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Crystal structures of rare disaccharides, α-d -glucopyranosyl β-d -psicofuranoside, and α-d -galactopyranosyl β-d -psicofuranoside
Carbohydrate Research 346 (2011) 1182–1185
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Carbohydrate Research journal homepage: www.elsevier.com/locate/carres
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Crystal structures of rare disaccharides, a-D-glucopyranosyl b-D-psicofuranoside, and a-D-galactopyranosyl b-D-psicofuranoside Shigehiro Kamitori a,⇑, Atsushi Ueda b, Yasuhiro Tahara a,c, Hiromi Yoshida a, Tomohiko Ishii c, Jun’ichi Uenishi b a
Life Science Research Center and Faculty of Medicine, Kagawa University, 1750-1 Ikenobe, Miki-cho, Kagawa 761-0793, Japan Kyoto Pharmaceutical University, Misasagi, Yamashina, Kyoto 607-8412, Japan c Faculty of Engineering, Kagawa University, 2217-20 Hayashi-machi, Takamatsu, Kagawa 761-0396, Japan b
a r t i c l e
i n f o
Article history: Received 14 February 2011 Received in revised form 24 March 2011 Accepted 3 April 2011 Available online 9 April 2011 Keywords: X-ray crystal structure D-Psicose Rare sugar Disaccharide
a b s t r a c t The crystal structures of a-D-glucopyranosyl b-D-psicofuranoside and a-D-galactopyranosyl b-D-psicofuranoside were determined by a single-crystal X-ray diffraction analysis, refined to R1 = 0.0307 and 0.0438, respectively. Both disaccharides have a similar molecular structure, in which psicofuranose rings adopt an intermediate form between 4E and 4T3. Unique molecular packing of the disaccharides was found in crystals, with the molecules forming a layered structure stacked along the y-axis. Ó 2011 Elsevier Ltd. All rights reserved.
D-Psicose is a C-3 epimer of D-fructose, and exists in small amounts in nature, belonging to the ‘rare sugars’. In the past decade, a strategy for the bioproduction of D-psicose was developed by Granström and Izumori et al.,1 and the physiological functions of D-psicose have been extensively investigated, such as the postprandial blood glucose suppressive effect.2 D-Psicose possibly exists as linear, pyranose ring, and furanose ring forms (Fig. 1). Three-dimensional structures of D-psicose are helpful for understanding the mechanism of its physiological functions. Crystal structures of b-D-psicopyranose were reported, in which uncommon trans–gauche orientation of the hydroxymethyl group relative to the pyranose ring was observed.3,4 Although D-psicose with a linear conformation and a-D-psicofuranose were found as substrates bound to L-rhamnose isomerase,5 their precise structures could not be elucidated because of the limited resolution for protein crystallography. Structural information on crystal forms of Dpsicose derivatives is also available,6–13 but does not show the inherent structure of D-psicose due to the introduction of bulky substituent groups. Recently, dissacharides composed of a b-D-psicofuranose unit were successfully synthesized by the glycosylation reaction of monosaccharide acceptors with a D-psicofuranosyl ben-
Abbreviations: GlcPsi, a-D-glucopyranosyl b-D-psicofuranoside; GalPsi, a-Dgalactopyranosyl b-D-psicofuranoside. ⇑ Corresponding author. Tel./fax: +81 87 891 2421. E-mail address: [email protected] (S. Kamitori). 0008-6215/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.carres.2011.04.003
zyl phthalate derivative.14 These non-reducing disaccharides are expected to have new biological activities, and to be useful in elucidating the precise structure of b-D-psicofuranose. We have determined the crystal structures of a-D-glucopyranosyl b-Dpsicofuranoside (GlcPsi) and a-D-galactopyranosyl b-D-psicofuranoside (GalPsi, Fig. 1). The molecular features and intermolecular interactions in crystals of these disaccharides, and a structural comparison with a-D-glucopyranosyl b-D-fructofuranoside (sucrose, CCDC 634580)15,16 are presented herein. The molecular structure of GlcPsi and GalPsi is shown in Figure 2a and b, respectively. Geometrical parameters are listed in Table 1. All bond lengths and angles between non-hydrogen atoms are in the normal range, and the mean values are well consistent with those of sucrose (1.534 Å for C–C, 1.431 Å for C–O, 110.0° for X–C–X, and 113.5° for C–O–C). All torsion angles except those involving O4G are similar between GlcPsi and GalPsi, suggesting the three-dimensional structure of these molecules to be almost the same. The root mean square deviation of non-hydrogen atoms except O4G is 0.074 Å. The O6G atoms adopt a gauche–trans conformation, and O6G of GalPsi forms an intramolecular hydrogen bond with O6P. Another intramolecular hydrogen bond is found between O2G and O1P (Fig. 2 and Table 2), helping to fix the relative orientation of the pyranose and furanose rings. In sucrose, two intramolecular hydrogen bonds are found in O2G–O1F and O5G– O6F (Fig. 2c), and O6G adopts a gauche–gauche conformation to avoid an unusual short contact with O6F. Although this difference
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S. Kamitori et al. / Carbohydrate Research 346 (2011) 1182–1185
Figure 1. Chemical structure of D-psicose with a linear conformation, b-D-psicopyranose, a-D-psicofuranose, a-D-glucopyranosyl b-D-psicofuranoside (GlcPsi) and a-Dgalactopyranosyl b-D-psicofuranoside (GalPsi).
