Peptide Synthesis of Gold Nanoparticles: The Early Steps of Gold

Feb 14, 2011 - Gold nanoparticles can be synthesized by reducing chloroaurate(III) ions in the presence of peptides. Here, such reduction for serine a...
0 downloads 0 Views 2MB Size
LETTER pubs.acs.org/NanoLett

Peptide Synthesis of Gold Nanoparticles: The Early Steps of Gold Reduction Investigated by Density Functional Theory Dimitrios Toroz and Stefano Corni* Centro S3, CNR—Istituto Nanoscienze, Via Campi 213/A, 41125 Modena, Italy

bS Supporting Information ABSTRACT: Gold nanoparticles can be synthesized by reducing chloroaurate(III) ions in the presence of peptides. Here, such reduction for serine and tyrosine is studied by density functional theory including solvent effects. We find that the formation of chloroaurate complexes of these amino acids is thermodynamically viable and facilitates the reduction of Au(III), to a greater degree for tyrosine as found in experiments. Our results also suggest a rationale for the behavior of tyrosineintercalated peptides. KEYWORDS: Nanoparticle formation, protein-nanoparticle interactions, gold chloroaurate reduction, ab initio calculations

T

he synthesis and design of metal nanoparticles constitute an evolving branch of nanoscience and nanotechnology.1 The synthesis in particular of gold nanoparticles has received considerable attention due to their application in various fields such as catalysis2-4 and biomedical applications.5-10 Remarkably, it has been reported that various peptides can produce accelerated growth of metal nanoparticles (in some cases with uncommon shapes) which is the result of the intervention of the peptide in the process of gold salt reduction and metal cluster growth.11,12 Such behavior is intimately related to the capability of peptides or proteins to specifically bind to selected inorganic solids (and even to particular surface planes of them), which is highly promising as a general tool to implement nano- and biotechnology applications.13 To date there are a number of studies that have been focused on experimental synthesis procedures for obtaining gold nanoparticles by peptides and amino acids. Several studies have been focused on the kinetics of the reaction between the tetrachloroaurate(III) ions (AuCl4-) and the peptides14-16 whereas others have investigated, apart from the synthesis, also the spectroscopic and structural characterization of the metal nanoparticles.17-22 To the best of our knowledge, however, the microscopic mechanism of the formation of gold nanoparticles in the presence of peptides is still unknown. Here we address by density functional theory (DFT) calculations the role of peptides in the reduction of chloroaurate ions: Can the peptides bind such gold nanoparticle precursors? If so, is the resulting gold complex easier to be reduced? Will the bound peptide directly act as a reducing agent for Au(III)? Despite the considerable theoretical literature on gold,23 these issues are still unaddressed. In our calculations we have considered two amino acids, serine (ser) and tyrosine (tyr), which both contain a hydroxyl group as the terminal part of their side chain. Wang et al. presented a bottom up approach to set the design rules for the size and shape controlled peptide synthesis of gold nanoparticles from the properties of the r 2011 American Chemical Society

20 natural amino acids for AuCl4- reduction.14 Among the findings of this study was the reduction capability rating for amino acids where ser was able to promote gold nanoparticle formation but presented much less reduction capability than tyr. In agreement with these experimental findings, our results suggest that both ser and tyr favor the reduction of gold and that tyr is more effective than ser. In particular, we find that tyr, once bound to Au(III), can reduce the gold ion to Au(II), and the reaction can then follow a well-known pathway leading to dityrosine formation. We remark that here we focus on the initial reduction from Au(III) to Au(II). In fact, once the unstable Au(II) is formed, it is known to undergo fast disproportionation to Au(III) and Au(I); the latter can further disproportionate to Au(III) and Au(0).24,25 As the first step of our study, we modeled the possible binding of the chloroaurate ion to the amino acids. We have considered the reaction where one ligand of the chloroaurate ions is replaced by tyr or ser, binding Au via their side chain, to form AuCl3-amino acid complexes. Gold complexation with the backbone has not been considered, as the strong dependency on the amino acid nature seen in the experimental reduction studies suggests that interactions take place mainly with the side chains of the peptide.26 To investigate the role of the peptide backbone,27,28 we have considered both the entire, capped tyr and ser molecules and the simplest analogues of the bare side chains of ser and tyrosine (methanol and 4-methylphenol). Full details on these and the other calculations of the present work are given in the Supporting Information. In summary, we have used B3LYP exchange-correlation functional in its restricted (for singlet species) or unrestricted (for all the others) form, employing the LANL2DZ basis set Received: December 16, 2010 Revised: January 25, 2011 Published: February 14, 2011 1313

dx.doi.org/10.1021/nl1043924 | Nano Lett. 2011, 11, 1313–1318

Nano Letters

LETTER

Scheme 1. Individual Reaction Free Energies (in kJ/mol) for Different Ligand Displacement Reaction to Form AuCl3-ser and AuCl3-tyr Complexesa

