Studying confined polymers using single-molecule DNA experiments

  • Hsieh, Chih-Chen (Department of Chemical Engineering, National Taiwan University) ;
  • Doyle, Patrick S. (Department of Chemical Engineering, Massachusetts Institute of Technology)
  • Published : 2008.09.30

Abstract

The development of fluorescence microscopy of single-molecule DNA in the last decade has fostered a bold jump in the understanding of polymer physics. With the recent advance of nanotechnology, devices with well-defined dimensions that are smaller than typical DNA molecules can be readily manufactured. The combination of these techniques has provided an unprecedented opportunity for researchers to examine confined polymer behavior, a topic far less understood than its counterpart. Here, we review the progress reported in recent studies that investigate confined polymer dynamics by means of single-molecule DNA experiments.

Keywords

References

  1. Bakajin, O. B., T. A. J. Duke, C. F. Chou, S. S. Chan, R. H. Austin and E. C. Cox, 1998, Electrohydrodynamic stretching of DNA in confined environments, Phys. Rev. Lett. 80, 2737-2740 https://doi.org/10.1103/PhysRevLett.80.2737
  2. Balducci, A. and C. C. Hsieh, P. S. Doyle, 2007, Relaxation of stretched DNA in slitlike confinement, Phys. Rev. Lett. 99, 4
  3. Balducci, A., P. Mao, J. Y. Han and P. S. Doyle, 2006, Doublestranded DNA diffusion in slitlike nanochannels, Macromolecules 39, 6273-6281 https://doi.org/10.1021/ma061047t
  4. Batchelor, G. K., 1967, An introduction to fluid dynamics, Cambridge University Press, Cambridge
  5. Baumann, C. G., S. B. Smith, V. A. Bloomfield and C. Bustamante, 1997, Ionic effects on the elasticity of single DNA molecules, Proc. Natl. Acad. Sci. USA 94, 6185-6190
  6. Brochard, F., 1977, Dynamics of polymer chains trapped in a slit, J. Phys. (Paris) 38, 1285-1291 https://doi.org/10.1051/jphys:0197700380100128500
  7. Brochard, F. and P. G. de Gennes, 1977, Dynamics of confined polymer chains, J. Chem. Phys. 67, 52-56 https://doi.org/10.1063/1.434540
  8. Burkhardt, T. W., 1995, Free energy of a semiflexible polymer confined along an axis, J. Phys. A 28, L629-L635
  9. Burkhardt, T. W., 1997, Free energy of a semiflexible polymer in a tube and statistics of a randomlyaccelerated particle, J. Phys. A 30, L167-L172
  10. Cabodi, M., S. W. P. Turner and H. G. Craighead, 2002, Entropic recoil separation of long DNA molecules, Anal. Chem. 74, 5169-5174 https://doi.org/10.1021/ac025879a
  11. Campbell, L. C., M. J. Wilkinson, A. Manz, P. Camilleri and C. J. Humphreys, 2004, Electrophoretic manipulation of single molecules in nanofabricated capillaries, Lab Chip 4, 225-229 https://doi.org/10.1039/b312592k
  12. Chan, E. Y., N. M. Goncalves, R. A. Haeusler, A. J. Hatch, J. W. Larson, A. M. Maletta, G. R. Yantz, E. D. Carstea, M. Fuchs, G. G. Wong, S. R. Gullans and R. Gilmanshin, 2004, DNA mapping using microfluidic stretching and single-molecule detection of fluorescent site-specific tags, Genome Res. 14, 1137-1146 https://doi.org/10.1101/gr.1635204
  13. Chen, Y. L., M. D. Graham, J. J. de Pablo, K. Jo and D. C. Schwartz, 2005, DNA molecules in microfluidic oscillatory flow, Macromolecules 38, 6680-6687 https://doi.org/10.1021/ma050238d
