Conformation of disordered peptides modulated by distributions of charged residues: Case study of random peptides composed of arginines and aspartic acids

Kang Wen-Bin; Wang Jun; Wang Wei

doi:10.7498/aps.67.20172246

Abstract

The relationship between the sequential and structural features of intrinsically disordered peptides (IDPs) has attracted much attention during the recent decade. One essential problem relating to sequence-structure relationship is how the distribution of charged residues affects the structure of IDP. In this work, we address this problem with simulations on a series of random peptides composed of arginine and aspartic acids. With the ABSINTH implicit solvation model, the structural ensembles are generated with Markov Chain Monte Carlo method and replica-exchange sampling. The relations between various structural features (including the gyration radius, the tail distance, the distance between residues, and asphericity) and the distribution of charged residues are analyzed. Several limit cases (with parts of interactions switched off) are also calculated for comparison. The conversion from extended conformations to compact structures is observed, following the demixing of negatively and positively charged residues along the sequence. For the cases with well-mixed charges, the intra-chain electrostatic repulsions and attractions are balanced, which results in a generic Flory random coil-like conformation. Differently, for the case with well-separated charged residues, the electrostatic attraction between residues distant along the sequence induces a semi-compact hairpin-like conformation. This is consistent with the observations of Pappu group. Our results suggest that the structural dependence on charge distribution would not be sensitive to the selection of amino acid, and is determined by the patterns of charges, which demonstrates the robustness of the mechanism that the charge distribution modulates the structural features in the IDP system. Our results may broaden our understanding of the sequence-structure relation of IDP system.

Keywords:

Authors and contacts

1.
School of Physics, Nanjing University, Nanjing 210093, China;
2.
Department of Mathematics and Physics, Hubei University of Medicine, Shiyan 442000, China;
3.
Bio-X Research Center, Hubei University of Medicine, Shiyan 442000, China

Corresponding author: Kang Wen-Bin, wbkang@hbmu.edu.cn;wangj@nju.edu.cn;wangwei@nju.edu.cn ; Wang Jun, wbkang@hbmu.edu.cn;wangj@nju.edu.cn;wangwei@nju.edu.cn ; Wang Wei, wbkang@hbmu.edu.cn;wangj@nju.edu.cn;wangwei@nju.edu.cn

Funds: Project supported by the National Basic Research Program of China (Grant No. 2013CB834100), the National Natural Science Foundation of China (Grant Nos. 11334004, 11174133, 81421091, 11774157), the 2017 National Training Program of Innovation and Entrepreneurship for Undergraduates, China (Grant No. 201710929002), and the Initial Project for Post-Graduates of Hubei University of Medicine, China (Grant No. 2011QDZR-11).

