Polyarginine (poly-Arg) and arginine-rich peptides have been attracting enormous interest in chemical and cell biology as cell-penetrating peptides capable of direct intracellular penetration. Owing to advances in protein engineering, arginine-rich fragments are often incorporated into multifunctional bioorganic/inorganic core–shell nanoparticles, enabling them the novel unique ability to cross cells and deliver biopharmaceutical cargos. Therefore, understanding the molecular details of the adsorption, packing, and release of poly-Arg onto or from metal nanoparticles is one of the current challenges. In this work, we carry out atomistic molecular dynamics simulations to identify the most favorable location, orientation, and conformation of poly-Arg adsorbed onto a silver nanoparticle (AgNP). Herein, we utilize the constant protonation approach to identify the role of protonation of side chain arginine moieties in the adsorption of poly-Arg to AgNP as a function of pH. The strong adsorption of unprotonated poly-Arg30 onto the quasispherical surface of AgNP with an average diameter of 3.9 nm is primarily governed by multiple interactions of side chain guanidinium (Gdm) moieties, which get stacked and align flat onto the surface. The protonation of the arginine side chain enhances the protein–solvent interactions and promotes the weakening of the protein–nanoparticle binding. The formation of multiple H-bonds between the protonated Arg residues and water molecules favors exposing the charged Gdm+ moieties to the solvent. Protonated poly-Arg30 is found to be partially bound to AgNP due to some weak protein–nanoparticle contacts, maintained by binding of the amide oxygen atoms of the peptide bond. These results suggest that reversible acid–base switching between the arginine protonation states is able to drive the rearrangement of the polyarginine coating around AgNPs, which could be important for a rational design of “intelligent” multifunctional core–shell nanosystems.
REFERENCES
1.
F.
Furno
, K. S.
Morley
, B.
Wong
, B. L.
Sharp
, P. L.
Arnold
, S. M.
Howdle
, R.
Bayston
, P. D.
Brown
, P. D.
Winship
, and H. J.
Reid
, “Silver nanoparticles and polymeric medical devices: A new approach to prevention of infection?
,” J. Antimicrob. Chemother.
54
(6
), 1019
–1024
(2004
). 2.
G.
Franci
, A.
Falanga
, S.
Galdiero
, L.
Palomba
, M.
Rai
, G.
Morelli
, and M.
Galdiero
, “Silver nanoparticles as potential antibacterial agents
,” Molecules
20
(5
), 8856
–8874
(2015
). 3.
P.
Prasher
, M.
Singh
, and H.
Mudila
, “Silver nanoparticles as antimicrobial therapeutics: Current perspectives and future challenges
,” 3 Biotech
8
(10
), 411
(2018
). 4.
A. R.
Tao
, S.
Habas
, and P.
Yang
, “Shape control of colloidal metal nanocrystals
,” Small
4
(3
), 310
–325
(2008
). 5.
I.
Ojea-Jiménez
, L.
García-Fernández
, J.
Lorenzo
, and V. F.
Puntes
, “Facile preparation of cationic gold nanoparticle-bioconjugates for cell penetration and nuclear targeting
,” ACS Nano
6
(9
), 7692
–7702
(2012
). 6.
S.
Du
, S. S.
Liew
, L.
Li
, and S. Q.
Yao
, “Bypassing endocytosis: Direct cytosolic delivery of proteins
,” J. Am. Chem. Soc.
140
(47
), 15986
–15996
(2018
). 7.
M.
Motornov
, Y.
Roiter
, I.
Tokarev
, and S.
Minko
, “Stimuli-responsive nanoparticles, nanogels and capsules for integrated multifunctional intelligent systems
,” Prog. Polym. Sci.
35
(1
), 174
–211
(2010
). 8.
S.
Kango
, S.
Kalia
, A.
Celli
, J.
Njuguna
, Y.
Habibi
, and R.
Kumar
, “Surface modification of inorganic nanoparticles for development of organic–inorganic nanocomposites—A review
,” Prog. Polym. Sci.
38
(8
), 1232
–1261
(2013
). 9.
S.-S.
Nasiri
, M.
Salami-Kalajahi
, H.
Roghani-Mamaqani
, and E.
Dehghani
, “Stimuli-responsive behavior of smart copolymers-grafted magnetic nanoparticles: Effect of sequence of copolymer blocks
,” Inorganica Chim. Acta
476
, 83
–92
(2018
). 10.
