Internal vs Fishhook Hairpin DNA: Unzipping Locations and Mechanisms in the α-Hemolysin Nanopore

Journal of Physical Chemistry B

Volumn 118, Issue 45, 2014, Pages 12873-12882

  Ding, Yun ^a   Fleming, Aaron M ^a   White, Henry S ^a   Burrows, Cynthia J ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; NANOPORES; NUCLEIC ACIDS; NUCLEOTIDES; THERMODYNAMICS;

CHEMICAL EQUATIONS; CURRENT DIFFERENCE; CURRENT LEVELS; CURRENT PATTERNS; DOUBLE STRANDED DNA; FUTURE APPLICATIONS; SEQUENCE-DEPENDENT DNA; SYSTEMATIC STUDY;

DNA;

DNA; HEMOLYSIN; PROTEIN BINDING;

BASE PAIRING; CHEMISTRY; CONFORMATION; KINETICS; NANOPORE; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

BASE PAIRING; BASE SEQUENCE; DNA; HEMOLYSIN PROTEINS; KINETICS; NANOPORES; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84927554011     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp5101413     Document Type: Article

References (57)

1. Wanunu, M. Nanopores: A journey towards DNA sequencing Phys. Life Rev. 2012, 9, 125 - 158
2. Ashkenasy, N.; Sánchez-Quesada, J.; Bayley, H.; Ghadiri, M. R. Recognizing a single base in an individual DNA strand: a step toward DNA sequencing in nanopores Angew. Chem., Int. Ed. 2005, 44, 1401 - 1404
3. Howorka, S.; Cheley, S.; Bayley, H. Sequence-specific detection of individual DNA strands using engineered nanopores Nat. Biotechnol. 2001, 19, 636 - 639
4. Butler, T. Z.; Gundlach, J. H.; Troll, M. Ionic current blockades from DNA and RNA molecules in the alpha-hemolysin nanopore Biophys. J. 2007, 93, 3229 - 3240
5. Zhao, Q.; Dimitrov, V.; Yemenicioglu, S.; Aksimentiev, A.; Timp, G. Stretching and unzipping nucleic acid hairpins using a synthetic nanopore Nucleic Acids Res. 2008, 36, 1532 - 1541
6. Kasianowicz, J.; Brandin, E.; Deamer, D. Characterization of individual polynucleotide molecules using a membrane channel Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 13770 - 13773
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-A precision Nat. Biotechnol. 2012, 30, 344 - 348
8. Tian, K.; He, Z.; Wang, Y.; Chen, S.-J.; Gu, L.-Q. Designing a polycationic probe for simultaneous enrichment and detection of microRNAs in a nanopore ACS Nano 2013, 7, 3962 - 3969
9. Shasha, C.; Henley, R. Y.; Stoloff, D. H.; Rynearson, K. D.; Hermann, T.; Wanunu, M. Nanopore-based conformational analysis of a viral RNA drug target ACS Nano 2014, 8, 6425 - 6430
10. 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, 6, 668 - 674
11. Rosen, C. B.; Rodriguez-Larrea, D.; Bayley, H. Single-molecule site-specific detection of protein phosphorylation with a nanopore Nat. Biotechnol. 2014, 32, 179 - 181
12. Rodriguez-Larrea, D.; Bayley, H. Multistep protein unfolding during nanopore translocation Nat. Nanotechnol. 2013, 8, 288 - 295
13. Cracknell, J. A.; Japrung, D.; Bayley, H. Translocating kilobase RNA through the staphylococcal α-hemolysin nanopore Nano Lett. 2013, 13, 2500 - 2505
14. Boersma, A. J.; Bayley, H. Continuous stochastic detection of amino acid enantiomers with a protein nanopore Angew. Chem., Int. Ed. 2012, 51, 9606 - 9609
15. Song, L.; Hobaugh, M.; Shustak, C.; Cheley, S.; Bayley, H.; Gouaux, J. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore Science 1996, 274, 1859 - 1866
16. 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
17. Ayub, M.; Hardwick, S. W.; Luisi, B. F.; Bayley, H. Nanopore-based identification of individual nucleotides for direct RNA sequencing Nano Lett. 2013, 13, 6144 - 6150
18. Dudko, O. K.; Mathé, J.; Szabo, A.; Meller, A.; Hummer, G. Extracting kinetics from single-molecule force spectroscopy: nanopore unzipping of DNA hairpins Biophys. J. 2007, 92, 4188 - 4195
