Attenuation of the early events of α-synuclein aggregation: A fluorescence correlation spectroscopy and laser scanning microscopy study in the presence of surface-coated Fe3O4 nanoparticles

Langmuir

Volumn 31, Issue 4, 2015, Pages 1469-1478

  Joshi, Nidhi ^a   Basak, Sujit ^a   Kundu, Sangeeta ^a   De, Goutam ^b   Mukhopadhyay, Anindita ^b   Chattopadhyay, Krishnananda ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b CSIR CENTRAL GLASS AND CERAMIC RESEARCH INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; LASER APPLICATIONS; MOLECULES; NANOPARTICLES; SURFACE ANALYSIS; TOXICITY;

AMYLOID FIBRIL; FLUORESCENCE CORRELATION SPECTROSCOPY; LASER SCANNING MICROSCOPY; MONOMERIC PROTEINS; PARKINSONS DISEASE; SINGLE-MOLECULE RESOLUTION; SMALL MOLECULES; THERAPEUTIC APPLICATION;

SPECTROSCOPIC ANALYSIS;

ALPHA SYNUCLEIN; MAGNETITE; METAL NANOPARTICLE;

CHEMISTRY; CONFOCAL MICROSCOPY; ENTROPY; PROCEDURES; SPECTROFLUOROMETRY; SURFACE PROPERTY; TRANSMISSION ELECTRON MICROSCOPY;

ALPHA-SYNUCLEIN; CHEMISTRY; ENTROPY; FERROSOFERRIC OXIDE; METAL NANOPARTICLES; METHODS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; SPECTROMETRY, FLUORESCENCE; SURFACE PROPERTIES;

EID: 84964284895     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la503749e     Document Type: Article

References (45)