  14. Chen, Y. L., M. D. Graham, J. J. de Pablo, G. C. Randall, M. Gupta and P. S. Doyle, 2004, Conformation and dynamics of single DNA molecules in parallel-plate slit microchannels, Phys. Rev. E 70, 060901
  15. Craighead, H., 2006, Future lab-on-a-chip technologies for interrogating individual molecules, Nature 442, 387-393 https://doi.org/10.1038/nature05061
  16. Cross, J. D., E. A. Strychalski and H. G. Craighead, 2007, Sizedependent DNA mobility in nanochannels, J. Appl. Phys. 102, 024701 https://doi.org/10.1063/1.2757202
  17. Daoud, M. and P. G. de Gennes, 1977, Statistics of macromolecular solutions trapped in small pores, J. Phys. (Paris) 38, 85-93
  18. de Gennes, P. G., 1976, Dynamics of entangled polymer-solutions 1. rouse model, Macromolecules 9, 587-593 https://doi.org/10.1021/ma60052a011
  19. Dechadilok, P. and W. M. Deen, 2006, Hindrance factors for diffusion and convection in pores, Ind. Engin. Chem. Res. 45, 6953-6959 https://doi.org/10.1021/ie051387n
  20. Deen, W. M., 1987, Hindered transport of large molecules in liquid-filled pores, AICHE J. 33, 1409-1425 https://doi.org/10.1002/aic.690330902
  21. Des Cloizeaux, J. and G. Jannink, 1990, Polymers in solution : their modelling and structure, Oxford science publications, Oxford University Press, New York
  22. Dobrynin, A. V., 2005, Electrostatic persistence length of semiflexible and flexible polyelectrolytes, Macromolecules 38, 9304-9314 https://doi.org/10.1021/ma051353r
  23. Dobrynin, A. V., 2006, Effect of counterion condensation on rigidity of semiflexible polyelectrolytes, Macromolecules 39, 9519-9527 https://doi.org/10.1021/ma061030a
  24. Dobrynin, A. V. and M. Rubinstein, 2005, Theory of polyelectrolytes in solutions and at surfaces, Prog. Polym. Sci. 30, 1049-1118 https://doi.org/10.1016/j.progpolymsci.2005.07.006
  25. Douville, N., D. Huh and S. Takayama, 2008, DNA linearization through confinement in nanofluidic channels, Anal. Bioanal. Chem. 391(7), 2395-2409 https://doi.org/10.1007/s00216-008-1995-y
  26. Eijkel, J. C. T. and A. van den Berg, 2005, Nanofluidics: what is it and what can we expect from it?, Microfluidics and Nanofluidics 1, 249-267 https://doi.org/10.1007/s10404-004-0012-9
  27. Fang, L., C. C. Hsieh and R. G. Larson, 2007, Molecular imaging of shear-induced polymer migration in dilute solutions near a surface, Macromolecules 40, 8490-8499 https://doi.org/10.1021/ma062630c
  28. Ferree, S. and W. H. Blanch, 2003, Electrokinetic stretching of tethered DNA, Biophys. J. 85, 2539-2546 https://doi.org/10.1016/S0006-3495(03)74676-1
  29. Fixman, M. and J. Skolnick, 1978, Polyelectrolyte excluded volume paradox, Macromolecules 11, 863-867 https://doi.org/10.1021/ma60065a004
  30. Gorbunov, A. A. and A. M. Skvortsov, 1995, Statistical properties of confined macromolecules, Adv. Colloid Interface Sci. 62, 31-108 https://doi.org/10.1016/0001-8686(95)00270-Z
  31. Guo, L. J., X. Cheng and C. F. Chou, 2004, Fabrication of sizecontrollable nanofluidic channels by nanoimprinting and its application for DNA stretching, Nano Lett. 4, 69-73 https://doi.org/10.1021/nl034877i
  32. Han, J. and H. G. Craighead, 2000, Separation of long DNA molecules in a microfabricated entropic trap array, Science 288, 1026-1029 https://doi.org/10.1126/science.288.5468.1026
  33. Han, J., S. W. Turner and H. G. Craighead, 1999, Entropic trapping and escape of long DNA molecules at submicron size constriction, Phys. Rev. Lett. 83, 1688-1691 https://doi.org/10.1103/PhysRevLett.83.1688