M.
von der Lühe
, A.
Weidner
, S.
Dutz
, and F. H.
Schacher
, “Reversible electrostatic adsorption of polyelectrolytes and bovine serum albumin onto polyzwitterion-coated magnetic multicore nanoparticles: Implications for sensing and drug delivery
,” ACS Appl. Nano Mater.
1
(1
), 232
–244
(2018
). 11.
M.
Wei
, Y.
Gao
, X.
Li
, and M. J.
Serpe
, “Stimuli-responsive polymers and their applications
,” Polym. Chem.
8
(1
), 127
–143
(2017
). 12.
Z.
Shen
, M.-P.
Nieh
, and Y.
Li
, “Decorating nanoparticle surface for targeted drug delivery: Opportunities and challenges
,” Polymers
8
(3
), 83
(2016
). 13.
B. T.
Mai
, S.
Fernandes
, P. B.
Balakrishnan
, and T.
Pellegrino
, “Nanosystems based on magnetic nanoparticles and thermo- or pH-responsive polymers: An update and future perspectives
,” Acc. Chem. Res.
51
(5
), 999
–1013
(2018
). 14.
P.
Schattling
, F. D.
Jochum
, and P.
Theato
, “Multi-stimuli responsive polymers—The all-in-one talents
,” Polym. Chem.
5
(1
), 25
–36
(2014
). 15.
J.
Dong
, R.
Zhang
, H.
Wu
, X.
Zhan
, H.
Yang
, S.
Zhu
, and G.
Wang
, “Polymer nanoparticles for controlled release stimulated by visible light and pH
,” Macromol. Rapid Commun.
35
(14
), 1255
–1259
(2014
). 16.
K.
Stamplecoskie
, “Silver nanoparticles: From bulk material to colloidal nanoparticles
,” in Silver Nanoparticle Applications: In the Fabrication and Design of Medical and Biosensing Devices
, edited by E. I.
Alarcon
, M.
Griffith
, and K. I.
Udekwu
(Springer International Publishing
, Cham
, 2015
), pp. 1
–12
.17.
M.
Lozano
, G.
Lollo
, M.
Alonso-Nocelo
, J.
Brea
, A.
Vidal
, D.
Torres
, and M.
Alonso
, “Polyarginine nanocapsules: A new platform for intracellular drug delivery
,” J. Nanopart. Res.
15
, 1515
(2013
). 18.
M.
Vazdar
, J.
Heyda
, P. E.
Mason
, G.
Tesei
, C.
Allolio
, M.
Lund
, and P.
Jungwirth
, “Arginine “magic”: Guanidinium like-charge ion pairing from aqueous salts to cell penetrating peptides
,” Acc. Chem. Res.
51
(6
), 1455
–1464
(2018
). 19.
E.
Vivès
, J.
Schmidt
, and A.
Pèlegrin
, “Cell-penetrating and cell-targeting peptides in drug delivery
,” Biochim. Biophys. Acta
1786
(2
), 126
–138
(2008
). 20.
S.
Futaki
and I.
Nakase
, “Cell-surface interactions on arginine-rich cell-penetrating peptides allow for multiplex modes of internalization
,” Acc. Chem. Res.
50
(10
), 2449
–2456
(2017
). 21.
F.
Tanvir
, A.
Yaqub
, S.
Tanvir
, and A. W.
Anderson
, “Poly-l-arginine coated silver nanoprisms and their anti-bacterial properties
,” Nanomaterials
7
(10
), 296
(2017
). 22.
M.
Kumar
, W.
Tegge
, N.
Wangoo
, R.
Jain
, and R. K.
Sharma
, “Insights into cell penetrating peptide conjugated gold nanoparticles for internalization into bacterial cells
,” Biophys. Chem.
237
, 38
–46
(2018
). 23.
K.
Praveen
, S.
Das
, V.
Dhaware
, B.
Pandey
, B.
Mondal
, and S. S.
Gupta
, “pH-responsive “supra-amphiphilic” nanoparticles based on homoarginine polypeptides
,” ACS Appl. Bio Mater.
2
(10
), 4162
–4172
(2019
). 24.
V.
Ganesan
and A.
Jayaraman
, “Theory and simulation studies of effective interactions, phase behavior and morphology in polymer nanocomposites
,” Soft Matter
10
(1
), 13
–38
(2014
). 25.