1. Fink, A. L. The aggregation and fibrillation of alpha-synuclein Acc. Chem. Res. 2006, 39 (9) 628-34
2. Hejjaoui, M.; Haj-Yahya, M.; Kumar, K. S. A.; Brik, A.; Lashuel, H. A. Towards Elucidation of the Role of Ubiquitination in the Pathogenesis of Parkinsons Disease with Semisynthetic Ubiquitinated α-Synuclein Angew. Chem., Int. Ed. 2011, 50 (2) 405-409
3. Polymeropoulos, M. H.; Lavedan, C.; Leroy, E.; Ide, S. E.; Dehejia, A.; Dutra, A.; Pike, B.; Root, H.; Rubenstein, J.; Boyer, R.; Stenroos, E. S.; Chandrasekharappa, S.; Athanassiadou, A.; Papapetropoulos, T.; Johnson, W. G.; Lazzarini, A. M.; Duvoisin, R. C.; Di Iorio, G.; Golbe, L. I.; Nussbaum, R. L. Mutation in the alpha-synuclein gene identified in families with Parkinsons disease Science 1997, 276 (5321) 2045-2047
4. Conway, K. A.; Lee, S. J.; Rochet, J. C.; Ding, T. T.; Williamson, R. E.; Lansbury, P. T., Jr. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinsons disease: implications for pathogenesis and therapy Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (2) 571-576
5. Glabe, C. G. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease Neurobiol. Aging 2006, 27 (4) 570-575
6. Ikenoue, T.; Lee, Y. H.; Kardos, J.; Yagi, H.; Ikegami, T.; Naiki, H.; Goto, Y. Heat of supersaturation-limited amyloid burst directly monitored by isothermal titration calorimetry Proc. Natl. Acad. Sci. U. S. A. 2014, 111 (18) 6654-6659
7. Vekrellis, K.; Stefanis, L. Targeting intracellular and extracellular alpha-synuclein as a therapeutic strategy in Parkinsons disease and other synucleinopathies Expert Opin. Ther. Targets 2012, 16 (4) 421-432
8. Thirunavukkuarasu, S.; Jares-Erijman, E. A.; Jovin, T. M. Multiparametric fluorescence detection of early stages in the amyloid protein aggregation of pyrene-labeled alpha-synuclein J. Mol. Biol. 2008, 378 (5) 1064-1073
9. Celej, M. S.; Jares-Erijman, E. A.; Jovin, T. M. Fluorescent N-arylaminonaphthalene sulfonate probes for amyloid aggregation of alpha-synuclein Biophys. J. 2008, 94 (12) 4867-4879
10. Yushchenko, D. A.; Fauerbach, J. A.; Thirunavukkuarasu, S.; Jares-Erijman, E. A.; Jovin, T. M. Fluorescent ratiometric MFC probe sensitive to early stages of alpha-synuclein aggregation J. Am. Chem. Soc. 2010, 132 (23) 7860-7861
11. Nath, S.; Meuvis, J.; Hendrix, J.; Carl, S. A.; Engelborghs, Y. Early aggregation steps in alpha-synuclein as measured by FCS and FRET: evidence for a contagious conformational change Biophys. J. 2010, 98 (7) 1302-1311
12. Roberti, M. J.; Morgan, M.; Menéndez, G.; Pietrasanta, L. a. I.; Jovin, T. M.; Jares-Erijman, E. A. Quantum Dots As Ultrasensitive Nanoactuators and Sensors of Amyloid Aggregation in Live Cells J. Am. Chem. Soc. 2009, 131 (23) 8102-8107
13. Krol, S.; Macrez, R.; Docagne, F.; Defer, G.; Laurent, S.; Rahman, M.; Hajipour, M. J.; Kehoe, P. G.; Mahmoudi, M. Therapeutic benefits from nanoparticles: the potential significance of nanoscience in diseases with compromise to the blood brain barrier Chem. Rev. 2013, 113 (3) 1877-1903
14. Qiao, R.; Jia, Q.; Huwel, S.; Xia, R.; Liu, T.; Gao, F.; Galla, H. J.; Gao, M. Receptor-mediated delivery of magnetic nanoparticles across the blood-brain barrier ACS Nano 2012, 6 (4) 3304-3310
15. Yoffe, S.; Leshuk, T.; Everett, P.; Gu, F. Superparamagnetic iron oxide nanoparticles (SPIONs): synthesis and surface modification techniques for use with MRI and other biomedical applications Curr. Pharm. Des 2013, 19 (3) 493-509
16. Joshi, N.; Mukhopadhyay, A.; Basak, S.; De, G.; Chattopadhyay, K. Surface Coating Rescues Proteins from Magnetite Nanoparticle Induced Damage Part. Part. Syst. Charact. 2013, 30 (8) 683-694
17. Yang, H. M.; Park, C. W.; Ahn, T.; Jung, B.; Seo, B. K.; Park, J. H.; Kim, J. D. A direct surface modification of iron oxide nanoparticles with various poly(amino acid)s for use as magnetic resonance probes J. Colloid Interface Sci. 2012, 391, 158-167
18. Ghosh, R.; Sharma, S.; Chattopadhyay, K. Effect of arginine on protein aggregation studied by fluorescence correlation spectroscopy and other biophysical methods Biochemistry 2009, 48 (5) 1135-1143
19. Magde, D.; Elson, E.; Webb, W. W. Thermodynamic Fluctuations in a Reacting Systemâ€"Measurement by Fluorescence Correlation Spectroscopy Phys. Rev. Lett. 1972, 29 (11) 705-708
20. Nag, S.; Chen, J.; Irudayaraj, J.; Maiti, S. Measurement of the attachment and assembly of small amyloid-beta oligomers on live cell membranes at physiological concentrations using single-molecule tools Biophys. J. 2010, 99 (6) 1969-1975
21. Liang, Y.; Lynn, D. G.; Berland, K. M. Direct observation of nucleation and growth in amyloid self-assembly J. Am. Chem. Soc. 2010, 132 (18) 6306-6308
22. Basak, S.; Chattopadhyay, K. Fluorescence correlation spectroscopy study on the effects of the shape and size of a protein on its diffusion inside a crowded environment Langmuir 2013, 29 (47) 14709-14717
23. Tcherniak, A.; Reznik, C.; Link, S.; Landes, C. F. Fluorescence correlation spectroscopy: criteria for analysis in complex systems Anal. Chem. 2009, 81 (2) 746-754
