Spectroscopic Evidences for Strong Hydrogen Bonds with

Letter pubs.acs.org/JPCL

Spectroscopic Evidences for Strong Hydrogen Bonds with Selenomethionine in Proteins V. Rao Mundlapati,†,‡ Dipak Kumar Sahoo,†,‡ Sanat Ghosh,§ Umesh Kumar Purame,‡,∥ Shubhant Pandey,‡,∥ Rudresh Acharya,‡,∥ Nitish Pal,†,‡,⊥ Prince Tiwari,†,‡,# and Himansu S. Biswal*,†,‡ †

School of Chemical Sciences, National Institute of Science Education and Research (NISER), PO- Bhimpur-Padanpur, Via-Jatni, District- Khurda, PIN - 752050, Bhubaneswar, India ‡ Homi Bhabha National Institute, Training School Complex, Anushakti Nagar, Mumbai 400094, India § Tata Institute of Fundamental Research, Homi Bhabha Road, Mumbai 400005, India ∥ School of Biological Sciences, National Institute of Science Education and Research (NISER), PO- Bhimpur-Padanpur, Via-Jatni, District- Khurda, PIN - 752050, Bhubaneswar, India S Supporting Information *

ABSTRACT: Careful protein structure analysis unravels many unknown and unappreciated noncovalent interactions that control protein structure; one such unrecognized interaction in protein is selenium centered hydrogen bonds (SeCHBs). We report, for the first time, SeCHBs involving the amide proton and selenium of selenomethionine (Mse), i.e., amide−N−H···Se Hbonds discerned in proteins. Using mass selective and conformer specific high resolution vibrational spectroscopy, gold standard quantum chemical calculations at CCSD(T), and indepth protein structure analysis, we establish that amide−N−H···Se and amide−N−H···Te Hbonds are as strong as conventional amide−NH···O and amide−NH···OC H-bonds despite smaller electronegativity of selenium and tellurium than oxygen. It is in fact, electronegativity, atomic charge, and polarizability of the H-bond acceptor atoms are at play in deciding the strength of H-bonds. The amide−N−H···Se and amide−N−H···Te H-bonds presented here are not only new additions to the ever expanding world of noncovalent interactions, but also are of central importance to design new force-fields for better biomolecular structure simulations.

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acceptor than S or O, which is in line with the aforementioned statement. However, many recent fundamental studies overrule the concept of electronegativity of H-bond acceptor in determining the H-bond strength.11,12 The 105 years old concept of H-bond becomes more elusive and interesting if one considers the H-bond ability of S in methionine and cysteine.13−15 Utilizing an arsenal of benchmark quantum chemical calculations and high-resolution laser spectroscopy techniques on simple molecular clusters16,17 to model peptides13,14 to proteins,15 Biswal and co-workers established that S can be a potential H-bond acceptor.11,12 In contrast to S,18 the potential of hydrogen bond formation by closely related third chalcogen Se in proteins has not yet been explored. In quest of a similar but chemically more stable Hbond system, the role of Se is inevitable due to its electronegativity close to but redox potential lower than that of sulfur. Se occurs in proteins and small peptides as selenocysteine19 (Sec) or selenomethionine (Mse), which are selenium analogues of cysteine (Cys) and methionine (Met), respectively, in which S is replaced by Se. They are functionally and structurally almost similar to their natural counterparts, and

he centennial of the discovery of hydrogen bond (HBond)1 in 2012 and the upcoming bicentennial of the discovery of selenium2,3 in 2017 remind us of two of the greatest discoveries in chemistry and their discoverers, British chemists T. S. Moore and T. F. Winmill1 and Swedish chemist J. J. Berzelius,3 respectively. Two recent articles (a) “100 years of the hydrogen bond” by Goymer4 and (b) “Why Nature Chose Selenium” by Reich and Hondal5 are fitting tributes to these notable occasions. The first one deals with one of the ubiquitous noncovalent interactions in nature and the later describes the unique properties of selenium that enabled the “Moon Metal” as Nature’s choice over sulfur. The special properties of selenium include lower basicity6 and higher nucleophilicity7 of selenate ions, better leaving group ability, higher polarizability, greater tolerance for hypervalence,8 enhanced stability and reversibility of selenyl radicals.9,10 However, one of the very important properties of Se, i.e., Hbonding with selenium, is belittled in the literature. For example, Reich and Hondal reported “in protic solvents the weaker hydrogen bond acceptor properties of selenolates vs thiolates contribute to higher nucleophilicity”.5 This statement is a common consensus: as one goes down a group in the periodic table, the electronegativity of the element decreases. It is expected that Se, being the third element of the group with electronegativity comparable to that of C, is a weaker H-bond © 2017 American Chemical Society

