Study of wild-type α-synuclein binding and orientation on gold nanoparticles

Langmuir

Volumn 29, Issue 14, 2013, Pages 4603-4615

  Yang, Jie An ^a   Johnson, Brittany J ^a   Wu, Sway ^a   Woods, Wendy S ^b   George, Julia M ^b,c   Murphy, Catherine J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION CONSTANT; EQUILIBRIUM ASSOCIATION CONSTANT; GOLD NANOPARTICLES; NEGATIVELY CHARGED; NEUROLOGICAL DISEASE; PARKINSON'S DISEASE; PROTEASE DIGESTION; PROTEIN-PROTEIN INTERACTIONS;

DISEASES; EQUILIBRIUM CONSTANTS; GOLD; METAL NANOPARTICLES; PHYSIOLOGY; PROTEINS;

GOLD ALLOYS;

ALPHA SYNUCLEIN; GOLD; METAL NANOPARTICLE; TRYPSIN;

ADSORPTION; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; PARTICLE SIZE; PROTEIN BINDING; PROTEIN DEGRADATION; SPECTROFLUOROMETRY;

ADSORPTION; ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; GOLD; HUMANS; METAL NANOPARTICLES; MOLECULAR SEQUENCE DATA; PARTICLE SIZE; PROTEIN BINDING; PROTEOLYSIS; SPECTROMETRY, FLUORESCENCE; TRYPSIN;

EID: 84875968263     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la400266u     Document Type: Article

References (60)

