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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Calcineurin may regulate multiple endocytic processes in C. elegans

  • Song, Hyun-Ok (Department of Infection Biology, Zoonosis Research Center, Wonkwang University School of Medicine) ;
  • Ahnn, Joo-Hong (Department of Life Science, BK21 (Life Science for Global Warming Team), College of Natural Sciences, Hanyang University)
  • Received : 2010.11.01
  • Accepted : 2010.12.08
  • Published : 2011.02.28
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Abstract

Calcineurin is a serine/threonine protein phosphatase controlled by $Ca^{2+}$ and calmodulin that has been implicated in various signaling pathways. Previously, we reported that calcineurin regulates coelomocyte endocytosis in Caenorhabditis elegans. So far, simple and powerful in vivo approaches have been developed to study various endocytic processes in C. elegans. Using these in vivo assays, we further analyzed the endocytic phenotypes of calcineurin mutants. We observed that the calcineurin mutants were defective in apical endocytosis in the intestine as well as synaptic vesicle recycling in the nerve cord. However, we found that calcineurin mutants displayed normal receptor-mediated endocytosis in oocytes. Therefore, our results suggest that calcineurin may regulate specific sets of endocytic processes in nematode.

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References

  1. Klee, C. B., Crouch, T. H. and Krinks, M. H. (1979) Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 76, 6270-6273. https://doi.org/10.1073/pnas.76.12.6270
  2. Stewart, A. A., Ingebritsen, T. S., Manalan, A., Klee, C. B. and Cohen, P. (1982) Discovery of a $Ca^{2+}$- and calmodulin-dependent protein phosphatase: probable identity with calcineurin (CaM-BP80). FEBS Lett. 137, 80-84. https://doi.org/10.1016/0014-5793(82)80319-0
  3. Klee, C. B., Ren, H. and Wang, X. (1998) Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J. Biol. Chem. 273, 13367-13370..0 https://doi.org/10.1074/jbc.273.22.13367
  4. Crabtree, G. R. (1999) Generic signals and specific outcomes: signaling through $Ca^{2+}$, calcineurin, and NF-AT. Cell 96, 611-614. https://doi.org/10.1016/S0092-8674(00)80571-1
  5. Klee, C. B., Draetta, G. F. and Hubbard, M. J. (1988) Calcineurin. Adv. Enzymol. Relat. Areas. Mol. Biol. 61, 149-200.
  6. Stark, M. J. (1996) Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation. Yeast 12, 1647-1675. https://doi.org/10.1002/(SICI)1097-0061(199612)12:16<1647::AID-YEA71>3.0.CO;2-Q
  7. Schreiber, S. L. and Crabtree, G. R. (1992) The mechanism of action of cyclosporin A and FK506. Immunol. Today 13, 136-142. https://doi.org/10.1016/0167-5699(92)90111-J
  8. Shibasaki, F. and McKeon, F. (1995) Calcineurin functions in $Ca^{2+}$-activated cell death in mammalian cells. J. Cell Biol. 131, 735-743. https://doi.org/10.1083/jcb.131.3.735
  9. Mulkey, R. M., Endo, S., Shenolikar, S. and Malenka, R. C. (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369, 486-488. https://doi.org/10.1038/369486a0
  10. Molkentin, J. D., Lu, J. R., Antos, C. L., Markham, B., Richardson, J., Robbins, J., Grant, S. R. and Olson, E. N. (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228. https://doi.org/10.1016/S0092-8674(00)81573-1
  11. Bandyopadhyay, J., Lee, J., Lee, J. I., Yu, J. R., Jee, C., Cho, J. H., Jung, S., Lee, M. H., Zannoni, S., Singson, A., Kim, D. H., Koo, H. S. and Ahnn, J. (2002) Calcineurin, a calcium/calmodulin-dependent protein phosphatase, is involved in movement, fertility, egg laying, and growth in Caenorhabditis elegans. Mol. Biol. Cell 13, 3281-3293. https://doi.org/10.1091/mbc.E02-01-0005
  12. Kuhara, A., Inada, H., Katsura, I. and Mori, I. (2002) Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 33, 751-763. https://doi.org/10.1016/S0896-6273(02)00607-4
  13. Lee, J., Jee, C., Song, H. O., Bandyopadhyay, J., Lee, J. I., Yu, J. R., Park, B. J. and Ahnn, J. (2004) Opposing functions of calcineurin and CaMKII regulate G-protein signaling in egg-laying behavior of C. elegans. J. Mol. Biol. 344, 585-595. https://doi.org/10.1016/j.jmb.2004.09.050