A.
Karatrantos
, N.
Clarke
, and M.
Kröger
, “Modeling of polymer structure and conformations in polymer nanocomposites from atomistic to mesoscale: A review
,” Polym. Rev.
56
(3
), 385
–428
(2016
). 26.
H.-M.
Ding
and Y.-Q.
Ma
, “Design strategy of surface decoration for efficient delivery of nanoparticles by computer simulation
,” Sci. Rep.
6
, 26783
(2016
). 27.
A.
Kyrychenko
, G. V.
Karpushina
, S. I.
Bogatyrenko
, A. P.
Kryshtal
, and A. O.
Doroshenko
, “Preparation, structure, and a coarse-grained molecular dynamics model for dodecanethiol-stabilized gold nanoparticles
,” Comput. Theor. Chem.
977
(1–3
), 34
–39
(2011
). 28.
A.
Kyrychenko
, G. V.
Karpushina
, D.
Svechkarev
, D.
Kolodezny
, S. I.
Bogatyrenko
, A. P.
Kryshtal
, and A. O.
Doroshenko
, “Fluorescence probing of thiol-functionalized gold nanoparticles: Is alkylthiol coating of a nanoparticle as hydrophobic as expected?
,” J. Phys. Chem. C
116
(39
), 21059
–21068
(2012
). 29.
M. V.
Slavgorodska
and A. V.
Kyrychenko
, “Binding preference of α-cyclodextrin onto gold nanoparticles
,” Nanosistemi Nanomateriali Nanotehnologii
17
(1
), 133
–144
(2019
), see https://www.imp.kiev.ua/nanosys/media/pdf/2019/1/nano_vol17_iss1_p0133p0144_2019.pdf.30.
M.
Yoneya
and S.-Y.
Sugisawa
, “Simulation of colloidal silver nanoparticle formation from a precursor complex
,” J. Phys. Chem. C
123
(17
), 11257
–11263
(2019
). 31.
M. V.
Slavgorodska
and A.
Kyrychenko
, “Adsorption behavior of β-cyclodextrin onto gold nanoparticles
,” J. Mol. Graph. Model.
94
, 107483
(2020
). 32.
Q.
Shao
and C. K.
Hall
, “Selectivity of glycine for facets on gold nanoparticles
,” J. Phys. Chem. B
122
(13
), 3491
–3499
(2018
). 33.
L. B.
Wright
, N. A.
Merrill
, M. R.
Knecht
, and T. R.
Walsh
, “Structure of arginine overlayers at the aqueous gold interface: Implications for nanoparticle assembly
,” ACS Appl. Mater. Inter.
6
(13
), 10524
–10533
(2014
). 34.
A.
Kyrychenko
, O. M.
Korsun
, I. I.
Gubin
, S. M.
Kovalenko
, and O. N.
Kalugin
, “Atomistic simulations of coating of silver nanoparticles with poly(vinylpyrrolidone) oligomers: Effect of oligomer chain length
,” J. Phys. Chem. C
119
(14
), 7888
–7899
(2015
). 35.
G.
Milano
, G.
Santangelo
, F.
Ragone
, L.
Cavallo
, and A.
Di Matteo
, “Gold nanoparticle/polymer interfaces: All atom structures from molecular dynamics simulations
,” J. Phys. Chem. C
115
(31
), 15154
–15163
(2011
). 36.
J.
Hwang
, Y.
Shim
, S.-M.
Yoon
, S. H.
Lee
, and S.-H.
Park
, “Influence of polyvinylpyrrolidone (PVP) capping layer on silver nanowire networks: Theoretical and experimental studies
,” RSC Adv.
6
(37
), 30972
–30977
(2016
). 37.
A.
Kyrychenko
, D. A.
Pasko
, and O. N.
Kalugin
, “Poly(vinyl alcohol) as a water protecting agent for silver nanoparticles: The role of polymer size and structure
,” Phys. Chem. Chem. Phys.
19
(13
), 8742
–8756
(2017
). 38.
S.
Qing
and K. H.
Carol
, “Protein adsorption on nanoparticles: Model development using computer simulation
,” J. Phys. Condens. Matter
28
(41
), 414019
(2016
). 39.
A.
Kyrychenko
, “NANOGOLD decorated by pHLIP peptide: Comparative force field study
,” Phys. Chem. Chem. Phys.