1. Madeo, G.; Martella, G.; Schirinzi, T.; Ponterio, G.; Shen, J.; Bonsi, P.; Pisani, A. Aberrant Striatal Synaptic Plasticity in Monogenic Parkinsonisms Neuroscience 2012, 211, 126-135
2. Olanow, C. W.; Prusiner, S. B. Is Parkinson's Disease a Prion Disorder? Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 12571-12572
3. Spillantini, M. G.; Schmidt, M. L.; Lee, V. M.; Trojanowski, J. Q.; Jakes, R.; Goedert, M. Alpha-Synuclein in Lewy Bodies Nature 1997, 388, 839-840
4. Feany, M. B.; Bender, W. W. A Drosophila Model of Parkinson's Disease Nature 2000, 404, 394-398
5. Masliah, E.; Rockenstein, E.; Veinbergs, I.; Mallory, M.; Hashimoto, M.; Takeda, A.; Sagara, Y.; Sisk, A.; Mucke, L. Dopaminergic Loss and Inclusion Body Formation in α-Synuclein Mice: Implications for Neurodegenerative Disorders Science 2000, 287, 1265-1269
6. Desplats, P.; Lee, H.-J.; Bae, E.-J.; Patrick, C.; Rockenstein, E.; Crews, L.; Spencer, B.; Masliah, E.; Lee, S.-J. Inclusion Formation and Neuronal Cell Death Through Neuron-to-Neuron Transmission of α-Synuclein Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 13010-13015
7. Seo, J.-H.; Rah, J.-C.; Choi, S. H.; Shin, J. K.; Min, K.; Kim, H.-S.; Park, C. H.; Kim, S.; Kim, E.-M.; Lee, S.-H.; Lee, S.; Suh, S. W.; Suh, Y.-H. α-Synuclein Regulates Neuronal Survival via Bcl-2 Family Expression and PI3/Akt Kinase Pathway FASEB J. 2002, 16, 1826-1828
8. Weinreb, P. H.; Zhen, W.; Poon, A. W.; Conway, K. A.; Lansbury, P. T. NACP, A Protein Implicated in Alzheimer's Disease and Learning, Is Natively Unfolded Biochemistry 1996, 35, 13709-13715
9. Uversky, V. N. Neuropathology, Biochemistry, and Biophysics of A-synuclein Aggregation J. Neurochem. 2007, 103, 17-37
10. Trexler, A. J.; Rhoades, E. α-Synuclein Binds Large Unilamellar Vesicles as an Extended Helix Biochemistry 2009, 48, 2304-2306
11. Uversky, V. N.; Li, J.; Fink, A. L. Evidence for a Partially Folded Intermediate in Alpha-Synuclein Fibril Formation J. Biol. Chem. 2001, 276, 10737-10744
12. Uversky, V. N.; Li, J.; Fink, A. L. Metal-Triggered Structural Transformations, Aggregation, and Fibrillation of Human Alpha-Synuclein. A Possible Molecular NK Between Parkinson's Disease and Heavy Metal Exposure J. Biol. Chem. 2001, 276, 44284-44296
13. Breydo, L.; Wu, J. W.; Uversky, V. N. α-Synuclein Misfolding and Parkinson's Disease BBA-Mol. Basis Dis. 2012, 1822, 261-285
14. Winner, B.; Jappelli, R.; Maji, S. K.; Desplats, P. A.; Boyer, L.; Aigner, S.; Hetzer, C.; Loher, T.; Vilar, M.; Campioni, S.; Tzitzilonis, C.; Soragni, A.; Jessberger, S.; Mira, H.; Consiglio, A.; Pham, E.; Masliah, E.; Gage, F. H.; Riek, R. In Vivo Demonstration that Alpha-Synuclein Oligomers Are Toxic Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 4194-4199
15. Dev, K. K.; Hofele, K.; Barbieri, S.; Buchman, V. L.; van der Putten, H. Part II: α-Synuclein and Its Molecular Pathophysiological Role in Neurodegenerative Disease Neuropharmacology 2003, 45, 14-44
16. Dreaden, E. C.; Alkilany, A. M.; Huang, X.; Murphy, C. J.; El-Sayed, M. A. The Golden Age: Gold Nanoparticles for Biomedicine Chem. Soc. Rev. 2012, 41, 2740-2779
17. Dreaden, E. C.; Mackey, M. A.; Huang, X.; Kang, B.; El-Sayed, M. A. Beating Cancer in Multiple Ways Using Nanogold Chem. Soc. Rev. 2011, 40, 3391-3404
18. Alkilany, A. M.; Nagaria, P. K.; Hexel, C. R.; Shaw, T. J.; Murphy, C. J.; Wyatt, M. D. Cellular Uptake and Cytotoxicity of Gold Nanorods: Molecular Origin of Cytotoxicity and Surface Effects Small 2009, 5, 701-708
19. Cedervall, T.; Lynch, I.; Foy, M.; BerggaÌŠrd, T.; Donnelly, S. C.; Cagney, G.; Linse, S.; Dawson, K. A. Detailed Identification of Plasma Proteins Adsorbed on Copolymer Nanoparticles Angew. Chem., Int. Ed. 2007, 46, 5754-5756
20. Walczyk, D.; Bombelli, F. B.; Monopoli, M. P.; Lynch, I.; Dawson, K. A. What the Cell "Sees" in Bionanoscience J. Am. Chem. Soc. 2010, 132, 5761-5768
