On the electrostatics of DNA in chromatin

Klemen Bohinc; Leo Lue; Klemen Bohinc; Leo Lue

doi:10.3934/biophy.2016.1.75

AIMS Biophysics

2016, Volume 3, Issue 1: 75-87. doi: 10.3934/biophy.2016.1.75

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On the electrostatics of DNA in chromatin

Klemen Bohinc ^{1
,
,},
Leo Lue ²

1.
Faculty of Health Sciences, University of Ljubljana, Zdravstvena 5, SI-1000 Ljubljana, Slovenia
2.
Department of Chemical and Process Engineering, University of Strathclyde, James Weir Building, 75 Montrose Street, Glasgow G1 1XJ, UK

Received: 13 November 2015 Accepted: 24 January 2016 Published: 03 February 2016

We examine the interaction between DNA molecules immersed in an aqueous solution of oppositely charged, trivalent spermidine molecules. The DNA molecules are modeled as planar, likecharged surfaces immersed in an aqueous solution of multivalent, rod-like ions consisting of rigidly bonded point charges. An approximate field theory is used to determine the properties of this system from the weak to the intermediate through to the strong coupling regimes. In the weak coupling limit, the interaction between the charged surfaces is only repulsive, whereas in the intermediate coupling regime, the rod-like ions with spatial charge distribution can induce attractive force between the charged surfaces. In the strong coupling limit, the inter-ionic charge correlations induce attractive interaction at short separations between the surfaces. This theoretical study can give new insights in the problem of interaction between DNA molecules mediated by trivalent spermidine molecules.
- electrostatics,
- field theory,
- DNA,
- multivalent ions,
- chromatin
Citation: Klemen Bohinc, Leo Lue. On the electrostatics of DNA in chromatin[J]. AIMS Biophysics, 2016, 3(1): 75-87. doi: 10.3934/biophy.2016.1.75

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Abstract

We examine the interaction between DNA molecules immersed in an aqueous solution of oppositely charged, trivalent spermidine molecules. The DNA molecules are modeled as planar, likecharged surfaces immersed in an aqueous solution of multivalent, rod-like ions consisting of rigidly bonded point charges. An approximate field theory is used to determine the properties of this system from the weak to the intermediate through to the strong coupling regimes. In the weak coupling limit, the interaction between the charged surfaces is only repulsive, whereas in the intermediate coupling regime, the rod-like ions with spatial charge distribution can induce attractive force between the charged surfaces. In the strong coupling limit, the inter-ionic charge correlations induce attractive interaction at short separations between the surfaces. This theoretical study can give new insights in the problem of interaction between DNA molecules mediated by trivalent spermidine molecules.

