Imaging nanometer-sized α-synuclein aggregates by superresolution fluorescence localization microscopy

Biophysical Journal

Volumn 102, Issue 7, 2012, Pages 1598-1607

  Roberti, M Julia ^a,b   Fölling, Jonas ^b   Celej, M Soledad ^b   Bossi, Mariano ^b   Jovin, Thomas M ^b   Jares Erijman, Elizabeth A ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; NANOMATERIAL; RHODAMINE;

ARTICLE; CHEMISTRY; COLOR; FLUORESCENCE MICROSCOPY; HELA CELL; HUMAN; INTRACELLULAR SPACE; METABOLISM; METHODOLOGY; MOLECULAR IMAGING; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

ALPHA-SYNUCLEIN; COLOR; HELA CELLS; HUMANS; INTRACELLULAR SPACE; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; NANOSTRUCTURES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RHODAMINES;

EID: 84859391023     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.03.010     Document Type: Article

References (56)

1. C.P. Dohm, P. Kermer, and M. Bähr Aggregopathy in neurodegenerative diseases: mechanisms and therapeutic implication Neurodegener. Dis. 5 2008 321 338
2. V.N. Uversky α-Synuclein misfolding and neurodegenerative diseases Curr. Protein Pept. Sci. 9 2008 507 540
3. V.N. Uversky Mysterious oligomerization of the amyloidogenic proteins FEBS J. 277 2010 2940 2953
4. M. Stefani Protein aggregation diseases: toxicity of soluble prefibrillar aggregates and their clinical significance Methods Mol. Biol. 648 2010 25 41
5. A.M. Morris, M.A. Watzky, and R.G. Finke Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature Biochim. Biophys. Acta 1794 2009 375 397
6. K.A. Malkus, E. Tsika, and H. Ischiropoulos Oxidative modifications, mitochondrial dysfunction, and impaired protein degradation in Parkinson's disease: how neurons are lost in the Bermuda triangle Mol. Neurodegener. 4 2009 24
7. S. Seshadri, K.A. Oberg, and V.N. Uversky Mechanisms and consequences of protein aggregation: the role of folding intermediates Curr. Protein Pept. Sci. 10 2009 456 463
8. J.A. Fauerbach, and S. Yushchenko E.A. Jares-Erijman Supramolecular non-amyloid intermediates in the early stages of α-synuclein aggregation Biophys. J. 102 2012 1127 1136
9. M.E. van Raaij, I.M. Segers-Nolten, and V. Subramaniam Quantitative morphological analysis reveals ultrastructural diversity of amyloid fibrils from α-synuclein mutants Biophys. J. 91 2006 L96 L98
10. W. Hoyer, and D. Cherny T.M. Jovin Rapid self-assembly of α-synuclein observed by in situ atomic force microscopy J. Mol. Biol. 340 2004 127 139
11. K. Sweers, and K. van der Werf V. Subramaniam Nanomechanical properties of α-synuclein amyloid fibrils: a comparative study by nanoindentation, harmonic force microscopy, and Peakforce QNM Nanoscale Res. Lett. 6 2011 270
12. L.A. Munishkina, and A.L. Fink Fluorescence as a method to reveal structures and membrane-interactions of amyloidogenic proteins Biochim. Biophys. Acta 1768 2007 1862 1885
13. C.W. Bertoncini, and M.S. Celej Small molecule fluorescent probes for the detection of amyloid self-assembly in vitro and in vivo Curr. Protein Pept. Sci. 12 2011 205 220
14. M. Lindgren, and P. Hammarström Amyloid oligomers: spectroscopic characterization of amyloidogenic protein states FEBS J. 277 2010 1380 1388
