Conformations in polysaccharides and complex carbohydrates

Proc. Int. Symp. Biomol. Struct. Interactions, Supp. J. Biosci.,Vol. 8, Nos 1 & 2, August 1985, pp. 375–387 © Printed in India.

Conformations in polysaccharides and complex carbohydrates

EDWARD ATKINS

H H Wills Physics Laboratory, University of Bristol, Tyndall Avenue, Bristol BS8 1TL, U.K Abstract. A review is presented focussing attention on the structural molecular biology ofpolysaccharides and complex carbohydrates, using examples obtained from terraqueous plants, animals, bacteria and insects The type and sequence of the condensation linkages in polysaccharides dominate their conformation, flexibility and interactions The extensive variety of geometries is overlaid by the constituent saccharide units themselves, decoration by side appendages and post-polymerisation chemical and structural modification X-ray diffraction information from oriented samples and computerised modelling has been used to analyse molecular conformation and geometry In general the relationship between glycosidiclinkage geometry and conformation for the chemically simpler polysaccharides is understood In the case of more complex carbohydrates, unique solutions using diffraction methods alone are harder to establish In mixed protein carbohydrate systems, such as the glycoprotein antifreezes and protein-polysaccharide fibrous composites in insect cuticle, novel features in structure, morphology and interactions can usefully be explored and examined. Keywords. Conformation; polysaccharides; carbohydrates; X-ray diffraction; computer modelling.

Introduction Carbohydrate molecules are ubiquitous in nature. The structure and textures of terraqueous plants are dominated by polysaccharides such as cellulose, mannan, alginate and xylans Chitin plays a major role in the structure and organisation of insect cuticle, usually blending with globular proteins and often interacting with crystalline inorganic salts in an analogous manner to the calcification of collagen in bone In animal tissues carbohydrate substances, for example: hyaluronic acid, chondroitin and dermatan sulphates, function as lubricants, gels and compliant matrices and provide viscoelastic properties; their polyelectrolytic character promotes conformational variations in the presence of different cations and changes in ionic strength Many bacteria are encapsulated with a swollen polysaccharide network; particular species often exhibiting a variety of serotypes, each with a signature in the form of a precisely defined covalent structure These polysaccharides can be harvested on an industrial scale by continuous fermentation procedures to produce commercially valuable emulsifiers and gelling agents for food products In many instances carbohydrates are covalently attached to proteins to form proteoglycans and glycoproteins and which serve as vital functional operators in molecular biology The blood group substances are delineated by their carbohydrate components and cell surfaces are decorated with carbohydrate substances, for example heparan sulphate, which influences cell adhesion and recognition The polysaccharide heparin suppresses blood clotting and certain glycoproteins act as antifreeze agents in the blood of polar fish. These examples highlight part of the spectrum of occurrences, properties and functions of carbohydrate polymers

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Unlike their protein counterparts the carbohydrate molecules exhibit a variety of condensation linkages When this extra dimension of glycosidic linkage geometry is coupled with a variable sequence of saccharides, chosen from a reservoir of some 30–40 different saccharide monomers, a wonderful world of shapes and architectures is generated. This bewildering array of geometries is sometimes overlaid and further enhanced and embroidered by post-polymerisation alterations in chemistry and structure. A description of some examples is presented in an attempt to illustrate the differences in geometry and to indicate the current level of our understanding.

Conformational changes as a function of glycosidic linkage geometry The common constituent of plants is cellulose, a linear polymer of glucose, itself a six membered ring, and contiguous glucose units are equatorially linked between atoms 1 and 4 via an oxygen atom to form the glycosidic linkage. This particular linkage geometry generates a rather extended, gently undulating ribbon-like polymer with two- fold symmetry and which usually interacts with adjacent parallel chains to form hydrogen bonded sheets These sheets stack to form three-dimensional crystallites (figure 1 a) The structure of cellulose, or 1e–4e* linked polyglucose, exhibits features analogous to the classical β-structures found in proteins, in particular the fibrous silks Bundles of cellulose chains with this crystal structure form microfibrils with diameters about 20 nm which are the morphological units in plant cell wall, usually surrounded by a less organised matrix of cellulose, xyloglucans or mixtures of other carbohydrate constituents to create a composite material with desirable, biological, biochemical and physical properties.

