Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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A Mutation of cdc-25.1 Causes Defects in Germ Cells But Not in Somatic Tissues in C. elegans

  • Kim, Jiyoung (Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University) ;
  • Lee, Ah-Reum (Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University) ;
  • Kawasaki, Ichiro (Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University) ;
  • Strome, Susan (Department of Molecular Cell and Developmental Biology, University of California Santa Cruz) ;
  • Shim, Yhong-Hee (Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University)
  • Received : 2009.04.17
  • Accepted : 2009.04.24
  • Published : 2009.07.31
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Abstract

By screening C. elegans mutants for severe defects in germline proliferation, we isolated a new loss-of-function allele of cdc-25.1, bn115. bn115 and another previously identified loss-of-function allele nr2036 do not exhibit noticeable cell division defects in the somatic tissues but have reduced numbers of germ cells and are sterile, indicating that cdc-25.1 functions predominantly in the germ line during postembryonic development, and that cdc-25.1 activity is probably not required in somatic lineages during larval development. We analyzed cell division of germ cells and somatic tissues in bn115 homozygotes with germline-specific anti-PGL-1 immunofluorescence and GFP transgenes that express in intestinal cells, in distal tip cells, and in gonadal sheath cells, respectively. We also analyzed the expression pattern of cdc-25.1 with conventional and quantitative RT-PCR. In the presence of three other family members of cdc-25.1 in C. elegans, defects are observed only in the germ line but not in the somatic tissues in cdc-25.1 single mutants, and cdc-25.1 is expressed predominantly, if not exclusively, in the germ line during postembryonic stages. Our findings indicate that the function of cdc-25.1 is unique in the germ line but likely redundant with other members in the soma.

Keywords

Acknowledgement

Supported by : Korea Forest Service, Konkuk University, NIH

References

  1. Ashcroft, N., and Golden, A. (2002). CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33, 1-7 https://doi.org/10.1002/gene.10083
  2. Ashcroft, N.R., Kosinski, M.E., Wickramasinghe, D., Donovan, P.J., and Golden, A. (1998). The four cdc25 genes from the nematode Caenorhabditis elegans. Gene 214, 59-66 https://doi.org/10.1016/S0378-1119(98)00228-5
  3. Ashcroft, N.R., Srayko, M., Kosinski, M.E., Mains, P.E., and Golden, A. (1999). RNA-Mediated interference of a cdc25 homolog in Caenorh abditis results in defects in the embryonic cortical membrane, meiosis, and mitosis. Dev. Biol. 206, 15-32 https://doi.org/10.1006/dbio.1998.9135
  4. Austin, J., and Kimble, J. (1987). glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51, 589-599 https://doi.org/10.1016/0092-8674(87)90128-0
  5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94
  6. Clucas, C., Cabello, J., Bussing, I., Schnabel, R., and Johnstone, I.L. (2002). Oncogenic potential of a C. elegans cdc25 gene is demonstrated by a gain-of-function allele. EMBO J. 21, 665-674 https://doi.org/10.1093/emboj/21.4.665
  7. Crittenden, S.L., Troemel, E.R., Evans, T.C., and Kimble, J. (1994). GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120, 2901-2911
  8. Hebeisen, M., and Roy, R. (2008). CDC-25.1 stability is regulated by distinct domains to restrict cell division during embryogenesis in . Development 135, 1259-1269 https://doi.org/10.1242/dev.014969
  9. Hirsh, D., Oppenheim, D., and Klass, M. (1976). Development of the reproductive system of Caenorhabditis elegnas. Dev. Biol. 49, 200-219 https://doi.org/10.1016/0012-1606(76)90267-0
  10. Kawasaki, I., Shim, Y.H., Kirchner, J., Kaminker, J., Wood, W.B., and Strome, S. (1998). PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94, 635-645 https://doi.org/10.1016/S0092-8674(00)81605-0
  11. Kawasaki, I., Amiri, A., Fan, Y., Meyer, N., Dunkelbarger, S., Motohashi, T., Karashima, T., Bossinger, O., and Strome, S. (2004). The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegnas germline development. Genetics 167, 645-661 https://doi.org/10.1534/genetics.103.023093
  12. Kim, S., Park, D.H., and Shim, J. (2008). Thymidylate synthase and dihydropyrimidine dehydrogenase levels are associated with response to 5-fluorouracil in Caenorhabditis elegnas. Mol. Cells 26, 344-349
  13. Kimble, J., and Crittenden, S.L. (2005). Germline proliferation and its control. WormBook, 1-14
  14. Kimble, J., and Hirsh, D. (1979). The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegnas. Dev. Biol. 70, 396-417 https://doi.org/10.1016/0012-1606(79)90035-6
  15. Kimble, J.E., and White, J.G. (1981). On the control of germ cell development in Caenorhabditis elegnas. Dev. Biol. 81, 208-219 https://doi.org/10.1016/0012-1606(81)90284-0
  16. Kostic, I., and Roy, R. (2002). Organ-specific cell division abnormalities caused by mutation in a general cell cycle regulator in C. elegans. Development 129, 2155-2165
  17. Nelson, G.A., Lew, K.K., and Ward, S. (1978). Intersex, a temperature- sensitive mutant of the nematode Caenorhabditis elegnas. Dev. Biol. 66, 386-409 https://doi.org/10.1016/0012-1606(78)90247-6
  18. Reinke, V., Gil, I.S., Ward, S., and Kazmer, K. (2004). Genomewide germline-enriched and sex-biased expression profiles in Caenorhabditis elegnas. Development 131, 311-323 https://doi.org/10.1242/dev.00914
  19. Russell, P., and Nurse, P. (1986). cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45, 145-153 https://doi.org/10.1016/0092-8674(86)90546-5
  20. Strome, S. (1986). Asymmetric movements of cytoplasmic components in Caenorhabditis elegnas zygotes J. Embryol. Exp. Morph. 97, 15-29
  21. Strome, S., and Wood, W.B. (1983). Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell 35, 15-25 https://doi.org/10.1016/0092-8674(83)90203-9
  22. Sulston, J.E., and Horvitz, H.R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegnas Dev. Biol. RSI 110-156
  23. Sulston, J.E., Schierenberg, E., White, J.G., and Thomson, J.N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegnas. Dev. Biol. 100, 64-119 https://doi.org/10.1016/0012-1606(83)90201-4

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