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The crystal and molecular structure of 2-sulfamino-2-deoxy-α-d -glucopyranose sodium salt·2H2O (glucosamine 2-sulfate)
The crystal and molecular structure of 2-sulfami no-2-deoxy-=-D-glucopyranose sodium salt.2H20 (glucosamine 2-sulfate) E. A. Yates, W. M a c k i e Department of Biochemistry and Molecular Biology, University of Leeds, Leeds LS2 9JT, UK and D. Lamba* Max Planck Institut f(~r Biochemie, Abt. Strukturforschung, D-82152 Martinsried bei Munchen, Germany Received 7 November 1994 The crystal and molecular structure of 2-sulfamino-2-deoxy-~-D-glucopyranose has been determined by direct methods. The crystal belongs to the space group P212121 and has unit cell dimensions a=7.713 A, b=9.390 A and c= 17.222 A. The sugar ring has the expected conformation (4C1) and the geometry of the N-sulfate moiety is comparable with that found in previous investigations of monosaccharide O-sulfates. The sodium ion is octahedrally coordinated involving one ring oxygen, two hydroxyls, one sulfate oxygen and two water oxygens.
Keywords: glucosamine 2-sulfate; glucosamine N-sulfate; crystal and molecular structure
Sulfated monosaccharides occur most frequently in plants and animals as building blocks of polysaccharides. These include various polysaccharides from red algae and the proteoglycan and glycosaminoglycan components (chondroitin, dermatan and keratan sulfates, heparin and heparan sulfates) of the extracellular matrix and cells of many animal tissues a 3. Of these, only heparin and heparan sulfate preparations have been shown to contain sulfated 2-amino-2-deoxy-D-glucopyranose (Dglucosamine) units. Various biological activities and affinities have been ascribed to heparin and heparan sulfates including anti-coagulant activity, angiogenesis, cell adhesion, growth factor and cell proliferation activity4 7. The extent and pattern of sulfation of D-glucosamine residues often appears to be crucial to their activities. Effects of this kind are probably best documented with regard to the anti-coagulant activity of heparin in which the active sequence has been identified as a pentasaccharide containing three D-glucosamine units of which the non-reducing terminal unit is mono-sulfated (6-sulfate), the central unit is tris-sulfated (2,3,6-sulfate) and the reducing unit is bis-sulfated * On leavefromIstitutodi StrutturisticaChimica'GiordanoGiacomello', Area della Recerca di Roma, CP 10, 1-00016 Monterotondo Stazione, Rome, Italy
0141-8130/95/$09.50 ~ 1995ElsevierScienceB.V.All rights reserved
(2,6-sulfate) 4'8. Not surprisingly, in efforts to determine the precise role of sulfate groups in these biological interactions, much time has been devoted to structural studies of the conformation, cation coordination and charge distributions of sulfate groups and the influence which these parameters have on the host molecules 4'9. The present study, in which the crystal and molecular structure of 2-sulfamino-2-deoxy-ct-D-glucopyranose (1) is reported, forms part of our ongoing studies of sulfated monosaccharides by X-ray crystallography 1° 12, The results represent part of a series of recently completed investigations in our laboratory, including those on D-glucosamine 2,3-bis-sulfate 13 and its methyl glycoside, and may help to give some insight into the structural factors that determine the important biological functions of heparin and heparan sulfates.
Experimental X-ray crystallography 2-sulfamino-2-deoxy-~-D-glucopyranose sodium salt, [~]2o= + 55 ° (c, 2.0 water), was purchased from Sigma Chemical Company. Crystals suitable for diffraction experiments were grown by slow evaporation of an aqueous propan-2-ol solution. Oscillation and Weissenberg photographs indicated an orthorhombic unit cell and
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The crystal and molecular structure of glucosamine 2-sulfate: E. A. Yates et al. Table 1 Crystal data and details of the structural analysis of (I) Crystal size (mm) Formula Crystal system Space group Unit cell dimensions (A) a b c Volume (A3) Z Formula weight D, (mg m- 3) V (000) ,u CuK~ (cm -1)
0.10 × 0.20 × 0.20 C6H~2OsNS-Na-2H20 Orthorhombic P2,2~21 7.713111 9.390(2) 17.222(2) 1247.3(15) 4 317.24 1.689 664.0 31.10
space g r o u p P212121. A crystal (0.10 × 0.20 × 0.20 mm) was sealed in a L i n d e m a n n glass capillary tube a n d set on an E n r a f - N o n i u s C A D - 4 F diffractometer. Accurate unit cell p a r a m e t e r s were d e t e r m i n e d by a least-squares fit of 40 high 0 reflections with 27 ° < 0 < 44 °. T h e crystal d a t a are given in Table 1. T h e intensity d a t a were collected in the 0,,--20 scan mode, using nickel-filtered C u K , r a d i a t i o n up to 2 0 = 120 ° for a t o t a l of 4071 reflections of which 730 were considered weak (according to the criterion I > 3a(I)) a n d 68 were controls. Indices were in the following ranges: h, - 8 to 0; k, - 1 0 to 10; a n d l, - 19 to 19. The c o n t r o l reflection - 1 2 0 was m e a s u r e d every h o u r of e x p o s u r e time a n d the average value of the intensity of this s t a n d a r d was 1217.1 counts with a s t a n d a r d d e v i a t i o n (of the distribution) of 16.7 11.37%). L o r e n t z a n d p o l a r i z a t i o n corrections were applied, b u t no a b s o r p t i o n c o r r e c t i o n was made. The d a t a were merged using the S H E L X T L - p l u s p a c k a g e ~4 to give 869 unique reflections, of which 828 with F o > 3a(Fo) were used in the structure analysis, m e r g i n g to R = 0 . 0 5 9 . The structure was solved by direct m e t h o d s 14 which identified all the n o n - h y d r o g e n atoms, a n d the initial residual for these positions was 0.39. The structure was then refined isotropically (R =0.089, unit weights) a n d anisotropically, minimizing the function E ~ [ F o ] - [F~]) 2 where ~o= 1/a2(Fo). A t t e m p t s to locate the h y d r o g e n a t o m s were only p a r t i a l l y successful, a n d so h y d r o g e n a t o m s for 0 4 , 0 6 , N a n d the water molecules were not included in the refinement. All the r e m a i n i n g h y d r o g e n a t o m s were included in the latter stages of refinement, with fixed i s o t r o p i c t e m p e r a t u r e factors equal to the equivalent i s o t r o p i c t e m p e r a t u r e factor of their carrier atom. T h e final R was 0.057 a n d wR was 0.060. The average a n d m a x i m u m shift-to-error ratios were 0.356 a n d 0.078, respectively, a n d the final difference F o u r i e r m a p showed m a x i m u m a n d m i n i m u m peaks of 0.50 e/~-3 a n d - 0 . 3 9 e/k-3. The a t o m i c scattering factors used were those in the S H E L X T L - p l u s p a c k a g e ~* a n d are in the analytical form given in the I n t e r n a t i o n a l Tables for X-ray C r y s t a l l o g r a p h y tS. T h e final p o s i t i o n a l p a r a m e t e r s for all the n o n - h y d r o g e n a t o m s are given in Table 2 a n d the description of the internal g e o m e t r y of the molecule is shown in Table 3. The c o o r d i n a t i o n of the s o d i u m ion a n d details of the short contacts are given in Tables 4 a n d 5 respectively. The m o l e c u l a r g e o m e t r y p a r a m e t e r s were a n a l y s e d using the P A R S T p r o g r a m :6. The two p r o c h i r a l h y d r o g e n a t o m s a t t a c h e d to C6 were differentiated a c c o r d i n g to the rules p r o p o s e d b y H a n s o n ~7.
