Nonequilibrium capture rates induce protein accumulation and enhanced adsorption to solid-state nanopores

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12238-12249

  Freedman, Kevin J ^a   Haq, Syed Raza ^b   Fletcher, Michael R ^c   Foley, Joe P ^c   Jemth, Per ^b   Edel, Joshua B ^a   Kim, Min Jun ^d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UPPSALA UNIVERSITY   (Sweden)

^c DREXEL UNIVERSITY   (United States)

^d Drexel University   (United States)

Author keywords

biosensors; capture rate; energy barrier; nanopores; protein adsorption; protein kinetics

Indexed keywords

ADSORPTION; BIOCHEMISTRY; BIOSENSORS; ENERGY BARRIERS; MOLECULES; PROTEINS;

CAPTURE RATE; ENHANCED ADSORPTIONS; FUNDAMENTAL MECHANISMS; PROTEIN ACCUMULATION; PROTEIN ADSORPTION; PROTEIN AGGREGATION; PROTEIN KINETICS; SOLID-STATE NANOPORE;

NANOPORES;

ARTIFICIAL MEMBRANE; PROTEIN;

ADSORPTION; ARTIFICIAL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DIFFUSION; ELECTRIC CONDUCTIVITY; NANOPORE; PROTEIN TERTIARY STRUCTURE; PROTEIN UNFOLDING;

ADSORPTION; DIFFUSION; ELECTRIC CONDUCTIVITY; MEMBRANES, ARTIFICIAL; MODELS, MOLECULAR; NANOPORES; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; PROTEINS;

EID: 84919765192     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn5062645     Document Type: Article

References (62)

