Plasmonic Nanopores for Trapping, Controlling Displacement, and Sequencing of DNA

ACS Nano

Volumn 9, Issue 11, 2015, Pages 10598-10611

  Belkin, Maxim ^a   Chao, Shu Han ^a   Jonsson, Magnus P ^b,c   Dekker, Cees ^c   Aksimentiev, Aleksei ^a  

^a University of Illinois at Urbana Champaign   (United States)

^b LINKÖPING UNIVERSITY   (Sweden)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

DNA sequencing; molecular dynamics; nanoplasmonics; nanopore; plasmonic tweezers

Indexed keywords

BIOINFORMATICS; DNA; DNA SEQUENCES; MOLECULAR DYNAMICS; MOLECULES; NANOPORES; NUCLEIC ACIDS; NUCLEOTIDES; PLASMONS; RAMAN SCATTERING; RAMAN SPECTROSCOPY; SURFACE SCATTERING;

DNA SEQUENCING; METALLIC NANOSTRUCTURE; MOLECULAR DYNAMICS SIMULATIONS; NANOPLASMONICS; NUCLEOTIDE COMPOSITION; PLASMONIC TWEEZERS; SURFACE ENHANCED RAMAN SCATTERING (SERS); SURFACE ENHANCED RAMAN SPECTROSCOPY;

GENE ENCODING;

DNA; SINGLE STRANDED DNA;

DNA SEQUENCE; GENETICS; MOLECULAR DYNAMICS; NANOPORE; NUCLEOTIDE SEQUENCE; RAMAN SPECTROMETRY;

BASE SEQUENCE; DNA; DNA, SINGLE-STRANDED; MOLECULAR DYNAMICS SIMULATION; NANOPORES; SEQUENCE ANALYSIS, DNA; SPECTRUM ANALYSIS, RAMAN;

EID: 84948442592     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b04173     Document Type: Article

References (72)