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Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
Table 2 Atomic coordinates and equivalent isotropic displacement coefficients IA21 of (11 Atom
\.'a
yh
C1 C2 C3 C4 C5 C6 O1 N 03 04 05 06 S1 O1S O2S O3S Na O1W O2W
- 0.290819) 0.2762(8) -0.3600(8) 0.5417191 -0.5425(9) -0.7224(9) 0.1826181 -0.0893(7) -0.3589(7) - 0.6068(7) -0.466317) -0.813717) -0.0274(3) 0.1616171 0.0985(7) -0.0860(7) 0.3389(4) -0.5642(8) -0.333318)
-0.4868(7) 0.3855(7) -0.2409(7) -0.2623(7) -0.3661171 -0.4003(8) -0.4433(7) -0.3689(7) -0.1575(5) -0.1282(6) -0.5000(5) -0.4877(6) -0.4366(2) 0.4221(61 0.3575(6) -0.5841161 0.2012(31 -0.3713(61 -0.2519(7)
z.'c
U~q"
-0.6275(5) 0.6952(5) -0.6772(4) -0.6473(4) -0.5800(4) -0.5502(5) 0.5682(4) -0.718214) -0.7464(3) -0.6207(4) -0.6027(3) -0.6035(4) -0.801411) 0.797114) 0.866114) -0.8010(41 -0.8826(2) 0.8878(4) - 1.019614)
0.0356(8) 0.03 ! 118) 0.0264171 0.030117t 0.0322(8) 0.040417/ 0.0531171 0.0359(8) 0.0340(8) 0.0395(8) 0.0328(7) 0.0491181 0.0322(5) 0.0427(7) 0.0448(7) 0.045116) 0./1351t61 0.0503(7) 0.0522(71
a U~4= I/3 EiXiUija*a*aiaj Table 3 Molecular geometry of (!) Bond lengths (~) C1-C2 C2-C3 C3 C4 C4-C5 C5 C6 CI O1 C2-N C3 03 Bond angles (') C1-C2-C3 C2 C3 C4 C3 C4-C5 C4-C5-C6 C2-C3-O3 C3C4 04 C4 C5-O5 C5-C606 C6-C5-O5 C5 O5-C1 O5-C1-C2 Ol CI C2
1.508(10) 1.536(91 1.507191 1.515(101 1.513(10) 1.382(10) 1.504(9) 1.426191 111.8161 110.0(6) 110.6(6) 113.5(6) 108.3(6) 108.6(5) 110.6(61 111.1(6) 106.3(61 113.1(5) 111.0(6) 109.9(61
Torsion angles C) Endocyclic O5-C1-C2 C3 CI C2 C3 C4 C2-C3-C4-C5 03 C3 C4 04 C4-C5-O5-C 1 C5 05 CI C2
53.5(8) -51.4(8) 52.7(7) -68.1(7) 60.2(7) -58.4(7)
Aminosuljate C1-C2- N S C3-C2-N S C2-N-S-O1S C2 N S O3S C2-N-S-O2S
110.6(6) 124.9(61 170.6(51 -51.7(61 70.3(6)
C4 04 C5 05 C6 06 05 C1 N-S S~O1S S-O2S S O3S 03 C3 C4 O4-C4-C5 O5-C1 O1 CI-C2-N N-C2-C3 C2-N-S N S-O1S N S O2S N S O3S O1S S O2S O2S S O3S O1S-S-O3S Exocyclic O1-CI-C2-N N C2 C3 03 C3-C4-C5-O5 04 C4~C5-C6 C4-C5-C6-O6 C5-O5 C 1 0 l O5-C5-C6-O6
1.431181 1.442(81 1.418(101 1.425191 1.638171 1.466161 1.446(61 1.457161 111.4161 108.616) 112.2161 109.9161 111.4151 118.0151 102.1131 111.3141 106.0141 111.6141 112.0141 113.4141
53.1181 63.2(7) - 56.9(7) 64.7(8) 72.0(8) 65.0(8) -49.8(8)
R e s u l t s and d i s c u s s i o n Molecular geometry A perspective view of the molecule (1) together with the n u m b e r i n g scheme is shown in Fioure 1. The o b s e r v e d b o n d lengths a n d valence angles of the p y r a n o s e ring are within the range r e p o r t e d for c a r b o h y d r a t e s 18-z°. The c o n f o r m a t i o n along the sequence C 5 - C 6 - O 6 is
The crystal and molecular structure of glucosamine 2-suffate." E. A, Yateset al. Table 4 Geometryof the sodium coordination
Type
Interatomic distance (A)
Type
Na...O3(I) Na...OS(II-a-2c) Na...O6(II-a-2c) Na...O2S(I) Na...O1W(I) Na...OZW(I)
2.385(7) 2.428(6) 2.338(7) 2.382(7) 2.362(7) 2.408(7)
O1W(I) O2S(I) O2S(I) O3(I)
Angle (°)
05(II-a-2c)...Na...06(II-a-2c) ...Na...OS(II-a-2c) ...Na...O6(II-a-2c) ...Na...OlW(I) ...Na...O2W(I)
68.5(2) 93.9(2) 98.6(2) 99.3(2) 177.0(3)
Symmetry codes: (I) x, y, z; (II) - x , 0.5+y, 0 . 5 - z
Table 5 Molecular interactions Short contacts
Distance (A)
O l W(1)...O2W(I) Ol(I) ...O6(I+ a) N(I) ...O6(I+ a) O 1S(I) ...O1W(I+ a) Ol(I) ...O2W(II- a - b) O2S(I) ...O2W(III- b - 2c) O1W(I)...O2W(III- a - b - 2c) N(I) ...O3S(IV- 2c) O3(1) ...O1S(IV- 2c) O4(I) ...O3S(IV-a- 2c) O4(I) ...O1W(IV- a - 2c)
3.096(9) 2.939(9) 3.109(9) 2.672(9) 2.984(9) 3.019(9) 2.861(9) 3.015(8) 2.787(7) 2.758(8) 2.753(8)
Symmetry codes: (I) x, y, z; (II) 0.5- x, - y , 0.5 + z; (III) 0.5 + x, 0.5- y, - z ; (IV) - x , 0.5+y, 0 . 5 - z
0-6
•C•_6
0-4 G-4 0-3
0-5
C-I 0-2S 0-1 ,-3S
Figure 1 Perspective view and atom labelling of 2-sulfamino-2-deoxyc~-o-glucopyranose (1) with thermal ellipsoids at 50% probability level
gauche--gauche (the torsion angles defined by O 5 - C 5 C6-O6 and C 4 - C 5 - C 6 - O 6 being -49.8(8) ° and 72.0(8) °, respectively), which is one of the two preferred noneclipsed orientations in the solid state for monosaccharides having the glueo configuration 21. The molecule has the
Vibrational parameters U 0 and U~o together with tables of bond lengths, valence angles and lists of structure factors have been deposited with and may be obtained from the Director, Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK.
expected 4C 1 chair conformation 22 with ring-puckering parameters 23'24 Q = 0.55(1) A, 4~= - 51(13)° and 0 = 2.9(7)°. There is no significant increase in the length of the C 2 - N bond (1.504(9)/~) when compared to 2-amino-2-deoxy-~D-glucopyranose-3-sulfate25 (1.493(7)A), 2-amino-2-deoxyfl-v-glucopyranose-6-sulfate26 (1.480(8) A), 3-a m l"no-l,6anhydro-3-deoxy-fl-o-glucopyranose27 (1.470(3)A; a slight increase), 2-amino-2,6-dideoxy-~-o-glucopyranose 6sulfonic acid 26 (1.495/~), methyl 2-amino-2,6-dideoxy-cto-glucopyranoside-6-sulfonic acid 23 (1.502(4) A) and chondrosine 19 (1.50(1)A). The H2-C2 bond is eclipsed with respect to the N-S bond in order to minimize steric interactions, and the value of the torsion angle H 2 - C 2 - N - S (9(1) °) together with that of C 2 - N - S (118.0(5) °) indicates that the nitrogen atom has sp 2 hybridization and is part of a planar system. The value of the angle C 2 - N - S (118.0(5) °) is similar to that found in the O-sulfates for the sequence C - O - S (average 119(2)o)1o 12,3o,31, and the angles between sulfamino oxygens in the sequence OiS-S-OiS (111.6(4) °, 112.0(4) ° and 113.4(4) ° compare with the average value in the O-sulfates of 113.0(1.9) °1° 12,3o,31. The angles in the sequence N - S - O i S show more variation: N - S - O 1 S (102.1(3) °) and N - S - O 3 S (106.0(4) °) are close to the values found in the sequence O - S - O i S (average 105.2(2.5)o)1o 12,29.3o, whereas N - S - O 2 S (111.3(4) °) is relatively large. The S-O2S bond length is also shorter than $431S and S-O3S (1.446(6) A compared to 1.466(6) A and 1.457(6)A). These observations suggest that the negative charge carried on the sulfate group is shared by O1S and O3S, and that S-O2S has double bond character. A similar situation was observed in the crystal structure of fl-o-glucopyranose-6-sulfate potassium salt 11. The only sulfamino group oxygen involved in coordination of the sodium ion is O2S as shown in Figure 2. The bond angles at the point of attachment defined by C 1 - C 2 - N and C 3 - C 2 - N are 109.9(6) ° and 111.4(5) ° respectively, and are comparable to those found in the non-substituted amino sugars: 109.1(4) ° and 111.5(4) ° in 2-amino-2-deoxy~t-D-glucopyranose-3-sulfate25, 108.4(5) ° and 111.0(6) ° in 2-amino-2-deoxy-/%o-glucopyranose-6-sulfate2s, 109.9(4)° and 110.6(4) ° in 2-amino-2,6-dideoxy-ct-o-glucopyranose6-sulfonic acid 26 and 108.7(2 °) and 109.6(2) ° in methyl 2amino-2,6-dideoxy-~-o-glucopyranoside-6-sulfonic acid 28.
Sodium ion coordination The sodium ion is coordinated by six oxygen atoms in an octahedral arrangement involving one ring oxygen, two water molecules, one sulfamino oxygen and .two hydroxyl oxygens. The sodium-to-oxygen distances (average 2.38(3)A) are within the range expected for six-fold coordination 32.
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221
The crystal and molecular structure of glucosamine 2-sulfate. E. A. Yates et al. 0-3(')
Packin.q ./eatures
o-6L-----~-~~ ~
":
) 0-2S(0
O-IWO) O' .a-~)
O-2W(|)
Figure2 Geometry of the sodium ion coordination
~f
The crystal packing includes an extended hydrogenbonded network and is stabilized by coordination of the sodium ion (Figure 3). All of the hydroxyl and suifamino oxygens and the two water molecules are involved in this network. As we were unable to locate the hydrogen atoms attached to 04, 0 6 and N in the final difference map, we are unable to characterize the hydrogen bonding network unambiguously. Consequently, only relevant inter-atomic distances ( < 3.2 A) between putative hydrogen bond donors or acceptors are listed in TaMe 5.
Acknowledgements The authors are grateful to the Science and Engineering Research Council (E.A.Y.) and the Italian National Research Council special ad hoc programme 'Cimica Fine II' subproject 3 (D.L.) for financial support, and to the University of Leeds Computing Service for the provision of computing facilities.
d
/ /
) it I
iI I
)/t
/
)"
Figure 3 View of the unit cell of (1) along the a axis
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The crystal and molecular structure of glucosamine 2-sulfate." E. A. Yates et al.