ΔΔGreac is relative to the ΔGreac calculated for the displacement by oxalate, equation (1), while estimated ΔGreac is obtained by summing to ΔΔGreac the experimental ΔGreac for oxalate. a

(and effective core potential for Au).29 Solvation effects were taken into account by the Integral Equation Formalism Polarizable Continuum Model (IEF-PCM).30 All the calculations have been performed with the Gaussian 03 suite of codes.31 The ligand displacement reactions and their corresponding standard free energies (ΔGreac) data are presented in Scheme 1. As absolute values of ΔGreac are difficult to be reliably predicted by calculations, we first calculated ΔGreac,calc for the various reactions in Scheme 1 relative to the calculated ΔGreac,ref for a similar reaction whose equilibrium constant is known. For the latter, we used the ligand displacement in AuCl4- by an oxalate ion (C2O42-) in water:32 AuCl4 - þC2 O4 2-fAuCl3 ðC2 O4 Þ2- þCl-

ð1Þ

The calculated ΔΔGreac = ΔGreac,calc - ΔGreac,ref are reported in Scheme 1. From them, an estimate of ΔGreac has been obtained by using the experimental value of ΔGreac for the eq 1, -36.3 kJ/mol, deduced from the equilibrium constant given in ref 33 and using pKa2 = 4.27 for the oxalic acid. Hence, estimated ΔGreac = ΔΔGreac - 36.3 kJ/mol. For the chloroaurate ions, we have used AuCl4- and AuCl3OHas representatives of the various chlorohydroxoaurate ions (AuClxOH4-x-) that may be present depending on the solution pH.33 Since the thermodynamic constant of the equilibrium between AuCl4- and AuCl3OH- is experimentally known,32 we have used the corresponding free energy to calculate ΔGreac for reactions involving AuCl3OHfrom those involving AuCl4-. According to the calculations the formation of the amino acid-Au complexes from AuCl4- is moderately thermodynamically favorable for ser (ΔGreac = -22 kJ/ mol), which may explain the observed ability of ser to promote the formation of protein-fiber bound metal nanoparticles.34 The formation of the tyr complex is moderately unfavorable (ΔGreac = 37 kJ/ mol). From the reaction free energies it could be concluded that ser favors the formation of gold-peptide complexes more than tyr (ΔΔG ≈ -60 kJ/mol). However, it is to be remarked that in the AuCl3-ser and AuCl3-tyr complexes the hydroxyl proton is expected to be more acidic than in the unbound amino acids due to the interaction with the Au center (strong Lewis acid).

Therefore, depending on pH, the deprotonated species (indicated by AuCl3-ser-O- and AuCl3-tyr-O- from now on) may be the dominant ones and need to be considered here. For them, we find a negative ΔGreac and, more importantly, that the deprotonated complex resulting from tyr is now more favored than those resulting from ser. This result highlights a possible mechanism through which the pH affects the relative behavior of different amino acids. Additionally the formation of complexes resulting from AuCl3OH- have reaction free energies less favorable than the complexes formed from the AuCl4- ion. We have to remark, however, that the equilibria involving AuCl3OH- and tyr/ser are pH dependent, as OH- appears among products. Although we are not aware of experimental data on the equilibria in Scheme 1, a fast exchange of Au ligands with methionine in aqueous methanol was reported in ref 35. In the analysis on the structural characteristics the geometry obtained for the AuCl3-ser complex is characterized by a folded structure where a strong (OH 3 3 3 O) hydrogen bonding interaction occurs between the hydroxyl hydrogen of ser side chain with the carboxyl oxygen of the peptide backbone. In addition another (NH 3 3 3 O) hydrogen bonding interaction occurs between the NH of the peptide backbone and one of the carbonyl groups of the peptide backbone. Finally a weak interaction occurs between the NH of the peptide backbone and one chlorine atom (see Figure 1a, where interactions are presented with the dotted lines). On the other hand the geometry obtained for the AuCl3-tyr complex is characterized by an extended structure where no hydrogen bonding interactions are taking place, as the long and rigid side chain keeps the hydroxyl group and the backbone well separated. A discussion of the role of the backbone in determining ΔGreac is reported in the Supporting Information. There, in Figure S1 and Table S1, we also report the calculated vibrational spectra and the main geometrical parameters for all the discussed complexes, which may be useful for experimental studies of these reactions. The donation of electrons from the ligand to the Au center is a simple index of the ligand propensity to reduce gold. The charge distribution on the chloroaurate ions and the amino acid-Au(III) complexes is presented in Table 1 in terms of atomic charges obtained 1314

