Condensin dysfunction is a reproductive isolating barrier in mice

  • Coyne, J. A. & Orr, H. A. Speciation (Sinauer, 2004).

  • Orr, H. A., Masly, J. P. & Presgraves, D. C. Speciation genes. Curr. Opin. Genet. Dev. 14, 675–679 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Johnson, N. A. Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet. 26, 317–325 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Miyanari, Y., Ziegler-Birling, C. & Torres-Padilla, M.-E. Live visualization of chromatin dynamics with fluorescent TALEs. Nat. Struct. Mol. Biol. 20, 1321–1324 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Narayanswami, S. et al. Cytological and molecular characterization of centromeres in Mus domesticus and Mus spretus. Mamm. Genome 2, 186–194 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wong, A. K. C., Biddle, F. G. & Rattner, J. B. The chromosomal distribution of the major and minor satellite is not conserved in the genus Mus. Chromosoma 99, 190–195 (1990).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hirano, T. Condensin-based chromosome organization from bacteria to vertebrates. Cell 164, 847–857 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hoencamp, C. et al. 3D genomics across the tree of life reveals condensin II as a determinant of architecture type. Science 372, 984–989 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mihola, O., Trachtulec, Z., Vlcek, C., Schimenti, J. C. & Forejt, J. A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323, 373–375 (2009).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Brideau, N. J. et al. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314, 1292–1295 (2006).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Phadnis, N. et al. An essential cell cycle regulation gene causes hybrid inviability in Drosophila. Science 350, 1552–1555 (2015).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Suzuki, T. A. & Nachman, M. W. Speciation and reduced hybrid female fertility in house mice. Evolution 69, 2468–2481 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sturtevant, A. H. Genetic studies on Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5, 488–500 (1920).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chiang, T., Schultz, R. M. & Lampson, M. A. Meiotic origins of maternal age-related aneuploidy. Biol. Reprod. 86, 1–7 (2012).

    Article 
    PubMed 

    Google Scholar
     

  • Kitajima, T. S. Mechanisms of kinetochore-microtubule attachment errors in mammalian oocytes. Dev. Growth Differ. 60, 33–43 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Nagaoka, S. I., Hassold, T. J. & Hunt, P. A. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13, 493–504 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thomas, C., Cavazza, T. & Schuh, M. Aneuploidy in human eggs: contributions of the meiotic spindle. Biochem. Soc. Trans. 49, 107–118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sebestova, J., Danylevska, A., Novakova, L., Kubelka, M. & Anger, M. Lack of response to unaligned chromosomes in mammalian female gametes. Cell Cycle 11, 3011–3018 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Asakawa, T., Ishikawa, M., Shimizu, T. & Dukelow, W. R. The chromosomal normality of in vitro-fertilized rabbit oocytes. Biol. Reprod. 38, 292–295 (1988).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nicodemo, D. et al. Frequency of aneuploidy in in vitro-matured MII oocytes and corresponding first polar bodies in two dairy cattle (Bos taurus) breeds as determined by dual-color fluorescent in situ hybridization. Theriogenology 73, 523–529 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vozdová, M. et al. Frequency of aneuploidy in pig oocytes matured in vitro and of the corresponding first polar bodies detected by fluorescent in situ hybridization. Theriogenology 56, 771–776 (2001).

    Article 
    PubMed 

    Google Scholar
     

  • Koehler, K. E., Schrump, S. E., Cherry, J. P., Hassold, T. J. & Hunt, P. A. Near-human aneuploidy levels in female mice with homeologous chromosomes. Curr. Biol. 16, R579–R580 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Reichmann, J. et al. Dual-spindle formation in zygotes keeps parental genomes apart in early mammalian embryos. Science 361, 189–193 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Hirota, T., Gerlich, D., Koch, B., Ellenberg, J. & Peters, J.-M. Distinct functions of condensin I and II in mitotic chromosome assembly. J. Cell Sci. 117, 6435–6445 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ono, T. et al. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115, 109–121 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ono, T., Fang, Y., Spector, D. L. & Hirano, T. Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell 15, 3296–3308 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ono, T., Yamashita, D. & Hirano, T. Condensin II initiates sister chromatid resolution during S phase. J. Cell Biol. 200, 429–441 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lee, J., Ogushi, S., Saitou, M. & Hirano, T. Condensins I and II are essential for construction of bivalent chromosomes in mouse oocytes. Mol. Biol. Cell 22, 3465–3477 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Houlard, M. et al. Condensin confers the longitudinal rigidity of chromosomes. Nat. Cell Biol. 17, 771–781 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Abe, S. et al. The initial phase of chromosome condensation requires Cdk1-mediated phosphorylation of the CAP-D3 subunit of condensin II. Genes Dev. 25, 863–874 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Choi, T. et al. Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development 113, 789–795 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Davydenko, O., Schultz, R. M. & Lampson, M. A. Increased CDK1 activity determines the timing of kinetochore-microtubule attachments in meiosis I. J. Cell Biol. 202, 221–229 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yoshida, S., Kaido, M. & Kitajima, T. S. Inherent instability of correct kinetochore-microtubule attachments during meiosis I in oocytes. Dev. Cell 33, 589–602 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pommier, Y., Nussenzweig, A., Takeda, S. & Austin, C. Human topoisomerases and their roles in genome stability and organization. Nat. Rev. Mol. Cell Biol. 23, 407–427 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, J. et al. Topoisomerase II dysfunction causes metaphase I arrest by activating Aurora B, SAC and MPF and prevents PB1 abscission in mouse oocytes. Biol. Reprod. 106, 900–909 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Li, X.-M. et al. DNA topoisomerase II is dispensable for oocyte meiotic resumption but is essential for meiotic chromosome condensation and separation in mice. Biol. Reprod. 89, 118 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • Arora, U. P., Charlebois, C., Lawal, R. A. & Dumont, B. L. Population and subspecies diversity at mouse centromere satellites. BMC Genom. 22, 279 (2021).

