Ceramide glucosyltransferase of the nematode Caenorhabditis elegans is involved in oocyte formation and in early embryonic cell division

Glycobiology

Volumn 21, Issue 6, 2011, Pages 834-848

  Nomura, Kazuko H ^a,b   Murata, Daisuke ^a,b   Hayashi, Yasuhiro ^a,e   Dejima, Katsufumi ^a,b,f   Mizuguchi, Souhei ^a,b,g   Kage Nakadai, Eriko ^b,c   Gengyo Ando, Keiko ^b,c,h   Mitani, Shohei ^b,c   Hirabayashi, Yoshio ^b,d   Ito, Makoto ^a,b   Nomura, Kazuya ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^e TEIKYO UNIVERSITY   (Japan)

^f UNIVERSITY OF MINNESOTA   (United States)

^g KUMAMOTO UNIVERSITY   (Japan)

^h SAITAMA UNIVERSITY   (Japan)

Author keywords

germline; glycosphingolipid; mitosis; sphingomyelin; Ugcg

Indexed keywords

CERAMIDE GLUCOSYLTRANSFERASE; SPHINGOMYELIN;

ARTICLE; CAENORHABDITIS ELEGANS; CELL DIVISION; FERTILIZATION; GENE FUNCTION; GENE INACTIVATION; NONHUMAN; OOCYTE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CAENORHABDITIS ELEGANS; CELL DIVISION; GLUCOSYLTRANSFERASES; OOCYTES;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 79956133856     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwr019     Document Type: Article

References (51)

1. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics. 77:71-94.
2. Dejima K, Murata D, Mizuguchi S, Nomura KH, Izumikawa T, Kitagawa H, Gengyo-Ando K, Yoshina S, Ichimiya T, Nishihara S, et al. 2010. Two Golgi-resident 3′-phosphoadenosine 5′-phosphosulfate transporters play distinct roles in heparan sulfate modifications and embryonic and larval development in Caenorhabditis elegans. J Biol Chem. 285:24717-24728.
3. Dejima K, Seko A, Yamashita K, Gengyo-Ando K, Mitani S, Izumikawa T, Kitagawa H, Sugahara K, Mizuguchi S, Nomura K. 2006. Essential roles of 3′-phosphoadenosine 5′-phosphosulfate synthase in embryonic and larval development of the nematode Caenorhabditis elegans. J Biol Chem. 281:11431-11440. (Pubitemid 43855568)
4. Furusato M, Sueyoshi N, Mitsutake S, Sakaguchi K, Kita K, Okino N, Ichinose S, Omori A, Ito M. 2002. Molecular cloning and characterization of sphingolipid ceramide N-deacylase from a marine bacterium, Shewanella alga G8. J Biol Chem. 277:17300-17307. (Pubitemid 34967765)
5. Gengyo-Ando K, Mitani S. 2000. Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem Biophys Res Commun. 269:64-69. (Pubitemid 30440255)
6. Green RA, Audhya A, Pozniakovsky A, Dammermann A, Pemble H, Monen J, Portier N, Hyman A, Desai A, Oegema K. 2008. Expression and imaging of fluorescent proteins in the C. elegans gonad and early embryo. Methods Cell Biol. 85:179-218.
7. Griffitts JS, Haslam SM, Yang T, Garczynski SF, Mulloy B, Morris H, Cremer PS, Dell A, Adang MJ, Aroian RV. 2005. Glycolipids as receptors for Bacillus thuringiensis crystal toxin. Science. 307:922-925. (Pubitemid 40229228)
8. Grishok A, Sinskey JL, Sharp PA. 2005. Transcriptional silencing of a trans-gene by RNAi in the soma of C. elegans. Genes Dev. 19:683-696. (Pubitemid 40395080)
9. Hidari KIPJ, Ichikawa S, Fujita T, Sakiyama H, Hirabayashi Y. 1996. Complete removal of sphingolipids from the plasma membrane disrupts cell to substratum adhesion of mouse melanoma cells. J Biol Chem. 271:14636-14641. (Pubitemid 26190372)
10. Hwang HY, Olson SK, Esko JD, Horvitz HR. 2003. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature. 423:439-443. (Pubitemid 36626995)
11. Ichikawa S, Hirabayashi Y. 1998. Glucosylceramide synthase and glycosphin-golipid synthesis. Trends Cell Biol. 8:198-202.
12. Ichikawa S, Nakajo N, Sakiyama H, Hirabayashi Y. 1994. A mouse B16 melanoma mutant deficient in glycolipids. Proc Natl Acad Sci USA. 91:2703-2707. (Pubitemid 24139416)
13. Ichikawa S, Sakiyama H, Suzuki G, Hidari KI, Hirabayashi Y. 1996. Expression cloning of a cDNA for human ceramide glucosyltransferase that catalyzes the first glycosylation step of glycosphingolipid synthesis. Proc Natl Acad Sci USA. 93:4638-4643. (Pubitemid 26163495)
14. Ideo H, Fukushima K, Gengyo-Ando K, Mitani S, Dejima K, Nomura K, Yamashita K. 2009. A Caenorhabditis elegans glycolipid-binding galectin functions in host defense against bacterial infection. J Biol Chem. 284:26493-26501.
15. Ishitsuka R, Yamaji-Hasegawa A, Makino A, Hirabayashi Y, Kobayashi T. 2004. A lipid-specific toxin reveals heterogeneity of sphingomyelin-containing membranes. Biophys J. 86:296-307. (Pubitemid 38067457)
16. Izumikawa T, Kitagawa H, Mizuguchi S, Nomura KH, Nomura K, Tamura J, Gengyo-Ando K, Mitani S, Sugahara K. 2004. Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division. J Biol Chem. 279:53755-53761. (Pubitemid 40051884)
17. Jennemann R, Sandhoff R, Wang S, Kiss E, Gretz N, Zuliani C, Martin-Villalba A, Jager R, Schorle H, Kenzelmann M, et al. 2005. Cell-specific deletion of glucosylceramide synthase in brain leads to severe neural defects after birth. Proc Natl Acad Sci USA. 102:12459-12464. (Pubitemid 41266381)
18. Kachur TM, Audhya A, Pilgrim DB. 2008. UNC-45 is required for NMY-2 contractile function in early embryonic polarity establishment and germline cellularization in C. elegans. Dev Biol. 314:287-299.
19. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, et al. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 421:231-237. (Pubitemid 36139121)
20. Kiyokawa E, Baba T, Otsuka N, Makino A, Ohno S, Kobayashi T. 2005. Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J Biol Chem. 280:24072-24084. (Pubitemid 40884895)
21. Kodama Y, Rothman JH, Sugimoto A, Yamamoto M. 2002. The stem-loop binding protein CDL-1 is required for chromosome condensation, progression of cell death and morphogenesis in Caenorhabditis elegans. Development. 129:187-196. (Pubitemid 34863787)
22. Kohyama-Koganeya A, Sasamura T, Oshima E, Suzuki E, Nishihara S, Ueda R, Hirabayashi Y. 2004. Drosophila glucosylceramide synthase: A negative regulator of cell death mediated by proapoptotic factors. J Biol Chem. 279:35995-36002. (Pubitemid 39100607)
23. Lavie Y, Cao H, Bursten SL, Giuliano AE, Cabot MC. 1996. Accumulation of glucosylceramides in multidrug-resistant cancer cells. J Biol Chem. 271:19530-19536. (Pubitemid 26271630)
24. Leipelt M, Warnecke DC, Hube B, Zahringer U, Heinz E. 2000. Characterization of UDP-glucose:ceramide glucosyltransferases from different organisms. Biochem Soc Trans. 28:751-752. (Pubitemid 32163255)
25. Leipelt M, Warnecke D, Zahringer U, Ott C, Muller F, Hube B, Heinz E. 2001. Glucosylceramide synthases, a gene family responsible for the biosynthesis of glucosphingolipids in animals, plants, and fungi. J Biol Chem. 276:33621-33629.
