Partitioning of individual flexible polymers into a nanoscopic protein pore

Biophysical Journal

Volumn 85, Issue 2, 2003, Pages 897-910

  Movileanu, Liviu ^a   Cheley, Stephen ^a   Bayley, Hagan ^a,b  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; BACTERIAL PROTEIN; HEMOLYSIN; MACROGOL; MEMBRANE PROTEIN; NANOPARTICLE; POLYMER; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; BIOTECHNOLOGY; DYNAMICS; ELECTRICITY; IONIC STRENGTH; KINETICS; MASS; MOLECULAR WEIGHT; NONHUMAN; PARTICLE SIZE; PROTEIN STRUCTURE; REACTION ANALYSIS; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); MUS; POSIBACTERIA; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 0041843734     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74529-9     Document Type: Article

References (89)

1. Akeson, M., D. Branton, J. J. Kasianowicz, E. Brandin, and D. W. Deamer. 1999. 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.
2. Ambjornsson, T., S. P. Apell, Z. Konkoli, E. A. Di Marzio, and J. J. Kasianowicz. 2002. Charged polymer membrane translocation. J. Chem. Phys. 117:4063-4073.
3. Bayley, H., O. Braha, and L.-Q. Gu. 2000. Stochastic sensing with protein pores. Adv. Matter. 12:139-142.
4. Bayley, H., and P. S. Cremer. 2001. Stochastic sensors inspired by biology. Nature. 413:226-230.
5. Berezhkovskii, A. M., and I. V. Gopich. 2003. Translocation of rodlike polymers through membrane channels. Biophys. J. 84:787-793.
6. Bezrukov, S. M., and I. Vodyanoy. 1993. Probing alamethicin channels with water-soluble polymers. Effect on conductance of channel states. Biophys. J. 64:16-25.
7. Bezrukov, S. M., I. Vodyanoy, and V. A. Parsegian. 1994. Counting polymers moving through a single ion channel. Nature. 370:279-281.
8. Bezrukov, S. M., and I. Vodyanoy. 1995. Noise-induced enhancement of signal transduction across voltage-dependent ion channels. Nature. 378:362-364.
9. Bezrukov, S. M., I. Vodyanoy, R. A. Brutyan, and J. J. Kasianowicz. 1996. Dynamics and free energy of polymer partitioning into a nanoscale pore. Macromolecules. 29:8517-8522.
10. Bezrukov, S. M., and J. J. Kasianowicz. 1997. The charge state of an ion channel controls neutral polymer entry into its pore. Eur. Biophys. J. 26:471-476.
11. Bezrukov, S. M. 2000. Ion channels as molecular Coulter counters to probe metabolite transport. J. Membr. Biol. 174:1-13.
12. Bhakdi, S., R. Füssle, and J. Tranum-Jensen. 1981. Staphylococcal α-toxin: oligomerization of hydrophilic monomers to form amphiphilic hexamers induced through contact with deoxycholate micelles. Proc. Natl. Acad. Sci. USA. 78:5475-5479.
13. Bläsi, U., and R. Young. 1996. Two beginnings for a single purpose: the dual-start holins in the regulation of phage lysis. Mol. Microbial. 21:675-682.
14. Blatz, A. L., and K. L. Magleby. 1986. Correcting single channel data for missed events. Biophys. J. 49:967-980.
15. Boyd, R. H., R. R. Chance, and G. Ver Strate. 1996. Effective dimensions of oligomers in size exclusion chromatography. A molecular dynamics simulation study. Macromolecules. 29:1182-1190.
16. Braha, O., B. Walker, S. Cheley, J. J. Kasianowicz, L. Song, J. E. Gouaux, and H. Bayley. 1997. Designed protein pores as components for biosensors. Chem. Biol. 4:497-505.
17. Carneiro, C. M. M., O. V. Krasilnikov, L. N. Yuldasheva, A. C. Campos de Carvalho, and R. A. Nogueira. 1997. Is the mammalian porin channel, VDAC, a perfect cylinder in the high conductance state? FEBS Lett. 416:187-189.
18. Cheley, S., O. Braha, X. Lu, S. Conlan, and H. Bayley. 1999. A functional protein pore with a "retro" transmembrane domain. Protein Sci. 8:1257-1267.
19. Cifra, P., and T. Bleha. 2001. Partition coefficients and the free energy of confinement from simulations of nonideal polymer systems. Macromolecules. 34:605-613.
