Abstract
The oocyte-to-embryo transition is a precisely coordinated process in which an oocyte becomes fertilized and transitions to an embryonic program of events. The molecules involved in this process have not been well studied. Recently, a group of interacting molecules in C. elegans have been described as coordinating the oocyte-to-embryo transition with the advancement of the cell cycle. Genes egg-3, egg-4, and egg-5 represent a small class of regulatory molecules known as protein–tyrosine phosphase-like proteins, which can bind phosphorylated substrates and act as scaffolding molecules or inhibitors. These genes are responsible for coupling the movements and activities of regulatory kinase mbk-2 with advancement of the cell cycle during the oocyte-to-embryo transition.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Austin J, Kimble J (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589–599
Bellec Y, Harrar Y, Butaeye C, Darnet S, Bellini C, Faure JD (2002) Pasticcino2 is a protein tyrosine phosphatase-like involved in cell proliferation and differentiation in Arabidopsis. Plant J 32:713–722
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
Burrows AE, Sceurman BK, Kosinski ME, Richie CT, Sadler PL, Schumacher JM, Golden A (2006) The C. elegans Myt1 ortholog is required for the proper timing of oocyte maturation. Development 133:697–709
Chalfie M, Tu Y, Euskirchen G, Ward W, Prasher D (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805
Cheng KC, Klancer R, Singson A, Seydoux G (2009) Regulation of MBK-2/DYRK by CDK-1 and the pseudophosphatases EGG-4 and EGG-5 during the oocyte-to-embryo transition. Cell 139:560–572
Coghlan A, Stajich JE, Harris TW (2006) Comparative genomics in C. elegans, C. briggsae, and other Caenorhabditis species. Methods Mol Biol 351:13–29
Da Costa M, Bach L, Landrieu I, Bellec Y, Catrice O, Brown S, De Veylder L, Lippens G, Inzé D, Faure JD (2006) Arabidopsis PASTICCINO2 is an antiphosphatase involved in regulation of cyclin-dependent kinase A. Plant Cell 18:1426–1437
Detwiler MR, Reuben M, Li X, Rogers E, Lin R (2001) Two zinc finger proteins, OMA-1 and OMA-2, are redundantly required for oocyte maturation in C. elegans. Dev Cell 1:187–199
Ducibella T, Fissore R (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315:257–279
Evsikov AV, Marin de Evsikova C (2009) Gene expression during the oocyte-to-embryo transition in mammals. Mol Reprod Dev 76:805–818
Fire A (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811
Gonczy P, Rose LS (2005) Asymmetric cell division and axis formation in the embryo. WormBook: 1–20
Govindan JA, Greenstein D (2007) Embryogenesis: anchors away! Curr Biol 17:R890–R892
Granger L, Martin E, Segalat L (2004) Mos as a tool for genome-wide insertional mutagenesis in Caenorhabditis elegans: results of a pilot study. Nucleic Acids Res 32:e117
Greenstein D (2005) Control of oocyte meiotic maturation and fertilization. WormBook: 1–12
Hadwiger G, Dour S, Arur S, Fox P, Nonet ML (2010) A monoclonal antibody toolkit for C. elegans. PLoS One 5:e10161
Harris JE, Govindan JA, Yamamoto I, Schwartz J, Kaverina I, Greenstein D (2006) Major sperm protein signaling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev Biol 299:105–121
Hedgecock E, Sulston J, Thomson J (1983) Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220:1277–1299
Hubbard EJ, Greenstein D (2000) The Caenorhabditis elegans gonad: a test tube for cell and developmental biology. Dev Dyn 218:2–22
Jensen VL, Albert PS, Riddle DL (2007) Caenorhabditis elegans SDF-9 enhances insulin/insulin-like signaling through interaction with DAF-2. Genetics 177:661–666
Johnston WL, Krizus A, Dennis JW (2006) The eggshell is required for meiotic fidelity, polar-body extrusion and polarization of the C. elegans embryo. BMC Biol 4:36
Kadandale P, Chatterjee I, Singson A (2009) Germline transformation of Caenorhabditis elegans by injection. Methods Mol Biol 518:123–133
Kadandale P, Stewart-Michaelis A, Gordon S, Rubin J, Klancer R, Schweinsberg P, Grant BD, Singson A (2005) The egg surface LDL receptor repeat-containing proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans. Curr Biol 15:2222–2229
Kimble J, Crittenden S (2005) Germline proliferation and its control. WormBook: 1–14
Klass M, Wolf N, Hirsh D (1976) Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans. Dev Biol 52:1–18
Kuwabara PE (2003) The multifaceted C. elegans major sperm protein: an ephrin signaling antagonist in oocyte maturation. Genes Dev 17:155–161
L’Hernault SW (2006) Spermatogenesis. WormBook: 1–14
LaMunyon CW, Ward S (1994) Assessing the viability of mutant and manipulated sperm by artificial insemination of Caenorhabditis elegans. Genetics 138:689–692
