Structure and Dynamics of L-Selenomethionine in the Solid State

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J. Phys. Chem. B 2006, 110, 25692-25701

Structure and Dynamics of L-Selenomethionine in the Solid State Jaroslaw Gajda,† Justyna Pacholczyk,† Anna Bujacz,‡ Elz3 bieta Bartoszak-Adamska,§ Grzegorz Bujacz,‡ Wlodzimierz Ciesielski,† and Marek J. Potrzebowski*,† Centre of Molecular and Macromolecular Studies, Polish Academy of Sciences, Sienkiewicza 112, 90-363 Ło´ dz´, Poland, Institute of Technical Biochemistry, Technical UniVersity of Ło´ dz´, Stefanowskiego 4/10, 90-924 Ło´ dz´, Poland, Department of Chemistry, Adam Mickiewicz UniVersity, Grunwaldzka 6, 60-780 Poznan´ , Poland ReceiVed: May 30, 2006; In Final Form: September 29, 2006

L-selenomethionine 1 crystallizes in P21 space group with two molecules in the asymmetric unit. Solid-state NMR spectroscopy is used for searching of structure and dynamics of 1 in the crystal lattice. The distinct molecular motion of side chains for A and B molecules of 1 is apparent from measurements of relaxation parameters (1H Τ1F, 13C T1) and analysis of CSA data (2D-PASS experiment). The 13C δii and 77Se δii parameters are correlated with theoretical shielding parameters obtained by means DFT GIAO calculations. Attempt to explain the mechanism of phase transition of crystals of 1 at 313K is presented.

Introduction Selenium is an important trace element involved in a number of metabolic processes of living organisms.1 It forms the active center for seleno-enzymes that carry out redox reactions such as glutathione peroxidase, thioredoxin reductase, thyroid hormone deiodinase, etc.2 Selenium is present in proteins in the form of either selenocysteine (SeCys) or selenomethionine (SeMet).3 The significance of SeCys in metabolic process, as well as methods of selenium supplementation and its role as potential therapeutic and chemopreventive agent were recently discussed.4 L-SeMet is an isosteric analogue of L-Met (methionine) and its abundance in living organism depends on the availability of dietary selenium as an essential element of nutrition.5 An important issue is the SeMet/Met ratio in food products. SeMet does not have a specific codon and is usually incorporated into proteins by the same AUG codon as Met.6 SeMet mimics almost all the functions of methionine and, therefore, is randomly incorporated into proteins due to the editing tolerance of methionyl-tRNA synthetase. Attention was paid to structural studies of L-SeMet in different environments.7 A number of experimental techniques were employed to study the structure and molecular dynamics in the liquid phase.8 The X-ray crystallography is the best diagnostic technique, which provides direct information about molecular geometry and important intra- and intermolecular interactions in the solid state. It is rather surprising that, so far, no X-ray structure of L-SeMet has been reported despite the fact that selenomethionyl proteins now account for about twothirds of all new protein crystal structures phased by multiwavelength anomalous diffraction (MAD).9 In this work, we present the first crystal structure of L-selenomethionine 1 determined by X-ray diffraction experiment at low temperature (130 K). The cryo-cooling of crystals has now become standard procedure in crystallography of biological samples.10 However, there is a risk that structures determined at low temperature may * Corresponding author phone: +48 42 680 3240; fax: +48 42 680 3261; e-mail: [email protected]. † Polish Academy of Sciences. ‡ Technical University of Ło ´ dz´. § Adam Mickiewicz University.

suggest conclusions based on aspects of the structure that not necessarily relevant at room temperature.11 Hence the knowledge about room-temperature structures obtained from X-ray data collection or employing other complementary techniques dedicated to search of solid phase is still desirable. In this report we present a systematic study of the thermal processes in L-SeMet crystals using differential scanning calorimetry (DSC) and variable temperature (VT) solid-state NMR techniques. These results are correlated with X-ray diffraction data collected at 130 K. Experimental Section X-ray Analysis. A plate crystal with the dimensions 0.03 × 0.4 × 0.6 mm was used for X-ray measurements. The intensities were collected at 130 K using a KM4-CCD diffractometer43 equipped with an Oxford low-temperature device44 and graphitemonochromated Mo KR radiation. We collected 1062 ω scans in four orientations of the crystal with 0.75° intervals. The integrated intensities and direction cosines were obtained using CrysAlis program.45 The data set consisted of 4460 observations, which were reduced in the 2/m Laue group to 2683 unique data (redundancy 2.7). Numerical absorption correction was used to reduce the absorption effect. Rint after absorption correction is 9.0% (before correction, 11.7%). Experimental details and crystal data are given in Table 1. The structure was solved by direct methods using SHELXS46 and refined by least-squares minimization of Σw(Fo2 - Fc2)2 for all reflections (SHELXL47). All hydrogen atoms were placed geometricaly and were refined as riding. For the terminal methyl and the ammonia groups, free rotation was allowed around the pivot bonds. Non-hydrogen atoms atoms were included in the refinement with anisotropic displacement parameters. The isotropic thermal parameters of the hydrogens were set to 1.3 of the corresponding isotropic equivalent of the parent atoms. The selected geometrical parameters are given in Table 2. Atomic displacement coordinates in CIF format are available as Electronic Supplementary Publication from the Cambridge Crystallographic Data Center (CCDC reference no. 298805). NMR Measurements. The solid-state CP MAS experiments were performed on a BRUKER Avance DSX 300 spectrometer

10.1021/jp063332k CCC: $33.50 © 2006 American Chemical Society Published on Web 12/01/2006