1. Schloss, J. A. How to Get Genomes at One Ten-Thousandth the Cost Nat. Biotechnol. 2008, 26, 1113-1115 10.1038/nbt1008-1113
2. Kasianowicz, J. J.; Brandin, E.; Branton, D.; Deamer, D. W. Characterization of Individual Polynucleotide Molecules Using a Membrane Channel Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 13770-13773 10.1073/pnas.93.24.13770
3. Branton, D.; Deamer, D. W.; Marziali, A.; Bayley, H.; Benner, S. A.; Butler, T.; Di Ventra, M.; Garaj, S.; Hibbs, A.; Huang, X. et al. The Potential and Challenges of Nanopore Sequencing Nat. Biotechnol. 2008, 26, 1146-1153 10.1038/nbt.1495
4. Venkatesan, B. M.; Bashir, R. Nanopore Sensors for Nucleic Acid Analysis Nat. Nanotechnol. 2011, 6, 615-624 10.1038/nnano.2011.129
5. Manrao, E. A.; Derrington, I. M.; Laszlo, A. H.; Langford, K. W.; Hopper, M. K.; Gillgren, N.; Pavlenok, M.; Niederweis, M.; Gundlach, J. H. Reading DNA at Single-Nucleotide Resolution With a Mutant MspA Nanopore and Phi29 DNA Polymerase Nat. Biotechnol. 2012, 30, 349-353 10.1038/nbt.2171
6. Laszlo, A. H.; Derrington, I. M.; Ross, B. C.; Brinkerhoff, H.; Adey, A.; Nova, I. C.; Craig, J. M.; Langford, K. W.; Samson, J. M.; Daza, R. et al. Decoding Long Nanopore Sequencing Reads of Natural DNA Nat. Biotechnol. 2014, 32, 829-833 10.1038/nbt.2950
7. Cherf, G. M.; Lieberman, K. R.; Rashid, H.; Lam, C. E.; Karplus, K.; Akeson, M. Automated Forward and Reverse Ratcheting of DNA in a Nanopore at 5-Å Precision Nat. Biotechnol. 2012, 30, 344-348 10.1038/nbt.2147
8. McNally, B.; Singer, A.; Yu, Z.; Sun, Y.; Weng, Z.; Meller, A. Optical Recognition of Converted DNA Nucleotides for Single-Molecule DNA Sequencing Using Nanopore Arrays Nano Lett. 2010, 10, 2237-2244 10.1021/nl1012147
9. Tabard-Cossa, V.; Wiggin, M.; Trivedi, D.; Jetha, N. N.; Dwyer, J. R.; Marziali, A. Single- Molecule Bonds Characterized by Solid-State Nanopore Force Spectroscopy ACS Nano 2009, 3, 3009-3014 10.1021/nn900713a
10. Zwolak, M.; Di Ventra, M. Colloquium: Physical Approaches to DNA Sequencing and Detection Rev. Mod. Phys. 2008, 80, 141-165 10.1103/RevModPhys.80.141
11. Saha, K.; Drndić, M.; Nikolić, B. K. DNA Base-Specific Modulation of Microampere Transverse Edge Currents Through a Metallic Graphene Nanoribbon With a Nanopore Nano Lett. 2012, 12, 50-55 10.1021/nl202870y
12. Pang, P.; Ashcroft, B. A.; Song, W.; Zhang, P.; Biswas, S.; Qing, Q.; Yang, J.; Nemanich, R. J.; Bai, J.; Smith, J. T. et al. Fixed-Gap Tunnel Junction for Reading DNA Nucleotides ACS Nano 2014, 8, 11994-12003 10.1021/nn505356g
13. Li, J.; Gershow, M.; Stein, D.; Brandin, E.; Golovchenko, J. A. DNA Molecules and Configurations in a Solid-State Nanopore Microscope Nat. Mater. 2003, 2, 611-615 10.1038/nmat965
14. Storm, A. J.; Storm, C.; Chen, J. H.; Zandbergen, H. W.; Joanny, J.-F.; Dekker, C. Fast DNA Translocation Through a Solid-State Nanopore Nano Lett. 2005, 5, 1193-1197 10.1021/nl048030d
15. Heng, J. B.; Ho, C.; Kim, T.; Timp, R.; Aksimentiev, A.; Grinkova, Y. V.; Sligar, S.; Schulten, K.; Timp, G. Sizing DNA Using a Nanometer-Diameter Pore Biophys. J. 2004, 87, 2905-2911 10.1529/biophysj.104.041814
16. Wanunu, M.; Sutin, J.; McNally, B.; Chow, A.; Meller, A. DNA Translocation Governed by Interactions With Solid-State Nanopores Biophys. J. 2008, 95, 4716-4725 10.1529/biophysj.108.140475
17. Rosenstein, J. K.; Wanunu, M.; Merchant, C. A.; Drndic, M.; Shepard, K. L. Integrated Nanopore Sensing Platform With Sub-Microsecond Temporal Resolution Nat. Methods 2012, 9, 487-492 10.1038/nmeth.1932