1. Li, J.; Stein, D.; McMullan, C.; Branton, D.; Aziz, M.; Golovchenko, J. Ion-Beam Sculpting at Nanometre Length Scales Nature 2001, 412, 166-169
2. Fologea, D.; Ledden, B.; McNabb, D.; Li, J. Electrical Characterization of Protein Molecules by a Solid-State Nanopore Appl. Phys. Lett. 2007, 91, 053901
3. Talaga, D.; Li, J. Single-Molecule Protein Unfolding in Solid State Nanopores J. Am. Chem. Soc. 2009, 131, 9287-9297
4. Freedman, K. J.; Haq, S. R.; Edel, J. B.; Jemth, P.; Kim, M. J. Single Molecule Unfolding and Stretching of Protein Domains inside a Solid-State Nanopore by Electric Field Sci. Rep. 2013, 3
5. Wei, R.; Gatterdam, V.; Wieneke, R.; Tampé, R.; Rant, U. Stochastic Sensing of Proteins with Receptor-Modified Solid-State Nanopores Nat. Nanotechnol. 2012, 7, 257-263
6. Freedman, K. J.; Bastian, A. R.; Chaiken, I.; Kim, M. J. Solid-State Nanopore Detection of Protein Complexes: Applications in Healthcare and Protein Kinetics Small 2013, 9, 750-759
7. Han, A.; Creus, M.; Schürmann, G.; Linder, V.; Ward, T. R.; de Rooij, N. F.; Staufer, U. Label-Free Detection of Single Protein Molecules and Protein-Protein Interactions Using Synthetic Nanopores Anal. Chem. 2008, 80, 4651-4658
8. Yusko, E.; Johnson, J.; Majd, S.; Prangkio, P.; Rollings, R.; Li, J.; Yang, J.; Mayer, M. Controlling Protein Translocation through Nanopores with Bio-Inspired Fluid Walls Nat. Nanotechnol. 2011, 6, 253-260
9. Wanunu, M.; Morrison, W.; Rabin, Y.; Grosberg, A. Y.; Meller, A. Electrostatic Focusing of Unlabelled DNA into Nanoscale Pores Using a Salt Gradient Nat. Nanotechnol. 2010, 5, 160-165
10. Mihovilovic, M.; Hagerty, N.; Stein, D. Statistics of DNA Capture by a Solid-State Nanopore Phys. Rev. Lett. 2013, 110, 028102
11. He, Y.; Tsutsui, M.; Fan, C.; Taniguchi, M.; Kawai, T. Gate Manipulation of DNA Capture into Nanopores ACS Nano 2011, 5, 8391-8397
12. Henrickson, S. E.; Misakian, M.; Robertson, B.; Kasianowicz, J. J. Driven DNA Transport into an Asymmetric Nanometer-Scale Pore Phys. Rev. Lett. 2000, 85, 3057-3060
13. Grosberg, A. Y.; Rabin, Y. DNA Capture into a Nanopore: Interplay of Diffusion and Electrohydrodynamics J. Chem. Phys. 2010, 133, 165102
14. Pastoriza-Gallego, M.; Rabah, L.; Gibrat, G.; Thiebot, B.; van der Goot, F. G.; Auvray, L.; Betton, J.-M.; Pelta, J. Dynamics of Unfolded Protein Transport through an Aerolysin Pore J. Am. Chem. Soc. 2011, 133, 2923-2931
15. Oukhaled, A.; Cressiot, B.; Bacri, L.; Pastoriza-Gallego, M.; Betton, J.-M.; Bourhis, E.; Jede, R.; Gierak, J.; Auvray, L. c.; Pelta, J. Dynamics of Completely Unfolded and Native Proteins through Solid-State Nanopores as a Function of Electric Driving Force ACS Nano 2011, 5, 3628-3638
16. Miles, B.; Ivanov, A.; Wilson, K.; Dogan, F.; Japrung, D.; Edel, J. Single Molecule Sensing with Solid-State Nanopores: Novel Materials, Methods, and Applications Chem. Soc. Rev. 2013, 42, 15-28
17. Cheley, S.; Xie, H.; Bayley, H. A Genetically Encoded Pore for the Stochastic Detection of a Protein Kinase ChemBioChem 2006, 7, 1923-1927
18. Cressiot, B.; Oukhaled, A.; Patriarche, G.; Pastoriza-Gallego, M.; Betton, J.-M.; Auvray, L.; Muthukumar, M.; Bacri, L.; Pelta, J. Protein Transport through a Narrow Solid-State Nanopore at High Voltage: Experiments and Theory ACS Nano 2012, 6, 6236-6243
19. Japrung, D.; Dogan, J.; Freedman, K. J.; Nadzeyka, A.; Bauerdick, S.; Albrecht, T.; Kim, M. J.; Jemth, P.; Edel, J. B. Single-Molecule Studies of Intrinsically Disordered Proteins Using Solid-State Nanopores Anal. Chem. 2013, 85, 2449-2456
20. Siwy, Z.; Trofin, L.; Kohli, P.; Baker, L. A.; Trautmann, C.; Martin, C. R. Protein Biosensors Based on Biofunctionalized Conical Gold Nanotubes J. Am. Chem. Soc. 2005, 127, 5000-5001
21. Li, W.; Bell, N. A. W.; Hernández-Ainsa, S.; Thacker, V. V.; Thackray, A. M.; Bujdoso, R.; Keyser, U. F. Single Protein Molecule Detection by Glass Nanopores ACS Nano 2013, 7, 4129-4134