20. Colquhoun, D., and F. J. Sigworth. 1995. Fitting and statistical analysis of single channel records. In Single-Channel Recording. Plenum Press, New York.
21. Daoud, M., and P.-G. de Gennes. 1977. Statistics of macromolecular solutions trapped in small pores. J. Physique. 38:85-93.
22. de Gennes, P.-G. 1979. Scaling Concepts in Polymer Physics. Cornell University Press, Ithaca, NY.
23. de Gennes, P.-G. 1999a. Flexible polymers in nanopores. Adv. Polym. Sci. 138:91-105.
24. de Gennes, P.-G. 1999b. Passive entry of DNA molecule into a small pore. Proc. Natl. Acad. Sci. USA. 96:7262-7264.
25. Deamer, D. W., and M. Akeson. 2000. Nanopores and nucleic acids: prospects for ultrarapid sequencing. Trends Biotechnol. 18:147-151.
26. Deamer, D. W., and D. Branton. 2002. Characterization of nucleic acids by nanopore analysis. Acc. Chem. Res. 35:817-825.
27. Dhara, D., and P. R. Chatterji. 1999. Electrophoretic transport of poly(ethylene glycol) chains through poly(acrylamide) gel. J. Phys. Chem. B. 103:8458-8461.
28. Gedde, U. W. 1995. Polymer Physics. Chapman & Hall, London, UK.
29. 1-ATPase. Nature. 409:637-641.
30. Gorbunov, A. A., and A. M. Skvortsov. 1995. Statistical properties of confined molecules. Adv. Coll. Interf. Sci. 62:31-108.
31. Gouaux, E. 1998. α-Hemolysin from Staphylococcus aureus: an archetype of β-barrel, channel-forming toxins. J. Struct. Biol. 121:110-122.
32. Gu, L.-Q., O. Braha, S. Conlan, S. Cheley, and H. Bayley. 1999. Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter. Nature. 398:686-690.
33. Gu, L.-Q., and H. Bayley. 2000. Interaction of the non-covalent molecular adapter, β-cyclodextrin, with the staphylococcal α-hemolysin pore. Biophys. J. 79:1967-1975.
34. Gu, L.-Q., S. Cheley, and H. Bayley. 2001a. Capture of a single molecule in a nanocavity. Science. 291:636-640.
35. Gu, L.-Q., S. Cheley, and H. Bayley. 2001b. Prolonged residence time of a noncovalent molecular adapter, β-cyclodextrin, within the lumen of mutant α-hemolysin pores. J. Gen. Physiol. 118:481-494.
36. Hanke, W., and W.-R. Schlue. 1993. Planar Lipid Bilayers. Academic Press, London.
37. Henrickson, S. E., M. Misakian, B. Robertson, and J. J. Kasianowicz. 2000. Driven DNA transport into an asymmetric nanometer-scale pore. Phys. Rev. Lett. 85:3057-3060.
38. Howorka, S., L. Movileanu, X. Lu, M. Magnon, S. Cheley, O. Braha, and H. Bayley. 2000. A protein pore with a single polymer chain tethered within the lumen. J. Am. Chem. Soc. 122:2411-2416.
39. Howorka, S., L. Movileanu, O. Braha, and H. Bayley. 2001a. Kinetics of duplex formation for individual DNA strands within a single protein nanopore. Proc. Natl. Acad. Sci. USA. 98:12996-13001.
40. Howorka, S., S. Cheley, and H. Bayley. 2001b. Sequence-specific detection of individual DNA strands using engineered nanopores. Nat. Biotechnol. 19:636-639.
41. Howorka, S., and H. Bayley. 2002. Probing distance and electrical potential within a protein pore with tethered DNA. Biophys. J. 83:3202-3210.
42. Jeppesen, C., J. Y. Wong, T. L. Kuhl, J. N. Israelachvili, N. Mullah, S. Zalipsky, and C. M. Marques. 2001. Impact of polymer tether length on multiple ligand-receptor bond formation. Science. 293:465-468.
43. Johnson, A. E., and M. A. van Waes. 1999. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15:799-842.
44. Kasianowicz, J. J., E. Brandin, D. Branton, and D. W. Deamer. 1996. Characterization of individual polynucleotide molecules using a membrane channel. Proc. Natl. Acad. Sci. USA. 93:13770-13773.