Received: December 13, 2016 Accepted: February 1, 2017 Published: February 1, 2017 794

DOI: 10.1021/acs.jpclett.6b02931 J. Phys. Chem. Lett. 2017, 8, 794−800

Letter

The Journal of Physical Chemistry Letters

Figure 1. Frequencies of amide−N−H···Se hydrogen bond donor−acceptor distances in selenomethionine (Mse) containing proteins with assigned hydrogen coordinates by REDUCE43,44 program. Values of the N−H···Se distance are from protein crystal structures. (a) Complete H-bond distance distribution; (b) distribution within the +0.2 Å of the sum of the van der Waal’s radii of H and Se (rH = 1.2 Å, rSe = 1.9 Å). Two representative examples of amide−N−H···Se hydrogen bond observed in (c) human inositol 1,4,5-trisphosphate 3-kinase (PDB: 1w2f, Resolution: 1.8 Å)35 and (d) phosphoethanolamine N-methyltransferase (PDB: 4krg, Resolution: 1.8 Å).36 The plots of the reduced density gradient (s) versus the sign of the second eigen value of the electron-density Hessian matrix (λ2) times electron density (sign(λ2)ρ) for (e) 1w2f and (f) 4krg with the bond critical point (BCP) of amide−N−H···Se hydrogen bond indicated.

exploration to assess the strength of amide−N−H···Se H-bonds in biomolecules. Our study intends to provide precise quantitative data to conceive and construe SeCHBs in proteins and other biomolecular systems. These studies not only enhance our basic understanding of the fundamental concepts, but also are helpful for IUPAC’s new definition and criteria of H-bonds as proposed by Arunan et al. to reconsider and redefine it.32 PDB Structure Analysis. The protein structure coordinates were retrieved from the RCSB31 Web site, which satisfied the following criteria: structure resolved by X-ray crystallography at less than 2.5 Å resolution, comprising of Se (Mse: selenomethionine) and with less than 30% sequence identity among the proteins. A histogram of NH···Se H-bond distance distribution was produced using 0.4 Å and 0.1 Å bar width for Figure 1a,b, respectively. Figure 1a shows a complete H-bond distance (dH···Se) distribution, while Figure 1b depicts the distribution within the +0.2 Å of the sum of the van der Waal’s radii of H and Se (rH = 1.2 Å, rSe = 1.9 Å).33,34 It is observed for many cases that the distances between Se and H are within the sum of the van der Waal’s radii, suggesting attractive

thus can be easily incorporated in protein during translation via Sec and Mse charged t-RNA; hence they are widely used as atoms of choice in solving protein crystal structure by experimental phasing methods.20 Se is documented as the best substituent for S in enzyme-catalyzed reactions, which is further evident by its stoichiometric presence in the active center of various enzymes,21 e.g., glutathione peroxidase, thioredoxin reductase, iodothyronine deiodinase, etc.22 Replacements of oxygen of the nucleotide nucleobases with selenium are also well documented in the literature.23−25 Se substitution on the nucleobase neither alters the structure nor the H-bonding network in the base pairs.26−28 In some cases it is mentioned that amide−N−H···Se H-bonds29,30 are weaker compared to amide−N−H···O H-bonds in nucleobase pairs. However, there are no concrete evidence/assessments on the strength of N−H···Se H-bond at the molecular level, which encouraged us to study such H-bonds more precisely. As discussed in the following sections, we have employed highresolution vibrational spectroscopy, gold standard quantum chemical calculations at the Coupled Cluster Doubles Triples (CCSD(T)) level, and Protein Data Bank (PDB)31 structure 795