dx.doi.org/10.1021/nl1043924 |Nano Lett. 2011, 11, 1313–1318

Nano Letters

LETTER

Figure 1. Representation of the atomic charges calculated from natural bond orbital (NBO) analysis for AuCl3-ser and AuCl3-tyr complexes in the neutral (a) and in the anion (b) state. The color of the atoms refers to the charge sign (blue = negative, red = positive) while the size of the atom is proportional to the charge magnitude. An isosurface of the differential electron density between the neutral and the anion state is reported in column c (blue = decreased density, red = increased density).

Table 1. Sum of the NBO Atomic Charges for the Ligand in the Studied Chloroaurate(III) Complexes, And Ligand Charge Donation to the AuCl3 Moietya complex

ligand

ligand charge (e) ligand charge donation (e)

-

-0.479

AuCl3OH-

OH-

-0.472

-0.528

AuCl3-ser AuCl3-tyr

ser tyr

0.289 0.332

-0.289 -0.332

AuCl3OHCH3

CH3OH

0.227

-0.227

AuCl3Cl

-

Cl

-0.521

0.286

-0.286

AuCl3-ser-O- ser-O-

-0.445

-0.556

AuCl3-tyr-O- tyr-O-

-0.302

-0.697

AuCl3OCH3

CH3O-

-0.420

-0.580

AuCl3OPhCH3

CH3PhO-

-0.264

-0.736

AuCl3OHPhCH3 CH3PhOH

a

The trends emerging from this table do not depend on the details of the population analysis, as another approach (Mulliken) provides the same qualitative picture (see Table S2 in the Supporting Information).

from natural bond orbital (NBO) analysis36 summed on chemical groups (the individual atomic charges are presented in Tables S3 and S4 in the Supporting Information). The total charges of the ligands in the AuCl3-ser and AuCl3-tyr complexes indicate that a charge transfer process takes place from the side chains of the peptides to the gold atom. The comparison among the charge donation from OH- (-0.528 e) and Cl- (-0.521 e) and that from ser (-0.289 e) and tyr (-0.332 e) shows that once gold has been bound to the amino acid it is in a similar charge state as in the precursors (i.e., no direct reduction takes place). (e is the absolute value of the electron

charge.) The picture changes remarkably when we consider the deprotonated form AuCl3-ser-O- and AuCl3-tyr-O-. For AuCl3-ser-O-, the charge donation increases to -0.556 e, which is however still comparable to the donation in the gold precursors. For AuCl3-tyr-O- the donation reaches -0.697 e, and when only the side chain is considered, donation is -0.736 e. This hints at the tendency of tyr to reduce Au. To investigate this tendency further, we have considered an electronic state of AuCl3-tyr-O- where the intramolecular reduction of gold from Au(III) to Au(II) (and the concurrent oxidation of tyr) can take place. The expected final electronic state for such reduction would be a diradical, having one unpaired electron on Au (as Au(II) has a d9 configuration) and one unpaired electron on tyr. We have therefore performed unrestricted DFT calculations for the lowest energy state with two excess spin R electrons of AuCl3-tyr-O-. An isosurface of the resulting spin density is plotted in Figure 2. It is apparent from there that the unpaired electrons are localized on the AuCl3 moiety (occupying the dx2-y2 orbital as expected by ligand-field theory for a d9 complex, hybridized with ligand orbitals) and on the π cloud of tyr (in particular, on the phenol oxygen and the ortho and para phenyl C atoms, as expected for a tyr radical). The NBO population analysis assigns approximately one unpaired electron to AuCl3 and one to tyr, confirming the diradical nature of this electronic state. To be relevant for the reduction mechanism, this Au(II) state should be within a few kT from the ground state of AuCl3-tyrO-. Our calculations show that it is indeed only 12 kJ/mol (∼5 kT at room temperature) less stable than the ground state, confirming that this state may be reasonably populated at room temperature. 1315

dx.doi.org/10.1021/nl1043924 |Nano Lett. 2011, 11, 1313–1318

Nano Letters

LETTER

Figure 2. Spin density (FR-Fβ) isosurface for the lowest triplet state of the deprotonated form of AuCl3-tyr complex. The spin density is localized on the AuCl3 moiety, on the phenol oxygen, and in the ortho and para sites on the phenol ring of tyr.