in intramolecular hydrogen bonds between GlcPsi/GalPsi and sucrose seems to be due to the glycoside linkage between the pyranose and furanose rings, the glycoside linkage conformations are not so varied among GlcPsi, GalPsi, and sucrose; torsion angles of O5G–C1G–O1G–C2P/F and C1G–O1G–C2P/F–O5P/F are 115.4° and 52.1° (GlcPsi), 110.0° and 48.5° (GalPsi), and 108.4° and 44.3° (sucrose), respectively. The puckering of a sugar ring is generally represented by Cremer–Pople parameters,17 as listed in Table 1. The relatively large amplitude (q) and polar angle (h) close to 0.0° of the glycopyranose rings of GlcPsi (0.573 Å, 5.4°) and galactopyranose ring of GalPsi (0.573 Å, 4.8°) suggest that pyranose rings adopt an ideal chair (C) form of 4C1. Pseudorotation angles (/) of psicofuranose rings are 278° (GlcPsi) and 281° (GalPsi), indicating that these five-membered rings are puckered in the intermediate form between 4E (288°) and 4T3 (270°). The angle of the fructofuranose ring of sucrose is 264.5°, being the intermediate form between 4T3 (270°) and E3 (252°).15 This deviation of / between psicofuranose and
Table 1 Geometrical and Cremer–Pople parameters for GlcPsi and GalPsi Mean bond distances (Å) C–C C–O
GlcPsi 1.518(9) 1.420(1)
GalPsi 1.51(1) 1.43(1)
Mean bond angles (°) X–C–X (X = C or O) C–O–C
GlcPsi 109(4) 114(5)
GalPsi 109(4) 113(5)
Glycoside linkage torsion angles (°) O5G C1G O1G C2P C1G O1G C2P O5P Hydroxymethyl group torsion angles (°) O5G C5G C6G O6G O5P C5P C6P O6P O1P C1P C2P O5P Cremer–Pople parameters Pyranose ring q (Å) h (°) / (°)
GlcPsi 0.573(3) 5.0(3) 115(3)
GlcPsi 115.4(2) 52.1(3)
GalPsi 110.0(6) 48.5(8)
64.6(3) 62.5(3) 176.5(2)
58.5(8) 66.4(9) 172.4(6)
Furanose ring GalPsi 0.574(7) 4.7(7) 151(9)
q (Å) / (°)
GlcPsi 0.435(3) 278.0(3)
GalPsi 0.438(8) 281.1(9)
fructofuranose rings is caused by the different configurations of C3P and C3F in furanose rings. The C4P atoms of GlcPsi/GalPsi move above the furanose ring to avoid steric hinderance between O3P and O4P at the same side of the furanose plane. The ring puckering of a furanose ring affects the positions of O6P and O6F. The O6P of GlcPsi/GalPsi is far from O5G, while the O6F of sucrose is close enough to O5G to form a hydrogen bond. Therefore, the formation of an intramolecular hydrogen bond by O6P/O6F is thought
Table 2 Geometry of hydrogen bonds of GlcPsi and GalPsi D–H A
D–H (Å) H A (Å) D A (Å) D–H A (°) Symmetry code
GlcPsi Intramolecular hydrogen bond O1P–H O2G 0.82 1.95 O3G–H O2G 0.82 2.53 Intermolecular O–H O O2G–H O6G O3G–H O6P O4G–H O3P O4G–H O5G O6G–H O4P O3P–H O3G O4P–H O1P O6P–H O4G C–H O C2G–H O6G
2.724(3) 2.839(3)
158 104
hydrogen bond 0.82 0.82 0.82 0.82 0.82 0.82 0.82 0.82
1.90 2.09 2.33 2.40 1.92 1.86 1.88 2.32
2.670(3) 2.861(3) 3.048(3) 2.807(3) 2.719(3) 2.648(3) 2.697(3) 3.090(3)
155 158 147 111 164 162 171 157
x, y, z1 x1, y, z1 x+1, y1/2, z+1 x1, y, z x+2, y1/2, z+2 x+1, y+1/2, z+1 x, y, z+1 x+1, y, z
0.98
2.57
3.097(3)
114
x, y, z1
GalPsi Intramolecular hydrogen bond O1P–H O2G 0.82 1.94 O6P–H O6G 0.82 2.52
2.731(8) 2.922(9)
162 112
Intermolecular O–H O O2G–H O6G O3G–H O6P O4G–H O1P O6G–H O3P O6G–H O4P O3P–H O3G O4P–H O1P C–H O C1G–H O3G
hydrogen bond 0.82 0.82 0.82 0.82 0.82 0.82 0.82
1.93 2.07 2.11 2.35 2.20 1.82 1.98
2.705(8) 2.804(8) 2.922(8) 3.035(7) 2.906(8) 2.624(7) 2.780(8)
157 149 172 142 144 168 164
x, y, z1 x1, y, z1 x+1, y1/2, z+1 x+2, y1/2, z+2 x+2, y1/2, z+2 x+1, y+1/2, z+1 x, y, z+1
0.98
2.53
3.414(10) 150
x+1, y+1/2, z+1
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Figure 2. Molecular and crystal structures of (a) GlcPsi, (b) GalPsi, and (c) sucrose15 from CCDC 634580.16 Displacement ellipsoids for non-hydrogen atoms are drawn at the 50% probability level and intramolecular hydrogen bonds are indicated by dotted lines. The original molecule, Mol-1, translation symmetry operated molecules, (Mol-2, -3, and -4), and 21 symmetry operated molecules (Mol-5, -6, -7, and -8) are shown with green, gray, and yellow carbons, respectively. Intermolecular hydrogen bonds are indicated by dotted lines and the arrows show the direction of 21 axes. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
to depend on the puckering of the furanose ring, rather than the glycoside linkage conformation. The bulky substituent groups at c-2 of the furanose ring also affect the puckering of psicofuranose ring. Since GlcPsi/GalPsi has a bulky substituent group (glucopyranosyl group) at the opposite side to O3P, there is no direct interaction between a glucopyranosyl group and O3P. The crystal structure of 1-(2-b-D-psicofuranosyl)-cytosine,8 in which a bulky substituent group (cytosinyl group) is at the opposite side to O3P and O4P like GlcPsi/GalPsi, has the same puckering of psicofuranose ring as GlcPsi/GalPsi (/ = 279°). On the other, in the crystal structure of methyl 1-deoxy-1-(N1-thyminyl)-b-D-psicofuranoside9 with a thyminyl group at the same side as O3P, a psicofuranose ring is found to be puckered in the form of E3 (/ = 252°), because the O3P is positioned by van der Waals contacts with a thyminyl group.