References

[1]	Korolev N, Vorontsova OV, Nordenskiold L (2007) Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Prog Biophys Mol Biol 95: 23–49. doi: 10.1016/j.pbiomolbio.2006.11.003
[2]	Bloomfield VA (1997) DNA condensation by multivalent cations. Biopolymers 44: 269.
[3]	Teif VB, Bohinc K (2011) Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Prog Biophys Mol Biol 105: 208–282. doi: 10.1016/j.pbiomolbio.2010.07.002
[4]	Radler JO, Koltover I, Salditt T, et al. (1997) Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275: 810–814. doi: 10.1126/science.275.5301.810
[5]	Chow MH, Yan KTH, Bennett MJ, et al. (2010) Birefringence and DNA condensation of liquid crystalline chromosomes. Eukaryotic Cell 9:1577-1587. doi: 10.1128/EC.00026-10
[6]	Gelbart WM, Bruinsma RF, Pincus PA, et al. (2000) DNA-inspired electrostatics Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Physics Today 53:38–44.
[7]	Mengistu DH, Bohinc K, May S, (2009) Binding of DNA to zwitterionic lipid layers mediated by divalent cations. J Phys Chem B 113: 12277–12282. doi: 10.1021/jp904986j
[8]	Raedler JO, Koltover I, Salditt T, et al. (1997) Structure of DNA-cationic liposome complexes: DNA intercalation in multilamellar membranes in distinct interhelical packing regimes. Science 275: 810–814. doi: 10.1126/science.275.5301.810
[9]	Evans DF, Wennerström H (1994) The colloidal domain, where physics, chemistry, biology and technology meet. , 2 Eds., New York: VCH Publishers.
[10]	Butler JC, Angelini T, Tang JX, et al. (2003) Ion multivalence and like-charge polyelectrolyte attraction. Phys Rev Lett 91: 028301. doi: 10.1103/PhysRevLett.91.028301
[11]	Angelini TE, Liang H, Wriggers W, et al. (2003) Like-charge attraction between polyelectrolytes induced by counterion charge density waves. Proc Nat Acad Sci U S A 100: 8634–8637.
[12]	Bohinc K, Brezesinski G, May S (2012) Modeling the influence of adsorbed DNA on the lateral pressure and tilt transition of a zwitterionic lipid monolayer. Phys Chem Chem Phys 40: 10613–10621.
[13]	Gouy MG (1910) Sur la constitution dela charge electrique ala surface d‘un electrolyte. J Phys Radium (Paris) 9: 457–468.
[14]	Chapman DL (1913) A Contribution to the Theory of Electrocapillarity. Philos Mag 6: 455–481.
[15]	Moreira AG, Netz RR (2001) Binding of similarly charged plates with counterions only Modeling the influence of adsorbed DNA on the lateral pressure and tilt transition of a zwitterionic lipid monolayer. Phys Rev Lett 87: 078301. doi: 10.1103/PhysRevLett.87.078301
[16]	Shklovskii BI (1999) Screening of a macroion by multivalent ions: Correlation-induced inversion of charge. Phys Rev E 60: 5802–5811.
[17]	Carnie S, McLaughlin S (1983) Large divalent-cations and electrostatic potentials adjacent to membranes - a theoretical calculation. Biophys J 44: 325–332. doi: 10.1016/S0006-3495(83)84306-9
[18]	Kirkwood JG, Shumaker JB (1953) Forces Between Protein Molecules in Solution Arising from Fluctuations in Proton Charge and Configuration. Proc Nat Acad Sci U S A 38: 863–871.
[19]	Guldbrand L, Jönsson B, Wennerström H, et al. (1984) Electrical double layer forces. A Monte Carlo study. J Chem Phys 80: 2221–2228.
[20]	Reščič J, Linse P (2000) Charged colloidal solutions with short flexible counterions. J Phys Chem B 32: 7852–7857.
[21]	Svensson B, Jönsson B (1984) The interaction between charged aggregates in electrolyte solution - a Monte-Carlo simulation study. Chem Phys Lett 108: 580–584.
[22]	Coalson RD, Duncan A (1992) Systematic ionic screening theory of macroions. J Chem Phys 97: 5653–5661. doi: 10.1063/1.463950
[23]	Coalson RD, Walsh AM, Duncan A, et al. (1995) Statistical-mechanics of a Coulomb gas with finite-size particles - a lattice field theory. J Chem Phys 102: 4584–4594.
[24]	Tsonchev S, Coalson RD, Duncan A (1999) Statistical mechanics of charged polymers in electrolyte solutions: A lattice field theory approach. Phys Rev E 60: 4257–4267.
[25]	Tsonchev S, Coalson RD, Duncan A (2007) Partitioning of a polymer chain between a confining cavity and a gel. Phys Rev E 76: 041804. doi: 10.1103/PhysRevE.76.041804
[26]	Navarre WW, Porwollik S, Wang Y, et al. (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313: 236–238. doi: 10.1126/science.1128794
[27]	Bohinc K, Igliˇ c A, May S (2004) Interaction between macroions mediated by divalent rod-like ions. Europhys Lett 68: 494–500.
[28]	May S, Igliˇ c S, Reščič S, et al. (2008) Bridging like-charged macroions through long divalent rodlike ions. J Phys Chem B 112: 1685–1692. doi: 10.1021/jp073355e
[29]	Maset S, Bohinc K (2007) Orientations of dipoles restricted by two oppositely charged walls. J Phys A 40: 11815–11826.
[30]	Maset S, Reščič J, May S, et al. (2009) Attraction between like-charged surfaces induced by orientational ordering of divalent rigid rod-like counterions: theory and simulations. J Phys A 42: 105401. doi: 10.1088/1751-8113/42/10/105401
[31]	May S, Bohinc K (2014) Mean-field electrostatics of stiff rod-like ions, Eedited by: Dean D, Dobnikar J, Naji A and Podgornik R, lectrostatics of Soft and Disordered Matter, 1.st Eds., Pan Stanford Publishing, 335–346.