17
(19
), 12648
–12660
(2015
). 40.
R.
Li
, R.
Chen
, P.
Chen
, Y.
Wen
, P. C.
Ke
, and S. S.
Cho
, “Computational and experimental characterizations of silver nanoparticle–apolipoprotein biocorona
,” J. Phys. Chem. B
117
(43
), 13451
–13456
(2013
). 41.
M. J. A.
Hore
, “Polymers on nanoparticles: Structure & dynamics
,” Soft Matter
15
(6
), 1120
–1134
(2019
). 42.
R. G.
Capelo
, L.
Leppert
, and R. Q.
Albuquerque
, “The concept of localized atomic mobility: Unraveling properties of nanoparticles
,” J. Phys. Chem. C
118
(37
), 21647
–21654
(2014
). 43.
A.
Kyrychenko
, M. M.
Blazhynska
, M. V.
Slavgorodska
, and O. N.
Kalugin
, “Stimuli-responsive adsorption of poly(acrylic acid) onto silver nanoparticles: Role of polymer chain length and degree of ionization
,” J. Mol. Liq.
276
, 243
–254
(2019
). 44.
M. M.
Blazhynska
, A. V.
Kyrychenko
, and O. N.
Kalugin
, “Polarizable force field for molecular dynamics simulations of silver nanoparticles
,” V.N. Karazin Kharkiv Natl Univ. Bull. Chem. Ser.
32
, 46
–58
(2019
). 45.
M. M.
Blazhynska
, A.
Kyrychenko
, and O. N.
Kalugin
, “Molecular dynamics simulation of the size-dependent morphological stability of cubic shape silver nanoparticles
,” Mol. Simul.
44
(12
), 981
–991
(2018
). 46.
D.
Van Der Spoel
, E.
Lindahl
, B.
Hess
, G.
Groenhof
, A. E.
Mark
, and H. J. C.
Berendsen
, “GROMACS: Fast, flexible, and free
,” J. Comput. Chem.
26
(16
), 1701
–1718
(2005
). 47.
J.-M.
Hu
, W.-D.
Tian
, and Y.-Q.
Ma
, “Computational investigations of arginine-rich peptides interacting with lipid membranes
,” Macromol. Theory Simul.
24
(4
), 399
–406
(2015
). 48.
Y.
Hu
, S. K.
Sinha
, and S.
Patel
, “Reconciling structural and thermodynamic predictions using all-atom and coarse-grain force fields: The case of charged oligo-arginine translocation into DMPC bilayers
,” J. Phys. Chem. B
118
(41
), 11973
–11992
(2014
). 49.
Y.
Hu
, X.
Liu
, S. K.
Sinha
, and S.
Patel
, “Translocation thermodynamics of linear and cyclic nonaarginine into model DPPC bilayer via coarse-grained molecular dynamics simulation: Implications of pore formation and nonadditivity
,” J. Phys. Chem. B
118
(10
), 2670
–2682
(2014
). 50.
A.
Kubíčková
, T.
Křížek
, P.
Coufal
, E.
Wernersson
, J.
Heyda
, and P.
Jungwirth
, “Guanidinium cations pair with positively charged arginine side chains in water
,” J. Phys. Chem. Lett.
2
(12
), 1387
–1389
(2011
). 51.
J.
Vondrášek
, P. E.
Mason
, J.
Heyda
, K. D.
Collins
, and P.
Jungwirth
, “The molecular origin of like-charge arginine−arginine pairing in water
,” J. Phys. Chem. B
113
(27
), 9041
–9045
(2009
). 52.
M.
Vazdar
, E.
Wernersson
, M.
Khabiri
, L.
Cwiklik
, P.
Jurkiewicz
, M.
Hof
, E.
Mann
, S.
Kolusheva
, R.
Jelinek
, and P.
Jungwirth
, “Aggregation of oligoarginines at phospholipid membranes: Molecular dynamics simulations, time-dependent fluorescence shift, and biomimetic colorimetric assays
,” J. Phys. Chem. B
117
(39
), 11530
–11540
(2013
). 53.
Z.
Wu
, Q.
Cui
, and A.
Yethiraj
, “Why do arginine and lysine organize lipids differently? Insights from coarse-grained and atomistic simulations
,” J. Phys. Chem. B
117
(40
), 12145
–12156
(2013
). 54.