References

[1]	Tantos A, Han K H, Tompa P 2012 Mol. Cell. Endocrinol. 348 457
[2]	Dyson H J, Wright P E 2005 Nat. Rev. Mol. Cell Biol. 6 197
[3]	Uversky V N 2002 Eur. J. Biochem. 69 2
[4]	Das R K, Pappu R V 2013 Proc. Natl. Acad. Sci. USA 110 13392
[5]	Yu J F, Dou X H, Sha Y J, Wang C L, Wang H B, Chen Y T, Zhang F, Zhou Y, Wang J H 2017 BMC Bioinform. 18 206
[6]	Piovesan D, Tabaro F, Micetic I, et al. 2017 Nucl. Acids Res. 45 D1123
[7]	Potenza E, Di Domenico T, Walsh I, Tosatto S C 2015 Nucl. Acids Res. 43 D315
[8]	Varadi M, Kosol S, Lebrun P, Valentini E, Blackledge M, Dunker A K, Felli I C, Forman-Kay J D, Kriwacki R W, Pierattelli R, Sussman J, Svergun D I, Uversky V N, Vendruscolo M, Wishart D, Wright P E, Tompa P 2014 Nucl. Acids Res. 42 D326
[9]	Sickmeier M, Hamilton J A, LeGall T, Vacic V, Cortese M S, Tantos A, Szabo B, Tompa P, Chen J, Uversky V N, Obradovic Z, Dunker A K 2007 Nucl. Acids Res. 35 D786
[10]	Sim K L, Uchida T, Miyano S 2001 Bioinformatics 17 379
[11]	Forbes J G, Jin A J, Ma K, Gutierrez-Cruz G, Tsai W L, Wang K 2005 J. Muscle Res. Cell Motil. 26 291
[12]	Uversky V N 2002 Protein Sci. 11 739
[13]	Mao A H, Crick S L, Vitalis A, Chicoine C L, Pappu R V 2010 Proc. Natl. Acad. Sci. USA 107 8183
[14]	Kumar S, Hoh J H 2004 Biochem. Biophys. Res. Commun. 324 489
[15]	Hendus-Altenburger R, Lambrughi M, Terkelsen T, Pedersen S F, Papaleo E, Lindorff-Larsen K, Kragelund B B 2017 Cell. Signal 37 40
[16]	Malka-Gibor E, Kornreich M, Laser-Azogui A, Doron O, Zingerman-Koladko I, Harapin J, Medalia O, Beck R 2017 Biophys. J. 112 892
[17]	Khan S H, McLaughlin W A, Kumar R 2017 Sci. Rep. 7 15440
[18]	Lousa P, Nedozralova H, Zupa E, Novacek J, Hritz J 2017 Biophys. Chem. 223 25
[19]	Stakkestad O, Lyngstadaas S P, Thiede B, Vondrasek J, Skalhegg B S, Reseland J E 2017 Front. Physiol. 8 531
[20]	Liu J J, Dai J, He J F, Niemi A J, Ilieva N 2017 Phys. Rev. E 95 032406
[21]	Das R K, Huang Y, Phillips A H, Kriwacki R W, Pappu R V 2016 Proc. Natl. Acad. Sci. USA 113 5616
[22]	Lange J, Wyrwicz L S, Vriend G 2016 Bioinformatics 32 932
[23]	Arya S, Mukhopadhyay S 2014 J. Phys. Chem. B 118 9191
[24]	Kister A E, Potapov V 2013 Biochem. Soc. Trans. 41 616
[25]	Hoang T X, Trovato A, Seno F, Banavar J R, Maritan A 2012 Phys. Rev. E 86 050901