Table 2. Adiabatic Electron Affinities Computed for the Studied Chloroaurate(III) Complexes complex

electron affinity (eV)

AuCl4-

4.93

AuCl3OH-

4.39

AuCl3-ser

5.14

AuCl3-tyr

5.40

AuCl3OHCH3

5.36

AuCl3OHPhCH3

5.35

AuCl3-ser-OAuCl3-tyr-O-

4.24 4.36

AuCl3OCH3-

4.27

AuCl3OPhCH3-

4.36

The resulting tyr radical may then follow a typical reaction pathway leading to the formation of dityrosine by cross-linking to another tyr molecule,37 e.g., from the same peptide or by encountering another tyr. This reaction would be hindered by the presence of amino acids with bulky side chain close to tyr, as they would screen it from the interaction with other tyr. Such scenario could explain the experimental observation that while tyr molecules are effective in reducing chloroaurate precursor, this is no longer the case for heptapeptides with interdigitated tyr and the bulky tryptophan. In fact, even if the tyr can bind to gold and a tyr radical may be created, the latter is a dead end for reduction: it is able neither to meet another tyr molecule (due to the steric hindrance of tryptophan) nor to oxidize the tryptophan itself.38 On the contrary, peptides containing multiple tyr may be more effective than single tyr amino acids as the incoming tyr is already in situ (and, thermodynamically, the entropic cost of fixing another molecule would be saved). Interestingly, if the tyr molecules that cross-link are all bonded to Au (which is favored as they would be both “activated” for this process), a high local concentration of Au ions is obtained, which may become a nucleus for nanoparticle growth (Au(II) is even able to form

dinuclear complexes).24 Possible Coulombic repulsion between the encountering negative AuCl3-tyr-O- complexes may be relieved if a Cl- ion is spontaneously detaching from the Au(II) species, as proposed for AuCl42-.39 Finally, to investigate the different propensities of the Au(III) complexes to be reduced to Au(II), we calculated their electron affinities (EAs). The higher the EA, the easier the reduction is expected to be, as found, e.g., for Pt-DNA adducts.40 Table 2 presents the adiabatic EA of the AuCl4- and AuCl3OHions and the corresponding AuCl3-ser and AuCl3-tyr complexes in the neutral and in their deprotonated form. The computed EA for the substituted aurate complexes are higher than those for the AuCl4and AuCl3OH- ions, showing that complexation via these amino acids is facilitating the reduction. For amino acids with stronger interactions with gold, the opposite effect was previously suggested.14 The EA of AuCl3-ser and AuCl3-tyr is much higher than that for AuCl3OH- (0.75 eV for ser and 1.01 eV for tyr) and also higher than that for AuCl4- (0.21 eV for ser and 0.47 eV for tyr). Remarkably, tyr is increasing the EA ∼0.25 eV more than ser, which may also contribute to the better performance of tyr as a gold reducing agent. The comparison with the EA results for aurate complexes containing only amino acid side chains shows that the presence of the backbone does not affect tyr behavior, while it is decreasing the EA for ser. In fact, the backbone replaces solvating water molecules which may stabilize the reduced species. Similar effects may be at work between neighbor side chains in peptides and may also contribute to give origin to the complex nonlinear reduction behaviors of peptides with mixed sequences noted in ref 14. The deprotonated amino acid-aurate complexes present, as we discussed above, a charge distribution closer to a reduced Au center than the protonated forms. Therefore, the addition of an extra electron is expected to be less favorable than for the protonated complexes. This is indeed the case, as EA become comparable to that of AuCl3OH- and smaller than for AuCl4-. To monitor and interpret the changes in the molecular electronic density upon reduction of the chloroaurate complexes, we have calculated the difference of the electron density between the original state and that with an added electron. Figure 1 refers to Au-ser and Au-tyr complexes. Similar pictures for (i) AuCl4- and AuCl3OH-; (ii) the complex with the side chains (in the protonated and deprotonated form); and (iii) the AuCl3-ser-O- and AuCl3tyr-O- complexes are depicted in Figures S2, S3, and S4 of the Supporting Information, respectively. From Figure 1a,b (and Figures S2-S4a,b, Supporting Information), a noticeable depletion of the atomic charges (i.e., an increase of electron density) of the gold and chlorine atoms upon reduction is seen (the gold atom becomes less positive and chlorine atoms become more negative), while the differences of the atomic charges of the other atoms in Figure 1 (C, N, O, and H) are relatively indistinguishable. This suggests that the extra electron is indeed localized on the gold region, although mainly delocalized on Cl ligands. The electron density in the amino acid is also changing (Figure.1c), which can be interpreted as a polarization of the electron density in response to the added electron. An analysis of the numerical values of the variation of the atomic charge (Table 3) backs-up the finding that electron is indeed mainly localized on the gold region. In fact, from Table 3 it is noticeable that the change of the sum of the atomic charges of gold and chlorine atoms upon adding an electron (Δq) is relatively large and similar for the gold precursors and the Au(III) complexes (ranging between -0.75 e to -0.89 e) which confirms that the added electron is distributing in the gold atom region. A notable exception to this trend is AuCl3-tyr-O- (and AuCl3OPhCH3-), for which Δq is 1316

