RNase a does not translocate the alpha-hemolysin pore

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Krasniqi, Besnik ^a   Lee, Jeremy S ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; RIBONUCLEASE A;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME CONFORMATION; MOLECULAR DYNAMICS; NANOPORE; PARTICLE SIZE; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN REFOLDING; PROTEIN TRANSPORT; PROTEIN UNFOLDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SURFACE CHARGE; ZETA POTENTIAL;

HEMOLYSIN PROTEINS; NANOPORES; NANOSTRUCTURES; NANOTECHNOLOGY; PROTEIN TRANSPORT; RIBONUCLEASE, PANCREATIC;

EID: 84895115435     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088004     Document Type: Article

References (60)

1. Kasianowicz JJ, Brandin E, Branton D, Deamer DW (1996) Characterization of individual polynucleotide molecules using a membrane channel. Proc Natl Acad Sci 93: 13770-13773. (Pubitemid 26424195)
2. Oukhaled G, Mathe J, Biance AL, Bacri L, Betton JM, et al. (2007) Unfolding of proteins and long transient conformations detected by single nanopore recording. Phys Rev Lett 98: 158101.
3. Baran C, Smith GS, Bamm VV, Harauz G, Lee JS (2010) Divalent cations induce a compaction of intrinsically disordered myelin basic protein. Biochem Biophys Res Commun 391: 224-229.
4. Madampage CA, Andrievskaia O, Lee JS (2010) Nanopore detection of antibody prion interactions. Anal Biochem 396: 36-41.
5. Stefureac RI, Madampage CA, Andrievskaia O, Lee JS (2010) Nanopore analysis of the interaction of metal ions with prion proteins and peptides. Biochem Cell Biol 88: 347-358.
6. Stefureac RI, Trivedi D, Marziali A, Lee JS (2010) Evidence that small proteins translocate through silicon nitride pores in a folded conformation. J Phys: Condens Matter 22: 454133.
7. Stefureac R, Waldner L, Howard P, Lee JS (2008) Nanopore analysis of a small 86-residue protein. Small 4: 59-63. (Pubitemid 351205734)
8. Stefureac RI, Lee JS (2008) Nanopore analysis of the folding of zinc fingers. Small 4: 1646-1650.
9. Zhao Q, de Zoysa RS, Wang D, Jayawardhana DA, Guan X (2009) Real-time monitoring of peptide cleavage using a nanopore probe. J Am Chem Soc 131: 6324-6325.
10. Merstorf C, Cressiot B, Pastoriza-Gallego M, Oukhaled A, Betton JM, et al. (2012) Wild type, mutant protein unfolding and phase transition detected by single-nanopore recording. ACS Chem Biol 7: 652-658.
11. Oukhaled A, Bacri L, Pastoriza-Gallego M, Betton JM, Pelta J (2012) Sensing proteins through nanopores: fundamental to applications. ACS Chem Biol 7: 1935-1949.
12. Oukhaled A, Cressiot B, Bacri L, Pastoriza-Gallego M, Betton JM, et al. (2011) Dynamics of completely unfolded and native proteins through solid-state nanopores as a aunction of electric driving force. ACS Nano 5: 3628-3638.
13. Pastoriza-Gallego M, Rabah L, Gibrat G, Thiebot B, van der Goot FG, et al. (2011) Dynamics of unfolded protein transport through an aerolysin pore. J Am Chem Soc 133: 2923-2931.
14. Rodriguez-Larrea D, Bayley H (2013) Multistep protein unfolding during nanopore translocation. Nat Nanotechnol 8: 288-295.
15. Nivala J, Marks DB, Akeson M (2013) Unfoldase-mediated protein translocation through an alpha-hemolysin nanopore. Nat Biotechnol 31: 247-250.
16. Jetha NN, Semenchenko V, Wishart DS, Cashman NR, Marziali A (2013) Nanopore analysis of wild-type and mutant Prion protein (PrP(C)): single molecule discrimination and PrP(C) kinetics. PLoS One 8: e54982.
17. Mohammad, Prakash S, Matouschek A, Movileanu L (2008) Controlling a single protein in a nanopore through electrostatic traps. J Am Chem Soc 130: 4081-4088.
