Nanopore-based single-molecule DNA analysis

Nanomedicine

Volumn 2, Issue 4, 2007, Pages 459-481

  Healy, Ken ^a  

^a UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

hemolysin; DNA and RNA translocation; DNA sequencing; Single molecule analysis; Solid state nanopores; Synthetic

Indexed keywords

ALPHA HEMOLYSIN; AVIDIN; BETA CYCLODEXTRIN; BIOTIN; DNA; DOUBLE STRANDED DNA; ELECTROLYTE; HEMOLYSIN; MACROGOL; POLYADENYLIC ACID; POLYCYTIDYLIC ACID; POLYMER; POLYNUCLEOTIDE; SINGLE STRANDED DNA; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; AUTOMATION; BASE PAIRING; BIOSENSOR; CALCULATION; DNA DENATURATION; DNA DETERMINATION; DNA HYBRIDIZATION; DNA SEQUENCE; ELECTRIC CURRENT; ELECTRIC POTENTIAL; ELECTROPHORETIC MOBILITY; GENOTYPE; HIDDEN MARKOV MODEL; ION TRANSPORT; MOLECULAR DYNAMICS; NANOPORE; NUCLEIC ACID TRANSPORT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; SUPPORT VECTOR MACHINE; TEMPERATURE DEPENDENCE;

DNA; ELECTROCHEMISTRY; MICROMANIPULATION; MOLECULAR PROBE TECHNIQUES; NANOSTRUCTURES; OPTICAL TWEEZERS; POROSITY;

EID: 34548505259     PISSN: 17435889     EISSN: None     Source Type: Journal    
DOI: 10.2217/17435889.2.4.459     Document Type: Review

References (121)