19. Vercoutere, W. A.; Winters-Hilt, S.; Olsen, H.; Deamer, D.; Haussler, D.; Akeson, M. Rapid discrimination among individual DNA hairpin molecules at single-nucleotide resolution using an ion channel Nat. Biotechnol. 2001, 19, 248 - 252
20. Vercoutere, W. A.; Winters-Hilt, S.; DeGuzman, V. S.; Deamer, D.; Ridino, S. E.; Rodgers, J. T.; Olsen, H. E.; Marziali, A.; Akeson, M. Discrimination among individual Watson-Crick base pairs at the termini of single DNA hairpin molecules Nucleic Acids Res. 2003, 31, 1311 - 1318
21. Winters-Hilt, S.; Vercoutere, W.; DeGuzman, V. S.; Deamer, D.; Akeson, M.; Haussler, D. Highly accurate classification of Watson-Crick basepairs on termini of single DNA molecules Biophys. J. 2003, 84, 967 - 976
22. Mathé, J.; Visram, H.; Viasnoff, V.; Rabin, Y.; Meller, A. Nanopore unzipping of individual DNA hairpin molecules Biophys. J. 2004, 87, 3205 - 3212
23. Mathé, J.; Aksimentiev, A.; Nelson, D. R.; Schulten, K.; Meller, A. Orientation discrimination of single-stranded DNA inside the α-hemolysin membrane channel Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 12377 - 12382
24. Deamer, D. W.; Vercoutere, W. A.; DeGuzman, V. S.; Lee, C. C. Sequence-dependent gating of an ion channel by DNA hairpin molecules Nucleic Acids Res. 2006, 34, 6425 - 6437
25. Renner, S.; Bessonov, A.; Gerland, U.; Simmel, F. C. Sequence-dependent unfolding kinetics of DNA hairpins studied by nanopore force spectroscopy J. Phys.: Condens. Matter 2010, 22, 454119 - 454119
26. Branton, D.; Sauer-Budge, A. F.; Nyamwanda, J. A.; Lubensky, D. K. Unzipping kinetics of double-stranded DNA in a nanopore Phys. Rev. Lett. 2003, 90, 238101 - 238104
27. Jin, Q.; Fleming, A. M.; Burrows, C. J.; White, H. S. Unzipping kinetics of duplex DNA containing oxidized lesions in an alpha-hemolysin nanopore J. Am. Chem. Soc. 2012, 134, 11006 - 11011
28. Schibel, A. E. P.; Fleming, A. M.; Jin, Q.; An, N.; Liu, J.; Blakemore, C. P.; White, H. S.; Burrows, C. J. Sequence-specific single-molecule analysis of 8-oxo-7,8-dihydroguanine lesions in DNA based on unzipping kinetics of complementary probes in ion channel recordings J. Am. Chem. Soc. 2011, 133, 14778 - 14784
29. Jin, Q.; Fleming, A. M.; Ding, Y.; Burrows, C. J.; White, H. S. Structural destabilization of DNA duplexes containing single-base lesions investigated by nanopore measurements Biochemistry 2013, 52, 7870 - 7877
30. Liu, A.; Zhao, Q.; Krishantha, D. M.; Guan, X. Unzipping of double-stranded DNA in engineered alpha-hemolysin pores J. Phys. Chem. Lett. 2011, 2, 1372 - 1376
31. Wang, Y.; Tian, K.; Hunter, L. L.; Ritzo, B.; Gu, L. Q. Probing molecular pathways for DNA orientational trapping, unzipping and translocation in nanopores by using a tunable overhang sensor Nanoscale 2014, 6, 11372 - 11379
32. Hyeon, C.; Thirumalai, D. Forced-unfolding and force-quench refolding of RNA hairpins Biophys. J. 2006, 90, 3410 - 3427
33. Woodside, M. T.; Behnke-Parks, W. M.; Larizadeh, K.; Travers, K.; Herschlag, D.; Block, S. M. Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6190 - 6195
34. Schink, S.; Renner, S.; Alim, K.; Arnaut, V.; Simmel, F. C.; Gerland, U. Quantitative analysis of the nanopore translocation dynamics of simple structured polynucleotides Biophys. J. 2012, 102, 85 - 95
35. Liphardt, J.; Onoa, B.; Smith, S. B.; Tinoco, I.; Bustamante, C. Reversible unfolding of single RNA molecules by mechanical force Science 2001, 292, 733 - 737
36. Clausen-Schaumann, H.; Rief, M.; Tolksdorf, C.; Gaub, H. E. Mechanical stability of single DNA molecules Biophys. J. 2000, 78, 1997 - 2007
37. Bustamante, C.; Smith, S. B.; Liphardt, J.; Smith, D. Single-molecule studies of DNA mechanics Curr. Opin. Struct. Biol. 2000, 10, 279 - 285
38. Drew, H. R.; Wing, R. M.; Takano, T.; Broka, C.; Tanaka, S.; Itakura, K.; Dickerson, R. E. Structure of a B-DNA dodecamer: conformation and dynamics Proc. Natl. Acad. Sci. U.S.A. 1981, 78, 2179 - 2183
