Detection of two isomeric binding configurations in a protein-Aptamer complex with a biological nanopore

ACS Nano

Volumn 8, Issue 12, 2014, Pages 12826-12835

  Van Meervelt, Veerle ^a   Soskine, Misha ^a   Maglia, Giovanni ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

aptamer; nanopore; protein:DNA interactions; single molecule; thrombin

Indexed keywords

DNA; ENZYMES;

APTAMERS; CONFORMATIONAL HETEROGENEITY; DNA INTERACTION; NUCLEOBASE SUBSTITUTION; PROTEIN-DNA INTERACTIONS; SINGLE MOLECULE; SINGLE MOLECULE LEVEL; THROMBIN;

NANOPORES;

APTAMER; PROTEIN BINDING; THROMBIN; THROMBIN APTAMER;

CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; ISOMERISM; KINETICS; METABOLISM; NANOPORE; NANOTECHNOLOGY; PROCEDURES; PROTEIN CONFORMATION;

APTAMERS, NUCLEOTIDE; HUMANS; ISOMERISM; KINETICS; MODELS, MOLECULAR; NANOPORES; NANOTECHNOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; THROMBIN;

EID: 84919742978     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn506077e     Document Type: Article

References (61)

1. Hurt, N.; Wang, H.; Akeson, M.; Lieberman, K. R. Specific Nucleotide Binding and Rebinding to Individual DNA Polymerase Complexes Captured on a Nanopore J. Am. Chem. Soc. 2009, 3772-3778
2. Cockroft, S. L.; Chu, J.; Amorin, M.; Ghadiri, M. R. A Single-Molecule Nanopore Device Detects DNA Polymerase Activity with Single-Nucleotide Resolution J. Am. Chem. Soc. 2008, 818-820
3. Bikwemu, R.; Wolfe, A. J.; Xing, X.; Movileanu, L. Facilitated Translocation of Polypeptides through a Single Nanopore J. Phys.: Condens. Matter 2010, 454117
4. Wolfe, A. J.; Mohammad, M. M.; Cheley, S.; Bayley, H.; Movileanu, L. Catalyzing the Translocation of Polypeptides through Attractive Interactions J. Am. Chem. Soc. 2007, 14034-14041
5. Movileanu, L.; Schmittschmitt, J. P.; Scholtz, J. M.; Bayley, H. Interactions of Peptides with a Protein Pore Biophys. J. 2005, 1030-1045
6. Payet, L.; Martinho, M.; Pastoriza-Gallego, M.; Betton, J. M.; Auvray, L.; Pelta, J.; Mathe, J. Thermal Unfolding of Proteins Probed at the Single Molecule Level Using Nanopores Anal. Chem. 2012, 4071-4076
7. 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, 2923-2931
8. 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, 158101
9. Stefureac, R.; Waldner, L.; Howard, P.; Lee, J. S. Nanopore Analysis of a Small 86-Residue Protein Small 2008, 59-63
10. Stefureac, R.; Long, Y. T.; Kraatz, H. B.; Howard, P.; Lee, J. S. Transport of Alpha-Helical Peptides through Alpha-Hemolysin and Aerolysin Pores Biochemistry 2006, 9172-9179
11. Rodriguez-Larrea, D.; Bayley, H. Multistep Protein Unfolding during Nanopore Translocation Nat. Nanotechnol. 2013, 288-295
12. Nivala, J.; Marks, D. B.; Akeson, M. Unfoldase-Mediated Protein Translocation through an Alpha-Hemolysin Nanopore Nat. Biotechnol. 2013, 247-250
13. Fologea, D.; Ledden, B.; McNabb, D. S.; Li, J. Electrical Characterization of Protein Molecules by a Solid-State Nanopore Appl. Phys. Lett. 2007, 539011-539013
14. Han, A.; Creus, M.; Schurmann, 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, 4651-4658
15. Stefureac, R. I.; Trivedi, D.; Marziali, A.; Lee, J. S. Evidence That Small Proteins Translocate through Silicon Nitride Pores in a Folded Conformation J. Phys.: Condens. Matter 2010, 454133
16. Oukhaled, A.; Bacri, L.; Pastoriza-Gallego, M.; Betton, J. M.; Pelta, J. Sensing Proteins through Nanopores: Fundamental to Applications ACS Chem. Biol. 2012, 1935-1949
17. Firnkes, M.; Pedone, D.; Knezevic, J.; Doblinger, M.; Rant, U. Electrically Facilitated Translocations of Proteins through Silicon Nitride Nanopores: Conjoint and Competitive Action of Diffusion, Electrophoresis, and Electroosmosis Nano Lett. 2010, 2162-2167
18. Yusko, E. C.; Johnson, J. M.; Majd, S.; Prangkio, P.; Rollings, R. C.; Li, J.; Yang, J.; Mayer, M. Controlling Protein Translocation through Nanopores with Bio-Inspired Fluid Walls Nat. Nanotechnol. 2011, 253-260
