Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

LIN-23, an E3 Ubiquitin Ligase Component, Is Required for the Repression of CDC-25.2 Activity during Intestinal Development in Caenorhabditis elegans

  • Son, Miseol (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Kawasaki, Ichiro (Department of Bioscience and Biotechnology, Konkuk University) ;
  • Oh, Bong-Kyeong (Institute of Medical Science, Hanyang University College of Medicine) ;
  • Shim, Yhong-Hee (Department of Bioscience and Biotechnology, Konkuk University)
  • Received : 2016.10.10
  • Accepted : 2017.11.07
  • Published : 2016.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

Caenorhabditis elegans (C. elegans) utilizes two different cell-cycle modes, binucleations during the L1 larval stage and endoreduplications at four larval moltings, for its postembryonic intestinal development. Previous genetic studies indicated that CDC-25.2 is specifically required for binucleations at the L1 larval stage and is repressed before endoreduplications. Furthermore, LIN-23, the C. elegans ${\beta}$-TrCP ortholog, appears to function as a repressor of CDC-25.2 to prevent excess intestinal divisions. We previously reported that intestinal hyperplasia in lin-23(e1883) mutants was effectively suppressed by the RNAi depletion of cdc-25.2. Nevertheless, LIN-23 targeting CDC-25.2 for ubiquitination as a component of E3 ubiquitin ligase has not yet been tested. In this study, LIN-23 is shown to be the major E3 ubiquitin ligase component, recognizing CDC-25.2 to repress their activities for proper transition of cell-cycle modes during the C. elegans postembryonic intestinal development. In addition, for the first time that LIN-23 physically interacts with both CDC-25.1 and CDC-25.2 and facilitates ubiquitination for timely regulation of their activities during the intestinal development.