The crystal structure of GlcPsi and GalPsi is shown in Figure 2a and b, respectively. Interestingly, in spite of the different configurations of C4G, GlcPsi, and GalPsi show similar molecular packing in crystal form. Translated molecules along x- and z-axes, Mol-1 (x, y, z), -2 (x1, y, z), -3 (x, y, z+1), and -4 (x1, y, z1) form a layer, and the 21 symmetry operated molecules, Mol-5 (x+2, y+1/2, z+1), -6 (x+1, y+1/2, z+1), -7 (x+2, y+1/2, z+2), and -8 (x+1, y+1/2, z), form another layer, to give a unique molecular layer-structure stacked along the y-axis. The neighboring layers are connected by intermolecular hydrogen bonds between furanose moieties from Mol-1, -2, -3, and -4 and pyranose moieties from Mol-5, -6, -7, and -8. As listed in Table 2, the numbers of independent intermolecular hydrogen bonds by hydroxyl groups are eight (GlcPsi) and seven (GalPsi), and the manner, in which O4G atoms form the hydrogen bonds, differs between GlcPsi and GalPsi.
S. Kamitori et al. / Carbohydrate Research 346 (2011) 1182–1185 Table 3 Crystal data and structure refinement details for GlcPsi and GalPsi
Crystal data Empirical formula Formula weight (g mol1) Crystal system Space group a (Å) b (Å) c (Å) b (°) V (Å3) Z l (mm1) Tmin/Tmax F(0 0 0) Crystal size (mm) Crystal color Data collection Diffractometer Monochrometer Radiation type Wavelength (Å) T (K) h range (°) Indexes range
Measured reflections Independent reflections Observed reflections (Io > 2r(Io)) Rint Refinement Refinement on Data/restraints/parameters R (F 2o > 2r(F 2o ) R (all data) Gof Weighted parameter a/b
GlcPsi
GalPsi
C12H22O11 341.30 Monoclinic P21 6.3766(3) 15.4173(7) 7.5938(3) 94.287(3) 744.46(6) 2 1.192 0.642/1.000 364 0.30 0.15 0.10 Colorless
C12H22O11 341.30 Monoclinic P21 5.9667(3) 15.5620(7) 7.8789(4) 94.668(3) 729.16(6) 2 1.217 0.789/1.000 364 0.1 0.05 0.05 Colorless
Rigaku RAPID2 Graphite Cu Ka 1.5418 293(2) 5.74–72.05 7 6 h 6 7 18 6 k 6 18 9 6 l 6 9 8015 1508 1367
Rigaku RAPID2 Graphite Cu Ka 1.5418 293(2) 5.63–72.01 7 6 h 6 7 18 6 k 6 19 9 6 l 6 9 6380 1483 943
0.0550
0.0339
F 2o 1508/1/216 R1 = 0.0307; wR2 = 0.0739 R1 = 0.0364; wR2 = 0.0845 1.063 0.0455/0.1252
F 2o 1483/1/216 R1 = 0.0438; wR2 = 0.0914 R1 = 0.0994; wR2 = 0.1510 1.142 0.0357/1.5107
P P R1 = R||Fo| |Fc||/R|Fo|; wR2 ¼ ½ wðjF 2o j jF 2c jÞ2= wF 4o 1=2 ; weighting scheme: w ¼ 1=½r2 ðF 2o Þ þ ðaPÞ2 þ bP where P ¼ ðF 2o þ 2F 2c Þ=3.
In GlcPsi, O4G of Mol-6 forms a hydrogen bond with O3P of Mol-1, and O4G of Mol-1 forms hydrogen bonds with O5G and O6P of Mol-2, while in GalPsi, O4G of Mol-6 forms a hydrogen bond with O1P of Mol-1, and O4G of Mol-1 does not form a notable hydrogen bond as a hydrogen-acceptor. Sucrose has a completely different molecular packing structure from GlcPsi and GalPsi, as shown in Figure 2c, in which molecules do not form a layered structure, but interdigitate. The configuration of C3P/F affects more the intermolecular interactions than does the configuration of C4G, leading to the similar molecular packing between GlcPsi and GalPsi, and the difference between GlcPsi/GalPsi and sucrose. This is because the puckering of furanose rings varies depending on the configuration of C3P/F, but pyranose rings adopt a stable 4C1 form regardless of the configuration of C4G. 1. Experimental The synthesis of GlcPsi and GalPsi was reported, previously.14 Crystals suitable for collecting X-ray data were obtained from a MeOH solution of the disaccharides.