A constituent of starch is amylose which is another polyglucose macromolecule but in this case linked 1 a-4e Although the glycosidic linkage occurs again through the 1 and 4 positions of contiguous glucose rings the axial disposition of one bond (at position 1) has a dramatic effect on the local stereochemistry and polymer conformation Figure lb illustrates the geometry of a polymorph of amylose crystallized from starch The polysaccharide chain traces out a hollow helical tube-like structure which is stabilised by intra-chain hydrogen bonding between successive turns of the six-fold helix This structure has many similarities to the commonly occurring α-helix in proteins. These self stabilising amylose tubes do not favour such strong interchain associations as is evident in cellulose and an entirely different texture and pattern of behaviour is observed and understood in terms of the- differences in molecular conformation.

A third example in this theme is provided by an extracellular microbial polysaccharide which is used as a gelling agent in food and known as curdlan This polymer is a le–3e linked polyglucose The molecule consists of three parallel chains twisting inunison around a common axis The result is a three-strand, solid rope-like molecule with the individual chains fitting neatly together as illustrated in figure 1c. A triad of interchain hydrogen bonds occurs along the core of the molecule at approximately 0·3 nm intervals yielding a very stable structure. This structure bears a striking architectural resemblance to the protein collagen.

* The symbols a and e refer to axially disposed and equatorally disposed bonds.

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Figure 1. Three forms of polyglucose(A). Cellulose, 1e–4e linked polyglucose is a gentle undulating ribbon-like polymer (see forexample Gardner and Blackwell, 1974) The conformation is similar to the ß-conformation inprotein. (B)Amylose, 1a–4e linked polyglucose in the V form is a hollow helical tube (see for examplethe work of Sarko (1975)) The conformation is stabilised by intrachain hydrogen bonds and issimilar to the α-helix in proteins.(C) curdlan, 1e–3e linked polyglucose forms a triple stranded rope (see for example Fulton andAtkins, 1980) The conformation bears a striking resemblance to the protein collagen

In these three examples the saccharide component has remained unchanged andrelatively straightforward (i.e. glucose) so that attention can be directed to and focussed on the importance of glycosidic linkage geometry and its relationship to polysaccharide structure It is interesting to note in passing that just examining three types of polyglucose, and there are more (e.g. dextran, linked through 1 and 6), carbohydrate polymers have already minimiced the three commonly occurring regular forms of protein structure! Two features emerge from these and similar results that deserve consideration. The first is where a particular glycosidic linkage geometry is maintained while the chemistry of the saccharide units is altered Will the polymer conformation remain similar? For the 1e–4e linkage geometry (i.e. cellulose) this would appear to be the case Poly-N-acetylglucosamine (chitin), mannan, polymannuronic acid, even 1e–4e

378 Atkins linked xylan to some extent, yield similar extended conformations and patterns of behaviour (Gardner and Blackwell, 1975; Minke and Blackwell, 1978; Frei and Preston, 1968, Nieduszynski and Marchessault, 1972; Atkins et al., 1973). In the case of amylose there is unfortunately no other polysaccharide available for meaningful comparison Curdlan has a 1e–3e linked xylan counterpart, which occurs in siphoneous green algae, and which also exists as an almost identical triple-strand rope In fact the structure of the xylan was examined and elucidated first (Atkins et al., 1968; Atkins and Parker, 1969) and it was exciting to find that a change in the saccharide chemistry, from xylose to glucose, did not overrule the glycosidic linkage geometry constraints or desirability to form a rope-like macromolecule. It is worthwhile to recall that these two polysacc harides are biosynthesised in entirely different biological systems: the xylan in algae and the curdlan from bacteria, yet they develop the same complex and ingenious hierarchical structure. Similar influence of glycosodic linkage geometry on polymer conformation is evident in comparisons between the more chemically complex polysaccharides For example the connective tissue polydisaccharides hyaluronic acid, chondroitin – 4 and – 6 sulphate, and the microbial polysaccharides from pneumococ- cus type III and Klebsiella K25 all exhibit similar patterns of behaviour (Elloway et al., 1980). These polymers are all linked 1e–3e and 1e–4e in an alternating fashion althoughthe chemistry of the saccharide units changes considerably and Klebsiella K25 even has a disaccharide side appendage (figure 2). The polyelectrolytic nature of these polymersmeans that the conformation is quite sensitive to the environment and many polymorphs have been observed for these polysaccharides.