Keywords

References

  1. 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
  2. An, J.H., and Blackwell, T.K. (2003). SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17, 1882-1893. https://doi.org/10.1101/gad.1107803
  3. Brenner, S. (1974). The Genetics of Caenorhabditis elegans. Genetics 77, 71-94.
  4. Burger, J., Merlet, J., Tavernier, N., Richaudeau, B., Arnold, A., Ciosk, R., Bowerman, B., and Pintard, L. (2013). $CRL2^{LRR-1}$ E3-Ligase Regulates Proliferation and Progression through Meiosis in the Caenorhabditis elegans Germline. PLoS Genet. 9, e1003375. https://doi.org/10.1371/journal.pgen.1003375
  5. 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
  6. Crowe, E., and Candido, E.P. (2004). Characterization of C. elegans RING finger protein 1, a binding partner of ubiquitinconjugating enzyme 1. Dev. Biol. 265, 446-459. https://doi.org/10.1016/j.ydbio.2003.09.037
  7. Deppe, U., Schierenberg, E., Cole, T., Krieg, C., Schmitt, D., Yoder, B., and von Ehrenstein, G. (1978). Cell lineages of the embryo of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 75, 376-380. https://doi.org/10.1073/pnas.75.1.376
  8. DeRenzo, C., Reese, K.J., and Seydoux, G. (2003). Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424, 685-689. https://doi.org/10.1038/nature01887
  9. Du, Z., He, F., Yu, Z., Bowerman, B., and Bao, Z. (2015). E3 ubiquitin ligases promote progression of differentiation during C. elegans embryogenesis. Dev. Biol. 398, 267-279. https://doi.org/10.1016/j.ydbio.2014.12.009
  10. Fantes, P. (1979). Epistatic gene interactions in the control of division in fission yeast. Nature 279, 428-430. https://doi.org/10.1038/279428a0
  11. Fuchs, S.Y., Spiegelman, V.S., and Kumar, K.G.S. (2004). The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 23, 2028-2036. https://doi.org/10.1038/sj.onc.1207389
  12. Golden, A., Sadler, P.L., Wallenfang, M.R., Schumacher, J.M., Hamill, D.R., Bates, G., Bowerman, B., Seydoux, G., and Shakes, D.C. (2000). Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J Cell Biol. 151, 1469-1482. https://doi.org/10.1083/jcb.151.7.1469
  13. Hebeisen, M., and Roy, R. (2008). CDC-25.1 stability is regulated by distinct domains to restrict cell division during embryogenesis in C. elegans. Development 135, 1259-1269. https://doi.org/10.1242/dev.014969
  14. Hedgecock, E.M., and White, J.G. (1985). Polyploid tissues in the nematode Caenorhabditis elegans. Dev. Biol. 107, 128-133. https://doi.org/10.1016/0012-1606(85)90381-1
  15. Huang, P., Ma, X., Zhao, Y., and Miao, L. (2013). The C. elegans Homolog of RBBP6 (RBPL-1) Regulates Fertility through Controlling Cell Proliferation in the Germline and Nutrient Synthesis in the Intestine. PLoS One 8, e58736. https://doi.org/10.1371/journal.pone.0058736
  16. Kamura, T., Koepp, D.M., Conrad, M.N., Skowyra, D., Moreland, R.J., Iliopoulos, O., Lane, W.S., Kaelin Jr., W.G., Elledge, S.J., Conaway, R.C. et al. (1999). Rbx1, a Component of the VHL Tumor Suppressor Complex and SCF Ubiquitin Ligase. Science 284, 657-661. https://doi.org/10.1126/science.284.5414.657
  17. Kipreos, E.T., Lander, L.E., Wing, J.P., He, W.W., and Hedgecock, E.M. (1996). cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839. https://doi.org/10.1016/S0092-8674(00)81267-2
  18. Kipreos, E.T., Gohel, S.P., and Hedgecock, E.M. (2000). The C. elegans F-box/WD-repeat protein LIN-23 functions to limit cell division during development. Development 127, 5071-5082.
  19. 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.
  20. Lee, H., Alpi, A.F., Park, M.S., Rose, A., and Koo, H.S. (2013). C. elegans Ring Finger Protein RNF-113 Is Involved in Interstrand DNA Crosslink Repair and Interacts with a RAD51C Homolog. PLoS One 8, e60071. https://doi.org/10.1371/journal.pone.0060071
  21. Lee, Y.U., Son, M., Kim, J., Shim, Y.H., and Kawasaki, I. (2016). CDC-25.2, a C. elegans ortholog of cdc25, is essential for the progression of intestinal divisions. Cell Cycle 15, 654-666. https://doi.org/10.1080/15384101.2016.1146839
  22. Leung, B., Hermann, G.J., and Priess, J.R. (1999). Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216, 114-134. https://doi.org/10.1006/dbio.1999.9471
  23. Libina, N., Berman, J.R., and Kenyon, C. (2003). Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115, 489-502. https://doi.org/10.1016/S0092-8674(03)00889-4
  24. Mallo, G.V., Kurz, C.L., Couillault, C., Pujol, N., Granjeaud, S., Kohara, Y., and Ewbank, J.J. (2002). Inducible antibacterial defense system in C. elegans. Curr. Biol. 12, 1209-1214. https://doi.org/10.1016/S0960-9822(02)00928-4
  25. Maniatis, T. (1999). A ubiquitin ligase complex essential for the NF-${\kappa}B$, Wnt/Wingless, and Hedgehog signaling pathways. Genes Dev. 13, 505-510. https://doi.org/10.1101/gad.13.5.505
  26. Nayak, S., Santiago, F.E., Jin, H., Lin, D., Schedl, T., and Kipreos, E.T. (2002). The Caenorhabditis elegans Skp1-related gene family: Diverse functions in cell proliferation, morphogenesis, and meiosis. Curr. Biol. 12, 277-287. https://doi.org/10.1016/S0960-9822(02)00682-6
  27. Pintard, L., Willis, J.H., Willems, A., Johnson, J.L., Srayko, M., Kurz, T., Glaser, S., Mains, P.E., Tyers, M., Bowerman, B. et al. (2003). The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature 425, 311-316. https://doi.org/10.1038/nature01959
  28. Sharrock, W.J. (1983). Yolk proteins of Caenorhabditis elegans. Dev. Biol. 96, 182-188. https://doi.org/10.1016/0012-1606(83)90321-4
  29. Sonneville, R., and Gonczy, P. (2004). zyg-11 and cul-2 regulate progression through meiosis II and polarity establishment in C. elegans. Development 131, 3527-3543. https://doi.org/10.1242/dev.01244
  30. Sulston, J.E., and Horvitz, H.R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156. https://doi.org/10.1016/0012-1606(77)90158-0
  31. Sulston, J.E., Schierenberg, E., White, J.G., and Thomson, J.N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119. https://doi.org/10.1016/0012-1606(83)90201-4
  32. Yoo, J.E., Park, Y.N., and Oh, B.K. (2014). PinX1, a telomere repeat-binding factor 1 (TRF1)-interacting protein, maintains telomere integrity by modulating TRF1 homeostasis, the process in which human telomerase reverse transcriptase (hTERT) plays dual roles. J. Biol. Chem. 289, 6886-6898. https://doi.org/10.1074/jbc.M113.506006

Cited by

  1. Developmental Control of the Cell Cycle: Insights from Caenorhabditis elegans vol.211, pp.3, 2016, https://doi.org/10.1534/genetics.118.301643