X-ray crystallographic studies of unique cross-linked lattices between four isomeric biantennary oligosaccharides and soybean agglutinin

Laurence R. Olsen, Andréa Dessen, Dipti Gupta, Subramaniam Sabesan, James C. Sacchettini, Curtis F. Brewer

Research output: Contribution to journalArticle

85 Citations (Scopus)

Abstract

Soybean agglutinin (SBA) (Glycine max) is a tetrameric GalNAc/Gal- specific lectin which forms unique cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta et al. (1994) Biochemistry 33, 7495-7504]. We recently reported the X-ray crystal structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen [Dessen et al. (1995) Biochemistry 34, 4933-4942]. In order to determine the molecular basis of different carbohydrate-lectin cross-linked lattices, a comparison has been made of the X-ray crystallographic structures of SBA cross-linked with four isomeric analogs of the biantennary blood group I carbohydrate antigen. The four pentasaccharides possess the common structure of (β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3. The β-LacNAc moieties in the four carbohydrates are linked to the 2,3-, 2,4-, 3,6-, and 2,6-positions of the core Gal residue(s), respectively. The structures of all four complexes have been refined to approximately 2.4-2.8 Å. Noncovalent lattice formation in all four complexes is promoted uniquely by the bridging action of the two arms of each bivalent carbohydrate. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharides at identical sites in each monomer, with the sugar(s) cross-linking to a symmetry-related neighbor molecule. While the 2,4-, 3,6-, and 2,6- pentasaccharide complexes possess a common P6422 space group, their unit cell dimensions differ. The 2,3-pentasaccharide cross-linked complex, on the other hand, possesses the space group I4122. Thus, all four complexes are crystallographically distinct. The four cross-linking carbohydrates axe in similar conformations, possessing a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry in each lattice. In the case of the 3,6-and 2,6-pentasaccharides, the symmetry of their cross-linked lattices requires different rotamer orientations about their β(1,6) glycosidic bonds. The results demonstrate that crystal packing interactions are the molecular basis for the formation of distinct cross-linked lattices between SBA and four isomeric pentasaccharides. The present findings are discussed in terms of lectins forming unique cross-linked complexes with glycoconjugate receptors in biological systems.

Original languageEnglish (US)
Pages (from-to)15073-15080
Number of pages8
JournalBiochemistry
Volume36
Issue number49
DOIs
StatePublished - Dec 9 1997

Fingerprint

Oligosaccharides
Carbohydrates
X-Rays
X rays
Lectins
Biochemistry
Blood Group Antigens
Glycoconjugates
Biological systems
Soybeans
Sugars
Glycine
Conformations
Monomers
Crystal structure
soybean lectin
Crystals
Molecules
I-antigen
Thomsen-Friedenreich antigen

ASJC Scopus subject areas

  • Biochemistry

Cite this

X-ray crystallographic studies of unique cross-linked lattices between four isomeric biantennary oligosaccharides and soybean agglutinin. / Olsen, Laurence R.; Dessen, Andréa; Gupta, Dipti; Sabesan, Subramaniam; Sacchettini, James C.; Brewer, Curtis F.

In: Biochemistry, Vol. 36, No. 49, 09.12.1997, p. 15073-15080.

Research output: Contribution to journalArticle

Olsen, Laurence R. ; Dessen, Andréa ; Gupta, Dipti ; Sabesan, Subramaniam ; Sacchettini, James C. ; Brewer, Curtis F. / X-ray crystallographic studies of unique cross-linked lattices between four isomeric biantennary oligosaccharides and soybean agglutinin. In: Biochemistry. 1997 ; Vol. 36, No. 49. pp. 15073-15080.
@article{2756bfc125db486d807b5f2e96e8c4fe,
title = "X-ray crystallographic studies of unique cross-linked lattices between four isomeric biantennary oligosaccharides and soybean agglutinin",
abstract = "Soybean agglutinin (SBA) (Glycine max) is a tetrameric GalNAc/Gal- specific lectin which forms unique cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta et al. (1994) Biochemistry 33, 7495-7504]. We recently reported the X-ray crystal structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen [Dessen et al. (1995) Biochemistry 34, 4933-4942]. In order to determine the molecular basis of different carbohydrate-lectin cross-linked lattices, a comparison has been made of the X-ray crystallographic structures of SBA cross-linked with four isomeric analogs of the biantennary blood group I carbohydrate antigen. The four pentasaccharides possess the common structure of (β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3. The β-LacNAc moieties in the four carbohydrates are linked to the 2,3-, 2,4-, 3,6-, and 2,6-positions of the core Gal residue(s), respectively. The structures of all four complexes have been refined to approximately 2.4-2.8 {\AA}. Noncovalent lattice formation in all four complexes is promoted uniquely by the bridging action of the two arms of each bivalent carbohydrate. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharides at identical sites in each monomer, with the sugar(s) cross-linking to a symmetry-related neighbor molecule. While the 2,4-, 3,6-, and 2,6- pentasaccharide complexes possess a common P6422 space group, their unit cell dimensions differ. The 2,3-pentasaccharide cross-linked complex, on the other hand, possesses the space group I4122. Thus, all four complexes are crystallographically distinct. The four cross-linking carbohydrates axe in similar conformations, possessing a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry in each lattice. In the case of the 3,6-and 2,6-pentasaccharides, the symmetry of their cross-linked lattices requires different rotamer orientations about their β(1,6) glycosidic bonds. The results demonstrate that crystal packing interactions are the molecular basis for the formation of distinct cross-linked lattices between SBA and four isomeric pentasaccharides. The present findings are discussed in terms of lectins forming unique cross-linked complexes with glycoconjugate receptors in biological systems.",
author = "Olsen, {Laurence R.} and Andr{\'e}a Dessen and Dipti Gupta and Subramaniam Sabesan and Sacchettini, {James C.} and Brewer, {Curtis F.}",
year = "1997",
month = "12",
day = "9",
doi = "10.1021/bi971828+",
language = "English (US)",
volume = "36",
pages = "15073--15080",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "49",

