Insulin-degrading enzyme prevents α-synuclein fibril formation in a nonproteolytical manner

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Sharma, Sandeep K ^a   Chorell, Erik ^a   Steneberg, Pär ^b   Vernersson Lindahl, Emma ^b   Edlund, Helena ^b   Wittung Stafshede, Pernilla ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; INSULINASE; THIAZOLE DERIVATIVE; THIOFLAVINE;

ATOMIC FORCE MICROSCOPY; CALORIMETRY; CHEMISTRY; PROCEDURES; PROTEIN MULTIMERIZATION;

ALPHA-SYNUCLEIN; AMYLOID; CALORIMETRY; INSULYSIN; MICROSCOPY, ATOMIC FORCE; PROTEIN MULTIMERIZATION; THIAZOLES;

EID: 84938523810     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12531     Document Type: Article

References (44)

1. Brender, J. R., Salamekh, S. & Ramamoorthy, A. Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective. Acc Chem Res 45, 454-462, doi: 10.1021/ar200189b (2012).
2. DeToma, A. S., Salamekh, S., Ramamoorthy, A. & Lim, M. H. Misfolded proteins in Alzheimer's disease and type II diabetes. Chem Soc Rev 41, 608-621, doi: 10.1039/c1cs15112f (2012).
3. Kotler, S. A., Walsh, P., Brender, J. R. & Ramamoorthy, A. Differences between amyloid-beta aggregation in solution and on the membrane: insights into elucidation of the mechanistic details of Alzheimer's disease. Chem Soc Rev 43, 6692-6700, doi: 10.1039/c3cs60431d (2014).
4. Patel, H. R., Pithadia, A. S., Brender, J. R., Fierke, C. A. & Ramamoorthy, A. In Search of Aggregation Pathways of IAPP and Other Amyloidogenic Proteins: Finding Answers through NMR Spectroscopy. J. Phys. Chem. Lett. 5, 1864-1870, doi: 10.1021/jz5001775 (2014).
5. Galvin, J. E. et al. Pathobiology of the Lewy body. Adv Neurol 80, 313-324 (1999).
6. Winner, B. et al. In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci USA 108, 4194-4199.
7. Kirschner, R. J. & Goldberg, A. L. A high molecular weight metalloendoprotease from the cytosol of mammalian cells. J Biol Chem 258, 967-976 (1983).
8. Duckworth, W. C., Bennett, R. G. & Hamel, F. G. Insulin degradation: progress and potential. Endocr Rev 19, 608-624, doi: 10.1210/edrv.19.5.0349 (1998).
9. Diabetes Genetics Initiative of Broad Institute of, H. et al. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316, 1331-1336, doi: 10.1126/science.1142358 (2007).
10. Scott, L. J. et al. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316, 1341-1345, doi: 10.1126/science.1142382 (2007).
11. Steneberg, P. et al. The type 2 diabetes-associated gene ide is required for insulin secretion and suppression of alpha-synuclein levels in beta-cells. Diabetes 62, 2004-2014, doi: 10.2337/db12-1045 (2013).
12. Farris, W. et al. Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA 100, 4162-4167, doi: 10.1073/pnas.0230450100 (2003).
13. de Tullio, M. B., Morelli, L. & Castano, E. M. The irreversible binding of amyloid peptide substrates to insulin-degrading enzyme: a biological perspective. Prion 2, 51-56 (2008).
14. Llovera, R. E. et al. The catalytic domain of insulin-degrading enzyme forms a denaturant-resistant complex with amyloid beta peptide: implications for Alzheimer disease pathogenesis. J Biol Chem 283, 17039-17048, doi: 10.1074/jbc.M706316200 (2008).
15. Eliezer, D., Kutluay, E., Bussell, R., Jr. & Browne, G. Conformational properties of alpha-synuclein in its free and lipid-associated states. J Mol Biol 307, 1061-1073 (2001).
16. Crowther, R. A., Jakes, R., Spillantini, M. G. & Goedert, M. Synthetic filaments assembled from C-terminally truncated alphasynuclein. FEBS Lett 436, 309-312 (1998).
17. Kessler, J. C., Rochet, J. C. & Lansbury, P. T., Jr. The N-terminal repeat domain of alpha-synuclein inhibits beta-sheet and amyloid fibril formation. Biochemistry 42, 672-678, doi: 10.1021/bi020429y (2003).
18. Shen, Y., Joachimiak, A., Rosner, M. R. & Tang, W. J. Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 443, 870-874, doi: 10.1038/nature05143 (2006).
19. Noinaj, N. et al. Identification of the allosteric regulatory site of insulysin. PLoS One 6, e20864, doi: 10.1371/journal.pone.0020864 (2011).
20. McCord, L. A. et al. Conformational states and recognition of amyloidogenic peptides of human insulin-degrading enzyme. Proc Natl Acad Sci USA 110, 13827-13832, doi: 10.1073/pnas.1304575110 (2013).
21. Im, H. et al. Structure of substrate-free human insulin-degrading enzyme (IDE) and biophysical analysis of ATP-induced conformational switch of IDE. J Biol Chem 282, 25453-25463, doi: 10.1074/jbc.M701590200 (2007).