  34. Han, J. Y. and H. G. Craighead, 2002, Characterization and optimization of an entropic trap for DNA separation, Anal. Chem. 74, 394-401 https://doi.org/10.1021/ac0107002
  35. Han, J. Y., J. P. Fu and R. B. Schoch, 2008, Molecular sieving using nanofilters: Past, present and future, Lab Chip 8, 23-33 https://doi.org/10.1039/b714128a
  36. Harden, J. L. and M. Doi, 1992, Diffusion of macromolecules in narrow capillaries, J. Phys. Chem. 96, 4046-4052 https://doi.org/10.1021/j100189a025
  37. Hsieh, C. C., A. Balducci and P. S. Doyle, 2007, An experimental study of DNA rotational relaxation time in nanoslits, Macromolecules 40, 5196-5205 https://doi.org/10.1021/ma070570k
  38. Hsieh, C. C., A. Balducci and P. S. Doyle, 2008, Ionic effects on the equilibrium dynamics of dna confined in nanoslits, Nano Lett. 8, 1683-1688 https://doi.org/10.1021/nl080605+
  39. Huh, D., K. L. Mills, X. Y. Zhu, M. A. Burns, M. D. Thouless and S. Takayama, 2007, Tuneable elastomeric nanochannels for nanofluidic manipulation, Nat. Mater. 6, 424-428 https://doi.org/10.1038/nmat1907
  40. Israelachvili, J. N., 1991, Intermolecular and surface forces, Academic Press, London ; San Diego, 2nd edition
  41. Jendrejack, R. M., E. T. Dimalanta, D. C. Schwartz, M. D. Graham and J. J. de Pablo, 2003a, DNA dynamics in a microchannel, Phys. Rev. Lett. 91, 038102 https://doi.org/10.1103/PhysRevLett.91.038102
  42. Jendrejack, R. M., D. C. Schwartz, M. D. Graham and J. J. de Pablo, 2003b, Effect of confinement on DNA dynamics in microfluidic devices, J. Chem. Phys. 119, 1165-1173 https://doi.org/10.1063/1.1575200
  43. Jo, K., D. M. Dhingra, T. Odijk, J. J. de Pablo, M. D. Graham, R. Runnheim, D. Forrest and D. C. Schwartz, 2007, A singlemolecule barcoding system using nanoslits for DNA analysis, Proc. Natl. Acad. Sci. USA 104, 2673-2678
  44. Juang, Y. J., S. Wang, X. Hu and L. J. Lee, 2004, Dynamics of single polymers in a stagnation flow induced by electrokinetics, Phys. Rev. Lett. 93, 268105 https://doi.org/10.1103/PhysRevLett.93.268105
  45. 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
  46. Krishnan, M., I. Monch and P. Schwille, 2007, Spontaneous stretching of DNA in a two-dimensional nanoslit, Nano Lett. 7, 1270-1275 https://doi.org/10.1021/nl0701861
  47. Larson, J. W., G. R. Yantz, Q. Zhong, R. Charnas, C. M. D'Antoni, M. V. Gallo, K. A. Gillis, L. A. Neely, K. M. Phillips, G. G. Wong, S. R. Gullans and R. Gilmanshin, 2006, Single DNA molecule stretching in sudden mixed shear and elongational microflows, Lab Chip 6, 1187-1199 https://doi.org/10.1039/b602845d
  48. Leal, L. G., 1992, Laminar flow and convective transport processes : scaling principles and asymptotic analysis, Butterworth-Heinemann, Boston
  49. Lin, P. K., C. C. Fu, Y. L. Chen, Y. R. Chen, P. K. Wei, C. H. Kuan and W. S. Fann, 2007, Static conformation and dynamics of single DNA molecules confined in nanoslits, Phys. Rev. E 76, 011806 https://doi.org/10.1103/PhysRevE.76.011806
  50. Long, D., J. L. Viovy and A. Ajdari, 1996, Simultaneous action of electric fields and nonelectric forces on a polyelectrolyte: Motion and deformation, Phys. Rev. Lett. 76, 3858-3861 https://doi.org/10.1103/PhysRevLett.76.3858
