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Control of asymmetric cell division in early C. elegans embryogenesis: teaming-up translational repression and protein degradation

  • Hwang, Sue-Yun (Department of Animal Biotechnology, Graduate School of Informatics and Biotechnology, Hankyong National University) ;
  • Rose, Lesilee S. (Department of Molecular and Cellular Biology, University of California)
  • Published : 2010.02.28

Abstract

Asymmetric cell division is a fundamental mechanism for the generation of body axes and cell diversity during early embryogenesis in many organisms. During intrinsically asymmetric divisions, an axis of polarity is established within the cell and the division plane is oriented to ensure the differential segregation of developmental determinants to the daughter cells. Studies in the nematode Caenorhabditis elegans have contributed greatly to our understanding of the regulatory mechanisms underlying cell polarity and asymmetric division. However, much remains to be elucidated about the molecular machinery controlling the spatiotemporal distribution of key components. In this review we discuss recent findings that reveal intricate interactions between translational control and targeted proteolysis. These two mechanisms of regulation serve to carefully modulate protein levels and reinforce asymmetries, or to eliminate proteins from certain cells.

Keywords

References

  1. Farley, B. and Ryder, S. (2008) Regulation of maternal mRNAs in early development. Crit. Rev. Biochem. Mol. Biol. 43, 135-162 https://doi.org/10.1080/10409230801921338
  2. Vardy, L. and Orr-Weaver, T. (2007) Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 17, 547-554 https://doi.org/10.1016/j.tcb.2007.09.002
  3. Evans, T. C. and Hunter, C. P. (2005) Translational control of maternal RNAs (November 10, 2005), WormBook, ed. The C. elegans Research Community, WormBook, doi/ 10.1895/wormbook.1.34.1, http://www.wormbook.org
  4. Kuersten, S. and Goodwin, E. (2003) The power of the 3'-UTR: translational control and development. Nat. Rev. Genet. 4, 626-637 https://doi.org/10.1038/nrg1125
  5. Cowan, C. and Hyman, A. (2007) Acto-myosin reorganization and PAR polarity in C. elegans. Development 134, 1035-1043 https://doi.org/10.1242/dev.000513
  6. Galli, M. and van den Heuvel, S. (2008) Determination of the cleavage plane in early C. elegans embryos. Annu. Rev. Genet. 42, 389-411 https://doi.org/10.1146/annurev.genet.40.110405.090523
  7. Gonczy, P. (2008) Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell. Biol. 9, 355-366 https://doi.org/10.1038/nrm2388
  8. Goldstein, B. and Macara, I. (2007) The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622 https://doi.org/10.1016/j.devcel.2007.10.007
  9. Suzuki, A. and Ohno, S. (2006) The PAR-aPKC system; lessons in polarity. J. Cell. Sci. 119, 979-998 https://doi.org/10.1242/jcs.02898
  10. Nance, J. (2005) PAR proteins and the establishment of cell polarity during C. elegans development. BioEssays 27, 126-135 https://doi.org/10.1002/bies.20175
  11. Hao, Y., Boyd, L. and Seydoux, G. (2006) Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev. Cell 10, 199-208
  12. Labbe, J-C., Pacquelet, A., Marty, T. and Gotta, M. (2006) A genomewide screen for suppressors of par-2 uncovers potential regulators of PAR-protein dependent cell polarity in Caenorhabditis elegans. Genetics. 174, 285-295 https://doi.org/10.1534/genetics.106.060517
  13. Hyenne, V., Desrosiers, M. and Labbe, J-C. (2008) C. elegans Brat homologs regulate PAR protein-dependent polarity and asymmetric cell division. Dev. Biol. 321, 368-378 https://doi.org/10.1016/j.ydbio.2008.06.037
  14. Sonoda, J. and Wharton, R. (2001) Drosophila Brain Tumor is a translational repressor. Genes. Dev. 15, 762-773 https://doi.org/10.1101/gad.870801