18. Smeets, R. M. M.; Keyser, U. F.; Dekker, N. H.; Dekker, C. Noise in Solid-State Nanopores Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 417-421 10.1073/pnas.0705349105
19. Keyser, U. F.; Koeleman, B. N.; van Dorp, S.; Krapf, D.; Smeets, R. M. M.; Lemay, S. G.; Dekker, N. H.; Dekker, C. Direct Force Measurements on DNA in a Solid-State Nanopore Nat. Phys. 2006, 2, 473-477 10.1038/nphys344
20. Peng, H.; Ling, X. S. Reverse DNA Translocation Through a Solid-State Nanopore by Magnetic Tweezers Nanotechnology 2009, 20, 185101 10.1088/0957-4484/20/18/185101
21. Mirsaidov, U.; Comer, J.; Dimitrov, V.; Aksimentiev, A.; Timp, G. Slowing the Translocation of Double-Stranded DNA Using a Nanopore Smaller Than the Double Helix Nanotechnology 2010, 21, 395501 10.1088/0957-4484/21/39/395501
22. Kowalczyk, S. W.; Wells, D. B.; Aksimentiev, A.; Dekker, C. Slowing Down DNA Translocation Through a Nanopore in Lithium Chloride Nano Lett. 2012, 12, 1038-44 10.1021/nl204273h
23. Keyser, U. F. Controlling Molecular Transport Through Nanopores J. R. Soc., Interface 2011, 8, 1369-1378 10.1098/rsif.2011.0222
24. 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 10.1038/nnano.2009.379
25. Di Fiori, N.; Squires, A.; Bar, D.; Gilboa, T.; Moustakas, T. D.; Meller, A. Optoelectronic Control of Surface Charge and Translocation Dynamics in Solid-State Nanopores Nat. Nanotechnol. 2013, 8, 946-951 10.1038/nnano.2013.221
26. Liu, X.; Skanata, M. M.; Stein, D. Entropic Cages for Trapping DNA Near a Nanopore Nat. Commun. 2015, 6, 6222 10.1038/ncomms7222
27. Jonsson, M. P.; Dekker, C. Plasmonic Nanopore for Electrical Profiling of Optical Intensity Landscapes Nano Lett. 2013, 13, 1029-1033 10.1021/nl304213s
28. Juan, M. L.; Righini, M.; Quidant, R. Plasmon Nano-Optical Tweezers Nat. Photonics 2011, 5, 349-356 10.1038/nphoton.2011.56
29. Li, Y.; Nicoli, F.; Chen, C.; Lagae, L.; Groeseneken, G.; Stakenborg, T.; Zandbergen, H. W.; Dekker, C.; Van Dorpe, P.; Jonsson, M. P. Photoresistance Switching of Plasmonic Nanopores Nano Lett. 2015, 15, 776-782 10.1021/nl504516d
30. Garcés-Chávez, V.; Quidant, R.; Reece, P. J.; Badenes, G.; Torner, L.; Dholakia, K. Extended Organization of Colloidal Microparticles by Surface Plasmon Polariton Excitation Phys. Rev. B: Condens. Matter Mater. Phys. 2006, 73, 085417 10.1103/PhysRevB.73.085417
31. Grigorenko, A. N.; Roberts, N. W.; Dickinson, M. R.; Zhang, Y. Nanometric Optical Tweezers Based on Nanostructured Substrates Nat. Photonics 2008, 2, 365-370 10.1038/nphoton.2008.78
32. Huang, L.; Maerkl, S. J.; Martin, O. J. F. Integration of Plasmonic Trapping in a Microfluidic Environment Opt. Express 2009, 17, 6018-6024 10.1364/OE.17.006018
33. Miao, X.; Lin, L. Y. Large Dielectrophoresis Force and Torque Induced by Localized Surface Plasmon Resonance of Au Nanoparticle Array Opt. Lett. 2007, 32, 295-297 10.1364/OL.32.000295
34. Pang, Y.; Gordon, R. Optical Trapping of 12 nm Dielectric Spheres Using Double-Nanoholes in a Gold Film Nano Lett. 2011, 11, 3763-3767 10.1021/nl201807z
35. Pang, Y.; Gordon, R. Optical Trapping of a Single Protein Nano Lett. 2012, 12, 402-406 10.1021/nl203719v
36. Nicoli, F.; Verschueren, D.; Klein, M.; Dekker, C.; Jonsson, M. P. DNA Translocations Through Solid-State Plasmonic Nanopores Nano Lett. 2014, 14, 6917-6925 10.1021/nl503034j
