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Glycobiology Advance Access originally published online on December 12, 2005
Glycobiology 2006 16(4):343-348; doi:10.1093/glycob/cwj070
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© The Author 2005. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Observation of a unique pattern of bifurcated hydrogen bonds in the crystal structures of the N-glycoprotein linkage region models

Duraikkannu Loganathan1 and Udayanath Aich

Department of Chemistry, Indian Institute of Technology Madras, Chennai 600036, Tamil Nadu, India

1 To whom correspondence should be addressed; e-mail: loganath{at}iitm.ac.in

Received on October 21, 2005; revised on November 29, 2005; accepted on December 9, 2005


   Abstract
Top
 Abstract
Introduction
 Results and Discussion
 Materials and Methods
 Acknowledgments
 References
 
Elucidation of the intra- and intermolecular carbohydrate–protein interactions would greatly contribute toward obtaining a better understanding of the structure–function correlations of the protein-linked glycans. The weak interactions involving C–H...O have recently been attracting immense attention in the domain of biomolecular recognition. However, there has been no report so far on the occurrence of C–H...O hydrogen bonds in the crystal structures of models and analogs of N-glycoproteins. We present herein an analysis of C–H...O interactions in the crystal structures of all N-glycoprotein linkage region models and analogs. The study reveals a cooperative network of bifurcated hydrogen bonds consisting of N–H...O and C–H...O interactions seen uniquely for the models. The cooperative network consists of two antiparallel chains of bifurcated hydrogen bonds, one involving N1–H, C2'–H and O1' of the aglycon moiety and the other involving N2–H, C1–H and O1'' of the sugar. Such bifurcated hydrogen bonds between the core glycan and protein are likely to play an important role in the folding and stabilization of proteins.

Key words: carbohydrates / C–H...O interactions / H bonding / N-glycoprotein models and analogs / X-ray diffraction


   Introduction
Top
 Abstract
 Introduction
Results and Discussion
 Materials and Methods
 Acknowledgments
 References
 
The oligosaccharide components of glycoproteins play key roles in many extracellular as well as intracellular processes as recognition determinants and modulators of intrinsic properties, including folding and stability, of proteins (Varki et al., 1999Go). Owing to their structural complexity, microheterogeneity, flexibility, and non-availability in sufficient amounts, understanding the structure–function correlations of the protein-linked glycans is indeed a challenging problem in glycobiology. The linkage region constituents, GlcNAc and Asn, are conserved in the N-glycoproteins of all eukaryotes, and interestingly Gln, a single carbon homolog of Asn, has not been found to be glycosylated in nature (Spiro, 2002Go). Elucidation of the conformation of the N-glycoprotein linkage region and the molecular basis of intramolecular glycan–protein interactions is of fundamental importance considering that (a) motion of the GlcNAc–Asn linkage can profoundly influence the presentation of the glycan chains on the cell surface and (b) the protein folding and quality-control mechanisms depend on the precise location of the N-glycosylation sites.

The crystallization of glycoproteins remains a formidable task and even among the crystal structures of glycoproteins reported, most often part or all of the glycan chain is not observed in the high-resolution electron density map (Imberty and Perez, 1995Go; Petrescu et al., 2004Go). The statistical analysis of N-glycosidic linkages in 26 glycoproteins revealed that the rotomer distribution of the Asn side chains conformed to that observed on non-glycosylated structures (Imberty and Perez, 1995Go). The protein–glycan interactions were characterized by some hydrogen bonds. In particular, the N-linked GlcNAc was observed to interact through O6 and N2, both acting as donors, with the side chains of amino acids surrounding the linkage region. Recent analysis of N-glycosylation sites in 506 glycoprotein crystal structures showed that glycosylation altered the Asn side chain torsion angle distribution and reduced its flexibility (Petrescu et al., 2004Go). In globular proteins, the N-linked GlcNAc residue was found to be in contact with the protein surface. In many cases, the Asn and core glycan residue(s) were seen to fill a groove and to make extensive contacts with the protein surface.