[26]	Huang Y Q, Liu Z R 2010 Acta Phys. Chim. Sin. 26 2061 (in Chinese) [黄永棋, 刘志荣 2010 物理化学学报 26 2061]
[27]	Dunker A K, Lawson J D, Brown C J, Williams R M, Romero P, Oh J S, Oldfield C J, Campen A M, Ratliff C M, Hipps K W, Ausio J, Nissen M S, Reeves R, Kang C, Kissinger C R, Bailey R W, Griswold M D, Chiu W, Garner E C, Obradovic Z 2001 J. Mol. Graph. Model. 19 26
[28]	Wang J, Wang W 1999 Nat. Struct. Biol. 6 1033
[29]	Li W F, Qin M, Tie Z X, Wang W 2011 Phys. Rev. E 84 041933
[30]	Wang J, Wang W 2016 Adv. Phys. X 1 444
[31]	Vitalis A, Pappu R V 2009 Annu. Rep. Comput. Chem. 5 49
[32]	Vitalis A, Pappu R V 2009 J. Comput. Chem. 30 673
[33]	Pappu R V, Wang X, Vitalis A, Crick S L 2008 Arch. Biochem. Biophys. 469 132
[34]	Cragnell C, Durand D, Cabane B, Skepo M 2016 Proteins 84 777
[35]	Venditto J G, Wolf S, Curotto E, Mella M 2015 Chem. Phys. Lett. 635 127
[36]	Wu H H, Chen C C, Chen C M 2012 J. Comput. Aided Mol. Des. 26 363
[37]	Liu Y, Kellogg E, Liang H J 2012 J. Chem. Phys. 137 045103
[38]	Odriozola G, Berthier L 2011 J. Chem. Phys. 134 054504
[39]	Turner C H, Brennan J K, Lisal M 2007 J. Phys. Chem. C 111 15706
[40]	Kokubo H, Okamoto Y 2004 J. Chem. Phys. 120 10837
[41]	Nakazawa T, Ban S, Okuda Y, Masuya M, Mitsutake A, Okamoto Y 2002 Biopolymers 63 273
[42]	Uversky V N 2013 Intrinsically Disordered Proteins 1 e24684
[43]	Childers M C, Towse C L, Daggett V 2016 Protein Eng. Des. Sel. 29 271
[44]	Yu C, Niu X, Jin F, Liu Z, Jin C, Lai L 2016 Sci. Rep. 6 22298
[45]	Guharoy M, Bhowmick P, Tompa P 2016 J. Biol. Chem. 291 6723
[46]	Nagibina G S, Tin U F, Glukhov A S, Melnik T N, Melnik B S 2016 Protein Pept. Lett. 23 176
[47]	Noivirt-Brik O, Horovitz A, Unger R 2009 PLoS Comput. Biol. 5 e1000592
[48]	Cheng Y, LeGall T, Oldfield C J, Mueller J P, Van Y Y, Romero P, Cortese M S, Uversky V N, Dunker A K 2006 Trends Biotechnol. 24 435
[49]	Ambroggio X I, Kuhlman B 2006 Curr. Opin. Struct. Biol. 16 525
[50]	Meng G Z 1986 Prog. Biochem. Biophys. 13 3 (in Chinese) [盂广震 1986 生物化学与生物物理进展 13 3]
[51]	Wang D C 2008 Protein Engineering (Vol. 1) (Beijing: Chemical Industry Press) p65 (in Chinese) [王大成 2008 蛋白质工程 (北京: 化学工业出版社) 第65页]
[52]	Deng H Y, Jia Y, Zhang Y 2016 Acta Phys. Sin. 65 178701 (in Chinese) [邓海游, 贾亚, 张阳 2016 65 178701]