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The collection and processing of diffraction data were carried out on a Rigaku RAPID2 imaging plate diffractometer system with a fine focus sealed tube X-ray generator and graphite monochromated Cu Ka radiation (Rigaku Ltd, Japan). The structure was solved and refined using the program SHELX97.18 Non-hydrogen atoms were refined anisotropically, and hydrogen atoms were found in difference Fourier maps and treated as riding, with C–H distances of 0.97–0.98 Å, O–H distances of 0.82 Å and Uiso(H) = 1.2 Ueq(C) and/or 1.5 Ueq(O). Friedel opposites were merged and the absolute structure was assigned based on the known stereochemistry. The data collection and refinement statistics are summarized in Table 3. The figures were prepared using the program ORTEP-319 for windows20 and PYMOL.21 Cremer–Pople parameters were calculated by the program PLATON.22 2. Supplementary data Complete crystallographic data for the structural analyses have been deposited with the Cambridge Crystallographic Data Centre, CCDC No. 811116 (GlcPsi) and 811117 (GalPsi). Copies of this information may be obtained free of charge from the Director, Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge, CB2, 1EZ, UK (fax: +44 1223 336033, e-mail: [email protected]. uk or via www.ccdc.cam.ac.uk). Acknowledgment This research was supported in part by the Kagawa University Characteristic Prior Research Fund 2009–2010. References 1. Granström, T. B.; Takata, G.; Tokuda, M.; Izumori, K. J. Biosci. Bioeng. 2004, 97, 89–94. 2. Hayashi, N.; Iida, T.; Yamada, T.; Okuma, K.; Takehara, I.; Yamamoto, T.; Yamada, K.; Tokuda, M. Biosci. Biotechnol. Biochem. 2010, 74, 510–519. 3. Kwiecien, A.; Slepokura, K.; Lis, T. Carbohydr. Res. 2008, 343, 2336–2339. 4. Fukada, K.; Ishii, T.; Tanaka, K.; Yamaji, M.; Yamaoka, Y.; Kobayashi, K.; Izumori, K. Bull. Chem. Soc. Jpn. 2010, 83, 1193–1197. 5. Yoshida, H.; Yamaji, M.; Ishii, T.; Izumori, K.; Kamitori, S. FEBS J. 2010, 277, 1045–1057. 6. Yu, J.; Zhang, S.; Li, Z.; Lu, W.; Zhou, R.; Liu, Y.; Cai, M. Carbohydr. Res. 2003, 338, 257–261. 7. Watkin, D. J.; Glawar, A. F. G.; Soengas, R.; Izumori, K.; Wormald, M. R.; Dwek, R. A.; Fleet, G. W. Acta Crystallogr., Sect. E 2005, 61, o2949–o2951. 8. Gurskaya, G. V.; Pzhvadova, G. M.; Zavgorodnii, S. G.; Tsilevich, T. L.; Gottikh, B. P. Cryst. Struct. Commun. 1982, 11, 1259–1264. 9. Roivainen, J.; Reuter, H.; Mikhailopulo, I. A.; Eickmeier, H. Acta Crystallogr., Sect. E 2007, 63, o4294. 10. Gurskaya, G. V.; Dzhavadova, G. M.; Tsapkina, E. N.; Tsilevich, T. L.; Zavgorodnii, S. G.; Florent’ev, V. L. Dokl. Akad. Nauk. SSSR (Russ.) 1983, 273, 340–343. 11. Gurskaya, G. V.; Dzhavadova, G. M.; Zavgorodnii, S. G.; Florent’ev, V. L.; Gottikh, B. P. Bioorg. Khim. (Russ.) 1987, 13, 1382–1387. 12. Roivainen, J.; Mikhailopulo, I.; Reuter, H.; Eickmeier, H. Acta Crystallogr., Sect. C 2006, 62, o659–o660. 13. Gurskaya, G. V.; Dzhavadova, G. M.; Sobolev, A. N.; Chernikova, N. Y.; Zavgorodnii, S. G.; Florent’ev, V. L.; Gottikh, B. P. Bioorg. Khim. (Russ.) 1987, 13, 1388–1398. 14. Ueda, A.; Yamashita, T.; Uenishi, J. Carbohydr. Res. 2010, 345, 1722–1729. 15. Jaradat, D. M. M.; Mebs, S.; Che˛cinska, L.; Luger, P. Carbohydr. Res. 2007, 342, 1480–1489. 16. Cambridge Structural Database (CSD): Allen, F. H. Acta Crystallogr., Sect. B 2002, 58, 380–388. 17. Cremer, D.; Pople, J. A. J. Am. Chem. Soc. 1975, 97, 1354–1358. 18. Sheldrick, G. M. Acta Crystallogr., Sect. A 2008, 64, 112–122. 19. Burnett, M. N.; Johnson, C. K. ORTEP-III: Oak Ridge Thermal Ellipsoid Plot Program for Crystal Structure Illustrations; Oak Ridge National Laboratory Report ORNL6895; 1996. 20. Farrugia, L. J. J. Appl. Crystallogr. 1997, 30, 565. 21. DeLano, W. L. The PYMOL Molecular Graphics System, Version 1.3; Schrödinger, LLC, 2002. 22. Spek, A. L. Acta Crystallogr., Sect. D 2009, 65, 148–155.