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bond strength varies. The obvious reason is the conformational constraints of the amino acid residues and several noncovalent interactions at play that lead to an equilibrium N−H···Se Hbond geometry. Analyzing only PDB structures may not give exact information about H-bond ability of selenomethionine in proteins. We need to study those interactions in isolated conditions by eliminating conformational constraints and solvent effects. This could be achieved with the help of supersonic jet cooled molecular beam experiments where 1:1 H-bond donor−acceptor molecular complexes are studied very precisely and in quantitative manner. High-Resolution Laser Spectroscopy. Mass selected IR/UV double resonance spectroscopy was employed to extract spectroscopic signature of N−H···Se H-bond in an isolated environment. This technique has recently been elegantly used to get very precise spectroscopic information on the structure,47,48 bonding15,49−53 and dynamics54 of biomolecules and model molecular complexes. The quantitative information on N−H···Se H-bond strength can be obtained by monitoring the red shift in N−H stretching frequency. N-phenylacetamide (NPAA) and 2-pyridone (2PY) were chosen as cis and trans amide-NH H-bond donors, respectively. They also represent the trans and cis amide groups of peptides and nucleobases, respectively. Dimethylselenide (DMSe) and dimethylsufide (DMS), representing side chains of selenomethionine and methionine, respectively, were chosen as H-bond acceptors. The combination of above-mentioned H-bond donors and acceptors enabled us to compare N−H···Se and N−H···S Hbonds directly without the interventions of other noncovalent interactions or structural constraints or solvent effects. Figure 2 shows IR spectra of NPAA and 2PY monomer and their respective 1:1 H-bond complexes with DMSe and DMS obtained using resonant ion dip infrared (RIDIR) spectroscopy. The computational IR spectra calculated at RI-B97-D3/def2TZVPP level of theory were also included in the Figure 2 as stick diagrams. Detail computational method and scaling factor for computed IR frequencies have been explained in the Supporting Information. There is an excellent match between the experimental and computed IR spectra. Both experimental and computational data suggest that there are red shifts in N− H stretching frequencies (ΔνNH) in N−H···Se and N−H···S Hbond complexes with respect to those of their corresponding monomers. In case of NPAA (trans amide) the ΔνNH values for N−H···Se and N−H···S H-bond complexes are 91 and 96 cm−1, respectively, indicating thereby that H-bond strengths are of almost equal magnitude. On the other hand in the cis amide (2PY) the ΔνNH is 262 cm−1 for N−H···Se H-bond complex and 291 cm−1 for N−H···S H-bond complex, suggesting that N−H···Se H-bond is a little weaker compared to N−H···S Hbond. Nevertheless the substantial red shifts in both cis and trans amide−N−H···Se H-bond complexes confirm Se as a potential H-bond acceptors in proteins and nucleobases. This is also in excellent agreement with observations made from PDB structure analysis (vide supra). It should be noted that the cisamide−N−H···Se H-bonds are stronger than N−H···O Hbonds and N−H···π H-bonds are significantly weaker than both N−H···Se and N−H···S H-bonds.15 Although red shift in the N−H stretching frequencies can be used as spectroscopic markers for H-bonds, recently Scheiner55 reported that “... IR band shifts will occur even if the two groups experience weak or no attractive force, or if they are drawn in so close together that their interaction is heavily repulsive. The mere presence of a protonacceptor molecule can af fect the chemical shielding of a position

interactions between them. The natural bond orbital (NBO) analysis and atoms in molecules (AIM) electron density topology also confirm the aforementioned interactions are attractive, vide inf ra. We found in 2251 cases (∼52% of total interactions) the distances between Se and H are sign(λ2)ρ > −0.06)45,46 and even stronger than N−H···S H-bonds involving cysteine SH.18 In all the cases, the laplacians of the electron densities (∇2(p(r)) at the bond critical points are positive integers, suggesting that N−H···Se H-bonds are closed shell interactions. It is noteworthy to stress a point here that depending on the distance between H and Se and H-bond angle the N−H···Se H796


