Nanopore Analysis of Wild-Type and Mutant Prion Protein (PrPC): Single Molecule Discrimination and PrPC Kinetics

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Jetha, Nahid N ^a   Semenchenko, Valentyna ^b   Wishart, David S ^b,c   Cashman, Neil R ^d   Marziali, Andre ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; ASPARAGINE; ASPARTIC ACID; PRION PROTEIN;

ACCURACY; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CREUTZFELDT JAKOB DISEASE; FATAL FAMILIAL INSOMNIA; MOLECULAR DYNAMICS; NANOANALYSIS; NANOPORE; POINT MUTATION; PREDICTIVE VALUE; PROTEIN CONFORMATION; PROTEIN STABILITY; WILD TYPE;

KINETICS; MUTATION; NANOPORES; PRION DISEASES; PRIONS; PROTEIN CONFORMATION;

EID: 84873504625     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054982     Document Type: Article

References (45)

1. Collinge J, (2001) Prion diseases of humans and animals: Their causes and molecular basis. Annu. Rev. Neurosci. 24: 519-550.
2. Prusiner SB, (1982) Novel proteinaceous infectious particles cause scrapie. Science. 216: 136-144.
3. Prusiner SB, (1998) Prions. Proc. Natl. Acad. Sci. USA. 95: 13363-13383.
4. Coulthart MB, Cashman NR, (2001) Variant Creutzfeldt-Jakob disease: A summary of current scientific knowledge in relation to public health. Can. Med. Assoc. J. 165: 51-58.
5. Caughey B, Kocisko DA, Raymond GJ, Lansbury PT Jr, (1995) Aggregates of scrapie-associated prion protein induce the cell-free conversion of protease-sensitive prion protein to the protease-resistant state. Chem. Biol. 2: 807-817.
6. Caughey B, Raymond GJ, Kocisko DA, Lansbury PT Jr, (1997) Scrapie infectivity correlates with converting activity, protease resistance, and aggregation of scrapie-associated prion protein in guanidine denaturation studies. J. Virol. 71: 4107-4110.
7. van der Kamp MW, Daggett V, (2010) Pathogenic Mutations in the Hydrophobic Core of the Human Prion Protein Can Promote Structural Instability and Misfolding. J. Mol. Biol. 404: 732-748.
8. Vanik DL, Surewicz WK, (2002) Disease-associated F198S Mutation Increases the Propensity of the Recombinant Prion Protein for Conformational Conversion to Scrapie-like Form. J. Biol. Chem. 277: 49065-49070.
9. Meli M, Gasset M, Colombo G, (2011) Dynamic diagnosis of familial prion diseases supports the β2-α2 loop as a universal interference target. PLoS One. 6: e19093.
10. Ma L, Cockroft SL, (2010) Biological nanopores for single molecule biophysics. ChemBioChem. 11: 25-34.
11. DeGuzman VS, Lee CC, Deamer DW, Vercoutere WA, (2006) Sequence-dependent gating of an ion channel by DNA hairpin molecules. Nucleic Acids Res. 34: 6425-6437.
12. Manrao EA, Derrington IM, Laszlo AH, Langford KW, Hopper MK, et al. (2012) Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase. Nat. Biotechnol. 30: 349-353.
13. Lin J, Kolomeisky A, Meller A, (2010) Helix-coil kinetics of individual polyadenylic acid molecules in a protein channel. Phys. Rev. Lett. 104: 158101.
14. Venkatesan BM, Bashir R, (2011) Nanopore sensors for nucleic acid analysis. Nat. Nanotechnol. 6: 615-624.
15. Branton D, Deamer DW, Marziali A, Bayley H, Benner SA, et al. (2008) The potential and challenges of nanopore sequencing. Nat. Biotechnol. 26: 1146-1153.
16. Payet L, Martinho M, Pastoriza-Gallego M, Betton JM, Auvray L, et al. (2012) Thermal unfolding of proteins probed at the single molecule level using nanopores. Anal. Chem. 84: 4071-4076.
17. 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.
18. Movileanu L, Schmittschmitt JP, Scholtz JM, Bayley H, (2005) Interactions of peptides with a protein pore. Biophys. J. 89: 1030-1045.
19. Mohammad MM, Movileanu L, (2008) Excursion of a single polypeptide into a protein pore: Simple physics but complicated biology. Eur. Biophys. J. 37: 913-925.
20. Mohammad MM, Prakash S, Matouschek A, Movileanu L, (2008) Controlling a single protein in a nanopore through electrostatic traps. J. Am. Chem. Soc. 130: 4081-4088.
21. Soskine M, Biesemans A, Moeyaert B, Cheley S, Bayley H, et al. (2012) An Engineered ClyA Nanopore Detects Folded Target Proteins by Selective External Association and Pore Entry. Nano Lett. 12: 4895-4900.
22. Pastoriza-Gallego M, Rabah L, Gibrat G, Thiebot B, Gisou van der Gout F, et al. (2011) Dynamics of unfolded protein transport through an aerolysin pore. J. Am. Chem. Soc. 133: 2923-2931.