18. Kowalczyk SW, Hall AR, Dekker C (2010) Detection of local protein structures along DNA using solid-state nanopores. Nano Lett 10: 324-328.
19. Kukwikila M, Howorka S (2010) Electrically sensing protease activity with nanopores. J Phys: Condens Matter 22: 454103.
20. Mohammad MM, Iyer R, Howard KR, McPike MP, Borer PN, et al. (2012) Engineering a rigid protein tunnel for biomolecular detection. J Am Chem Soc 134: 9521-9531.
21. Fennouri A, Daniel R, Pastoriza-Gallego M, Auvray L, Pelta J, et al. (2013) Kinetics of Enzymatic Degradation of High Molecular Weight Polysaccharides through a Nanopore: Experiments and Data-Modeling. Anal Chem 85: 8488-8492.
22. Hornblower B, Coombs A, Whitaker RD, Kolomeisky A, Picone SJ, et al. (2007) Single-molecule analysis of DNA-protein complexes using nanopores. Nat Meth 4: 315-317. (Pubitemid 46766974)
23. Smeets RMM, Kowalczyk SW, Hall AR, Dekker NH, Dekker C (2009) Translocation of RecA-coated double-stranded DNA through solid-state nanopores. Nano Lett 9: 3089-3095.
24. Hall AR, van Dorp S, Lemay SG, Dekker C (2009) Electrophoretic Force on a Protein-Coated DNA Molecule in a Solid-State Nanopore. Nano Lett 9: 4441-4445.
25. Niedzwiecki DJ, Iyer R, Borer PN, Movileanu L (2013) Sampling a biomarker of the human immunodeficiency virus across a synthetic nanopore. ACS Nano 7: 3341-3350.
26. Ivankin A, Carson S, Kinney SRM, Wanunu M (2013) Fast, Label-Free Force Spectroscopy of Histone-DNA Interactions in Individual Nucleosomes Using Nanopores. J Am Chem Soc 135: 15350-15352.
27. Soni GV, Dekker C (2012) Detection of nucleosomal substructures using solid-state nanopores. Nano Lett 12: 3180-3186.
28. Talaga DS, Li J (2009) Single-molecule protein unfolding in solid state nanopores. J Am Chem Soc 131: 9287-9297.
29. Payet L, Martinho M, Pastoriza-Gallego M, Betton J-M, Auvray L, et al. (2012) Thermal unfolding of proteins probed at the single molecule level using nanopores. Anal Chem 84: 4071-4076.
30. Bahrami A, Dogan F, Japrung D, Albrecht T (2012) Solid-state nanopores for biosensing with submolecular resolution. Biochem Soc Trans 40: 624-628.
31. Ma L, Cockroft SL (2010) Biological nanopores for single-molecule biophysics. Chembiochem 11: 25-34.
32. Majd S, Yusko EC, Billeh YN, Macrae MX, Yang J, et al. (2010) Applications of biological pores in nanomedicine, sensing, and nanoelectronics. Curr Opin Biotechnol 21: 439-476.
33. Miles BN, Ivanov AP, Wilson KA, Dogan F, Japrung D, et al. (2013) Single molecule sensing with solid-state nanopores: novel materials, methods, and applications. Chem Soc Rev 42: 15-28.
34. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, et al. (1996) Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274: 1859-1866. (Pubitemid 26424757)
35. Meng H, Detillieux D, Baran C, Krasniqi B, Christensen C, et al. (2010) Nanopore analysis of tethered peptides. J Pept Sci 16: 701-708.
36. Christensen C, Baran C, Krasniqi B, Stefureac RI, Nokhrin S, et al. (2011) Effect of charge, topology and orientation of the electric field on the interaction of peptides with the alpha-hemolysin pore. J Pept Sci 17: 726-734.
37. Movileanu L, Schmittschmitt JP, Scholtz JM, Bayley H (2005) Interactions of peptides with a protein pore. Biophys J 89: 1030-1045. (Pubitemid 41098986)
38. Firnkes M, Pedone D, Knezevic J, Doblinger M, Rant U (2010) Electrically facilitated translocations of proteins through silicon nitride nanopores: conjoint and competitive action of diffusion, electrophoresis, and electroosmosis. Nano Lett 10: 2162-2167.
39. Fennouri A, Przybylski C, Pastoriza-Gallego M, Bacri L, Auvray L, et al. (2012) Single molecule detection of Glycosaminoglycan Hyaluronic Acid Oligosaccharides and Depolymeri-zation enzyme activity using a protein nanopore. ACS Nano 6: 9672-9678.
