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MEL-47, a novel protein required for early cell divisions in the nematode Caenorhabditis elegans

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Abstract

In the early Caenorhabditis elegans embryo, a rapid succession of cell divisions, many of them asymmetric, form blastomeres that differ in size, cell cycle duration and developmental potential. These early cell cycles are highly regulated and controlled by maternally contributed products. We describe here a novel gene, mel-47, that is required maternally for the proper execution of the early cell cycles. mel-47(yt2) mutants arrest as completely disorganized embryos with 50–80 cells of variable size. The earliest defects we found are changes in the absolute and relative duration of the very early embryonic cell cycles. In particular, the posterior cell of the two-cell embryo divides late compared with its anterior sister. Frequently the daughter cells remain connected through chromatin bridges after the early cleavage divisions indicating that the chromosomes do not segregate properly. The cell cycle delay can be suppressed by knocking down a DNA replication check point. Therefore we propose that mel-47 is required for proper DNA replication in the early embryo.

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References

  • Brauchle M, Baumer K, Gonczy P (2003) Differential activation of the DNA replication checkpoint contributes to asynchrony of cell division in C. elegans embryos. Curr Biol 13:819–827

    Article  CAS  Google Scholar 

  • Brunschwig K, Wittmann C, Schnabel R, Burglin TR, Tobler H, Muller F (1999) Anterior organization of the Caenorhabditis elegans embryo by the labial-like Hox gene ceh-13. Development 126:1537–1546

    CAS  Google Scholar 

  • Cote J, Richard S (2005) Tudor domains bind symmetrical dimethylated arginines. J Biol Chem 280:28476–28483

    Article  CAS  Google Scholar 

  • Edgar LG, McGhee JD (1988) DNA synthesis and the control of embryonic gene expression in C. elegans. Cell 53:589–599

    Article  CAS  Google Scholar 

  • Edgar LG, Wolf N, Wood WB (1994) Early transcription in Caenorhabditis elegans embryos. Development 120:443–451

    CAS  Google Scholar 

  • Encalada SE et al (2000) DNA replication defects delay cell division and disrupt cell polarity in early Caenorhabditis elegans embryos. Dev Biol 228:225–238

    Article  CAS  Google Scholar 

  • Fay DS (2005) The cell cycle and development: lessons from C. elegans. Semin Cell Dev Biol 16:397–406

    Article  CAS  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  CAS  Google Scholar 

  • Hodgkin J (1999) Conventional genetics. In: Hope IA (ed) C. elegans a practical approach. Oxford University Press, Oxford, pp 245–270

    Google Scholar 

  • Hodgkin J (2002) Exploring the envelope. Systematic alteration in the sex-determination system of the nematode Caenorhabditis elegans. Genetics 162:767–780

    Google Scholar 

  • Holway AH, Kim SH, La Volpe A, Michael WM (2006) Checkpoint silencing during the DNA damage response in Caenorhabditis elegans embryos. J Cell Biol 172:999–1008

    Article  CAS  Google Scholar 

  • Jin Y (1999) Transformation. In: Hope IA (ed) C. elegans a practical approach. Oxford University Press, Oxford, pp 69–96

    Google Scholar 

  • Kamath RS et al (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237

    Article  CAS  Google Scholar 

  • Kodoyianni V, Maine EM, Kimble J (1992) Molecular basis of loss-of-function mutations in the glp-1 gene of Caenorhabditis elegans. Mol Biol Cell 3:1199–1213

    CAS  Google Scholar 

  • Labouesse M, Mango SE (1999) Patterning the C. elegans embryo: moving beyond the cell lineage. Trends Genet 15:307–313

    Article  CAS  Google Scholar 

  • Lo MC, Gay F, Odom R, Shi Y, Lin R (2004) Phosphorylation by the beta-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans. Cell 117:95–106

    Article  CAS  Google Scholar 

  • Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. Embo J 10:3959–3970

    CAS  Google Scholar 

  • Miller DM, Shakes DC (1995) Immunofluorescence microscopy. In: Epstein HF, Shakes DC (eds) Caenorhabditis elegans modern biological analysis of an organism. Academic, San Diego, pp 365–394

    Google Scholar 

  • Molin L, Schnabel H, Kaletta T, Feichtinger R, Hope IA, Schnabel R (1999) Complexity of developmental control: analysis of embryonic cell lineage specification in Caenorhabditis elegans using pes-1 as an early marker. Genetics 151:131–141