1. Marzialli A, Akeson M: New DNA sequencing methods. Annu. Rev. Biomed. Eng. 3, 195-223 (2001).
2. Metzker ML: Emerging technologies in DNA sequencing. Genome Res. 15, 1767-1776 (2005).
3. Gabig-Ciminska M: Developing nucleic acid-based electrical detection systems. Microb. Cell Fact. 5, 9 (2006).
4. Deamer DW, Akeson M: Nanopores and nucleic acids: prospects for ultrarapid sequencing. Trends Biotechnol. 18, 147-151 (2000).
5. Deamer DW, Branton D: Characterization of nucleic acids by nanopore analysis. Acc. Chem. Res. 35, 817-825 (2002).
6. Nakane JJ, Akeson M, Marziali A: Nanopore sensors for nucleic acid analysis. J. Phys. Condens. Matter 15, R1365-R1393 (2003).
7. Rhee M, Burns MA: Nanopore sequencing technology: research trends and applications. Trends Biotechnol. 24, 580-586 (2006).
8. Dekker C: Solid-state nanopores. Nat. Nanotechnol. 2, 209-215 (2007).
9. Wanunu M, Meller A: Single molecule analysis of nucleic acids and DNA-protein interactions using nanopores. In: Laboratory Manual on Single Molecules. Ha T, Selvin P (Eds). Cold Spring Harbor Press, NY, USA (2007).
10. Meller A: Dynamics of polynucleotide transport through nanometre-scale pores. J. Phys. Condens. Matter 15, R581-R607 (2003).
11. Bezrukov SM, Vodyanoy I, Parsegian VA: Counting polymers moving through a single-ion channel. Nature 370, 279-281 (1994).
12. Movileanu L, Howorka S, Braha O, Bayley H: Detecting protein analytes that modulate transmembrane movement of a polymer chain within a single protein pore. Nat. Biothecnol. 18, 1091-1095 (2000).
13. Sun L, Crooks RM: Single carbon nanotube membranes: a well-defined model for studying mass transport through nanoporous materials. J. Am. Chem. Soc. 122, 12340-12345 (2000).
14. Howorka S, Nam J, Bayley H, Kahne D: Stochastic detection of monovalent and bivalent protein-ligand interactions. Agnew. Chem. Int. Ed. 43, 842-846 (2004).
15. Heins EA, Siwy ZS, Baker LA, Martin CR: Detecting single porphyrin molecules in a conically shaped synthetic nanopore. Nano. Lett. 5, 1824-1829 (2005).
16. Siwy Z, Trofin L, Kohli P, Baker LA, Trautmann C, Martin CR: Protein biosensors based on biofunctionalized conical gold nanotubes. J. Am. Chem. Soc. 127, 5000-5001 (2005).
17. Stefureac R, Long YT, Kraatz HB, Howard P, Lee JS: Transport of α-helical peptides through a-hemolysin and aerolysin pores. Biochemistry 45, 9172-9179 (2006).
18. Kraslinikov OV, Rodrigues CG, Bezrukov SM: Single polymer molecules in a Protein nanopore in the limit of a strong polymer-pore attraction. Phys. Rev. Lett. 97, 018301 (2006).
19. Kasianowicz JJ, Brandin E, Branton D, Deamer DW: Characterization of individual polynucleotide molecules using a membrane channel. Proc. Natl Acad. Sci. USA 93, 13770-13773 (1996).
20. DeBlois RW, Bean CP: Counting and sizing of submicron particles by resistive pulse technique. Rev. Sci. Instrum. 41, 909-916 (1970).
21. DeBlois RW, Bean CP, Wesley RKA: Electrokinetic mesurements with submicron particles and pores by resistive pulse technique. J. Colloid Interface Sci. 61, 323-335 (1977).
22. Hille B: Ion Channels of Excitable Membranes (3rd Edition). Sinauer, Sunderland, MA, USA (2001).
23. Mueller P, Rudin DO, Tien HT, Wescott WC: Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 194, 979-980 (1962).
24. Bean RC, Shepherd WC, Chan H, Eichner J: Discrete conductance fluctuations in lipid bilayer protein membranes. J. Gen. Physiol. 53, 741-757 (1969).
25. Hladky SB, Haydon DA: Discreteness of conductance change in bimolecular lipid membranes in presence of certain antibiotics. Nature 225, 451-453 (1970).
26. Montal M, Mueller P: Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl Acad. Sci. USA 69, 3561-3566 (1972).
27. Neher E, Sakman B, Steinbach JH: The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pflügers Arch. 375, 219-228 (1978).
28. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ: Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391, 85-100 (1981).
29. Neher E, Sakmann B: Single-channel currents recorded from membrane of denervated frog muscle-fibers. Nature 260, 799-802 (1976).
30. Krasilnikov OV, Sabirov RZ, Ternovsky VI, Merzliak PG, Tashmukhamedov BA: The structure of Staphylococcus-aureus α-toxin-induced ionic channel. Gen. Physiol. Biophys. 7, 467-473 (1988).
31. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H: Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1865 (1996).
32. Szabo I, Bathori G, Tombola F, Brini M, Coppola A, Zoratti M: DNA translocation across planar bilayers containing Bacillus subtilis ion channels. J Biol. Chem. 272, 25275-25282 (1997).
33. Szabo I, Bathori G, Tombola F et al.: Double-stranded DNA can be translocated across a planar membrane containing purified mitochondrial porin. FASEB J. 12, 495-502 (1998).
34. Akeson M, Branton D, Kasianowicz JJ, Brandin E, Deamer DW: Microsecond time-scale discrimination among polycytidylic acid, polyadenylic acid, and polyuridylic acid as homopolymers or as segments within single RNA molecules. Biophys. J. 77, 3227-3233 (1999).
35. Meller A, Nivon L, Brandin E, Golovchenko J, Branton D: Rapid nanopore discrimination between single polynucleotide molecules. Proc. Natl Acad. Sci. USA 97, 1079-1084 (2000).
36. Khulbe PK, Mansuripur M, Gruener R: DNA translocation through α-hemolysin nanopores with potential application to macromolecular data storage. J. Appl. Phys. 97, 104317 (2005).
37. Wang H, Dunning JE, Huang APH, Nyamwanda JA, Branton D: DNA heterogeneity and phosphorylation unveiled by single-molecule electrophoresis. Proc. Natl Acad. Sci. USA 101, 13472-13477 (2004).
38. Mathé J, Aksimentiev A, Nelson DR, Schulten K, Meller A: Orientation discrimination of single-stranded DNA Inside the α-hemolysin membrane channel. Proc. Natl. Acad. Sci. USA 102,12377-12382 (2005).
39. Butler TZ, Gundlach JH, Troll MA: Determination of RNA orientation during translocation through a biological nanopore. Biophys. J. 90, 190-199 (2006).
40. Meller A, Branton D: Single molecule measurements of DNA transport through a nanopore. Electrophoresis 23, 2583-2591 (2002).
41. Henrickson SE, Misakian M, Robertson B, Kasianowicz JJ: Driven DNA transport into an asymmetric nanometer-scale pore. Phys. Rev. Lett. 85, 3057-3060 (2000).
42. Nakane J, Akeson M, Marziall A: Evaluation of nanopores as candidates for electronic analyte detection. Electrophores 23, 2592-2601 (2002).
43. Meller A, Nivon L, Branton D: Voltage-driven DNA translocation through a nanopore. Phys. Rev. Lett. 86, 3435-3438 (2001).
44. Muthukumar M: Polymer translocation through a hole. J. Chem. Phys. 111, 10371-10374 (1999).
45. Lubensky DK, Nelson DR: Driven polymer translocation through a narrow pore. Biophys. J. 77, 1824-1838 (1999).
46. Jeon TJ, Malmstadt N, Schmidt JJ: Hydrogel-encapsulated lipid membranes. J. Am. Chem. Soc. 128, 42-43 (2006).
47. Kasianowicz JJ, Henrickson SE, Weetall HH, Robertson B: Simultaneous multianalyte detection with a nanometer-scale pore. Anal. Chem 73, 2268-2272 (2001).
48. Chandler EL, Smith AL, Burden LM, Kasianowicz JJ, Burden DL: Membrane surface dynamics of DNA-threaded nanopores revealed by simultaneous single-molecule optical and ensemble electrical recording. Langmuir 20, 898-905 (2004).
49. Nakane J, Wiggin M, Marziali A: A nanosensor for transmembrane capture and identification of single nucleic acid molecules. Biophys. J. 87, 615-621 (2004).
50. Tropini C, Marziali A: Multi-nanopore force spectroscopy for DNA analysis. Biophys. J, 92, 1632-1637 (2007).