  15. Pacquelet, A., Zanin, E., Ashiono, C. and Gotta, M. (2008) PAR-6 levels are regulated by NOS-3 in a CUL-2 dependent manner in Caenorhabditis elegans. Dev. Biol. 319, 267-272 https://doi.org/10.1016/j.ydbio.2008.04.016
  16. Kraemer, B., Crittenden, S., Gallegos, M., Moulder, G., Barstead, R., Kimble, J. and Wickens, M. (1999) NANOS-3 and FBF proteins physically interact to control the spermoocyte switch in Caenorhabditis elegans. Cur. Biol. 9, 1009-1018 https://doi.org/10.1016/S0960-9822(99)80449-7
  17. Starostina, N., Lim, J-M., Schvarzstein, M., Wells, L., Spence, A. and Kipreos, E. (2007) A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination. Dev. Cell 13, 127-139 https://doi.org/10.1016/j.devcel.2007.05.008
  18. DeRenzo, C., Reese, K. and Seydoux, G. (2003) Exclusion of germ plasm proteins from somatic lineage by cullin-dependent degradation. Nature 424, 685-689 https://doi.org/10.1038/nature01887
  19. Liu, J., Vasudevan, S. and Kipreos, E. (2004) CUL-2 and ZYG-11 promote meiotic anaphase II and the proper placement of the anterior-posterior axis in C. elegans. Development 131, 3515-3525
  20. Lee, C-Y., Wilkinson, B., Siegrist, S., Wharton, R. and Doe, C. (2006) Brat is a Miranda cargo protein that promotes neuronal differentiation and neuroblast self renewal. Dev. Cell 10, 441-449 https://doi.org/10.1016/j.devcel.2006.01.017
  21. Frank, D. and Roth, M. (1998) ncl-1 is required for the regulation of cell size and ribosomal RNA synthesis in Caenorhabditis elegans. J. Cell. Sci. 140, 1321-1329 https://doi.org/10.1083/jcb.140.6.1321
  22. Gudgen, M., Chandrasekaran, A, Frazier, T. and Boyd, L. (2004) Interactions within the ubiquitin pathway of Caenorhabditis elegans. Biochem. Biophys. Res. Comm. 325, 479-486 https://doi.org/10.1016/j.bbrc.2004.10.047
  23. Bowerman, B. and Kurz, T. (2006) Degrade to create: developmental requirements for ubiquitin mediated proteolysis during early C. elegans embryogenesis. Development 133, 773-784 https://doi.org/10.1242/dev.02276
  24. Schubert, C., Lim, R., de Vries, D., Plastert, R. and Priess, J. (2000) MEX-5 and MEX-6 function to establish soma/ germline asymmetry in early C. elegans embryos. Mol. Cell 5, 671-682 https://doi.org/10.1016/S1097-2765(00)80246-4
  25. Ogura, K-I., Kishimoto, N., Mitani, S., Gengyo-Ando, K. and Kohara, Y. (2003) Translational control of maternal glp-1 mRNA by POS-1 and its interacting protein SPN-4 in Caenorhabditis elegans. Development 140, 2495-2503
  26. Reese, K., Dunn, M., Waddle, J. and Seydoux, G. (2000) Asymmetric segregation of PIE-1 in C. elegans is mediated by two complimentary mechanisms that act through separate PIE-1 protein domains. Mol. Cell. 6, 445-455 https://doi.org/10.1016/S1097-2765(00)00043-5
  27. Pagano, J., Farley, B., McCoig, L. and Ryder, S. (2007) Molecular basis of RNA recognition by the embryonic polarity determinant MEX-5. J. Biol. Chem. 282, 8883-8894 https://doi.org/10.1074/jbc.M700079200
  28. Tenlen, J., Schisa, J., Diede, S. and Page, B. (2006) Reduceddosage of pos-1 suppresses Mex mutants and reveals complex interaction among CCCH zinc-finger proteins during Caenorhabditis elegans embryogenesis. Genetics 174, 1933-1945 https://doi.org/10.1534/genetics.105.052621
  29. Mello, C., Draper, B. and Priess, J. (1994) The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77, 95-106 https://doi.org/10.1016/0092-8674(94)90238-0
  30. Marin, V. and Evans, T. (2003) Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130, 2623-2632 https://doi.org/10.1242/dev.00486
  31. Lei, H., Liu, J., Fukushige, T., Fire, A. and Kraus, M. (2009) Caudal-like PAL-1 directly activates the bodywall muscle module regulator hlh-1 in C. elegans to initiate the embryonic muscle gene regulatory network. Development 136, 1241-1249 https://doi.org/10.1242/dev.030668