  14. Song, H. O., Lee, J., Ji, Y. J., Dwivedi, M., Cho, J. H., Park, B. J. and Ahnn, J. (2010) Calcineurin regulates coelomocyte endocytosis via DYN-1 and CUP-4 in Caenorhabditis elegans. Mol. Cells 30, 255-262. https://doi.org/10.1007/s10059-010-0116-x
  15. Fares, H. and Greenwald, I. (2001) Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159, 133-145.
  16. Schneider, W. J. (1996) Vitellogenin receptors: oocytesspecific members of the low-density lipoprotein receptor supergene family. Int. Rev. Cytol. 166, 103-137. https://doi.org/10.1016/S0074-7696(08)62507-3
  17. Grant, B. and Hirsh, D. (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326. https://doi.org/10.1091/mbc.10.12.4311
  18. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H. and Hirsh, D. (2001) Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579. https://doi.org/10.1038/35078549
  19. Zhang, Y., Grant, B. and Hirsh, D. (2001) RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell 12, 2011-2021. https://doi.org/10.1091/mbc.12.7.2011
  20. Grant, B. D. and Sato, M. (2006) Intracellular trafficking. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.77.1, http://www.wormbook.org.
  21. Dal Santo, P., Logan, M. A., Chisholm, A. D. and Jorgensen, E. M. (1999) The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98, 757-767. https://doi.org/10.1016/S0092-8674(00)81510-X
  22. McGhee, J. D. (2007) The C. elegans intestine. WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.133.1, http://www.wormbook.org.
  23. Parker, S., Walker, D. S., Ly, S. and Baylis, H. A. (2009) Caveolin-2 is required for apical lipid trafficking and suppresses basolateral recycling defects in the intestine of Caenorhabditis elegans. Mol. Biol. Cell 20, 1763-1771. https://doi.org/10.1091/mbc.E08-08-0837
  24. Kimble, J. and Sharrock, W. J. (1983) Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev. Biol. 96, 189-196. https://doi.org/10.1016/0012-1606(83)90322-6
  25. Fares, H. and Grant, B. (2002) Deciphering endocytosis in Caenorhabditis elegans. Traffic 3, 11-9. https://doi.org/10.1034/j.1600-0854.2002.30103.x
  26. Lai, M. M., Hong, J. J., Ruggiero, A. M., Burnett, P. E., Slepnev, V. I., De Camilli, P. and Snyder, S. H. (1999) The calcineurin-dynamin 1 complex as a calcium sensor for synaptic vesicle endocytosis. J. Biol. Chem. 274, 25963-25966. https://doi.org/10.1074/jbc.274.37.25963
  27. Tan, T. C., Valova, V. A., Malladi, C. S., Graham, M. E., Berven, L. A., Jupp, O. J., Hansra, G., McClure, S. J., Sarcevic, B., Boadle, R. A., Larsen, M. R., Cousin, M. A. and Robinson, P. J. (2003) Cdk5 is essential for synaptic vesicle endocytosis. Nat. Cell Biol. 5, 701-710. https://doi.org/10.1038/ncb1020
  28. Jorgensen, E. M., Hartwieg, E., Schuske, K., Nonet, M. L., Jin, Y. and Horvitz, H. R. (1995) Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378, 196-199. https://doi.org/10.1038/378196a0
  29. Nonet, M. L. (1999) Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J. Neurosci. Methods 89, 33-40. https://doi.org/10.1016/S0165-0270(99)00031-X
  30. McIntire, S. L., Reimer, R. J., Schuske, K., Edwards, R. H. and Jorgensen, E. M. (1997) Identification and characterization of the vesicular GABA transporter. Nature 389, 870-876. https://doi.org/10.1038/39908
  31. White, J. G., Albertson, D. G. and Anness, M. A. (1978) Connectivity changes in a class of motoneurone during the development of a nematode. Nature 271, 764-766. https://doi.org/10.1038/271764a0
  32. Colavita, A., Krishna, S., Zheng, H., Padgett, R. W. and Culotti, J. G. (1998) Pioneer axon guidance by UNC-129, a C. elegans TGF-beta. Science 281, 706-709. https://doi.org/10.1126/science.281.5377.706
  33. Morck, C. and Pilon, M. (2006) C. elegans feeding defective mutants have shorter body lengths and increased autophagy. BMC Dev. Biol. 6, 39. https://doi.org/10.1186/1471-213X-6-39
  34. Donohoe, D. R., Jarvis, R. A., Weeks, K., Aamodt, E. J. and Dwyer, D. S. (2009) Behavioral adaptation in C. elegans produced by antipsychotic drugs requires serotonin and is associated with calcium signaling and calcineurin inhibition. Neurosci. Res. 64, 280-289. https://doi.org/10.1016/j.neures.2009.03.012
  35. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94.

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