39. An, N.; Fleming, A. M.; Burrows, C. J. Interactions of the human telomere sequence with the nanocavity of the α-hemolysin ion channel reveal structure-dependent electrical signatures for hybrid folds J. Am. Chem. Soc. 2013, 135, 8562 - 8570
40. Shim, J. W.; Gu, L.-Q. Encapsulating a single G-quadruplex aptamer in a protein nanocavity J. Phys. Chem. B 2008, 112, 8354 - 8360
41. An, N.; Fleming, A. M.; Middleton, E. G.; Burrows, C. J. Size-selective property of α-hemolysin provides signatures for DNA nanostructures formed by the human telomere sequence Proc. Natl. Acad. Sci. U.S.A. 2014, 111, 14325 - 14331
42. McNally, B.; Wanunu, M.; Meller, A. Electromechanical unzipping of individual DNA molecules using synthetic sub-2 nm pores Nano Lett. 2008, 8, 3418 - 3422
43. Sutherland, T. C.; Dinsmore, M. J.; Kraatz, H.-B.; Lee, J. S. An analysis of mismatched duplex DNA unzipping through a bacterial nanopore Biochem. Cell Biol. 2004, 82, 407 - 412
44. Viasnoff, V.; Chiaruttini, N.; Bockelmann, U. Probing DNA base pairing energy profiles using a nanopore Eur. Biophys. J. 2009, 38, 263 - 269
45. Zhang, X.; Wang, Y.; Fricke, B. L.; Gu, L.-Q. Programming nanopore ion flow for encoded multiplex microRNA detection ACS Nano 2014, 8, 3444 - 3450
46. Johnson, R. P.; Fleming, A. M.; Jin, Q.; Burrows, C. J.; White, H. S. Temperature and electrolyte optimization of the α-hemolysin latch sensing zone for detection of base modification in double-stranded DNA Biophys. J. 2014, 107, 924 - 931
47. Mathé, J.; Arinstein, A.; Rabin, Y.; Meller, A. Equilibrium and irreversible unzipping of DNA in a nanopore Europhys. Lett. 2006, 73, 128 - 134
48. White, R. J.; Ervin, E. N.; Yang, T.; Chen, X.; Daniel, S.; Cremer, P. S.; White, H. S. Single ion-channel recordings using glass nanopore membranes J. Am. Chem. Soc. 2007, 129, 11766 - 11775
49. Zhang, B.; Galusha, J.; Shiozawa, P. G.; Wang, G.; Bergren, A. J.; Jones, R. M.; White, R. J.; Ervin, E. N.; Cauley, C. C.; White, H. S. Bench-top method for fabricating glass-sealed nanodisk electrodes, glass nanopore electrodes, and glass nanopore membranes of controlled size Anal. Chem. 2007, 79, 4778 - 4787
50. Henrickson, S. E.; DiMarzio, E. A.; Wang, Q.; Stanford, V. M.; Kasianowicz, J. J. Probing single nanometer-scale pores with polymeric molecular rulers J. Chem. Phys. 2010, 132, 135101 - 135108
51. An, N.; Fleming, A. M.; White, H. S.; Burrows, C. J. Crown ether-electrolyte interactions permit nanopore detection of individual DNA abasic sites in single molecules Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 11504 - 11509
52. Maglia, G.; Heron, A. J.; Stoddart, D.; Japrung, D.; Bayley, H. Analysis of single nucleic acid molecules with protein nanopores Methods Enzymol. 2010, 475, 591 - 623
53. Stoddart, D.; Heron, A. J.; Mikhailova, E.; Maglia, G.; Bayley, H. Single-nucleotide discrimination in immobilized DNA oligonucleotides with a biological nanopore Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 7702 - 7707
54. Rouzina, I.; Bloomfield, V. A. Force-induced melting of the DNA double helix 1. Thermodynamic analysis Biophys. J. 2001, 80, 882 - 893
55. McCauley, M. J.; Williams, M. C. Mechanisms of DNA binding determined in optical tweezers experiments Biopolymers 2007, 85, 154 - 168
56. van Dongen, M. J. P.; Mooren, M. M. W.; Willems, E. F. A.; van der Marel, G. A.; van Boom, J. H.; Wijmenga, S. S.; Hilbers, C. W. Structural features of the DNA hairpin d(ATCCTA-GTTA-TAGGAT): formation of a G-A base pair in the loop Nucleic Acids Res. 1997, 25, 1537 - 1547
57. Krueger, A.; Protozanova, E.; Frank-Kamenetskii, M. D. Sequence-dependent basepair opening in DNA double helix Biophys. J. 2006, 90, 3091 - 3099