  32. Edgar, L., Carr, S., Wang, H. and Wood, W. (2001) Zygotic expression of the caudal homolog pal-1 is required for posterior patterning in Caenorhabditis elegans embryogenesis. Dev. Biol. 229, 71-88 https://doi.org/10.1006/dbio.2000.9977
  33. Mlodzik, M., Gibson, G. and Gehring, W. (1990) Effects of ectopic expression of caudal during Drosophila development. Development 109, 271-277
  34. Hunter, C. and Kenyon, C. (1996) Spatial and temporal controls target pal-1 blastomere specification activity to a single blastomere lineage in C. elegans embryo. Cell 87, 217-226 https://doi.org/10.1016/S0092-8674(00)81340-9
  35. Bowerman, B., Ingran, M. and Hunter, C. (1997) The maternal par genes and the segregation of cell fate specification activities in early Caenorhabditis elegans embryos. Development 124, 3815-3826
  36. Mootz, D., Ho, D. and Hunter, C. (2004) The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans PAL-1. Development 131, 3263-3272 https://doi.org/10.1242/dev.01196
  37. Huang, N., Mootz, D., Albertha, J., Walhout, J., Vidal, M. and Hunter, C. (2002) MEX-3 interacting proteins link cell polarity to asymmetric gene expression in Caenorhabditis elegans. Development 129, 747-759
  38. Pagano, J., Farley, B., Essien, K. and Ryder, S. (2009) RNA recognition by the embryonic cell fate determinant and germline totipotency factor MEX-3. Proc. Natl. Acad. Sci. U.S.A. 106, 20252-20257 https://doi.org/10.1073/pnas.0907916106
  39. Jadhav, S., Rana, M. and Subramaniam, K. (2008) Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos-2 to primordial germ cells. Development 135, 1803-1812 https://doi.org/10.1242/dev.013656
  40. Farley, B., Pagano, J. and Ryder, S. (2008) RNA target specificity of the embryonic cell fate determinant POS-1. RNA 14, 2685-2697 https://doi.org/10.1261/rna.1256708
  41. McNally, K., Audhya, A., Oegema, K. and McNally, F. (2006) Katanin controls mitotic and meiotic spindle length. J. Cell. Biol. 175, 881-891 https://doi.org/10.1083/jcb.200608117
  42. Kurz, T., Pintard, L., Willis, J., Hamill, D., Gonczy, P., Peter, M. and Bowerman, B. (2002) Cytoskeletal regulation by the Nedd8 ubiquitin-like protein modification pathway. Science 295, 1294-1298 https://doi.org/10.1126/science.1067765
  43. Srayko, M., Buster, D., Bazirgan, O., McNally, F. and Mains, P. (2000) MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes. Dev. 14,1072-1084
  44. Clark-Maguire, S. and Mains, P. (1994) Localization of the mei-1 gene product of Caenorhabditis elegans, a meiotic- specific spindle component. J. Cell. Biol. 126, 199-209 https://doi.org/10.1083/jcb.126.1.199
  45. Johnson, J-L., Lu, C., Raharjo, E., McNally, K., McNally, F. and Mains, P. (2009) Levels of the ubiquitin ligase substrate adaptor MEL-26 are inversely correlated with MEI- 1/katanin microtubule-severing activity during both meiosis and mitosis. Dev. Biol. 330, 349-357 https://doi.org/10.1016/j.ydbio.2009.04.004
  46. Lu, C. and Mains, P. (2007) The C. elegans anaphase promoting complex and MBK-2/DYRK kinase act redundantly with CUL-3/MEL-26 ubiquitin ligase to degrade MEI-1 microtubule- severing activity after meiosis. Dev. Biol. 302, 438-447 https://doi.org/10.1016/j.ydbio.2006.09.053
  47. Pang, K., Ishidate, T., Nakamura, K., Shirayama, M., Trzepacz, C., Schubert, C., Priess, J. and Mello, C. (2004) The minibrain kinase homolog, mbk-2, is required for spindle positioning and asymmetric cell division in early C. elegans embryos. Dev. Biol. 265, 127-139 https://doi.org/10.1016/j.ydbio.2003.09.024
  48. Pellettieri, J., Reinke, V., Kim, S. K. and Seydoux, G. (2003). Coordinated activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell. 5, 451-462 https://doi.org/10.1016/S1534-5807(03)00231-4