Structure and Dynamics of L-Selenomethionine at 75.47 MHz frequency for 13C equipped with a MAS probehead using 4-mm and 7-mm ZrO2 rotors. A sample of glycine was used for setting the Hartmann-Hahn condition and adamantane was used as a secondary chemical shift reference δ ) 38.48 and 29.46 ppm from external TMS.48 The conventional spectra were recorded with a proton 90 degree pulse length of 3.5 µs and a contact time of 1 ms. The repetition delay was 10 s and the spectral width was 25 kHz. The FIDs were accumulated with a time domain size of 2 K data points. The RAMP shape pulse49 was used during the cross-polarization and TPPM decoupling50 with τp ) 6.8 µs and a phase angle of 20° during the acquisition. The cross-polarization efficiency was measured with contact times between 10 µs and 12 ms. The spectra data were processed using the WIN-NMR program.51 13C T parameters were measured by means of Torchia sequence 1 and processed employing standard BRUKER software. 5-π pulse 2D-PASS scheme and 500 Hz sample spinning speed was used in the 2D experiments.17 π-pulse length was 6 µs. Sixteen t1 increments using the timings described by Levitt and co-workers were used in the 2D PASS experiments.17 Each increment accumulated 640 scans. Since the pulse positions in t1 set back to their original positions after a full cycle and the t1-FID forms a full echo, the 16-point experimental t1 data were replicated to 256 points. After the Fourier transformation in the direct dimension, the 2D spectrum was sheared so as to align all sidebands with the center bands in the indirect dimension of the 2D spectrum. One-dimensional CSA spinning sideband patterns was obtained from t1 slices taken at isotropic chemical shifts in the t2 dimension of the 2D spectrum. The magnitudes of the principal elements of the CSA tensor were obtained from the best-fitting simulated spinning sideband pattern. Simulations of the spinning CSA sidebands spectra were carried out on a PC using the SIMPSON program under the LINUX environment. Errors in δii parameters were estimated employing WINMAS program.51 Moreover, accuracy of fitted δii values was verified by comparison of experimental and simulated spectra recorded at very low spinning speed, 500 and 300 Hz. The fitted spectra and subspectra for each carbon atom are shown in the Supporting Information. 77Se 57.203 MHz spectra were recorded on BRUKER DSX 300 spectrometer equipped with MAS probe head using 4-mm ZrO2 rotors. Diamonium selenate was employed to setup of Hartman-Hahn condition. π/2 pulse was 4.0 µs, contact time 4 ms, spectral width 50 kHz and time domain 4 kHz. Two hundred scans were accumulated for each experiment. The 77Se chemical shifts were calibrated indirectly through ammonium selenate used as a secondary chemical shift reference standard, set at δ ) 1040.2 ppm (dimethyl selenide as primary reference, δ ) 0 ppm). DFT GIAO calculations were carried out with the GAUSSIAN 98 program running on a Silicon Graphics Power Challenge computer. The GIAO method with the B3PW91 hybrid method and 6-311++G** basis set was used to calculate NMR parameters. DSC measurements were carried out on TA instruments, 2920 Modulated DSC analyzer, with 1 deg/min heating rate in temperature range from 173 to 353 K.

J. Phys. Chem. B, Vol. 110, No. 51, 2006 25693 TABLE 1: Crystal Data and Structure Refinement for 1 structure 1 empirical formula formula weight temperature wavelength crystal system space group unit cell dimensions

volume Z calculated density absorption coefficient F(000) crystal size θ range for data collection limiting indices reflections collected/unique reflections observed F > 4σ(F) refinement method data/restraints/parameters goodness-of-fit on F2 (all data) final R indices [F > 4σ(F)] R indices (all data) largest diff. peak and hole

C5H11NO2Se 196.11 130(1)K 0.71073 Å monoclinic P21 a ) 9.5042(9) Å b ) 5.0999(7) Å c ) 15.6638(14) Å β ) 100.54(1)° 746.42(14) Å3 4 1.745 g/cm3 4.962 mm-1 392 0.6 × 0.4 × 0.03 mm 2.65 to 29.95° -12 e h e 13 -6 e k e 3 -20 e l e 21 7271/ 2683 [R(int) ) 0.0900] 2198 full-matrix least-squares on F2 2683/0/ 167 1.041 R1 ) 0.0554, wR2 ) 0.1462 R1 ) 0.0672, wR2 ) 0.1601 1.232 and -1.045 e. Å-3

of the carboxylate groups, the negative charge is almost evenly distributed between the two oxygen atoms. In both molecules, the C1-O1 distance is slightly longer then the C1-O2 distance. This can indicate that the C1-O1 bond has more of a single bond character and the negative charge is slightly shifted in the direction of the O1 atom (see Table 2). The conformation of the two molecules in the dimer is different. The carbonyl group in molecule A is almost coplanar with the plane of the main chain N1-C2-C1, which can be expressed by the torsion angle of O1A-C1A-C2A-N1A equal to -10.1(7)°. In molecule B, the carbonyl group is twisted with respect to the main chain and the corresponding torsion angle O1B-C1B-C2BN1B is equal to -40.5(7)°. The main conformational differences between molecules A and B are seen in the side chains. In molecule A, the torsion angles χ1 (N1-C2-C3-C4), χ2 (C2-C3-C4-Se), and χ3 (C3-C4-Se-C5) are -167.6, 161.7, and 61.2 respectively, whereas corresponding torsion angles in molecule B are -59.7, -66.7, and -76.9 degrees. The most frequent conformation of the methionine side chain in proteins corresponds to gauche χ1, anti-periplanar χ2, and gauche χ3.12 The conformation of the side chain of molecules A and B of 1 represents the second and third most common conformations of side chains for this residue. It is noteworthy that these conformations are slightly different compared to L-Met 2 (see Figure 3).13 The dimer of 1 is stabilized by strong hydrogen bond interactions between the negatively charged carboxylate groups

