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J. Biol. Chem., Vol. 279, Issue 29, 30440-30448, July 16, 2004

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Loss of srf-3-encoded Nucleotide Sugar Transporter Activity in Caenorhabditis elegans Alters Surface Antigenicity and Prevents Bacterial Adherence^*

From the ^aABI/Molecular Neurogenetics, Ludwig-Maximilians University, 80336 Munich, Germany, ^bInstitute for Biology III, Bioinformatics and Molecular Genetics, 79104 Freiburg, Germany, the ^dDepartment of Molecular and Cell Biology, Boston University School of Dental Medicine, Boston, Massachusetts 02118, the ^eGenetics Unit, Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, United Kingdom, the ^fDepartment of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, Massachusetts 01609, and the ^gDepartment of Microbiology, University of Alabama at Birmingham, Birmingham, Alabama 35294-2170

During the establishment of a bacterial infection, the surface molecules of the host organism are of particular importance, since they mediate the first contact with the pathogen. In Caenorhabditis elegans, mutations in the srf-3 locus confer resistance to infection by Microbacterium nematophilum, and they also prevent biofilm formation by Yersinia pseudotuberculosis, a close relative of the bubonic plague agent Yersinia pestis. We cloned srf-3 and found that it encodes a multitransmembrane hydrophobic protein resembling nucleotide sugar transporters of the Golgi apparatus membrane. srf-3 is exclusively expressed in secretory cells, consistent with its proposed function in cuticle/surface modification. We demonstrate that SRF-3 can function as a nucleotide sugar transporter in heterologous in vitro and in vivo systems. UDP-galactose and UDP-N-acetylglucosamine are substrates for SRF-3. We propose that the inability of Yersinia biofilms and M. nematophilum to adhere to the nematode cuticle is due to an altered glycoconjugate surface composition of the srf-3 mutant.

Received for publication, March 3, 2004 , and in revised form, April 29, 2004.

^* Work in the laboratory of C. B. H. and P. B. was supported in part by National Institutes of Health (NIH) Grant RO1 GM 30365. Work in the Hodgkin laboratory was supported by the United Kingdom Medical Research Council. Work in the laboratory of R. B. was funded by the Friedrich-Baur-Stiftung, the VERUM Foundation, the Fonds der Chemischen Industrie, and the European Community. 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 an additional figure.

^c Supported by a travel grant from Boehringer Ingelheim Foundation.

^h Supported by institutional development funds of the University of Alabama at Birmingham.

ⁱ Supported in part by NIH Grant R15 AI 37768.

^j To whom correspondence should be addressed: Bio3/Bioinformatics and Molecular Genetics, Schaenzlestr. 1, D-79104 Freiburg (Brsg.), Germany. Tel.: 49-761-203-2786; Fax: 49-761-203-2860; E-mail: baumeister{at}celegans.de.

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