45. Kasianowicz, J. J., S. E. Henrickson, H. H. Weetall, and B. Robertson. 2001. Simultaneous multianalyte detection with a nanometer-scale pore. Analyt. Chem. 73:2268-2272.
46. Kienberger, F., V. P. Pastushenko, G. Kada, H. J. Gruber, C. Riener, H. Schindler, and P. Hinterdorf. 2000. Static and dynamical properties of single poly(ethylene glycol) molecules investigated by force spectroscopy. Single Mol. 1:123-128.
47. Kong, C. Y., and M. Muthukumar. 2002. Modeling of polynucleotide translocation through proteins and nanotubes. Electrophoresis. 23:2697-2703.
48. Korchev, Y. E., G. M. Alder, A. Bakhramov, C. L. Bashford, B. S. Joomun, E. V. Sviderskaya, P. N. R. Usherwood, and C. A. Pasternak. 1995. Staphylococcus aureus alpha-toxin-induced pores: channel-like behavior in lipid bilayers and patch clamped cells. J. Membr. Biol. 143:143-151.
49. Krasilnikov, O. V., R. Z. Sabirov, V. I. Temovsky, P. G. Merzliak, and J. N. Muratkhodjaev. 1992. A simple method for the determination of the pore radius of ions channels in planar lipid bilayer membranes. FEMS Microbiol. Immunol. 105:93-100.
50. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
51. LeDuc, P., C. Haber, G. Bao, and D. Wirtz. 1999. Dynamics of individual flexible polymers in a shear flow. Nature. 399:564-566.
52. Liu, L., P. Li, and S. A. Asher. 1999. Entropic trapping of macromolecules by mesoscopic periodic voids in a polymer hydrogel. Nature. 397:141-144.
53. Lubensky, D. K., and D. R. Nelson. 1999. Driven polymer translocation through a narrow pore. Biophys. J. 77:1824-1838.
54. Madden, J. C., N. Ruiz, and M. Caparon. 2001. Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in gram-positive bacteria. Cell. 104:143-152.
55. Marziali, A., and M. Akeson. 2001. New DNA sequencing methods. Ann. Rev. Biomed. Eng. 3:195-223.
56. McManus, O. B., A. L. Blatz, and K. L. Magleby. 1987. Sampling, log binning, fitting, and plotting durations of open and shut intervals from single channels and the effects of noise. Pflugers Arch. 410:530-553.
57. McManus, O. B., and K. L. Magleby. 1988. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. 402:79-120.
58. Meller, A., L. Nivon, E. Brandin, J. Golovchenko, and D. Branton. 2000. Rapid nanopore discrimination between single polynucleotide molecules. Proc. Natl. Acad. Sci. USA. 97:1079-1084.
59. Meller, A., L. Nivon, and D. Branton. 2001. Voltage-driven DNA translocations through a nanopore. Phys. Rev. Lett. 86:3435-3438.
60. Meller, A., and D. Branton. 2002. Single molecule measurements of DNA transport through a nanopore. Electrophoresis. 23:2583-2591.
61. Menestrina, G. 1986. Ionic channels formed by Staphylococcus aureus alpha-toxin: voltage-dependent inhibition by divalent and trivalent cations. J. Membr. Biol. 90:177-190.
62. Merzlyak, P. G., L. N. Yuldasheva, C. G. Rodrigues, C. M. M. Cameiro, O. V. Krasilnikov, and S. M. Bezrukov. 1999. Polymeric nonelectrolytes to probe pore geometry: application to the α-toxin transmembrane channel. Biophys. J. 77:3023-3033.
63. Montal, M., and P. Mueller. 1972. Formation of bimolecular membranes from lipid monolayers and study of their electrical properties. Proc. Natl. Acad. Sci. USA. 69:3561-3566.
64. Movileanu, L., S. Howorka, O. Braha, and H. Bayley. 2000. Detecting protein analytes that modulate transmembrane movement of a polymer chain within a single protein pore. Nat. Biotechnol. 18:1091-1095.
65. Movileanu, L., S. Cheley, S. Howorka, O. Braha, and H. Bayley. 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.
66. Movileanu, L., and H. Bayley. 2001. Partitioning of a polymer into a nanoscopic protein pore obeys a simple scaling law. Proc. Natl. Acad. Sci. USA. 98:10137-10141.