15. G.S. Kaminski Schierle, and C.W. Bertoncini C.F. Kaminski A FRET sensor for non-invasive imaging of amyloid formation in vivo Chem. Phys. Chem. 12 2011 673 680
16. T.J. van Ham, and A. Esposito C.W. Bertoncini Towards multiparametric fluorescent imaging of amyloid formation: studies of a YFP model of α-synuclein aggregation J. Mol. Biol. 395 2010 627 642
17. M.J. Roberti, and C.W. Bertoncini T.M. Jovin Fluorescence imaging of amyloid formation in living cells by a functional, tetracysteine-tagged α-synuclein Nat. Methods 4 2007 345 351
18. S. Thirunavukkuarasu, E.A. Jares-Erijman, and T.M. Jovin Multiparametric fluorescence detection of early stages in the amyloid protein aggregation of pyrene-labeled α-synuclein J. Mol. Biol. 378 2008 1064 1073
19. M.J. Roberti, and M. Morgan E.A. Jares-Erijman Quantum dots as ultrasensitive nanoactuators and sensors of amyloid aggregation in live cells J. Am. Chem. Soc. 131 2009 8102 8107
20. D.A. Yushchenko, and J.A. Fauerbach T.M. Jovin Fluorescent ratiometric MFC probe sensitive to early stages of α-synuclein aggregation J. Am. Chem. Soc. 132 2010 7860 7861
21. M.J. Roberti, and L. Giordano E.A. Jares-Erijman FRET imaging by k(t)/k(f) Chem. Phys. Chem. 12 2011 563 566
22. M.J. Roberti, T.M. Jovin, and E.A. Jares-Erijman Confocal fluorescence anisotropy and FRAP imaging of α-synuclein amyloid aggregates in living cells PLoS ONE 6 2011 e23338
23. S.W. Hell Far-field optical nanoscopy Science 316 2007 1153 1158
24. S.W. Hell Microscopy and its focal switch Nat. Methods 6 2009 24 32
25. G. Patterson, and M. Davidson J. Lippincott-Schwartz Superresolution imaging using single-molecule localization Annu. Rev. Phys. Chem. 61 2010 345 367
26. E. Betzig, and G.H. Patterson H.F. Hess Imaging intracellular fluorescent proteins at nanometer resolution Science 313 2006 1642 1645
27. M.J. Rust, M. Bates, and X. Zhuang Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) Nat. Methods 3 2006 793 795
28. J. Fölling, and M. Bossi S.W. Hell Fluorescence nanoscopy by ground-state depletion and single-molecule return Nat. Methods 5 2008 943 945
29. M. Fernández-Suárez, and A.Y. Ting Fluorescent probes for super-resolution imaging in living cells Nat. Rev. Mol. Cell Biol. 9 2008 929 943
30. T.F. Outeiro, and P. Putcha P.J. McLean Formation of toxic oligomeric α-synuclein species in living cells PLoS One 3 2008 e1867
31. M.A. Thompson, and J.S. Biteen W.E. Moerner Molecules and methods for super-resolution imaging Methods Enzymol. 475 2010 27 59
32. J. Vogelsang, and T. Cordes P. Tinnefeld Intrinsically resolution enhancing probes for confocal microscopy Nano Lett. 10 2010 672 679
33. J. Fölling, and V. Belov S.W. Hell Photochromic rhodamines provide nanoscopy with optical sectioning Angew. Chem. Int. Ed. Engl. 46 2007 6266 6270
34. M. Bossi, and J. Fölling S.W. Hell Multicolor far-field fluorescence nanoscopy through isolated detection of distinct molecular species Nano Lett. 8 2008 2463 2468
35. V.N. Belov, and M.L. Bossi S.W. Hell Rhodamine spiroamides for multicolor single-molecule switching fluorescent nanoscopy Chemistry 15 2009 10762 10776
36. M. Bates, and B. Huang X. Zhuang Multicolor super-resolution imaging with photo-switchable fluorescent probes Science 317 2007 1749 1753
