Testis-specific sulfoglycolipid, seminolipid, is essential for germ cell function in spermatogenesis

Glycobiology

Volumn 15, Issue 6, 2005, Pages 649-654

  Zhang, Yanlong ^a,b   Hayashi, Yoshihiro ^a   Cheng, Xinyao ^b   Watanabe, Tae ^b   Wang, Xiangchun ^b   Taniguchi, Naoyuki ^b   Honke, Koichi ^a,c  

^a KOCHI MEDICAL SCHOOL   (Japan)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cereboroside sulfotransferase; Germ cell transplantation; Green flourescent protein; Knockout mouse; Testis

Indexed keywords

GLYCEROGLYCOLIPID; GLYCOLIPID; GREEN FLUORESCENT PROTEIN; SEMINOLIPID; SULFATIDE; SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL CULTURE; CELL FUNCTION; CELL MEMBRANE; CONTROLLED STUDY; CST GENE; GENE; GERM CELL; GOLGI COMPLEX; IMMUNOHISTOCHEMISTRY; MALE; MALE INFERTILITY; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; SULFATION; TESTIS;

ANIMALS; GERM CELLS; GLYCOLIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SEMINIFEROUS TUBULES; SERTOLI CELLS; SPERMATOGENESIS; STEM CELL TRANSPLANTATION; SULFOTRANSFERASES; TESTIS;

MAMMALIA;

EID: 24044474068     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwi043     Document Type: Article

References (32)