dx.doi.org/10.1021/nl1043924 |Nano Lett. 2011, 11, 1313–1318

Nano Letters

LETTER

Table 3. Sum of the NBO Atomic Charges of the Gold and Chorine Atoms in the (formally) Au(III) State q[AuCl3](III) and in the Au(II) State q[AuCl3](II) and Their Difference Δqa atomic charges (e) complex -

q[AuCl3](III)

q[AuCl3](II)

Δq -0.797

figures with atomic charges and electron density difference for choloroaurate ions and for side chains and deprotonated choloroaurate complexes, figure with calculated vibrational spectra of the studied chloraurate complexes, tables with individual atomic charges calculated by NBO analysis, table with main geometrical parameters of calculated chloroaurate structures, and analogues of Tables 1 and 3 with atomic charge values calculated by the Mulliken population analysis. This material is available free of charge via the Internet at http://pubs.acs.org.

-0.521

-1.318

AuCl3OH-

-0.528

-1.330

-0.801

AuCl3-ser

-0.289

-1.146

-0.856

AuCl3-tyr

-0.332

-1.102

-0.770

’ AUTHOR INFORMATION

AuCl3OHCH3 AuCl3OHPhCH3

-0.227 -0.287

-1.116 -1.095

-0.889 -0.810

Corresponding Author

AuCl3-ser-O-

-0.555

-1.306

-0.751

AuCl3-tyr-O-

-0.697

-1.286

-0.589

AuCl3OCH3-

-0.580

-1.341

-0.762

AuCl3OPhCH3-

-0.736

-1.297

-0.560

AuCl3Cl

a

Individual atomic charges are reported in Tables S3 and S4 (Supporting Information). The trends emerging from this table do not depend on the details of the population analysis, as another approach (Mulliken, see Table S5 (Supporting Information) provides the same qualitative picture.

only -0.59 e. This is again in line with a picture where the deprotonated tyr is close to an oxidized form and can therefore compete with gold for the incoming electron. In conclusion the reduction of chloroaurate(III) ions in the presence of the amino acids ser and tyr has been described by means of first principle calculations. These hydroxyl amino acids have been found to be able to compete with the Cl- ligands from the chloroaurate ion AuCl4-, as the estimated reaction free energies of the resulting Au(III)-amino acid complexes are moderately negative (for AuCl3-ser, AuCl3-ser-O- and AuCl3-tyr-O-) or moderately positive (AuCl3-tyr) in aqueous solution. Depending on the pH, tyr may show a more favorable complex formation free energy that ser. Furthermore, the formation of the complexes was shown to promote further reduction of gold, as revealed by the increase of the electron affinity for both amino acids (again, higher for tyr). In the case of the deprotonated AuCl3-tyr complex, an incipient intramolecular reduction was inferred from the electronic distribution result, and the product of such intramolecular redox reaction (a Au(II)-tyr 3 diradical) was found to be a few kT less stable than the Au(III) complex. A pathway to conclude such a reaction, possibly leading to a local nucleus of gold atoms, has been proposed on the basis of the known biochemistry of tyr. The results of calculations on the AuCl3-tyr complexes provided a possible explanation for the behavior of tyr-intercalated peptides.14 Of course, many other intriguing aspects of the peptide synthesis of gold nanoparticles, such as the capability of favoring particular shapes, are likely related to steps following those we have studied here. Nevertheless, the present work provides a chemical rationale to different nontrivial experimental findings at the basis of design rules for gold-nanoparticle-forming peptides,14 and it is also relevant for understanding the general mechanisms underlying the formation of gold nanoparticles via reduction of chloroaurate precursors by organic molecules.1