37. Reiner, J. E.; Robertson, J. W. F.; Burden, D. L.; Burden, L. K.; Balijepalli, A.; Kasianowicz, J. J. Temperature Sculpting in Yoctoliter Volumes J. Am. Chem. Soc. 2013, 135, 3087-3094 10.1021/ja309892e
38. Nam, S.; Choi, I.; Fu, C.; Kim, K.; Hong, S.; Choi, Y.; Zettl, A.; Lee, L. P. Graphene Nanopore With a Self-Integrated Optical Antenna Nano Lett. 2014, 14, 5584-5589 10.1021/nl503159d
39. Jeanmaire, D. L.; van Duyne, R. P. Surface Raman Spectroelectrochemistry: Part I: Heterocyclic Aromatic, and Aliphatic Amines Adsorbed on the Anodized Silver Electrode J. Electroanal. Chem. Interfacial Electrochem. 1977, 84, 1-20 10.1016/S0022-0728(77)80224-6
40. Nie, S.; Emory, S. R. Probing Single Molecules and Single Nanoparticles by Surface-Enhanced Raman Scattering Science 1997, 275, 1102-1106 10.1126/science.275.5303.1102
41. Chen, C.; Hutchison, J.; Clemente, F.; Kox, R.; Uji-I, H.; Hofkens, J.; Lagae, L.; Maes, G.; Borghs, G.; Van Dorpe, P. Direct Evidence of High Spatial Localization of Hot Spots in Surface-Enhanced Raman Scattering Angew. Chem., Int. Ed. 2009, 48, 9932-9935 10.1002/anie.200905389
42. Chen, C.; Ye, J.; Li, Y.; Lagae, L.; Stakenborg, T.; Van Dorpe, P. Detection of DNA Bases and Oligonucleotides in Plasmonic Nanoslits Using Fluidic SERS IEEE J. Sel. Top. Quantum Electron. 2013, 19, 4600707-4600707 10.1109/JSTQE.2012.2226564
43. Kneipp, K.; Kneipp, H. Single Molecule Raman Scattering Appl. Spectrosc. 2006, 60, 322A-334A 10.1366/000370206779321418
44. Kneipp, K.; Kneipp, H.; Kartha, V. B.; Manoharan, R.; Deinum, G.; Itzkan, I.; Dasari, R. R.; Feld, M. S. Detection and Identification of a Single DNA Base Molecule Using Surface-Enhanced Raman Scattering (SERS) Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 1998, 57, R6281-R6284 10.1103/PhysRevE.57.R6281
45. Cecchini, M. P.; Wiener, A.; Turek, V. A.; Chon, H.; Lee, S.; Ivanov, A. P.; McComb, D. W.; Choo, J.; Albrecht, T.; Maier, S. A. et al. Rapid Ultrasensitive Single Particle Surface-Enhanced Raman Spectroscopy Using Metallic Nanopores Nano Lett. 2013, 13, 4602-4609 10.1021/nl402108g
46. Aksimentiev, A.; Heng, J. B.; Timp, G.; Schulten, K. Microscopic Kinetics of DNA Translocation Through Synthetic Nanopores Biophys. J. 2004, 87, 2086-2097 10.1529/biophysj.104.042960
47. Oubre, C.; Nordlander, P. Optical Properties of Metallodielectric Nanostructures Calculated Using the Finite Difference Time Domain Method J. Phys. Chem. B 2004, 108, 17740-17747 10.1021/jp0473164
48. Belkin, M.; Maffeo, C.; Wells, D. B.; Aksimentiev, A. Stretching and Controlled Motion of Single-Stranded DNA in Locally Heated Solid-State Nanopores ACS Nano 2013, 7, 6816-6824 10.1021/nn403575n
49. Crick, C. R.; Albella, P.; Ng, B.; Ivanov, A. P.; Roschuk, T.; Cecchini, M. P.; Bresme, F.; Maier, S. A.; Edel, J. B. Precise Attoliter Temperature Control of Nanopore Sensors Using a Nanoplasmonic Bullseye Nano Lett. 2015, 15, 553-559 PMID: 25467211 10.1021/nl504536j
50. Dahlin, A. B. Sensing Applications Based on Plasmonic Nanopores: The Hole Story Analyst 2015, 140, 4748-4759 10.1039/C4AN02258K
51. Wells, D. B.; Belkin, M.; Comer, J.; Aksimentiev, A. Assessing Graphene Nanopores for Sequencing DNA Nano Lett. 2012, 12, 4117-4123 10.1021/nl301655d
52. Luan, B.; Peng, H.; Polonsky, S.; Rossnagel, S.; Stolovitzky, G.; Martyna, G. Base-By-Base Ratcheting of Single Stranded DNA Through a Solid-State Nanopore Phys. Rev. Lett. 2010, 104, 238103 10.1103/PhysRevLett.104.238103