Cited By

[1]	Tantos A, Han K H, Tompa P 2012 Mol. Cell. Endocrinol. 348 457
[2]	Dyson H J, Wright P E 2005 Nat. Rev. Mol. Cell Biol. 6 197
[3]	Uversky V N 2002 Eur. J. Biochem. 69 2
[4]	Das R K, Pappu R V 2013 Proc. Natl. Acad. Sci. USA 110 13392
[5]	Yu J F, Dou X H, Sha Y J, Wang C L, Wang H B, Chen Y T, Zhang F, Zhou Y, Wang J H 2017 BMC Bioinform. 18 206
[6]	Piovesan D, Tabaro F, Micetic I, et al. 2017 Nucl. Acids Res. 45 D1123
[7]	Potenza E, Di Domenico T, Walsh I, Tosatto S C 2015 Nucl. Acids Res. 43 D315
[8]	Varadi M, Kosol S, Lebrun P, Valentini E, Blackledge M, Dunker A K, Felli I C, Forman-Kay J D, Kriwacki R W, Pierattelli R, Sussman J, Svergun D I, Uversky V N, Vendruscolo M, Wishart D, Wright P E, Tompa P 2014 Nucl. Acids Res. 42 D326
[9]	Sickmeier M, Hamilton J A, LeGall T, Vacic V, Cortese M S, Tantos A, Szabo B, Tompa P, Chen J, Uversky V N, Obradovic Z, Dunker A K 2007 Nucl. Acids Res. 35 D786
[10]	Sim K L, Uchida T, Miyano S 2001 Bioinformatics 17 379
[11]	Forbes J G, Jin A J, Ma K, Gutierrez-Cruz G, Tsai W L, Wang K 2005 J. Muscle Res. Cell Motil. 26 291
[12]	Uversky V N 2002 Protein Sci. 11 739
[13]	Mao A H, Crick S L, Vitalis A, Chicoine C L, Pappu R V 2010 Proc. Natl. Acad. Sci. USA 107 8183
[14]	Kumar S, Hoh J H 2004 Biochem. Biophys. Res. Commun. 324 489
[15]	Hendus-Altenburger R, Lambrughi M, Terkelsen T, Pedersen S F, Papaleo E, Lindorff-Larsen K, Kragelund B B 2017 Cell. Signal 37 40
[16]	Malka-Gibor E, Kornreich M, Laser-Azogui A, Doron O, Zingerman-Koladko I, Harapin J, Medalia O, Beck R 2017 Biophys. J. 112 892
[17]	Khan S H, McLaughlin W A, Kumar R 2017 Sci. Rep. 7 15440
[18]	Lousa P, Nedozralova H, Zupa E, Novacek J, Hritz J 2017 Biophys. Chem. 223 25
[19]	Stakkestad O, Lyngstadaas S P, Thiede B, Vondrasek J, Skalhegg B S, Reseland J E 2017 Front. Physiol. 8 531
[20]	Liu J J, Dai J, He J F, Niemi A J, Ilieva N 2017 Phys. Rev. E 95 032406
[21]	Das R K, Huang Y, Phillips A H, Kriwacki R W, Pappu R V 2016 Proc. Natl. Acad. Sci. USA 113 5616
[22]	Lange J, Wyrwicz L S, Vriend G 2016 Bioinformatics 32 932
[23]	Arya S, Mukhopadhyay S 2014 J. Phys. Chem. B 118 9191
[24]	Kister A E, Potapov V 2013 Biochem. Soc. Trans. 41 616
[25]	Hoang T X, Trovato A, Seno F, Banavar J R, Maritan A 2012 Phys. Rev. E 86 050901