Conformations of glycoprotein antifreeze Glycoproteins found in the blood of certain species of polar fish decrease the freezing temperature of the fish sera (Feeney and Yeh, 1978; de Vries et al., 1970). A relativelylarge freezing point depression is obtained for low concentrations of the antifreeze glycoprotein (AFGP) making it more efficient than the usual colligative mechanism, i.e. a function of the molarity of salts present. AFGP has a regular primary structure consisting of a repeating tripeptide backbone of alanine-alanine-threonine. Each threonine is D-glycosylated by the disaccharide α-D-N-acetyl galactosamine (3→1)-β- D-galactose (figure 3a). In some instances alanine residues are replaced with proline(Feeney and Yeh, 1978). It is worth noting the hydrophobic nature of the polypeptide backbone which is in striking contrast to the hydrophobicity of the carbohydrate appendages. Recent experimental work has shown that AFGP molecules are adsorbed on to the surface of the ice crystals (Brown et al., 1984). A mechanism for interactionbetween ice nuclei and molecules of AFGP is expected to rely on a structural relationship between the glycoprotein in its active state and the ice/water interface The scope of the present work is to examine a number of possible conformations for the secondary structure of AFGP, based on known regular protein conformations, using computer modelling (Sansom et al., 1985a, b). Modelling procedures

Structures of AFGP were modelled and refined by Miss C. Sansom and Dr. C. Upstill


Figure 2. Projections along the helix axis of the three-fold helical conformations of themicrobial extracellilar polysaccharide from Klebsiella K25 and the animal connective tissue polysaccharides: hyaluronic acid (HA), chondroitin 4-sulphate (C4-S) and chondroitin 6- sulphate (C6-S). The backbone conformation of these four, 1e–3e followed by 1e–4e linked, polydisaccharides is almost identical.

using our implementation of the Linked-Atom-Least-Squares (LALS) system (Smith and Arnott, 1978) running on an IBM 3081 computer. AFGP structures were refined against stereochemical information, with certain geometrical constraints and restraints imposed on the conformation using Lagrange undetermined multipliers (Sansom et al., 1985b). The pyranose rings were fixed in the standard 1C4 chair conformation using coordinates derived from Arnott and Scott (1972). The coordinates of the amino acid side groups were taken from single crystal diffraction studies of the amino acids alanine and threonine (Brown and Trotter, 1955; Shoemaker et al., 1950). The conformations used for the protein backbone were taken from similar analyses of many protein structures by Fraser and MacRae (1973). Conformations

Conformations of the AFGP backbone studied were close to each of the three regular polypeptide structures found in proteins. These are the α-helix (a right-handed helix with 3·6 residues per turn), the β-chain (a helix with two residues per turn) and a left- handed helix with three residues per turn based on the structures of polyglycine II, poly(L-proline II) and related conformations (Fraser and MacRae, 1973). Implicit in our choice of conformations to study was the assumption that the glycosylation does not distort the polypeptide backbone significantly from any known regular protein conformations. This was implied by the CD studies of AFGP (Franks and Morris, 1978; Bush et al., 1981).

α-Helix: An interesting feature of this structure is the left-handed six-fold helical

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Figure 3. Α. Chemical structure of the antifreeze glycoprotein. B. Projections per- pendiction and parallel to the helix axis of the three-fold left-handed structure of AFGP. Note the disaccharide appendages form a one dimensional stack.

Symmetry of the disaccharide appendages. This symmetry arises because the repeat unit of AFGP is a tripeptide and the angle of twist per peptide in a standard α-helix is 100° (3·6 residues per turn). The angle of twist per repeat unit is an α-helical polytripeptide is therefore 300°, which of course is equivalent to – 60°, and generates six-fold helicalsymmetry of opposite chirality to the backbone.

