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J. Biol. Chem., Vol. 280, Issue 29, 27310-27318, July 22, 2005

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Novel Class of Glycosphingolipids Involved in Male Fertility^*

Roger Sandhoff, Rudolf Geyer¶, Richard Jennemann, Claudia Paret||, Eva Kiss, Tadashi Yamashita**, Karin Gorgas, Tjeerd P. Sijmonsma, Masao Iwamori, Catherine Finaz¶¶, Richard L. Proia**, Herbert Wiegandt, and Hermann-Josef Gröne||||

From the Department of Cellular and Molecular Pathology and the ^||Department of Tumor Progression and Tumor Defense, German Cancer Research Center, INF 280, Heidelberg 69120, Germany, the ^¶Institute of Biochemistry, Faculty of Medicine, University of Giessen, Giessen 35392, Germany, the ^**Genetics of Development and Disease Branch, NIDDK, National Institutes of Health, Bethesda, Maryland 20892, Department of Anatomy and Cell Biology II, University of Heidelberg, INF 307, Heidelberg 69120, Germany, the Department of Biochemistry, Faculty of Science and Technology, Kinki University, 3-4-1 Kowakae, Higashiosaka, Osaka 577-8502, Japan, and ^¶¶INSERM U 566-CEA-University Paris 7-11, Atomic Energy Department/Radiobiology and Radiopathology Department/Laboratory of Gametogenesis, Apoptosis, and Genotoxicity, BP 6, Fontenay-aux-roses 92265, France

Mice require testicular glycosphingolipids (GSLs) for proper spermatogenesis. Mutant mice strains deficient in specific genes encoding biosynthetic enzymes of the GSL pathway including Galgt1 (encoding GM2 synthase) and Siat9 (encoding GM3 synthase) have been established lacking various overlapping subsets of GSLs. Although male Galgt1-/- mice are infertile, male Siat9-/- mice are fertile. Interestingly, GSLs thought to be essential for male spermatogenesis are not synthesized in either of these mice strains. Hence, these GSLs cannot account for the different phenotypes. A novel class of GSLs was observed composed of eight fucosylated molecules present in fertile but not in infertile mutant mice. These GSLs contain polyunsaturated very long chain fatty acid residues in their ceramide moieties. GSLs of this class are expressed differentially in testicular germ cells. More importantly, the neutral subset of this new GSL class strictly correlates with male fertility. These data implicate polyunsaturated, fucosylated GSLs as essential for spermatogenesis and male mouse fertility.

Received for publication, March 14, 2005 , and in revised form, May 24, 2005.

^* This work was supported by German Research Foundation Grants SFB 405, B10, and FG GKG 886 (to H.-J. G.) and SFB 535 and Z1 (to R. G.). 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 may be addressed. Tel.: 49-6221-424-368; Fax: 49-6221-424-352; E-mail: r.sandhoff{at}dkfz-heidelberg.de.

^|||| To whom correspondence may be addressed. Tel.: 49-6221-424-368; Fax: 49-6221-424-352; E-mail: h.-j.groene{at}dkfz.de.

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