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A novel F-box protein with leucine-rich repeats affects defecation frequency and daumone response in Caenorhabditis elegans

  • Kim, Sung-Moon (Graduate School of Biology and Information Technology, Institute of Genetic Engineering, Hankyong National University) ;
  • Jang, Sang-Ho (Graduate School of Biology and Information Technology, Institute of Genetic Engineering, Hankyong National University) ;
  • Son, Na-Rae (Graduate School of Biology and Information Technology, Institute of Genetic Engineering, Hankyong National University) ;
  • Han, Ching-Tack (Department of Life Science, Sogang University) ;
  • Min, Kwan-Sik (Graduate School of Biology and Information Technology, Institute of Genetic Engineering, Hankyong National University) ;
  • Lee, Hak-Kyo (Department of Bioengineering, Hankyong National University) ;
  • Hwang, Sue-Yun (Graduate School of Biology and Information Technology, Institute of Genetic Engineering, Hankyong National University)
  • Received : 2012.02.02
  • Accepted : 2012.02.07
  • Published : 2012.08.31

Abstract

Targeted degradation of proteins through ubiquitin-mediated proteolysis is an important control mechanism in various cellular processes. The process of ubiquitin conjugation is achieved by three enzyme complexes, among which the ubiquitin ligase complex (E3) is in charge of substrate specificity. The SCF (SKP1-CUL1-F-box) family portrays the largest and the most characterized member of the E3 ligases. For each SCF complex, the ubiquitination target is recognized by the F-box protein subunit, which interacts with the substrate through a unique C-terminal domain. We have characterized a novel F-box protein CFL-1 that represents a single LRR-type F-box (FBXL) in the Caenorhabditis elegans genome. CFL-1 is highly homologous to FBXL20 and FBXL2 of mammals, which are known to regulate synaptic vesicle release and cell cycle, respectively. A green fluorescence protein (GFP)-reporter gene fused to the cfl-1 promoter showed restricted expression around the amphid and the anus. Modulation of CFL-1 activity by RNAi affected the time interval between defecations. RNAi-treated worms also exhibited reduced tendency to form dauer when exposed to daumone. The potential involvement of CFL-1 in the control of defecation and pheromone response adds to the ever expanding list of cellular processes controlled by ubiquitin-mediated proteolysis in C. elegans. We suggest that CFL-1, as a single LRR-type F-box protein in C. elegans, may portray a prototype gene exerting diverse functions that are allocated among multiple FBXLs in higher organisms.

