The Synaptonemal Complex of Basal Metazoan Hydra: More Similarities to Vertebrate than Invertebrate Meiosis Model Organisms

Department of Cell and Developmental Biology, Biocenter, University of Würzburg, D-97074 Würzburg, Germany

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Corresponding author: E-mail address: johanna.fraune@uni-wuerzburg.de (Johanna Fraune); E-mail address: benavente@biozentrum.uni-wuerzburg.de (Ricardo Benavente)

摘要

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Abstract: The synaptonemal complex (SC) is an evolutionarily well-conserved structure that mediates chromosome synapsis during prophase of the first meiotic division. Although its structure is conserved, the characterized protein components in the current metazoan meiosis model systems (Drosophila melanogaster, Caenorhabditis elegans, and Mus musculus) show no sequence homology, challenging the question of a single evolutionary origin of the SC. However, our recent studies revealed the monophyletic origin of the mammalian SC protein components. Many of them being ancient in Metazoa and already present in the cnidarian Hydra. Remarkably, a comparison between different model systems disclosed a great similarity between the SC components of Hydra and mammals while the proteins of the ecdysozoan systems (D. melanogaster and C. elegans) differ significantly. In this review, we introduce the basal-branching metazoan species Hydra as a potential novel invertebrate model system for meiosis research and particularly for the investigation of SC evolution, function and assembly. Also, available methods for SC research in Hydra are summarized.
- Meiosis /
- Synaptonemal complex /
- Evolution