51. Sauer-Budge AF, Nyamwanda JA, Lubensky DK, Branton D: Unzipping kinetics of double-stranded DNA in a nanopore. Phys. Rev. Lett. 90, 238101 (2003).
52. Mathé J, Visram H, Viasnoff V, Rabin Y, Meller A: Nanopore unzipping of individual DNA hairpin molecules. Biophys J. 87, 3205-3212 (2004).
53. Mathé J, Arinstein A, Rabin Y. Meffer A: Equilibrium and irreversible unzipping of DNA in a nanopore. Europhys. Lett. 73, 128-134 (2006).
54. Bates M, Burns M, Meller A: Dynamics of DNA molecules in a membrane channel probed by active control techniques. Biophys. J. 84, 2366-2372 (2003).
55. Hornblower B, Coombs A, Whitaker RD et al.: Single-molecule analysis of DNA-protein complexes using nanopores. Nat. Methods, 4, 315-317 (2007).
56. Sánchez-Quesada J, Saghatelian A, Cheley S, Bayley H, Ghadirt MR: Single DNA rotaxanes of a transmembrane pore protein. Agnew. Chem. Int. Ed. 43, 3063-3067 (2004).
57. Ashkenasy N, Sanchez-Quesada J, Bayley H, Ghadiri MR: Recognizing a single base in an individual DNA strand: a step toward DNA sequencing in nanopores. Agnew. Chem. Int. Ed. 44, 1401-1404 (2005).
58. Vercoutere W, Winters-Hilt S, Olsen H, Dearner D, Haussler D, Akeson M: Rapid discrimination among individual DNA hairpin molecules at single-nucleotide resolution using an ion channel. Nat. Biotechnol.. 19, 248-252 (2001).
59. Winters-Hilt S, Vercoutere W, DeGuzman VS, Dearner D, Akeson M, Haussier D: Highly accurate classification of Watson-Crick basepairs on termini of single DNA molecules. Biophys. J. 84, 967-976 (2003).
60. Winters-Hilt S, Akeson M: Nanopore chemininformatics. DNA Cell Biol. 23, 675-683 (2004).
61. Vercoutere WA, Winters-Hilt S, DeGuzman VS et al.: Discrimination among individual Watson-Crick base pairs at the termini of single DNA hairpin molecules, Nucleic Acids Res. 31, 1311-1318 (2003).
62. DeCuzman VS, Lee CC, Dearner DW, Vercoutere WA: Sequence-dependent gating of an ion channel by DNA hairpin molecules. Nucleic Acids Res. 34, 6425-6437 (2006).
63. Iqbal R, Landry M, Winters-Hilt S: DNA molecule classification using feature primitives. BMC Bioinformatics 7 (Suppl. 2), S15 (2006).
64. Landry M, Winters-Hilt S: Analysis of nanopore detector measurements using machine learning methods, with application to single-molecule kinetic analysis. BMC Bioinformatics (2007) (In press).
65. Churbanov A, Baribault C, Winters-Hilt S: Duration learning for nanopore ionic flow blockade analysis. BMC Bioinformatics (2007) (In press).
66. Winters-Hilt S, Landry M, Akeson M et al.: Cheminformatics methods for novel nanopore analysis of HIV DNA termini. BMC Bioinformatics 7(Suppl. 2), S22 (2006).
67. Winters-Hilt S, Davis A, Amin I, Morales E: Preliminary nanopore cheminformatics of protein binding to non-terminal and terminal DNA regions: analysis of transcription factor binding and retroviral DNA terminus. dynamics. BMC Bionformatics (2007) (In press).
68. Thomson K, Amin I, Moral E: Winters-Hilt S: Preliminary nanopore cheminformatics analysis of aptamer-target binding strength. BMC Bioinformatics (2007) (In press).
69. Winters-Hilt S: The α-hemolysin nanopore transduction detector: single-molecule binding studies and immunological screening of antibodies and aptamers. BMC Bioinformatics (2007) (In press).
70. Feynman RP: Simulating physics with computers. Int. J. Theor. Phys. 21, 467-488. (1982).
71. DiVincenzo DP: Quantum computation. Science 270, 255-261 (1995).
72. Howorka S, Cheley S, Bayley H: Sequence-specific detection of individual DNA strands using engineered nanopores. Nat. Biotechnol. 19, 636-639 (2001).
73. Howorka S, Movileanu L, Braha O. Bayley H: Kinetics of duplex formation for individual DNA strands within a single protein nanopore. Proc. Natl. Acad. Sci. USA 98, 12996-13001 (2001).