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, 2449-2456
20. Wei, R.; Gatterdam, V.; Wieneke, R.; Tampe, R.; Rant, U. Stochastic Sensing of Proteins with Receptor-Modified Solid-State Nanopores Nat. Nanotechnol. 2012, 257-263
21. Smeets, R. M.; Kowalczyk, S. W.; Hall, A. R.; Dekker, N. H.; Dekker, C. Translocation of Reca-Coated Double-Stranded DNA through Solid-State Nanopores Nano Lett. 2009, 3089-3096
22. Mahmood, M. A.; Ali, W.; Adnan, A.; Iqbal, S. M. 3d Structural Integrity and Interactions of Single-Stranded Protein-Binding DNA in a Functionalized Nanopore J. Phys. Chem. B 2014, 5799-5806
23. Japrung, D.; Bahrami, A.; Nadzeyka, A.; Peto, L.; Bauerdick, S.; Edel, J. B.; Albrecht, T. Ssb Binding to Single-Stranded DNA Probed Using Solid-State Nanopore Sensors J. Phys. Chem. B 2014, 11605-11612
24. Raillon, C.; Cousin, P.; Traversi, F.; Garcia-Cordero, E.; Hernandez, N.; Radenovic, A. Nanopore Detection of Single Molecule RNAp-DNA Transcription Complex Nano Lett. 2012, 1157-1164
25. 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, 658-663
26. 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, 13456-13463
27. Soskine, M.; Biesemans, A.; Moeyaert, B.; Cheley, S.; Bayley, H.; Maglia, G. An Engineered ClyA Nanopore Detects Folded Target Proteins by Selective External Association and Pore Entry Nano Lett. 2012, 4895-4900
28. Franceschini, L.; Soskine, M.; Biesemans, A.; Maglia, G. A Nanopore Machine Promotes the Vectorial Transport of DNA across Membranes Nat. Commun. 2013, 2415
29. Mueller, M.; Grauschopf, U.; Maier, T.; Glockshuber, R.; Ban, N. The Structure of a Cytolytic Alpha-Helical Toxin Pore Reveals Its Assembly Mechanism Nature 2009, 726-730
30. Biffi, G.; Tannahill, D.; McCafferty, J.; Balasubramanian, S. Quantitative Visualization of DNA G-Quadruplex Structures in Human Cells Nat. Chem. 2013, 182-186
31. Wu, Y.; Brosh, R. M., Jr. G-Quadruplex Nucleic Acids and Human Disease FEBS J. 2010, 3470-3488
32. Gonzalez, V.; Guo, K.; Hurley, L.; Sun, D. Identification and Characterization of Nucleolin as a C-Myc G-Quadruplex-Binding Protein J. Biol. Chem. 2009, 23622-23635
33. Bidzinska, J.; Cimino-Reale, G.; Zaffaroni, N.; Folini, M. G-Quadruplex Structures in the Human Genome as Novel Therapeutic Targets Molecules 2013, 12368-12395
34. Fry, M. Tetraplex DNA and Its Interacting Proteins Front. Biosci. 2007, 4336-4351
35. von Hacht, A.; Seifert, O.; Menger, M.; Schutze, T.; Arora, A.; Konthur, Z.; Neubauer, P.; Wagner, A.; Weise, C.; Kurreck, J. Identification and Characterization of RNA Guanine-Quadruplex Binding Proteins Nucleic Acids Res. 2014, 6630-6644
36. Pabo, C. O.; Nekludova, L. Geometric Analysis and Comparison of Protein-DNA Interfaces: Why Is There No Simple Code for Recognition J. Mol. Biol. 2000, 597-624
37. Siggers, T. W.; Silkov, A.; Honig, B. Structural Alignment of Protein-DNA Interfaces: Insights into the Determinants of Binding Specificity J. Mol. Biol. 2005, 1027-1045
38. Chen, F. E.; Ghosh, G. Regulation of DNA Binding by Rel/Nf-Kappab Transcription Factors: Structural Views Oncogene 1999, 6845-6852
39. Burns, V.; Kerppola, T. K. Opposite Orientations of a Transcription Factor Heterodimer Bind DNA Cooperatively with Interaction Partners but Have Different Effects on Interferon-Beta Gene Transcription J. Biol. Chem. 2012, 31833-31844
40. Chen, L.; Oakley, M. G.; Glover, J. N.; Jain, J.; Dervan, P. B.; Hogan, P. G.; Rao, A.; Verdine, G. L. Only One of the Two DNA-Bound Orientations of Ap-1 Found in Solution Cooperates with Nfatp Curr. Biol. 1995, 882-889
41. Chytil, M.; Peterson, B. R.; Erlanson, D. A.; Verdine, G. L. The Orientation of the Ap-1 Heterodimer on DNA Strongly Affects Transcriptional Potency Proc. Natl. Acad. Sci. U.S.A. 1998, 14076-14081
