Understanding the influence of a crowded intracellular environment on the structure and solvation of DNA functionalized gold nanoparticles (ss-DNA AuNP) is necessary for designing applications in nanomedicine. In this study, the effect of single (Gly, Ser, Lys) and mixture of amino acids (Gly+Ser, Gly+Lys, Ser+Lys) at crowded concentrations is examined on the structure of the ss-DNA AuNP using molecular dynamics simulations. Using the structural estimators such as pair correlation functions and ligand shell positional fluctuations, the solvation entropy is estimated. Combining the AuNP–solvent interaction energy with the solvation entropy estimates, the free energy of solvation of the AuNP in crowded solutions is computed. The solvation entropy favours the solvation free energy which becomes more favourable for larger effective size of AuNP in crowded solutions relative to that in water. The effective size of AuNP depends on the different propensity of the crowders to adsorb on Au surface, with the smallest crowder (Gly) having the highest propensity inducing the least effective AuNP size as compared to other single crowder solutions. In mixed crowded solutions of amino acids of variable size and chemistry, distinctive local adsorption of the crowders on the gold surface is observed that controls the additive or non-additive crowding effects which govern an increase (in Gly+Ser) or decrease (in Gly+Lys) in nanoparticle effective size respectively. The results shed light into the fundamental understanding of the influence of intracellular crowding on structure of ss-DNA AuNP and plausible employability of crowding as a tool to design programmable self-assembly of functionalized nanoparticles.
REFERENCES
1.
J. J.
Storhoff
and C. A.
Mirkin
, “Programmed materials synthesis with DNA
,” Chem. Rev.
99
, 1849
–1862
(1999
).2.
S. Y.
Park
, A. K.
Lytton-Jean
, B.
Lee
, S.
Weigand
, G. C.
Schatz
, and C. A.
Mirkin
, “DNA-programmable nanoparticle crystallization
,” Nature
451
, 553
–556
(2008
).3.
K.
Saha
, S. S.
Agasti
, C.
Kim
, X.
Li
, and V. M.
Rotello
, “Gold nanoparticles in chemical and biological sensing
,” Chem. Rev.
112
, 2739
–2779
(2012
).4.
W.
Zhao
, M. A.
Brook
, and Y.
Li
, “Design of gold nanoparticle-based colorimetric biosensing assays
,” ChemBioChem
9
, 2363
–2371
(2008
).5.
N. L.
Rosi
and C. A.
Mirkin
, “Nanostructures in biodiagnostics
,” ChemInform
36
, 1547
–1562
(2005
).6.
D. A.
Giljohann
, D. S.
Seferos
, W. L.
Daniel
, M. D.
Massich
, P. C.
Patel
, and C. A.
Mirkin
, “Gold nanoparticles for biology and medicine
,” Angew. Chem., Int. Ed.
49
, 3280
–3294
(2010
).7.
H.
Wang
, R.
Yang
, L.
Yang
, and W.
Tan
, “Nucleic acid conjugated nanomaterials for enhanced molecular recognition
,” ACS Nano
3
, 2451
–2460
(2009
).8.
O. S.
Lee
, T. R.
Prytkova
, and G. C.
Schatz
, “Using DNA to link gold nanoparticles, polymers, and molecules: A theoretical perspective
,” J. Phys. Chem. Lett.
1
, 1781
–1788
(2010
).9.
S.
Asakura
and F.
Oosawa
, “Interaction between particles suspended in solutions of macromolecules
,” Journal of Polymer Science
33
, 183
–192
(1958
).10.
R.
Bhat
and S. N.
Timasheff
, “Steric exclusion is the principal source of the preferential hydration of proteins in the presence of polyethylene glycols
,” Protein Sci.
1
, 1133
–1143
(1992
).11.
R. J.
Ellis
, “Macromolecular crowding: An important but neglected aspect of the intracellular environment
,” Curr. Opin. Struct. Biol.
11
, 114
–119
(2001
).12.
S. B.
Zimmerman
and A. P.
Minton
, “Macromolecular crowding: Biochemical, biophysical, and physiological consequences
,” Annu. Rev. Biophys. Biomol. Struct.
22
, 27
–65
(1993
).13.
H. X.
Zhou
, G.