  51. Lubensky, D. K. and D. R. Nelson, 1999, Driven polymer translocation through a narrow pore, Biophys. J. 77, 1824-1838 https://doi.org/10.1016/S0006-3495(99)77027-X
  52. Maier, B. and J. O. Rädler, 1999, Conformation and self-diffusion of single DNA molecules confined to two dimensions, Phys. Rev. Lett. 82, 1911-1914 https://doi.org/10.1103/PhysRevLett.82.1911
  53. Maier, B. and J. O. Rädler, 2000, DNA on fluid membranes: A model polymer in two dimensions, Macromolecules 33, 7185-7194 https://doi.org/10.1021/ma000075n
  54. Maier, B. and J. O. Radler, 2001, Shape of self-avoiding walks in two dimensions, Macromolecules 34, 5723-5724 https://doi.org/10.1021/ma002005m
  55. Maier, B., U. Seifert and J. O. Radler, 2002, Elastic response of DNA to external electric fields in two dimensions, Europhys. Letters 60, 622-628 https://doi.org/10.1209/epl/i2002-00263-9
  56. Mannion, J. T. and H. G. Craighead, 2007, Nanofluidic structures for single biomolecule fluorescent detection, Biopolymers 85, 131-143 https://doi.org/10.1002/bip.20629
  57. Mannion, J. T., C. H. Reccius, J. D. Cross and H. G. Craighead, 2006, Conformational analysis of single DNA molecules undergoing entropically induced motion in nanochannels, Biophys. J. 90, 4538-4545 https://doi.org/10.1529/biophysj.105.074732
  58. Milchev, A. and K. Binder, 1996, Dynamics of polymer chains confined in slit-like pores, J. Phys. (Paris) 6, 21-31
  59. Nykypanchuk, D., H. H. Strey and D. A. Hoagland, 2002, Brownian motion of DNA confined within a two dimensional array, Science 297, 987-990 https://doi.org/10.1126/science.1073277
  60. Nykypanchuk, D., H. H. Strey and D. A. Hoagland, 2005, Single molecule visualizations of polymer partitioning within model pore geometries, Macromolecules 38, 145-150 https://doi.org/10.1021/ma048062n
  61. Odijk, T., 1977, Polyelectrolyte near rod limit, J. Polym. Sci. BPolym. Phys. 15, 477-483 https://doi.org/10.1002/pol.1977.180150307
  62. Odijk, T., 1983, On the statistics and dynamics of confined or entangled stiff polymers, Macromolecules 16, 1340-1344 https://doi.org/10.1021/ma00242a015
  63. Odijk, T., 2006, DNA confined in nanochannels: Hairpin tightening by entropic depletion, J. Chem. Phys. 125, 204904 https://doi.org/10.1063/1.2400227
  64. Odijk, T. and A. C. Houwaart, 1978, Theory of excluded-volume effect of a polyelectrolyte in a 1-1 electrolyte solution, J. Polym. Sci. B-Polym. Phys. 16, 627-639 https://doi.org/10.1002/pol.1978.180160405
  65. Olson, D. J., J. M. Johnson, P. D. Patel, E. S. G. Shaqfeh, S. G. Boxer and G. G. Fuller, 2001, Electrophoresis of DNA adsorbed to a cationic supported bilayer, Langmuir 17, 7396-7401 https://doi.org/10.1021/la010475j
  66. Perkins, T. T., S. R. Quake, D. E. Smith and S. Chu, 1994, Relaxation of a single DNA molecule observed by optical microscopy, Science 264, 822-826 https://doi.org/10.1126/science.8171336
  67. Perkins, T. T., D. E. Smith, R. G. Larson and S. Chu, 1995, Stretching of a single tethered polymer in a uniform-flow, Science 268, 83-87 https://doi.org/10.1126/science.7701345
  68. Randall, G. C., 2006, Single molecule analysis of DNA electrophoresis in microdevices, Ph.D. thesis
  69. Randall, G. C. and P. S. Doyle, 2004, Electrophoretic collision of a DNA molecule with an insulating post, Phys. Rev. Lett. 93, 058104