Contents lists available at ScienceDirect
Carbohydrate Research journal homepage: www.elsevier.com/locate/carres
Note
Crystal structures of rare disaccharides, a-D-glucopyranosyl b-D-psicofuranoside, and a-D-galactopyranosyl b-D-psicofuranoside Shigehiro Kamitori a,⇑, Atsushi Ueda b, Yasuhiro Tahara a,c, Hiromi Yoshida a, Tomohiko Ishii c, Jun’ichi Uenishi b a
Life Science Research Center and Faculty of Medicine, Kagawa University, 1750-1 Ikenobe, Miki-cho, Kagawa 761-0793, Japan Kyoto Pharmaceutical University, Misasagi, Yamashina, Kyoto 607-8412, Japan c Faculty of Engineering, Kagawa University, 2217-20 Hayashi-machi, Takamatsu, Kagawa 761-0396, Japan b
a r t i c l e
i n f o
Article history: Received 14 February 2011 Received in revised form 24 March 2011 Accepted 3 April 2011 Available online 9 April 2011 Keywords: X-ray crystal structure D-Psicose Rare sugar Disaccharide
a b s t r a c t The crystal structures of a-D-glucopyranosyl b-D-psicofuranoside and a-D-galactopyranosyl b-D-psicofuranoside were determined by a single-crystal X-ray diffraction analysis, refined to R1 = 0.0307 and 0.0438, respectively. Both disaccharides have a similar molecular structure, in which psicofuranose rings adopt an intermediate form between 4E and 4T3. Unique molecular packing of the disaccharides was found in crystals, with the molecules forming a layered structure stacked along the y-axis. Ó 2011 Elsevier Ltd. All rights reserved.
D-Psicose is a C-3 epimer of D-fructose, and exists in small amounts in nature, belonging to the ‘rare sugars’. In the past decade, a strategy for the bioproduction of D-psicose was developed by Granström and Izumori et al.,1 and the physiological functions of D-psicose have been extensively investigated, such as the postprandial blood glucose suppressive effect.2 D-Psicose possibly exists as linear, pyranose ring, and furanose ring forms (Fig. 1). Three-dimensional structures of D-psicose are helpful for understanding the mechanism of its physiological functions. Crystal structures of b-D-psicopyranose were reported, in which uncommon trans–gauche orientation of the hydroxymethyl group relative to the pyranose ring was observed.3,4 Although D-psicose with a linear conformation and a-D-psicofuranose were found as substrates bound to L-rhamnose isomerase,5 their precise structures could not be elucidated because of the limited resolution for protein crystallography. Structural information on crystal forms of Dpsicose derivatives is also available,6–13 but does not show the inherent structure of D-psicose due to the introduction of bulky substituent groups. Recently, dissacharides composed of a b-D-psicofuranose unit were successfully synthesized by the glycosylation reaction of monosaccharide acceptors with a D-psicofuranosyl ben-
Abbreviations: GlcPsi, a-D-glucopyranosyl b-D-psicofuranoside; GalPsi, a-Dgalactopyranosyl b-D-psicofuranoside. ⇑ Corresponding author. Tel./fax: +81 87 891 2421. E-mail address: [email protected] (S. Kamitori). 0008-6215/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.carres.2011.04.003
zyl phthalate derivative.14 These non-reducing disaccharides are expected to have new biological activities, and to be useful in elucidating the precise structure of b-D-psicofuranose. We have determined the crystal structures of a-D-glucopyranosyl b-Dpsicofuranoside (GlcPsi) and a-D-galactopyranosyl b-D-psicofuranoside (GalPsi, Fig. 1). The molecular features and intermolecular interactions in crystals of these disaccharides, and a structural comparison with a-D-glucopyranosyl b-D-fructofuranoside (sucrose, CCDC 634580)15,16 are presented herein. The molecular structure of GlcPsi and GalPsi is shown in Figure 2a and b, respectively. Geometrical parameters are listed in Table 1. All bond lengths and angles between non-hydrogen atoms are in the normal range, and the mean values are well consistent with those of sucrose (1.534 Å for C–C, 1.431 Å for C–O, 110.0° for X–C–X, and 113.5° for C–O–C). All torsion angles except those involving O4G are similar between GlcPsi and GalPsi, suggesting the three-dimensional structure of these molecules to be almost the same. The root mean square deviation of non-hydrogen atoms except O4G is 0.074 Å. The O6G atoms adopt a gauche–trans conformation, and O6G of GalPsi forms an intramolecular hydrogen bond with O6P. Another intramolecular hydrogen bond is found between O2G and O1P (Fig. 2 and Table 2), helping to fix the relative orientation of the pyranose and furanose rings. In sucrose, two intramolecular hydrogen bonds are found in O2G–O1F and O5G– O6F (Fig. 2c), and O6G adopts a gauche–gauche conformation to avoid an unusual short contact with O6F. Although this difference
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S. Kamitori et al. / Carbohydrate Research 346 (2011) 1182–1185
Figure 1. Chemical structure of D-psicose with a linear conformation, b-D-psicopyranose, a-D-psicofuranose, a-D-glucopyranosyl b-D-psicofuranoside (GlcPsi) and a-Dgalactopyranosyl b-D-psicofuranoside (GalPsi).