References 1 2 3 4 5 6 7 8 9 10 11 12 13
14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
Table A2
Mackie, W. and Preston, R.D. in 'Algal Physiology and Biochemistry' (Ed W.D.P. Stewart), Blackwell, Oxford, 1974, pp 40-85 Kjellen, L. and Lindahl, U. Annu. Rev. Biochem. 1991, 60, 443 Jackson, R.L., Busch, S.J. and Cardin, A.D. Physiol. Rev. 1991, 71, 481 Van Boeckel, C.A.A. and Petitou, M. Angew. Chem. 1993, 32, 1671 Hahnenberger, R., Jackobson, A., Ansari, A., Wehler, T., Svahn, C.M. and Lindahl, U. Glycobiolooy 1993, 3, 567 Turnbull, J.E., Fernig, D., Ke, Y. and Gallagher, J.T.J. Biol. Chem. 1992, 267, 10337 Schmidt, A., Yoshida, K. and Buddecke, E. J. Biol. Chem. 1992, 267, 19242 Petitou, M., Duchaussoy, P., Lederman, I., Choay, J., Sinay, P., Jacquinet, J.-C. and Torri, G. Carbohydr. Res. 1986, 147, 221 Mulloy, B., Forster, M.J., Jones, C., Drake, A.F., Johnson, E.A. and Davies, D.B. Carbohydr. Res. 1994, 255, 151 Lamba, D., Glover, S., Mackie, W., Rashid, A., Sheldrick, B. and Perez, S. Glycobiology 1994, 4, 151 Lamba, D., Mackie, W., Sheldrick, B., Belton, P. and Tanner, S. Carbohydr. Res. 1988, 180, 183 Lamba, D., Mackie, W., Rashid, A., Sheldrick, B. and Yates, E.A. Carbohydr. Res. 1993, 241, 89 Research results presented at the Third International Symposium on Conformational Analysis of Carbohydrates and Protein/ Carbohydrate Interactions, Val Morin, Qu6bec, Canada, 24-28 July 1994 Sheldrick, G.M. 'SHELXTL-plus. Release 4.2 for Siemens R3m/V Crystallographic Research Systems', Siemens Analytical X-ray Instruments Inc, Madison, Wisconsin, USA, 1991 'International Tables for X-ray Crystallography', Kynoch Press, Birmingham, 1974, volume 4 (present distributor: Kluwer Academic Publishers, Dordrecht) Nardelli, M. Comput. Chem. 1983, 7, 95 Hanson, K.R.J. Am. Chem. Soc. 1966, 88, 2731 Allen, F.H., Kennard, O., Watson, D.G., Brammer, L., Orpen, A.G. and Taylor, R. J. Chem. Soc. Perkin Trans. II 1987, S1-S19 Allen, F.H. Acta Crystallogr. 1986, 1342, 515 Arnott, S. and Scott, W.E.J. Chem. Soc. Perkin Trans. H 1972, 324 Allen, F.H. and Fortier, S. Acta Crystallogr. 1993, !!49, 1021 Marchessault, R.H. and Perez, S. Biopolymers 1979, 18, 2369 Cremer, D. and Popple, J.A.J. Am. Chem. Soc. 1975, 97, 1354 Jeffrey, G.A. and Yates, J.H. Carbohydr. Res. 1979, 74, 319 Mackie, W., Yates, E.A. and Lamba, D. Carbohydr. Res. 1995, 266, 65-74 Vega, R., Lopez-Castro, A. and Marquez, R. Acta Crystallogr. 1986, C42, 1066 Noordik, J.H. and Jeffrey, G.A. Acta Crystallogr. 1977, B33, 403 Fernandez-Bolanos, J.G., Morales, J., Garcia, S., Dianez, M.J., Estrada, M.D., Lopez-Castro, A. and Perez, S. Carbohydr. Res. 1993, 248, 1 Senma, M., Taga, T. and Osaki, K. Chem. Let(. 1974, 1415 Kanters, J.A., van Dijk, B. and Kroon, J. Carbohydr. Res. 1991, 212, 1 Polvorinos, A.J., Contreras, R.R., Martin-Ramos, D., Romero, J. and Hidalgo, M. Carbohydr. Res. 1994, 257, 1 Brown, I.D. Acta Crystalloor. 1988, B44, 545
Appendix Table A1 H atom coordinates (× 104) and isotropic displacement coefficients (A 2 x 103) for (1) Atom
x/a
y/b
z/c
Ui,o
H1 H2 H3 H4 H5 H6S H6R HO1 HO3
-2450(10) -3470(10) -2890(10) -6130(10) -4730(10) -7930(10) -7100(10) --1680(10) -3240(10)
-5840(10) --4250(10) -1860(10) -2940(10) -3150(10) -3020(10) -4510(10) --4470(10) -0600(10)
-6440(10) -7400(10) -6330(10) -6930(10) -5370(10) -5450(10) -4920(10) --5110(10) -7650(10)
36(1) 31(1) 26(1) 30(1) 32(1) 40(1) 40(1) 53(1) 34(1)
Anisotropic displacement coefficients a (A2 x 103) for (1)
Atom
U11
U22
U33
UI2
UI3
U23
C1 C2 C3 C4 C5 C6 O1 N 03 04 05 06 S O1S O2S O3S OlW O2W Na
37(1) 25(1) 26(1) 31(1) 38(1) 38(1) 39(1) 29(1) 44(1) 37(1) 29(1) 34(1) 29(1) 24(1) 45(1) 46(1) 48(1) 71(1) 38(1)
32(1) 36(1) 27(1) 28(1) 28(1) 32(1) 75(1) 36(1) 30(1) 27(1) 31(1) 42(1) 33(1) 50(1) 49(1) 26(1) 35(1) 52(1) 32(1)
37(1) 33(1) 26(1) 31(1) 31(1) 51(1) 45(1) 42(1) 28(1) 54(1) 39(1) 72(1) 34(1) 54(1) 41(1) 63(1) 68(1) 34(1) 36(1)
8(1) -2(1) 0(1) 4(1) 0(1) 3(1) - 7(1) 0(1) -2(1) 3(1) 4(1) -3(1) 5(1) 0(1) 12(1) 5(1) - 10(1) 6(1) 3(I)
5(1) 1(1) -5(1) 4(1) 15(1) 12(1) - 11(1) 6(1) 4(1) 5(1) 7(1) -2(1) 4(1) 3(1) 5(1) -2(1) 4(1) 0(1) 2(1)
12(1) -2(1) 2(1) -6(1) -2(1) 6(1) 21(1) 3(1) 8(1) -7(1) 8(1) -5(1) 4(1) 4(1) 7(1) -13(1) 2(1) -6(1) -2(I)
a The anisotropic displacement factor exponent takes the form: - 27z2(h2a*2Ull +... + 2hka*b*U12 )
Table A3
Structu~ ~ctors
h
k
l
2 4 6 8 2 4 6 8 0 2 4 8 2 6 8 0 2 4 6 8 2 4 6 0 2 4 6 2 0 4 2 4 0 2 1 2 3 4 5 6 8 0 I 2 3 4
0 0 0 0 1 1 1 1 2 2 2 2 3 3 3 4 4 4 4 4 5 5 5 6 6 6 6 7 8 8 9 9 10 10 1 1 1 1 1 1 1 2 2 2 2 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 I
10F 0
10F c
h
146 331 280 116 234 949 269 80 523 111 574 71 650 96 135 363 244 186 372 73 480 61 205 252 80 102 74 100 199 71 186 129 65 173 514 409 376 638 251 174 109 870 846 546 353 376
130 316 277 104 232 885 239 107 522 111 527 77 616 101 133 317 253 191 360 66 415 30 213 221 73 92 60 89 185 80 193 148 50 165 601 406 362 569 233 148 91 816 828 523 308 368
5 6 7 8 1 2 3 4 5 7 8 0 1 2 3 4 5 6 7 1 2 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 5 6 0 1 2 3 4 5 1 2
k
1 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 8 9 9
10F 0
10F c
206 190 159 107 258 934 356 144 360 117 53 790 234 111 92 74 71 363 72 239 82 285 156 172 141 62 409 252 137 185 142 135 72 172 130 184 76 177 61 350 84 218 143 115 69 68
210 170 153 122 205 876 370 133 346 109 42 758 237 102 84 79 70 355 69 222 81 287 152 174 133 45 379 213 117 171 141 133 84 178 123 177 60 178 68 329 77 206 141 123 52 79
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
22.3
The crystal and molecular structure of glucosamine 2-sulfate." E. A. Yates el al. Table A3 continued h
k
4 1 2 1 2 3 4 8 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 8 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 0 1 2 4 5 1 2 3 4 0 1 2 1 2
9 10 10 0 0 0 0 0
224
2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 9 9 9 9 10 10 10 1 1
1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 3 3
10F o 46 68 69 163 563 508 211 101 437 757 258 358 448 172 106 268 686 435 75 173 77 71 139 107 470 79 362 173 116 102 85 582 157 379 326 294 202 171 103 194 162 276 153 206 212 60 240 140 281 189 179 305 97 54 107 136 234 250 114 97 209 113 189 118 96 161 88 148 136 110 80 98 625 211
10F¢ 31 69 55 164 555 483 182 99 489 772 26l 318 421 160 106 248 687 454 84 190 59 59 141 108 460 60 374 150 111 84 92 531 147 359 326 289 193 157 109 178 153 267 157 220 204 56 204 120 276 176 176 295 103 63 98 136 239 242 105 106 197 117 178 110 106 159 80 137 133 111 84 102 712 204
h
k
3 4 5 6 7 0 1 2 3 4 5 6 7 8 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 ! 2 3 4 5 6 7 0 1 2 3 5 6 1 2 3 4 5 6 0 1 2 3 4 5 1 2 3 0 2 l 2 3 4 5 7 8
1 I 1 1 1 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 8 9 9 9 10 10 0 0 0 0 0 0 0
/ 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4
10F o
10Fc
302 325 342 138 68 303 588 154 416 195 122 332 113 85 287 268 246 165 205 417 77 53 251 397 105 214 99 60 172 296 98 149 188 92 182 69 214 144 216 131 202 61 391 252 57 290 67 61 216 128 99 92 252 93 210 70 159 72 100 319 240 477 54 347 197 99 244 538 141 305 176 259 131 193
258 298 314 127 60 285 566 163 414 180 111 310 109 93 265 284 271 159 194 389 89 45 235 391 89 219 89 86 179 269 97 134 187 81 190 71 205 131 209 127 199 79 370 237 36 264 52 67 191 115 100 85 250 97 216 61 166 73 100 350 226 478 27 322 195 95 283 568 131 318 161 257 132 134
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
h
k
/
l 2 3 4 5 6 7 8 1 2 4 5 6 7 8 0 1 2 3 4 5 6 7 1 2 3 4 5 7 0 ! 3 4 5 6 1 2 3 5 6 0 1 2 3 4 5 1 2 3 4 0 1 2 1 2 3 4 5 6 8 0 ! 2 3 4 6 7 8 1 2 3 4 5 6
2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 8 9 9 9 9 l0 10 10 1 1 1 1 l 1 1 2 2 2 2 2 2 2 2 3 3 3 3 3 3
4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5
10F o 112 261 391 131 158 297 116 70 157 314 94 367 152 160 52 258 222 161 76 139 191 242 73 489 302 128 120 280 88 422 76 214 159 123 56 238 195 141 65 58 246 138 199 142 93 105 75 206 64 90 136 69 54 535 258 233 298 204 136 58 220 205 283 88 323 55 172 68 334 140 263 124 253 343
10F, 120 261 385 124 150 283 105 67 155 319 83 361 158 158 36 245 225 169 90 149 187 260 76 475 294 119 109 301 93 417 87 201 151 132 65 222 211 138 61 88 243 139 210 142 87 112 78 192 61 87 136 71 60 572 283 219 299 192 127 42 220 210 283 90 335 60 158 37 321 138 281 105 260 345
h 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 4 5 1 2 3 0 1 3 5 7
k 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 9 9 9 0 0 0 0 0
/ 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
10F o
10b
7(1 166 401 102 163 79 322 177 101 504 181 54 137 163 88 66 78 287 173 71 218 76 171 322 172 291 75 102 41 178 98 215 120 63 213 104 114 287 711 60 667 101 223 236 248 211 350 301 144 426 323 838 458 163 2O3 153 115 217 228 45t 138 312 172 49 253 133 118 97 196 137 331 275 91 237
