Histone H3 phosphorylation and elimination of paternal X chromosomes at early cleavages in sciarid flies

Abstract

SummaryIn sciarid flies (Diptera, Sciaridae), one or two paternally derived X chromosomes are discarded from the soma at early cleavages to determine the sex of the embryo (XX, females; X0, males). X chromosome(s) elimination is achieved by an abnormal anaphase segregation so that X sister chromatids do not reach the poles and are not included in the daughter nuclei. A cis-acting locus (CE) within the heterochromatin proximal to the centromere is known to regulate X chromosome elimination. By immunofluorescence analysis in early embryos from Sciara ocellaris and Sciara coprophila, we investigated histone H3 phosphorylation at Ser10, Ser28 and Thr3 prior to, and during, the X elimination process. We found that the regular syncytial nuclear divisions are characterized by a gradual loss of H3S10 phosphorylation along the chromosome arms at anaphase. Importantly, the eliminating X chromosomes show a retardation in anaphase chromatid segregation and high levels of H3S10 phosphorylation in the chromosome arms. In the present study, we provide the first evidence linking the hyper-phosphorylated H3 status of the X chromosome with a delay in sister chromatid separation at anaphase. Our findings support the idea that the CE induces a deficiency in H3 dephosphorylation in the paternal X chromosomes to be eliminated.

Histone H3 Threonine Phosphorylation Regulates Asymmetric Histone Inheritance in the Drosophila Male Germline

“…Furthermore, the signal from H3T3P immunostaining (Figure S1E) was enriched but not restricted to the centromeric region labelled with an antibody against a centromere-specific H3 variant Cid (Centromere identifier, Figure S1E). In summary, the temporal and spatial distributions of H3T3P in Drosophila male germ cells are comparable to what has been reported in other cell types from other systems (Caperta et al, 2008; Dai et al, 2005; Escriba and Goday, 2013; Markaki et al, 2009; Wang et al, 2010). …”

A Peak of H3T3 Phosphorylation Occurs in Synchrony with Mitosis in Sea Urchin Early Embryos

“…Later on, we observe a bright T3H3ph signal distributed along the chromosome arms, both during the prometaphase and metaphase (Figure 2 and Figure S3). Sea urchins thus differ significantly from other invertebrates, such as dipterans and tunicates, in which T3H3ph occupies the pericentromeric region during the metaphase [20,45]. In fact, our results reveal that the subcellular distribution of T3H3ph during the sea urchin first cell division is similar to that observed in mammalian somatic cells [18,19].…”

“…The presence of high levels of phosphorylated histone H3 is one of the unequivocal signatures of cell division, and it is well established that the H3 Ser10 and Ser28 residues are phosphorylated during chromosome condensation in multiple species [15][16][17]. However, the H3 also becomes phosphorylated at Thr3 during mitosis in many different taxa, including mammals [18,19], insects [20], plants [21] and fungi [22]. In mammalian cells, the levels of the T3H3 phosphorylated form (T3H3ph) oscillate following a strict temporal and spatial pattern.…”

Programmed DNA elimination in multicellular organisms

“…Loss or alterations in centromeres, kinetochore assembly, microtubule attachment, or chromosome segregation could lead to DNA elimination. Studies on chromosome elimination in insects suggest that chromosome loss is most likely a function of a segregation defect in the metaphase/anaphase transition [48,51]. In sciarid flies, reduction in the dephosphorylation of H3S10P is associated with a failure or retardation in sister chromatid separation [48].…”

“…Studies on chromosome elimination in insects suggest that chromosome loss is most likely a function of a segregation defect in the metaphase/anaphase transition [48,51]. In sciarid flies, reduction in the dephosphorylation of H3S10P is associated with a failure or retardation in sister chromatid separation [48]. In contrast, chromosome elimination in finches may be associated with a defect in kinetochore–microtubule interactions [47].…”