in intramolecular hydrogen bonds between GlcPsi/GalPsi and sucrose seems to be due to the glycoside linkage between the pyranose and furanose rings, the glycoside linkage conformations are not so varied among GlcPsi, GalPsi, and sucrose; torsion angles of O5G–C1G–O1G–C2P/F and C1G–O1G–C2P/F–O5P/F are 115.4° and 52.1° (GlcPsi), 110.0° and 48.5° (GalPsi), and 108.4° and 44.3° (sucrose), respectively. The puckering of a sugar ring is generally represented by Cremer–Pople parameters,17 as listed in Table 1. The relatively large amplitude (q) and polar angle (h) close to 0.0° of the glycopyranose rings of GlcPsi (0.573 Å, 5.4°) and galactopyranose ring of GalPsi (0.573 Å, 4.8°) suggest that pyranose rings adopt an ideal chair (C) form of 4C1. Pseudorotation angles (/) of psicofuranose rings are 278° (GlcPsi) and 281° (GalPsi), indicating that these five-membered rings are puckered in the intermediate form between 4E (288°) and 4T3 (270°). The angle of the fructofuranose ring of sucrose is 264.5°, being the intermediate form between 4T3 (270°) and E3 (252°).15 This deviation of / between psicofuranose and
Table 1 Geometrical and Cremer–Pople parameters for GlcPsi and GalPsi Mean bond distances (Å) C–C C–O
GlcPsi 1.518(9) 1.420(1)
GalPsi 1.51(1) 1.43(1)
Mean bond angles (°) X–C–X (X = C or O) C–O–C
GlcPsi 109(4) 114(5)
GalPsi 109(4) 113(5)
Glycoside linkage torsion angles (°) O5G C1G O1G C2P C1G O1G C2P O5P Hydroxymethyl group torsion angles (°) O5G C5G C6G O6G O5P C5P C6P O6P O1P C1P C2P O5P Cremer–Pople parameters Pyranose ring q (Å) h (°) / (°)
GlcPsi 0.573(3) 5.0(3) 115(3)
GlcPsi 115.4(2) 52.1(3)
GalPsi 110.0(6) 48.5(8)
64.6(3) 62.5(3) 176.5(2)
58.5(8) 66.4(9) 172.4(6)
Furanose ring GalPsi 0.574(7) 4.7(7) 151(9)
q (Å) / (°)
GlcPsi 0.435(3) 278.0(3)
GalPsi 0.438(8) 281.1(9)
fructofuranose rings is caused by the different configurations of C3P and C3F in furanose rings. The C4P atoms of GlcPsi/GalPsi move above the furanose ring to avoid steric hinderance between O3P and O4P at the same side of the furanose plane. The ring puckering of a furanose ring affects the positions of O6P and O6F. The O6P of GlcPsi/GalPsi is far from O5G, while the O6F of sucrose is close enough to O5G to form a hydrogen bond. Therefore, the formation of an intramolecular hydrogen bond by O6P/O6F is thought
Table 2 Geometry of hydrogen bonds of GlcPsi and GalPsi D–H A
D–H (Å) H A (Å) D A (Å) D–H A (°) Symmetry code
GlcPsi Intramolecular hydrogen bond O1P–H O2G 0.82 1.95 O3G–H O2G 0.82 2.53 Intermolecular O–H O O2G–H O6G O3G–H O6P O4G–H O3P O4G–H O5G O6G–H O4P O3P–H O3G O4P–H O1P O6P–H O4G C–H O C2G–H O6G
2.724(3) 2.839(3)
158 104
hydrogen bond 0.82 0.82 0.82 0.82 0.82 0.82 0.82 0.82
1.90 2.09 2.33 2.40 1.92 1.86 1.88 2.32
2.670(3) 2.861(3) 3.048(3) 2.807(3) 2.719(3) 2.648(3) 2.697(3) 3.090(3)
155 158 147 111 164 162 171 157
x, y, z1 x1, y, z1 x+1, y1/2, z+1 x1, y, z x+2, y1/2, z+2 x+1, y+1/2, z+1 x, y, z+1 x+1, y, z
0.98
2.57
3.097(3)
114
x, y, z1
GalPsi Intramolecular hydrogen bond O1P–H O2G 0.82 1.94 O6P–H O6G 0.82 2.52
2.731(8) 2.922(9)
162 112
Intermolecular O–H O O2G–H O6G O3G–H O6P O4G–H O1P O6G–H O3P O6G–H O4P O3P–H O3G O4P–H O1P C–H O C1G–H O3G
hydrogen bond 0.82 0.82 0.82 0.82 0.82 0.82 0.82
1.93 2.07 2.11 2.35 2.20 1.82 1.98
2.705(8) 2.804(8) 2.922(8) 3.035(7) 2.906(8) 2.624(7) 2.780(8)
157 149 172 142 144 168 164
x, y, z1 x1, y, z1 x+1, y1/2, z+1 x+2, y1/2, z+2 x+2, y1/2, z+2 x+1, y+1/2, z+1 x, y, z+1
0.98
2.53
3.414(10) 150
x+1, y+1/2, z+1
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Figure 2. Molecular and crystal structures of (a) GlcPsi, (b) GalPsi, and (c) sucrose15 from CCDC 634580.16 Displacement ellipsoids for non-hydrogen atoms are drawn at the 50% probability level and intramolecular hydrogen bonds are indicated by dotted lines. The original molecule, Mol-1, translation symmetry operated molecules, (Mol-2, -3, and -4), and 21 symmetry operated molecules (Mol-5, -6, -7, and -8) are shown with green, gray, and yellow carbons, respectively. Intermolecular hydrogen bonds are indicated by dotted lines and the arrows show the direction of 21 axes. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
to depend on the puckering of the furanose ring, rather than the glycoside linkage conformation. The bulky substituent groups at c-2 of the furanose ring also affect the puckering of psicofuranose ring. Since GlcPsi/GalPsi has a bulky substituent group (glucopyranosyl group) at the opposite side to O3P, there is no direct interaction between a glucopyranosyl group and O3P. The crystal structure of 1-(2-b-D-psicofuranosyl)-cytosine,8 in which a bulky substituent group (cytosinyl group) is at the opposite side to O3P and O4P like GlcPsi/GalPsi, has the same puckering of psicofuranose ring as GlcPsi/GalPsi (/ = 279°). On the other, in the crystal structure of methyl 1-deoxy-1-(N1-thyminyl)-b-D-psicofuranoside9 with a thyminyl group at the same side as O3P, a psicofuranose ring is found to be puckered in the form of E3 (/ = 252°), because the O3P is positioned by van der Waals contacts with a thyminyl group.