Results and Discussion X-ray Studies of L-Selenomethionine. Compound 1 crystallizes in the P21 space group (Table 1). The asymmetric unit comprises a “head-to-head” dimer. The A and B molecules in the dimer and the numbering system are presented in Figure 1. Crystal packing is shown in Figure 2. Both molecules in the dimer exist in the zwitterionic form. According to the geometry

Figure 1. ORTEP plot with atom numbering scheme for the L-SeMet dimer, with atom displacement ellipsoids drawn at the 50% probability level. Hydrogen atoms are represented by spheres of arbitrary radius. The hydrogen bonds responsible for dimer formation are marked by dashed lines.

25694 J. Phys. Chem. B, Vol. 110, No. 51, 2006

Figure 2. The crystal packing of compound 1. The hydrogen bonds at the polar interface are marked by dashed lines and the van der Waals contacts at the hydrophobic interface by doted lines. The bonds between molecules related by the y translation are not shown.

Gajda et al.

Figure 3. Overlapped structures of L-selenomethionine (dark) and L-methionine (light) taken from X-ray measurement at 120 K (refcode LMETON02, ref 13a).

and the positively charged ammonium groups. The intermolecular hydrogen bonds, which stabilize the dimer, have slightly different geometry and the difference is mainly reflected in the N-H-O angles. The dimer that makes up the asymmetric unit is located approximately on the shorter diagonal of the (010) face of the unit cell. The crystal packing shows layers parallel to (001), composed of molecules with similar orientation. Each layer possesses a hydrophilic and a hydrophobic side. Consecutive layers are related by 21 axes leading to alternating polar and hydrophobic interfaces. The main interactions at the TABLE 2: Selected Geometrical Parameters in the Crystal Structurea molecule A Bond Lengths (Å) 1.963(6) 1.939(11) 1.261(7) 1.248(8)

Se1 C4 Se1 C5 O1 C1 O2 C1 C4 Se1 C5 O1 C1 O2 Dihedral angles (deg) N1 C2 C1 O1 N1 C2 C3 C4 C2 C3 C4 Se1 C3 C4 Se1 C5

molecule B 1.953(7) 1.916(9) 1.264(7) 1.246(8)

Bond Angles (deg) 98.7(4) 125.8(6)

96.1(3) 125.9(6)

10.1(7) -167.6(5) 161.7(4) 61.2(5)

40.5(7) -59.7(7) -66.7(7) -76.9(5)

Dihedral Angles Between Least-Squares Planes (deg) N1 C2 C1/C1 O1 O2 11.2(4) 39.2(5) X-H‚‚‚Y N1A H11A O1B N1A H11A O2B N1A H12A O1B N1A H13A O2A N1B H11B O1A N1B H12B O1A N1B H12B O2A N1B H13B O2B

Dist. H-Y

Dist. X-Y

Hydrogen Bondsg 2.23(1) 2.845(7) 2.43(1) 3.074(7) 1.94(1) 2.735(6) 2.05(3) 2.846(7) 2.03(1) 2.792(7) 2.53(3) 3.059(7) 2.02(2) 2.805(6) 2.01(3) 2.808(7)

Angle(X-H‚‚‚Y) 134(2)b 138(2)c 174(2)d 175(3)c 160(3)b 125(3)e 168(3)e 173(3)c

van der Waals Contacts in Hydrophobic Interface h C3A H32A Se1B 3.03(1) 3.973(6) 165(1)e C5A H52A Se1B 3.26(3) 3.871(9) 124(3)e C3B H32B Se1A 3.10(1) 3.788(6) 130(1)d C5B H53B Se1A 3.08(4) 3.746(7) 128(3)f a Superscripts b-f denote symmetry operations: bxyz; cx,1+y,z; d1x,1/2+y,1-z; e2-x,1/2+y,1-z; f1+x,y,1+z. g NH- distance 0.80 Å. h CH- distance 0.96 Å

Figure 4. Variable temperature (183-313 K) spectra of L-selenomethionine.

13

C CP/MAS NMR

polar interface are hydrogen bonds. The interactions creating the dimer (v. supra) are located in the polar interface. Additional hydrogen bonds between the ammonium and carboxylate groups occur inside the same layer. The ammonium hydrogen H12A creates a hydrogen bond with carbonyl oxygen O1B. Due to the short b dimension of the unit cell, the next hydrogen bond H13A-O2A occurs between two molecules related by y translation. The hydrogen H12B forms a bifurcated hydrogen bond with two oxygens from the symmetry related molecule. The first strong one with O2A and the second, longer and weaker, with O1A. The third hydrogen H13B from the ammonia group interacts with the carboxyl oxygen O2B of the molecule related by y translation. The tight network of hydrogen bonds makes the polar interface rigid. The temperature factors are lower for the main chain atoms than for the side chain atoms, especially the terminal ones. A detailed description of the hydrogen bonds is presented in Table 2. In the hydrophobic interface, the interactions have the form of van der Waals contacts and the closest one occurs between