  49. Pintard, L., Kurz, T., Glaser, S, Willis, J, Peter, M. and Bowerman, B. (2003) Neddylation and deneddylation of CUL-3 is required to target MEI-1/katanin for degradation at the meiosis-to-mitosis transition in C. elegans. Curr. Biol. 13, 911-921 https://doi.org/10.1016/S0960-9822(03)00336-1
  50. Pintard, L., Willis, J., Willems, A., Johnson, J., Srayko, M., Kurz, T., Glaser, S., Mains, P., Tyers, M. and Bowerman, B. (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
  51. Quintin, S., Mains, P., Zinke, A. and Hyman, A. (2003). The mbk-2 kinase is required for inactivation of MEI-1/katanin in the one-cell Caenorhabditis elegans embryo. EMBO Rep. 4, 1175-1181 https://doi.org/10.1038/sj.embor.7400029
  52. Stitzel, M., Pellettieri, J. and Seydoux, G. (2006) The C. elegans DYRK Kinase MBK-2 marks oocyte proteins for degradation in response to meiotic maturation. Curr. Biol. 16, 56-62 https://doi.org/10.1016/j.cub.2005.11.063
  53. Stitzel., M., Cheng, K. and Seydoux, G. (2007) Regulation of MBK-2/DYRK kinase by dynamic cortical anchoring during the oocyte-to-zygote transition. Curr. Biol. 17, 1545-1554 https://doi.org/10.1016/j.cub.2007.08.049
  54. Li, W., DeBella, L., Guven-Ozkan, T., Lin, R. and Rose, L. (2009) An eIF4E-binding protein regulates katanin protein levels in C. elegans embryos. J. Cell. Biol. 187, 33-42 https://doi.org/10.1083/jcb.200903003
  55. Nakamura, A., Sato, K. and Hanyu-Nakamura, K. (2004) Drosophila Cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell. 6, 69-78 https://doi.org/10.1016/S1534-5807(03)00400-3
  56. Nelson, M., Leidal, A. and Smibert, C. (2004) Drosophila Cup is an eIF4E-binding protein that functions in Smaugmediated translational repression. EMBO J. 23, 150-159 https://doi.org/10.1038/sj.emboj.7600026
  57. Nishi, Y. and Lin, R. (2005) DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. Dev. Biol. 288, 139-149 https://doi.org/10.1016/j.ydbio.2005.09.053
  58. Shirayama, M., Soto, M., Ishidate, T., Kim, S., Nakamura, K., Bei, Y., van den Heuvel, S. and Mello. C. (2006) The conserved kinases CDK-1, GSK-3, KIN-19, and MBK-2 promote OMA-1 destruction to regulate the oocyte-to-embryo transition in C. elegans. Curr. Biol. 16, 47-55 https://doi.org/10.1016/j.cub.2005.11.070
  59. DeBella, L, Hayashi, A. and Rose, L. (2006) LET-711, the Caenorhabditis elegans NOT1 ortholog, is required for spindle positioning and regulation of microtubule length in embryos. Mol. Biol. Cell. 17, 4911-4924 https://doi.org/10.1091/mbc.E06-02-0107
  60. Collart, M. and Timmers, H. (2004) The eukayotic Ccr4-Not complex: a regulatory platform integrating mRNA metabolism with cellular signaling pathways. Prog. Nucleic. Acid. Res. Mol. Biol. 77, 289-322 https://doi.org/10.1016/S0079-6603(04)77008-7
  61. Cui, Y., Ramnarain, D., Chiang, Y., Ding, L., McMahon, J. and Denis, C. (2008) Genome wide expression analysis of CCR4-NOT complex indicates that it consists of three modules with the NOT module controlling SAGA-responsive genes. Mol. Genet. Genomics. 279, 323-337 https://doi.org/10.1007/s00438-007-0314-1
  62. Panasenko, O., Landrieux, E., Feuermann, M, Finka, A., Paquet, N. and Collart, M. (2006) The yeast Ccr4-Not complex controls uniquitination of the nascent-associated polypeptide (NAC-EGD) complex. J. Biol. Chem. 281, 31389-31398 https://doi.org/10.1074/jbc.M604986200
  63. Albert, T., Hanzawa, H., Legtenberg, Y., de Ruwe, M., van den Heuvel, F., Collart, M., Boelens, R. and Timmers, H. (2002) Identification of a ubiquitin-protein ligase subunit within the CCR4-NOT transcription repressor complex. EMBO J. 21, 355-364 https://doi.org/10.1093/emboj/21.3.355
  64. Gallo, C., Munro, E., Rasoloson, D., Merritt, C. and Seydoux, G. (2008) Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryo. Dev. Biol. 323, 76-87 https://doi.org/10.1016/j.ydbio.2008.07.008

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