X-ray Crystal Structure of the Soybean Agglutinin Cross-Linked with a Biantennary Analog of the Blood Group I Carbohydrate Antigen

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

Research output: Contribution to journalArticle

140 Citations (Scopus)

Abstract

Soybean agglutinin (SBA) (Glycine max), which is a tetrameric Ga1NAc/Gal-specific lectin, has recently been reported to form unique, highly organized cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta, D., Bhattacharyya, L., Fant, J., Macaluso, F., Sabesan, S., & Brewer, C. F. (1994) Biochemistry 33, 7495-7504], In order to elucidate the nature of these complexes, the X-ray crystallographic structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen is reported. The structure reveals that lattice formation is promoted uniquely by the bridging action of the bivalent pentasaccharide β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3and the β-LacNAc moieties are linked to the 2 and 6 positions of the core Gal. The structure of SBA complexed with the synthetic biantennary pentasaccharide has thus been determined by molecular replacement techniques and refined at 2.6 Å resolution to an R value of 20.1%. The crystals are hexagonal with a P6422 space group, which differs significantly from that of crystals of the free protein. In the structure, each monomeric asymmetric unit contains a Man9 oligomannose-type chain at Asn 75, with only the first two GlcNAc residues visible. The overall tertiary structure of the SBA subunit is similar to that of other legume lectins as well as certain animal lectins. However, the dimer interface in the SBA tetramer is unusual in that only one complete peptide chain is sterically permitted, thus requiring juxtapositioning of one C-terminal fragmented subunit together with an intact subunit. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharide at identical sites in each monomer, with the sugar cross-linking to a symmetry-related neighbor molecule. The cross-linking pentasaccharide is in a conformation that possesses a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry of the lattice. Hence, the symmetry properties of the bivalent oligosaccharide as well as the lectin are structural determinants of the lattice. The results are discussed in terms of multidimensional carbohydrate-lectin cross-linked complexes, as well as the signal transduction properties of multivalent lectins.

Original languageEnglish (US)
Pages (from-to)4933-4942
Number of pages10
JournalBiochemistry
Volume34
Issue number15
DOIs
StatePublished - Apr 1 1995

Fingerprint

Blood Group Antigens
Lectins
Crystal structure
X-Rays
X rays
Carbohydrates
Signal transduction
Crystals
Biochemistry
Oligosaccharides
Soybeans
Fabaceae
Sugars
Dimers
Glycine
Conformations
soybean lectin
I-antigen
Signal Transduction
Monomers

ASJC Scopus subject areas

  • Biochemistry

Cite this

X-ray Crystal Structure of the Soybean Agglutinin Cross-Linked with a Biantennary Analog of the Blood Group I Carbohydrate Antigen. / Dessen, Andréa; Sacchettini, James C.; Gupta, Dipti; Brewer, Curtis F.; Sabesan, Subramaniam.

In: Biochemistry, Vol. 34, No. 15, 01.04.1995, p. 4933-4942.

Research output: Contribution to journalArticle

Dessen, Andréa ; Sacchettini, James C. ; Gupta, Dipti ; Brewer, Curtis F. ; Sabesan, Subramaniam. / X-ray Crystal Structure of the Soybean Agglutinin Cross-Linked with a Biantennary Analog of the Blood Group I Carbohydrate Antigen. In: Biochemistry. 1995 ; Vol. 34, No. 15. pp. 4933-4942.
@article{d8c78f0b259f4734bbcfc2d2b3747879,
title = "X-ray Crystal Structure of the Soybean Agglutinin Cross-Linked with a Biantennary Analog of the Blood Group I Carbohydrate Antigen",
abstract = "Soybean agglutinin (SBA) (Glycine max), which is a tetrameric Ga1NAc/Gal-specific lectin, has recently been reported to form unique, highly organized cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta, D., Bhattacharyya, L., Fant, J., Macaluso, F., Sabesan, S., & Brewer, C. F. (1994) Biochemistry 33, 7495-7504], In order to elucidate the nature of these complexes, the X-ray crystallographic structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen is reported. The structure reveals that lattice formation is promoted uniquely by the bridging action of the bivalent pentasaccharide β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3and the β-LacNAc moieties are linked to the 2 and 6 positions of the core Gal. The structure of SBA complexed with the synthetic biantennary pentasaccharide has thus been determined by molecular replacement techniques and refined at 2.6 {\AA} resolution to an R value of 20.1{\%}. The crystals are hexagonal with a P6422 space group, which differs significantly from that of crystals of the free protein. In the structure, each monomeric asymmetric unit contains a Man9 oligomannose-type chain at Asn 75, with only the first two GlcNAc residues visible. The overall tertiary structure of the SBA subunit is similar to that of other legume lectins as well as certain animal lectins. However, the dimer interface in the SBA tetramer is unusual in that only one complete peptide chain is sterically permitted, thus requiring juxtapositioning of one C-terminal fragmented subunit together with an intact subunit. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharide at identical sites in each monomer, with the sugar cross-linking to a symmetry-related neighbor molecule. The cross-linking pentasaccharide is in a conformation that possesses a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry of the lattice. Hence, the symmetry properties of the bivalent oligosaccharide as well as the lectin are structural determinants of the lattice. The results are discussed in terms of multidimensional carbohydrate-lectin cross-linked complexes, as well as the signal transduction properties of multivalent lectins.",
author = "Andr{\'e}a Dessen and Sacchettini, {James C.} and Dipti Gupta and Brewer, {Curtis F.} and Subramaniam Sabesan",
year = "1995",
month = "4",
day = "1",
doi = "10.1021/bi00015a004",
language = "English (US)",
volume = "34",
pages = "4933--4942",
journal = "Biochemistry",
issn = "0006-2960",
publisher = "American Chemical Society",
number = "15",