Structure and Dynamics of L-Selenomethionine the terminal methyl group and the selenium atom from molecules of neighboring layers. The terminal methylene group C5B remains in close contact with selenium Se1A and the methylene group from the other molecule creating dimer C5A interacts with the Se1B. Additionally, in the same layer the β methylene group C3B interacts with the selenium atom Se1A, while the β methylene group of molecule A (C3A) interacts with Se1B. There are a number of weaker interactions at the hydrophobic interface. The packing at this interface is less tight and the thermal vibrations of the atoms are larger. The internal structure of the crystals determines their morphology. The growth rate is much faster when extending a molecular layer in the x and y directions then in the z direction, requiring the creation of new layers. This leads to a thin, plate-like crystal. Molecular packing of 1 is similar to packing of L-Met, which also forms structures with alternating hydrophobic and hydrophilic layers.13 The hydrophobic layers contain the unpolar side chains, while the hydrophilic layers are composed of the charged carboxylate and amino groups. The latter layer consists of two identical sheets related by a 2-fold axis. 13C CP/MAS and 77Se CP/MAS Measurements-Analysis of Isotropic and Anisotropic Values. Preliminary high resolution solid-state NMR results for 1 have been reported elsewhere.14 The previously observed phase transition of 1 at 310 K is supported by the DSC results.15 Figure 4 shows the 13C CP/MAS spectra of 1 recorded in the temperature range 183313 K. The 13C signal labeling using standard notation for amino acids is shown on top of the spectrum. It is apparent from these data that two molecules of 1 in the crystal are not equivalent, as each signal is split. A challenging question is the assignment of the signals to the A and B molecules. This problem is solved by means of a theoretical approach (section 3) and analysis of intramolecular dynamics (section 4). At 183 K, the largest distinction in isotropic chemical shifts between A and B is seen for the R carbons (∆δ ) 5 ppm), slightly smaller for the β carbons (∆δ ) 3 ppm), and only 1 ppm for the γ carbons. The methyl groups (δ carbons) are also split (∆δ ) 1.5 ppm). With the increase of temperature, the ∆δ values decrease for the γ and δ carbons, while for the R and β they remain unchanged. Such result suggests that the carbon atoms of 1 are under different motional regime, with a relatively rigid backbone (C0 and CR carbons) and a mobile side chain (β, γ and δ carbons). At 253 K, coalescence of the γ and δ signals is observed, whereas the R and β are still split. The important information is the apparent change of the spectral pattern for the R and β carbons at 310 K. At 313 K, after the phase transition, single resonances for each carbon atom indicates that there is only one independent molecule in the unit cell. The 13C δii data for the carboxyl group of L-SeMet were published.14 It has to be stressed, that investigations of CST for the aliphatic signals is more demanding. At low spinning speed (Figure 5), the overlap between different spinning sidebands manifolds and analysis of the spectrum is ambiguous since the deconvolution procedure is equivocal. The separation of isotropic and anisotropic parts of the spectra with heavily overlapped systems is still a challenge for solidstate NMR spectroscopy. There are several approaches, which allow achieving this goal.16 In our project, we have employed the 2D-PASS sequence, which compared to other techniques, offers good sensitivity and does not require any hardware modifications or a special probe-head.17 Figure 6 shows the 2DPASS spectrum of 1, recorded at 278 K with the spinning rate

J. Phys. Chem. B, Vol. 110, No. 51, 2006 25695

Figure 5. 13C CP/MAS NMR spectrum of L-selenomethionine recorded at temperature 278 K with the spinning rate of 700 Hz.

Figure 6. 2D-PASS spectrum of L-selenomethionine recorded at temperature 278 K with the spinning rate of 500 Hz (a), and the expanded aliphatic part of the spectrum after data shearing (b).

of 500 Hz. By proper data shearing (Figure 6b) it is possible to separate the spinning sidebands for each carbon and calculate the 13C δii parameters. It is clear from such presentation that the F2 projection corresponds to a TOSS18 spectrum, while F1 represents CSA. The 13C shielding parameters are collected in Table 3. The experimental and the best-fitting simulated 1D spinning CSA sideband pattern for selected carbons of 1 are shown in Figure 7. It is clear that for β carbons, the Ω value expressed by the equation Ω ) (δ11 - δ33) is two times larger for molecule A than for B. It suggests a significant distinction of intramolecular dynamics of the side-chains. At higher temperature, above the


Gajda et al.

TABLE 3: Chemical Shift Tensors Parameters for L-selenomethionine Obtained from 2D-PASS Experiment and Estimated from Simulation Using Simpson Program; 13C: (a) 278 K (b) 313 K: 77Se (c)183 K (d) 297 Ka compound/temperature

δiso (ppm)

δ11 (ppm)

δ22 (ppm)

δ33 (ppm)

Ω (ppm)

κ

109.6 ( 1.5 106.7 ( 2.7 42.0 ( 1.0 35.4 ( 0.2 16.8 ( 2.5 25.4 ( 0.4 10.7 ( 0.3 -7.8 ( 0.9

131 135 28 33 40 21 22 29

-0.03 -0.04 -0.29 -0.11 0.14 0.27 0.03 0.15

T ) 278 K

C0 (B) C0 (A) CR (A) CR (B) Cβ (A) Cβ (B) Cγ Cδ

177.5 177.1 56.8 53.3 34.5 32.6 21.7 4.4

L-Selenomethionine 240.9 ( 1.5 182.1 ( 0.5 241.6 ( 2.7 182.9 ( 2.8 69.5 ( 1.0 58.6 ( 1.7 67.9 ( 0.2 56.6 ( 0.1 57.3 ( 2.5 29.3 ( 1.3 45.8 ( 0.4 26.7 ( 0.2 32.5 ( 0.3 21.9 ( 0.3 21.2 ( 0.9 0.3 ( 1.5