79 171 392 97 182 8l 343 167 103 502 t59 55 147 162 105 80 71 281 173 64 230 69 177 315 166 291 76 1(~) 56 175 88 211 117 66 195 95 118 321 744 49 642 99 244 244 249 213 347 31)9 143 431 353 876 462 151 193 150 123 223 246 477 131 327 176 46 254 130 128 105 186 138 337 267 101 232
The crystal and molecular structure of glucosamine 2-suffate: E. A: Yates et al. Table A3 continued h
k
1
5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 0 2 3 4 1 2 3 0 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 1 2 3 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 4 5 6 1 4 5 0 1 2 3 4 1 2
5 5 5 6 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 9 9 9 10 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 6 7 7 7 8 8 8 8 8 9 9
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7
10F o 185 170 97 457 49 151 129 353 94 96 173 307 59 100 96 78 185 156 88 125 103 121 64 429 201 327 204 284 238 59 429 320 290 460 350 124 164 122 197 481 106 165 282 155 111 241 281 105 258 275 74 264 312 80 125 129 95 158 63 207 62 185 58 113 170 174 81 94 82 112 71 146 134 87
10F= 197 176 103 469 54 156 131 380 100 93 160 307 67 102 109 76 183 173 94 118 104 116 85 477 211 332 214 284 238 54 475 349 299 491 343 108 171 121 219 495 104 163 282 155 96 245 297 112 278 293 59 269 316 74 135 134 84 161 55 212 71 193 47 122 189 182 66 78 84 106 94 137 131 92
h 3 0 2 3 4 5 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 0 1 2 3 4 6 1 2 3 4 5 0 1 2 3 4 1 2 2 3 4 5 6 7 0 1 2 3 4 5 6 7
k 9 0 0 0 0 0 0 1 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 9 9 1 1 1 1 1 1 2 2 2 2 2 2 2 2
1 7 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 9 9 9 9 9 9 9 9 9 9 9 9 9 9
10F o 98 222 137 102 379 115 86 313 79 179 262 113 81 174 473 203 155 330 82 264 161 265 180 96 95 207 183 124 87 483 169 155 281 240 117 135 128 117 134 76 202 163 • 562 204 135 166 78 59 156 273 153 109 91 236 61 180 114 60 102 93 101 119 237 199 241 106 498 368 392 236 225 124 190 58
10F c 96 241 163 98 413 115 78 312 95 207 262 116 80 165 524 203 161 338 85 250 159 284 196 100 92 201 196 126 98 500 182 144 297 243 124 140 130 115 141 79 212 . 178 572 198 147 147 82 70 160 298 156 109 112 247 35 191 111 59 104 98 97 116 242 196 237 102 533 409 407 236 210 129 192 50
h
k
1
1 2 3 4 5 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 5 1 2 3 4 5 0 1 2 3 1 0 1 2 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 7 1 2 3 4 5 6 0 1 2 3 5 6 1 2 3 4 5 6 0
3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 7 7 7 7 7 8 8 8 8 9 0 0 0 0 0 0 0 1 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 5 5 5 5 5 5 6
9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10
10F o 242 198 239 233 177 77 213 154 183 112 210 98 103 228 122 217 185 73 69 104 210 98 272 124 220 88 149 120 62 55 251 72 45 68 662 137 322 102 235 125 58 76 109 189 177 281 51 56 445 90 415 125 163 159 80 131 116 284 241 150 130 75 215 155 139 119 104 132 177 61 88 100 112 145
10F c 244 214 233 244 178 96 221 152 190 115 221 109 116 245 131 214 197 76 53 100 223 100 297 131 230 99 156 126 61 67 264 57 48 60 729 154 313 118 250 119 43 78 99 190 172 288 35 50 469 91 436 143 165 172 94 130 119 281 243 146 133 72 226 152 146 116 110 134 183 68 95 90 115 148
h 1 2 3 4 5 2 3 4 0 1 2 3 1 2 3 4 5 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 4 5 6 1 2 3 4 5 1 2 3 4 5 2 3 0 1 0 1 2 1 2 3 4 5 6 0 1 2 3 4 6 1 2 3 4 5 6 .0
k
1
6 6 6 6 6 7 7 7 8 8 8 8 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 6 6 6 6 6 7 7 8 8 0 0 0 1 1 1 1 1 1 2 2 2 2 2 2 3 3 3 3 3 3 4
10 10 10 10 10 10 10 10 10 10 10 10 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12
10F o 231 112 59 193 81 110 78 75 75 89 121 51 192 112 199 304 138 79 185 105 121 96 147 51 96 142 97 132 115 178 67 246 57 131 60 144 72 150 109 116 160 219 127 252 175 110 109 68 146 59 115 110 591 47 72 110 146 200 126 161" 69 154 293 184 94 94 135 112 101 189 95 114 67 176
Int. J. Biol. Macromol. Volume 17 Number 3 - 4 1995
10Fc 230 108 45 198 71 111 81 94 76 87 116 42 204 106 223 316 139 83 183 90 122 111 138 36 99 139 96 142 121 181 52 251 56 127 55 150 70 149 113 107 160 225 127 260 178 117 106 73 147 67 117 107 584 29 62 98 139 202 127 161 60 152 291 191 90 89 133 113 113 187 111 112 69 190
225
The crystal and molecular structure of glucosamine 2-sulfate: E. A. Yates et al. Table A3 continued h 1 3 4 5 1 2 3 5 0 1 2 3 4 1 2 3 0 1 1 2 4 5 6 0 1 2 3 4 5 6 1 2 3 4 5 0
226
k
l
4 4 4 4 5 5 5 5 6 6 6 6 6 7 7 7 8 8 1 1 1 1 l 2 2 2 2 2 2 2 3 3 3 3 3 4
12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13
10Fo 88 220 89 62 172 160 122 82 124 100 91 89 55 172 95 131 92 101 246 146 113 160 147 307 218 181 144 63 85 99 126 199 227 68 91 84
10Fc 90 221 83 56 170 151 130 73 136 107 98 94 62 169 94 140 88 101 254 149 114 160 154 308 210 184 135 47 83 96 135 205 222 73 82 73
h l 3 4 1 2 3 4 0 2 3 4 ! 2 0 l 2 3 4 1 2 3 5 0 1 2 3 4 5 1 2 3 5 0 l 2 3
k
1
4 4 4 5 5 5 5 6 6 6 6 7 7 0 0 0 0 0 1 1 1 I 2 2 2 2 2 2 3 3 3 3 4 4 4 4
13 13 13 13 13 13 13 13 13 13 13 13 13 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14
10F o 186 149 124 48 90 86 96 62 84 80 76 195 56 86 175 98 257 100 171 423 119 73 101 169 211 122 157 211 270 76 138 134 135 107 121 125
IOF~ 189 138 131 35 84 79 93 18 86 74 83 199 46 81 172 98 256 103 170 418 121 67 97 172 221 124 169 202 264 73 129 128 135 119 114 Ill
Int. J. Biol. Macromol. Volume 17 Number 3 - 4 1995
h 4 1 2 3 4 0 1 2 3 1 2 3 4 5 0 1 3 4 5 1 2 3 4 0 1 2 3 4 1 2 3 2 0 1 2 3
k
/
4 5 5 5 5 6 6 6 6 1 I I 1 I 2 2 2 2 2 3 3 3 3 4 4 4 4 4 5 5 5 6 0 0 0 0
14 14 14 14 14 14 14 14 14 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 16 16 16 16
10F o 133 102 93 167 82 133 64 63 62 303 73 52 61 141 169 126 220 173 122 168 176 84 156 188 86 77 67 64 149 124 126 68 298 121 101 289
I()F, 128 ll5 86 149 82 129 62 58 50 299 72 47 55 123 165 119 199 162 117 157 178 70 158 202 83 72 69 52 137 140 116 70 301 118 95 270
h 1 2 3 4 1 2 3 4 1 2 3 4 0 3 1 2 1 2 3 4 0 1 2 3 1 2 0 1 2 0 1 2 3 0 l 2
k 1 l 1 l 2 2 2 2 3 3 3 3 4 4 5 5 1 1 1 1 2 2 2 2 3 3 4 4 4 0 0 0 1 2 2 2
1
lOFo
10F
16 16 16 16 16 16 16 16 16 16 16 16 16 16 16 16 17 17 17 17 17 17 17 17 17 17 17 17 17 18 18 18 18 18 18 18
187 155 59 81 116 65 93 95 163 162 151 92 92 129 104 67 185 97 67 98 55 120 66 144 103 57 119 112 64 167 65 127 51 81 69 80
186 143 35 82 116 58 82 98 148 148 135 79 89 116 107 44 178 92 60 90 57 118 70 131 t04 45 125 94 50 167 73 117 52 64 55 73
Keywords: glucosamine 2-sulfate; glucosamine N-sulfate; crystal and molecular structure
Sulfated monosaccharides occur most frequently in plants and animals as building blocks of polysaccharides. These include various polysaccharides from red algae and the proteoglycan and glycosaminoglycan components (chondroitin, dermatan and keratan sulfates, heparin and heparan sulfates) of the extracellular matrix and cells of many animal tissues a 3. Of these, only heparin and heparan sulfate preparations have been shown to contain sulfated 2-amino-2-deoxy-D-glucopyranose (Dglucosamine) units. Various biological activities and affinities have been ascribed to heparin and heparan sulfates including anti-coagulant activity, angiogenesis, cell adhesion, growth factor and cell proliferation activity4 7. The extent and pattern of sulfation of D-glucosamine residues often appears to be crucial to their activities. Effects of this kind are probably best documented with regard to the anti-coagulant activity of heparin in which the active sequence has been identified as a pentasaccharide containing three D-glucosamine units of which the non-reducing terminal unit is mono-sulfated (6-sulfate), the central unit is tris-sulfated (2,3,6-sulfate) and the reducing unit is bis-sulfated * On leavefromIstitutodi StrutturisticaChimica'GiordanoGiacomello', Area della Recerca di Roma, CP 10, 1-00016 Monterotondo Stazione, Rome, Italy
0141-8130/95/$09.50 ~ 1995ElsevierScienceB.V.All rights reserved
(2,6-sulfate) 4'8. Not surprisingly, in efforts to determine the precise role of sulfate groups in these biological interactions, much time has been devoted to structural studies of the conformation, cation coordination and charge distributions of sulfate groups and the influence which these parameters have on the host molecules 4'9. The present study, in which the crystal and molecular structure of 2-sulfamino-2-deoxy-ct-D-glucopyranose (1) is reported, forms part of our ongoing studies of sulfated monosaccharides by X-ray crystallography 1° 12, The results represent part of a series of recently completed investigations in our laboratory, including those on D-glucosamine 2,3-bis-sulfate 13 and its methyl glycoside, and may help to give some insight into the structural factors that determine the important biological functions of heparin and heparan sulfates.