21. Roach, P.; Farrar, D.; Perry, C. C. Surface Tailoring for Controlled Protein Adsorption: Effect of Topography at the Nanometer Scale and Chemistry J. Am. Chem. Soc. 2006, 128, 3939-3945
22. Shrivastava, S.; Nuffer, J. H.; Siegel, R. W.; Dordick, J. S. Position-Specific Chemical Modification and Quantitative Proteomics Disclose Protein Orientation Adsorbed on Silica Nanoparticles Nano Lett. 2012, 12, 1583-1587
23. Lee, D.; Choe, Y.-J.; Choi, Y. S.; Bhak, G.; Lee, J.; Paik, S. R. Photoconductivity of Pea-Pod-Type Chains of Gold Nanoparticles Encapsulated Within Dielectric Amyloid Protein Nanofibrils of α-Synuclein Angew. Chem., Int. Ed. 2011, 50, 1332-1337
24. Lee, D.; Choe, Y.-J.; Lee, M.; Jeong, D. H.; Paik, S. R. Protein-Based SERS Technology Monitoring the Chemical Reactivity on an α-Synuclein- Mediated Two-Dimensional Array of Gold Nanoparticles Langmuir 2011, 27, 12782-12787
25. Roberti, M. J.; Morgan, M.; Menéndez, G.; Pietrasanta, L. 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, 8102-8107
26. 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 β Protein Fibrillation by Polymeric Nanoparticles J. Am. Chem. Soc. 2008, 130, 15437-15443
27. Cabaleiro-Lago, C.; Quinlan-Pluck, F.; Lynch, I.; Dawson, K. A.; Linse, S. Dual Effect of Amino Modified Polystyrene Nanoparticles on Amyloid β Protein Fibrillation ACS Chem. Neurosci. 2010, 1, 279-287
28. Saraiva, A. M.; Cardoso, I.; Pereira, M. C.; Coelho, M. A. N.; Saraiva, M. J.; Möhwald, H.; Brezesinski, G. Controlling Amyloid-beta Peptide(1-42) Oligomerization and Toxicity by Fluorinated Nanoparticles ChemBioChem 2010, 11, 1905-1913
29. O'Brien, E. P.; Straub, J. E.; Brooks, B. R.; Thirumalai, D. Influence of Nanoparticle Size and Shape on Oligomer Formation of an Amyloidogenic Peptide J. Phys. Chem. Lett. 2011, 2, 1171-1177
30. Ji, X.; Song, X.; Li, J.; Bai, Y.; Yang, W.; Peng, X. Size Control of Gold Nanocrystals in Citrate Reduction: The Third Role of Citrate J. Am. Chem. Soc. 2007, 129, 13939-13948
31. Perrault, S. D.; Chan, W. C. W. Synthesis and Surface Modification of Highly Monodispersed, Spherical Gold Nanoparticles of 50-200 nm J. Am. Chem. Soc. 2009, 131, 17042-17043
32. Kloepper, K. D.; Woods, W. S.; Winter, K. A.; George, J. M.; Rienstra, C. M. Preparation of α-Synuclein Fibrils for Solid-state NMR: Expression, Purification, and Incubation of Wild-type and Mutant Forms Prot. Expr. Purif. 2006, 48, 112-117
33. Narhi, L.; Wood, S. J.; Steavenson, S.; Jiang, Y.; Wu, G. M.; Anafi, D.; Kaufman, S. A.; Martin, F.; Sitney, K.; Denis, P.; Louis, J.-C.; Wypych, J.; Biere, A. L.; Citron, M. Both Familial Parkinson's Disease Mutations Accelerate α-Synuclein Aggregation J. Biol. Chem. 1999, 274, 9843-9846
34. Morar, A. S.; Olteanu, A.; Young, G. B.; Pielak, G. J. Solvent-induced Collapse of α-Synuclein and Acid-Denatured Cytochrome c Protein Sci. 2001, 10, 2195-2199
35. Hall, W. P.; Ngatia, S. N.; Van Duyne, R. P. LSPR Biosensor Signal Enhancement Using Nanoparticle-Antibody Conjugates J. Phys. Chem. C 2011, 115, 1410-1414
36. Hasadsri, L.; Kreuter, J.; Hattori, H.; Iwasaki, T.; George, J. M. Functional Protein Delivery into Neurons Using Polymeric Nanoparticles J. Biol. Chem. 2009, 284, 6972-6981
37. 2 Nanotube Arrays for the Detection of α-Synuclein Chem.-Eur. J. 2010, 16, 14439-14446
38. Haes, A. J.; Van Duyne, R. P. A Nanoscale Optical Biosensor: Sensitivity and Selectivity of an Approach Based on the Localized Surface Plasmon Resonance Spectroscopy of Triangular Silver Nanoparticles J. Am. Chem. Soc. 2002, 124, 10596-10604
39. Vangala, K.; Ameer, F.; Salomon, G.; Le, V.; Lewis, E.; Yu, L.; Liu, D.; Zhang, D. Studying Protein and Gold Nanoparticle Interaction Using Organothiols as Molecular Probes J. Phys. Chem. C 2012, 116, 3645-3652
40. Jans, H.; Liu, X.; Austin, L.; Maes, G.; Huo, Q. Dynamic Light Scattering as a Powerful Tool for Gold Nanoparticle Bioconjugation and Biomolecular Binding Studies Anal. Chem. 2009, 81, 9425-9432