T ) 313 K

C0 CR (A) Cβ (A) Cγ Cδ

176.8 55.5 34.9 20.6 5.4

239.3 ( 1.8 67.5 ( 0.4 49.8 ( 0.4 27.1 ( 0.2 14.8 ( 0.4

181.4 ( 1.0 56.2 ( 0.3 35.8 ( 0.2 20.3 ( 2.1 4.5 ( 0.6

109.6 ( 1.8 42.8 ( 0.4 18.9 ( 0.4 14.2 ( 1.2 -3.0 ( 0.4

129 25 31 13 18

-0.03 -0.25 -0.04 0.05 0.02

T ) 183 K

Se (A) Se (B)

123.0 72.6

388 ( 12 339 ( 9

178 ( 10 154 ( 10

-197 ( 12 -276 ( 9

585 615

-0.09 -0.13

T ) 297 K

Se (A) Se (B)

122.9 84.3

384 ( 16 311 ( 8

181 ( 17 179 ( 11

-196 ( 16 -237 ( 8

580 548

-0.13 -0.17

T ) 298 K

C0 CR (A) CR (B) Cβ (A) Cβ (B) Cγ Cδ

177.1 56.7 52.3 32.5 31.4 17.8 15.8

L-Methionineb 244 ( 4 68 ( 2 66 ( 2 46 ( 1 42 ( 3 28 ( 2 29 ( 2

180 ( 3 55 ( 2 53 ( 2 33 ( 2 32 ( 2 19 ( 2 16 ( 2

107 ( 3 44 ( 2 39 ( 2 19 ( 2 20 ( 2 6(2 3(1

137 24 27 30 22 22 26

-0.07 0.03 0.68 0.03 0.05 0.01 0.02

a Data are taken from ref 14. b Data are taken from ref 19. Experimental and simulated 1D 13C CP MAS spectra of L-SeMet confirming accuracy of fitting, were recorded at spinning speed 500 Hz (278 K) and 300 Hz (313 K) and are attached as Supporting Information.

phase transition, the range of Ω is significantly reduced, which provides further confirmation that Ω is related to the molecular motion. It is noteworthy that for the β atom at 313 K the span of Ω has an average value comparable to that at 278 K. The presented 13C δii values were compared with data for free amino acids reported by Ye et al.19 Since in the cited paper there is no data for L-SeMet, we used 13C δii parameters of L-Met 2 as a reference. The 13C δii value for the carbon atoms of L-SeMet are roughly similar to those of L-Met, however some differences have to be noted. In particular, the 13C δii of the β atoms of the A and B molecules of 1 are different compared to 2. The CST parameters of the R and β carbons of amino acids, have recently received much attention since the knowledge of 13C δ values also provides information about the higher order ii structure of oligopeptides.20 From the present results it is clear that both conformation and dynamic processes have to be considered for oligopeptides containing L-SeMet. 77Se CP/MAS spectra of 1 at room temperature and at 313 K (above the phase transition) have been reported previously, and the principal components of the 77Se δii tensor have been established.14 In the present project, we have focused on low temperature measurements. Figure 8a shows the experimental 77Se CP/MAS spectrum recorded at 183 K with a spinning rate of 4 K in order to obtain sufficient spinning sideband pattern necessary for 77Se δii calculations. Figure 8b displays the spectrum calculated using the SIMPSON program.21 From the analysis of the data in Table 3, it is apparent that the shielding parameters of the 77Se nuclei are dependent on the temperature of measurement. At 183 K the Ω values are larger compared to those observed at 298 K. The difference is found to be ca 70 ppm for molecule B. A more spectacular narrowing of the 77Se line is observed at 313K, after the phase transition.14 The difference in span values is 200 ppm. This result proves that C3V rotation of the Se-Me group has a significant influence on the 77Se δii parameters.

Calculation of 13C and 77Se NMR Shielding Parameters. A number of methods are currently available for the computation of NMR parameters.22,23 The high reliability of the theoretical approach in relation to shielding elements of carbon-13 nucleus has been proved.24 In our work, the GIAO B3PW91 and B3LYP hybrid methods with the 6-311G** basis set were used for the calculation of the 13C parameters of 1 employing the Gaussian program.25 The low-temperature X-ray structure of 1 was taken as input. The calculations were carried out with a dimer. In general, the advantage of such an approach is related to the fact that it is possible to compare the theoretical and experimental results for molecules with exactly the same geometry of heavy atoms. The calculated values of the 13C shielding parameters are collected in Table 4. With the full set of 13C isotropic chemical shifts, we are in position to assign the 13C resonances to the carbons of the A and B molecules of the crystallographic asymmetric unit. Figure 9 shows the correlation between values of the shielding and chemical shift parameters. The obtained equation σii ) -0.983δii + 175 can be used to convert shielding to chemical shift elements. By comparing the theoretical values with those obtained from the 2D-PASS experiment, interesting conclusions regarding the molecular motion in the lattice can be drawn. First, the scatter of a few points representing β and γ carbons from linear regression is seen. Such an effect is often observed when dynamic processes strongly influence the CSA. Similar observation was recently reported in a paper published elsewhere.26 Second, the calculated span parameters Ω for the R carbons are very close to the experimental value. Furthermore, theoretical calculations predict significant distinction of Ω for the β carbons as function of C(0)-C(R)-C(β)-C(γ) torsion angle. For A and B molecules the appropriate torsion angles are 69.1° and 178.7°, respectively. For trans geometry (molecule B), the calculated Ω is two times smaller as compared to the gauche conformation.

Structure and Dynamics of L-Selenomethionine


Figure 7. Experimental (left) and best-fitting (right) simulated 1D spinning CSA sidebands patterns for individual carbon atoms.