Structural investigation using well-defined model compounds of N-glycoproteins is a valuable approach to obtain the finer details of atomic architecture and molecular recognition and also to understand the effect of structural variation on the linkage region conformation. A major program of our research based on this approach is focused on X-ray crystallographic investigation of N-glycoprotein linkage region models and analogs. Our recent crystallographic examination (Lakshmanan et al., 2003Go) of several ß-1-N-acylamidoglycopyranose derivatives demonstrated, for the first time, the effect of structural variation in both the linkage region sugar and its aglycon moiety on the N-glycosidic torsion. As the structure of saccharide or aglycon moiety is varied, the torsion angle fN (O5-C1-N1-C1') sweeps a range of values deviating from that of the reference model GlcNAcßNHAc.1H2O (1) (Figure 1), by as much as 31.9°. In an effort to rationalize the differences in the torsion values and to obtain a better understanding of the structural significance of the linkage region constituents, we have now undertaken a comprehensive analysis of glycan assembly in the crystal structures of all N-glycoprotein models and analogs reported in literature (Delbaere, 1974Go; Ohenassien et al., 1980Go; Bush et al., 1982Go; Sriram et al., 1997Go; Sriram D, Lakshmanan T et al., 1998Go; Sriram D, Srinivasan S et al., 1998Go; Lakshmanan and Loganathan, 2001Go; Aich et al., 2003Go; Lakshmanan et al., 2003Go). We disclose herein that GlcNAcßNHAc.1H2O (1) exhibits unique antiparallel chains of hydrogen bonds involving N–H...O and C–H...O interactions, a feature shared only by GlcNAcßAsn (3) (Delbaere, 1974Go; Ohenassien et al., 1980Go) and not by any analog including GlcNAcßNHPr.1H2O (12).


Figure 1
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  		Fig. 1. Structures of N-glycoprotein linkage region models 1 and 3 and an analog 12.

 

The weak interactions involving C–H...O have been attracting immense attention in the domain of biomolecular recognition (Jeffrey and Saenger, 1991Go; Desiraju and Steiner, 1999Go). These unconventional hydrogen bonds occurring in the crystal structures of biological macromolecules are suggested to play an important role in their stabilization and function (Wahl and Sundaralingam, 1997Go). There has, however, been no report so far on the occurrence of C–H...O hydrogen bonds in the crystal structures of models and analogs of N-glycoproteins. In the present study, analysis of C–H...X (where X = O / N / Cl) interactions present in the crystal structures of 14 compounds (Figure 2) has been performed.


Figure 2
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  		Fig. 2. Chemical structures of all compounds whose X-ray data have been examined.

 


   Results and Discussion
Top
 Abstract
 Introduction
 Results and Discussion
Materials and Methods
 Acknowledgments
 References
 
Among the compounds examined, GlcNAcßNHAc.1H2O (1) (Sriram D, Lakshmanan T et al., 1998Go) represents the simplest model of the highly conserved GlcNAc–Asn linkage region. The benzamido analog of 1, namely GlcNAcßNHBz.1H2O (2) (Sriram D, Lakshmanan T et al., 1998Go), serves to evaluate the competition between {pi}–{pi} stacking and C–H...O hydrogen bonding on the molecular assembly. GlcßNHAc (5) (Sriram et al., 1997Go) and RhaßNHAc (6) (Lakshmanan et al., 2003Go) are models of GlcßAsn and RhaßAsn, respectively, of the unusual N-glycosidic linkages found in Halobacter halobium S layer glycoprotein and surface layer glycoprotein of Bacillus stearothermophillus, while LacßNHAc.2H2O (7) (Lakshmanan and Loganathan, 2001Go) is a disaccharide analog of 5. Compounds 8, 9 and 10 are ß-1-N-acetamido derivatives (Lakshmanan et al., 2003Go) of Gal, Man, and Xyl, respectively, and these sugar residues are typically linked to Ser/Thr in O-glycoproteins. The propionamido derivatives, GlcßNHPr (11) (Lakshmanan et al., 2003Go), and GlcNAcßNHPr (12) (Lakshmanan et al., 2003Go) are analogs of the respective sugar conjugates of Gln, hitherto unknown in nature. The influence of chlorine in place of the methyl group present in the propionamido analog (11) on the molecular assembly was sought to be probed by examining the crystal structures of the ß-1-N-chloroacetamido derivatives (Aich et al., 2003Go) of Glc (13) and Gal (14). A comparative analysis of hydrogen bond networks present in these 12 crystal structures reported from our laboratory with those of GlcNAcßAsn [3a, trihydrate (Delbaere, 1974Go); 3b, polyhydrate (Ohenassien et al., 1980Go)] and GlcßAsn 14, monohydrate (Delbaere, 1974Go), reported by others, was carried out.