22. Guo, Q., Manolopoulou, M., Bian, Y., Schilling, A. B. & Tang, W. J. Molecular basis for the recognition and cleavages of IGF-II, TGF-alpha, and amylin by human insulin-degrading enzyme. J Mol Biol 395, 430-443, doi: 10.1016/j.jmb.2009.10.072 (2010).
23. Malito, E. et al. Molecular bases for the recognition of short peptide substrates and cysteine-directed modifications of human insulin-degrading enzyme. Biochemistry 47, 12822-12834, doi: 10.1021/bi801192h (2008).
24. Naiki, H., Higuchi, K., Hosokawa, M. & Takeda, T. Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1. Anal Biochem 177, 244-249 (1989).
25. Giehm, L., Svergun, D. I., Otzen, D. E. & Vestergaard, B. Low-resolution structure of a vesicle disrupting α-synuclein oligomer that accumulates during fibrillation. Proc Natl Acad Sci USA 108, 3246-3251, doi: 10.1073/pnas.1013225108 (2011).
26. Ahmad, A. DnaK/DnaJ/GrpE of Hsp70 system have differing effects on alpha-synuclein fibrillation involved in Parkinson's disease. Int J Biol Macromol 46, 275-279, doi: 10.1016/j.ijbiomac.2009.12.017 (2010).
27. Horvath, I. et al. Mechanisms of protein oligomerization: inhibitor of functional amyloids templates alpha-synuclein fibrillation. J Am Chem Soc 134, 3439-3444 (2012).
28. Johnson, G. D. & Ahn, K. Development of an internally quenched fluorescent substrate selective for endothelin-converting enzyme-1. Anal Biochem 286, 112-118, doi: 10.1006/abio.2000.4772 (2000).
29. Song, E. S., Rodgers, D. W. & Hersh, L. B. A monomeric variant of insulin degrading enzyme (IDE) loses its regulatory properties. PLoS One 5, e9719, doi: 10.1371/journal.pone.0009719 (2010).
30. Algamal, M., Milojevic, J., Jafari, N., Zhang, W. & Melacini, G. Mapping the interactions between the Alzheimer's Abeta-peptide and human serum albumin beyond domain resolution. Biophys J 105, 1700-1709, doi: 10.1016/j.bpj.2013.08.025 (2013).
31. Milojevic, J., Costa, M., Ortiz, A. M., Jorquera, J. I. & Melacini, G. In vitro amyloid-beta binding and inhibition of amyloid-beta self-association by therapeutic albumin. J Alzheimers Dis 38, 753-765, doi: 10.3233/JAD-131169 (2014).
32. Milojevic, J., Esposito, V., Das, R. & Melacini, G. Understanding the molecular basis for the inhibition of the Alzheimer's Abetapeptide oligomerization by human serum albumin using saturation transfer difference and off-resonance relaxation NMR spectroscopy. J Am Chem Soc 129, 4282-4290, doi: 10.1021/ja067367+ (2007).
33. Milojevic, J. & Melacini, G. Stoichiometry and affinity of the human serum albumin-Alzheimer's Abeta peptide interactions. Biophys J 100, 183-192, doi: 10.1016/j.bpj.2010.11.037 (2011).
34. Milojevic, J., Raditsis, A. & Melacini, G. Human serum albumin inhibits Abeta fibrillization through a "monomer-competitor" mechanism. Biophys J 97, 2585-2594, doi: 10.1016/j.bpj.2009.08.028 (2009).
35. Raditsis, A. V., Milojevic, J. & Melacini, G. Abeta association inhibition by transferrin. Biophys J 105, 473-480, doi: 10.1016/j. bpj.2013.03.065 (2013).
36. de Tullio, M. B. et al. Proteolytically inactive insulin-degrading enzyme inhibits amyloid formation yielding non-neurotoxic abeta peptide aggregates. PLoS One 8, e59113, doi: 10.1371/journal.pone.0059113 (2013).
37. Cho, M. K., Kim, H. Y., Fernandez, C. O., Becker, S. & Zweckstetter, M. Conserved core of amyloid fibrils of wild type and A30P mutant alpha-synuclein. Protein Sci 20, 387-395, doi: 10.1002/pro.570 (2011).
38. Runyan, K., Duckworth, W. C., Kitabchi, A. E. & Huff, G. The effect of age on insulin-degrading activity in rat tissue. Diabetes 28, 324-325 (1979).
39. Han, H., Weinreb, P. H. & Lansbury, P. T., Jr. The core Alzheimer's peptide NAC forms amyloid fibrils which seed and are seeded by beta-amyloid: is NAC a common trigger or target in neurodegenerative disease? Chem Biol 2, 163-169 (1995).
40. Yoshimoto, M. et al. NACP, the precursor protein of the non-amyloid beta/A4 protein (A beta) component of Alzheimer disease amyloid, binds A beta and stimulates A beta aggregation. Proc Natl Acad Sci USA 92, 9141-9145 (1995).
41. Culvenor, J. G. et al. Non-Abeta component of Alzheimer's disease amyloid (NAC) revisited. NAC and alpha-synuclein are not associated with Abeta amyloid. Am J Pathol 155, 1173-1181 (1999).
42. Hashimoto, M., Takenouchi, T., Mallory, M., Masliah, E. & Takeda, A. The role of NAC in amyloidogenesis in Alzheimer's disease. Am J Pathol 156, 734-736 (2000).
43. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293 (1995).
44. Helgstrand, M., Kraulis, P., Allard, P. & Hard, T. Ansig for Windows: an interactive computer program for semiautomatic assignment of protein NMR spectra. J Biomol NMR 18, 329-336 (2000).