’ ASSOCIATED CONTENT

bS

Supporting Information. Details on methods, analogues of Scheme 1 for side-chain complexes, and related discussion,

*E-mail: [email protected].

’ ACKNOWLEDGMENT The authors gratefully acknowledge funding from the Italian Institute of Technology (IIT) under the Seed project “MOPROSURF” and the MIUR under the FIRB Italnanonet. ’ REFERENCES (1) (a) Ozin, G. A. Adv. Mater. 1992, 4, 612. (b) Daniel, M. C.; Astruc, D. Chem. Rev. 2004, 104, 293. (c) Xia, Y.; Xiong, Y. J.; Lim, B.; Skrabalak, S. E. Angew. Chem., Int. Ed. 2009, 48, 60. (d) Huang, X. H.; Neretina, S.; El-Sayed, M. A. Adv. Mater. 2009, 21, 4880. (2) Andres, R. P.; Bein, T.; Dorogi, M.; Feng, S.; Henderson, J. I.; Kubiak, C. P. W.; Mahoney, R. G.; Osifchin, R. G.; Reifenberger, R. Science 1996, 272, 1323. (3) Galletto, P.; Brevet, P. F.; Girauit, H. H.; Antoine, R.; Broyer, M. J. Phys. Chem. B 1999, 103, 8706. (4) Mirkin, C. A.; Letsinger, R. L.; Mucic, R. C.; Storhoff, J. J. Nature (London) 1996, 382, 607. (5) Anker, J. N.; Hall, W. P.; Lyandres, O.; Shah, N. C.; Zhao, J.; Van Duyne, R. P. Nat. Mater. 2008, 7, 442. (6) Murphy, C. J.; Gole, A. M.; Hunyadi, S. E.; Stone, J. W.; Sisco, P. N.; Alkilany, A.; Kinard, B. E.; Hankins, P. Chem. Commun. 2006, 544. (7) Thaxton, C. S.; Georganopoulou, D. G.; Mirkin, C. A. Clin. Chim. Acta 2006, 363, 120. (8) Sapulveda, B.; Angelome, P. C.; Lechuga, L. M.; Liz-Marzan, L. M. Nano Today 2009, 4, 244. (9) Hu, M. C. J.; Zhi-Yuan, L.; Leslie, A.; Hartland, G. V.; Li, X.; Marquez, M.; Xia, Y. Chem. Soc. Rev. 2006, 35, 1084. (10) Ghosha, P.; Hana, G.; Dea, M.; Kima, C. K.; Rotello, V. Drug Delivery Rev. 2008, 60, 1307. (11) Rajesh, N. S.; Stringer, J. S.; Agarwal, G.; Jones, S. E.; Stone, M. O. Nat. Mater. 2002, 1, 169. (12) (a) Crookes-Goodson, W. J.; Slocik, J. M.; Naik, R. R. Chem. Soc. Rev. 2008, 37, 2403. (b) Dickerson, M. B.; Sandhage, K. H.; Naik, R. R. Chem. Rev. 2008, 109, 4935. (13) Sarikaya, M.; Tamerler, C.; Jen, A. K. Y.; Schulten, K.; Baneyx, F. Nat. Mater. 2003, 2, 577. (14) Tan, Y. N.; Lee, J. Y.; Wang, D. I.C. J. Am. Chem. Soc. 2010, 132, 5677. (15) Vujacic, A. V.; Savic, J. Z.; Sovilj, S. P.; Szecsenyi, K. M.; Todorovic, N.; Petkovic, M.; Vasic, V. M. Polyhedron 2009, 28, 593. (16) Sen, P. K.; Gani, N.; Midya, J. K.; Pal, B. Transition Met. Chem. 2008, 33, 229. (17) Subramaniam, C.; Tom, R. T.; Pradeep, T. J. Nanopart. Res. 2005, 7, 209. (18) Mandal, S.; Selvkannan, P. R.; Phadtare, S.; Pasricha, R.; Sastry, M. Proc.—Indian Acad. Sci., Chem. Sci. 2002, 114, 513. (19) Kolev, Ts. K. B. B.; Zareva, S. Y.; Spiteller, M. Inorg. Chim. Acta 2006, 359, 4367. 1317