74. Howorka S, Bayley H: Probing distance and electrical potential within a protein pore with tethered DNA. Biophys. J. 83, 3202-3210 (2002).
75. Aksimentiev A, Schulten K: Imaging α-hemolysin with molecular dynamics: ionic conductance, osmotic permeability, and the electrostatic potential map. Biophys. J. 88, 3745-3761 (2005).
76. Astier Y, Braha O, Bayley H: Toward single molecule DNA sequencing: Direct identification of ribonucleoside and deoxyribonucleoside 5′-monophosphates by using an engineered protein nanopore equipped with a molecular adapter. J. Am. Chem. Soc. 128, 1705-1710 (2006).
77. Jett JH, Keller RA, Martin JC et al.: High-speed DNA sequencing: an approach based upon fluorescence detection of single molecules. J. Biomol. Struct. Dyn. 7 301-309 (1989).
78. White RJ, Zhang B, Daniel S et al.: Ionic conductivity of the aqueous layer separating a lipid bilayer membrane and a glass support. Langmuir 22, 10777-10783 (2006).
79. Kang XF, Cheley S, Rice-Ficht AC, Bayley H: A storable encapsulated bilayer chip containing a single protein nanopore. J. Am. Chem. Soc. 129, 4701-4705 (2007).
80. Li J, Stein D, McMullan C, Branton D, Aziz MJ, Golovchenko JA: Ion beam sculpting on the nanoscale. Nature 412, 166-169 (2001).
81. Kim MJ, Wanunu M, Bell DC, Meller A: Rapid fabrication of uniformly sized nanopores and nanopore arrays for parallel DNA analysis. Adv. Mater. 18, 3149-3153 (2006).
82. Wu S, Park SR, Ling XS: Lithography-free formation of nanopores in plastic membranes using laser heating. Nano Lett. 6, 2571-2576 (2006).
83. Park SR, Peng HB, Ling XS: Fabrication of nanopores in silicon chips using feedback chemical etching. Small 3, 116-119 (2007).
84. Healy K, Schiedt B, Morrison AP: A review of solid-state nanopore technologies for nanopore-based DNA analysis. Nanomedicine (In Press).
85. Li J, Gershow M, Stein D, Brandin E, Golovchenko JA: DNA molecules and configurations in a solid-state nanopore microscope. Nat. Mater. 2, 611-615 (2003).
86. Chang H, Kosari F, Andreadakis G, Alam MA, Vasmatzis G, Bashir R: DNA-mediated fluctuations in ionic current through silicon oxide nanopore channels. Nano Lett. 4, 1551-1556 (2004).
87. Ho C, Qiao R, Heng JB et al.: Electrolytic transport through a synthetic nanometer-diameter pore. Proc. Natl Acad Sci. USA 102, 10445-10450(2005).
88. Storm AJ, Chen JH, Zandbergen HW, Dekker C: Translocation of double-strand DNA through a silicon oxide nanopore. Phys. Rev. E 71, 051903 (2005).
89. Heng JB, Ho C. Kim T et al.: Sizing DNA using a nanometer-diameter pore. Biophys. J. 87, 2905-2911 (2004).
90. Heng JB, Dimitrov V, Grinkova YV et al.: The detection of DNA using a silicon nanopore. In: IEDM'03 Technical Digest. IEEE International, Washington, DC, USA 32.2.1-32.2.4 (2003).
91. Fologea D, Gershow M, Ledden B, McNabb DS, Golovchenko JA, Li J: Detecting single stranded DNA with a solid state nanopore. Nano Lett. 5, 1905-1909 (2005).
92. Harell CC, Choi Y, Horne LP, Baker LA, Siwy ZS, Martin CR: Resistive-pulse DNA detection with a conical nanopore sensor. Langmuir 22, 10837-10843 (2006).
93. Chen P, Gu JJ, Brandin E, Kim YR, Wang Q, Branton D: Probing angle DNA molecule transport using fabricated nanopores. Nano Lett. 4, 2293-2298 (2004).
94. Heng JB, Aksimentiev A, Ho C et al.: Stretching DNA using the electric field in a synthetic nanopore. Nano Lett. 5, 1883-1888 (2005).
95. Heng JB, Aksimentiev A, Ho C et al.: The electromechanics of DNA in a synthetic nanopore. Biophys J. 90, 1098-1106 (2006).
96. Mara A, Siwy Z, Trautmann C, Wan J, Kamme F: An asymmetric polymer nanopore for single molecule detection. Nano Lett. 4, 497-501 (2004).
97. Storm AJ, Storm C, Chen JH, Zandbergen H, Joanny JF, Dekker C: Fast DNA translocation through a solid-state nanopore. Nano Lett. 5, 1193-1197 (2005).