Experimental X-ray crystallography 2-sulfamino-2-deoxy-~-D-glucopyranose sodium salt, [~]2o= + 55 ° (c, 2.0 water), was purchased from Sigma Chemical Company. Crystals suitable for diffraction experiments were grown by slow evaporation of an aqueous propan-2-ol solution. Oscillation and Weissenberg photographs indicated an orthorhombic unit cell and
Int. J. Biol. Macromol. Volume 1 7 Number 3-4 1995
219
The crystal and molecular structure of glucosamine 2-sulfate: E. A. Yates et al. Table 1 Crystal data and details of the structural analysis of (I) Crystal size (mm) Formula Crystal system Space group Unit cell dimensions (A) a b c Volume (A3) Z Formula weight D, (mg m- 3) V (000) ,u CuK~ (cm -1)
0.10 × 0.20 × 0.20 C6H~2OsNS-Na-2H20 Orthorhombic P2,2~21 7.713111 9.390(2) 17.222(2) 1247.3(15) 4 317.24 1.689 664.0 31.10
space g r o u p P212121. A crystal (0.10 × 0.20 × 0.20 mm) was sealed in a L i n d e m a n n glass capillary tube a n d set on an E n r a f - N o n i u s C A D - 4 F diffractometer. Accurate unit cell p a r a m e t e r s were d e t e r m i n e d by a least-squares fit of 40 high 0 reflections with 27 ° < 0 < 44 °. T h e crystal d a t a are given in Table 1. T h e intensity d a t a were collected in the 0,,--20 scan mode, using nickel-filtered C u K , r a d i a t i o n up to 2 0 = 120 ° for a t o t a l of 4071 reflections of which 730 were considered weak (according to the criterion I > 3a(I)) a n d 68 were controls. Indices were in the following ranges: h, - 8 to 0; k, - 1 0 to 10; a n d l, - 19 to 19. The c o n t r o l reflection - 1 2 0 was m e a s u r e d every h o u r of e x p o s u r e time a n d the average value of the intensity of this s t a n d a r d was 1217.1 counts with a s t a n d a r d d e v i a t i o n (of the distribution) of 16.7 11.37%). L o r e n t z a n d p o l a r i z a t i o n corrections were applied, b u t no a b s o r p t i o n c o r r e c t i o n was made. The d a t a were merged using the S H E L X T L - p l u s p a c k a g e ~4 to give 869 unique reflections, of which 828 with F o > 3a(Fo) were used in the structure analysis, m e r g i n g to R = 0 . 0 5 9 . The structure was solved by direct m e t h o d s 14 which identified all the n o n - h y d r o g e n atoms, a n d the initial residual for these positions was 0.39. The structure was then refined isotropically (R =0.089, unit weights) a n d anisotropically, minimizing the function E ~ [ F o ] - [F~]) 2 where ~o= 1/a2(Fo). A t t e m p t s to locate the h y d r o g e n a t o m s were only p a r t i a l l y successful, a n d so h y d r o g e n a t o m s for 0 4 , 0 6 , N a n d the water molecules were not included in the refinement. All the r e m a i n i n g h y d r o g e n a t o m s were included in the latter stages of refinement, with fixed i s o t r o p i c t e m p e r a t u r e factors equal to the equivalent i s o t r o p i c t e m p e r a t u r e factor of their carrier atom. T h e final R was 0.057 a n d wR was 0.060. The average a n d m a x i m u m shift-to-error ratios were 0.356 a n d 0.078, respectively, a n d the final difference F o u r i e r m a p showed m a x i m u m a n d m i n i m u m peaks of 0.50 e/~-3 a n d - 0 . 3 9 e/k-3. The a t o m i c scattering factors used were those in the S H E L X T L - p l u s p a c k a g e ~* a n d are in the analytical form given in the I n t e r n a t i o n a l Tables for X-ray C r y s t a l l o g r a p h y tS. T h e final p o s i t i o n a l p a r a m e t e r s for all the n o n - h y d r o g e n a t o m s are given in Table 2 a n d the description of the internal g e o m e t r y of the molecule is shown in Table 3. The c o o r d i n a t i o n of the s o d i u m ion a n d details of the short contacts are given in Tables 4 a n d 5 respectively. The m o l e c u l a r g e o m e t r y p a r a m e t e r s were a n a l y s e d using the P A R S T p r o g r a m :6. The two p r o c h i r a l h y d r o g e n a t o m s a t t a c h e d to C6 were differentiated a c c o r d i n g to the rules p r o p o s e d b y H a n s o n ~7.
220
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
Table 2 Atomic coordinates and equivalent isotropic displacement coefficients IA21 of (11 Atom
\.'a
yh
C1 C2 C3 C4 C5 C6 O1 N 03 04 05 06 S1 O1S O2S O3S Na O1W O2W
- 0.290819) 0.2762(8) -0.3600(8) 0.5417191 -0.5425(9) -0.7224(9) 0.1826181 -0.0893(7) -0.3589(7) - 0.6068(7) -0.466317) -0.813717) -0.0274(3) 0.1616171 0.0985(7) -0.0860(7) 0.3389(4) -0.5642(8) -0.333318)
-0.4868(7) 0.3855(7) -0.2409(7) -0.2623(7) -0.3661171 -0.4003(8) -0.4433(7) -0.3689(7) -0.1575(5) -0.1282(6) -0.5000(5) -0.4877(6) -0.4366(2) 0.4221(61 0.3575(6) -0.5841161 0.2012(31 -0.3713(61 -0.2519(7)
z.'c
U~q"
-0.6275(5) 0.6952(5) -0.6772(4) -0.6473(4) -0.5800(4) -0.5502(5) 0.5682(4) -0.718214) -0.7464(3) -0.6207(4) -0.6027(3) -0.6035(4) -0.801411) 0.797114) 0.866114) -0.8010(41 -0.8826(2) 0.8878(4) - 1.019614)
0.0356(8) 0.03 ! 118) 0.0264171 0.030117t 0.0322(8) 0.040417/ 0.0531171 0.0359(8) 0.0340(8) 0.0395(8) 0.0328(7) 0.0491181 0.0322(5) 0.0427(7) 0.0448(7) 0.045116) 0./1351t61 0.0503(7) 0.0522(71
a U~4= I/3 EiXiUija*a*aiaj Table 3 Molecular geometry of (!) Bond lengths (~) C1-C2 C2-C3 C3 C4 C4-C5 C5 C6 CI O1 C2-N C3 03 Bond angles (') C1-C2-C3 C2 C3 C4 C3 C4-C5 C4-C5-C6 C2-C3-O3 C3C4 04 C4 C5-O5 C5-C606 C6-C5-O5 C5 O5-C1 O5-C1-C2 Ol CI C2
1.508(10) 1.536(91 1.507191 1.515(101 1.513(10) 1.382(10) 1.504(9) 1.426191 111.8161 110.0(6) 110.6(6) 113.5(6) 108.3(6) 108.6(5) 110.6(61 111.1(6) 106.3(61 113.1(5) 111.0(6) 109.9(61
Torsion angles C) Endocyclic O5-C1-C2 C3 CI C2 C3 C4 C2-C3-C4-C5 03 C3 C4 04 C4-C5-O5-C 1 C5 05 CI C2
53.5(8) -51.4(8) 52.7(7) -68.1(7) 60.2(7) -58.4(7)
Aminosuljate C1-C2- N S C3-C2-N S C2-N-S-O1S C2 N S O3S C2-N-S-O2S
110.6(6) 124.9(61 170.6(51 -51.7(61 70.3(6)
C4 04 C5 05 C6 06 05 C1 N-S S~O1S S-O2S S O3S 03 C3 C4 O4-C4-C5 O5-C1 O1 CI-C2-N N-C2-C3 C2-N-S N S-O1S N S O2S N S O3S O1S S O2S O2S S O3S O1S-S-O3S Exocyclic O1-CI-C2-N N C2 C3 03 C3-C4-C5-O5 04 C4~C5-C6 C4-C5-C6-O6 C5-O5 C 1 0 l O5-C5-C6-O6
1.431181 1.442(81 1.418(101 1.425191 1.638171 1.466161 1.446(61 1.457161 111.4161 108.616) 112.2161 109.9161 111.4151 118.0151 102.1131 111.3141 106.0141 111.6141 112.0141 113.4141
53.1181 63.2(7) - 56.9(7) 64.7(8) 72.0(8) 65.0(8) -49.8(8)