D.
Sun
, J.
Forsman
, and C. E.
Woodward
, “Atomistic molecular simulations suggest a kinetic model for membrane translocation by arginine-rich peptides
,” J. Phys. Chem. B
119
(45
), 14413
–14420
(2015
). 55.
A. D.
Robison
, S.
Sun
, M. F.
Poyton
, G. A.
Johnson
, J.-P.
Pellois
, P.
Jungwirth
, M.
Vazdar
, and P. S.
Cremer
, “Polyarginine interacts more strongly and cooperatively than polylysine with phospholipid bilayers
,” J. Phys. Chem. B
120
(35
), 9287
–9296
(2016
). 56.
G.
Tesei
, M.
Vazdar
, M. R.
Jensen
, C.
Cragnell
, P. E.
Mason
, J.
Heyda
, M.
Skepö
, P.
Jungwirth
, and M.
Lund
, “Self-association of a highly charged arginine-rich cell-penetrating peptide
,” Proc. Natl. Acad. Sci. U.S.A.
114
(43
), 11428
(2017
). 57.
K.
Huang
and A. E.
García
, “Free energy of translocating an arginine-rich cell-penetrating peptide across a lipid bilayer suggests pore formation
,” Biophys. J.
104
(2
), 412
–420
(2013
). 58.
C.
Oostenbrink
, A.
Villa
, A. E.
Mark
, and W. F.
Van Gunsteren
, “A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6
,” J. Comput. Chem.
25
(13
), 1656
–1676
(2004
). 59.
M. D.
Smith
, J. S.
Rao
, E.
Segelken
, and L.
Cruz
, “Force-field induced bias in the structure of Aβ21–30: A comparison of OPLS, AMBER, CHARMM, and GROMOS force fields
,” J. Chem. Inf. Model.
55
(12
), 2587
–2595
(2015
). 60.
O. S.
Zhelavskyi
and A.
Kyrychenko
, “Atomistic molecular dynamics simulations of the LCST conformational transition in poly(N-vinylcaprolactam) in water
,” J. Mol. Graph. Model.
90
, 51
–58
(2019
). 61.
D.
Gurina
, O.
Surov
, M.
Voronova
, A.
Zakharov
, and M.
Kiselev
, “Water effects on molecular adsorption of poly(N-vinyl-2-pyrrolidone) on cellulose nanocrystals surfaces: Molecular dynamics simulations
,” Materials
12
(13
), 2155
(2019
). 62.
T. E.
Gartner
and A.
Jayaraman
, “Modeling and simulations of polymers: A roadmap
,” Macromolecules
52
(3
), 755
–786
(2019
). 63.
D.
Svechkarev
, A.
Kyrychenko
, W. M.
Payne
, and A. M.
Mohs
, “Probing the self-assembly dynamics and internal structure of amphiphilic hyaluronic acid conjugates by fluorescence spectroscopy and molecular dynamics simulations
,” Soft Matter
14
(23
), 4762
–4771
(2018
). 64.
W. M.
Payne
, D.
Svechkarev
, A.
Kyrychenko
, and A. M.
Mohs
, “The role of hydrophobic modification on hyaluronic acid dynamics and self-assembly
,” Carbohydr. Polym.
182
, 132
–141
(2018
). 65.
J.
Hermans
, H. J. C.
Berendsen
, W. F.
Van Gunsteren
, and J. P. M.
Postma
, “A consistent empirical potential for water–protein interactions
,” Biopolymers
23
(8
), 1513
–1518
(1984
). 66.
Y.
Huang
, R. C.
Harris
, and J.
Shen
, “Generalized born based continuous constant pH molecular dynamics in AMBER: Implementation, benchmarking and analysis
,” J. Chem. Inf. Model.
58
(7
), 1372
–1383
(2018
). 67.
E.
Socher
and H.
Sticht
, “Mimicking titration experiments with MD simulations: A protocol for the investigation of pH-dependent effects on proteins
,” Sci. Rep.
6
, 22523
(2016
). 68.
J.
Landsgesell
, L.
Nová
, O.
Rud
, F.
Uhlík
, D.
Sean
, P.
Hebbeker
, C.
Holm
, and P.
Košovan
, “Simulations of ionization equilibria in weak polyelectrolyte solutions and gels
,” Soft Matter
15
(6
), 1155
–1185
(2019
). 69.
