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Originally published In Press as doi:10.1074/jbc.M409557200 on September 27, 2004

J. Biol. Chem., Vol. 279, Issue 51, 52893-52903, December 17, 2004
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srf-3, a Mutant of Caenorhabditis elegans, Resistant to Bacterial Infection and to Biofilm Binding, Is Deficient in Glycoconjugates*

John F. Cipollo{ddagger}, Antoine M. Awad{ddagger}, Catherine E. Costello§, and Carlos B. Hirschberg{ddagger}

From the {ddagger}Department of Molecular and Cell Biology, Boston University, Goldman School of Dental Medicine, Boston, Massachusetts 02118-2526 and the §Mass Spectrometry Resource, Department of Biochemistry, Boston University School of Medicine, Boston, Massachusetts 02118-2526

srf-3 is a mutant of C. elegans that is resistant to infection by Microbacterium nematophilum and to binding of the biofilm produced by Yersinia pseudotuberculosis and Yersinia pestis. Recently, SRF-3 was characterized as a nucleotide sugar transporter of the Golgi apparatus occurring exclusively in hypodermal seam cells, pharyngeal cells, and spermatheca. Based on the above observations, we hypothesized that srf-3 may have altered glyconjugates that may enable the mutant nematode to grow unaffected in the presence of the above pathogenic bacteria. Following analyses of N- and O-linked glycoconjugates of srf-3 and wild type nematodes using a combination of enzymatic degradation, permethylation, and mass spectrometry, we found in srf-3 a 65% reduction of acidic O-linked glycoconjugates containing glucuronic acid and galactose as well as a reduction of N-linked glycoconjugates containing galactose and fucose. These results are consistent with the specificity of SRF-3 for UDP-galactose and strongly suggest that the above glycoconjugates play an important role in allowing adhesion of M. nematophilum or Y. pseudotuberculosis biofilm to wild type C. elegans. Furthermore, because seam cells as well as pharyngeal cells secrete their glycoconjugates to the cuticle and surrounding surfaces, the results also demonstrate the critical role of these cells and their secreted glycoproteins in nematode-bacteria interactions and offer a mechanistic basis for strategies to block such recognition processes.

Received for publication, August 19, 2004 , and in revised form, September 21, 2004.

* This work was supported by National Research Service Award F32 GM66486 (to J. F. C.) and National Institutes of Health Grants RO1 GM30365 (to C. B. H.) and P41 RR10888 and S10 RR15942 (to C. E. C.). 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.

To whom correspondence should be addressed: Dept. of Molecular and Cell Biology, Boston University Goldman School of Dental Medicine, 715 Albany St., Evans 437, Boston, MA 02118. Tel.: 6174141040; Fax: 6174141041; E-mail: chirschb{at}bu.edu.


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