67. Muthukumar, M. 1999. Polymer translocation through a hole. J. Chem. Phys. 111:10371-10374.
68. Muthukumar, M. 2001. Translocation of a confined polymer through a hole. Phys. Rev. Lett. 86:3188-3191.
69. Muthukumar, M. 2002. Theory of sequence effects on DNA translocation through proteins and nanopores. Electrophoresis. 23:1417-1420.
70. Nakane, J., M. Akeson, and A. Marziali. 2002. Evaluation of nanopores as candidates for electronic analyte detection. Electrophoresis. 23:2592-2601.
71. Parsegian, V. A., S. M. Bezrukov, and I. Vodyanoy. 1995. Watching small molecules move: interrogating ionic channels using neutral solutes. Biosci. Rep. 15:503-514.
72. Rex, S., M. J. Zuckermann, M. Lafleur, and J. R. Silvius. 1998. Experimental and Monte Carlo simulation studies of the thermodynamics of polyethylene glycol chains grafted to lipid bilayers. Biophys. J. 75:2900-2914.
73. Rostovtseva, T. K., E. M. Nestorovich, and S. M. Bezrukov, 2002. Partitioning of differently sized poly(ethylene glycol)s into OmpF porin. Biophys. J. 82:160-169.
74. Salman, H., D. Zbaida, Y. Rabin, D. Chatenay, and M. Elbaum. 2001. Kinetics and mechanism of DNA uptake into the cell nucleus. Proc. Natl. Acad. Sci. USA. 98:7247-7252.
75. Slater, G. W., S. Guillouzic, M. G. Gauthier, J.-F. Mercier, M. Kenward, L. C. McCormick, and F. Tessier. 2002. Theory of DNA electrophoresis. Electrophoresis. 23:3791-3816.
76. Smith, D. E., H. P. Babcock, and S. Chu. 1999. Single-polymer dynamics in steady shear flow. Science. 283:1724-1727.
77. Song, L., M. R. Hobaugh, C. Shustak, S. Cheley, H. Bayley, and J. E. Gouaux. 1996. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1859-1865.
78. Strobl, G. 1997. The Physics of Polymers, 2nd Ed. Springer, Berlin.
79. Sung, W., and P. J. Park. 1996. Polymer translocation through a pore in a membrane. Phys. Rev. Lett. 77:783-786.
80. Vercoutere, W., S. Winters-Hilt, H. Olsen, D. Deamer, D. Haussler, and M. Akeson. 2001. Rapid discrimination among individual DNA hairpin molecules at single-nucleotide resolution using an ion channel. Nat. Biotechnol. 19:248-252.
81. Vercoutere, W., and M. Akeson. 2002. Biosensors for DNA sequence detection. Curr. Opin. Chem. Biol. 6:816-822.
82. Vercoutere, W. A., S. Winters-Hilt, V. S. DeGuzman, D. Deamer, S. E. Ridino, J. T. Rodgers, H. E. Olsen, A. Marziali, and M. Akeson. 2003. Discrimination among individual Watson-Crick bases pairs at the termini of single DNA hairpin molecules. Nucleic Acids Res. 31:1311-1318.
83. Vodyanoy, I., and S. M. Bezrukov. 1992. Sizing of an ion pore by access resistance measurements. Biophys. J. 62:10-11.
84. Walker, B. J., M. Krishnasastry, L. Zorn, J. J. Kasianowicz, and H. Bayley. 1992. Functional expression of the α-hemolysin of Staphylococcus aureus in intact Escherichia coli and in cell lysates. J. Biol. Chem. 267:10902-10909.
85. Wang, H., and D. Branton. 2001. Nanopores with a spark for single-molecule detection. Nat. Biotechnol. 19:622-623.
86. Winters-Hilt, S., W. Vercoutere, V. S. DeGuzman, D. Deamer, M. Akeson, and D. Haussler. 2003. Highly accurate classification of Watson-Crick basepairs on termini of single DNA molecules. Biophys. J. 84:967-976.
87. Wong, J. Y., T. L. Kuhl, J. N. Israelachvili, N. Mullah, and S. Zalipsky. 1997. Direct measurement of a tethered ligand-receptor interaction potential. Science. 275:820-822.
88. Zimmerberg, J., and V. A. Parsegian. 1986. Polymer inaccessible volume changes during opening and closing of a voltage-dependent ionic channel. Nature. 323:36-39.
89. Zimmerman, S. B., and L. D. Murphy. 1996. Electrophoresis of polyethylene glycols and related materials as sodium dodecyl sulfate complexes. Anal. Biochem. 234:190-193.