24. Sengupta, P.; Garai, K.; Balaji, J.; Periasamy, N.; Maiti, S. Measuring size distribution in highly heterogeneous systems with fluorescence correlation spectroscopy Biophys. J. 2003, 84 (3) 1977-1984
25. Sarkar, S.; Chattopadhyay, K. Studies of early events of folding of a predominately beta-sheet protein using fluorescence correlation spectroscopy and other biophysical methods Biochemistry 2014, 53 (9) 1393-1402
26. Frimpong, A. K.; Abzalimov, R. R.; Uversky, V. N.; Kaltashov, I. A. Characterization of intrinsically disordered proteins with electrospray ionization mass spectrometry: conformational heterogeneity of alpha-synuclein Proteins 2009, 78 (3) 714-722
27. Haldar, S.; Sil, P.; Thangamuniyandi, M.; Chattopadhyay, K. Conversion of Amyloid Fibrils of Cytochrome c to Mature Nanorods through a Honeycomb Morphology Langmuir 2014, 10.1021/la5029993
28. Zeng, S.; Huang, Y. M.; Chang, C. E.; Zhong, W. Protein binding for detection of small changes on a nanoparticle surface Analyst 2014, 139 (6) 1364-1371
29. Auffan, M.; Achouak, W.; Rose, J.; Roncato, M. A.; Chaneac, C.; Waite, D. T.; Masion, A.; Woicik, J. C.; Wiesner, M. R.; Bottero, J. Y. Relation between the redox state of iron-based nanoparticles and their cytotoxicity toward Escherichia coli Environ. Sci. Technol. 2008, 42 (17) 6730-6735
30. Laurent, S.; Forge, D.; Port, M.; Roch, A.; Robic, C.; Vander Elst, L.; Muller, R. N. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications Chem. Rev. 2008, 108 (6) 2064-2110
31. Hoozemans, J. J.; Chafekar, S. M.; Baas, F.; Eikelenboom, P.; Scheper, W. Always around, never the same: pathways of amyloid beta induced neurodegeneration throughout the pathogenic cascade of Alzheimers disease Curr. Med. Chem. 2006, 13 (22) 2599-2605
32. Paleologou, K. E.; Kragh, C. L.; Mann, D. M.; Salem, S. A.; Al-Shami, R.; Allsop, D.; Hassan, A. H.; Jensen, P. H.; El-Agnaf, O. M. Detection of elevated levels of soluble alpha-synuclein oligomers in post-mortem brain extracts from patients with dementia with Lewy bodies Brain 2009, 132 (Pt 4) 1093-1101
33. Cabaleiro-Lago, C.; Quinlan-Pluck, F.; Lynch, I.; Lindman, S.; Minogue, A. M.; Thulin, E.; Walsh, D. M.; Dawson, K. A.; Linse, S. Inhibition of amyloid beta protein fibrillation by polymeric nanoparticles J. Am. Chem. Soc. 2008, 130 (46) 15437-15443
34. Cabaleiro-Lago, C.; Szczepankiewicz, O.; Linse, S. The Effect of Nanoparticles on Amyloid Aggregation Depends on the Protein Stability and Intrinsic Aggregation Rate Langmuir 2012, 28 (3) 1852-1857
35. Mukhopadhyay, A.; Joshi, N.; Chattopadhyay, K.; De, G. A facile synthesis of PEG-coated magnetite (Fe3O4) nanoparticles and their prevention of the reduction of cytochrome c ACS Appl. Mater. Interfaces 2011, 4 (1) 142-149
36. Sweers, K. K.; van der Werf, K. O.; Bennink, M. L.; Subramaniam, V. Atomic force microscopy under controlled conditions reveals structure of C-terminal region of alpha-synuclein in amyloid fibrils ACS Nano 2012, 6 (7) 5952-5960
37. Szczepankiewicz, O.; Cabaleiro-Lago, C.; Tartaglia, G. G.; Vendruscolo, M.; Hunter, T.; Hunter, G. J.; Nilsson, H.; Thulin, E.; Linse, S. Interactions in the native state of monellin, which play a protective role against aggregation Mol. Biosyst 2011, 7 (2) 521-532
38. Colombo, M.; Carregal-Romero, S.; Casula, M. F.; Gutierrez, L.; Morales, M. P.; Bohm, I. B.; Heverhagen, J. T.; Prosperi, D.; Parak, W. J. Biological applications of magnetic nanoparticles Chem. Soc. Rev. 2012, 41 (11) 4306-4334
39. McClendon, S.; Rospigliosi, C. C.; Eliezer, D. Charge neutralization and collapse of the C-terminal tail of alpha-synuclein at low pH Protein Sci. 2009, 18 (7) 1531-1540
40. Du, H.; Chandaroy, P.; Hui, S. W. Grafted poly-(ethylene glycol) on lipid surfaces inhibits protein adsorption and cell adhesion Biochim. Biophys. Acta 1997, 1326 (2) 236-248
41. Gref, R.; Luck, M.; Quellec, P.; Marchand, M.; Dellacherie, E.; Harnisch, S.; Blunk, T.; Muller, R. H. Stealth corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption Colloids Surf., B 2000, 18 (3-4) 301-313
42. Perry, J. L.; Reuter, K. G.; Kai, M. P.; Herlihy, K. P.; Jones, S. W.; Luft, J. C.; Napier, M.; Bear, J. E.; DeSimone, J. M. PEGylated PRINT nanoparticles: the impact of PEG density on protein binding, macrophage association, biodistribution, and pharmacokinetics Nano Lett. 2012, 12 (10) 5304-5310
43. van Vlerken, L. E.; Vyas, T. K.; Amiji, M. M. Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery Pharm. Res. 2007, 24 (8) 1405-1414
44. Blummel, J.; Perschmann, N.; Aydin, D.; Drinjakovic, J.; Surrey, T.; Lopez-Garcia, M.; Kessler, H.; Spatz, J. P. Protein repellent properties of covalently attached PEG coatings on nanostructured SiO(2)-based interfaces Biomaterials 2007, 28 (32) 4739-4747
45. Mahmoudi, M.; Simchi, A.; Imani, M.; Shokrgozar, M. A.; Milani, A. S.; Hafeli, U. O.; Stroeve, P. A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles Colloids Surf., B 2010, 75 (1) 300-309