A similar ratio of Ωtrans/Ωgauche is also seen for experimental values; however, the Ωexp are significantly smaller compared to Ωcalc. This distinction is caused by dynamic processes in the crystal lattice, which reduce the chemical shift anisotropy. This conclusion is also valid for the γ and δ carbons. For both atoms, the experimental span is much smaller compared to the theoretical values. Calculation of selenium NMR shielding parameters is still challenging for theoretical chemistry. Several authors have discussed this problem in detail.27 Recently Bayse has presented improved procedures which allows the calculation of reliable 77Se parameters for selenium proteins and selenomethionine.7,28 Shown in Table 4 are 77Se σii parameters for L-SeMet calculated with B3LYP functional and 6-311+G** basis set. Analysis of theoretical data reveals that the obtained results only roughly correspond to the experimental values. The difference between isotropic shielding values (∆σiso) for A and B molecules is 150

ppm while Ω are found to be 731 and 851 ppm, respectively. The appropriate 77Se chemical shift parameters at 297 K are ∆δiso ) 38.6 ppm and span 548 and 580 ppm. Variable temperature 77Se measurement shows that the dynamic processes have a significant influence on the CSA parameters. With decreasing temperature, the difference between77δiso values increases. A similar trend is observed for span values. Thus, we can conclude that unhindered rotation around Cγ-Se-Cδ bond reduces the CSA. This effect is clearly seen for molecule B. The measurements at very low temperature, much below 183 K, should further improve the consistency between theoretical calculations and measured values. The advantage of the theoretical approach is that, in contrast to the CP/MAS experiment, not only values but also the orientation of the principal elements of chemical shift tensors can be obtained. In this work, calculations were carried out for “frozen conformations” of A and B molecules of 1 with position


Gajda et al.

Figure 8. Experimental 77Se CP/MAS NMR spectrum of 1 recorded at 183 K with the spinning rate of 4 kHz (a) and the appropriate fitted spectrum obtained employing the SIMPSON program (b). Asterisks denote the isotropic lines.

TABLE 4: The Calculated Values of 77Se/13C Shielding Parameters Se/13C

σIso [ppm]

σ11 [ppm]

σ22 [ppm]

σ33 [ppm]

Ω [ppm]

A

Se C0 CR Cβ Cγ Cδ

1549.2 9.7 124.5 141.1 149.4 172.0

1244 -84 109 104 129 157

1430 40 124 150 147 171

1974 73 141 169 171 189

730 157 32 65 42 32

B

Se C0 CR Cβ Cγ Cδ

1699.2 8.3 125.2 147.3 149.6 168.6

1339 -87 113 129 131 145

1569 46 124 151 144 171

2190 66 140 163 174 190

851 153 27 34 43 45

molecule

77

of heavy atoms taken from X-ray at 130 K. Scheme 1 shows the orientation of 13C and 77Se σii parameters with respect to the molecular frame of 1. The appropriate values of angles defining orientation are given in Table 5. From analysis of calculated values it is apparent that the orientation of 13C tensors with respect to the molecular frame is different for A and B molecules in the unit cell and depends on the conformation of the side chain. Such a conclusion is consistent with data published by Havlin et al. who, after searching model systems containing such amino acids as glycine, alanine, valine, isoleucine, serine, and threonine by means of the ab initio method, have proved that tensors orientation for CR and Cβ carbons is sensitive to conformational effects.29 Finally, in this paper we show for the first time (to the best of our knowledge) the orientation of 77Se tensors versus the molecular structure of selenomethionine. Molecular Dynamics of the Side-Chain of 1. It is well know that side-chain carbons of L-methionine (L-Met) undergo complex internal molecular motion in the crystal lattice. The methyl group dynamics was investigated in detail by Oldfield and co-workers.30 Sparks et al. employing deuterium NMR spectroscopy have proved that molecules A and B of L-Met show two dynamically distinct types of side chains.31 Having in mind the values of CSA parameters discussed in sections 2 and 3, similar processes are expected for crystalline sample of 1. There is a number of NMR approaches, which allow us to investigate amplitude and mode of molecular motion in the solid state in a broad range. The method used most often is the measurement of relaxation parameters, e.g., 13C and 1H spinlattice relaxation times (13C T1 and 1H T1), carbon and proton

Figure 9. Correlation between values of 13C δii chemical shift and 13 C σii shielding parameters calculated with 6-311 +G** basis set. Most scatter points represent β and γ carbon atoms.

rotating frame relaxation times (13C T1F and 1H T1F), the C-H cross-relaxation time (TC-H) and the proton relaxation time in the dipolar state (T1D).32 For instance, the 13C T1 and 13C T1F measurements provide information on molecular motions in the megahertz and kilohertz frequency ranges, respectively. The other commonly used technique is 2H line shape analysis of selectively labeled models.33 The analysis of the cross-polarization profile is an important source of information about dynamics of system under investigation. Kolodziejski and Klinowski have recently reviewed this subject showing application of CP kinetics approach to solving of structural problems.34 Very recently Dybowski and co-workers have reported proton-carbon polarization-transfer kinetics for six common solid amino acids.35 Studying R-glycine, alanine, cysteine, leucine, isoleucine, and valine they showed that the presence of a mobile entity, such a methyl group shortens T1FH to a few milliseconds. After analyzing the CP profiles for 1, considerable differences between system under investigation and those reported elsewhere (ref 35) were apparent (Figure 10). The most important distinction is large amplitude oscillation for the short contact time (ranging from 0 to 0.5 ms). Such a build-up curve can reflect modulation of dipolar interactions caused by large scale molecular motion. SCHEME 1: The Orientation 13C and 77Se σii Parameters with Respect to Molecular Frame of 1.