dx.doi.org/10.1021/nl1043924 |Nano Lett. 2011, 11, 1313–1318

Nano Letters

LETTER

(20) Selvakannan, P. R.; Mandal, S.; Phadtare, S.; Gole, A.; Paricha, R.; Adyanthaya, S. D.; Sastry, M. J. Colloid Interface Sci. 2004, 269, 97. (21) Shao, Y.; Jin, Y.; Dong, S. Chem. Commun. 2004, 1104. (22) Wangoo, N.; Bhasin, K. K.; Mehta, S. K.; Suri, C. R. J. Colloid Interface Sci. 2008, 323, 247. (23) (a) Pyykk€o, P. Angew. Chem., Int. Ed. 2004, 43, 4412. (b) Pyykk€o, P. Inorg. Chim. Acta 2005, 358, 4113. (c) Pyykk€o, P. Chem. Soc. Rev. 2008, 37, 1967. (24) Laguna, A.; Laguna, M. Coord. Chem. Rev. 1999, 193-195, 837. (25) Eustis, S.; Hsu, H.-Y.; El-Sayed, M. A. J. Phys. Chem. B 2005, 109, 4811. (26) Zhang, C.; Anderson, A.; Delisi, C. J. Mol. Biol. 1998, 281, 929. (27) Best, S. L.; Chattopadhyay, T. K.; Djuran, M. I.; Palmer, R. A. J. Chem. Soc., Dalton Trans. 1997, 2587. (28) Weiken, M.; Lippert, B.; Zangrando, E.; Randaccio, L. Inorg. Chem. 1992, 31, 1983. (29) Hay, P. J.; Wadt, W. R. J. Chem. Phys. 1985, 82, 299. (30) (a) Mennucci, B.; Cances, E.; Tomasi, J. J. Phys. Chem. B 1997, 101, 10506. (b) Cances, E.; Mennucci, B.; Tomasi, J. J. Chem. Phys. 1997, 107, 3032. (c) Tomasi, J; Mennucci, B.; Cammi, R. Chem. Rev. 2005, 105, 2999. (31) Frisch, M. J.; et al. GAUSSIAN 03 (Revision B.04); Gaussian, Inc.: Wallingford, CT, 2004. (32) Soni, V.; Sindal, R. S.; Mehrotra, R. J. Inorg. Chim. Acta 2007, 360, 3141. (33) (a) Peck, J. A.; Tait, C. D.; Swanson, B. I.; Brown, G. E., Jr. Geochim. Cosmochim. Acta 1991, 55, 671. (b) Vasic, V.; Premovic, M.;  akar, M.; Radak, B.; Milovanovic, G. J. Serb. Chem. Soc. 2000, 65, 345. C (c) Wang, S.; Qian, K.; Bi, X.; Huang, W. J. Phys. Chem. C 2009, 113, 6505. (34) Kasotakis, E.; Mossou, E.; Adle-Abramovich, L.; Mitchell, E. P.; Forsyth, V. T.; Gazit, E.; Mitraki, A. Pept. Sci. 2009, 92, 164. (35) Natile, G.; Bordignon, E.; Cattalini, L. Inorg. Chem. 1976, 15, 246. (36) Foster, J. P.; Weinhold, F. J. Am. Chem. Soc. 1980, 102, 7211. (37) Giulivi, C.; Traaseth, N. J.; Davies, K. J. A. Amino Acids 2003, 25, 227. (38) DeFilippis, M. R.; Murthy, C. P.; Faraggi, M.; Klapper, M. H. Biochemistry 1989, 28, 4847. (39) Barakat, K. A.; Cundari, T. R.; Raba^a, H.; Omary, M. A. J. Phys. Chem. B 2006, 110, 14645. (40) Mertig, M.; Colombi Ciacchi, L.; Seidel, R.; Pompe, W. Nano Lett. 2002, 2, 841.

1318

dx.doi.org/10.1021/nl1043924 |Nano Lett. 2011, 11, 1313–1318