Proteolytically Inactive Insulin-Degrading Enzyme Inhibits Amyloid Formation Yielding Non-Neurotoxic Aβ Peptide Aggregates

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  de Tullio, Matias B ^a   Castelletto, Valeria ^b   Hamley, Ian W ^b   Martino Adami, Pamela V ^a   Morelli, Laura ^a   Castaño, Eduardo M ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AMYLOID; AMYLOID BETA PROTEIN[1-42]; CHAPERONE; GLUTAMIC ACID; GLUTAMINE; INSULIN; INSULIN RECEPTOR; RECOMBINANT ENZYME; RECOMBINANT INSULIN DEGRADING ENZYME; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENZYMATIC DEGRADATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INACTIVATION; ENZYME MECHANISM; IN VITRO STUDY; IN VIVO STUDY; LIGHT SCATTERING; MOLECULAR RECOGNITION; MUTANT; NEUROTOXICITY; NONHUMAN; PH; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; RAT; SOLUBILITY; STRUCTURE ANALYSIS;

AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CIRCULAR DICHROISM; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; INSULIN; INSULYSIN; KINETICS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR CHAPERONES; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; RATS; RECOMBINANT PROTEINS;

MAMMALIA;

EID: 84876102518     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059113     Document Type: Article

References (70)