A.
Damjanovic
, B. T.
Miller
, A.
Okur
, and B. R.
Brooks
, “Reservoir pH replica exchange
,” J. Chem. Phys.
149
(7
), 072321
(2018
). 70.
J. M.
Swails
, D. M.
York
, and A. E.
Roitberg
, “Constant pH replica exchange molecular dynamics in explicit solvent using discrete protonation states: Implementation, testing, and validation
,” J. Chem. Theory Comput.
10
(3
), 1341
–1352
(2014
). 71.
W.
Chen
, B. H.
Morrow
, C.
Shi
, and J. K.
Shen
, “Recent development and application of constant pH molecular dynamics
,” Mol. Simul.
40
(10–11
), 830
–838
(2014
). 72.
J.
Landsgesell
, C.
Holm
, and J.
Smiatek
, “Simulation of weak polyelectrolytes: A comparison between the constant pH and the reaction ensemble method
,” Eur. Phys. J. Spec. Top.
226
(4
), 725
–736
(2017
). 73.
B. K.
Radak
, C.
Chipot
, D.
Suh
, S.
Jo
, W.
Jiang
, J. C.
Phillips
, K.
Schulten
, and B.
Roux
, “Constant-pH molecular dynamics simulations for large biomolecular systems
,” J. Chem. Theory Comput.
13
(12
), 5933
–5944
(2017
). 74.
R. S.
Katiyar
and P. K.
Jha
, “Phase behavior of aqueous polyacrylic acid solutions using atomistic molecular dynamics simulations of model oligomers
,” Polymer
114
, 266
–276
(2017
). 75.
M. S.
Sulatha
and U.
Natarajan
, “Origin of the difference in structural behavior of poly(acrylic acid) and poly(methacrylic acid) in aqueous solution discerned by explicit-solvent explicit-ion MD simulations
,” Ind. Eng. Chem. Res.
50
(21
), 11785
–11796
(2011
). 76.
K.
Karatasos
and G.
Kritikos
, “A microscopic view of graphene-oxide/poly(acrylic acid) physical hydrogels: Effects of polymer charge and graphene oxide loading
,” Soft Matter
14
(4
), 614
–627
(2018
). 77.
I.
Kim
, T. A.
Pascal
, S.-J.
Park
, M.
Diallo
, W. A.
Goddard
III, and Y.
Jung
, “pH-dependent conformations for hyperbranched poly(ethylenimine) from all-atom molecular dynamics
,” Macromolecules
51
(6
), 2187
–2194
(2018
). 78.
K. P.
Jha
, S. P.
Desai
, J.
Li
, and G. R.
Larson
, “pH and salt effects on the associative phase separation of oppositely charged polyelectrolytes
,” Polymers
6
(5
), 1414
–1436
(2014
). 79.
R. S.
Katiyar
and P. K.
Jha
, “Mimicking the dissolution mechanisms of pH-responsive drug release formulations in atomistic MD simulations
,” Adv. Theory Simul.
2
(8
), 1900053
(2019
). 80.
K. H.
Patel
, R.
Chockalingam
, and U.
Natarajan
, “Molecular dynamic simulations study of the effect of salt valency on structure and thermodynamic solvation behaviour of anionic polyacrylate PAA in aqueous solutions
,” Mol. Simul.
43
(9
), 691
–705
(2017
). 81.
A. K.
Gupta
and U.
Natarajan
, “Anionic polyelectrolyte poly(acrylic acid) (PAA) chain shrinkage in water–ethanol solution in presence of Li+ and Cs+ metal ions studied by molecular dynamics simulations
,” Mol. Simul.
43
(8
), 625
–637
(2017
). 82.
A. K.
Gupta
and U.
Natarajan
, “Tacticity effects on conformational structure and hydration of poly-(methacrylic acid) in aqueous solutions—A molecular dynamics simulation study
,” Mol. Simul.
42
(9
), 725
–736
(2016
). 83.
D.
Romero Nieto
, A.
Lindbråthen
, and M.-B.
Hägg
, “Effect of water interactions on polyvinylamine at different pHs for membrane gas separation
,” ACS Omega
2
(11
), 8388
–8400
(2017
). 84.
G.
Bussi
, D.
Donadio
, and M.
Parrinello
, “Canonical sampling through velocity rescaling
,” J. Chem. Phys.