Structure and Dynamics of L-Selenomethionine


TABLE 5: Angles between Principal Axis i and Individual Bonds in Both Molecules of L-selenomethionine. molecule A i-C-δ-Se i-Se-Cδ i-Se-Cγ i-Cγ-Se i-Cγ-Cβ i-Cβ- Cγ i-Cβ-CR i-CR-Cβ i-CR-N i-CR-C0 i-C0-CR i-C0-O1 i-C0-O2

molecule B

σ11

σ22

σ33

σ11

σ22

σ33

83.3 31.7 67.5 82.0 75.8 72.6 68.4 76.8 85.1 48.0 11.2 52.0 71.2

85.4 87.8 89.5 85.8 26.8 52.9 72.8 24.4 87.5 45.9 78.9 38.1 16.3

8.1 58.4 22.5 9.1 67.8 42.3 28.2 69.8 5.5 74.8 89.1 88.1 89.1

82.8 40.8 57.7 87.2 53.3 54.6 86.5 26.6 71.6 87.5 12.5 73.5 55.0

80.8 79.1 76.4 84.1 50.6 50.4 86.5 64.6 68.0 41.7 77.7 19.7 35.4

11.7 51.3 35.7 6.5 60.7 59.5 4.9 82.7 29.3 48.4 87.6 79.6 84.8

Figure 10a displays CP curve for R carbons for molecule A of 1 as a function of contact time recorded at 293 K. The experimental results were fitted employing eq 1 which contains term b describing dipolar 1H-13C coupling.36

[

(

)

-t 1 -t 1 3 t I(t) ) I0 exp 1 - exp - exp cos T1FH 2 Tdf 2 2 Tdf

(bt2 )] (1)

At temperature 193 K the oscillations are not observed (Figure 10b) hence, the experimental CP profile was fitted using eq 2.37

[

TABLE 6: T1rho H and T1 Relaxation Times (a) 293 K (b) 193 Ka

(

)

-t -t 3 t 1 - λ exp - (1 - λ) exp exp I(t) ) I0 exp T1FH Tdf 2 Tdf

( )] -t2 T22

(2)

In eq 2, two time constants characterize the increase of polarization transfer: T2, which is dependent on the inverse direct C-H dipole-dipole interaction (which leads to a steep

carbon atom

T1FH (ms)

a

CR (A) CR (B) Cβ (A) Cβ (B) Cγ Cδ

2.00 10.30 3.77 5.65 5.64 6.10

b

CR (A) CR (B) Cβ (A) Cβ (B) Cγ (A) Cγ (B) Cδ (A) Cδ (B)

2.94 3.21 2.92 4.05 4.00 3.10 4.59 6.57

T1 (s) 38.24 5.35 10.77 2.12 4.05 4.23 204,10 126,60 158,70 33,40 68,00 1.80

a 13 C T1 relaxation times in temperature range 183-293 K are shown in the Supporting Information.

increase in 13C polarization at starting contact times), and Tdf, which is the spin diffusion from the neighboring protons to the direct-bonded ones (which leads to a slow increase at medium contact times). A third time constant characterizes the decrease of magnetization: T1FH, which is the relaxation time of the protons in the rotating frame. A fourth parameter (λ) is dependent theoretically on the number n of direct-bonded protons (λ) 1/(n + 1)); however, in practice, λ and the other CP kinetic parameters are dependent on group mobility. Therefore, λ is treated as an adjustable parameter. In eq 1, b parameter reflects direct dipolar coupling RDD. The derived 1H T1F parameters are collected in Table 6. From the established data, the significant difference between A and B molecules of L-SeMet is apparent. The distinction of T1FH for R carbons is spectacular. For B molecule (trans geometry) the T1FH is five times longer compared to molecule A while T1 at 293 K is seven times shorter. Moreover, the values of RDD are different (see Figure 10a and c). We conclude that molecular motion of the neighboring groups modulates the oscillation of

Figure 10. Cross-polarization profiles for CR atom of A molecule of 1 at (a) 293 K and (b) 193 K and CR atom of B molecule of 1 at (c) 293 K and (d) 193 K as a function of contact time. Fitting using I-I*-S model: (a) T1FH ) 2.11 ms, b ) 10.1 kHz, Tdf ) 6 µs; (b) T1FH ) 3.36 ms, λ ) 0.17, T2 ) 69 µs, Tdf) 32 µs; (c) T1FH ) 12.5 ms, b ) 15.0 kHz, Tdf ) 99 µs; (d) T1FH ) 3.05 ms, λ ) 0,01, T2 ) 95 µs Tdf ) 34 µs.


Gajda et al. evidence supporting the conclusion that a distinct barrier of rotation for methylene carbons exists. Conclusions

Figure 11. Correlation of lnT1 versus the temperature for individual carbon atoms of 1 (rhombuses CRA, empty circles CβB, squares CRB, filled triangles Cγ, asterisks CβA, filled circles Cδ).