The crystal structure of GlcPsi and GalPsi is shown in Figure 2a and b, respectively. Interestingly, in spite of the different configurations of C4G, GlcPsi, and GalPsi show similar molecular packing in crystal form. Translated molecules along x- and z-axes, Mol-1 (x, y, z), -2 (x1, y, z), -3 (x, y, z+1), and -4 (x1, y, z1) form a layer, and the 21 symmetry operated molecules, Mol-5 (x+2, y+1/2, z+1), -6 (x+1, y+1/2, z+1), -7 (x+2, y+1/2, z+2), and -8 (x+1, y+1/2, z), form another layer, to give a unique molecular layer-structure stacked along the y-axis. The neighboring layers are connected by intermolecular hydrogen bonds between furanose moieties from Mol-1, -2, -3, and -4 and pyranose moieties from Mol-5, -6, -7, and -8. As listed in Table 2, the numbers of independent intermolecular hydrogen bonds by hydroxyl groups are eight (GlcPsi) and seven (GalPsi), and the manner, in which O4G atoms form the hydrogen bonds, differs between GlcPsi and GalPsi.
S. Kamitori et al. / Carbohydrate Research 346 (2011) 1182–1185 Table 3 Crystal data and structure refinement details for GlcPsi and GalPsi
Crystal data Empirical formula Formula weight (g mol1) Crystal system Space group a (Å) b (Å) c (Å) b (°) V (Å3) Z l (mm1) Tmin/Tmax F(0 0 0) Crystal size (mm) Crystal color Data collection Diffractometer Monochrometer Radiation type Wavelength (Å) T (K) h range (°) Indexes range
Measured reflections Independent reflections Observed reflections (Io > 2r(Io)) Rint Refinement Refinement on Data/restraints/parameters R (F 2o > 2r(F 2o ) R (all data) Gof Weighted parameter a/b
GlcPsi
GalPsi
C12H22O11 341.30 Monoclinic P21 6.3766(3) 15.4173(7) 7.5938(3) 94.287(3) 744.46(6) 2 1.192 0.642/1.000 364 0.30 0.15 0.10 Colorless
C12H22O11 341.30 Monoclinic P21 5.9667(3) 15.5620(7) 7.8789(4) 94.668(3) 729.16(6) 2 1.217 0.789/1.000 364 0.1 0.05 0.05 Colorless
Rigaku RAPID2 Graphite Cu Ka 1.5418 293(2) 5.74–72.05 7 6 h 6 7 18 6 k 6 18 9 6 l 6 9 8015 1508 1367
Rigaku RAPID2 Graphite Cu Ka 1.5418 293(2) 5.63–72.01 7 6 h 6 7 18 6 k 6 19 9 6 l 6 9 6380 1483 943
0.0550
0.0339
F 2o 1508/1/216 R1 = 0.0307; wR2 = 0.0739 R1 = 0.0364; wR2 = 0.0845 1.063 0.0455/0.1252
F 2o 1483/1/216 R1 = 0.0438; wR2 = 0.0914 R1 = 0.0994; wR2 = 0.1510 1.142 0.0357/1.5107
P P R1 = R||Fo| |Fc||/R|Fo|; wR2 ¼ ½ wðjF 2o j jF 2c jÞ2= wF 4o 1=2 ; weighting scheme: w ¼ 1=½r2 ðF 2o Þ þ ðaPÞ2 þ bP where P ¼ ðF 2o þ 2F 2c Þ=3.
In GlcPsi, O4G of Mol-6 forms a hydrogen bond with O3P of Mol-1, and O4G of Mol-1 forms hydrogen bonds with O5G and O6P of Mol-2, while in GalPsi, O4G of Mol-6 forms a hydrogen bond with O1P of Mol-1, and O4G of Mol-1 does not form a notable hydrogen bond as a hydrogen-acceptor. Sucrose has a completely different molecular packing structure from GlcPsi and GalPsi, as shown in Figure 2c, in which molecules do not form a layered structure, but interdigitate. The configuration of C3P/F affects more the intermolecular interactions than does the configuration of C4G, leading to the similar molecular packing between GlcPsi and GalPsi, and the difference between GlcPsi/GalPsi and sucrose. This is because the puckering of furanose rings varies depending on the configuration of C3P/F, but pyranose rings adopt a stable 4C1 form regardless of the configuration of C4G. 1. Experimental The synthesis of GlcPsi and GalPsi was reported, previously.14 Crystals suitable for collecting X-ray data were obtained from a MeOH solution of the disaccharides.
