To what extent of ion neutralization can multivalent ion distributions around RNA-like macroions be described by Poisson-Boltzmann theory?

doi:10.1088/1674-1056/27/1/018203

Abstract Nucleic acids are negatively charged biomolecules, and metal ions in solutions are important to their folding structures and thermodynamics, especially multivalent ions. However, it has been suggested that the binding of multivalent ions to nucleic acids cannot be quantitatively described by the well-established Poisson-Boltzmann (PB) theory. In this work, we made extensive calculations of ion distributions around various RNA-like macroions in divalent and trivalent salt solutions by PB theory and Monte Carlo (MC) simulations. Our calculations show that PB theory appears to underestimate multivalent ion distributions around RNA-like macroions while can reliably predict monovalent ion distributions. Our extensive comparisons between PB theory and MC simulations indicate that when an RNA-like macroion gets ion neutralization beyond a “critical” value, the multivalent ion distribution around that macroion can be approximately described by PB theory. Furthermore, an empirical formula was obtained to approximately quantify the critical ion neutralization for various RNA-like macroions in multivalent salt solutions, and this empirical formula was shown to work well for various real nucleic acids including RNAs and DNAs.

Keywords: nucleic acids ion binding Poisson-Boltzmann theory Monte Carlo simulation

Received: 31 August 2017
Revised: 23 October 2017
Accepted manuscript online:

PACS:	82.35.Rs	(Polyelectrolytes)
	87.14.gn	(RNA)
	87.10.Rt	(Monte Carlo simulations)
	87.14.G-	(Nucleic acids)

Fund: Project supported by the National Natural Science Foundation of China (Grant Nos. 11374234, 11575128, 11774272, and 11647312).

Corresponding Authors: Xi Zhang, Zhi-Jie Tan
E-mail: xizhang@whu.edu.cn;zjtan@whu.edu.cn

Cite this article:

Gui Xiong(熊贵), Kun Xi(席昆), Xi Zhang(张曦), Zhi-Jie Tan(谭志杰) To what extent of ion neutralization can multivalent ion distributions around RNA-like macroions be described by Poisson-Boltzmann theory? 2018 Chin. Phys. B 27 018203