[26]	Huang Y Q, Liu Z R 2010 Acta Phys. Chim. Sin. 26 2061 (in Chinese) [黄永棋, 刘志荣 2010 物理化学学报 26 2061]
[27]	Dunker A K, Lawson J D, Brown C J, Williams R M, Romero P, Oh J S, Oldfield C J, Campen A M, Ratliff C M, Hipps K W, Ausio J, Nissen M S, Reeves R, Kang C, Kissinger C R, Bailey R W, Griswold M D, Chiu W, Garner E C, Obradovic Z 2001 J. Mol. Graph. Model. 19 26
[28]	Wang J, Wang W 1999 Nat. Struct. Biol. 6 1033
[29]	Li W F, Qin M, Tie Z X, Wang W 2011 Phys. Rev. E 84 041933
[30]	Wang J, Wang W 2016 Adv. Phys. X 1 444
[31]	Vitalis A, Pappu R V 2009 Annu. Rep. Comput. Chem. 5 49
[32]	Vitalis A, Pappu R V 2009 J. Comput. Chem. 30 673
[33]	Pappu R V, Wang X, Vitalis A, Crick S L 2008 Arch. Biochem. Biophys. 469 132
[34]	Cragnell C, Durand D, Cabane B, Skepo M 2016 Proteins 84 777
[35]	Venditto J G, Wolf S, Curotto E, Mella M 2015 Chem. Phys. Lett. 635 127
[36]	Wu H H, Chen C C, Chen C M 2012 J. Comput. Aided Mol. Des. 26 363
[37]	Liu Y, Kellogg E, Liang H J 2012 J. Chem. Phys. 137 045103
[38]	Odriozola G, Berthier L 2011 J. Chem. Phys. 134 054504
[39]	Turner C H, Brennan J K, Lisal M 2007 J. Phys. Chem. C 111 15706
[40]	Kokubo H, Okamoto Y 2004 J. Chem. Phys. 120 10837
[41]	Nakazawa T, Ban S, Okuda Y, Masuya M, Mitsutake A, Okamoto Y 2002 Biopolymers 63 273
[42]	Uversky V N 2013 Intrinsically Disordered Proteins 1 e24684
[43]	Childers M C, Towse C L, Daggett V 2016 Protein Eng. Des. Sel. 29 271
[44]	Yu C, Niu X, Jin F, Liu Z, Jin C, Lai L 2016 Sci. Rep. 6 22298
[45]	Guharoy M, Bhowmick P, Tompa P 2016 J. Biol. Chem. 291 6723
[46]	Nagibina G S, Tin U F, Glukhov A S, Melnik T N, Melnik B S 2016 Protein Pept. Lett. 23 176
[47]	Noivirt-Brik O, Horovitz A, Unger R 2009 PLoS Comput. Biol. 5 e1000592
[48]	Cheng Y, LeGall T, Oldfield C J, Mueller J P, Van Y Y, Romero P, Cortese M S, Uversky V N, Dunker A K 2006 Trends Biotechnol. 24 435
[49]	Ambroggio X I, Kuhlman B 2006 Curr. Opin. Struct. Biol. 16 525
[50]	Meng G Z 1986 Prog. Biochem. Biophys. 13 3 (in Chinese) [盂广震 1986 生物化学与生物物理进展 13 3]
[51]	Wang D C 2008 Protein Engineering (Vol. 1) (Beijing: Chemical Industry Press) p65 (in Chinese) [王大成 2008 蛋白质工程 (北京: 化学工业出版社) 第65页]
[52]	Deng H Y, Jia Y, Zhang Y 2016 Acta Phys. Sin. 65 178701 (in Chinese) [邓海游, 贾亚, 张阳 2016 65 178701]