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The collection and processing of diffraction data were carried out on a Rigaku RAPID2 imaging plate diffractometer system with a fine focus sealed tube X-ray generator and graphite monochromated Cu Ka radiation (Rigaku Ltd, Japan). The structure was solved and refined using the program SHELX97.18 Non-hydrogen atoms were refined anisotropically, and hydrogen atoms were found in difference Fourier maps and treated as riding, with C–H distances of 0.97–0.98 Å, O–H distances of 0.82 Å and Uiso(H) = 1.2 Ueq(C) and/or 1.5 Ueq(O). Friedel opposites were merged and the absolute structure was assigned based on the known stereochemistry. The data collection and refinement statistics are summarized in Table 3. The figures were prepared using the program ORTEP-319 for windows20 and PYMOL.21 Cremer–Pople parameters were calculated by the program PLATON.22 2. Supplementary data Complete crystallographic data for the structural analyses have been deposited with the Cambridge Crystallographic Data Centre, CCDC No. 811116 (GlcPsi) and 811117 (GalPsi). Copies of this information may be obtained free of charge from the Director, Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge, CB2, 1EZ, UK (fax: +44 1223 336033, e-mail: [email protected]. uk or via www.ccdc.cam.ac.uk). Acknowledgment This research was supported in part by the Kagawa University Characteristic Prior Research Fund 2009–2010. References 1. Granström, T. B.; Takata, G.; Tokuda, M.; Izumori, K. J. Biosci. Bioeng. 2004, 97, 89–94. 2. Hayashi, N.; Iida, T.; Yamada, T.; Okuma, K.; Takehara, I.; Yamamoto, T.; Yamada, K.; Tokuda, M. Biosci. Biotechnol. Biochem. 2010, 74, 510–519. 3. Kwiecien, A.; Slepokura, K.; Lis, T. Carbohydr. Res. 2008, 343, 2336–2339. 4. Fukada, K.; Ishii, T.; Tanaka, K.; Yamaji, M.; Yamaoka, Y.; Kobayashi, K.; Izumori, K. Bull. Chem. Soc. Jpn. 2010, 83, 1193–1197. 5. Yoshida, H.; Yamaji, M.; Ishii, T.; Izumori, K.; Kamitori, S. FEBS J. 2010, 277, 1045–1057. 6. Yu, J.; Zhang, S.; Li, Z.; Lu, W.; Zhou, R.; Liu, Y.; Cai, M. Carbohydr. Res. 2003, 338, 257–261. 7. Watkin, D. J.; Glawar, A. F. G.; Soengas, R.; Izumori, K.; Wormald, M. R.; Dwek, R. A.; Fleet, G. W. Acta Crystallogr., Sect. E 2005, 61, o2949–o2951. 8. Gurskaya, G. V.; Pzhvadova, G. M.; Zavgorodnii, S. G.; Tsilevich, T. L.; Gottikh, B. P. Cryst. Struct. Commun. 1982, 11, 1259–1264. 9. Roivainen, J.; Reuter, H.; Mikhailopulo, I. A.; Eickmeier, H. Acta Crystallogr., Sect. E 2007, 63, o4294. 10. Gurskaya, G. V.; Dzhavadova, G. M.; Tsapkina, E. N.; Tsilevich, T. L.; Zavgorodnii, S. G.; Florent’ev, V. L. Dokl. Akad. Nauk. SSSR (Russ.) 1983, 273, 340–343. 11. Gurskaya, G. V.; Dzhavadova, G. M.; Zavgorodnii, S. G.; Florent’ev, V. L.; Gottikh, B. P. Bioorg. Khim. (Russ.) 1987, 13, 1382–1387. 12. Roivainen, J.; Mikhailopulo, I.; Reuter, H.; Eickmeier, H. Acta Crystallogr., Sect. C 2006, 62, o659–o660. 13. Gurskaya, G. V.; Dzhavadova, G. M.; Sobolev, A. N.; Chernikova, N. Y.; Zavgorodnii, S. G.; Florent’ev, V. L.; Gottikh, B. P. Bioorg. Khim. (Russ.) 1987, 13, 1388–1398. 14. Ueda, A.; Yamashita, T.; Uenishi, J. Carbohydr. Res. 2010, 345, 1722–1729. 15. Jaradat, D. M. M.; Mebs, S.; Che˛cinska, L.; Luger, P. Carbohydr. Res. 2007, 342, 1480–1489. 16. Cambridge Structural Database (CSD): Allen, F. H. Acta Crystallogr., Sect. B 2002, 58, 380–388. 17. Cremer, D.; Pople, J. A. J. Am. Chem. Soc. 1975, 97, 1354–1358. 18. Sheldrick, G. M. Acta Crystallogr., Sect. A 2008, 64, 112–122. 19. Burnett, M. N.; Johnson, C. K. ORTEP-III: Oak Ridge Thermal Ellipsoid Plot Program for Crystal Structure Illustrations; Oak Ridge National Laboratory Report ORNL6895; 1996. 20. Farrugia, L. J. J. Appl. Crystallogr. 1997, 30, 565. 21. DeLano, W. L. The PYMOL Molecular Graphics System, Version 1.3; Schrödinger, LLC, 2002. 22. Spek, A. L. Acta Crystallogr., Sect. D 2009, 65, 148–155.