98. Fologea D, Brandin E, Uplinger J, Branton D, Li J: DNA conformation and base number simultaneously determined in a nanopore. Electrophories (2007) (In press).
99. Stellwagen E, Dong Q, Stellwagen NC: Monovalent cations affect the free solution mobility of DNA by perturbing the hydrogen-bonded structure of water. Biopolymers 78, 62-68 (2005).
100. Chen P, Mitsui T, Farmer DB, Golovchenko J, Gordon RG, Branton D: Atomic layer deposition to fine-tune the surface properties and diameters of fabricated nanopores. Nano Lett. 4, 1333-1337 (2004).
101. Frontali C, Dore E, Ferrauto A et al.: Absolute method for the determination of the persistence length of native DNA from electron-micrographs. Biopolymers 18, 1353-1373 (1979).
102. Baumann CG, Smith SB, Bloomfield VA, Bustamante C: Ionic effects on the elasticity of single DNA molecules. Proc. Natl Acad. USA 94, 6185-6190 (1997).
103. Fan R, Karnik R, Yue M, Li DY, Majumdar A, Yang PD: DNA translocation in inorganic nanotubes. Nano Lett. 5, 1633-1637 (2005).
104. Smeets RMM, Keyser UF, Krapf D, Wu MY, Dekker NH, Dekker C: Salt dependence of Ion transport and DNA translocation through solid-state nanopores. Nano Lett. 6, 89-95 (2006).
105. Chang H, Venkatesan B, Iqbal S et al.: DNA counterion current and saturation examined by a MEMS-based solid state nanopore sensor. Biomed. Microdev. 8, 263-269 (2006).
106. Fologea D, Uplinger J, Thomas B, McNabb DS, Li J: Slowing DNA translocation in a solid-state nanopore. Nano Lett. 5, 1734-1737 (2005).
107. Keyser UF, Koeleman BN, van Dorp S et al.: Direct force measurements on DNA in a solid-state nanopore. Nat. Phys. 2, 473-477 (2006).
108. Keyser UF, van der Does J, Dekker C, Dekker NH: Optical tweezers for force measurements on DNA in nanopores. Rev. Sci. Instrum. 77, 105105 (2006).
109. Storm AJ, Chen JH, Ling XS, Zandbergen HW, Dekker C: Fabrication of solid-state nanopores with single-nanometre precision. Nat. Mater. 2, 537-540 (2003).
110. Iqbal SM, Akin D, Bashir R: Solid-state nanopore channels with DNA selectivity. Nat. Nanotechnol. 2, 243-248 (2007).
111. Kohli P, Harrell CC, Cao Z, Gasparac R, Tan W, Martin CR: DNA-functionalized nanotube membranes with single-base mismatch selectivity. Science 305, 984-986 (2004).
112. Healy K, Morrison AP: Recent progress in automated production and robust packaging for track-etched single-nanopores. Biophys. J. (Suppl.), 163A (2007).
113. Heng JB, Aksimentiev A, Ho C et al.: Beyond the gene chip. Bell Labs Tech. J. 10, 5-22 (2005).
114. Gracheva ME, Xiong AL, Aksimentiev A, Schulten K, Timp G, Leburton JP: Simulation of the electric response of DNA translocation through a semiconductor nanopore-capacitor. Nanotechnology 17, 622-633 (2006).
115. Gracheva ME, Aksimentiev A, Leburton JP: Electrical signatures of single-stranded DNA with single base mutations in a nanopore capacitor. Nanotechnology 17, 3160-3165 (2006).
116. King GM, Golovchenko JA: Probing nanotube-nanopore interactions. Phys. Rev. Lett. 95, 216103 (2005).
117. Lagerqvist J, Zwolak M, DiVentra M: Fast DNA sequencing via transverse electronic transport. Nano Lett. 6, 779-782 (2006).
118. Zhang XG, Krstic PS, Zikic R, Wells JC, Fuentes-Cabrera M: First-principles transversal DNA conductance deconstructed. Biophys. J. 91, L4-L6 (2006).
119. Fischbein MD, Drndic M: Sub-10 nm device fabrication in a transmission electron microscope. Nano Lett. 7, 1329-1337 (2007).
120. Mika S, Schäfer C, Laskov P, Tax D, Müller K: Support vector machines. In: Handbook of Computational Statistics: Concepts and Methods. Gentle JE, Härdle W, Mori Y (Eds). Springer, Heidelberg, Germany 841-876 (2004).
121. Aksimentiev A, Heng JB, Timp G, Schulten K: Microscopic kinetics of DNA translocation through synthetic nanopores. Biophys. J. 87, 2086-2097 (2004).