Binding of amyloid peptides to domain-swapped dimers of other amyloid-forming proteins may prevent their neurotoxicity

BioEssays

Volumn 32, Issue 12, 2010, Pages 1020-1024

  Taler Verčič, Ajda ^a   Žerovnik, Eva ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

Amyloid beta; Chaperone; Cystatins; Domain swapped dimers; Stefin B tetramer

Indexed keywords

AMYLOID PROTEIN; CYSTATIN C; DIMER; OLIGOMER;

AMINO ACID SEQUENCE; ARTICLE; NEUROFILAMENT; NEUROTOXICITY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT;

AMYLOID; AMYLOID BETA-PEPTIDES; AMYLOIDOGENIC PROTEINS; CYSTATINS; HUMANS; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; NEURODEGENERATIVE DISEASES; NEURONS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 78649525302     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000079     Document Type: Article

References (50)

1. Sastre M, Calero M, Pawlik M, Mathews PM, et al. 2004. Binding of cystatin C to Alzheimer's amyloid beta inhibits in vitro amyloid fibril formation. Neurobiol Aging 25: 1033-43.
2. Skerget K, Taler-Vercic A, Bavdek A, Hodnik V, et al. 2010. Interaction between oligomers of stefin B and amyloid-beta in vitro and in cells. J Biol Chem 285: 3201-10.
3. Wilhelmus MM, de Waal RM, Verbeek MM. 2007. Heat shock proteins and amateur chaperones in amyloid-Beta accumulation and clearance in Alzheimer's disease. Mol Neurobiol 35: 203-16.
4. Rekas A, Adda CG, Andrew Aquilina J, Barnham KJ, et al. 2004. Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 340: 1167-83.
5. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, et al. 1999. Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J Biol Chem 274: 25945-52.
6. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, et al. 2002. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416: 535-9.
7. Hartley DM, Walsh DM, Ye CP, Diehl T, et al. 1999. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J Neurosci 19: 8876-84.
8. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, et al. 2005. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84.
9. Reed MN, Hofmeister JJ, Jungbauer L, Welzel AT, et al. 2009. Cognitive effects of cell-derived and synthetically derived Abeta oligomers. Neurobiol Aging in press. DOI: 10.1016/j.neurobiolaging.2009.11.00.
10. Demuro A, Parker I, Stutzmann GE. 2010. Calcium signaling and amyloid toxicity in Alzheimer disease. J Biol Chem 285: 12463-8.
11. Anderluh G, Gutierrez-Aguirre I, Rabzelj S, Ceru S, et al. 2005. Interaction of human stefin B in the prefibrillar oligomeric form with membranes. Correlation with cellular toxicity. FEBS J 272: 3042-51.
12. Maury CP. 2009. The emerging concept of functional amyloid. J Intern Med 265: 329-34.
13. Fowler DM, Koulov AV, Balch WE, Kelly JW. 2007. Functional amyloid-from bacteria to humans. Trends Biochem Sci 32: 217-24.
14. Taru H, Suzuki T. 2009. Regulation of the physiological function and metabolism of AbetaPP by AbetaPP binding proteins. J Alzheimers Dis 18: 253-65.
15. + current. Neurobiol Aging 27: 1673-83.
16. Soscia SJ, Kirby JE, Washicosky KJ, Tucker SM, et al. 2010. The Alzheimer's disease-associated amyloid beta-protein is an antimicrobial peptide. PLoS One 5: e9505.
17. Rabzelj S, Viero G, Gutierrez-Aguirre I, Turk V, et al. 2008. Interaction with model membranes and pore formation by human stefin B: studying the native and prefibrillar states. FEBS J 275: 2455-66.
18. Bennett MJ, Sawaya MR, Eisenberg D. 2006. Deposition diseases and 3D domain swapping. Structure 14: 811-24.
19. Sonnen AFP, Yu C, Evans EJ, Stuart DI, et al. 2010. Domain metastability: a molecular basis for immunoglobulin deposition? J Mol Biol 399: 207-13.
20. Wahlbom M, Wang X, Lindstrom V, Carlemalm E, et al. 2007. Fibrillogenic oligomers of human cystatin C are formed by propagated domain swapping. J Biol Chem 282: 18318-26.
21. Siddhanta U, Presta A, Fan B, Wolan D, et al. 1998. Domain swapping in inducible nitric-oxide synthase. Electron transfer occurs between flavin and heme groups located on adjacent subunits in the dimer. J Biol Chem 273: 18950-8.
22. Fanning AS, Lye MF, Anderson JM, Lavie A. 2007. Domain swapping within PDZ2 is responsible for dimerization of ZO proteins. J Biol Chem 282: 37710-6.
23. Ivanov D, Stone JR, Maki JL, Collins T, et al. 2005. Mammalian SCAN domain dimer is a domain-swapped homolog of the HIV capsid C-terminal domain. Mol Cell 17: 137-43.
24. Janowski R, Kozak M, Jankowska E, Grzonka Z, et al. 2001. Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nat Struct Biol 8: 316-20.