[32]	Kim YW, Yi J, Pincus PA (2008) Attractions between Like-Charged Surfaces with DumbbellShaped Counterions. Phys Rev Lett 101: 208305. doi: 10.1103/PhysRevLett.101.208305
[33]	Grime MA, Khan MO, Bohinc K (2010) Interaction between Charged Surfaces Mediated by Rodlike Counterions: The Influence of Discrete Charge Distribution in the Solution and on the Surfaces. Langmuir 26: 6343–6349. doi: 10.1021/la903940j
[34]	Hatlo MM, Bohinc K, Lue L (2010) The properties of dimers confined between two charged plates. J Chem Phys 132: 114102. doi: 10.1063/1.3354121
[35]	Bohinc K, Reščič J, Maset S, et al. (2011) DebyeHckel theory for mixtures of rigid rodlike ions and salt. J Chem Phys 134: 074111-1-9. doi: 10.1063/1.3552226
[36]	Bohinc K, Grime JMA, Lue L (2012) The interactions between charged colloids with rod-like counterions. Soft matter 8: 5679–5686. doi: 10.1039/c2sm07463j
[37]	Urbanija J, Bohinc K, Bellen A, et al. (2008) Attraction between negatively charged surfaces mediated by spherical counterions with quadrupolar charge distribution. J Chem Phys 129: 105101/1-5.
[38]	Ibarra-Armenta JG, Mart´ ın-Molina A, Bohinc K, et al. (2012) Effects of the internal structure of spheroidal divalent ions on the charge density profiles of the electric double layer. J Chem Phys 137: 224701. doi: 10.1063/1.4768448
[39]	May S, Bohinc K (2011) Attraction between like charged surfaces mediated by uniformly charged spherical colloids in a salt solution. Croat Chem Acta 84: 251–257. doi: 10.5562/cca1824
[40]	Bohinc K, Reščič J, Dufreche JF, et al. (2013) Recycling of uranyl from contaminated water. J Phys Chem B 117: 10846–10851 251–257. doi: 10.1021/jp404822f
[41]	Gosule LC, Shellman JA (1976) Compact form of DNA induced by spermidine. Nature 259: 333–335. doi: 10.1038/259333a0
[42]	Lerman LS (1971) A transition to a compact form of DNA in polymer solutions. PNAS USA 78: 1886–1890.
[43]	Jary D, Sikorav JL (1999) Cyclization of globular DNA. Implications for DNA-DNA interactions in vivo. Biochemistry 38: 3223–3227.
[44]	Vijayanathan V, Thomas T, Shirahata A, et al. (2001) DNA condensation by polyamines: a laser light scattering study of structural effects.Cyclization of globular DNA. Implications for DNADNA interactions in vivo. Biochemistry 40: 13644–13651.
[45]	Slita AV, Kasyanenko NA, Nazarova OV, et al. (2007) DNA-polycation complexes: Effect of polycation structure on physico-chemical and biological properties. J Biotechnol 127: 679–693. doi: 10.1016/j.jbiotec.2006.07.016
[46]	Slonitskii SV, Kuptsov V (1989) Binding of polyamines by the double-helical DNA molecule in unfolded and compact forms. Mol Biol (Mosk) 23: 507–517.
[47]	Parsegian VA, Rand RP, Rau DC (2000) Osmotic stress, crowding, preferential hydration, and binding: A comparison of perspectives. Proc Natl Acad Sci U S A 97: 3987–3992. doi: 10.1073/pnas.97.8.3987
[48]	Strey HH, Podgornik R, Rau DC, et al. (1998) DNA-DNA interactions. Curr Opin Struct Biol 8: 309–313. doi: 10.1016/S0959-440X(98)80063-8
[49]	Marty R, N’soukpoe-Kossi CN, Charbonneau D, et al. (2009) Structural analysis of DNA complexation with cationic lipids. Nucl Acids Res 37: 849–857. doi: 10.1093/nar/gkn1003
[50]	Hud NV, Vilfan ID (2005) Toroidal DNA condensates: unraveling the fine structure and the role of nucleation in determining size. Annu Rev Biophys Biomol Struct 34: 295–318.
[51]	Hansma HG, Kasuya K, Oroudjev E (2004) Atomic force microscopy imaging and pulling of nucleic acids. Curr Opin Struct Biol 14: 380.
[52]	Keyser UF, van Dorp S, Lemay SG (2010) Tether forces in DNA electrophoresis. Chem Soc Rev 39: 939–47. doi: 10.1039/B902072C
[53]	Baumann CG, Bloomfield VA, Smith SB, et al. (2000) Stretching of single collapsed DNA molecules. Biophys J 78: 1965–1978. doi: 10.1016/S0006-3495(00)76744-0
[54]	Besteman K, Van Eijk K, Lemay SG (2007) Charge inversion accompanies DNA condensation by multivalent ions. Nat Phys 3: 641–644. doi: 10.1038/nphys697
[55]	Chien FT, Lin SG, Lai PY,et al. (2007) Observation of two forms of conformations in the reentrant condensation of DNA. Phys Rev E Stat Nonlin Soft Matter Phys 75: 041922. doi: 10.1103/PhysRevE.75.041922
[56]	Todd BA, Parsegian VA, Shirahata A, et al. (2008) Attractive forces between cation condensed DNA double helices. Biophys J 94: 4775–4782. doi: 10.1529/biophysj.107.127332
[57]	Bohinc K, Reščič J, Dufreche JF, et al. (2013) Recycling of Uranyl from Contaminated Water. J Phys Chem B 117: 10846–10851. doi: 10.1021/jp404822f
[58]	Bohinc K, Lue L (2011) Interaction of similarly charged surfaces mediated by nanoparticles. Chin J Polymer Sci 29: 414–420.
[59]	Grosberg AY, Nguyen TT, Shklovskii BI (2002) Colloquium: The physics of charge inversion in chemical and biological systems. Rev Mod Phys 74:329–345. doi: 10.1103/RevModPhys.74.329
[60]	Cherstvy AG, Teif V (2013) Structure-driven homology pairing of chromatin fibers: The role of electrostatics and protein bridging. J Biol Phys 39: 363–385. doi: 10.1007/s10867-012-9294-4
[61]	Cherstvy AG, Teif V (2014) Electrostatic effect of H1-histone protein binding on nucleosome repeat length. Phys Biol 11: 044001. doi: 10.1088/1478-3975/11/4/044001

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