β-Chain: The characteristic feature of the β-conformation in proteins is its two-foldsymmetry (angle of twist per residue = 180°) which generates an undulating ribbon- like structure. In proteins, either fibrous or globular, the conformation is stabilised by inter-molecular hydrogen bonds to form sheets (Fraser and MacRae, 1973). The β- chain would only be expected to form the active conformation of AFGP if stabilising attractive bonding between contiguous disaccharide appendages were present. These groups occur every 2·1 nm and are too far apart to allow any attractive interactions to form. The β-conformation is therefore unlikely to form the active structure of AFGP.

Three-fold helix: This conformation is shown in figure 3b. A noteworthy feature of thisstructure is that the disaccharide units occur along one side of the backbone. The


AFGP model based on this conformation exhibits one-dimensional stacking of the disaccharide appendages with a periodicity of 0·936 nm.

Discussion The interaction between AFGP, structured water and ice crystals, leading to the inhibition of freezing, takes place at the interface between the ice nuclei and the AFGP solution. Analysis of high resolution 1H NMR and circular dichroism (CD) data of AFGP in solution were interpreted by Franks and Morris (1978) to favour a specific peptide conformation. After estimation and subtraction of the carbohydrate contri- bution, the resulting spectra did not resemble those of either the α-helix or β-sheet conformations. More recent CD and NMR studies (Bush et al., 1981; Bush, 1984) also provide spectroscopic evidence for a regular conformation and favouring a 3-fold conformation. The lower molecular weight fractions of AFGP are known to contain appreciable fractions of proline instead of alanine (de Vries et al., 1971). Proline cannot be accommodated in either the α- or the β-conformations without disrupting the regularity of the structure. However, they occur frequently in 3-fold helical conformations (Fraser and MacRae, 1973).

The mechanism proposed for the adsorption of AFGP onto ice involves hydrogen bonding of water molecules preferentially to the strongly hydrophilic hydroxyl groups on the saccharide rings, whilst they are simultaneously repelled from the hydrophobic methyl groups on the protein backbone. The 3-fold helix conformation of AFGP can be modelled schematically as a regular one-dimensional array of alternating hydrophilic areas (the disaccharides) and the hydrophobic areas (the regions between the disaccharides). The linear nature of this structure would enable the AFGP-ice interaction to take place directly at the interface between the ice nucleus and the AFGP solution, leading to adsorption of the AFGP onto the surface of the ice nucleus. Moreover, it can be seen from a close examination of the β-fold conformation that the hydroxyl groups of the terminal galactose residue, particularly 02,03 and 04, would be accessible for hydrogen bonding to water molecules, Tait et al. (1972) has described saccharide water interactions in terms of a specific hydration model: if the saccharide residues are spatially arranged such that collinear hydrogen bonding with water is possible without undue distortion of the surrounding water-water bonding, then such hydration interactions will interfere with ice crystallization. The next nearest neighbour distances is of H2O molecules in water is 0·485 nm, which is also the spacing between equatorial hydroxyl groups off alternating carbon atoms in a pyranose ring. We are currently examining the detailed hydrogen bonding arrangements between AFGP in the 3-fold conformation and the structures of both water and ice.

Polysaccharide-protein complexes in insect cuticle

Insect cuticle needs to be a tough, resilient material – strong but not brittle and modestly compliant. Polymerie composites occur naturally and are fabricated in the synthetic polymer and plastics industries to achieve these desirable properties. Synthetic composites such as glass rods or carbon fibres immersed in epoxy resin are