25. Jerala R, Zerovnik E. 1999. Accessing the global minimum conformation of stefin A dimer by annealing under partially denaturing conditions. J Mol Biol 291: 1079-89.
26. Staniforth RA, Giannini S, Higgins LD, Conroy MJ, et al. 2001. Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily. EMBO J 20: 4774-81.
27. Calero M, Pawlik M, Soto C, Castano EM, et al. 2001. Distinct properties of wild-type and the amyloidogenic human cystatin C variant of hereditary cerebral hemorrhage with amyloidosis, Icelandic type. J Neurochem 77: 628-37.
28. Jenko Kokalj S, Guncar G, Stern I, Morgan G, et al. 2007. Essential role of proline isomerization in stefin B tetramer formation. J Mol Biol 366: 1569-79.
29. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, et al. 2008. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-42.
30. Smith AM, Jahn TR, Ashcroft AE, Radford SE. 2006. Direct observation of oligomeric species formed in the early stages of amyloid fibril formation using electrospray ionisation mass spectrometry. J Mol Biol 364: 9-19.
31. Takahashi T, Yamashita H, Nakamura T, Nagano Y, et al. 2002. Tyrosine 125 of alpha-synuclein plays a critical role for dimerization following nitrative stress. Brain Res 938: 73-80.
32. Ceru S, Konjar S, Maher K, Repnik U, et al. 2010. Stefin B interacts with histones and cathepsin L in the nucleus. J Biol Chem 285: 10078-86.
33. Turk V, Stoka V, Turk D. 2008. Cystatins: biochemical and structural properties, and medical relevance. Front Biosci 13: 5406-20.
34. Rawlings ND, Barrett AJ, Bateman A. 2010. MEROPS: the peptidase database. Nucleic Acids Res 38: D227-33.
35. Kordis D, Turk V. 2009. Phylogenomic analysis of the cystatin superfamily in eukaryotes and prokaryotes. BMC Evol Biol 9: 266.
36. Joensuu T, Lehesjoki AE, Kopra O. 2008. Molecular background of EPM1-Unverricht-Lundborg disease. Epilepsia 49: 557-63.
37. Lehtinen MK, Tegelberg S, Schipper H, Su H, et al. 2009. Cystatin B deficiency sensitizes neurons to oxidative stress in progressive myoclonus epilepsy, EPM1. J Neurosci 29: 5910-5.
38. Di Giaimo R, Riccio M, Santi S, Galeotti C, et al. 2002. New insights into the molecular basis of progressive myoclonus epilepsy: a multiprotein complex with cystatin B. Hum Mol Genet 11: 2941-50.
39. Kopitar-Jerala N, Schweiger A, Myers RM, Turk V, et al. 2005. Sensitization of stefin B-deficient thymocytes towards staurosporin-induced apoptosis is independent of cysteine cathepsins. FEBS Lett 579: 2149-55.
40. Tizon B, Ribe EM, Mi W, Troy CM, et al. 2010. Cystatin C protects neuronal cells from amyloid-beta-induced toxicity. J Alzheimers Dis 19: 885-94.
41. Mi W, Jung SS, Yu H, Schmidt SD, et al. 2009. Complexes of amyloid-beta and cystatin C in the human central nervous system. J Alzheimers Dis 18: 273-80.
42. Mi W, Pawlik M, Sastre M, Jung SS, et al. 2007. Cystatin C inhibits amyloid-beta deposition in Alzheimer's disease mouse models. Nat Genet 39: 1440-2.
43. Tizon B, Sahoo S, Yu H, Gauthier S, et al. 2010. Induction of autophagy by cystatin C: a mechanism that protects murine primary cortical neurons and neuronal cell lines. PLoS One 5: e9819.
44. Pirttila TJ, Lukasiuk K, Hakansson K, Grubb A, et al. 2005. Cystatin C modulates neurodegeneration and neurogenesis following status epilepticus in mouse. Neurobiol Dis 20: 241-53.
45. D'Amato E, Kokaia Z, Nanobashvili A, Reeben M, et al. 2000. Seizures induce widespread upregulation of cystatin B, the gene mutated in progressive myoclonus epilepsy, in rat forebrain neurons. Eur J Neurosci 12: 1687-95.
46. Kaeser SA, Herzig MC, Coomaraswamy J, Kilger E, et al. 2007. Cystatin C modulates cerebral beta-amyloidosis. Nat Genet 39: 1437-9.
47. Perez RG, Squazzo SL, Koo EH. 1996. Enhanced release of amyloid beta-protein from codon 670/671 "Swedish" mutant beta-amyloid precursor protein occurs in both secretory and endocytic pathways. J Biol Chem 271: 9100-7.
48. Cipollini E, Riccio M, Di Giaimo R, Dal Piaz F, et al. 2008. Cystatin B and its EPM1 mutants are polymeric and aggregate prone in vivo Biochim Biophys Acta 1783: 312-22.
49. Ceru S, Layfield R, Zavasnik-Bergant T, Repnik U, et al. 2010. Intracellular aggregation of human stefin B: confocal and electron microscopy study. Biol Cell 102: 319-34.
50. Waudby CA, Knowles TP, Devlin GL, Skepper JN, et al. 2010. The interaction of alphaB-crystallin with mature alpha-synuclein amyloid fibrils inhibits their elongation. Biophys J 98: 843-51.