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Oligosaccharide Binding Characteristics of the Molecular Chaperones Calnexin and Calreticulin

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Department of Biochemistry, University of Toronto, Toronto, Ontario M5S 1A8, Canada, Department of Biochemistry, University of Alberta, Edmonton, Alberta T6G 2S2, Canada, and Department of Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas 75235-9041
Cite this: Biochemistry 1998, 37, 10, 3480–3490
Publication Date (Web):February 18, 1998
https://doi.org/10.1021/bi972465g
Copyright © 1998 American Chemical Society

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    Abstract

    Calnexin and calreticulin are homologous molecular chaperones of the endoplasmic reticulum. Their binding to newly synthesized glycoproteins is mediated, at least in part, by a lectin site that recognizes the early N-linked oligosaccharide processing intermediate, Glc1Man9GlcNAc2. We compared the oligosaccharide binding specificities of calnexin and calreticulin in an effort to determine the basis for reported differences in their association with various glycoproteins. Using mono-, di-, and oligosaccharides to inhibit the binding of Glc1Man9GlcNAc2 to calreticulin and to a truncated, soluble form of calnexin, we show that the entire Glcα1−3Manα1−2Manα1−2Man structure, extending from the α1−3 branch point of the oligosaccharide core, is recognized by both proteins. Furthermore, analysis of the binding of monoglucosylated oligosaccharides containing progressively fewer mannose residues suggests that for both proteins the α1−6 mannose branch point of the oligosaccharide core is also essential for recognition. Consistent with their essentially identical substrate specificities, calnexin and calreticulin exhibited the same relative affinities when competing for binding to the Glc1Man9GlcNAc2 oligosaccharide. Thus, differential glycoprotein binding cannot be attributed to differences in the lectin specificities or binding affinities of calnexin and calreticulin. We also examined the effects of ATP, calcium, and disulfide reduction on the lectin properties of calnexin and calreticulin. Whereas oligosaccharide binding was only slightly enhanced for both proteins in the presence of high concentrations of a number of adenosine nucleotides, removal of bound calcium abrogated oligosaccharide binding, an effect that was largely reversible upon readdition of calcium. Disulfide reduction had no effect on oligosaccharide binding by calnexin, but binding by calreticulin was inhibited by 70%. Finally, deletion mutagenesis of calnexin and calreticulin identified a central proline-rich region characterized by two tandem repeat motifs as a segment capable of binding oligosaccharide. This segment bears no sequence homology to the carbohydrate recognition domains of other lectins.

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     This work was supported by grants from the National Cancer Institute of Canada with funds from the Canadian Cancer society (to D.B.W.), from the Medical Research Council of Canada (to M.M.), and from the NIH (Grant GM38545) and the Welch Foundation (Grant I-1168) (to M.A.L.). A.V. is the recipient of a Steve Fonyo Studentship from the National Cancer Institute of Canada. M.M. is a Medical Research Council of Canada Scientist and Senior Scholar of the Alberta Heritage Foundation for Medical Research.

     University of Toronto.

    §

     University of Alberta.

     University of Texas Southwestern Medical Center.

    *

     To whom correspondence should be addressed:  Department of Biochemistry, Medical Sciences Building, University of Toronto, Toronto, Ontario M5S 1A8, Canada. Tel (416) 978-2546; Fax (416) 978-8548; e-mail [email protected].

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