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[1]	Anokhin, B., Hemmrich-Stanisak, G., Bosch, T.C.G. Comp. Cytogenet., 4 (2010),pp. 97-110
[2]	Baier, A., Alsheimer, M., Benavente, R. Synaptonemal complex protein SYCP3: conserved polymerization properties among vertebrates Biochim. Biophys. Acta, 1774 (2007),pp. 595-602
[3]	Bickel, S.E., Wyman, D.W., Miyazaki, W.Y. et al. EMBO J., 15 (1996),pp. 1451-1459
[4]	Boehm, A.M., Khalturin, K., Anton-Erxleben, F. et al. FoxO is a critical regulator of stem cell maintenance in immortal Hydra Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 19697-19702
[5]	Bogdanov, Y.F., Grishaeva, T.M., Dadashev, S.Y. Similarity of the domain structure of proteins as a basis for the conservation of meiosis Int. Rev. Cytol., 257 (2007),pp. 83-142
[6]	Bolcun-Filas, E., Costa, Y., Speed, R. et al. SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination J. Cell Biol., 176 (2007),pp. 741-747
[7]	Bolcun-Filas, E., Hall, E., Speed, R. et al. PLoS Genet., 5 (2009),p. e1000393
[8]	Bosch, T.C., David, C.N. Proc. Natl. Acad. Sci. USA, 83 (1986),pp. 9478-9482
[9]	Bosch, T.C., Anton-Erxleben, F., Hemmrich, G. et al. Dev. Growth Differ., 52 (2010),pp. 15-25
[10]	Chapman, J.A., Kirkness, E.F., Simakov, O. et al. Nature, 464 (2010),pp. 592-596
[11]	Colaiacovo, M.P., MacQueen, A.J., Martinez-Perez, E. et al. Dev. Cell, 5 (2003),pp. 463-474
[12]	Costa, Y., Speed, R., Ollinger, R. et al. Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis J. Cell Sci., 118 (2005),pp. 2755-2762
[13]	Davies, O.R., Maman, J.D., Pellegrini, L. Structural analysis of the human SYCE2-TEX12 complex provides molecular insights into synaptonemal complex assembly Open Biol., 2 (2012),p. 120099
[14]	de Boer, E., Lhuissier, F.G., Heyting, C. Cytological analysis of interference in mouse meiosis Methods Mol. Biol., 558 (2009),pp. 355-382
[15]	de Vries, F.A., de Boer, E., van den Bosch, M. et al. Genes Dev., 19 (2005),pp. 1376-1389
[16]	Franzenburg, S., Fraune, S., Kunzel, S. et al. Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 19374-19379
[17]	Fraune, J., Alsheimer, M., Volff, J.N. et al. Proc. Natl. Acad. Sci. USA, 109 (2012),pp. 16588-16593
[18]	Fraune, J., Schramm, S., Alsheimer, M. et al. The mammalian synaptonemal complex: protein components, assembly and role in meiotic recombination Exp. Cell Res., 318 (2012),pp. 1340-1346
[19]	Fraune, J., Brochier-Armanent, C., Alsheimer, M. et al. Phylogenies of central element proteins reveal the dynamic evolutionary history of the mammalian synaptonemal complex: ancient and recent components Genetics, 195 (2013),pp. 781-793
[20]	Galliot, B. Int. J. Dev. Biol., 56 (2012),pp. 411-423
[21]	Hamer, G., Gell, K., Kouznetsova, A. et al. Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex J. Cell Sci., 119 (2006),pp. 4025-4032
[22]	Hamer, G., Wang, H., Bolcun-Filas, E. et al. Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex J. Cell Sci., 121 (2008),pp. 2445-2451
[23]	Handel, M.A., Schimenti, J.C. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility Nat. Rev. Genet., 11 (2010),pp. 124-136
[24]	Hassold, T., Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy Nat. Rev. Genet., 2 (2001),pp. 280-291
[25]	Hawley, R.S. Genetics, 189 (2011),pp. 405-409
[26]	Heyting, C. Synaptonemal complexes: structure and function Curr. Opin. Cell Biol., 8 (1996),pp. 389-396
[27]	Holstein, T.W., Hess, M.W., Salvenmoser, W. Methods Cell Biol., 96 (2010),pp. 285-306
[28]	Khalturin, K., Anton-Erxleben, F., Sassmann, S. et al. PLoS Biol., 6 (2008),p. e278
[29]	Kuznetsov, S., Lyanguzowa, M., Bosch, T.C. Zoology, 104 (2001),pp. 25-31
[30]	Lake, C.M., Hawley, R.S. Annu. Rev. Physiol., 74 (2012),pp. 425-451
[31]	Lammers, J.H., Offenberg, H.H., van Aalderen, M. et al. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes Mol. Cell Biol., 14 (1994),pp. 1137-1146
[32]	Lenhoff, H.M., Brown, R.D. Lab. Anim., 4 (1970),pp. 139-154
[33]	Littlefield, C.L. Germ cells in Hydra oligactis males. I. Isolation of a subpopulation of interstitial cells that is developmentally restricted to sperm production Dev. Biol., 112 (1985),pp. 185-193
[34]	Littlefield, C.L., Finkemeier, C., Bode, H.R. Dev. Biol., 146 (1991),pp. 292-300
[35]	MacQueen, A.J., Colaiacovo, M.P., McDonald, K. et al. Genes Dev., 16 (2002),pp. 2428-2442
[36]	Manheim, E.A., McKim, K.S. Curr. Biol., 13 (2003),pp. 276-285
[37]	Meuwissen, R.L., Offenberg, H.H., Dietrich, A.J. et al. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes EMBO J., 11 (1992),pp. 5091-5100
[38]	Miller, M.A., Technau, U., Smith, K.M. et al. Dev. Biol., 224 (2000),pp. 326-338
[39]	Moens, P.B., Kolas, N.K., Tarsounas, M. et al. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA–DNA interactions without reciprocal recombination J. Cell Sci., 115 (2002),pp. 1611-1622
[40]	Moens, P.B., Marcon, E., Shore, J.S. et al. Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes J. Cell Sci., 120 (2007),pp. 1017-1027
[41]	Nishimiya-Fujisawa, C., Sugiyama, T. Dev. Biol., 157 (1993),pp. 1-9
[42]	Offenberg, H.H., Schalk, J.A., Meuwissen, R.L. et al. SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat Nucleic Acids Res., 26 (1998),pp. 2572-2579
[43]	Öllinger, R., Alsheimer, M., Benavente, R. Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes Mol. Biol. Cell, 16 (2005),pp. 212-217
[44]	Padmore, R., Cao, L., Kleckner, N. Cell, 66 (1991),pp. 1239-1256
[45]	Page, S.L., Hawley, R.S. Genes Dev., 15 (2001),pp. 3130-3143
[46]	Page, S.L., Hawley, R.S. The genetics and molecular biology of the synaptonemal complex Annu. Rev. Cell Dev. Biol., 20 (2004),pp. 525-558
[47]	Page, S.L., Khetani, R.S., Lake, C.M. et al. PLoS Genet., 4 (2008),p. e1000194
[48]	Schild-Prüfert, K., Saito, T.T., Smolikov, S. et al. Genetics, 189 (2011),pp. 411-421
[49]	Schmekel, K., Daneholt, B. The central region of the synaptonemal complex revealed in three dimensions Trends Cell Biol., 5 (1995),pp. 239-242
[50]	Schramm, S., Fraune, J., Naumann, R. et al. A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility PLoS Genet., 7 (2011),p. e1002088
[51]	Smolikov, S., Eizinger, A., Schild-Prüfert, K. et al. Genetics, 176 (2007),pp. 2015-2025
[52]	Smolikov, S., Schild-Prüfert, K., Colaiacovo, M.P. PLoS Genet., 5 (2009),p. e1000669
[53]	Steele, R.E. Int. J. Dev. Biol., 56 (2012),pp. 535-542
[54]	Tarsounas, M., Morita, T., Pearlman, R.E. et al. RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes J. Cell Biol., 147 (1999),pp. 207-220
[55]	Webber, H.A., Howard, L., Bickel, S.E. The cohesion protein ORD is required for homologue bias during meiotic recombination J. Cell Biol., 164 (2004),pp. 819-829
[56]	Winkel, K., Alsheimer, M., Öllinger, R. et al. Protein SYCP2 provides a link between transverse filaments and lateral elements of mammalian synaptonemal complexes Chromosoma, 118 (2009),pp. 259-267
[57]	Wittlieb, J., Khalturin, K., Lohmann, J.U. et al. Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 6208-6211
[58]	Yang, F., de La Fuente, R., Leu, N.A. et al. Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis J. Cell Biol., 173 (2006),pp. 497-507
[59]	Yuan, L., Liu, J.G., Zhao, J. et al. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility Mol. Cell, 5 (2000),pp. 73-83
[60]	Yuan, L., Pelttari, J., Brundell, E. et al. J. Cell Biol., 142 (1998),pp. 331-339

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doi: 10.1016/j.jgg.2014.01.009

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The Synaptonemal Complex of Basal Metazoan Hydra: More Similarities to Vertebrate than Invertebrate Meiosis Model Organisms

Corresponding author: E-mail address: johanna.fraune@uni-wuerzburg.de (Johanna Fraune); E-mail address: benavente@biozentrum.uni-wuerzburg.de (Ricardo Benavente)

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doi: 10.1016/j.jgg.2014.01.009

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The Synaptonemal Complex of Basal Metazoan Hydra: More Similarities to Vertebrate than Invertebrate Meiosis Model Organisms

Corresponding author: E-mail address: johanna.fraune@uni-wuerzburg.de (Johanna Fraune); E-mail address: benavente@biozentrum.uni-wuerzburg.de (Ricardo Benavente)

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