    Article 
    CAS 

    Google Scholar
     

  • Yamashita, D. et al. MCPH1 regulates chromosome condensation and shaping as a composite modulator of condensin II. J. Cell Biol. 194, 841–854 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Houlard, M. et al. MCPH1 inhibits condensin II during interphase by regulating its SMC2-kleisin interface. eLife 10, e73348 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hale, D. W., Washburn, L. L. & Eicher, E. M. Meiotic abnormalities in hybrid mice of the C57BL/6J x Mus spretus cross suggest a cytogenetic basis for Haldane’s rule of hybrid sterility. Cytogenet. Cell Genet. 63, 221–234 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Davies, B. et al. Altering the binding properties of PRDM9 partially restores fertility across the species boundary. Mol. Biol. Evol. 38, 5555–5562 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dejager, L., Libert, C. & Montagutelli, X. Thirty years of Mus spretus: a promising future. Trends Genet. 25, 234–241 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Probst, A. V. et al. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev. Cell 19, 625–638 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Burton, A. et al. Heterochromatin establishment during early mammalian development is regulated by pericentromeric RNA and characterized by non-repressive H3K9me3. Nat. Cell Biol. 22, 767–778 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Terakawa, T. et al. The condensin complex is a mechanochemical motor that translocates along DNA. Science 358, 672–676 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kong, M. et al. Human condensin I and II drive extensive ATP-dependent compaction of nucleosome-bound DNA. Mol. Cell 79, 99–114 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kinoshita, K., Kobayashi, T. J. & Hirano, T. Balancing acts of two HEAT subunits of condensin I support dynamic assembly of chromosome axes. Dev. Cell 33, 94–106 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hsieh, T. Knotting of the circular duplex DNA by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258, 8413–8420 (1983).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Haase, J., Chen, R., Bonner, M. K., Jenkins, L. M. M. & Kelly, A. E. The TFIIH complex is required to establish and maintain mitotic chromosome structure. eLife https://doi.org/2021.11.06.467569 (2022).

  • Choppakatla, P. et al. Linker histone H1.8 inhibits chromatin binding of condensins and DNA topoisomerase II to tune chromosome length and individualization. eLife 10, e68918 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Akera, T., Trimm, E. & Lampson, M. A. Molecular strategies of meiotic cheating by selfish centromeres. Cell 178, 1132–1144 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Henikoff, S., Ahmad, K. & Malik, H. S. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098–1102 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • King, T. D. et al. Recurrent losses and rapid evolution of the condensin II complex in insects. Mol. Biol. Evol. 36, 2195–2204 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Phadnis, N. & Orr, H. A. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376–379 (2009).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Iwata-Otsubo, A. et al. Expanded satellite repeats amplify a discrete CENP-A nucleosome assembly site on chromosomes that drive in female meiosis. Curr. Biol. 27, 2365–2373 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stein, P. & Schindler, K. Mouse oocyte microinjection, maturation and ploidy assessment. J. Vis. Exp. https://doi.org/10.3791/2851 (2011).

  • Igarashi, H., Knott, J. G., Schultz, R. M. & Williams, C. J. Alterations of PLCβ1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev. Biol. 312, 321–330 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ostromyshenskiĭ, D. I., Kuznetsova, I. S., Golinishchev, F. N., Malikov, V. G. & Podgornaia, O. I. Satellite DNA as a phylogenetic marker: case study of three genera of the Murinae subfamily. Tsitologiia 53, 564–571 (2011).

    PubMed 

    Google Scholar
     

  • Tada, K., Susumu, H., Sakuno, T. & Watanabe, Y. Condensin association with histone H2A shapes mitotic chromosomes. Nature 474, 477–483 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Samoshkin, A. et al. Human condensin function is essential for centromeric chromatin assembly and proper sister kinetochore orientation. PLoS ONE 4, e6831 (2009).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Clift, D. et al. A method for the acute and rapid degradation of endogenous proteins. Cell 171, 1692–1706 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shintomi, K. & Hirano, T. Guiding functions of the C-terminal domain of topoisomerase IIα advance mitotic chromosome assembly. Nat. Commun. 12, 2917 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reference

    Denial of responsibility! Elite News is an automatic aggregator of Global media. In each content, the hyperlink to the primary source is specified. All trademarks belong to their rightful owners, and all materials to their authors. For any complaint, please reach us at – [email protected]. We will take necessary action within 24 hours.
    DMCA compliant image

    Leave a comment