382 Atkins used to produce tough, shock absorbing textures. Cracks which occur in the hard, often brittle, reinforcing rods are not transmitted throughout the composite material since the crack energy is dissipated in the rubbery matrix. A general weakness in man-made fibre reinforced composites is the relatively poor adhesion between the reinforcing fibres and the matrix which is exposed as the fibres slip relative to the matrix during mechanical stress. Examination of insect cuticle using X-ray diffraction and electron microscopy reveals that slender, precisely defined crystallites of the polysaccharide chitin are embedded in a globular protein matrix; the protein conformation chosen to be compatible with the surface topography of the chitin filament. The basic features of these polysaccharide-protein composites for the ovipositor of the ichnumon fly will be described, highlighting some of the ingenious aspects that emanate from a study of the structural molecular biology of insect cuticle. Ichnumon fly ovipositor: A typical ovipositor of the Rhyssa species is about 0·5 mmdiameter and a few centimeters long. Thin sections (~ 50 nm) of the material can beprepared by microtomy of samples supported in epoxy resin which are suitable for transmission electron microscopy. A typical cross-section is shown in figure 4a. Longitudinal sections, cut parallel to the ovipositor axis (figure 4b) confirm the chitin consists of long, slender rod-like filaments (Rudall, 1976). The chitin crystallites seen in cross section are of equal size, slightly less than 3 nm in diameter. They are not circular but show polygonal facets. Unfortunately the size of the chitin units is only marginally greater than the resolution in the image.

X-ray diffraction patterns taken of the ovipositor show a number of interesting features. First the diffractions signals in the direction perpendicular to the fibre axis, in particular the equator, are very broad indicating small crystallite size (figure 5). The

Figure 4. Transmission electron micrographs of the ovipositor with the protein matrixstained to enhance contrast. (A), Cross-section showing chitin crystallites approximately 3 nm in diameter embedded inprotein matrix. (B), Longitudinal section show the rod-like nature of the chitin crystallites.


Figure 5. X-ray fibre diffraction pattern of the ovipositor. Note the broadness of theeqiatorial diffraction signals and the two subsidiary maxima (marked with arrows) whichbelong to a set of five occurring between the origin and the 110 reflection. Note also the weakerlayer lines which emanate from the organised protein structure.

diffractions signals index on the α-chitin orthorhombic crystalline lattice (Minke and Blackwell, 1978) with dimensions a = 0·475 nm, b = 1·885 nm, c (fibre axis) = 1·032 nm. The space group is P212121 and so two chain segments, with opposite polarity, pass through the basal a b plane. The two most prominent diffraction signals are the 110, at spacing 0·46 nm, but overlaid to some extent by the 040 signal, and the 020 signal at spacing 0·45 nm (figure 6).

The low angle region is complicated by both the crystallite shape, function and the intercrystallite interference functions or superlattice (the lattice created by the array of chitin crystallites embedded in the protein matrix as seen in figure 4a). Fortunately this superlattice is rather poorly defined, with little long range order, and so diffraction signals die away at about 2 nm leaving the wide angle diffraction pattern intact. Thus no equatorial diffraction should occur between the 020 signal (at 0·95 nm) and the 110/040 doublet (at 0·46–0·48 nm). The X-ray diffraction pattern, illustrated in figure 5, shows two diffraction signals appearing in this “forbidden” region. The two peaks, with an intensity of about 1/50 of the 110 peak, are subsidiary maxima emanating from the limited number of diffracting planes in the crystallites. The observed peaks represent two of a set of five (figure 6) that derive from the strong 110 principal diffraction signal. Starting from the origin the first two peaks of this set are masked by the low angle interference function and crystallite shape function. The third is lost under the 020

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Figure 6. Schematic diagram of weighted hk0 reciprocal lattice net arising from theprecisely defined chitin crystallite outlined in figure 7.

signal and so only the fourth and fifth of the set are visible and occur between the 020 and the 110/040 composite signals. Since the number of planes diffracting is always two greater than the number of subsidiary maxima, these results argue for seven (110) (and 110) planes existing in the crystallite. Taking into account the overall size of thecrystallite from both electron microscopy and crystallite size measurements from line broadening measurements we are able to establish that each crystallite consists of 19 polysaccharide chains as illustrated in figure 7. Each of these crystallites is decorated in an organized fashion with globular protein molecules which give rise to the additional layer lines seen in figure 5. The details of association will be presented elsewhere

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Figure 7. Projection of chitin lattice along the chain direction (c) outlining the 19 chaincrystallite. The orthorhombic init cell is marked together with the 110 places (seven in all) which give rise to the five subsidiary maxima shown in figure 6.