[1]	Woodson S A 2005 Curr. Opin. Chem. Biol. 9 104
[2]	Draper D E, Grilley D and Soto A M 2005 Annu. Rev. Biophys. Biomol. Struct. 34 221
[3]	Chen S J 2008 Annu. Rev. Biophys. 37 197
[4]	Wong G C and Pollack L 2010 Annu. Rev. Phys. Chem. 61 171
[5]	Lipfert J, Doniach S, Das R and Herschlag D 2014 Annu. Rev. Biochem. 83 813
[6]	Bao L, Zhang X, Jin L and Tan Z J 2016 Chin. Phys. B 25 018703
[7]	Chen H, Meisburger S P, Pabit S A, Sutton J L, Webb W W and Pollack L 2012 Proc. Natl. Acad. Sci. USA 109 799
[8]	Tan Z J and Chen S J 2006 Biophys. J. 90 1175
[9]	Tan Z J and Chen S J 2011 Met Ions Life Sci. 9 101
[10]	Shi Y Z, Wang F H, Wu Y Y and Tan Z J 2014 J. Chem. Phys. 141 105102
[11]	Wang J, Zhao Y J, Wang J and Xiao Y 2015 Phys. Rev. E 92 062705
[12]	Shi Y Z, Jin L, Wang F H, Zhu X L and Tan Z J 2015 Biophys. J. 109 2654
[13]	Heilman Miller S L, Pan J, Thirumalai D and Woodson S A 2001 J. Mol. Biol. 309 57
[14]	Sun L Z, Zhang D and Chen S J 2017 Annu. Rev. Biophys. 46 227
[15]	Wang J and Xiao Y 2016 Phys. Rev. E 94 040401
[16]	Drozdetski A V, Tolokh I S, Pollack L, Baker N and Onufriev A V 2016 Phys. Rev. Lett. 117 028101
[17]	Tan Z J and Chen S J 2011 Biophys. J. 101 176
[18]	Tan Z J and Chen S J 2006 Nucleic Acids Res. 34 6629
[19]	Tan Z J and Chen S J 2008 Biophys. J. 94 3137
[20]	He Z J and Chen S J 2012 J. Chem. Theory Comput. 8 2095
[21]	Jacobson D R and Saleh O A 2017 Nucleic Acids Res. 45 1596
[22]	Fenley M O, Olson W K, Tobias I and Manning G S 1994 Biophys. Chem. 50 255
[23]	Wu Y Y, Zhang Z L, Zhang J S, Zhu X L and Tan Z J 2015 Nucleic Acids Res. 43 6156
[24]	Zhang Z L, Wu Y Y, Xi K, Sang J P and Tan Z J 2017 Biophys. J. 113 517
[25]	Widom J and Baldwin R L 1980 J. Mol. Biol. 144 431
[26]	Bloomfield V A 1997 Biopolymers 44 269
[27]	Qiu X Y, Andresen K, Kwok L W, Lamb J S, Park H Y and Pollack L 2007 Phys. Rev. Lett. 99 038104
[28]	Li W, Wong W J, Lim C J, Ju H P, Li M, Yan J and Wang P Y 2015 Chin. Phys. B 24 128704
[29]	Wang F H, Wu Y Y and Tan Z J 2013 Biopolymers 99 370
[30]	Tan Z J and Chen S J 2010 Biophys. J. 99 1565
[31]	Andresen K, Das R, Park H Y, Smith H, Kwok L W, Lamb J S, Kirkland E J, Herschlag D, Finkelstein K D and Pollack L 2004 Phys. Rev. Lett. 93 248103
[32]	Zhuang X, Bartley L E, Babcock H P, Russell R, Ha T, Herschlag D and Chu S 2000 Science 288 2048
[33]	Russell R, Zhuang X, Babcock H P, Millett I S, Doniach S, Chu S and Herschlag D 2002 Proc. Nalt. Acad. Sci. USA 99 155
[34]	Manning G S 1978 Q. Rev. Biophys. 11 179
[35]	Manning G S 2007 J. Phys. Chem. B 111 8554
[36]	Schurr J M and Fujimoto B S 2002 Biophys. Chem. 101 425
[37]	Gilson M K, Sharp K A and Honig B H 1988 J. Comput. Chem. 9 327
[38]	Sharp K A and Honig B 1990 J. Phys. Chem. 94 7684
[39]	Liu H Y and Zou X Q 2006 J. Phys. Chem. B 110 9304
[40]	Chen D, Chen Z, Chen C, Geng W and Wei G W 2011 J. Comput. Chem. 32 756
[41]	Grant J A, Pickup B T and Nicholls A 2001 J. Comput. Chem. 22 608
[42]	Ran S Y and Jia J L 2015 Chin. Phys. B 24 128702
[43]	Chu V B, Bai Y, Lipfert J, Herschlag D and Doniach S 2007 Biophys. J. 93 3202