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H···S and N−H···O H-bond complexes. The binding energies can be as high as 50 kJ mol−1 in case of 2PY-DMSe complex. This energy is considerable higher and the N−H···Se H-bond strength is comparable with any classical H-bond energies as listed in the Table S1. Because of unavailability of dimethyltelluride (DMTe), we could not perform IR-UV spectroscopy of DMTe complexes. However, our experimental IR data on other complexes are very useful to predict the amide−N−H stretching frequencies of DMTe complexes. A linear correlation between the computed and experimental vibrational frequencies was established (Supporting Information Figure S3). Then we used the fitted linear equation νNH(expt) = 0.9868 × νNH(comp.) + 11 to estimate amide−N− H stretching frequencies of DMTe complexes. From data in Table S1, it can be seen that Tellurium is not far behind oxygen, sulfur, and selenium; the ΔνNH values of DMTe complexes are very similar to those of N−H···X complexes, suggesting that tellurium can be as strong a H-bond acceptor as oxygen, despite having almost the same electronegativity as hydrogen. We would like to emphasize that the electronegativity concept of atoms (H-bond acceptors) in explaining the strength of H-bonds almost retires here. The red shifts of N−H stretching frequencies are solely because of the interaction of X and N−H, which was further confirmed by two of the most frequently used H-bond descriptors. Figure 3a

Figure 2. Gas phase vibrational spectra of monomer (a) Nphenylacetamide (NPAA) and (d) 2-pyridone (2PY) and their Hbond complexes with (b,e) selenium and (c,f) sulfur acceptors in the N−H stretch region, obtained by IR-UV double resonance spectroscopy. Underneath the experimental spectra, DFT-D calculated stick spectra are presented for the sake of comparison and assignment.

occupied by a proton donor by virtue of its electron density, even if there is no H-bond present.” The aforementioned statement is a valid point and needs to be considered carefully while using red shift in vibrational frequencies as the spectroscopic ruler for Hbond strength. Hence, a detailed high level computational study is indispensable to justify our claim and corroborate the experimental observations that N−H···Se H-bonds are as strong as N−H···O and N−H···OC H-bonds. CCSD(T) Energetics and Theoretical Studies. To support and assess our experimental outcome, H-bond energies were estimated at very high level of theory, e.g., at the CCSD(T)/ aug-cc-pVDZ level. Experimental red shifts of N−H stretching frequencies suggest that Se with smaller electronegativity than O can form stronger H-bonds than O. The experimental outcome is surprising and encouraging to go a step further by considering tellurium (Te) (similar electronegative element as hydrogen) as an H-bond acceptor, thereby forming N−H···Te H-bonded complexes. In addition to NPAA and 2PY complexes the 1:1 complexes of N-methylformamaide (NMFA) were also included in the theoretical study. Unlike 2PY and NPAA, NMFA does not contain aromatic ring, hence void of secondary interaction such as C−H···X and C−H···π H-bonding. Hence, NMFA is the smallest and ideal amide to investigate amide− NH···X (X = O, S, Se, Te) H-bonds. The binding energies of N−H···Se H-bond complexes are comparable to those of N−

Figure 3. N−H···Se H-bond in the NMFA−DMSe complex as revealed by (a) overlap of p-type selenium lone pair and N−H σ* orbital. (b) colored isosurfaces of the reduced electron density gradient (3D-NCI-plot) (c) Linear correlation plot between donor−acceptor interaction energies (EDA) and red shift of N−H stretching frequencies (ΔνNH) with the geometric mean of atomic charges (q) and spherically averaged static square root of polarizability ( αavg ) of H-bond acceptor atoms.

and 3b show natural bond orbital (NBO) and NCI plots of NMFA-DMSe complex, respectively. In the NBO formalism, the donor−acceptor interaction energy (EDA) were calculated with a second order perturbative method. Here donor is the lone pair (lp) orbital of Se and acceptor is the antibonding sigma N−H orbital (σ*NH). EDA is in fact a good H-bond strength marker. Figure S4 shows a perfect linear correlation between EDA and ΔνNH. Now, we can safely conclude that ΔνNH can be used as a spectroscopic marker of the H-bond strength of the amide-NH···X complexes investigated in this work. We extend our theoretical studies on clinical-drug containing selenium to verify that Se in such drugs is able to form Hbonds. Our model system is a complex of the selenium analogue of captopril (SeCap, a drug used for the treatment of hypertension and congestive heart failure) and Angiotensin-I 797