}

TY - JOUR

T1 - X-ray Crystal Structure of the Soybean Agglutinin Cross-Linked with a Biantennary Analog of the Blood Group I Carbohydrate Antigen

AU - Dessen, Andréa

AU - Sacchettini, James C.

AU - Gupta, Dipti

AU - Brewer, Curtis F.

AU - Sabesan, Subramaniam

PY - 1995/4/1

Y1 - 1995/4/1

N2 - Soybean agglutinin (SBA) (Glycine max), which is a tetrameric Ga1NAc/Gal-specific lectin, has recently been reported to form unique, highly organized cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta, D., Bhattacharyya, L., Fant, J., Macaluso, F., Sabesan, S., & Brewer, C. F. (1994) Biochemistry 33, 7495-7504], In order to elucidate the nature of these complexes, the X-ray crystallographic structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen is reported. The structure reveals that lattice formation is promoted uniquely by the bridging action of the bivalent pentasaccharide β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3and the β-LacNAc moieties are linked to the 2 and 6 positions of the core Gal. The structure of SBA complexed with the synthetic biantennary pentasaccharide has thus been determined by molecular replacement techniques and refined at 2.6 Å resolution to an R value of 20.1%. The crystals are hexagonal with a P6422 space group, which differs significantly from that of crystals of the free protein. In the structure, each monomeric asymmetric unit contains a Man9 oligomannose-type chain at Asn 75, with only the first two GlcNAc residues visible. The overall tertiary structure of the SBA subunit is similar to that of other legume lectins as well as certain animal lectins. However, the dimer interface in the SBA tetramer is unusual in that only one complete peptide chain is sterically permitted, thus requiring juxtapositioning of one C-terminal fragmented subunit together with an intact subunit. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharide at identical sites in each monomer, with the sugar cross-linking to a symmetry-related neighbor molecule. The cross-linking pentasaccharide is in a conformation that possesses a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry of the lattice. Hence, the symmetry properties of the bivalent oligosaccharide as well as the lectin are structural determinants of the lattice. The results are discussed in terms of multidimensional carbohydrate-lectin cross-linked complexes, as well as the signal transduction properties of multivalent lectins.

AB - Soybean agglutinin (SBA) (Glycine max), which is a tetrameric Ga1NAc/Gal-specific lectin, has recently been reported to form unique, highly organized cross-linked complexes with a series of naturally occurring and synthetic multiantennary carbohydrates with terminal GalNAc or Gal residues [Gupta, D., Bhattacharyya, L., Fant, J., Macaluso, F., Sabesan, S., & Brewer, C. F. (1994) Biochemistry 33, 7495-7504], In order to elucidate the nature of these complexes, the X-ray crystallographic structure of SBA cross-linked with a biantennary analog of the blood group I carbohydrate antigen is reported. The structure reveals that lattice formation is promoted uniquely by the bridging action of the bivalent pentasaccharide β-LacNAc)2Gal-β-R, where R is -O(CH2)5COOCH3and the β-LacNAc moieties are linked to the 2 and 6 positions of the core Gal. The structure of SBA complexed with the synthetic biantennary pentasaccharide has thus been determined by molecular replacement techniques and refined at 2.6 Å resolution to an R value of 20.1%. The crystals are hexagonal with a P6422 space group, which differs significantly from that of crystals of the free protein. In the structure, each monomeric asymmetric unit contains a Man9 oligomannose-type chain at Asn 75, with only the first two GlcNAc residues visible. The overall tertiary structure of the SBA subunit is similar to that of other legume lectins as well as certain animal lectins. However, the dimer interface in the SBA tetramer is unusual in that only one complete peptide chain is sterically permitted, thus requiring juxtapositioning of one C-terminal fragmented subunit together with an intact subunit. Association between SBA tetramers involves binding of the terminal Gal residues of the pentasaccharide at identical sites in each monomer, with the sugar cross-linking to a symmetry-related neighbor molecule. The cross-linking pentasaccharide is in a conformation that possesses a pseudo-2-fold axis of symmetry which lies on a crystallographic 2-fold axis of symmetry of the lattice. Hence, the symmetry properties of the bivalent oligosaccharide as well as the lectin are structural determinants of the lattice. The results are discussed in terms of multidimensional carbohydrate-lectin cross-linked complexes, as well as the signal transduction properties of multivalent lectins.

UR - http://www.scopus.com/inward/record.url?scp=0028921961&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0028921961&partnerID=8YFLogxK

U2 - 10.1021/bi00015a004

DO - 10.1021/bi00015a004

M3 - Article

VL - 34

SP - 4933

EP - 4942

JO - Biochemistry

JF - Biochemistry

SN - 0006-2960

IS - 15

ER -