ito, A., Akioka, M., Kikuchi, S., Sato, M., Ideno, S., Noda, M., Fukunari, A., Muramatsu, S., Itokazu, Y., Sato, K., Takahashi, H., Teplow, D. B., Nabeshima, Y., Kakita, A., Imahori, K., and Hoshi, M. (2009) Isolation and characterization of patient-derived, toxic, high mass amyloid beta-protein (Abeta) assembly from Alzheimer disease brains J. Biol. Chem. 284, 32895-32905
33. Wood, S. J., Wypych, J., Steavenson, S., Louis, J. C., Citron, M., and Biere, A. L. (1999) alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease J. Biol. Chem. 274, 19509-19512
34. Green, J. D., Goldsbury, C., Kistler, J., Cooper, G. J., and Aebi, U. (2004) Human amylin oligomer growth and fibril elongation define two distinct phases in amyloid formation J. Biol. Chem. 279, 12206-12212 (Pubitemid 38445785)
35. Devlin, G. L., Chow, M. K., Howlett, G. J., and Bottomley, S. P. (2002) Acid Denaturation of alpha1-antitrypsin: characterization of a novel mechanism of serpin polymerization J. Mol. Biol. 324, 859-870 (Pubitemid 36044118)
36. Miller, S. M., Simon, R. J., Ng, S., Zuckermann, R. N., Kerr, J. M., and Moos, W. H. (1995) Comparison of the Proteolytic Susceptibilities of Homologous L-Amino-Acid, D-Amino-Acid, and N-Substituted Glycine Peptide and Peptoid Oligomers Drug Dev. Res. 35, 20-32
37. Nguyen, J. T., Turck, C. W., Cohen, F. E., Zuckermann, R. N., and Lim, W. A. (1998) Exploiting the basis of proline recognition by SH3 and WW domains: design of N-substituted inhibitors Science 282, 2088-2092 (Pubitemid 29001266)
38. Goldschmidt, L., Teng, P. K., Riek, R., and Eisenberg, D. (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils Proc. Natl. Acad. Sci. U.S.A. 107, 3487-3492
39. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366 (Pubitemid 44118036)
40. Buhimschi, I. A., Zhao, G., Funai, E. F., Harris, N., Sasson, I. E., Bernstein, I. M., Saade, G. R., and Buhimschi, C. S. (2008) Proteomic profiling of urine identifies specific fragments of SERPINA1 and albumin as biomarkers of preeclampsia Am. J. Obstet. Gynecol. 199, 551 e1-16
41. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F., and Caughey, B. (2005) The most infectious prion protein particles Nature 437, 257-261 (Pubitemid 41294488)
42. 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
43. 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 beta -amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747 (Pubitemid 36034043)
44. Masuda, Y., Irie, K., Murakami, K., Ohigashi, H., Ohashi, R., Takegoshi, K., Shimizu, T., and Shirasawa, T. (2005) Verification of the turn at positions 22 and 23 of the beta-amyloid fibrils with Italian mutation using solid-state NMR Bioorg. Med. Chem. 13, 6803-6809 (Pubitemid 41571226)
45. Sigurdson, C. J., Nilsson, K. P., Hornemann, S., Manco, G., Polymenidou, M., Schwarz, P., Leclerc, M., Hammarstrom, P., Wuthrich, K., and Aguzzi, A. (2007) Prion strain discrimination using luminescent conjugated polymers Nature Methods 4, 1023-1030 (Pubitemid 350201774)
46. Kayed, R., Head, E., Sarsoza, F., Saing, T., Cotman, C. W., Necula, M., Margol, L., Wu, J., Breydo, L., Thompson, J. L., Rasool, S., Gurlo, T., Butler, P., and Glabe, C. G. (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers Mol. Neurodegener. 2, 18
47. Lambert, M. P., Velasco, P. T., Chang, L., Viola, K. L., Fernandez, S., Lacor, P. N., Khuon, D., Gong, Y., Bigio, E. H., Shaw, P., De Felice, F. G., Krafft, G. A., and Klein, W. L. (2007) Monoclonal antibodies that target pathological assemblies of Abeta J. Neurochem. 100, 23-35 (Pubitemid 46085837)
48. Fukumoto, H., Tokuda, T., Kasai, T., Ishigami, N., Hidaka, H., Kondo, M., Allsop, D., and Nakagawa, M. (2010) High-molecular-weight beta-amyloid oligomers are elevated in cerebrospinal fluid of Alzheimer patients FASEB J. 24, 2716-2726
49. Rahimi, F., Murakami, K., Summers, J. L., Chen, C. H., and Bitan, G. (2009) RNA aptamers generated against oligomeric Abeta40 recognize common amyloid aptatopes with low specificity but high sensitivity PLoS One 4, e7694
50. Bunka, D. H., Mantle, B. J., Morten, I. J., Tennent, G. A., Radford, S. E., and Stockley, P. G. (2007) Production and characterization of RNA aptamers specific for amyloid fibril epitopes J. Biol. Chem. 282, 34500-34509 (Pubitemid 350159445)
51. Yoshiike, Y., Minai, R., Matsuo, Y., Chen, Y. R., Kimura, T., and Takashima, A. (2008) Amyloid oligomer conformation in a group of natively folded proteins PLoS One 3, e3235
52. Masuda, M., Hasegawa, M., Nonaka, T., Oikawa, T., Yonetani, M., Yamaguchi, Y., Kato, K., Hisanaga, S., and Goedert, M. (2009) Inhibition of alpha-synuclein fibril assembly by small molecules: analysis using epitope-specific antibodies FEBS Lett. 583, 787-791
53. Sehlin, D., Sollvander, S., Paulie, S., Brundin, R., Ingelsson, M., Lannfelt, L., Pettersson, F. E., and Englund, H. (2010) Interference from Heterophilic Antibodies in Amyloid-beta Oligomer ELISAs J. Alzheimers Dis. 21, 1295-1301
54. Gunzburg, M. J., Perugini, M. A., and Howlett, G. J. (2007) Structural basis for the recognition and cross-linking of amyloid fibrils by human apolipoprotein E J. Biol. Chem. 282, 35831-35841 (Pubitemid 350277107)
55. Thompson, D., Pepys, M. B., Tickle, I., and Wood, S. (2002) The structures of crystalline complexes of human serum amyloid P component with its carbohydrate ligand, the cyclic pyruvate acetal of galactose J. Mol. Biol. 320, 1081-1086 (Pubitemid 34808825)