Ciliary control of meiotic chromosomal pairing mechanics and germ cell morphogenesis
Posted on: 15 February 2021
Preprint posted on 9 February 2021
Categories: cell biology, developmental biology, genetics, physiology
Cell division is driven by mechano-chemical macromolecular assemblies that create physical force to position the genome. During meiosis – the formation of haploid gametes – chromosomes undergo elaborate movements during prophase 1. Telomeres cluster at the nuclear envelope, forming a structure termed the chromosomal bouquet (Figure 1). The chromosomal bouquet promotes meiotic pairing of chromosome homologs and errors in its formation can result in infertility (Ding et al., 2007; Elkouby et al., 2016; Horn et al., 2013; Sato et al., 2009; Shibuya et al., 2014).
Cilia are hair-like organelles that in some cell types are considered incompatible with cell division. Mutations in ciliary genes often result in ciliopathies, disorders with a wide variety of symptoms, one of which is infertility.
In a recent preprint, Mytils, Kumar et al. report the zytgotene cilium – a cilium present during meiosis. They suggest that the zytgotene cilium is important for fertility through aiding mechanical positioning of the chromosome bouquet during gametogenesis.
Figure. 1: The chromosomal bouquet in prophase 1 of meiosis.
Key findings
Mytils, Kumar et al., used live imaging in zebrafish ovaries to record zygotene oocytes, observing that chromosomes rotate rapidly, in contrast to a positionally stable centrosome. Interestingly, the centrosome formed the base of a previously unrecognised cilium, marked by Arl13b, acetylated tubulin and glutamylated tubulin (Figure 2a). The presence of the zygotene cilia was confirmed by transmission electron microscopy and was stage specific, fully elaborated at zygotene but absent at pachytene.
Oocyte precursors develop in germline cysts – groups of developing cells that form close contacts with each other. Serial block face scanning electron microscopy showed that zygotene cilia extend throughout germline cysts and tangle in between cells (Figure 2b).
Figure. 2 Selected panels from Figure 1 of Mytilis, Kumar et al., 2021, reproduced with permission from the authors.
To understand whether zygotene cilia are important for meiosis, Mytils, Kumar et al. investigated the effects of loss of function of four different ciliary genes. cep290-/- , cep290-/-;kif7-/-, and cc2d2a-/- ciliary mutant fish were not embryonic lethal but no longer had zygotene cilia. This correlated with dysfunctional germ cell morphogenesis, ovarian development, infertility and abnormal chromosomal bouquet formation. Interestingly, cep290-/- mutants maintained a centrosome able to nucleate microtubules. Therefore, specifically the zygotene cilium may be required for bouquet function, in addition to cytoskeletal fibres from centrosomes. Finally, the authors show that the zygotene cilium is conserved not only in male meiosis in zebrafish, but also in mouse oogenesis. It is therefore not specific to one sex or one species.
Significance
Some ciliopathies are associated with infertility. This work predicts that these fertility issues could relate to dysfunction of the zygotene cilium, in addition to other known cilium-related issues such as sperm motility.
This preprint shows that cilia are not strictly incompatible with cell division, and moreover that they may play important roles during it, in agreement with other work in different systems (Riparbelli et al., 2012).
The centrosome is inherently mechanochemical, and yet the forces acting upon it are unclear. This preprint suggests that centrosome anchoring to a cilium is a method of force resistance required for chromosome movements, an exciting new theory.
References
Ding, X., Xu, R., Yu, J., Xu, T., Zhuang, Y., and Han, M. (2007). SUN1 Is Required for Telomere Attachment to Nuclear Envelope and Gametogenesis in Mice. Dev. Cell 12, 863–872.
Elkouby, Y.M., Jamieson-Lucy, A., and Mullins, M.C. (2016). Oocyte Polarization Is Coupled to the Chromosomal Bouquet, a Conserved Polarized Nuclear Configuration in Meiosis. PLOS Biol. 14, e1002335.
Horn, H.F., Kim, D.I., Wright, G.D., Wong, E.S.M., Stewart, C.L., Burke, B., and Roux, K.J. (2013). A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J. Cell Biol. 202, 1023–1039.
Riparbelli, M.G., Callaini, G., and Megraw, T.L. (2012). Assembly and Persistence of Primary Cilia in Dividing Drosophila Spermatocytes. Dev. Cell 23, 425–432.
Sato, A., Isaac, B., Phillips, C.M., Rillo, R., Carlton, P.M., Wynne, D.J., Kasad, R.A., and Dernburg, A.F. (2009). Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis. Cell 139, 907–919.
Shibuya, H., Ishiguro, K., and Watanabe, Y. (2014). The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat. Cell Biol. 16, 145–156.
doi: https://doi.org/10.1242/prelights.27402
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