1. Bellve, A.R., Cavicchia, J.C., Millette, C.F., O'Brien, D.A., Bhatnagar, Y.M., and Dym, M. (1977) Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol., 74, 68-85.
2. Brinster, R.L. (2002) Germline stem cell transplantation and transgenesis. Science, 296, 2174-2176.
3. Brinster, R.L. and Zimmermann, J.W. (1994) Spermatogenesis following male germ-cell transplantation. Proc. Natl Acad. Sci. USA, 91, 11298-11302.
4. Buschard, K., Josefsen, K., Hansen, S.V., Horn, T., Marshall, M.O., Persson, H., Mansson, J.E., and Fredman, P. (1994) Sulphatide in islets of Langerhans and in organs affected in diabetic late complications: a study in human and animal tissue. Diabetologia, 37, 1000-1006.
5. de Rooij, D.G. and Grootegoed, J.A. (1998) Spermatogonial stem cells. Curr. Opin. Cell Biol., 10, 694-701.
6. Dym, M. (1983) The male reproductive system. In Weiss, L. (Ed.), Histology: cell and tissue biology, 5th ed. Elsevier Science, New York, pp. 1000-1053.
7. Fredman, P., Mattson, L., Andersson, K., Davidsson, P., Ishizuka, I., Jeansson, S., Mansson, J.-E., and Svennerholm, L. (1988) Characterization of the binding epitope of a monoclonal antibody to sulphatide. Biochem. J., 251, 17-22.
8. Fujimoto, H., Tadano-Aritomi, K., Tokumasu, A., Ito, K., Hikita, T., Suzuki, K., and Ishizuka, I. (2000) Requirement of seminolipid in spermatogenesis revealed by UDP-galactose: ceramide galactosyltransferase- deficient mice. J. Biol. Chem., 275, 22623-22626.
9. Goossens, E., Frederickx, V., De Block, G., Van Steirteghem, A.C., and Tournaye, H. (2003) Reproductive capacity of sperm obtained after germ cell transplantation in a mouse model. Hum Reprod., 18, 1874-1880.
10. Handa, S., Yamato, K., Ishizuka, I., Suzuki, A., and Yamakawa, T. (1974) Biosynthesis of seminolipid: sulfation in vivo and in vitro. J. Biochem. (Tokyo), 75, 77-83.
11. Honaramooz, A., Behboodi, E., Blash, S., Megee, S.O., and Dobrinski, I. (2003) Germ cell transplantation in goats. Mol. Reprod. Dev., 64, 422-428.
12. Honke, K., Tsuda, M., Hirahara, Y., Ishii, A., Makita, A., and Wada, Y. (1997) Molecular cloning and expression of cDNA encoding human 3 -phosphoadenylylsulfate:galactosylceramide 3 -sulfotransferase. J. Biol. Chem., 272, 4864-4868.
13. Honke, K., Hirahara, Y., Dupree, J., Suzuki, K., Popko, B., Fukushima, K., Fukushima, J., Nagasawa, T., Yoshida, N., Wada, Y., and Taniguchi, N. (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc. Natl Acad. Sci. USA, 99, 4227-4232.
14. Huckins, C. (1971) The spermatogonial stem cell population in adult rats. Their morphology, proliferation and maturation. Anat. Rec., 169, 533-558.
15. Ishizuka, I. (1997) Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res., 36, 245-319.
16. Ishizuka, I., Suzuki, M., and Yamakawa, T. (1973) Isolation and characterization of a novel sulfoglycolipid, "seminolipid" from boar testis and spermatozoa. J. Biochem. (Tokyo), 73, 77-87.
17. Izadyar, F., Spierenberg, G.T., Creemers, L.B., den Ouden, K., and de Rooij, D.G. (2002) Isolation and purification of type A spermatogonia from the bovine testis. Reproduction, 124, 85-94.
18. Jegou, B. (1993) The sertoli-germ cell communication-network in mammals. Int. Rev. Cytol., 147, 25-96.
19. Kornblatt, M.J., Knapp, A., Levine, M., Schachter, H., and Murray, R.K. (1974) Studies on the strucuture and formation during spermatogenesis of the sulfoglycerogalactolipid of rat testis. Can. J. Biochem., 52, 689-697.
20. Ogawa, T., Arechaga, J.M., Avarbock, M.R., and Brinster, R.L. (1997) Transplantation of testis germinal cells into mouse seminiferous tubules. Int. J. Dev. Biol., 41, 111-122.
21. Ohta, H., Yomogida, K., Dohmae, K., and Nishimune, Y. (2000) Regulation of proliferation and differentiation in spermatogonial stem cells: the role of c-kit and its ligand SCF. Development, 127, 2125-2131.
22. Ohta, H., Yomogida, K., Tadokoro, Y., Tohda, A., Dohmae, K., and Nishimune, Y. (2001) Defect in germ cells, not in supporting cells, is the cause of male infertility in the cause of spermatogonial stem cells without differentiation. Int. J. Androl., 24, 15-23.
23. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T., and Nishimune, Y. (1997) "Green mice" as a source of ubiquitous green cells. FEBS Lett., 407, 313-319.
24. Rodemer, C., Thai, T.-P., Brugger, B., Kaercher, T., Werner, H., Nave, K.-A., Wieland, F., Gorgas, K., and Just, W.W. (2003) Inactivation of ether lipid biosynthesis causes male infertility, defects in eye development and optic nerve hypoplasia in mice. Hum. Mol. Genet., 12, 1881-1895.
25. Sette, C., Dolci, S., Geremia, R., and Rossi, P. (2000) The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. Int. J. Dev. Biol., 44, 599-608.
26. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes. Nature, 387, 569-572.
27. Speed, R. R., Taggart, M., and Cooke, H.J. (2003) Spermatogenesis in testes of Dazl null mice after transplantation of wild-type germ cells. Reproduction, 126, 599-604.
28. Tajima, Y., Sawada, K., Morimoto, T., and Nishimune, Y. (1994) Switching of mouse spermatogonial proliferation from the c-kit receptor-independent type to the receptor-dependent type during differentiation. J. Reprod. Fertil., 102, 117-122.
29. van Meer, G. (2002) The different hues of lipid rafts. Science, 296, 855-856.
30. Vos, J.P., Lopes-Cardozo, M., and Gadella, B.M. (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim. Biophys. Acta, 1211, 125-149.
31. Weerachatyanukul, W., Xu, H., Anupriwan, A., Carmona, E., Wade, M., Hermo, L., da Silva, S.M., Rippstein, P., Sobhon, P., Sretarugsa, P., and Tanphaichitr, N. (2003) Acquisition of arylsulfatase A onto the mouse sperm surface during epididymal transit. Biol. Reprod., 69, 1183-1192.
32. Yeom, Y.I., Fuhrmann, G., Ovitt, C.E., Brehm, A., Ohbo, K., Gross, M., Hubner, K., and Scholer, H.R. (1996) Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Development, 122, 881-894.