Keywords

References

  1. Altschul SF, Thomas LM, Alejandro AS, Zhang J, Zhang Z, Miller W, Limpman DJ. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. https://doi.org/10.1093/nar/25.17.3389
  2. Bargmann CI, Horvitz HR. 1991. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science 251:1243-1246. https://doi.org/10.1126/science.2006412
  3. Branicky R, Hekimi S. 2006. What keeps C. elegans regular: the genetics of defecation. Trends Genet. 22:571-579. https://doi.org/10.1016/j.tig.2006.08.006
  4. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
  5. Chen BB, Coon TA, Glasser JR, Mallampalli RK 2011. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol Cell Biol. 9:1905-1920.
  6. Chen BB, Glassier JR, Coon TA, Mallampalli RK. 2011. FBXL2 is an ubiquitin E3 ligase subunit that triggers mitotic arrest. Cell Cycle. 10:3487-3494. https://doi.org/10.4161/cc.10.20.17742
  7. Church DL, Guan KL, Lambie EJ. 1995. Three genes of the MAP kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121:2525-2535.
  8. Clifford R, Lee MH, Nayak S, Ohmachi M, Giorgini F, Shedle T. 2000. FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline. Development 127:5265-5276.
  9. Fey JP, Lanker S. 2007. Delayed accumulation of the yeast G1 cyclin Cln1 and Cln2 and the F-box protein Grr1 in response to glucose. Yeast 24:419-429. https://doi.org/10.1002/yea.1472
  10. Gracheva EO, Hadwiger G, Nonet M, Richmond J. 2008. Direct interaction between C. elegans RAB-3 and Rim provide a mechanism to target vesicles to the presynaptic density. Neuroscience Lett. 444:137-142. https://doi.org/10.1016/j.neulet.2008.08.026
  11. Han YK, Kim MD, Lee SH, Yun SH, Lee YW. 2007. A novel F-box protein involved in sexual development and pathogenesis in Gibberella zeae. Mol Microbiol. 63: 768-779.
  12. Jee C, Lee J, Lee JI, Lee WH, Park B-J, Yu J-R, Park E, Kim E, Ahnn J. 2004. SHN-1, a Shank homologue of C. elegans, affects defecation rhythm via the inositol- 1,4,5-trisphosphate receptor. FEBS Lett. 561:29-36. https://doi.org/10.1016/S0014-5793(04)00107-3
  13. Jeong PY, Jing M, Yim YH, Kim H, Park M, Hong E, Lee W, Kim K, Paik YK. 2005. Chemical structure and biological activity of the Caenorhabditis elegans dauerinducing pheromone. Nature 433:541-545. https://doi.org/10.1038/nature03201
  14. Jung T, Catalgol B, Grune T. 2009. The proteasomal system. Mol Asp Med. 30:191-296. https://doi.org/10.1016/j.mam.2009.04.001
  15. Kamath RS, Ahringer J. 2003. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30:313-321. https://doi.org/10.1016/S1046-2023(03)00050-1
  16. Kipreos ET, Pagano M. 2000. The F-box protein family. Genome Biol. 1:1-7.
  17. Lans H, Jansem G. 2006. Noncell- and cell-autonomous Gprotein- signaling converges with $Ca^{2+}$/mitogen-activated protein kinase signaling to regulate str-2 receptor gene expression in Caenorhabditis elegans. Genetics 173:1287-1299. https://doi.org/10.1534/genetics.106.058750
  18. Mello C, Fire A. 1995. DNA transformation. Methods Cell Biol. 48:451-482.
  19. Min K, Lee J. 2007. RNA interference in C. elegans: history, application and perspectives. Integr Biosci. 11:99-104. https://doi.org/10.1080/17386357.2007.9647321
  20. Polinsky C, Houston C, Vado J, Shaikh A, Kohn RE. 2006. Synaptic protein UNC-13 interacts with an F-box protein that may target it for degradation by proteasomes. Acta Biochim Pol. 53:145-148.
  21. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstruction phylogenetic tree. Mol Bio Evol. 4:406-425.
  22. Schackwitz WS, Inoue T, Thomas JH. 1996. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17:719-728. https://doi.org/10.1016/S0896-6273(00)80203-2
  23. Shakir MA, Miwa J, Siddiqui SS. 1993. A role of ADF chemosensory neurons in dauer formation behavior in C. elegans. Neuroreport 4:1151-1154.
  24. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599. https://doi.org/10.1093/molbev/msm092
  25. Walker DS, Grower NJD, Ly S, Bradley GL, Batlis HA. 2002. Regulated disruption of Inositol 1,4,5-trisphosphate signaling in Caenorhabditis elegans reveals new functions in feeding and embryogenesis. Mol Biol Cell 13:1329-1337. https://doi.org/10.1091/mbc.01-08-0422
  26. Wang C, Gale M, Jr, Keller BC, Huang H, Brown MS, Goldstein JL, Ye J. 2005. Identification of FBL2 as a genanylgeranylated cellular protein required for hepatitis C virus RNA replication. Mol Cell. 18:425-434. https://doi.org/10.1016/j.molcel.2005.04.004
  27. Willems AR, Schwab M, Tyers M. 2004. A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochem Biophys Acta 1695:133-170. https://doi.org/10.1016/j.bbamcr.2004.09.027
  28. Yao I, Takagi H, Ageta H, Kahyo T, Sato S, Hatanaka K, Fukuda Y, Chiba T, Morone N, Yuasa S, et al. 2007. SCRAPPER-dependent ubiquitination of active zone protein RIM1 regulates synaptic vesicle release. Cell 103:943-957.

Cited by

  1. CFL-1, a novel F-box protein with leucine-rich repeat may interact with UNC-10 for the regulation of defecation and daumone response in Caenorhabditis elegans vol.21, pp.3, 2012, https://doi.org/10.1080/19768354.2017.1325779