R e s u l t s and d i s c u s s i o n Molecular geometry A perspective view of the molecule (1) together with the n u m b e r i n g scheme is shown in Fioure 1. The o b s e r v e d b o n d lengths a n d valence angles of the p y r a n o s e ring are within the range r e p o r t e d for c a r b o h y d r a t e s 18-z°. The c o n f o r m a t i o n along the sequence C 5 - C 6 - O 6 is
The crystal and molecular structure of glucosamine 2-suffate." E. A, Yateset al. Table 4 Geometryof the sodium coordination
Type
Interatomic distance (A)
Type
Na...O3(I) Na...OS(II-a-2c) Na...O6(II-a-2c) Na...O2S(I) Na...O1W(I) Na...OZW(I)
2.385(7) 2.428(6) 2.338(7) 2.382(7) 2.362(7) 2.408(7)
O1W(I) O2S(I) O2S(I) O3(I)
Angle (°)
05(II-a-2c)...Na...06(II-a-2c) ...Na...OS(II-a-2c) ...Na...O6(II-a-2c) ...Na...OlW(I) ...Na...O2W(I)
68.5(2) 93.9(2) 98.6(2) 99.3(2) 177.0(3)
Symmetry codes: (I) x, y, z; (II) - x , 0.5+y, 0 . 5 - z
Table 5 Molecular interactions Short contacts
Distance (A)
O l W(1)...O2W(I) Ol(I) ...O6(I+ a) N(I) ...O6(I+ a) O 1S(I) ...O1W(I+ a) Ol(I) ...O2W(II- a - b) O2S(I) ...O2W(III- b - 2c) O1W(I)...O2W(III- a - b - 2c) N(I) ...O3S(IV- 2c) O3(1) ...O1S(IV- 2c) O4(I) ...O3S(IV-a- 2c) O4(I) ...O1W(IV- a - 2c)
3.096(9) 2.939(9) 3.109(9) 2.672(9) 2.984(9) 3.019(9) 2.861(9) 3.015(8) 2.787(7) 2.758(8) 2.753(8)
Symmetry codes: (I) x, y, z; (II) 0.5- x, - y , 0.5 + z; (III) 0.5 + x, 0.5- y, - z ; (IV) - x , 0.5+y, 0 . 5 - z
0-6
•C•_6
0-4 G-4 0-3
0-5
C-I 0-2S 0-1 ,-3S
Figure 1 Perspective view and atom labelling of 2-sulfamino-2-deoxyc~-o-glucopyranose (1) with thermal ellipsoids at 50% probability level
gauche--gauche (the torsion angles defined by O 5 - C 5 C6-O6 and C 4 - C 5 - C 6 - O 6 being -49.8(8) ° and 72.0(8) °, respectively), which is one of the two preferred noneclipsed orientations in the solid state for monosaccharides having the glueo configuration 21. The molecule has the
Vibrational parameters U 0 and U~o together with tables of bond lengths, valence angles and lists of structure factors have been deposited with and may be obtained from the Director, Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK.
expected 4C 1 chair conformation 22 with ring-puckering parameters 23'24 Q = 0.55(1) A, 4~= - 51(13)° and 0 = 2.9(7)°. There is no significant increase in the length of the C 2 - N bond (1.504(9)/~) when compared to 2-amino-2-deoxy-~D-glucopyranose-3-sulfate25 (1.493(7)A), 2-amino-2-deoxyfl-v-glucopyranose-6-sulfate26 (1.480(8) A), 3-a m l"no-l,6anhydro-3-deoxy-fl-o-glucopyranose27 (1.470(3)A; a slight increase), 2-amino-2,6-dideoxy-~-o-glucopyranose 6sulfonic acid 26 (1.495/~), methyl 2-amino-2,6-dideoxy-cto-glucopyranoside-6-sulfonic acid 23 (1.502(4) A) and chondrosine 19 (1.50(1)A). The H2-C2 bond is eclipsed with respect to the N-S bond in order to minimize steric interactions, and the value of the torsion angle H 2 - C 2 - N - S (9(1) °) together with that of C 2 - N - S (118.0(5) °) indicates that the nitrogen atom has sp 2 hybridization and is part of a planar system. The value of the angle C 2 - N - S (118.0(5) °) is similar to that found in the O-sulfates for the sequence C - O - S (average 119(2)o)1o 12,3o,31, and the angles between sulfamino oxygens in the sequence OiS-S-OiS (111.6(4) °, 112.0(4) ° and 113.4(4) ° compare with the average value in the O-sulfates of 113.0(1.9) °1° 12,3o,31. The angles in the sequence N - S - O i S show more variation: N - S - O 1 S (102.1(3) °) and N - S - O 3 S (106.0(4) °) are close to the values found in the sequence O - S - O i S (average 105.2(2.5)o)1o 12,29.3o, whereas N - S - O 2 S (111.3(4) °) is relatively large. The S-O2S bond length is also shorter than $431S and S-O3S (1.446(6) A compared to 1.466(6) A and 1.457(6)A). These observations suggest that the negative charge carried on the sulfate group is shared by O1S and O3S, and that S-O2S has double bond character. A similar situation was observed in the crystal structure of fl-o-glucopyranose-6-sulfate potassium salt 11. The only sulfamino group oxygen involved in coordination of the sodium ion is O2S as shown in Figure 2. The bond angles at the point of attachment defined by C 1 - C 2 - N and C 3 - C 2 - N are 109.9(6) ° and 111.4(5) ° respectively, and are comparable to those found in the non-substituted amino sugars: 109.1(4) ° and 111.5(4) ° in 2-amino-2-deoxy~t-D-glucopyranose-3-sulfate25, 108.4(5) ° and 111.0(6) ° in 2-amino-2-deoxy-/%o-glucopyranose-6-sulfate2s, 109.9(4)° and 110.6(4) ° in 2-amino-2,6-dideoxy-ct-o-glucopyranose6-sulfonic acid 26 and 108.7(2 °) and 109.6(2) ° in methyl 2amino-2,6-dideoxy-~-o-glucopyranoside-6-sulfonic acid 28.
Sodium ion coordination The sodium ion is coordinated by six oxygen atoms in an octahedral arrangement involving one ring oxygen, two water molecules, one sulfamino oxygen and .two hydroxyl oxygens. The sodium-to-oxygen distances (average 2.38(3)A) are within the range expected for six-fold coordination 32.
Int. J. Biol. Macromol. Volume 17 Number 3 - 4 1995
221
The crystal and molecular structure of glucosamine 2-sulfate. E. A. Yates et al. 0-3(')
Packin.q ./eatures
o-6L-----~-~~ ~
":
) 0-2S(0
O-IWO) O' .a-~)
O-2W(|)
Figure2 Geometry of the sodium ion coordination
~f
The crystal packing includes an extended hydrogenbonded network and is stabilized by coordination of the sodium ion (Figure 3). All of the hydroxyl and suifamino oxygens and the two water molecules are involved in this network. As we were unable to locate the hydrogen atoms attached to 04, 0 6 and N in the final difference map, we are unable to characterize the hydrogen bonding network unambiguously. Consequently, only relevant inter-atomic distances ( < 3.2 A) between putative hydrogen bond donors or acceptors are listed in TaMe 5.
Acknowledgements The authors are grateful to the Science and Engineering Research Council (E.A.Y.) and the Italian National Research Council special ad hoc programme 'Cimica Fine II' subproject 3 (D.L.) for financial support, and to the University of Leeds Computing Service for the provision of computing facilities.
d
/ /
) it I
iI I
)/t
/
)"
Figure 3 View of the unit cell of (1) along the a axis
222
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
The crystal and molecular structure of glucosamine 2-sulfate." E. A. Yates et al.