(Atkins, E. D. T., unpublished results) and differ from the helical arrangement proposed by Black well and Weih (1980) which assumed the chitin crystallites to be cylindrical rods. However for the sake of completeness some of the reasoning is outlined as follows.

The 010 surfaces of the crystallite have a lattice of 0·475 nm between chains and 1·032 nm along the chain. The periodicity of 0·475 nm is identical to that between the hydrogen bonded chains in a pleated sheet β-structure or cross- β structure (Geddes et al., 1969). It is also evident that twice the c axis repeat of chitin is the same as three times the repeat of a β-chain (3 × 0·69 nm = 2·07 nm). Thus the lattice on the 010 surfaces of chitin can be related to a chain folded sheet of β-structure. It is thought that a considerable amount of β-structure occurs in the globular proteins in the chitin-protein composite materials and so a patch of cross -β structure on the surface as shown in

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Figure 8. Schematic diagram of a suggested structure for the globular proteins decorating the chitin crystallite. A chain folded patch on the surface is able to match with the lattice on the 010 surfaces of the chitin crystallite.

figure 8 would act as a “sticky patch” for the globular proteins to attach themselves to the chitin crystallites and the organized decoration of globular proteins on the surfaces would give rise to the integer relationship between the protein layer lines and the chitin layer lines seen in figure 5.

Acknowledgements I would like to thank my students Sheila Farnell and Clare Sansom for allowing me topresent some of their results prior to publication and the Science and Engineering Research Council for financial support.

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Conformations in polysaccharides and complex carbohydrates 387 de Vries, A. L., Vanderbeede, J. and Feeney, R. E. (1971) J. Biol. Chem., 246, 305. Elloway, H. F., Isaac, D. H. and Atkins, E. D. T. (1980) in Fiber Diffraction Methods (eds A. D. French and

K. H. Gardner) (ACS Symposium Series), 141, 429. Feeney, R. E. and Yen, Y. (1978) Adv. Protein Chem., 32, 191. Franks, F. and Morris, Ε. R. (1978) Biochim. Biophys. Acta, 540, 346. Fraser, R. D. B. and MacRae, T. P. (1973) Conformation in Fibrous Proteins, (London: Academic Press).Frei, Ε. and Preston, R. D. (1968) Proc. Roy. Soc. B, 169, 127. Fulton, W. S. and Atkins, E. D. T. (1980) in Fiber Diffraction Methods (eds A. D. French and K. H. Gardner)

(ACS Symposiim Series) 141, 385. Gardner, K. H. and Blackwell, J. (1974) Biopolymers, 13, 1975. Gardner, Κ. Η. and Blackwell, J. (1975) Biopolymers, 14, 1581. Geddes, A. J., Parker, Κ. D., Atkins, Ε. D. Τ. and Beighton, Ε. (1968) J. Mol. Biol., 32, 343. Minke, R. and Blackwell, J. (1978) J. Mol. Biol., 120, 167. Nieduszynski, I. A. and Marchessault, R. H. (1972) Can. J. Chem., 50, 2130. Rudall, K. M. (1976) in The Insect Integument (ed. Η. R. Hepburn) (New York: Elsevier) Sansom, C. E., Atkins, E. D. T. and Upstill, C. (1985a) in Gums and Stabilizers for the Food Industry 3

(eds G. O. Phillips, D. J. Wedlock and P. A. Williams) (London: Pergamon Press) (in press). Sansom, C. E., Atkins, E. D. T. and Upstill, C. (1985b) Int. J. Biol. Macromol., (in press). Sarko, A. (1975) in Structure of Fibrous Biopolymers (eds E. D. T. Atkins and A. Keller) (London:

Butterworths) p. 335. Shoemaker, D. P., Donohue, J., Schomaker, V. and Corey, R. B. (1950) J. Chem. Soc., 72, 2328. Smith, P. J. and Arnott, S. (1978) Acta Crystalogr., A343. Tait, M. J., Suggett, Α., Franks, F., Ablett, S. and Quickended, P. A. (1972) J. Solution Chem., 1, 131.

Conformations in polysaccharides and complex carbohydrates

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