[1]	Liu Qiao, Huang Jia-Chen, Wang Hao, Deng Ya-Jun. Structure and migration mechanism of thin liquid film in vicinity of advancing contact line. Acta Physica Sinica, 2024, 73(1): 016801. doi: 10.7498/aps.73.20231296
[2]	Zhang Xue-Song, Fan Zhen-Zhong, Tong Qi-Lei, Fu Yuan-Feng. Analysis of nanobubble collapse process by molecular simulation method. Acta Physica Sinica, 2024, 73(20): 204701. doi: 10.7498/aps.73.20241105
[3]	Shu Pan-Pan, Zhao Peng-Cheng, Wang Rui. Electromagnetic particle simulation of secondary electron multipactor characteristics in inner surface of 110 GHz microwave output window. Acta Physica Sinica, 2023, 72(9): 095202. doi: 10.7498/aps.72.20222235
[4]	Chen Guang-Lin, Zhang Zhi-Yong. Exploring proten’s conformational space by using encoding layer supervised auto-encoder. Acta Physica Sinica, 2023, 72(24): 248705. doi: 10.7498/aps.72.20231060
[5]	Guan Xing-Yue, Huang Heng-Yan, Peng Hua-Qi, Liu Yan-Hang, Li Wen-Fei, Wang Wei. Machine learning in molecular simulations of biomolecules. Acta Physica Sinica, 2023, 72(24): 248708. doi: 10.7498/aps.72.20231624
[6]	Qiu Zi-Heng, Ahmed Yousif Ghazal, Long Jin-You, Zhang Song. Theoretical studies on molecular conformers and infrared spectra of triethylamine. Acta Physica Sinica, 2022, 71(10): 103601. doi: 10.7498/aps.71.20220123
[7]	Chen Jing-Jing, Qiu Xiao-Lin, Li Ke, Zhou Dan, Yuan Jun-Jun. Mechanical performance analysis of nanocrystalline CoNiCrFeMn high entropy alloy: atomic simulation method. Acta Physica Sinica, 2022, 71(19): 199601. doi: 10.7498/aps.71.20220733
[8]	Wang Yang, Zhao Ling-Ling. Viscoelastic relaxation time of the monoatomic Lennard-Jones system. Acta Physica Sinica, 2020, 69(12): 123101. doi: 10.7498/aps.69.20200138
[9]	Liang Yi-Ran, Liang Qing. Molecular simulation of interaction between charged nanoparticles and phase-separated biomembranes containning charged lipids. Acta Physica Sinica, 2019, 68(2): 028701. doi: 10.7498/aps.68.20181891
[10]	Qin Ya-Qiang, Chen Rui-Yun, Shi Ying, Zhou Hai-Tao, Zhang Guo-Feng, Qin Cheng-Bing, Gao Yan, Xiao Lian-Tuan, Jia Suo-Tang. The role of chain conformation in energy transfer properties of single conjugated polymer molecule. Acta Physica Sinica, 2017, 66(24): 248201. doi: 10.7498/aps.66.248201
[11]	Li Wen-Fei, Zhang Jian, Wang Jun, Wang Wei. Multiscale theory and computational method for biomolecule simulations. Acta Physica Sinica, 2015, 64(9): 098701. doi: 10.7498/aps.64.098701
[12]	Zhou Guang-Gang, Lu Gui-Wu, Jiao Yu-Qiu, Li Ying-Feng, Wang Kun, Yu Yang-Xin. A molecular simulation study on adsorption behavior of solid-liquid interface in KDP crystal. Acta Physica Sinica, 2012, 61(1): 010204. doi: 10.7498/aps.61.010204
[13]	Wen De-Zhi, Zhuo Ren-Hong, Ding Da-Jie, Zheng Hui, Cheng Jing, Li Zheng-Hong. Generation of correlated pseudorandom variables in Monte Carlo simulation. Acta Physica Sinica, 2012, 61(22): 220204. doi: 10.7498/aps.61.220204
[14]	Wang Ke-Dong, Gu Jun, Zhu Chuan-Chuan, Liu Yu-Fang. Ab initio study on CH3C(O)OSSOC(O)CH3: configurations and energies. Acta Physica Sinica, 2011, 60(7): 073102. doi: 10.7498/aps.60.073102
[15]	Xiang Hui, Liu Da-Huan, Yang Qing-Yuan, Mi Jian-Guo, Zhong Chong-Li. Effect of framework flexibility on diffusion of short alkanes in metal-organic framework. Acta Physica Sinica, 2011, 60(9): 093602. doi: 10.7498/aps.60.093602
[16]	Wang Dong-Yi, Xue Chun-Yu, Zhong Chong-Li. A molecular simulation of diffusion mechanism of n-alkanes in copper(Ⅱ) benzene-1,3,5-tricarboxylate metal-organic framework. Acta Physica Sinica, 2009, 58(8): 5552-5559. doi: 10.7498/aps.58.5552
[17]	Xu Hui, Guo Ai-Min, Ma Song-Shan. The influence of base pair sequence on electronic structure of DNA molecules. Acta Physica Sinica, 2007, 56(2): 1208-1213. doi: 10.7498/aps.56.1208
[18]	Li Kai, Liu Hong, Zhang Qing-Chuan, Hou Yi, Zhang Guang-Zhao, Wu Xiao-Ping. Investigation of conformation transition of poly(N-isopropylacrylamide) by surface stress detection using micro-cantilever. Acta Physica Sinica, 2006, 55(8): 4111-4116. doi: 10.7498/aps.55.4111
[19]	Xu Jing. Molecular dynamics modelling of adsorption of HEDP on calcite surface. Acta Physica Sinica, 2006, 55(3): 1107-1112. doi: 10.7498/aps.55.1107
[20]	WANG GUANG-RUI. THE PERIOD-DOUBLING BIFURCATION SEQUENCES OF THE TRIMOLECULAR MODEL WITH FORCED OSCILLATION TERM. Acta Physica Sinica, 1983, 32(7): 960-972. doi: 10.7498/aps.32.960

Catalog

Vol. 67, Issue 5 - 2018-03-05

Metrics

Abstract views: 7185
PDF Downloads: 178
Cited By: 0

姓名
邮箱
手机号码
标题
留言内容
验证码

Search

Article

留言板