References 1 2 3 4 5 6 7 8 9 10 11 12 13
14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32
Table A2
Mackie, W. and Preston, R.D. in 'Algal Physiology and Biochemistry' (Ed W.D.P. Stewart), Blackwell, Oxford, 1974, pp 40-85 Kjellen, L. and Lindahl, U. Annu. Rev. Biochem. 1991, 60, 443 Jackson, R.L., Busch, S.J. and Cardin, A.D. Physiol. Rev. 1991, 71, 481 Van Boeckel, C.A.A. and Petitou, M. Angew. Chem. 1993, 32, 1671 Hahnenberger, R., Jackobson, A., Ansari, A., Wehler, T., Svahn, C.M. and Lindahl, U. Glycobiolooy 1993, 3, 567 Turnbull, J.E., Fernig, D., Ke, Y. and Gallagher, J.T.J. Biol. Chem. 1992, 267, 10337 Schmidt, A., Yoshida, K. and Buddecke, E. J. Biol. Chem. 1992, 267, 19242 Petitou, M., Duchaussoy, P., Lederman, I., Choay, J., Sinay, P., Jacquinet, J.-C. and Torri, G. Carbohydr. Res. 1986, 147, 221 Mulloy, B., Forster, M.J., Jones, C., Drake, A.F., Johnson, E.A. and Davies, D.B. Carbohydr. Res. 1994, 255, 151 Lamba, D., Glover, S., Mackie, W., Rashid, A., Sheldrick, B. and Perez, S. Glycobiology 1994, 4, 151 Lamba, D., Mackie, W., Sheldrick, B., Belton, P. and Tanner, S. Carbohydr. Res. 1988, 180, 183 Lamba, D., Mackie, W., Rashid, A., Sheldrick, B. and Yates, E.A. Carbohydr. Res. 1993, 241, 89 Research results presented at the Third International Symposium on Conformational Analysis of Carbohydrates and Protein/ Carbohydrate Interactions, Val Morin, Qu6bec, Canada, 24-28 July 1994 Sheldrick, G.M. 'SHELXTL-plus. Release 4.2 for Siemens R3m/V Crystallographic Research Systems', Siemens Analytical X-ray Instruments Inc, Madison, Wisconsin, USA, 1991 'International Tables for X-ray Crystallography', Kynoch Press, Birmingham, 1974, volume 4 (present distributor: Kluwer Academic Publishers, Dordrecht) Nardelli, M. Comput. Chem. 1983, 7, 95 Hanson, K.R.J. Am. Chem. Soc. 1966, 88, 2731 Allen, F.H., Kennard, O., Watson, D.G., Brammer, L., Orpen, A.G. and Taylor, R. J. Chem. Soc. Perkin Trans. II 1987, S1-S19 Allen, F.H. Acta Crystallogr. 1986, 1342, 515 Arnott, S. and Scott, W.E.J. Chem. Soc. Perkin Trans. H 1972, 324 Allen, F.H. and Fortier, S. Acta Crystallogr. 1993, !!49, 1021 Marchessault, R.H. and Perez, S. Biopolymers 1979, 18, 2369 Cremer, D. and Popple, J.A.J. Am. Chem. Soc. 1975, 97, 1354 Jeffrey, G.A. and Yates, J.H. Carbohydr. Res. 1979, 74, 319 Mackie, W., Yates, E.A. and Lamba, D. Carbohydr. Res. 1995, 266, 65-74 Vega, R., Lopez-Castro, A. and Marquez, R. Acta Crystallogr. 1986, C42, 1066 Noordik, J.H. and Jeffrey, G.A. Acta Crystallogr. 1977, B33, 403 Fernandez-Bolanos, J.G., Morales, J., Garcia, S., Dianez, M.J., Estrada, M.D., Lopez-Castro, A. and Perez, S. Carbohydr. Res. 1993, 248, 1 Senma, M., Taga, T. and Osaki, K. Chem. Let(. 1974, 1415 Kanters, J.A., van Dijk, B. and Kroon, J. Carbohydr. Res. 1991, 212, 1 Polvorinos, A.J., Contreras, R.R., Martin-Ramos, D., Romero, J. and Hidalgo, M. Carbohydr. Res. 1994, 257, 1 Brown, I.D. Acta Crystalloor. 1988, B44, 545
Appendix Table A1 H atom coordinates (× 104) and isotropic displacement coefficients (A 2 x 103) for (1) Atom
x/a
y/b
z/c
Ui,o
H1 H2 H3 H4 H5 H6S H6R HO1 HO3
-2450(10) -3470(10) -2890(10) -6130(10) -4730(10) -7930(10) -7100(10) --1680(10) -3240(10)
-5840(10) --4250(10) -1860(10) -2940(10) -3150(10) -3020(10) -4510(10) --4470(10) -0600(10)
-6440(10) -7400(10) -6330(10) -6930(10) -5370(10) -5450(10) -4920(10) --5110(10) -7650(10)
36(1) 31(1) 26(1) 30(1) 32(1) 40(1) 40(1) 53(1) 34(1)
Anisotropic displacement coefficients a (A2 x 103) for (1)
Atom
U11
U22
U33
UI2
UI3
U23
C1 C2 C3 C4 C5 C6 O1 N 03 04 05 06 S O1S O2S O3S OlW O2W Na
37(1) 25(1) 26(1) 31(1) 38(1) 38(1) 39(1) 29(1) 44(1) 37(1) 29(1) 34(1) 29(1) 24(1) 45(1) 46(1) 48(1) 71(1) 38(1)
32(1) 36(1) 27(1) 28(1) 28(1) 32(1) 75(1) 36(1) 30(1) 27(1) 31(1) 42(1) 33(1) 50(1) 49(1) 26(1) 35(1) 52(1) 32(1)
37(1) 33(1) 26(1) 31(1) 31(1) 51(1) 45(1) 42(1) 28(1) 54(1) 39(1) 72(1) 34(1) 54(1) 41(1) 63(1) 68(1) 34(1) 36(1)
8(1) -2(1) 0(1) 4(1) 0(1) 3(1) - 7(1) 0(1) -2(1) 3(1) 4(1) -3(1) 5(1) 0(1) 12(1) 5(1) - 10(1) 6(1) 3(I)
5(1) 1(1) -5(1) 4(1) 15(1) 12(1) - 11(1) 6(1) 4(1) 5(1) 7(1) -2(1) 4(1) 3(1) 5(1) -2(1) 4(1) 0(1) 2(1)
12(1) -2(1) 2(1) -6(1) -2(1) 6(1) 21(1) 3(1) 8(1) -7(1) 8(1) -5(1) 4(1) 4(1) 7(1) -13(1) 2(1) -6(1) -2(I)
a The anisotropic displacement factor exponent takes the form: - 27z2(h2a*2Ull +... + 2hka*b*U12 )
Table A3
Structu~ ~ctors
h
k
l
2 4 6 8 2 4 6 8 0 2 4 8 2 6 8 0 2 4 6 8 2 4 6 0 2 4 6 2 0 4 2 4 0 2 1 2 3 4 5 6 8 0 I 2 3 4
0 0 0 0 1 1 1 1 2 2 2 2 3 3 3 4 4 4 4 4 5 5 5 6 6 6 6 7 8 8 9 9 10 10 1 1 1 1 1 1 1 2 2 2 2 2
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 I
10F 0
10F c
h
146 331 280 116 234 949 269 80 523 111 574 71 650 96 135 363 244 186 372 73 480 61 205 252 80 102 74 100 199 71 186 129 65 173 514 409 376 638 251 174 109 870 846 546 353 376
130 316 277 104 232 885 239 107 522 111 527 77 616 101 133 317 253 191 360 66 415 30 213 221 73 92 60 89 185 80 193 148 50 165 601 406 362 569 233 148 91 816 828 523 308 368
5 6 7 8 1 2 3 4 5 7 8 0 1 2 3 4 5 6 7 1 2 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 5 6 0 1 2 3 4 5 1 2
k
1 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 8 9 9
10F 0
10F c
206 190 159 107 258 934 356 144 360 117 53 790 234 111 92 74 71 363 72 239 82 285 156 172 141 62 409 252 137 185 142 135 72 172 130 184 76 177 61 350 84 218 143 115 69 68
210 170 153 122 205 876 370 133 346 109 42 758 237 102 84 79 70 355 69 222 81 287 152 174 133 45 379 213 117 171 141 133 84 178 123 177 60 178 68 329 77 206 141 123 52 79
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
22.3
The crystal and molecular structure of glucosamine 2-sulfate." E. A. Yates el al. Table A3 continued h
k
4 1 2 1 2 3 4 8 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 8 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 0 1 2 4 5 1 2 3 4 0 1 2 1 2
9 10 10 0 0 0 0 0
224
2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 9 9 9 9 10 10 10 1 1
1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 3 3
10F o 46 68 69 163 563 508 211 101 437 757 258 358 448 172 106 268 686 435 75 173 77 71 139 107 470 79 362 173 116 102 85 582 157 379 326 294 202 171 103 194 162 276 153 206 212 60 240 140 281 189 179 305 97 54 107 136 234 250 114 97 209 113 189 118 96 161 88 148 136 110 80 98 625 211
10F¢ 31 69 55 164 555 483 182 99 489 772 26l 318 421 160 106 248 687 454 84 190 59 59 141 108 460 60 374 150 111 84 92 531 147 359 326 289 193 157 109 178 153 267 157 220 204 56 204 120 276 176 176 295 103 63 98 136 239 242 105 106 197 117 178 110 106 159 80 137 133 111 84 102 712 204
h
k
3 4 5 6 7 0 1 2 3 4 5 6 7 8 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 ! 2 3 4 5 6 7 0 1 2 3 5 6 1 2 3 4 5 6 0 1 2 3 4 5 1 2 3 0 2 l 2 3 4 5 7 8
1 I 1 1 1 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 8 9 9 9 10 10 0 0 0 0 0 0 0
/ 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4
10F o
10Fc
302 325 342 138 68 303 588 154 416 195 122 332 113 85 287 268 246 165 205 417 77 53 251 397 105 214 99 60 172 296 98 149 188 92 182 69 214 144 216 131 202 61 391 252 57 290 67 61 216 128 99 92 252 93 210 70 159 72 100 319 240 477 54 347 197 99 244 538 141 305 176 259 131 193
258 298 314 127 60 285 566 163 414 180 111 310 109 93 265 284 271 159 194 389 89 45 235 391 89 219 89 86 179 269 97 134 187 81 190 71 205 131 209 127 199 79 370 237 36 264 52 67 191 115 100 85 250 97 216 61 166 73 100 350 226 478 27 322 195 95 283 568 131 318 161 257 132 134
Int. J. Biol. Macromol. Volume 17 Number 3-4 1995
h
k
/
l 2 3 4 5 6 7 8 1 2 4 5 6 7 8 0 1 2 3 4 5 6 7 1 2 3 4 5 7 0 ! 3 4 5 6 1 2 3 5 6 0 1 2 3 4 5 1 2 3 4 0 1 2 1 2 3 4 5 6 8 0 ! 2 3 4 6 7 8 1 2 3 4 5 6
2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 8 9 9 9 9 l0 10 10 1 1 1 1 l 1 1 2 2 2 2 2 2 2 2 3 3 3 3 3 3
4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5