126
(1
), 014101
(2007
). 85.
T.
Darden
, D.
York
, and L.
Pedersen
, “Particle mesh Ewald: An N(log(N) method for Ewald sums in large systems
,” J. Chem. Phys.
98
(12
), 10089
–10092
(1993
). 86.
B.
Hess
, H.
Bekker
, H. J. C.
Berendsen
, and J. G. E. M.
Fraaije
, “LINCS: A linear constraint solver for molecular simulations
,” J. Comput. Chem.
18
(12
), 1463
–1472
(1997
). 87.
W.
Humphrey
, A.
Dalke
, and K.
Schulten
, “VMD: Visual molecular dynamics
,” J. Mol. Graph.
14
(1
), 33
–38
(1996
). 88.
C. L. A.
Schmidt
, P. L.
Kirk
, and W. K.
Appleman
, “The apparent dissociation constants of arginine and of lysine and the apparent heats of ionization of certain amino acids
,” J. Biol. Chem.
88
(1
), 285
–293
(1930
).89.
H.
Nagai
, K.
Kuwabara
, and G.
Carta
, “Temperature dependence of the dissociation constants of several amino acids
,” J. Chem. Eng. Data
53
(3
), 619
–627
(2008
). 90.
B.
Noszál
and R.
Kassai-Tánczos
, “Microscopic acid–base equilibria of arginine
,” Talanta
38
(12
), 1439
–1444
(1991
). 91.
C. A.
Fitch
, G.
Platzer
, M.
Okon
, B.
Garcia-Moreno E
, and L. P.
McIntosh
, “Arginine: Its pKa value revisited
,” Protein Sci.
24
(5
), 752
–761
(2015
). 92.
B.
Xu
, M. I.
Jacobs
, O.
Kostko
, and M.
Ahmed
, “Guanidinium group remains protonated in a strongly basic arginine solution
,” ChemPhysChem
18
(12
), 1503
–1506
(2017
). 93.
N.
Sakai
and S.
Matile
, “Anion-mediated transfer of polyarginine across liquid and bilayer membranes
,” J. Am. Chem. Soc.
125
(47
), 14348
–14356
(2003
). 94.
H.
Heinz
and H.
Ramezani-Dakhel
, “Simulations of inorganic-bioorganic interfaces to discover new materials: Insights, comparisons to experiment, challenges, and opportunities
,” Chem. Soc. Rev.
45
(2
), 412
–448
(2016
). 95.
T. R.
Walsh
and M. R.
Knecht
, “Biointerface structural effects on the properties and applications of bioinspired peptide-based nanomaterials
,” Chem. Rev.
117
(20
), 12641
–12704
(2017
). 96.
T. R.
Walsh
, “Pathways to structure–property relationships of peptide–materials interfaces: Challenges in predicting molecular structures
,” Acc. Chem. Res.
50
(7
), 1617
–1624
(2017
). 97.
Z.
Xu
, X.
Yang
, Q.
Wei
, W.
Zhao
, B.
Cui
, X.
Yang
, and N.
Sahai
, “Quantitatively identifying the roles of interfacial water and solid surface in governing peptide adsorption
,” Langmuir
34
(26
), 7932
–7941
(2018
). 98.
D.
van der Spoel
, P. J.
van Maaren
, P.
Larsson
, and N.
Tîmneanu
, “Thermodynamics of hydrogen bonding in hydrophilic and hydrophobic media
,” J. Phys. Chem. B
110
(9
), 4393
–4398
(2006
). 99.
S.
Richert
, S.
Mosquera Vazquez
, M.
Grzybowski
, D. T.
Gryko
, A.
Kyrychenko
, and E.
Vauthey
, “Excited-state dynamics of an environment-sensitive push–pull diketopyrrolopyrrole: Major differences between the bulk solution phase and the dodecane/water interface
,” J. Phys. Chem. B
118
(33
), 9952
–9963
(2014
). 100.
H.
Heinz
, R. A.
Vaia
, B. L.
Farmer
, and R. R.
Naik
, “Accurate simulation of surfaces and interfaces of face-centered cubic metals using 12–6 and 9–6 Lennard-Jones potentials
,” J. Phys. Chem. C
112
(44
), 17281
–17290
(2008
). © 2020 Author(s).
2020
Author(s)
You do not currently have access to this content.