53. Shankla, M.; Aksimentiev, A. Conformational Transitions and Stop-And-Go Nanopore Transport of Single-Stranded DNA on Charged Graphene Nat. Commun. 2014, 5, 5171 10.1038/ncomms6171
54. Maffeo, C.; Ngo, T. T. M.; Ha, T.; Aksimentiev, A. A Coarse-Grained Model of Unstructured Single-Stranded DNA Derived From Atomistic Simulation and Single-Molecule Experiment J. Chem. Theory Comput. 2014, 10, 2891-2896 10.1021/ct500193u
55. Timp, W.; Comer, J.; Aksimentiev, A. DNA Base-Calling From a Nanopore Using a Viterbi Algorithm Biophys. J. 2012, 102, L37-L39 10.1016/j.bpj.2012.04.009
56. Le Ru, E. C.; Etchegoin, P. G. Quantifying SERS Enhancements MRS Bull. 2013, 38, 631-640 10.1557/mrs.2013.158
57. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics With NAMD J. Comput. Chem. 2005, 26, 1781-1802 10.1002/jcc.20289
58. Foloppe, N.; MacKerell, A. D., Jr. All-Atom Empirical Force Field for Nucleic Acids: I. Parameter Optimization Based on Small Molecule and Condensed Phase Macromolecular Target Data J. Comput. Chem. 2000, 21, 86-104 10.1002/(SICI)1096-987X(20000130)21:2<86::AID-JCC2>3.0.CO;2-G
59. Cruz-Chu, E. R.; Aksimentiev, A.; Schulten, K. Water-Silica Force Field for Simulating Nanodevices J. Phys. Chem. B 2006, 110, 21497-21508 10.1021/jp063896o
60. Braun, R.; Sarikaya, M.; Schulten, K. Genetically Engineered Gold-Binding Polypeptides: Structure Prediction and Molecular Dynamics J. Biomater. Sci., Polym. Ed. 2002, 13, 747-757 10.1163/156856202760197384
61. 2+ Ions for All-Atom Molecular Dynamics Simulations of Nucleic Acid Systems J. Phys. Chem. Lett. 2012, 3, 45-50 10.1021/jz201501a
62. Miyamoto, S.; Kollman, P. A. SETTLE: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Molecules J. Comput. Chem. 1992, 13, 952-962 10.1002/jcc.540130805
63. Batcho, P. F.; Case, D. A.; Schlick, T. Optimized Particle-Mesh Ewald/Multiple-Time Step Integration for Molecular Dynamics Simulations J. Chem. Phys. 2001, 115, 4003-4018 10.1063/1.1389854
64. Humphrey, W.; Dalke, A.; Schulten, K. VMD Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
65. van Dijk, M.; Bonvin, A. M. J. J. 3D-DART: a DNA Structure Modelling Server Nucleic Acids Res. 2009, 37, W235-W239 10.1093/nar/gkp287
66. Martyna, G. J.; Tobias, D. J.; Klein, M. L. Constant Pressure Molecular Dynamics Algorithms J. Chem. Phys. 1994, 101, 4177-4189 10.1063/1.467468
67. Belkin, M.; Chao, S.-H.; Giannetti, G.; Aksimentiev, A. Modeling Thermophoretic Effects in Solid-State Nanopores J. Comput. Electron. 2014, 13, 826-838 10.1007/s10825-014-0594-8
68. Wells, D. B.; Abramkina, V.; Aksimentiev, A. Exploring Transmembrane Transport Through α-Hemolysin With Grid-Steered Molecular Dynamics J. Chem. Phys. 2007, 127, 125101 10.1063/1.2770738
69. Futamata, M.; Maruyama, Y.; Ishikawa, M. Local Electric Field and Scattering Cross Section of Ag Nanoparticles Under Surface Plasmon Resonance by Finite Difference Time Domain Method J. Phys. Chem. B 2003, 107, 7607-7617 10.1021/jp022399e
70. Johnson, P. B.; Christy, R. W. Optical Constants of the Noble Metals Phys. Rev. B 1972, 6, 4370-4379 10.1103/PhysRevB.6.4370
71. Bohren, C. F.; Huffman, D. R. Absorption and Scattering of Light by Small Particles; John Wiley & Sons, Inc.: New York, 1983.
72. Kwon, Y.-W.; Choi, D. H.; Jin, J.-I. Optical, Electro-Optic and Optoelectronic Properties of Natural and Chemically Modified DNAs Polym. J. 2012, 44, 1191-1208 10.1038/pj.2012.165