22. Larkin, J.; Henley, R. Y.; Muthukumar, M.; Rosenstein, J. K.; Wanunu, M. High-Bandwidth Protein Analysis Using Solid-State Nanopores Biophys. J. 2014, 106, 696-704
23. Rotem, D.; Jayasinghe, L.; Salichou, M.; Bayley, H. Protein Detection by Nanopores Equipped with Aptamers J. Am. Chem. Soc. 2012, 134, 2781-2787
24. Merstorf, C. L.; Cressiot, B.; Pastoriza-Gallego, M.; Oukhaled, A.; Betton, J.-M.; Auvray, L.; Pelta, J. Wild Type, Mutant Protein Unfolding and Phase Transition Detected by Single-Nanopore Recording ACS Chem. Biol. 2012, 7, 652-658
25. Singh, P. R.; Bárcena-Uribarri, I.; Modi, N.; Kleinekathöfer, U.; Benz, R.; Winterhalter, M.; Mahendran, K. R. Pulling Peptides across Nanochannels: Resolving Peptide Binding and Translocation through the Hetero-Oligomeric Channel from Nocardia farcinica ACS Nano 2012, 6, 10699-10707
26. Wanunu, M.; Bhattacharya, S.; Xie, Y.; Tor, Y.; Aksimentiev, A.; Drndic, M. Nanopore Analysis of Individual RNA/Antibiotic Complexes ACS Nano 2011, 5, 9345-9353
27. Hornblower, B.; Coombs, A.; Whitaker, R. D.; Kolomeisky, A.; Picone, S. J.; Meller, A.; Akeson, M. Single-Molecule Analysis of DNA-Protein Complexes Using Nanopores Nat. Methods 2007, 4, 315-317
28. Galla, L.; Meyer, A. J.; Spiering, A.; Sischka, A.; Mayer, M.; Hall, A. R.; Reimann, P.; Anselmetti, D. Hydrodynamic Slip on DNA Observed by Optical Tweezers-Controlled Translocation Experiments with Solid-State and Lipid-Coated Nanopores Nano Lett. 2014, 14, 4176-4182
29. Wang, D.; Harrer, S.; Luan, B.; Stolovitzky, G.; Peng, H.; Afzali-Ardakani, A. Regulating the Transport of DNA through Biofriendly Nanochannels in a Thin Solid Membrane Sci. Rep. 2014, 4
30. Soskine, M.; Biesemans, A.; De Maeyer, M.; Maglia, G. Tuning the Size and Properties of ClyA Nanopores Assisted by Directed Evolution J. Am. Chem. Soc. 2013, 135, 13456-13463
31. Oukhaled, A.; Bacri, L.; Pastoriza-Gallego, M.; Betton, J.-M.; Pelta, J. Sensing Proteins through Nanopores: Fundamental to Applications ACS Chem. Biol. 2012, 7, 1935-1949
32. Schuler, B.; Hofmann, H. Single-Molecule Spectroscopy of Protein Folding Dynamics-Expanding Scope and Timescales Curr. Opin. Struct. Biol. 2013, 23, 36-47
33. Kaufman, L. J. Heterogeneity in Single-Molecule Observables in the Study of Supercooled Liquids Annu. Rev. Phys. Chem. 2013, 64, 177-200
34. Yu, H.; Liu, X.; Neupane, K.; Gupta, A. N.; Brigley, A. M.; Solanki, A.; Sosova, I.; Woodside, M. T. Direct Observation of Multiple Misfolding Pathways in a Single Prion Protein Molecule Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 5283-5288
35. Arai, M.; Ferreon, J. C.; Wright, P. E. Quantitative Analysis of Multisite Protein-Ligand Interactions by NMR: Binding of Intrinsically Disordered p53 Transactivation Subdomains with the TAZ2 Domain of CBP J. Am. Chem. Soc. 2012, 134, 3792-3803
36. Boehr, D. D.; Nussinov, R.; Wright, P. E. The Role of Dynamic Conformational Ensembles in Biomolecular Recognition Nat. Chem. Biol. 2009, 5, 789-796
37. Lange, O. F.; Lakomek, N.-A.; Farès, C.; Schröder, G. F.; Walter, K. F.; Becker, S.; Meiler, J.; Grubmüller, H.; Griesinger, C.; De Groot, B. L. Recognition Dynamics up to Microseconds Revealed from an RDC-Derived Ubiquitin Ensemble in Solution Science 2008, 320, 1471-1475
38. Sexton, L. T.; Mukaibo, H.; Katira, P.; Hess, H.; Sherrill, S. A.; Horne, L. P.; Martin, C. R. An Adsorption-Based Model for Pulse Duration in Resistive-Pulse Protein Sensing J. Am. Chem. Soc. 2010, 132, 6755-6763
39. Niedzwiecki, D. J.; Grazul, J.; Movileanu, L. Single-Molecule Observation of Protein Adsorption onto an Inorganic Surface J. Am. Chem. Soc. 2010, 132, 10816-10822
40. Stellwagen, N.; Gelfi, C.; Righetti, P. The Free Solution Mobility of DNA Biopolymers 1997, 42, 687-703
41. Heng, J.; Ho, C.; Kim, T.; Timp, R.; Aksimentiev, A.; Grinkova, Y.; Sligar, S.; Schulten, K.; Timp, G. Sizing DNA Using a Nanometer-Diameter Pore Biophys. J. 2004, 87, 2905-2911