42. Bock, L. C.; Griffin, L. C.; Latham, J. A.; Vermaas, E. H.; Toole, J. J. Selection of Single-Stranded DNA Molecules That Bind and Inhibit Human Thrombin Nature 1992, 564-566
43. Padmanabhan, K.; Tulinsky, A. An Ambiguous Structure of a DNA 15-Mer Thrombin Complex Acta Crystallogr. Sect. A: Found. Crystallogr. 1996, 272-282
44. Russo Krauss, I.; Merlino, A.; Randazzo, A.; Novellino, E.; Mazzarella, L.; Sica, F. High-Resolution Structures of Two Complexes between Thrombin and Thrombin-Binding Aptamer Shed Light on the Role of Cations in the Aptamer Inhibitory Activity Nucleic Acids Res. 2012, 8119-8128
45. Pica, A.; Russo Krauss, I.; Merlino, A.; Nagatoishi, S.; Sugimoto, N.; Sica, F. Dissecting the Contribution of Thrombin Exosite I in the Recognition of Thrombin Binding Aptamer FEBS J. 2013, 6581-6588
46. Kawano, R.; Osaki, T.; Sasaki, H.; Takinoue, M.; Yoshizawa, S.; Takeuchi, S. Rapid Detection of a Cocaine-Binding Aptamer Using Biological Nanopores on a Chip J. Am. Chem. Soc. 2011, 8474-8477
47. Wang, Y.; Zheng, D.; Tan, Q.; Wang, M. X.; Gu, L. Q. Nanopore-Based Detection of Circulating Micrornas in Lung Cancer Patients Nat. Nanotechnol. 2011, 668-674
48. Mohammad, M. M.; Iyer, R.; Howard, K. R.; McPike, M. P.; Borer, P. N.; Movileanu, L. Engineering a Rigid Protein Tunnel for Biomolecular Detection J. Am. Chem. Soc. 2012, 9521-9531
49. Arnaut, V.; Langecker, M.; Simmel, F. C. Nanopore Force Spectroscopy of Aptamer-Ligand Complexes Biophys. J. 2013, 1199-1207
50. An, N.; Fleming, A. M.; Middleton, E. G.; Burrows, C. J. Single-Molecule Investigation of G-Quadruplex Folds of the Human Telomere Sequence in a Protein Nanocavity Proc. Natl. Acad. Sci. U.S.A. 2014, 14325-14331
51. Rotem, D.; Jayasinghe, L.; Salichou, M.; Bayley, H. Protein Detection by Nanopores Equipped with Aptamers J. Am. Chem. Soc. 2012, 2781-2787
52. Macaya, R. F.; Waldron, J. A.; Beutel, B. A.; Gao, H.; Joesten, M. E.; Yang, M.; Patel, R.; Bertelsen, A. H.; Cook, A. F. Structural and Functional Characterization of Potent Antithrombotic Oligonucleotides Possessing Both Quadruplex and Duplex Motifs Biochemistry 1995, 4478-4492
53. German, I.; Buchanan, D. D.; Kennedy, R. T. Aptamers as Ligands in Affinity Probe Capillary Electrophoresis Anal. Chem. 1998, 4540-4545
54. Gong, M.; Nikcevic, I.; Wehmeyer, K. R.; Limbach, P. A.; Heineman, W. R. Protein-Aptamer Binding Studies Using Microchip Affinity Capillary Electrophoresis Electrophoresis 2008, 1415-1422
55. Huang, C.-C.; Cao, Z.; Chang, H.-T.; Tan, W. Protein-Protein Interaction Studies Based on Molecular Aptamers by Affinity Capillary Electrophoresis Anal. Chem. 2004, 6973-6981
56. Berezovski, M.; Nutiu, R.; Li, Y.; Krylov, S. N. Affinity Analysis of a Protein-Aptamer Complex Using Nonequilibrium Capillary Electrophoresis of Equilibrium Mixtures Anal. Chem. 2003, 1382-1386
57. Pinto, A.; Bermudo Redondo, M. C.; Ozalp, V. C.; OSullivan, C. K. Real-Time Apta-Pcr for 20 000-Fold Improvement in Detection Limit Mol. Biosyst. 2009, 548-553
58. Ostatna, V.; Vaisocherova, H.; Homola, J.; Hianik, T. Effect of the Immobilisation of DNA Aptamers on the Detection of Thrombin by Means of Surface Plasmon Resonance Anal. Bioanal. Chem. 2008, 1861-1869
59. Wilson, K. A.; Kellie, J. L.; Wetmore, S. D. DNA-Protein Pi-Interactions in Nature: Abundance, Structure, Composition and Strength of Contacts between Aromatic Amino Acids and DNA Nucleobases or Deoxyribose Sugar Nucleic Acids Res. 2014, 6726-6741
60. Kunapuli, S. P.; Bradford, H. N.; Jameson, B. A.; DeLa Cadena, R. A.; Rick, L.; Wassell, R. P.; Colman, R. W. Thrombin-Induced Platelet Aggregation Is Inhibited by the Heptapeptide Leu271-Ala277 of Domain 3 in the Heavy Chain of High Molecular Weight Kininogen J. Biol. Chem. 1996, 11228-11235
61. Maglia, G.; Heron, A. J.; Stoddart, D.; Japrung, D.; Bayley, H. Analysis of Single Nucleic Acid Molecules with Protein Nanopores Meth. Enzymol. 2010, 591-623