The crystal packing of all the 14 compounds was explored by analyzing their X-ray crystallographic data using the program Mercury 1.3. Each of the short C–H...X (X = O/N/Cl) contacts was ascertained using four different geometrical parameters viz., the distance C...X representing the donor–acceptor distance (D); the distance H...X (d), the hydrogen bond distance; the C–H...X angle (q); and the H...X-C angle (f). Only those interactions for which the D values are shorter than 3.6Å and q values greater than 110° are considered as significant, and these values for compounds 1, 3, and 12 are listed in Table I. The values of D, ranging from 3.179 to 3.452Å, and q, varying from 111 to 153°, are in good agreement with those reported (Jeffrey and Saenger, 1991Go; Desiraju and Steiner, 1999Go) for C–H...O interactions in small molecules. All these three compounds display a C–H...O hydrogen bond involving the anomeric hydrogen, whereas the one involving C2'–H of the aglycon moiety is observed only in 1 and 3 and not in the propionamide analog, 12. A combined examination of these C–H...O interactions along with the N–H...O hydrogen bonds reveals the unique cooperative network (Figures 3 and 4). In the crystal structures of 1 and 3, each of the amido oxygen atoms O1' and O1'' accepts the donation of two hydrogens from N1–H and C2'–H and N2–H and C1–H, respectively. This results in antiparallel chains of bifurcated hydrogen bonds extending infinitely to serve as double-reinforced pillars that stabilize the molecular architecture (Figures 3 and 4).


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  		Table I. Geometrical parameters for C–H...O hydrogen bonds observed in 1, 3 and 12

 

Figure 3
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  		Fig. 3. Packing diagram of GlcNAcßNHAc.1H2O (1) [P21, monoclinic]. Shown in dotted lines are the bifurcated hydrogen bonds involving N–H...O and C–H...O interactions forming a pair of antiparallel chains. H atoms attached to O are omitted for clarity.

 

Figure 4
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  		Fig. 4. Packing diagram of GlcNAcßAsn.nH2O (3b) [P21, monoclinic]. Shown in dotted lines are the bifurcated hydrogen bonds involving N–H...O and C–H...O interactions forming the same pattern as seen in Fig. 3. H atoms attached to O are omitted for clarity.

 

In sharp contrast, this unique stabilization motif is absent in 12, which exhibits only a single chain of bifurcated hydrogen bonds consisting of a C–H...O interaction involving the anomeric hydrogen (C1–H) (Figure 5). This striking difference is noteworthy considering that compound 12 is an analog of the hitherto unknown GlcNAcßGln linkage. The N–H...O and C–H...O hydrogen bonds observed for the benzamido analog, GlcNAcßNHBz.1H2O (2), are identical to those of the propionamide derivative 12 (Table II). The molecular assembly of the former is further stabilized by the complementary {pi}–{pi} interactions between the phenyl rings with a close contact of distance of 3.29Å as reported earlier (Sriram D, Lakshmanan T et al., 1998Go). Furthermore, all the other compounds 4–11 and 13–14 do not display any bifurcated hydrogen bonds involving C2'–H...O1’ and N1–H...O1’ interactions (Table II). Nevertheless, the monosaccharides 4, 5, 6, 11, and 13 derived from Glc and Rha, the residues that are known to be attached to Asn in certain bacteria, do consistently show one or more C–H...O interactions involving C2'–H of the aglycon moiety (Figures 6 and 7), revealing the propensity of the Asn side chain to engage in C–H...O interactions. Taken together, the above findings bring out the hallmark feature of the N-glycoprotein linkage region constituents GlcNAc and Asn—the double-reinforced pillars consisting of bifurcated hydrogen bonds consisting of C2'–H...O1' and N1–H...O1' and C1–H...O1'' and N2–H...O1'' interactions. Being adjacent to the electrophilic carbonyl carbon and hence acidic, C2'–H has the inherent potential to form a strong C–H...O hydrogen bond. The ready donation by the anomeric C1–H is also consistent with the earlier observation (Derewenda et al., 1995Go) that carbons adjacent to N atoms form particularly strong hydrogen bonds. Incidentally, no C–H...N interaction is noticed in any of the 14 compounds nor do the chloroacetamido compounds, 13 and 14, show any C–H...Cl hydrogen bond in the crystal.