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selenomethionine or substituting selenium in place of oxygen in nucleotides. Brief descriptions of experimental and computational methods are provided here, the detail can be found in the Supporting Information. The solid samples (H-bond donors: NPAA and 2-PY) are vaporized by thermal heating to 80−100 °C. About 0.2−0.5% premixture of H-bond acceptors (DMSe and DMS) in helium are used for the complex formation Both the H-bond donors and acceptors are entertained in supersonic jet expansion and cooled down to their zero point vibrational energy level. The supersonic-jet cooling (∼10−20 K) has many advantages. It reduces spectral congestion significantly that helps to identify and assign conformation-specific infrared spectra, in the form of well-separated narrow vibronic bands. During the pre-expansion H-bonded complexes are formed and skimmed prior to entering the ionization chamber of the linear time-of-flight spectrometer.16,17,60,61 The complexes are then studied using high-resolution IR and UV laser spectroscopy. UV excitation spectra are recorded with mass-selective resonant two-photon ionization (R2PI) spectroscopy while the singleconformation-specific IR spectra are obtained by IR/UV double resonance spectroscopy. The optimized structures of the monomers and H-bonded complexes are obtained at RI-B97D/def2-TZVPP level of theory. The IR spectra of the Hbonded complexes are also computed at the same level of theory. The scaled harmonic frequencies obtained from the calculations are helpful to assign experimental IR spectra to specific conformations. The H-bond energies are estimated at the CCSD(T)/aug-cc-pVDZ level of theory. The natural bond orbital (NBO) analysis38 provides the donor−acceptor pairwise interaction energies (EDA). The NBO-EDA energies are computed at MP2/aug-cc-pVDZ. The existences of H-bonds are further supported by noncovalent interaction (NCI) analyses40 using the wave functions of the optimized structures at MP2/aug-cc-pVDZ. The atomic charges and esp are calculated at the M06-2X/aug-cc-pVDZ level. Gaussian09,62 Turbomole 6.5,63 NCI-PLOT,40 and NBO-6.064 are employed to carry out all the computations.

Converting Enzyme (PDB ID: 2YDM, Figure S4). The NBO and NCI analysis infers that an N−H···Se H-bond exists between NH of histidine-387 and Se of SeCap. Electronegativity, Atomic Charge and Local Polarizability. The H-bond strength of NMFA-X complexes as observed from ΔνNH and EDA values follow the order N−H···S > N−H···Se > N−H···Te > N−H···O. On the other hand, the electronegativities of O, S, Se, and Te follow the order O (3.44) > S (2.58) > Se (2.55) > Te (2.1). One could see there is no correlation between the H-bond strengths and electronegativities of the H-bond acceptor atoms. Hence, it is no longer a rule that atoms with lower electronegativity will always form weak H-bonds. We have seen many exceptions in SCHB systems. To reason the fact, we calculated atomic charges (q) of the H-bond acceptor atoms by using electrostatic potential fitting method (CHarges from ELectrostatic Potentials using a Grid based method, CHELPG).56 The computed charges of O, S, Se, and Te are −0.3297, −0.2415, −0.2050, and −0.1532 au, respectively. These are exactly as the same order of their electronegativities; therefore atomic charges alone may not be sufficient to explain the observed H-bond strengths of the molecular complexes considered in this work. Going down the group in the periodic table not only the electropositive character of the elements enhances but also the atomic polarizability increases. Hence the possible contribution of polarizability of the H-bond acceptor atoms cannot be neglected or overlooked.17 We calculated spherically averaged static polarizability (αavg.) of O, S, Se, and Te in DME, DMS, DMSe, and DMTe, respectively using molecular polarizability partitioning method as described by Truhlar and coauthors.57 The αavg. values of O, S, Se, and Te in DME, DMS, DMSe, and DMTe are 3.48, 11.87, 14.60, and 20.42 au, respectively. Then the geometric mean of atomic charges and square root of polarizabilities of H-bond acceptors ( |q α | ) was considered as a possible H-bond descriptor. Figure 3c shows a linear correlation between |q α | and ΔνNH, and also between