CP build-up and distinction of proton rotating frame relaxation times. The CP profiles for β carbons are shown in the Supporting Information. The usefulness of 13C T1 measurements in studies of dynamic process in the solid state was exhaustively discussed.38 In our project, we measured 13C T1 in the temperature range from 193 to 293 K employing pulse sequence published by Torchia.39 The established relaxation parameters are collected in Table 1s.15 T1 parameter is sensitive to molecular motion occurring at rates comparable to the radio frequency field. The general formula, which describes the relationship between relaxation time and correlation time τ, is given by the formula 1/T1 ) B2τ/(1 + ω12τ2), where ω1 is the Larmor frequency of 13C and B2 is a measure of 13C-1H dipolar interaction strength. Since the rotation rate varies with temperature, τ and T1 will have a temperature dependence. The T1 will have a minimum at the temperature at which ωiτ ) 1. Figure 11 shows the correlation of lnT1 versus temperature. As seen, the R, β, and γ carbons present a similar trend with positive slope of regression lines. Such relation is typical for slow dynamic processes with correlation time above 10-9 s. The activation parameters for RB, βB, βA, γ are very similar, whereas this value is significantly larger for the RA carbon. It is worthy to note that δ methyl group follows an opposite trend compared to the groups discussed above. This result clearly shows that δ carbons are in fast exchange regime. Due to small rotation barrier around Se-C bond, the relaxation mechanism for δ is likely more complex and dipolar (DD), and spin rotation (SR) interactions have to be taken into consideration. Finally, in order to test the dynamics of the system, we performed a dipolar dephasing (DD) experiment.40 This method is often used as a spectral editing technique. In the simplest approach after CP, the 1H decoupler is turned off for ca 50 µs. This is a sufficient time for 13C-1H dipolar coupling to dephase the transverse magnetization for any 13C with a directly bonded 1H, as long as the dipolar coupling is not motionally averaged. This effectively suppresses the lines for rigid CHn. On the other hand, for mobile groups the dipolar dephasing experiment with a variable delay is one of the techniques for proving insight into the intramolecular dynamics. The T2D relaxation times measured as LWHH are found to be 36 µs and 70 µs for B and A, respectively. The variable temperature DD approach in the range from 293 to 183 K provides some semiquantitative

In this work we present the X-ray structure of L-selenomethionine. Our results show similarities and dissimilarities between SeMet 1 and Met 2 in the solid state. Crystals of 1 and 2 are almost isostructural (a difference in the unit cell dimension is less than 5.5%). As in the case of 2, two molecules of 1 form dimer and create asymmetric part of the unit cell; however, conformation of molecule B of 1 is different compared to molecule B of 2. The distinct molecular dynamics of side chains for molecules A and B of 1 is apparent from measurements of relaxation parameters and analysis of CSA data. The large amplitude motion of side chains at high temperature (below 310 K) anticipates the phase transition of crystals of 1. Correlation between X-ray crystallography and NMR spectroscopy in relation to important biological samples is still a hot and challenging problem. In recent papers, Yee et al.,41 as well as Hunt and co-workers,42 have proved that 2D NMR techniques in liquid phase and X-ray crystallography are complementary methods for small protein structure determination. Solid-state NMR is the technique that provides a link between NMR spectroscopic data in solution and results obtained from single-crystal diffraction studies. The important feature of SS NMR is the possibility to measure dynamic processes in a broad range of amplitudes and frequencies. Acknowledgment. We are grateful to Dr. Sebastian Olejniczak and Mr. Paweł Napora for help in preparation of final version of manuscript and the Polish Committee for Scientific Research, MEiN, grant no. 3T 09A 173 27 for financial support. Calculations were carried out in Interdisciplinary Centre for Mathematical and Computational Modeling, Warsaw University, within the confines of grant no. G29-8. Supporting Information Available: Additional figures and tables showing the fitted spectra and subspectra for each carbon atom and the CP profiles for β carbons. This material is available free of charge via the Internet at http://pubs.acs.org. References and Notes (1) Suzuki, K. T. J. Health Sci. 2005, 51, 107-114. (2) de Silva, V.; Woznichak, M. M.; Burns, K. L.; Grant, K. B.; May, S. W. J. Am. Chem. Soc. 2004, 126, 2409-2413. (3) Moroder, L. J. Pept. Sci. 2005, 11, 187-214. (4) (a) Soriano-Garcia, M. Curr. Med. Chem. 2004, 11, 1657-1669. (b) Medina, D.; Thompson, H.; Ganther, H.; Ip, C. Nutr. Cancer- Int. J. 2001, 40, 12-17. (5) Schrauzer, G. N. J. Nutr. 2000, 130,1653-1656. (6) (a) McConnell, K. P.; Hoffman, J. L. FEBS Lett. 1972, 24, 6062. (b) Butler, J. A.; Whanger, P. D. J. Nutr. 1989, 119, 1001-1009. (7) Ritchey, J. A.; Davis, B. M.; Pleban, P. A.; Bayse, C. A. Org. Biomol. Chem. 2005, 3, 4337-4342. and references cited therein. (8) Pan, W-H.; Fackler, J. P. J. Am. Chem. Soc. 1978, 100, 57835789. (9) Walsh, M. A.; Evans, G.; Sanishvili, R.; Dementieva, I.; Joachimiak, A. A. Cryst. Sect. D- Biol. Cryst. 1999, 55, 1726-1732. and references cited therein. (10) Garman, E. F.; Schneider, T. R. J. Appl. Cryst. 1997, 30, 211237. (11) a) Juers, D. H.; Matthews, B. W. Q. ReV. Biophys. 2004, 37, 105119. b) Dunlop, K. V.; Irvin, R. T.; Hazes, B. Acta Crystal. D 2005, 61, 80-87. c) Skrzypczak-Jankun, E.; Borbulevych, O. Y.; Zavodszky, M. I.; Baranski, M. R.; Padmanabhan, K.; Petricek, V.; Jankun, J. Acta Crystal D 2006, 62: 766-775. (12) Laskowski, R. A.; MacArthur, M.W.; Moss, D.S.; Thanton, J. M. J. Appl. Cryst. 1993, 26, 283-291.

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Structure and Dynamics of L-Selenomethionine in the Solid State

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