40. Tavassoly O, Lee JS (2012) Methamphetamine binds to alpha-synuclein and causes a conformational change which can be detected by nanopore analysis. FEBS Lett 586: 3222-3228.
41. Madampage C, Tavassoly O, Christensen C, Kumari M, Lee JS (2012) Nanopore analysis: An emerging technique for studying the folding and misfolding of proteins. Prion 6: 116-123.
42. Madampage CA, Maattanen P, Marciniuk K, Brownlie R, Andrievskaia O, et al. (2013) Binding of bovine T194A PrP (C) by PrP (Sc) -specific antibodies: Potential implications for immunotherapy of familial prion diseases. Prion 7: 301-311.
43. Krasniqi B, Lee JS (2012) The importance of adding EDTA for the nanopore analysis of proteins. Metallomics 4: 539-544.
44. Mohammad MM, Movileanu L (2008) Excursion of a single polypeptide into a protein pore: simple physics, but complicated biology. European biophysics journal : EBJ 37: 913-925.
45. Koriazova LK, Montal M (2003) Translocation of botulinum neurotoxin light chain protease through the heavy chain channel. Nat Struct Mol Biol 10: 13-18. (Pubitemid 36034171)
46. Krantz BA, Melnyk RA, Zhang S, Juris SJ, Lacy DB, et al. (2005) A Phenylalanine Clamp Catalyzes Protein Translocation Through the Anthrax Toxin Pore. Science 309: 777-781. (Pubitemid 41077325)
47. Cao A, Welker E, Scheraga HA (2001) Effect of mutation of proline 93 on redox unfolding/folding of bovine pancreatic ribonuclease A. Biochemistry 40: 8536-8541. (Pubitemid 32667259)
48. Miyamoto T, Okano S, Kasai N (2009) Irreversible thermoinactivation of ribonuclease-A by soft-hydrothermal processing. Biotechnol Prog 25: 1678-1685.
49. Wedemeyer WJ, Welker E, Narayan M, Scheraga HA (2000) Disulfide bonds and protein folding. Biochemistry 39: 4207-4216. (Pubitemid 30212634)
50. Neira JL, Rico M (1997) Folding studies on ribonuclease A, a model protein. Fold Des 2: R1-R11. (Pubitemid 127740446)
51. Reinstadler D, Fabian H, Backmann J, Naumann D (1996) Refolding of thermally and urea-denatured ribonuclease A monitored by time-resolved FTIR spectroscopy. Biochemistry 35: 15822-15830. (Pubitemid 26422320)
52. Raines RT (1998) Ribonuclease A. Chem Rev 98: 1045-1066.
53. Joseph-McCarthy D, Fedorov AA, Almo SC (1996) Comparison of experimental and computational functional group mapping of an RNase A structure: implications for computer-aided drug design. Protein Eng 9: 773-780. (Pubitemid 26308525)
54. Sela M, Anfinsen CB (1957) Some spectrophotometric and polarimetric experiments with ribonuclease. Biochim Biophys Acta 24: 229-235.
55. Bastings MM, van Baal I, Meijer EW, Merkx M (2008) One-step refolding and purification of disulfide-containing proteins with a C-terminal MESNA thioester. BMC Biotechnol 8: 76.
56. Japrung D, Dogan J, Freedman KJ, Nadzeyka A, Bauerdick S, et al. (2013) Single-molecule studies of intrinsically disordered proteins using solid-state nanopores. Anal Chem 85: 2449-2456.
57. Takahashi T, Irie M, Ukita T (1969) A comparative study on enzymatic activity of bovine pancreatic ribonuclease A, ribonuclease S and ribonuclease S′. J Biochem (Tokyo) 65: 55-62.
58. Safarian S, Moosavi-Movahedi A (2000) Binding patterns and kinetics of RNase A interaction with RNA. J Protein Chem 19: 335-344. (Pubitemid 32005003)
59. Arakawa H, Neault JF, Tajmir-Riahi HA (2001) Silver(I) complexes with DNA and RNA studied by Fourier transform infrared spectroscopy and capillary electrophoresis. Biophys J 81: 1580-1587. (Pubitemid 32783598)
60. Marino T, Russo N, Toscano M, Pavelka M (2012) Theoretical investigation on DNA/RNA base pairs mediated by copper, silver, and gold cations. Dalton Trans 41: 1816-1823. of Canada