Browse > Article
http://dx.doi.org/10.5483/BMBRep.2010.43.2.069

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)
Publication Information
BMB Reports / v.43, no.2, 2010 , pp. 69-78 More about this Journal
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
Asymmetric division; Caenorhabditis elegans; PAR proteins; Translational control; Ubiquitin proteolysis;
Citations & Related Records

Times Cited By Web Of Science : 2  (Related Records In Web of Science)
Times Cited By SCOPUS : 2
연도 인용수 순위
1 Goldstein, B. and Macara, I. (2007) The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 13, 609-622   DOI   ScienceOn
2 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   DOI   ScienceOn
3 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   DOI   ScienceOn
4 Farley, B. and Ryder, S. (2008) Regulation of maternal mRNAs in early development. Crit. Rev. Biochem. Mol. Biol. 43, 135-162   DOI   ScienceOn
5 Galli, M. and van den Heuvel, S. (2008) Determination of the cleavage plane in early C. elegans embryos. Annu. Rev. Genet. 42, 389-411   DOI   ScienceOn
6 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
7 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   DOI   ScienceOn
8 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   DOI   ScienceOn
9 DeRenzo, C., Reese, K. and Seydoux, G. (2003) Exclusion of germ plasm proteins from somatic lineage by cullin-dependent degradation. Nature 424, 685-689   DOI   ScienceOn
10 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
11 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   DOI   ScienceOn
12 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   DOI   ScienceOn
13 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   DOI   ScienceOn
14 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   DOI   ScienceOn
15 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   DOI   ScienceOn
16 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   PUBMED
17 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   DOI   ScienceOn
18 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   DOI   PUBMED   ScienceOn
19 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   DOI   ScienceOn
20 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   DOI   ScienceOn
21 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   DOI   PUBMED   ScienceOn
22 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   DOI   ScienceOn
23 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   DOI   ScienceOn
24 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   DOI   ScienceOn
25 Kuersten, S. and Goodwin, E. (2003) The power of the 3'-UTR: translational control and development. Nat. Rev. Genet. 4, 626-637   DOI   ScienceOn
26 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   DOI   ScienceOn
27 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   DOI   ScienceOn
28 Bowerman, B. and Kurz, T. (2006) Degrade to create: developmental requirements for ubiquitin mediated proteolysis during early C. elegans embryogenesis. Development 133, 773-784   DOI   ScienceOn
29 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   DOI   ScienceOn
30 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   PUBMED
31 Farley, B., Pagano, J. and Ryder, S. (2008) RNA target specificity of the embryonic cell fate determinant POS-1. RNA 14, 2685-2697   DOI   ScienceOn
32 Cowan, C. and Hyman, A. (2007) Acto-myosin reorganization and PAR polarity in C. elegans. Development 134, 1035-1043   DOI   ScienceOn
33 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   DOI   ScienceOn
34 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   DOI   ScienceOn
35 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   DOI   ScienceOn
36 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   DOI   ScienceOn
37 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   DOI   ScienceOn
38 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   DOI   ScienceOn
39 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   DOI   ScienceOn
40 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   DOI   ScienceOn
41 Nance, J. (2005) PAR proteins and the establishment of cell polarity during C. elegans development. BioEssays 27, 126-135   DOI   PUBMED   ScienceOn
42 Vardy, L. and Orr-Weaver, T. (2007) Regulating translation of maternal messages: multiple repression mechanisms. Trends Cell Biol. 17, 547-554   DOI   ScienceOn
43 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
44 Gonczy, P. (2008) Mechanisms of asymmetric cell division: flies and worms pave the way. Nat. Rev. Mol. Cell. Biol. 9, 355-366   DOI   ScienceOn
45 Mlodzik, M., Gibson, G. and Gehring, W. (1990) Effects of ectopic expression of caudal during Drosophila development. Development 109, 271-277   PUBMED
46 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   PUBMED
47 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   DOI   ScienceOn
48 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   DOI   ScienceOn
49 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   DOI   ScienceOn
50 McNally, K., Audhya, A., Oegema, K. and McNally, F. (2006) Katanin controls mitotic and meiotic spindle length. J. Cell. Biol. 175, 881-891   DOI   ScienceOn
51 Sonoda, J. and Wharton, R. (2001) Drosophila Brain Tumor is a translational repressor. Genes. Dev. 15, 762-773   DOI   ScienceOn
52 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   DOI   ScienceOn
53 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   DOI
54 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   DOI   ScienceOn
55 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   DOI   ScienceOn
56 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   DOI   ScienceOn
57 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   DOI   ScienceOn
58 Suzuki, A. and Ohno, S. (2006) The PAR-aPKC system; lessons in polarity. J. Cell. Sci. 119, 979-998   DOI   ScienceOn
59 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   DOI   ScienceOn
60 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   DOI   ScienceOn
61 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   DOI   ScienceOn
62 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   DOI   ScienceOn
63 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   DOI   ScienceOn
64 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   DOI   ScienceOn