  70. Randall, G. C. and P. S. Doyle, 2005a, DNA deformation in electric fields: DNA driven past a cylindrical obstruction, Macromolecules 38, 2410-2418 https://doi.org/10.1021/ma048073g
  71. Randall, G. C. and P. S. Doyle, 2005b, Permeation-driven flow in poly(dimethylsiloxane) microfluidic devices, Proc. Natl. Acad. Sci. USA 102, 10813-10818
  72. Randall, G. C. and P. S. Doyle, 2006, Collision of a DNA polymer with a small obstacle, Macromolecules 39, 7734-7745 https://doi.org/10.1021/ma061375t
  73. Randall, G. C., K. M. Schultz and P. S. Doyle, 2006, Methods to electrophoretically stretch DNA: microcontractions, gels, and hybrid gel-microcontraction devices, Lab Chip 6, 516-525 https://doi.org/10.1039/b515326c
  74. Reisner, W., J. P. Beech, N. B. Larsen, H. Flyvbjerg, A. Kristensen and J. O. Tegenfeldt, 2007, Nanoconfinementenhanced conformational response of single DNA molecules to changes in ionic environment, Phys. Rev. Lett. 99, 058302 https://doi.org/10.1103/PhysRevLett.99.058302
  75. Reisner, W., K. J. Morton, R. Riehn, Y. M. Wang, Z. N. Yu, M. Rosen, J. C. Sturm, S. Y. Chou, E. Frey and R. H. Austin, 2005, Statics and dynamics of single DNA molecules confined in nanochannels, Phys. Rev. Lett. 94, 196101 https://doi.org/10.1103/PhysRevLett.94.196101
  76. Riehn, R., M. C. Lu, Y. M. Wang, S. F. Lim, E. C. Cox and R. H. Austin, 2005, Restriction mapping in nanofluidic devices, Proc. Natl. Acad. Sci. USA 102, 10012-10016
  77. Rivetti, C., M. Guthold and C. Bustamante, 1996, Scanning force microscopy of DNA deposited onto mica: equilibration versus kinetic trapping studied by statistical polymer chain analysis, J. Mol. Biol. 264, 919-932 https://doi.org/10.1006/jmbi.1996.0687
  78. Rubinstein, M. and R. H. Colby, 2003, Polymer physics, Oxford University Press, Oxford ; New York
  79. Rybenkov, V. V., N. R. Cozzarelli and A. V. Vologodskii, 1993, Probability of DNA knotting and the effective diameter of the DNA double helix, Proc. Natl. Acad. Sci. USA 90, 5307-5311
  80. Sakaue, T. and E. Raphael, 2006, Polymer chains in confined spaces and flow-injection problems: Some remarks, Macromolecules 39, 2621-2628 https://doi.org/10.1021/ma0514424
  81. Salieb-Beugelaar, G. B., J. Teapal, J. Van Nieuwkasteele, D. Wijnperle, J. O. Tegenfeldt, F. Lisdat, A. van den Berg and J. C. T. Eijkel, 2008, Field-dependent DNA mobility in 20 nm high nanoslits, Nano Lett. 8, 1785-1790 https://doi.org/10.1021/nl080300v
  82. Savin, T. and P. S. Doyle, 2005, Static and dynamic errors in particle tracking microrheology, Biophys. J. 88, 623-638 https://doi.org/10.1529/biophysj.104.042457
  83. Shaqfeh, E. S. G., 2005, The dynamics of single-molecule DNA in flow, J. Non-Newtonian Fluid Mech. 130, 1-28 https://doi.org/10.1016/j.jnnfm.2005.05.011
  84. Shaw, S. Y. and J. C. Wang, 1993, Knotting of a DNA chain during ring-closure, Science 260, 533-536 https://doi.org/10.1126/science.8475384
  85. Skolnick, J. and M. Fixman, 1977, Electrostatic persistence length of a wormlike polyelectrolyte, Macromolecules 10, 944-948 https://doi.org/10.1021/ma60059a011
  86. Stein, D., F. H. J. van der Heyden, W. J. A. Koopmans and C. Dekker, 2006, Pressure-driven transport of confined DNA polymers in fluidic channels, Proc. Natl. Acad. Sci. USA 103, 15853-15858