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|q α | and EDA. In both the cases the correlation coefficient is more than 0.93. The linear correlation infers that not only the higher electronegativity or atomic charges of H-bond acceptor atoms are solely responsible for stronger H-bond formation but also polarizability plays a deciding role in determining H-bond strength. It is interestingly observed that |q α | of S is the highest and amide−N−H···S H-bonds are strongest among the others presented here, may be one of the reasons for which nature prefers methionine than its Se/Te/O counterpart. In conclusion, selenium centered hydrogen bonds (SeCHBs) observed in proteins as amide−N−H···Se H-bonds have been documented and analyzed by employing high resolution vibrational spectroscopy, bench mark quantum chemical calculations and PDB structure exploration. Both experimental and computational data firmly suggest that amide−N−H···Se H-bonds are as strong as classical amide−N−H···O and amide−N−H···OC H-bonds. Like our earlier studies on SCHBs, we would like to emphasize in this work that SeCHBs invoke special attention and critical rethinking of the concept of electronegativity and polarizability in predicting H-bond strength. This molecular level study on SeCHBs is very useful for theoretical and physical chemists while proposing new force field for biomolecular structure simulations58,59 and for structural and molecular biologists in de novo designing proteins by replacing methionine and/or other residues with

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpclett.6b02931. Details of experimental and computational methods, Cartesian coordinates of the optimized structures, NBO and NCI-plots of the H-bond complexes (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]; Phone: +91-674-2494 186/185. ORCID

Himansu S. Biswal: 0000-0003-0791-2259 Present Addresses ⊥

(N.P.) Institute for Physical Chemistry II, Ruhr-University Bochum, 44780 Bochum, Germany # (P.T.) Department of Chemistry and Applied Biosciences, ETH Zurich, HCI D 325, CH-8093 Zurich, Switzerland Author Contributions

H.S.B. conceived the project and planned the experiments. H.S.B., V.R.M., and S.G. performed the experiments. H.S.B., D.K.S., N.P., and P.T. did the computation. U.K.P., S.P., R.A., 798