1. Jarrett JT, Lansbury PT Jr, (1992) Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31: 12345-12352.
2. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, et al. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci U S A 100: 330-335.
3. Bernstein SL, Dupuis NF, Lazo ND, Wyttenbach T, Condron MM, et al. (2009) Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat Chem 1: 326-331.
4. Wang YQ, Buell AK, Wang XY, Welland ME, Dobson CM, et al. (2011) Relationship between prion propensity and the rates of individual molecular steps of fibril assembly. J Biol Chem 286: 12101-12107.
5. Necula M, Kayed R, Milton S, Glabe CG, (2007) Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282: 10311-10324.
6. Kumar A, Bullard RL, Patel P, Paslay LC, Singh D, et al. (2011) Non-esterified fatty acids generate distinct low-molecular weight amyloid-beta (Abeta42) oligomers along pathway different from fibril formation. PLoS One 6: e18759.
7. Kirkitadze MD, Bitan G, Teplow DB, (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies. J Neurosci Res 69: 567-577.
8. Cheng IH, Scearce-Levie K, Legleiter J, Palop JJ, Gerstein H, et al. (2007) Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models. J Biol Chem 282: 23818-23828.
9. Bolognesi B, Kumita JR, Barros TP, Esbjorner EK, Luheshi LM, et al. (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem Biol 5: 735-740.
10. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, et al. (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4: e6.
11. Konarkowska B, Aitken JF, Kistler J, Zhang S, Cooper GJ, (2006) The aggregation potential of human amylin determines its cytotoxicity towards islet beta-cells. FEBS J 273: 3614-3624.
12. Tsika E, Moysidou M, Guo J, Cushman M, Gannon P, et al. (2010) Distinct region-specific alpha-synuclein oligomers in A53T transgenic mice: implications for neurodegeneration. J Neurosci 30: 3409-3418.
13. Vidal R, Frangione B, Rostagno A, Mead S, Revesz T, et al. (1999) A stop-codon mutation in the BRI gene associated with familial British dementia. Nature 399: 776-781.
14. Vidal R, Revesz T, Rostagno A, Kim E, Holton JL, et al. (2000) A decamer duplication in the 3′ region of the BRI gene originates an amyloid peptide that is associated with dementia in a Danish kindred. Proc Natl Acad Sci U S A 97: 4920-4925.
15. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95: 6448-6453.
16. Gau JT, Steinhilb ML, Kao TC, D'Amato CJ, Gaut JR, et al. (2002) Stable beta-secretase activity and presynaptic cholinergic markers during progressive central nervous system amyloidogenesis in Tg2576 mice. Am J Pathol 160: 731-738.
17. Kuo YM, Beach TG, Sue LI, Scott S, Layne KJ, et al. (2001) The evolution of A beta peptide burden in the APP23 transgenic mice: implications for A beta deposition in Alzheimer disease. Mol Med 7: 609-618.
18. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, et al. (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 4: 887-893.
19. Van Nostrand WE, Melchor JP, Cho HS, Greenberg SM, Rebeck GW, (2001) Pathogenic effects of D23N Iowa mutant amyloid beta-protein. J Biol Chem 276: 32860-32866.
20. Perez RG, Soriano S, Hayes JD, Ostaszewski B, Xia W, et al. (1999) Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42. J Biol Chem 274: 18851-18856.
21. Soriano S, Chyung AS, Chen X, Stokin GB, Lee VM, et al. (1999) Expression of beta-amyloid precursor protein-CD3gamma chimeras to demonstrate the selective generation of amyloid beta(1-40) and amyloid beta(1-42) peptides within secretory and endocytic compartments. J Biol Chem 274: 32295-32300.
22. Grbovic OM, Mathews PM, Jiang Y, Schmidt SD, Dinakar R, et al. (2003) Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Abeta production. J Biol Chem 278: 31261-31268.
23. Haass C, Schlossmacher MG, Hung AY, Vigo-Pelfrey C, Mellon A, et al. (1992) Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 359: 322-325.
24. Friedrich RP, Tepper K, Ronicke R, Soom M, Westermann M, et al. (2010) Mechanism of amyloid plaque formation suggests an intracellular basis of Abeta pathogenicity. Proc Natl Acad Sci U S A 107: 1942-1947.
25. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, et al. (2002) Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 161: 1869-1879.
26. Oakley H, Cole SL, Logan S, Maus E, Shao P, et al. (2006) Intraneuronal beta-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.
27. Eckman EA, Watson M, Marlow L, Sambamurti K, Eckman CB, (2003) Alzheimer's disease beta-amyloid peptide is increased in mice deficient in endothelin-converting enzyme. J Biol Chem 278: 2081-2084.
28. Miller BC, Eckman EA, Sambamurti K, Dobbs N, Chow KM, et al. (2003) Amyloid-beta peptide levels in brain are inversely correlated with insulysin activity levels in vivo. Proc Natl Acad Sci U S A 100: 6221-6226.
29. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, et al. (2001) Metabolic regulation of brain Abeta by neprilysin. Science 292: 1550-1552.
30. Evans CG, Wisen S, Gestwicki JE, (2006) Heat shock proteins 70 and 90 inhibit early stages of amyloid beta-(1-42) aggregation in vitro. J Biol Chem 281: 33182-33191.
31. Lee S, Carson K, Rice-Ficht A, Good T, (2006) Small heat shock proteins differentially affect Abeta aggregation and toxicity. Biochem Biophys Res Commun 347: 527-533.
32. Humphreys DT, Carver JA, Easterbrook-Smith SB, Wilson MR, (1999) Clusterin has chaperone-like activity similar to that of small heat shock proteins. J Biol Chem 274: 6875-6881.
33. Yerbury JJ, Rybchyn MS, Easterbrook-Smith SB, Henriques C, Wilson MR, (2005) The acute phase protein haptoglobin is a mammalian extracellular chaperone with an action similar to clusterin. Biochemistry 44: 10914-10925.
34. French K, Yerbury JJ, Wilson MR, (2008) Protease activation of alpha2-macroglobulin modulates a chaperone-like action with broad specificity. Biochemistry 47: 1176-1185.
35. Yerbury JJ, Kumita JR, Meehan S, Dobson CM, Wilson MR, (2009) alpha2-Macroglobulin and haptoglobin suppress amyloid formation by interacting with prefibrillar protein species. J Biol Chem 284: 4246-4254.