  87. Stigter, D., 1977, Interactions of highly charged colloidal cylinders with applications to double-stranded DNA, Biopolymers 16, 1435-1448 https://doi.org/10.1002/bip.1977.360160705
  88. Tang, J. and P. S. Doyle, 2007, Electrophoretic stretching of DNA molecules using microscale t junctions, App. Phys. Lett. 90, 224103 https://doi.org/10.1063/1.2745650
  89. Teclemariam, N. P., V. A. Beck, E. S. G. Shaqfeh and S. J. Muller, 2007, Dynamics of DNA polymers in post arrays: Comparison of single molecule experiments and simulations, Macromolecules 40, 3848-3859 https://doi.org/10.1021/ma062892e
  90. Tegenfeldt, J. O., C. Prinz, H. Cao, S. Chou, W. W. Reisner, R. Riehn, Y. M. Wang, E. C. Cox, J. C. Sturm, P. Silberzan and R. H. Austin, 2004a, The dynamics of genomic-length DNA molecules in 100-nm channels, Proc. Natl. Acad. Sci. USA 101, 10979-10983
  91. Tegenfeldt, J. O., C. Prinz, H. Cao, R. L. Huang, R. H. Austin, S. Y. Chou, E. C. Cox and J. C. Sturm, 2004b, Micro- and nanofluidics for DNA analysis, Analytical and Bioanalytical Chemistry 378, 1678-1692 https://doi.org/10.1007/s00216-004-2526-0
  92. Teraoka, I., 1996, Polymer solutions in confining geometries, Prog. Polym. Sci. 21, 89-149 https://doi.org/10.1016/0079-6700(95)00018-6
  93. Turner, S. W. P., M. Cabodi and H. G. Craighead, 2002, Confinement-induced entropic recoil of single DNA molecules in a nanofluidic structure, Phys. Rev. Lett. 88, 128103 https://doi.org/10.1103/PhysRevLett.88.128103
  94. Ubbink, J. and T. Odijk, 1999, Electrostatic-undulatory theory of plectonemically superooiled DNA, Biophys. J. 76, 2502-2519 https://doi.org/10.1016/S0006-3495(99)77405-9
  95. Usta, O. B., A. J. C. Ladd and J. E. Butler, 2005, Lattice-boltzmann simulations of the dynamics of polymer solutions in periodic and confined geometries, J. Chem. Phys. 122, 094902 https://doi.org/10.1063/1.1854151
  96. Volkmuth, W. D. and R. H. Austin, 1992, DNA electrophoresis in microlithographic arrays, Nature 358, 600-602 https://doi.org/10.1038/358600a0
  97. Volkmuth, W. D., T. Duke, M. C. Wu, R. H. Austin and A. Szabo, 1994, DNA electrodiffusion in a 2d array of posts, Phys. Rev. Lett. 72, 2117-2120 https://doi.org/10.1103/PhysRevLett.72.2117
  98. Vologodskii, A. and N. Cozzarelli, 1995, Modeling of long-range electrostatic interactions in DNA, Biopolymers 35, 289-296 https://doi.org/10.1002/bip.360350304
  99. Wall, F. T., W. A. Seitz, J. C. Chin and P. G. de Gennes, 1978, Statistics of self-avoiding walks confined to strips and capillaries, Proc. Natl. Acad. Sci. USA 75, 2069-2070
  100. Wang, Y. M., J. O. Tegenfeldt, W. Reisner, R. Riehn, X. J. Guan, L. Guo, I. Golding, E. C. Cox, J. Sturm and R. H. Austin, 2005, Single-molecule studies of repressor-DNA interactions show long-range interactions, Proc. Natl. Acad. Sci. USA 102, 9796-9801
  101. Yamakawa, H., 1967, Modern Theory of Polymer Solutions, Harper and Row, New York
  102. Yang, Y. Z., T. W. Burkhardt and G. Gompper, 2007, Free energy and extension of a semiflexible polymer in cylindrical confining geometries, Phys. Rev. E 76, 011804 https://doi.org/10.1103/PhysRevE.76.011804
  103. Zhang, C., F. Zhang, J. A. van Kan and J. R. C. van der Maarel, 2008, Effects of electrostatic screening on the conformation of single dna molecules confined in a nanochannel, Journal of Chemical Physics 128, 225109 https://doi.org/10.1063/1.2937441