Figure 5
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  		Fig. 5. Packing diagram of GlcNAcßNHPr.1H2O 12 [P21, monoclinic]. Shown in dotted lines are the bifurcated hydrogen bonds involving N–H...O and C–H...O interactions forming only a single chain. H atoms attached to O are omitted for clarity.

 

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  		Table II. Geometrical parameters for C–H...O hydrogen bonds observed in 2, 4–11, and 13–14

 

Figure 6
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  		Fig. 6. Packing diagram of GlcßAsn.1H2O (4) [P21, monoclinic]. Shown in dotted lines are the N–H...O and C–H...O interactions. The bifurcated type of hydrogen bond involving N1–H, C2'–H and O1' is clearly absent. H atoms attached to O are omitted for clarity.

 

Figure 7
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  		Fig. 7. Packing diagram of L-RhaßNHAc (6) [P21, monoclinic]. Shown in dotted lines are the N–H...O and C–H...O interactions. The bifurcated type of hydrogen bond involving N1–H, C2'–H and O1' is clearly absent. H atoms attached to O are omitted for clarity.

 

In conclusion, we speculate that the results of the present work have significant implications in the folding and stabilization of proteins and also in the formation of the N-glycosidic linkage, the defining event in the biosynthesis of N-glycoproteins, catalyzed by the oligosaccharyltransferase. The speculation gains credence from the recent studies based on NMR spectroscopy. First, the measurement of nuclear Overhauser effects (NOEs) for a soluble form of human CD2, a cell-surface glycoprotein on T lymphocytes and natural killer cells, revealed that the protein-proximal GlcNAc–GlcNAc disaccharide was in close contact with amino acid residues of a ß-sheet and that proper orientation of this sheet within CD2 was required for folding of the CD58-binding site (Wyss et al., 1995Go). The C–H...O hydrogen bonds are weak individually with energies ranging from 1 to 2 kcal/mol. However, the combination of N–H...O and C–H...O interactions of the type unraveled in the present work can bring about pronounced effects on the folding equilibrium and stabilization of proteins, considering the narrow margins by which tertiary folds of proteins are stabilized over the denatured state. Second, analysis of the chemical shifts and NOE intensities measured for the amino acid residues close to the glycan chain at Asn78 in the {alpha}-subunit of human chorionic gonadotropin (Erbel et al., 2000Go) has shown that GlcNAc–Asn unit shields the protein surface through interactions with predominantly hydrophobic amino acid residues. Based on the present work, one can conceive that the carbonyl oxygen atoms of the C-2 acetamido group of each GlcNAc residue of the core disaccharide and also that of the amido aglycon moiety of the N-glycoprotein linkage region are the potentially strong acceptor sites in the glycan part for the C–H donation from the hydrophobic amino acid residues of the protein part. On the other hand, C2'–H of the Asn side chain and the anomeric C1–H represent the strong donors for the acceptor oxygen atoms present in the ß-sheet or ß-turns of the protein part. Last, the proposed cis-trans (E–Z) isomerism (Peluso et al., 2002Go) of the amido aglycon moiety during the oligosaccharyltransferase catalyzed en bloc attachment of glycan chain onto the amido nitrogen atom of the Asn could be a key structural transformation process, preceding protein folding, wherein the association–dissociation dynamics of C–H...O hydrogen bonds along with N–H...O interactions between the glycan and protein parts are likely to play a important role.