36. Yerbury JJ, Poon S, Meehan S, Thompson B, Kumita JR, et al. (2007) The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures. FASEB J 21: 2312-2322.
37. Bruinsma IB, de Jager M, Carrano A, Versleijen AA, Veerhuis R, et al. (2011) Small heat shock proteins induce a cerebral inflammatory reaction. J Neurosci 31: 11992-12000.
38. Calero M, Rostagno A, Frangione B, Ghiso J, (2005) Clusterin and Alzheimer's disease. Subcell Biochem 38: 273-298.
39. Liao L, Cheng D, Wang J, Duong DM, Losik TG, et al. (2004) Proteomic characterization of postmortem amyloid plaques isolated by laser capture microdissection. J Biol Chem 279: 37061-37068.
40. Martin-Rehrmann MD, Hoe HS, Capuani EM, Rebeck GW, (2005) Association of apolipoprotein J-positive beta-amyloid plaques with dystrophic neurites in Alzheimer's disease brain. Neurotox Res 7: 231-242.
41. Farris W, Mansourian S, Chang Y, Lindsley L, Eckman EA, et al. (2003) 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 U S A 100: 4162-4167.
42. Fernandez-Gamba A, Leal MC, Morelli L, Castaño EM, (2009) Insulin-degrading enzyme: structure-function relationship and its possible roles in health and disease. Curr Pharm Des 15: 3644-3655.
43. de Tullio MB, Morelli L, Castaño EM, (2008) The irreversible binding of amyloid peptide substrates to insulin-degrading enzyme: a biological perspective. Prion 2: 51-56.
44. Llovera RE, de Tullio M, Alonso LG, Leissring MA, Kaufman SB, et al. (2008) 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.
45. Hilbich C, Kisters-Woike B, Reed J, Masters CL, Beyreuther K, (1992) Substitutions of hydrophobic amino acids reduce the amyloidogenicity of Alzheimer's disease beta A4 peptides. J Mol Biol 228: 460-473.
46. Shen Y, Joachimiak A, Rosner MR, Tang WJ, (2006) Structures of human insulin-degrading enzyme reveal a new substrate recognition mechanism. Nature 443: 870-874.
47. Manolopoulou M, Guo Q, Malito E, Schilling AB, Tang WJ, (2009) Molecular basis of catalytic chamber-assisted unfolding and cleavage of human insulin by human insulin-degrading enzyme. J Biol Chem 284: 14177-14188.
48. Bulloj A, Leal MC, Surace EI, Zhang X, Xu H, et al. (2008) Detergent resistant membrane-associated IDE in brain tissue and cultured cells: Relevance to Abeta and insulin degradation. Mol Neurodegener 3: 22.
49. Bulloj A, Leal MC, Xu H, Castaño EM, Morelli L, (2010) Insulin-degrading enzyme sorting in exosomes: a secretory pathway for a key brain amyloid-beta degrading protease. J Alzheimers Dis 19: 79-95.
50. Morelli L, Llovera RE, Mathov I, Lue LF, Frangione B, et al. (2004) Insulin-degrading enzyme in brain microvessels: proteolysis of amyloid beta vasculotropic variants and reduced activity in cerebral amyloid angiopathy. J Biol Chem 279: 56004-56013.
51. Roher AE, Esh CL, Kokjohn TA, Castaño EM, Van Vickle GD, et al. (2009) Amyloid beta peptides in human plasma and tissues and their significance for Alzheimer's disease. Alzheimers Dement 5: 18-29.
52. Im H, Manolopoulou M, Malito E, Shen Y, Zhao J, et al. (2007) 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.
53. Noinaj N, Song ES, Bhasin S, Alper BJ, Schmidt WK, et al. (2012) Anion activation site of insulin-degrading enzyme. J Biol Chem 287: 48-57.
54. Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, et al. (2006) Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci U S A 103: 11172-11177.
55. Arimon M, Grimminger V, Sanz F, Lashuel HA, (2008) Hsp104 targets multiple intermediates on the amyloid pathway and suppresses the seeding capacity of Abeta fibrils and protofibrils. J Mol Biol 384: 1157-1173.
56. Morelli L, Llovera RE, Alonso LG, Frangione B, de Prat-Gay G, et al. (2005) Insulin-degrading enzyme degrades amyloid peptides associated with British and Danish familial dementia. Biochem Biophys Res Commun 332: 808-816.
57. Song ES, Juliano MA, Juliano L, Hersh LB, (2003) Substrate activation of insulin-degrading enzyme (insulysin). A potential target for drug development. J Biol Chem 278: 49789-49794.
58. Schumann W, (1999) FtsH - a single-chain charonin? FEMS Microbiol Rev 23: 1-11.
59. Wang CC, Tsou CL, (1998) Enzymes as chaperones and chaperones as enzymes. FEBS Lett 425: 382-384.
60. Hulko M, Lupas AN, Martin J, (2007) Inherent chaperone-like activity of aspartic proteases reveals a distant evolutionary relation to double-psi barrel domains of AAA-ATPases. Protein Sci 16: 644-653.
61. Ding L, Becker AB, Suzuki A, Roth RA, (1992) Comparison of the enzymatic and biochemical properties of human insulin-degrading enzyme and Escherichia coli protease III. J Biol Chem 267: 2414-2420.
62. Shinall H, Song ES, Hersh LB, (2005) Susceptibility of amyloid beta peptide degrading enzymes to oxidative damage: a potential Alzheimer's disease spiral. Biochemistry 44: 15345-15350.
63. Cordes CM, Bennett RG, Siford GL, Hamel FG, (2011) Redox regulation of insulin degradation by insulin-degrading enzyme. PLoS One 6: e18138.
64. Farris W, Mansourian S, Leissring MA, Eckman EA, Bertram L, et al. (2004) Partial loss-of-function mutations in insulin-degrading enzyme that induce diabetes also impair degradation of amyloid beta-protein. Am J Pathol 164: 1425-1434.
65. Johnson KA, Bhushan S, Stahl A, Hallberg BM, Frohn A, et al. (2006) The closed structure of presequence protease PreP forms a unique 10,000 Angstroms3 chamber for proteolysis. EMBO J 25: 1977-1986.
66. Mzhavia N, Berman YL, Qian Y, Yan L, Devi LA, (1999) Cloning, expression, and characterization of human metalloprotease 1: a novel member of the pitrilysin family of metalloendoproteases. DNA Cell Biol 18: 369-380.
67. Chow KM, Gakh O, Payne IC, Juliano MA, Juliano L, et al. (2009) Mammalian pitrilysin: substrate specificity and mitochondrial targeting. Biochemistry 48: 2868-2877.
68. Falkevall A, Alikhani N, Bhushan S, Pavlov PF, Busch K, et al. (2006) Degradation of the amyloid beta-protein by the novel mitochondrial peptidasome, PreP. J Biol Chem 281: 29096-29104.
69. Caceres A, Banker GA, Binder L, (1986) Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci 6: 714-722.
70. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG, (2010) Improving bioscience research reporting: The ARRIVE Guidelines for Reporting Animal Research. PLoS Biol 8(6): e1000412.