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Cyclin Cyc2 is required for elongation of meiotic micronucleus in Tetrahymena thermophila

ABSTRACT: Meiosis occurs in all sexually reproducing unicellular and multicellular eukaryotes. Bouquet formation is indispensible for homologous pairing or recombination during meiotic prophase I, but the regulatory mechanism of this process remain largely unknown. Cyclins regulate the precise meiosis progression by activating cyclin-dependent kinases. We therefore investigated the functional contribution of cyclin Cyc2p during bouquet (named crescent in Tetrahymena) formation in Tetrahymena thermophila. As a conjugation specific gene, CYC2 expression is significantly upregulated at 2-4 h after the initiation of conjugation and Cyc2p mainly localized in cytoplasm as well as weakly in the meiotic micronucleus (Mic). CYC2 knockout mutants failed to form elongated crescent structure and aborted meiotic development. Mic DNA double-strand breakage (DSB) decreased in ΔCYC2 cells as shown by γ-H2A.X staining, consistent with the finding that expression level of SPO11, DMC1, and RAD51 decreased in ΔCYC2 cells. However, ΔCYC2 cells failed to form crescent structure when artificial DSBs were induced, indicating that the inability to enter crescent phase was not completely due to the lack of DSBs. The localization of tubulin showed that impaired structure of nuclei and nuclear membrane may contribute to the blocked Mic elongation. This is further supported by the observation that expression levels of two microtubule associated kinesin genes, KIN11 and KIN141, were significantly downregulated in ΔCYC2 cells. Interestingly, scnRNA accumulation seemed intact in ΔCYC2 cells whereas the intensity of the heterochromatin marker H3K23me3 was abnormally increased. Together, these results showed that cyclin Cyc2p is required for micronuclear meiosis by controlling meiotic prophase chromosome breakage and the microtubule movement of nuclei in Tetrahymena.

ORGANISM(S): Tetrahymena thermophila

PROVIDER: GSE108064 | GEO | 2018/12/14

REPOSITORIES: GEO

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Project description:Dynamic nuclear architecture and chromatin organizations are the key features of the mid- prophase I in mammalian meiosis. Where the chromatin undergoes major changes, including meiosis-specific spatiotemporal arrangements and remodelling, the establishment of chromatin loop–axis structure, pairing, and crossing over between homologous chromosomes, any deficiencies in these events may induce genome instability, subsequently leading to failure to produce gametes and infertility. Despite the significance of chromatin structure, little is known about the location of chromatin marks and the necessity of their balance during meiosis prophase I. Here, we show a thorough cytological study of the surface-spread meiotic chromosomes of mouse spermatocytes for H3K9,14,18,23,27,36, H4K12,16 acetylation, and H3K4,9,27,36 methylation. Active acetylation and methylation marks on H3 and H4, such as H3K9ac, H3K14ac, H3K18ac, H3K36ac, H3K56ac, H4K12ac, H4K16ac, and H3K27me3 and H3K36me3 exhibited pan-nuclear localization away from heterochromatin. In comparison, repressive marks like H3K9me3 are localized to heterochromatin. In addition, we found that the intensities of H3K23ac, H3K27ac, and H3K9me3 enhanced during meiotic prophase I. Further, taking advantage of the delivery of small-molecule chemical inhibitors Methotrexate (MTX; heterochromatin enhancer), HMS-I1 (heterochromatin inhibitor), Anacardic acid (AA; histone acetyltransferase inhibitor), Trichostatin A (TSA; histone deacetylase inhibitor), IOX1 (JmjC demethylases inhibitor), and AZ505 (methyl transferase inhibitor) in seminiferous tubules through the rete testis route, revealed that alteration in histone modifications enhanced the centromere mislocalization, chromosome breakage, altered meiotic recombination and reduced sperm count. Notably, an imbalance in the histone modifications influences the chromosome axis length and chromatin loop size via transcriptional regulation of meiosis- specific genes. Our findings highlight the importance of balanced chromatin modifications in meiotic prophase I chromosome organization and instability.