42. Kasianowicz, J.; Brandin, E.; Branton, D.; Deamer, D. Characterization of Individual Polynucleotide Molecules Using a Membrane Channel Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 13770-13773
43. Oukhaled, G.; Mathé, J.; Biance, A. L.; Bacri, L.; Betton, J. M.; Lairez, D.; Pelta, J.; Auvray, L. Unfolding of Proteins and Long Transient Conformations Detected by Single Nanopore Recording Phys. Rev. Lett. 2007, 98, 158101
44. Plesa, C.; Kowalczyk, S. W.; Zinsmeester, R.; Grosberg, A. Y.; Rabin, Y.; Dekker, C. Fast Translocation of Proteins through Solid State Nanopores Nano Lett. 2013, 13, 658-663
45. Talaga, D. S.; Li, J. Single-Molecule Protein Unfolding in Solid State Nanopores J. Am. Chem. Soc. 2009, 131, 9287-9297
46. Arai, T.; Norde, W. The Behavior of Some Model Proteins at Solid-Liquid Interfaces Colloids Surf. 1990, 51, 1-15
47. Firnkes, M.; Pedone, D.; Knezevic, J.; Döblinger, M.; Rant, U. Electrically Facilitated Translocations of Proteins through Silicon Nitride Nanopores: Conjoint and Competitive Action of Diffusion, Electrophoresis, and Electroosmosis Nano Lett. 2010, 10, 2162-2167
48. Prabhu, A. S.; Jubery, T. Z. N.; Freedman, K. J.; Mulero, R.; Dutta, P.; Kim, M. J. Chemically Modified Solid State Nanopores for High Throughput Nanoparticle Separation J. Phys.: Condens. Matter 2010, 22, 454107
49. Gasteiger, E.; Hoogland, C.; Gattiker, A.; Wilkins, M. R.; Appel, R. D.; Bairoch, A. Protein Identification and Analysis Tools on the Expasy Server. In The Proteomics Protocols Handbook; Springer: Berlin, 2005; pp 571-607.
50. Ivarsson, Y. Plasticity of PDZ Domains in Ligand Recognition and Signaling FEBS Lett. 2012, 586, 2638-2647
51. Chi, C. N.; Bach, A.; Engström, Å.; Wang, H.; Strømgaard, K.; Gianni, S.; Jemth, P. A Sequential Binding Mechanism in a PDZ Domain Biochemistry 2009, 48, 7089-7097
52. Haq, S. R.; Jürgens, M. C.; Chi, C. N.; Koh, C.-S.; Elfström, L.; Selmer, M.; Gianni, S.; Jemth, P. The Plastic Energy Landscape of Protein Folding J. Biol. Chem. 2010, 285, 18051-18059
53. Kannam, S. K.; Kim, S. C.; Rogers, P. R.; Gunn, N.; Wagner, J.; Harrer, S.; Downton, M. T. Sensing of Protein Molecules through Nanopores: A Molecular Dynamics Study Nanotechnology 2014, 25, 155502
54. van Dorp, S.; Keyser, U. F.; Dekker, N. H.; Dekker, C.; Lemay, S. G. Origin of the Electrophoretic Force on DNA in Solid-State Nanopores Nat. Phys. 2009, 5, 347-351
55. Harjinder Singh, H.; Karlapalem, K.; Mitra, A. A Real Valued Genetic Algorithm for Generating Native Like Structure of Small Globular Protein IEEE Eng. Med. Biol. Soc. 2008, 1359-1362
56. Kohn, J. E.; Millett, I. S.; Jacob, J.; Zagrovic, B.; Dillon, T. M.; Cingel, N.; Dothager, R. S.; Seifert, S.; Thiyagarajan, P.; Sosnick, T. R. Random-Coil Behavior and the Dimensions of Chemically Unfolded Proteins Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 12491-12496
57. Zhou, H. Influence of Crowded Cellular Environments on Protein Folding, Binding, and Oligomerization: Biological Consequences and Potentials of Atomistic Modeling FEBS Lett. 2013, 587, 1053-1061
58. Zhou, H. X. Protein Folding and Binding in Confined Spaces and in Crowded Solutions J. Mol. Recognit. 2004, 17, 368-375
59. Shtilerman, M. D.; Ding, T. T.; Lansbury, P. T. Molecular Crowding Accelerates Fibrillization of α-Synuclein: Could an Increase in the Cytoplasmic Protein Concentration Induce Parkinsons Disease Biochemistry 2002, 41, 3855-3860
60. Soranno, A.; Koenig, I.; Borgia, M. B.; Hofmann, H.; Zosel, F.; Nettels, D.; Schuler, B. Single-Molecule Spectroscopy Reveals Polymer Effects of Disordered Proteins in Crowded Environments Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 4874-4879
61. Zhou, H.-X. Polymer Crowders and Protein Crowders Act Similarly on Protein Folding Stability FEBS Lett. 2013, 587, 394-397
62. Batra, J.; Xu, K.; Qin, S.; Zhou, H.-X. Effect of Macromolecular Crowding on Protein Binding Stability: Modest Stabilization and Significant Biological Consequences Biophys. J. 2009, 97, 906-911