Rivas
, and A. P.
Minton
, “Macromolecular crowding and confinement: Biochemical, biophysical, and potential physiological consequences
,” Annu. Rev. Biophys.
37
, 375
–397
(2008
).14.
R.
Harada
, N.
Tochio
, T.
Kigawa
, Y.
Sugita
, and M.
Feig
, “Reduced native state stability in crowded cellular environment due to protein-protein interactions
,” J. Am. Chem. Soc.
135
, 3696
–3701
(2013
).15.
M.
Senske
, L.
Törk
, B.
Born
, M.
Havenith
, C.
Herrmann
, and S.
Ebbinghaus
, “Protein stabilization by macromolecular crowding through enthalpy rather than entropy
,” J. Am. Chem. Soc.
136
, 9036
–9041
(2014
).16.
S. K.
Mukherjee
, S.
Gautam
, S.
Biswas
, J.
Kundu
, and P. K.
Chowdhury
, “Do macromolecular crowding agents exert only an excluded volume effect? A protein solvation study
,” J. Phys. Chem. B
119
, 14145
–14156
(2015
).17.
L.
Sapir
and D.
Harries
, “Is the depletion force entropic? Molecular crowding beyond steric interactions
,” Curr. Opin. Colloid Interface Sci.
20
, 3
–10
(2015
).18.
D.
Nayar
, “Small crowder interactions can drive hydrophobic polymer collapse as well as unfolding
,” Phys. Chem. Chem. Phys.
22
, 18091
–18101
(2020
).19.
M.
Sarkar
, C.
Li
, and G. J.
Pielak
, “Soft interactions and crowding
,” Biophys. Rev.
5
, 187
–194
(2013
).20.
D.
Nayar
, H. O. S.
Yadav
, B. S.
Jabes
, and C.
Chakravarty
, “Relating structure, entropy, and energy of solvation of nanoscale solutes: Application to gold nanoparticle dispersions
,” J. Phys. Chem. B
116
, 13124
–13132
(2012
).21.
O. S.
Lee
and G. C.
Schatz
, “Molecular dynamics simulation of DNA-functionalized gold nanoparticles
,” J. Phys. Chem. C
113
, 2316
–2321
(2009
).22.
R.
Jin
, G.
Wu
, Z.
Li
, C. A.
Mirkin
, and G. C.
Schatz
, “What controls the melting properties of DNA-linked gold nanoparticle assemblies?
,” J. Am. Chem. Soc.
125
, 1643
–1654
(2003
).23.
S. J.
Hurst
, H. D.
Hill
, and C. A.
Mirkin
, ““Three-Dimensional hybridization” with polyvalent DNA−Gold nanoparticle conjugates
,” J. Am. Chem. Soc.
130
, 12192
–12200
(2008
).24.
S. J.
Tan
, J. S.
Kahn
, T. L.
Derrien
, M. J.
Campolongo
, M.
Zhao
, D.-M.
Smilgies
, and D.
Luo
, “Crystallization of DNA-capped gold nanoparticles in high-concentration, divalent salt environments
,” Angew. Chem.
126
, 1340
–1343
(2014
).25.
G. P.
Goodrich
, M. R.
Helfrich
, J. J.
Overberg
, and C. D.
Keating
, “Effect of macromolecular crowding on DNA:Au nanoparticle bioconjugate assembly
,” Langmuir
20
, 10246
–10251
(2004
).26.
J.
Shin
, X.
Zhang
, and J.
Liu
, “DNA-functionalized gold nanoparticles in macromolecularly crowded polymer solutions
,” J. Phys. Chem. B
116
, 13396
–13402
(2012
).27.
P. E.
Theodorakis
, N. G.
Fytas
, G.
Kahl
, and C.
Dellago
, “Self-assembly of DNA-functionalized colloids
,” Condens. Matter Phys.
18
, 22801
–22824
(2015
).28.
A.
Seifpour
, S. R.
Dahl
, and A.
Jayaraman
, “Molecular simulation study of assembly of DNA-grafted nanoparticles: Effect of bidispersity in DNA strand length
,” Mol. Simul.
40
, 1085
–1098
(2014
).29.
N. K.
Li
, H. S.
Kim
, J. A.
Nash
, M.
