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J. Biol. Chem., Vol. 282, Issue 12, 9127-9142, March 23, 2007

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Dynamic Developmental Elaboration of N-Linked Glycan Complexity in the Drosophila melanogaster Embryo^*

Kazuhiro Aoki, Mindy Perlman, Jae-Min Lim, Rebecca Cantu, Lance Wells^¶1, and Michael Tiemeyer^¶2

From the Complex Carbohydrate Research Center, Department of Chemistry and ^¶Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602

The structural diversity of glycoprotein N-linked oligosaccharides is determined by the expression and regulation of glycosyltransferase activities and by the availability of the appropriate acceptor/donor substrates. Cells in different tissues and in different developmental stages utilize these control points to manifest unique glycan expression patterns in response to their surroundings. The activity of a Toll-like receptor, called Tollo/Toll-8, induces a pattern of incompletely defined, but neural specific, glycan expression in the Drosophila embryo. Understanding the full extent of the changes in glycan expression that result from altered Tollo/Toll-8 signaling requires characterization of the complete N-linked glycan profile of both wild-type and mutant embryos. N-Linked glycans harvested from wild-type or mutant embryos were subjected to direct structural analysis by analytic and preparative high pressure liquid chromatography, by multidimensional mass spectrometry, and by exoglycosidase digestion, revealing a predominance of high mannose and paucimannose glycans. Di-, mono-, and nonfucosylated forms of hybrid, complex biantennary, and triantennary glycans account for 12% of the total wild-type glycan profile. Two sialylated glycans bearing N-acetylneuraminic acid were detected, the first direct demonstration of this modification in Drosophila. Glycan profiles change during normal development consistent with increasing -mannosidase II and core fucosyl-transferase enzyme activities, and with decreasing activity of the Fused lobes processing hexosaminidase. In tollo/toll-8 mutants, a dramatic, expected loss of difucosylated glycans is accompanied by unexpected decreases in monofucosylated and nonfucosylated hybrid glycans and increases in some nonfucosylated paucimannose and biantennary glycans. Therefore, tollo/toll-8 signaling influences flux through several processing steps that affect the maturation of N-linked glycans.

Received for publication, July 14, 2006 , and in revised form, January 26, 2007.

^* This work was supported by NIGMS Grant 1-R01-GM072839 from the National Institutes of Health (to M. T.), by a Toyobo Biotechnology Foundation long term research grant (to K. A.), by National Affiliate Scientific Development Grant 0535220 from the American Heart Association (to L. W.), and by Grant 4074 from the Muscular Dystrophy Association (to L. W. and M. T.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables 1-3 and Figs. 1-5.

¹ Georgia Cancer Coalition Scholar.

² To whom correspondence should be addressed: The Complex Carbohydrate Research Center, 315 Riverbend Rd., Athens, GA 30602-4712. Tel.: 706-542-2740; Fax: 706-542-4412; E-mail: mtiemeyer{at}ccrc.uga.edu.

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