26. Lingwood D, Simons K. 2010. Lipid rafts as a membrane-organizing principle. Science. 327:46-50.
27. Liu YY, Yu JY, Yin D, Patwardhan GA, Gupta V, Hirabayashi Y, Holleran WM, Giuliano AE, Jazwinski SM, Gouaze-Andersson V, et al. 2008. A role for ceramide in driving cancer cell resistance to doxorubicin. FASEB J. 22:2541-2551. (Pubitemid 351948671)
28. Lochnit G, Bongaarts R, Geyer R. 2005. Searching new targets for anthel-minthic strategies: Interference with glycosphingolipid biosynthesis and phosphorylcholine metabolism affects development of Caenorhabditis elegans. Int J Parasitol. 35:911-923. (Pubitemid 40905207)
29. Marroquin LD, Elyassnia D, Griffitts JS, Feitelson JS, Aroian RV. 2000. Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics. 155:1693-1699. (Pubitemid 30626389)
30. Marza E, Simonsen KT, Faergeman NJ, Lesa GM. 2009. Expression of cera-mide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells. J Cell Sci. 122:822-833.
31. Matyash V, Entchev EV, Mende F, Wilsch-Brauninger M, Thiele C, Schmidt AW, Knolker HJ, Ward S, Kurzchalia TV. 2004. Sterol-derived hormone(s) controls entry into diapause in Caenorhabditis elegans by consecutive activation of DAF-12 and DAF-16. PLoS Biol. 2:e280.
32. Mizuguchi S, Uyama T, Kitagawa H, Nomura KH, Dejima K, Gengyo-Ando K, Mitani S, Sugahara K, Nomura K. 2003. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature. 423:443-448. (Pubitemid 36626996)
33. Morjani H, Aouali N, Belhoussine R, Veldman RJ, Levade T, Manfait M. 2001. Elevation of glucosylceramide in multidrug-resistant cancer cells and accumulation in cytoplasmic droplets. Int J Cancer. 94:157-165. (Pubitemid 32911407)
34. Praitis V, Casey E, Collar D, Austin J. 2001. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics. 157:1217-1226. (Pubitemid 32225014)
35. Reinke V, Cutter AD. 2009. Germline expression influences operon organization in the Caenorhabditis elegans genome. Genetics. 181:1219-1228.
36. Rittershaus PC, Kechichian TB, Allegood JC, Merrill AH, Jr, Hennig M, Luberto C, Del Poeta M. 2006. Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest. 116:1651-1659.
37. Ruckhaberle E, Karn T, Hanker L, Gatje R, Metzler D, Holtrich U, Kaufmann M, Rody A. 2009. Prognostic relevance of glucosylceramide synthase (GCS) expression in breast cancer. J Cancer Res Clin Oncol. 135:81-90.
38. Schaner CE, Kelly WG. 2006. Germline chromatin. In: WormBook, editors. The C. elegans Research Community, WormBook, doi/10.1895/worm-book.1.73.1, http://www.wormbook.org.
39. Seaman MN. 2005. Recycle your receptors with retromer. Trends Cell Biol. 15:68-75. (Pubitemid 40188216)
40. Seydoux G, Strome S. 1999. Launching the germline in Caenorhabditis elegans: Regulation of gene expression in early germ cells. Development. 126:3275-3283. (Pubitemid 29396768)
41. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, Plasterk RH, Fire A. 2001. On the role of RNA amplification in dsRNA-triggered gene silencing. Cell. 107:465-476. (Pubitemid 33152782)
42. Strome S, Powers J, Dunn M, Reese K, Malone CJ, White J, Seydoux G, Saxton W. 2001. Spindle dynamics and the role of gamma-tubulin in early Caenorhabditis elegans embryos. Mol Biol Cell. 12:1751-1764. (Pubitemid 33049727)
43. Sun YL, Zhou GY, Li KN, Gao P, Zhang QH, Zhen JH, Bai YH, Zhang XF. 2006. Suppression of glucosylceramide synthase by RNA interference reverses multidrug resistance in human breast cancer cells. Neoplasma. 53:1-8. (Pubitemid 43206931)
44. Takematsu H, Kozutsumi Y. 2006. Characterization of genes conferring resistance against ISP-1/myriocin-induced sphingolipid depletion in yeast. In: Hirabayashi Y, Igarashi Y, Merrill AH, Jr, editors. Sphingolipid Biology. Tokyo (Japan): Springer. p. 463-474.
45. Vazquez-Manrique RP, Gonzalez-Cabo P, Ortiz-Martin I, Ros S, Baylis HA, Palau F. 2007. The frataxin-encoding operon of Caenorhabditis elegans shows complex structure and regulation. Genomics. 89: 392-401. (Pubitemid 46205117)
46. Wang X, Zhao Y, Wong K, Ehlers P, Kohara Y, Jones SJ, Marra MA, Holt RA, Moerman DG, Hansen D. 2009. Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics. 10:213.
47. Yamashita T, Allende ML, Kalkofen DN, Werth N, Sandhoff K, Proia RL. 2005. Conditional LoxP-flanked glucosylceramide synthase allele controlling glycosphingolipid synthesis. Genesis. 43:175-180. (Pubitemid 43117833)
48. Yamashita T, Wada R, Sasaki T, Deng C, Bierfreund U, Sandhoff K, Proia RL. 1999. A vital role for glycosphingolipid synthesis during development and differentiation. Proc Natl Acad Sci USA. 96:9142-9147. (Pubitemid 29374721)
49. Yokoyama K, Suzuki M, Kawashima I, Karasawa K, Nojima S, Enomoto T, Tai T, Suzuki A, Setaka M. 1997. Changes in composition of newly synthesized sphingolipids of HeLa cells during the cell cycle. Eur J Biochem. 249:450-455.
50. Zama K, Hayashi Y, Ito S, Hirabayashi Y, Inoue T, Ohno K, Okino N, Ito M. 2009. Simultaneous quantification of glucosylceramide and galacto-sylceramide by normal-phase HPLC using O-phthalaldehyde derivatives prepared with sphingolipid ceramide N-deacylase. Glycobiology. 19:767-775.
51. Zhang X, Li J, Qiu Z, Gao P, Wu X, Zhou G. 2009. Co-suppression of MDR1 (multidrug resistance 1) and GCS (glucosylceramide synthase) restores sensitivity to multidrug resistance breast cancer cells by RNA interference (RNAi). Cancer Biol Ther. 8:1117-1121.