41. Wang, X.; Ramström, O.; Yan, M. Dynamic Light Scattering as an Efficient Tool to Study Glyconanoparticle-Lectin Interactions Analyst 2011, 136, 4174-4178
42. Mahtab, R.; Rogers, J. P.; Murphy, C. J. Protein-Sized Quantum Dot Luminescence Can Distinguish between "Straight", "Bend", and "Kinked" Oligonucleotides J. Am. Chem. Soc. 1995, 117, 9099-9100
43. Röcker, C.; Pötzl, M.; Zhang, F.; Parak, W. J.; Nienhaus, G. U. A Quantitative Fluorescence Study of Protein Monolayer Formation on Colloidal Nanoparticles Nat. Nanotechnol. 2009, 4, 577-580
44. Linse, S.; Cabaleiro-Lago, C.; Xue, W.-F.; Lynch, I.; Lindman, S.; Thulin, E.; Radford, S. E.; Dawson, K. A. Nucleation of Protein Fibrillation by Nanoparticles Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 8691-8696
45. Aguila, A.; Murray, R. W. Monolayer-Protected Clusters with Fluorescent Dansyl Ligands Langmuir 2000, 16, 5949-5954
46. Kamp, F.; Beyer, K. Binding of α-Synuclein Affects the Lipid Packing in Bilayers of Small Vesicles J. Biol. Chem. 2006, 281, 9251-9259
47. Middleton, E. R.; Rhoades, E. Effects of Curvature and Composition on α-Synuclein Binding to Lipid Vesicles Biophys. J. 2010, 99, 2279-2288
48. Davidson, W. S.; Jonas, A.; Clayton, D. F.; George, J. M. Stabilization of α-Synuclein Secondary Structure upon Binding to Synthetic Membranes J. Biol. Chem. 1998, 273, 9443-9449
49. Milani, S.; Baldelli Bombelli, F.; Pitek, A. S.; Dawson, K. A.; Rädler, J. Reversible Versus Irreversible Binding of Transferrin to Polystyrene Nanoparticles: Soft and Hard Corona ACS Nano 2012, 6, 2532-2541
50. Slocik, J. M.; Govorov, A. O.; Naik, R. R. Plasmonic Circular Dichroism of Peptide-Functionalized Gold Nanoparticles Nano Lett. 2011, 11, 701-705
51. Laera, S.; Ceccone, G.; Rossi, F.; Gilliland, D.; Hussain, R.; Siligardi, G.; Calzolai, L. Measuring Protein Structure and Stability of Protein-Nanoparticle Systems with Synchrotron Radiation Circular Dichroism Nano Lett. 2011, 11, 4480-4484
52. Shao, Q.; Wu, P.; Gu, P.; Xu, X.; Zhang, H.; Cai, C. Electrochemical and Spectroscopic Studies on the Conformational Structure of Hemoglobin Assembled on Gold Nanoparticles J. Phys. Chem. B 2011, 115, 8627-8637
53. Calzolai, L.; Franchini, F.; Gilliland, D.; Rossi, F. Protein-Nanoparticle Interaction: Identification of the Ubiquitin-Gold Nanoparticle Interaction Site Nano Lett. 2010, 10, 3101-3105
54. Ulmer, T. S.; Bax, A.; Cole, N. B.; Nussbaum, R. L. Structure and Dynamics of Micelle-Bound Human α-Synuclein J. Biol. Chem. 2005, 280, 9595-9603
55. Qin, Z.; Hu, D.; Han, S.; Hong, D.-P.; Fink, A. L. Role of Different Regions of α-Synuclein in the Assembly of Fibrils Biochemistry 2007, 46, 13322-13330
56. Jao, C. C.; Hegde, B. G.; Chen, J.; Haworth, I. S.; Langen, R. Structure of Membrane-Bound α-Synuclein from Site-Directed Spin Labeling and Computational Refinement Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 19666-19671
57. Karyagina, I.; Becker, S.; Giller, K.; Riedel, D.; Jovin, T. M.; Griesinger, C.; Bennati, M. Electron Paramagnetic Resonance Spectroscopy Measures the Distance Between the External β-Strands of Folded α-Synuclein in Amyloid Fibrils Biophys. J. 2011, 101, L1-L3
58. Comellas, G.; Lemkau, L. R.; Nieuwkoop, A. J.; Kloepper, K. D.; Ladror, D. T.; Ebisu, R.; Woods, W. S.; Lipton, A. S.; George, J. M.; Rienstra, C. M. Structured Regions of α-Synuclein Fibrils Include the Early-Onset Parkinson's Disease Mutation Sites J. Mol. Biol. 2011, 411, 881-895
59. Dedmon, M. M.; Lindorff-Larsen, K.; Christodoulou, J.; Vendruscolo, M.; Dobson, C. M. Mapping Long-Range Interactions in α-Synuclein Using Spin-Label NMR and Ensemble Molecular Dynamics Simulations J. Am. Chem. Soc. 2004, 127, 476-477
60. Bertoncini, C. W.; Jung, Y.-S.; Fernandez, C. O.; Hoyer, W.; Griesinger, C.; Jovin, T. M.; Zweckstetter, M. Release of Long-Range Tertiary Interactions Potentiates Aggregation of Natively Unstructured α-Synuclein Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 1430-1435