Lin R (2003) A gain-of-function mutation in oma-1, a C. elegans gene required for oocyte maturation, results in delayed degradation of maternal proteins and embryonic lethality. Dev Biol 258:226–239
Maeda I, Kohara Y, Yamamoto M, Sugimoto A (2001) Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr Biol 11:171–176
Maruyama R, Velarde N, Klancer R, Gordon S, Kadandale P, Parry JM, Hang JS, Rubin J, Stewart-Michaelis A, Schweinsberg P, Grant BD, Piano F, Sugimoto A, Singson A (2007) EGG-3 regulates cell-surface and cortex rearrangements during egg activation in Caenorhabditis elegans. Curr Biol 17:1555–1560
McCarter J, Bartlett B, Dang T, Schedl T (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205:111–128
McNally KL, McNally FJ (2005) Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282:218–230
Nishi Y, 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
Nishi Y, Rogers E, Robertson SM, Lin R (2008) Polo kinases regulate C. elegans embryonic polarity via binding to DYRK2-primed MEX-5 and MEX-6. Development 135:687–697
Oegema K, Hyman AA (2006) Cell division. WormBook: 1–40
Parry JM, Velarde N, Lefkovith AJ, Zegarek MH, Hang JS, Ohm J, Klancer R, Maruyama R, Druzhinina MK, Grant BD, Piano F, Singson A (2009) EGG-4 and EGG-5 link events of the oocyte-to-embryo transition with meiotic progression in C. elegans. Curr Biol 19:1752–1757
Pellettieri J, Reinke V, Kim SK, Seydoux G (2003) Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev Cell 5:451–462
Praitis V (2006) Creation of transgenic lines using microparticle bombardment methods. Methods Mol Biol 351:93–107
Putiri E, Zannoni S, Kadandale P, Singson A (2004) Functional domains and temperature-sensitive mutations in SPE-9, an EGF repeat-containing protein required for fertility in Caenorhabditis elegans. Dev Biol 272:448–459
Quintin S, Mains P, Zinke A, Hyman AA (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
Raich WB, Moorman C, Lacefield CO, Lehrer J, Bartsch D, Plasterk RH, Kandel ER, Hobert O (2003) Characterization of Caenorhabditis elegans homologs of the Down syndrome candidate gene DYRK1A. Genetics 163:571–580
Sato K, Sato M, Audhya A, Oegema K, Schweinsberg P, Grant BD (2006) Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans. Mol Biol Cell 17:3085–3094
Schubert CM, Lin R, de Vries CJ, Plasterk RH, Priess JR (2000) MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol Cell 5:671–682
Singson A, Hang J, Parry JM (2008) Genes required for the common miracle of fertilization. Int J Dev Biol 52:647–656
Singson A, Mercer KB, L’Hernault SW (1998) The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell 93:71–79
Stitzel ML, Cheng K, Seydoux G (2007) Regulation of MBK-2/Dyrk kinase by dynamic cortical anchoring during the oocyte-to-zygote transition. Curr Biol 17:1545–1554
Sulston J, Horvitz H (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110–156
Sundaram M (2006) RTK/Ras/MAPK signaling. WormBook: 1–19
Tonks N (2009) Pseudophosphatases: grab and hold on. Cell 139:464–465
Uwanogho DA, Hardcastle Z, Balogh P, Mirza G, Thornburg KL, Ragoussis J, Sharpe PT (1999) Molecular cloning, chromosomal mapping, and developmental expression of a novel protein tyrosine phosphatase-like gene. Genomics 62:406–416
Ward S, Carrel JS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73:304–321
Yamamoto I, Kosinski ME, Greenstein D (2006) Start me up: cell signaling and the journey from oocyte to embryo in C. elegans. Dev Dyn 235:571–585
Yang HY, McNally K, McNally FJ (2003) MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C elegans. Dev Biol 260:245–259
Zhang Y, Foster JM, Nelson LS, Ma D, Carlow CK (2005) The chitin synthase genes chs-1 and chs-2 are essential for C. elegans development and responsible for chitin deposition in the eggshell and pharynx, respectively. Dev Biol 285:330–339
Acknowledgments
The authors would like to thank members of the Singson Lab for input and discussion. Work in the Singson Lab has been supported by funds from the Waksman Institute and a grant from the United States National Institutes of Health (R01 HD054681).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Parry, J.M., Singson, A. (2011). EGG Molecules Couple the Oocyte-to-Embryo Transition with Cell Cycle Progression. In: Kubiak, J. (eds) Cell Cycle in Development. Results and Problems in Cell Differentiation. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19065-0_7
Download citation
DOI: https://doi.org/10.1007/978-3-642-19065-0_7
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-19064-3
Online ISBN: 978-3-642-19065-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)