    CAS  Google Scholar 

  • Newman-Smith ED, Rothman JH (1998) The maternal-to-zygotic transition in embryonic patterning of Caenorhabditis elegans. Curr Opin Genet Dev 8:472–480

    Article  CAS  Google Scholar 

  • Ponting CP (1997) Tudor domains in proteins that interact with RNA. Trends Biochem Sci 22:51–52

    Article  CAS  Google Scholar 

  • Powell-Coffman JA, Knight J, Wood WB (1996) Onset of C. elegans gastrulation is blocked by inhibition of embryonic transcription with an RNA polymerase antisense RNA. Dev Biol 178:472–483

    Article  CAS  Google Scholar 

  • Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157:1217–1226

    CAS  Google Scholar 

  • Reese KJ, Dunn MA, Waddle JA, Seydoux G (2000) Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol Cell 6:445–455

    Article  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schierenberg E, Wood WB (1985) Control of cell-cycle timing in early embryos of Caenorhabditis elegans. Dev Biol 107:337–354

    Article  CAS  Google Scholar 

  • Schnabel H (1999) Microscopy. In: Hope IA (ed) C. elegans a practical approach. Oxford University Press, Oxford, pp 119–141

    Google Scholar 

  • Seydoux G, Fire A (1994) Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans. Development 120:2823–2834

    CAS  Google Scholar 

  • Stiernagle T (1999) Maintenance of C. elegans. In: Hope IA (ed) C. elegans a practical approach. Oxford University Press, Oxford, pp 51–67

    Google Scholar 

  • Streit A et al (2002) Conserved regulation of the Caenorhabditis elegans labial/Hox1 gene ceh-13. Dev Biol 242:96–108

    Article  CAS  Google Scholar 

  • Thomson T, Lasko P (2005) Tudor and its domains: germ cell formation from a Tudor perspective. Cell Res 15:281–291

    Article  CAS  Google Scholar 

  • Wallenfang MR, Seydoux G (2000) Polarization of the anterior–posterior axis of C. elegans is a microtubule-directed process. Nature 408:89–92

    Article  CAS  Google Scholar 

  • Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28:160–164

    Article  CAS  Google Scholar 

  • Wittmann C et al (1997) The expression of the C. elegans labial-like Hox gene ceh-13 during early embryogenesis relies on cell fate and on anteroposterior cell polarity. Development 124:4193–4200

    CAS  Google Scholar 

  • Yochem J, Gu T, Han M (1998) A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis. Genetics 149:1323–1334

    CAS  Google Scholar 

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Acknowledgments

Some of the C. elegans strains were supplied by the Caenorhabditis Genetics Center, which is funded by the National Institutes of Health National Center for Research Resources. We thank Pierre Gönczy for originally pointing out to us that the P1 cell divided late. We are thankful to the many members of the worm community who provided us with strains, clones and regents, in particular Rueyling Lin, Min Han, Ray Hong, Yuji Kohara, Pierre Gönczy and Ralf J. Sommer. Special thanks to Fritz Müller and Verena Zimmermann, who have ensured that we had unlimited access to the Müller lab strain and clone collections and who have sent many packages from Fribourg to Tübingen. We thank all the members of our lab and of the Sommer and Spang labs for helpful discussions and technical support in particular Metta Ribesell for assistance with microscopy, Linda Nemetschke for picking countless worms and Hedda May for preparing all the worm plates. We thank Ralf Sommer, Pierre Gönczy and Ray Hong for critical reading of earlier versions of the manuscript and Johannes Soeding for assistance with the statistical analysis of data.

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  1. Max Planck Institute for Developmental Biology, Spemannstrasse 37, 72076, Tübingen, Germany

    Ryuji Minasaki & Adrian Streit

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  1. Ryuji Minasaki
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  2. Adrian Streit
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Correspondence to Adrian Streit.

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Communicated by S. Hekimi.

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Minasaki, R., Streit, A. MEL-47, a novel protein required for early cell divisions in the nematode Caenorhabditis elegans . Mol Genet Genomics 277, 315–328 (2007). https://doi.org/10.1007/s00438-006-0191-z

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  • DOI: https://doi.org/10.1007/s00438-006-0191-z

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