[44]	López García J J, Horno J and Grosse C 2011 Langmuir 27 13970
[45]	Das T, Bratko D, Bhuiyan L B and Outhwaite C W 1997 J. Chem. Phys. 107 9197
[46]	Lu B Z, Chen W Z, Wang C X and Xu X J 2002 Proteins 48 497
[47]	Lu B Z, Zhou Y C, Holst M J and McCammon J A 2008 Commun. Comput. Phys. 3 973
[48]	Borukhov I, Andelman D and Orland H 1997 Phys. Rev. Lett. 79 435
[49]	Tan Z J and Chen S J 2005 J. Chem. Phys. 122 044903
[50]	Bacquet R and Rossky P J 1984 J. Chem. Phys. 88 2660
[51]	Draper D E 1995 Annu. Rev. Biochem. 64 593
[52]	Wette P, Schöpe H J and Palberg T 2002 J. Chem. Phys. 116 10981
[53]	Boschitsch A H, Fenley M O and Zhou H X 2002 J. Phys. Chem. B 106 2741
[54]	Baker N A 2004 Method. Enzymol. 383 94
[55]	Wagoner J and Baker N A 2004 J. Comput. Chem. 25 1623
[56]	Wei G W, Zheng Q, Chen Z and Xia K L 2012 SIAM Rev. 54 699
[57]	Lyklema J 2015 J. Colloid Interf. Sci. 446 308
[58]	Lozada Cassou M 1983 J. Phys. Chem. 87 3729
[59]	Vlachy V 1999 Annu. Rev. Phys. Chem. 50 145
[60]	Bai Y, Greenfeld M, Travers K J, Chu V B, Lipfert J, Doniach S and Herschlag D 2007 J. Am. Chem. Soc. 129 14981
[61]	Qiu X Y, Parsegian V A and Rau D C 2010 Proc. Natl. Acad. Sci. USA 107 21482
[62]	Trachman R J and Draper D E 2017 Nucleic Acids Res. 45 4733
[63]	Giambaşu G M, Luchko T, Herschlag D, York D M and Case D A 2014 Biophys. J. 106 883
[64]	Misra V K and Draper D E 2002 J. Mol. Biol. 317 507
[65]	Sushko M L, Thomas D G, Pabit S A, Pollack L, Onufriev A V and Baker N A 2016 Biophys. J. 110 315
[66]	Baker N A, Sept D, Joseph S, Holst M J and McCammon J A 2001 Proc. Natl. Acad. Sci. USA 98 10037
[67]	Bao L, Zhang X, Shi Y Z, Wu Y Y and Tan Z J 2017 Biophys. J. 112 1094
[68]	Ermak D L and McCammon J A 1978 J. Chem. Phys. 69 1352
[69]	Deserno M, Holm C and May S 2000 Macromolecules 33 199
[70]	Carnal F and Stoll S 2012 J. Phys. Chem. A 116 6600
[71]	Zhang X, Zhang J S, Shi Y Z, Zhu X L and Tan Z J 2016 Sci. Rep. 6 23434
[72]	Qi W P, Lei X L and Fang H P 2010 Chem. Phys. Chem. 11 2146
[73]	Qi W P, Song B, Lei X L, Wang C L and Fang H P 2011 Biochemistry 50 9628
[74]	Zhang Y J, Zhang J and Wang W 2011 J. Am. Chem. Soc. 133 6882
[75]	Su X H, Lei Q L and Ren C L 2015 Chin. Phys. B 24 113601
[76]	Wei J Y, Ran S Y, He L L, Wang X H and Zhang L X 2015 Chin. Phys. B 24 118701
[77]	Marcus Y 1985 Ion Solvation (New York: Wiley)
[78]	Wu Y Y, Wang F H and Tan Z J 2013 Phys. Lett. A 377 1911
[79]	Zhang X, Bao L, Wu Y Y, Zhu X L and Tan Z J 2017 J. Chem. Phys. 147 054901
[80]	Gutin A M and Shakhnovich E I 1994 Phys. Rev. E 50 R3322
[81]	Salerno K M, Frischknecht A L and Stevens M J 2016 J. Phys. Chem. B 120 5927
[82]	dos Santos A P, Diehl A and Levin Y 2010 J. Chem. Phys. 132 104105
[83]	Murthy C S, Bacquet R J and Rossky P J 1985 J. Phys. Chem. 89 701
[84]	Jayaram B, Swaminathan S, Beveridge D L, Sharp K and Honig B 1990 Macromolecules 23 3156
[85]	Hyeon C, Dima R I and Thirumalai D 2006 J. Chem. Phys. 125 194905
[86]	Sun L Z and Chen S J 2016 J. Chem. Theory Comput. 12 3370
[87]	Zhu Y H and Chen S J 2014 J. Chem. Phys. 141 055101
[88]	Henke P S and Mak C H 2016 J. Chem. Phys. 144 105104