Lim
, and Y. G.
Yingling
, “Progress in molecular modelling of DNA materials
,” Mol. Simul.
40
, 777
–783
(2014
).30.
A. D.
MacKerell
et al, “All-atom empirical potential for molecular modeling and dynamics studies of proteins
,” The Journal of Physical Chemistry B
102
, 3586
–3616
(1998
).31.
J.
Yoo
and A.
Aksimentiev
, “Improved parameterization of amine-carboxylate and amine-phosphate interactions for molecular dynamics simulations using the charmm and amber force fields
,” J. Chem. Theory Comput.
12
, 430
–443
(2016
).32.
S.
Panigrahy
, R.
Sahu
, S. K.
Reddy
, and D.
Nayar
, “Structure, energetics and dynamics in crowded amino acid solutions: A molecular dynamics study
,” Phys. Chem. Chem. Phys.
25
, 5430
–5442
(2023
).33.
J.
Hautman
and M. L.
Klein
, “Simulation of a monolayer of alkyl thiol chains
,” J. Chem. Phys.
91
, 4994
–5001
(1989
).34.
B.
Hess
, C.
Kutzner
, D.
van der Spoel
, and E.
Lindahl
, “GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation
,” J. Chem. Theory Comput.
4
, 435
–447
(2008
).35.
T.
Darden
, D.
York
, and L.
Pedersen
, “Particle mesh ewald: An nlog(n) method for ewald sums in large systems
,” J. Chem. Phys.
98
, 10089
–10092
(1993
).36.
A.
Ben-Naim
, “Standard thermodynamics of transfer. Uses and misuses
,” J. Phys. Chem.
82
, 792
–803
(1978
).37.
T.
Lazaridis
, “Inhomogeneous fluid approach to solvation thermodynamics. 1. Theory
,” J. Phys. Chem. B
102
, 3531
–3541
(1998
).38.
T.
Lazaridis
, “Inhomogeneous fluid approach to solvation thermodynamics. 2. Applications to simple fluids
,” J. Phys. Chem. B
102
, 3542
–3550
(1998
).39.
A.
Baranyai
and D. J.
Evans
, “Direct entropy calculation from computer simulation of liquids
,” Phys. Rev. A
40
, 3817
–3822
(1989
).40.
D. C.
Wallace
, “On the role of density fluctuations in the entropy of a fluid
,” J. Chem. Phys.
87
, 2282
–2284
(1987
).41.
J. G.
Kirkwood
and F. P.
Buff
, “The statistical mechanical theory of solutions. I
,” J. Chem. Phys.
19
, 774
–777
(1951
).42.
V.
Pierce
, M.
Kang
, M.
Aburi
, S.
Weerasinghe
, and P.
Smith
, “Recent applications of kirkwood-buff theory to biological systems
,” Cell Biochem. Biophys.
50
, 1
–22
(2008
).43.
Z.
Li
, V. G.
Ruiz
, M.
Kanduč
, and J.
Dzubiella
, “Ion-specific adsorption on bare gold (Au) nanoparticles in aqueous solutions: Double-layer structure and surface potentials
,” Langmuir
36
, 13457
–13468
(2020
).44.
Z.
Li
, V. G.
Ruiz
, M.
Kanduč
, and J.
Dzubiella
, “Highly heterogeneous polarization and solvation of gold nanoparticles in aqueous electrolytes
,” ACS Nano
15
, 13155
–13165
(2021
).45.
J.
Schlitter
, “Estimation of absolute and relative entropies of macromolecules using the covariance matrix
,” Chem. Phys. Lett.
215
, 617
–621
(1993
).46.
P.
Ganguly
, N. F. A.
van der Vegt
, and van der Vegt
, “Convergence of sampling kirkwood–buff integrals of aqueous solutions with molecular dynamics simulations
,” J. Chem. Theory Comput.
9
, 1347
–1355
(2013
).47.
J.
Milzetti
, D.
Nayar
, and N. F.
Van Der Vegt
, “Convergence of kirkwood-buff integrals of ideal and nonideal aqueous solutions using molecular dynamics simulations
,” J. Phys. Chem. B
122
, 5515
–5526
(2018
).© 2024 Author(s). Published under an exclusive license by AIP Publishing.
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