   Materials and Methods
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
Acknowledgments
 References
 
Analysis of the X-ray data set
The atomic coordinates of 17 X-ray crystal structures of N-glycoprotein models and analogs were obtained from the Cambridge Structural Database (CSD, November 2004 release). The reference codes of 15 of these structures in the CSD, their crystallographic quality factors (R) and the corresponding compound codes and numbers used in the present work are as follows: CAKFAV, 2.50, GlcNAcßNHAc.1H2O, 1; CAKHIF, 3.30, GlcNAcßNHBz.1H2O, 2; BEHPIN, 5.40, GlcNAcßAsn.3H2O, 3a; ASGPRS, 6.00, GlcNAcßAsn.nH2O, 3b; BEHPOT, 7.20, GlcßAsn.1H2O, 4; RESJEE, 3.28, GlcßNHAc, 5; AVUVAO, 2.49, L-RhaßNHAc, 6; OCATAN, 2.69, LacßNHAc.2H2O, 7; AVUVIW, 3.82, GalßNHAc, 8; AVUVES, 4.02, ManßNHAc.1H2O, 9; AVUVOC, 3.86, XylßNHAc, 10; AVUTOA, 5.65, GlcßNHPr, 11; AVUTUG, 5.26, GlcNAcßNHPr.1H2O, 12; ERESAV, 4.94, GlcßNHCOCH2Cl, 13; ERESEZ, 2.64, GalßNHCOCH2Cl, 14.

All structures are based on room temperature measurements. Among 34 C–H...O contacts observed, 28 of them are bonded with dH...O < 2.7Å, four of them bonded with dH...O < 2.5Å, and two of them bonded with dH...O < 2.4Å. Among acceptor oxygen atoms involved in C–H...O contacts, 15 of them are carbonyl oxygens, 13 are hydroxyl oxygens, five are ring oxygens (O5) and only one is from water molecule. All the C–H...O contacts observed are of intermolecular hydrogen bond type. The two additional structures available in the CSD with the reference codes of BUBTIB and PUVQUS were not included in the study. The former corresponds to an anhydrous form (Bush et al., 1982Go) of compound 1 and several H atoms of both the acetamido groups are missing in the reported structure. The latter structure corresponds to the ß-1-N-benzamido-D-glucopyranose (Sriram D, Srinivasan S et al., 1998Go) that has oxygen atoms O2 and O6 disordered over two positions.


   Acknowledgments
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
 Acknowledgments
References
 
The work performed was financially supported by the Indo-French Centre for Promotion of Advanced Research (IFCPAR), New Delhi. One of us (U.A.) thanks CSIR, New Delhi for the Senior Research Fellowship. We also thank CCDC, UK for making the program Mercury 1.3 available for use.


   Footnotes
 
Dedicated to late Prof. George Alan Jeffrey


   References
Top
 Abstract
 Introduction
 Results and Discussion
 Materials and Methods
 Acknowledgments
 References
 
Aich, U., Lakshmanan, T., Varghese, B., and Loganathan, D. (2003) Crystal structure of ß-1-N-cholaracetamido derivatives of D-glucose and D-galactose. J. Carbohydr. Chem., 22, 891–901.[CrossRef]

Bush, C.A., Blumberg, K., and Brown, J.N. (1982) Crystal structure and solution conformation of, 1-N-acetyl-beta-D-glucopyranosyl amine: a model for the glycopeptide linkage. Biopolymers, 21, 1971–1977.[CrossRef][ISI][Medline]

Delbaere, L.T.J. (1974) The molecular and crystal structures of, 4-N-(2-acetamido-2-deoxy-beta-D-glucopyranosyl)-L-asparagine trihydrate and 4-N-(beta-D-glucopyranosyl)-L-asparagine monohydrate. The X-ray analysis of a carbohydrate-peptide linkage. Biochem. J., 143, 197–205.[ISI][Medline]

Derewenda, S.Z., Lee, L., and Derewenda, U. (1995) The occurrence of C–H...O hydrogen bonds in proteins. J. Mol. Biol., 252, 248–262.[CrossRef][ISI][Medline]

Desiraju, G.R. and Steiner, T. (1999) The Weak Hydrogen Bond in Structural Chemistry and Biology. Oxford University Press, New York.