[1]	Abnormal magnetic behavior of prussian blue analogs modified with multi-walled carbon nanotubes Jia-Jun Mo(莫家俊), Pu-Yue Xia(夏溥越), Ji-Yu Shen(沈纪宇), Hai-Wen Chen(陈海文), Ze-Yi Lu(陆泽一), Shi-Yu Xu(徐诗语), Qing-Hang Zhang(张庆航), Yan-Fang Xia(夏艳芳), Min Liu(刘敏). Chin. Phys. B, 2023, 32(4): 047503.
[2]	Computational studies on magnetism and ferroelectricity Ke Xu(徐可), Junsheng Feng(冯俊生), and Hongjun Xiang(向红军). Chin. Phys. B, 2022, 31(9): 097505.
[3]	Steady-state and transient electronic transport properties of β-(Al_xGa_1-x)₂O₃/Ga₂O₃ heterostructures: An ensemble Monte Carlo simulation Yan Liu(刘妍), Ping Wang(王平), Ting Yang(杨婷), Qian Wu(吴茜), Yintang Yang(杨银堂), and Zhiyong Zhang(张志勇). Chin. Phys. B, 2022, 31(11): 117305.
[4]	Monte Carlo simulations of electromagnetically induced transparency in a square lattice of Rydberg atoms Shang-Yu Zhai(翟尚宇) and Jin-Hui Wu(吴金辉). Chin. Phys. B, 2021, 30(7): 074206.
[5]	Zero-field skyrmions in FeGe thin films stabilized through attaching a perpendicularly magnetized single-domain Ni layer Zi-Bo Zhang(张子博) and Yong Hu(胡勇). Chin. Phys. B, 2021, 30(7): 077503.
[6]	Emergent O(4) symmetry at the phase transition from plaquette-singlet to antiferromagnetic order in quasi-two-dimensional quantum magnets Guangyu Sun(孙光宇), Nvsen Ma(马女森), Bowen Zhao(赵博文), Anders W. Sandvik, and Zi Yang Meng(孟子杨). Chin. Phys. B, 2021, 30(6): 067505.
[7]	Correlated insulating phases in the twisted bilayer graphene Yuan-Da Liao(廖元达), Xiao-Yan Xu(许霄琰), Zi-Yang Meng(孟子杨), and Jian Kang(康健). Chin. Phys. B, 2021, 30(1): 017305.
[8]	Tunable deconfined quantum criticality and interplay of different valence-bond solid phases Bowen Zhao(赵博文), Jun Takahashi, Anders W. Sandvik. Chin. Phys. B, 2020, 29(5): 057506.
[9]	Magnetic properties of La₂CuMnO₆ double perovskite ceramic investigated by Monte Carlo simulations S Mtougui, I EL Housni, N EL Mekkaoui, S Ziti, S Idrissi, H Labrim, R Khalladi, L Bahmad. Chin. Phys. B, 2020, 29(5): 056101.
[10]	Two types of highly efficient electrostatic traps for single loading or multi-loading of polar molecules Bin Wei(魏斌), Hengjiao Guo(郭恒娇), Yabing Ji(纪亚兵), Shunyong Hou(侯顺永), Jianping Yin(印建平). Chin. Phys. B, 2020, 29(4): 043701.
[11]	Phase transition of DNA compaction in confined space: Effects of macromolecular crowding are dominant Erkun Chen(陈尔坤), Yangtao Fan(范洋涛), Guangju Zhao(赵光菊), Zongliang Mao(毛宗良), Haiping Zhou(周海平), Yanhui Liu(刘艳辉). Chin. Phys. B, 2020, 29(1): 018701.
[12]	Variational and diffusion Monte Carlo simulations of a hydrogen molecular ion in a spherical box Xuehui Xiao(肖学会), Kuo Bao(包括), Youchun Wang(王友春), Hui Xie(谢慧), Defang Duan(段德芳), Fubo Tian(田夫波), Tian Cui(崔田). Chin. Phys. B, 2019, 28(5): 056401.
[13]	Computational study of inverse ferrite spinels A EL Maazouzi, R Masrour, A Jabar, M Hamedoun. Chin. Phys. B, 2019, 28(5): 057504.
[14]	Phase diagrams and magnetic properties of the mixed spin-1 and spin-3/2 Ising ferromagnetic thin film:Monte Carlo treatment B Boughazi, M Boughrara, M Kerouad. Chin. Phys. B, 2019, 28(2): 027501.
[15]	Effect of particle size distribution on magnetic behavior of nanoparticles with uniaxial anisotropy S Rizwan Ali, Farah Naz, Humaira Akber, M Naeem, S Imran Ali, S Abdul Basit, M Sarim, Sadaf Qaseem. Chin. Phys. B, 2018, 27(9): 097503.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Metrics
Related Articles

To what extent of ion neutralization can multivalent ion distributions around RNA-like macroions be described by Poisson-Boltzmann theory?

Cite this article:

Online attention