23. Goldfarb LG, Petersen RB, Tabaton M, Brown P, LeBlanc AC, et al. (1992) Fatal familial insomnia and familial Creutzfeldt Jakob disease: disease phenotype determined by a DNA polymorphism. Science 258: 806-808.
24. Monari L, Chen SG, Brown P, Parachi P, Petersen RB, et al. (1994) Fatal familial insomnia and familial Creutzfeldt-Jakob disease: different prion proteins determined by a DNA polymorphism. Proc. Natl. Acad. Sci. USA. 91: 2839-2842.
25. Julien O, Chatterjee S, Bjorndahl TC, Sweeting B, Acharya S, et al. (2011) Relative and regional stabilities of the hamster, mouse, rabbit, and bovine prion proteins toward urea unfolding assessed by nuclear magnetic Resonance and circular dichroism spectroscopies. Biochemistry. 50: 7536-7545.
26. Bjorndahl TC, Zhou G, Liu X, Perez-Pineiro R, Semenchenko V, et al. (2011) Detailed biophysical characterization of the acid-induced PrPC to PrPβ conversion process. Biochemistry. 50: 1162-1173.
27. Perez-Pineiro R, Bjorndahl TC, Berjanskii MV, Hau D, Li L, et al. (2011) The prion protein binds thiamine. FEBS J. 278: 4002-4014.
28. Akeson M, Branton D, Kasianowicz JJ, Brandin E, Deamer DW, (1999) Microsecond timescale discrimination among polycytidylic acid, polyadenylic acid, and polyuridylic acid as homopolymers or as segments within single RNA molecules. Biophys. J. 77: 3227-3233.
29. Jetha N, Wiggin M, Marziali A (2009) Forming an α-hemolysin nanopore for single molecule analysis. In: Lee JW, Foote RS, editors. Micro and Nano Technologies in Bioanalysis. Humana Press, Totowa NJ. 113-127.
30. Wanunu M, Morrison W, Rabin Y, Grosberg AY, Meller A, (2010) Electrostatic focusing of unlabelled DNA into nanoscale pores using a salt gradient. Nat. Nanotechnol. 5: 160-165.
31. Hatlo MM, Panja D, Roij RV, (2011) Translocation of DNA molecules through nanopores with salt gradients: The role of osmotic flow. Phys. Rev. Lett. 107: 068101.
32. Nandi PK, Leclerc E, Marc D, (2002) Unusual property of prion protein unfolding in neutral salt solution. Biochemistry. 41: 11017-11024.
33. Apetri AC, Surewicz WK, (2003) Atypical effect of salts on the thermodynamic stability of human prion protein, J. Biol. Chem. 278: 22187-22192.
34. Movileanu L, Cheley S, Howorka S, Braha O, Bayley H, (2001) Location of a constriction in the lumen of a transmembrane pore by targeted covalent attachment of polymer molecules. J. Gen. Physiol. 117: 239-251.
35. Jetha N, Wiggin M, Marziali A (2009) Nanopore force spectroscopy on DNA duplexes. In: Lee JW, Foote RS, editors. Micro and Nano Technologies in Bioanalysis. Humana Press, Totowa NJ. 129-150.
36. Chung SH, Moore JB, Xia L, Premkumar LS, Gage PW, (1990) Characterization of single channel currents using digital signal processing techniques based on hidden markov models. Phil. Trans. R. Soc. Lond. B. 329: 265-285.
37. Churbanov A, Winters-Hilt S, (2008) Clustering ionic flow blockade toggles with a mixture of HMMs. BMC Bioinf. 9: S13.
38. Venkataramanan L, Sigworth FJ, (2002) Applying hidden markov models to the analysis of single ion channel activity. Biophys. J. 82: 1930-1942.
39. Winters-Hilt S, Vercoutere W, DeGuzman VS, Deamer D, Akeson M, et al. (2003) Highly accurate classification of watson-crick basepairs on termini of single DNA molecules. Biophys. J. 84: 967-976.
40. Vercoutere WA, Winters-Hilt S, DeGuzman VS, Deamer D, Ridino SE, et al. (2003) Discrimination among individual Watson-Crick base pairs at the termini of single DNA hairpin molecules. Nucleic Acids Res. 31: 1311-1318.
41. Rabiner LR, (1989) A tutorial on hidden markov models and selected applications in speech recognition. Proc. IEEE. 77: 257-286.
42. Alonso DO, DeArmond SJ, Cohen FE, Daggett V, (2001) Mapping the early steps in the pH-induced conformational conversion of the prion protein. Proc. Natl. Acad. Sci. USA. 98: 2985-2989.
43. Riek R, Wider G, Billeter M, Hornemann S, Glockshuber R, et al. (1998) Prion protein NMR structure and familial human spongiform encephalopathies. Proc. Natl. Acad. Sci. USA. 95: 11667-11672.
44. Zuegg J, Gready JE, (1999) Molecular dynamics simulations of human prion protein: Importance of correct treatment of electrostatic interactions. Biochemistry. 38: 13862-13876.
45. Barducci A, Chelli R, Procacci P, Schettino V, (2005) Misfolding pathways of the prion protein probed by molecular dynamics simulations. Biophys. J. 88: 1334-1343.