10F o 112 261 391 131 158 297 116 70 157 314 94 367 152 160 52 258 222 161 76 139 191 242 73 489 302 128 120 280 88 422 76 214 159 123 56 238 195 141 65 58 246 138 199 142 93 105 75 206 64 90 136 69 54 535 258 233 298 204 136 58 220 205 283 88 323 55 172 68 334 140 263 124 253 343
10F, 120 261 385 124 150 283 105 67 155 319 83 361 158 158 36 245 225 169 90 149 187 260 76 475 294 119 109 301 93 417 87 201 151 132 65 222 211 138 61 88 243 139 210 142 87 112 78 192 61 87 136 71 60 572 283 219 299 192 127 42 220 210 283 90 335 60 158 37 321 138 281 105 260 345
h 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 4 5 1 2 3 0 1 3 5 7
k 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 5 6 6 6 6 6 6 6 7 7 7 7 7 7 8 8 8 8 8 9 9 9 0 0 0 0 0
/ 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 5 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
10F o
10b
7(1 166 401 102 163 79 322 177 101 504 181 54 137 163 88 66 78 287 173 71 218 76 171 322 172 291 75 102 41 178 98 215 120 63 213 104 114 287 711 60 667 101 223 236 248 211 350 301 144 426 323 838 458 163 2O3 153 115 217 228 45t 138 312 172 49 253 133 118 97 196 137 331 275 91 237
79 171 392 97 182 8l 343 167 103 502 t59 55 147 162 105 80 71 281 173 64 230 69 177 315 166 291 76 1(~) 56 175 88 211 117 66 195 95 118 321 744 49 642 99 244 244 249 213 347 31)9 143 431 353 876 462 151 193 150 123 223 246 477 131 327 176 46 254 130 128 105 186 138 337 267 101 232
The crystal and molecular structure of glucosamine 2-suffate: E. A: Yates et al. Table A3 continued h
k
1
5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 0 2 3 4 1 2 3 0 1 2 3 4 5 6 8 0 1 2 3 4 5 6 7 1 2 3 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 4 5 6 1 4 5 0 1 2 3 4 1 2
5 5 5 6 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 9 9 9 10 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 6 7 7 7 8 8 8 8 8 9 9
6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7 7
10F o 185 170 97 457 49 151 129 353 94 96 173 307 59 100 96 78 185 156 88 125 103 121 64 429 201 327 204 284 238 59 429 320 290 460 350 124 164 122 197 481 106 165 282 155 111 241 281 105 258 275 74 264 312 80 125 129 95 158 63 207 62 185 58 113 170 174 81 94 82 112 71 146 134 87
10F= 197 176 103 469 54 156 131 380 100 93 160 307 67 102 109 76 183 173 94 118 104 116 85 477 211 332 214 284 238 54 475 349 299 491 343 108 171 121 219 495 104 163 282 155 96 245 297 112 278 293 59 269 316 74 135 134 84 161 55 212 71 193 47 122 189 182 66 78 84 106 94 137 131 92
h 3 0 2 3 4 5 7 1 2 3 4 5 6 7 0 1 2 3 4 5 6 1 2 3 4 5 6 7 0 1 2 3 4 5 6 7 1 2 3 4 5 6 0 1 2 3 4 6 1 2 3 4 5 0 1 2 3 4 1 2 2 3 4 5 6 7 0 1 2 3 4 5 6 7
k 9 0 0 0 0 0 0 1 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 3 4 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 6 7 7 7 7 7 8 8 8 8 8 9 9 1 1 1 1 1 1 2 2 2 2 2 2 2 2
1 7 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 8 9 9 9 9 9 9 9 9 9 9 9 9 9 9
10F o 98 222 137 102 379 115 86 313 79 179 262 113 81 174 473 203 155 330 82 264 161 265 180 96 95 207 183 124 87 483 169 155 281 240 117 135 128 117 134 76 202 163 • 562 204 135 166 78 59 156 273 153 109 91 236 61 180 114 60 102 93 101 119 237 199 241 106 498 368 392 236 225 124 190 58
10F c 96 241 163 98 413 115 78 312 95 207 262 116 80 165 524 203 161 338 85 250 159 284 196 100 92 201 196 126 98 500 182 144 297 243 124 140 130 115 141 79 212 . 178 572 198 147 147 82 70 160 298 156 109 112 247 35 191 111 59 104 98 97 116 242 196 237 102 533 409 407 236 210 129 192 50
h
k
1
1 2 3 4 5 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 5 1 2 3 4 5 0 1 2 3 1 0 1 2 4 5 6 7 1 2 3 4 5 6 7 0 1 2 3 4 5 7 1 2 3 4 5 6 0 1 2 3 5 6 1 2 3 4 5 6 0
3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 5 6 6 6 6 6 7 7 7 7 7 8 8 8 8 9 0 0 0 0 0 0 0 1 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 5 5 5 5 5 5 6
9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10
10F o 242 198 239 233 177 77 213 154 183 112 210 98 103 228 122 217 185 73 69 104 210 98 272 124 220 88 149 120 62 55 251 72 45 68 662 137 322 102 235 125 58 76 109 189 177 281 51 56 445 90 415 125 163 159 80 131 116 284 241 150 130 75 215 155 139 119 104 132 177 61 88 100 112 145
10F c 244 214 233 244 178 96 221 152 190 115 221 109 116 245 131 214 197 76 53 100 223 100 297 131 230 99 156 126 61 67 264 57 48 60 729 154 313 118 250 119 43 78 99 190 172 288 35 50 469 91 436 143 165 172 94 130 119 281 243 146 133 72 226 152 146 116 110 134 183 68 95 90 115 148
h 1 2 3 4 5 2 3 4 0 1 2 3 1 2 3 4 5 7 0 1 2 3 4 5 6 1 2 3 4 5 6 0 1 2 3 4 5 6 1 2 3 4 5 1 2 3 4 5 2 3 0 1 0 1 2 1 2 3 4 5 6 0 1 2 3 4 6 1 2 3 4 5 6 .0
k
1
6 6 6 6 6 7 7 7 8 8 8 8 1 1 1 1 1 1 2 2 2 2 2 2 2 3 3 3 3 3 3 4 4 4 4 4 4 4 5 5 5 5 5 6 6 6 6 6 7 7 8 8 0 0 0 1 1 1 1 1 1 2 2 2 2 2 2 3 3 3 3 3 3 4
10 10 10 10 10 10 10 10 10 10 10 10 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 11 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12
10F o 231 112 59 193 81 110 78 75 75 89 121 51 192 112 199 304 138 79 185 105 121 96 147 51 96 142 97 132 115 178 67 246 57 131 60 144 72 150 109 116 160 219 127 252 175 110 109 68 146 59 115 110 591 47 72 110 146 200 126 161" 69 154 293 184 94 94 135 112 101 189 95 114 67 176
Int. J. Biol. Macromol. Volume 17 Number 3 - 4 1995
10Fc 230 108 45 198 71 111 81 94 76 87 116 42 204 106 223 316 139 83 183 90 122 111 138 36 99 139 96 142 121 181 52 251 56 127 55 150 70 149 113 107 160 225 127 260 178 117 106 73 147 67 117 107 584 29 62 98 139 202 127 161 60 152 291 191 90 89 133 113 113 187 111 112 69 190
225
The crystal and molecular structure of glucosamine 2-sulfate: E. A. Yates et al. Table A3 continued h 1 3 4 5 1 2 3 5 0 1 2 3 4 1 2 3 0 1 1 2 4 5 6 0 1 2 3 4 5 6 1 2 3 4 5 0
226
k
l
4 4 4 4 5 5 5 5 6 6 6 6 6 7 7 7 8 8 1 1 1 1 l 2 2 2 2 2 2 2 3 3 3 3 3 4
12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 12 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13 13
10Fo 88 220 89 62 172 160 122 82 124 100 91 89 55 172 95 131 92 101 246 146 113 160 147 307 218 181 144 63 85 99 126 199 227 68 91 84
10Fc 90 221 83 56 170 151 130 73 136 107 98 94 62 169 94 140 88 101 254 149 114 160 154 308 210 184 135 47 83 96 135 205 222 73 82 73
h l 3 4 1 2 3 4 0 2 3 4 ! 2 0 l 2 3 4 1 2 3 5 0 1 2 3 4 5 1 2 3 5 0 l 2 3
k
1
4 4 4 5 5 5 5 6 6 6 6 7 7 0 0 0 0 0 1 1 1 I 2 2 2 2 2 2 3 3 3 3 4 4 4 4
13 13 13 13 13 13 13 13 13 13 13 13 13 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14 14
10F o 186 149 124 48 90 86 96 62 84 80 76 195 56 86 175 98 257 100 171 423 119 73 101 169 211 122 157 211 270 76 138 134 135 107 121 125
IOF~ 189 138 131 35 84 79 93 18 86 74 83 199 46 81 172 98 256 103 170 418 121 67 97 172 221 124 169 202 264 73 129 128 135 119 114 Ill
Int. J. Biol. Macromol. Volume 17 Number 3 - 4 1995
h 4 1 2 3 4 0 1 2 3 1 2 3 4 5 0 1 3 4 5 1 2 3 4 0 1 2 3 4 1 2 3 2 0 1 2 3
k
/
4 5 5 5 5 6 6 6 6 1 I I 1 I 2 2 2 2 2 3 3 3 3 4 4 4 4 4 5 5 5 6 0 0 0 0
14 14 14 14 14 14 14 14 14 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 15 16 16 16 16
10F o 133 102 93 167 82 133 64 63 62 303 73 52 61 141 169 126 220 173 122 168 176 84 156 188 86 77 67 64 149 124 126 68 298 121 101 289
I()F, 128 ll5 86 149 82 129 62 58 50 299 72 47 55 123 165 119 199 162 117 157 178 70 158 202 83 72 69 52 137 140 116 70 301 118 95 270
h 1 2 3 4 1 2 3 4 1 2 3 4 0 3 1 2 1 2 3 4 0 1 2 3 1 2 0 1 2 0 1 2 3 0 l 2
k 1 l 1 l 2 2 2 2 3 3 3 3 4 4 5 5 1 1 1 1 2 2 2 2 3 3 4 4 4 0 0 0 1 2 2 2
1
lOFo
10F
16 16 16 16 16 16 16 16 16 16 16 16 16 16 16 16 17 17 17 17 17 17 17 17 17 17 17 17 17 18 18 18 18 18 18 18
187 155 59 81 116 65 93 95 163 162 151 92 92 129 104 67 185 97 67 98 55 120 66 144 103 57 119 112 64 167 65 127 51 81 69 80
186 143 35 82 116 58 82 98 148 148 135 79 89 116 107 44 178 92 60 90 57 118 70 131 t04 45 125 94 50 167 73 117 52 64 55 73