37. J. Vogelsang, and C. Steinhauer P. Tinnefeld Make them blink: probes for super-resolution microscopy Chem. Phys. Chem. 11 2010 2475 2490
38. A. Egner, and C. Geisler S.W. Hell Fluorescence nanoscopy in whole cells by asynchronous localization of photoswitching emitters Biophys. J. 93 2007 3285 3290
39. H. Heise, and W. Hoyer M. Baldus Molecular-level secondary structure, polymorphism, and dynamics of full-length α-synuclein fibrils studied by solid-state NMR Proc. Natl. Acad. Sci. USA 102 2005 15871 15876
40. C.O. Fernández, and W. Hoyer T.M. Jovin NMR of α-synuclein-polyamine complexes elucidates the mechanism and kinetics of induced aggregation EMBO J. 23 2004 2039 2046
41. T. Antony, and W. Hoyer V. Subramaniam Cellular polyamines promote the aggregation of α-synuclein J. Biol. Chem. 278 2003 3235 3240
42. M.F. Ahmad, and T. Ramakrishna ChM. Rao Fibrillogenic and non-fibrillogenic ensembles of SDS-bound human α-synuclein J. Mol. Biol. 364 2006 1061 1072
43. T. Ban, and K. Morigaki Y. Goto Real-time and single fibril observation of the formation of amyloid β spherulitic structures J. Biol. Chem. 281 2006 33677 33683
44. J. Fölling, and V. Belov S.W. Hell Fluorescence nanoscopy with optical sectioning by two-photon induced molecular switching using continuous-wave lasers Chem. Phys. Chem. 9 2008 321 326
45. C.B. Andersen, and H. Yagi C. Rischel Branching in amyloid fibril growth Biophys. J. 96 2009 1529 1536
46. T. Ban, K. Yamaguchi, and Y. Goto Direct observation of amyloid fibril growth, propagation, and adaptation Acc. Chem. Res. 39 2006 663 670
47. G.S. Kaminski Schierle, and S. van de Linde C.F. Kaminski In situ measurements of the formation and morphology of intracellular β-amyloid fibrils by super-resolution fluorescence imaging J. Am. Chem. Soc. 133 2011 12902 12905
48. W.C. Duim, and B. Chen W.E. Moerner Sub-diffraction imaging of huntingtin protein aggregates by fluorescence blink-microscopy and atomic force microscopy Chem. Phys. Chem. 12 2011 2387 2390
49. H.J. Lee, and S.J. Lee Characterization of cytoplasmic α-synuclein aggregates. Fibril formation is tightly linked to the inclusion-forming process in cells J. Biol. Chem. 277 2002 48976 48983
50. T.T. Ding, and S.J. Lee P.T. Lansbury Jr. Annular α-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes Biochemistry 41 2002 10209 10217
51. S.H. Xu Aggregation drives "misfolding" in protein amyloid fiber formation Amyloid 14 2007 119 131
52. S. Engelender, and Z. Kaminsky C.A. Ross Synphilin-1 associates with α-synuclein and promotes the formation of cytosolic inclusions Nat. Genet. 22 1999 110 114
53. M.L. Kramer, and W.J. Schulz-Schaeffer Presynaptic α-synuclein aggregates, not Lewy bodies, cause neurodegeneration in dementia with Lewy bodies J. Neurosci. 27 2007 1405 1410
54. D.A. Scott, and I. Tabarean S. Roy A pathologic cascade leading to synaptic dysfunction in α-synuclein-induced neurodegeneration J. Neurosci. 30 2010 8083 8095
55. S.A. Jones, and S.H. Shim X. Zhuang Fast, three-dimensional super-resolution imaging of live cells Nat. Methods 8 2011 499 508
56. C.C. Spagnuolo, R.J. Vermeij, and E.A. Jares-Erijman Improved photostable FRET-competent biarsenical-tetracysteine probes based on fluorinated fluoresceins J. Am. Chem. Soc. 128 2006 12040 12041