}

TY - JOUR

T1 - X-ray crystallographic studies of unique cross-linked lattices between four isomeric biantennary oligosaccharides and soybean agglutinin

AU - Olsen, Laurence R.

AU - Dessen, Andréa

AU - Gupta, Dipti

AU - Sabesan, Subramaniam

AU - Sacchettini, James C.

AU - Brewer, Curtis F.

PY - 1997/12/9

Y1 - 1997/12/9

N2 - Soybean agglutinin (SBA) (Glycine max) is a tetrameric GalNAc/Gal- specific lectin which forms unique cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta et al. (1994) Biochemistry 33, 7495-7504]. We recently reported the X-ray crystal structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen [Dessen et al. (1995) Biochemistry 34, 4933-4942]. In order to determine the molecular basis of different carbohydrate-lectin cross-linked lattices, a comparison has been made of the X-ray crystallographic structures of SBA cross-linked with four isomeric analogs of the biantennary blood group I carbohydrate antigen. The four pentasaccharides possess the common structure of (β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3. The β-LacNAc moieties in the four carbohydrates are linked to the 2,3-, 2,4-, 3,6-, and 2,6-positions of the core Gal residue(s), respectively. The structures of all four complexes have been refined to approximately 2.4-2.8 Å. Noncovalent lattice formation in all four complexes is promoted uniquely by the bridging action of the two arms of each bivalent carbohydrate. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharides at identical sites in each monomer, with the sugar(s) cross-linking to a symmetry-related neighbor molecule. While the 2,4-, 3,6-, and 2,6- pentasaccharide complexes possess a common P6422 space group, their unit cell dimensions differ. The 2,3-pentasaccharide cross-linked complex, on the other hand, possesses the space group I4122. Thus, all four complexes are crystallographically distinct. The four cross-linking carbohydrates axe in similar conformations, possessing a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry in each lattice. In the case of the 3,6-and 2,6-pentasaccharides, the symmetry of their cross-linked lattices requires different rotamer orientations about their β(1,6) glycosidic bonds. The results demonstrate that crystal packing interactions are the molecular basis for the formation of distinct cross-linked lattices between SBA and four isomeric pentasaccharides. The present findings are discussed in terms of lectins forming unique cross-linked complexes with glycoconjugate receptors in biological systems.

AB - Soybean agglutinin (SBA) (Glycine max) is a tetrameric GalNAc/Gal- specific lectin which forms unique cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta et al. (1994) Biochemistry 33, 7495-7504]. We recently reported the X-ray crystal structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen [Dessen et al. (1995) Biochemistry 34, 4933-4942]. In order to determine the molecular basis of different carbohydrate-lectin cross-linked lattices, a comparison has been made of the X-ray crystallographic structures of SBA cross-linked with four isomeric analogs of the biantennary blood group I carbohydrate antigen. The four pentasaccharides possess the common structure of (β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3. The β-LacNAc moieties in the four carbohydrates are linked to the 2,3-, 2,4-, 3,6-, and 2,6-positions of the core Gal residue(s), respectively. The structures of all four complexes have been refined to approximately 2.4-2.8 Å. Noncovalent lattice formation in all four complexes is promoted uniquely by the bridging action of the two arms of each bivalent carbohydrate. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharides at identical sites in each monomer, with the sugar(s) cross-linking to a symmetry-related neighbor molecule. While the 2,4-, 3,6-, and 2,6- pentasaccharide complexes possess a common P6422 space group, their unit cell dimensions differ. The 2,3-pentasaccharide cross-linked complex, on the other hand, possesses the space group I4122. Thus, all four complexes are crystallographically distinct. The four cross-linking carbohydrates axe in similar conformations, possessing a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry in each lattice. In the case of the 3,6-and 2,6-pentasaccharides, the symmetry of their cross-linked lattices requires different rotamer orientations about their β(1,6) glycosidic bonds. The results demonstrate that crystal packing interactions are the molecular basis for the formation of distinct cross-linked lattices between SBA and four isomeric pentasaccharides. The present findings are discussed in terms of lectins forming unique cross-linked complexes with glycoconjugate receptors in biological systems.

UR - http://www.scopus.com/inward/record.url?scp=0030720932&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030720932&partnerID=8YFLogxK

U2 - 10.1021/bi971828+

DO - 10.1021/bi971828+

M3 - Article

VL - 36

SP - 15073

EP - 15080

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 49

ER -