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(17) Biswal, H. S.; Wategaonkar, S. Nature of the N-H•••S Hydrogen Bond. J. Phys. Chem. A 2009, 113, 12763−12773. (18) Van Bergen, L. A. H.; Alonso, M.; Palló, A.; Nilsson, L.; De Proft, F.; Messens, J. Revisiting Sulfur H-bonds in Proteins: The Example of Peroxiredoxin AhpE. Sci. Rep. 2016, 6, 30369. (19) Atkins, J. F.; Gesteland, R. F. The Twenty-First Amino acid. Nature 2000, 407, 463−465. (20) Hendrickson, W. A.; Horton, J. R.; LeMaster, D. M. Selenomethionyl Proteins Produced for Analysis by Multiwavelength Anomalous Diffraction (MAD): A Vehicle for Direct Determination of Three Dimensional Structure. EMBO J. 1990, 9, 1665−16672. (21) Moroder, L. Isosteric Replacement of Sulfur with Other Chalcogens in Peptides and Proteins. J. Pept. Sci. 2005, 11, 187−214. (22) Iwaoka, M.; Arai, K. From Sulfur to Selenium. A New Research Arena in Chemical Biology and Biological Chemistry. Curr. Opin. Chem. Biol. 2013, 7, 2−24. (23) Carrasco, N.; Buzin, Y.; Tyson, E.; Halpert, E.; Huang, Z. Selenium Derivatization and Crystallization of DNA and RNA Oligonucleotides for X-ray Crystallography using Multiple Anomalous Dispersion. Nucleic Acids Res. 2004, 32, 1638−1646. (24) Höbartner, C.; Rieder, R.; Kreutz, C.; Puffer, B.; Lang, K.; Polonskaia, A.; Serganov, A.; Micura, R. Syntheses of RNAs with up to 100 Nucleotides Containing Site-Specific 2′-Methylseleno Labels for Use in X-ray Crystallography. J. Am. Chem. Soc. 2005, 127, 12035− 12045. (25) Wang, L.; Xie, J.; Schultz, P. G. Expanding the Genetic Code. Annu. Rev. Biophys. Biomol. Struct. 2006, 35, 225−249. (26) Salon, J.; Sheng, J.; Jiang, J.; Chen, G.; Caton-Williams, J.; Huang, Z. Oxygen Replacement with Selenium at the Thymidine 4position for the Se Base Pairing and Crystal Structure Studies. J. Am. Chem. Soc. 2007, 129, 4862−4863. (27) Salon, J.; Jiang, J.; Sheng, J.; Gerlits, O. O.; Huang, Z. Derivatization of DNAs with Selenium at 6-position of Guanine for Function and Crystal Structure Studies. Nucleic Acids Res. 2008, 36, 7009−7018. (28) Sheng, J.; Zhang, W.; Hassan, A. E. A.; Gan, J.; Soares, A. S.; Geng, S.; Ren, Y.; Huang, Z. Hydrogen Bond Formation between the Naturally Modified Nucleobase and Phosphate Backbone. Nucleic Acids Res. 2012, 40, 8111−8118. (29) Hassan, A. E. A.; Sheng, J.; Zhang, W.; Huang, Z. High Fidelity of Base Pairing by 2-Selenothymidine in DNA. J. Am. Chem. Soc. 2010, 132, 2120−2121. (30) Sheng, J.; Gan, J.; Soares, A. S.; Salon, J.; Huang, Z. Structural Insights of Non-Canonical U•U Pair and Hoogsteen Interaction Probed with Se Atom. Nucleic Acids Res. 2013, 41, 10476−10487. (31) Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissig, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank. Nucleic Acids Res. 2000, 28, 235−242. (32) Arunan, E.; Desiraju, G. R.; Klein, R. A.; Sadlej, J.; Scheiner, S.; Alkorta, I.; Clary, D. C.; Crabtree, R. H.; Dannenberg, J. J.; Hobza, P.; et al. Defining the Hydrogen Bond: An Account (IUPAC Technical Report). Pure Appl. Chem. 2011, 83, 1619−1636. (33) Bondi, A. Van der Waals Volumes and Radii. J. Phys. Chem. 1964, 68, 441−451. (34) Rowland, R. S.; Taylor, R. Intermolecular Nonbonded Contact Distances in organic Crystal Structures: Comparison with Distances Expected from Van der Waals Radii. J. Phys. Chem. 1996, 100, 7384− 7391. (35) González, B.; Schell, M. J.; Letcher, A. J.; Veprintsev, D. B.; Irvine, R. F.; Williams, R. L. Structure of a Human Inositol 1,4,5Trisphosphate 3-Kinase: Substrate Binding Reveals Why It is Not A Phosphoinositide 3-Kinase. Mol. Cell 2004, 15, 689−701. (36) Lee, S. G.; Jez, J. M. Evolution of Structure and Mechanistic Divergence in Di-Domain Methyltransferases from Nematode Phosphocholine Biosynthesis. Structure 2013, 21, 1778−1787. (37) Reed, A. E.; Curtiss, L. A.; Weinhold, F. Intermolecular Interactions from a Natural Bond Orbital, Donor-Acceptor Viewpoint. Chem. Rev. 1988, 88, 899−926.

and H.S.B. carried out the protein structure analysis using the code written by R.A. H.S.B analyzed the data and wrote the manuscript. All the authors discussed the results and made comments on the manuscript. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The work is dedicated to the bicentennial of the discovery of selenium and Professor Sanjay Wategaonkar on the occasion of his 60th birthday. The authors thank Prof. A. C. Dash and Dr. Aditi Bhattacherjee for the stimulating discussion. The authors also thank Dr. Pranay Swain for careful reading of the manuscript. H.S.B. acknowledges financial support from Department of Science and Technology (DST), India (Grant No: IFA11-CH-01).

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NOTE ADDED AFTER ASAP PUBLICATION This paper was published ASAP on February 2, 2017. Figure 3 was revised and minor updates were made throughout the article text. The revised paper was reposted on February 7, 2017.

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Spectroscopic Evidences for Strong Hydrogen Bonds with

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