Erbel, P.J., Karimi-Nejad, Y., van Kuik, J.A., Boelens, R., Kamerling, J.P., and Vliegenthart, J.F.G. (2000) Effects of the N-linked glycans on the 3D structure of the free {alpha}-subunit of human chorionic gonadotropin. Biochemistry, 39, 6012–6021.[CrossRef][Medline]

Imberty, A. and Perez, S. (1995) Stereochemistry of the N-glycosylation sites in glycoproteins. Protein Eng., 8, 699–709.[Abstract/Free Full Text]

Jeffrey, G.A. and Saenger, W. (1991) Hydrogen Bonding in Biological Structures. Springer-Verlag, New York.

Lakshmanan, T. and Loganathan, D. (2001) ß-1-N-Acetamido-(4-O-ß-D-galactopyranosyl)-D-glucopyranose dihydrate. Acta Crystallogr. C, C57, 825–826.

Lakshmanan, T., Sriram, D., Priya, K., and Loganathan, D. (2003) On the structural significance of the linkage region constituents of N-glycoproteins: an X-ray crystallographic investigation using models and analogs. Biochem. Biophys. Res. Commun., 312, 405–413.[CrossRef][ISI][Medline]

Ohenassien, J., Avenel, D., Neuman, A., and Giller-Pandraud, H.G. (1980) Structure cristalline de la 2-acetamido-1-N-(L-aspart-4-oyl)-2-desoxy-ß-D-glucopyranosylamine. Carbohydr. Res., 80, 1–13.

Peluso, S., Ufret, M.L., O’Reilly, M.K., and Imperiali, B. (2002) Neoglycopeptides as inhibitors of oligosaccharyl transferase: insight into negotiating product inhibition. Chem. Biol., 9, 1323–1328.[CrossRef][ISI][Medline]

Petrescu, A.J., Milac, A.L., Petrescu, S.M., Dwek, R.A., and Wormald, M.R. (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology, 14, 103–114.[Abstract/Free Full Text]

Spiro, R.J. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology, 12, 43R–56R.[Abstract/Free Full Text]

Sriram, D., Lakshmanan, T., Loganathan, D., and Srinivasan, S. (1998) Crystal structure of a hydrated N-glycoprotein linkage region model and its analogue: hydrogen bonding and Pi–Pi stacking driven molecular assembly. Carbohydr. Res., 309, 227–236.[CrossRef]

Sriram, D., Srinivasan, S., Priya, K., Aruna, V., and Loganathan, D. (1998) ß-1-N-benzamido-D-glucopyranose. Acta Crystallogr. C, C54, 1670–1672.[CrossRef]

Sriram, D., Srinivasan, H., Srinivasan, S., Priya, K., Vishnu Thirtha, M., and Loganathan, D. (1997) ß-1-N-acetamido-D-glucopynanose. Acta Crystallogr. C, C53, 1075–1077.[CrossRef]

Varki, A., Cummings, R., Esko, J., Freeze, H., Hart, G., and Marth, J. (1999) Essentials of Glycobiology. Cold Spring Harbor Laboratories press, Cold Spring Harbor, New York.

Wahl, M.C. and Sundaralingam, M. (1997) C–H...O hydrogen bonding in biology. Trends Biochem. Sci., 22, 97–102.[CrossRef][ISI][Medline]

Wyss, D.F., Choi, J.S., Li, J., Knoppers, M.H., Willis, K.J., Arulanandam, A.R., Smolyar, A., Reinherz, E.L., and Wagner, G. (1995) CHO structure, conformation and function of the N-linked glycan in the adhesion domain of human CD2. Science, 269, 1273–1278.[Abstract/Free Full Text]


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