Abstract
SummaryAlthough nuclei are the defining features of eukaryotes, we still do not fully understand how the nuclear compartment is duplicated and partitioned during division. This is especially the case for organisms that do not completely disassemble their nuclear envelope upon entry into mitosis. In studying this process in Drosophila neural stem cells, which undergo asymmetric divisions, we find that the nuclear compartment boundary persists during mitosis thanks to the maintenance of a supporting nuclear lamina. This mitotic nuclear envelope is then asymmetrically remodeled and partitioned to give rise to two daughter nuclei that differ in envelope composition and exhibit a >30-fold difference in volume. The striking difference in nuclear size was found to depend on two consecutive processes: asymmetric nuclear envelope resealing at mitotic exit at sites defined by the central spindle, and differential nuclear growth that appears to depend on the available local reservoir of ER/nuclear membranes, which is asymmetrically partitioned between the two daughter cells. Importantly, these asymmetries in size and composition of the daughter nuclei, and the associated asymmetries in chromatin organization, all become apparent long before the cortical release and the nuclear import of cell fates determinants. Thus, asymmetric nuclear remodeling during stem cell divisions may contribute to the generation of cellular diversity by initiating distinct transcriptional programs in sibling nuclei that contribute to later changes in daughter cell identity and fate.
Highlights
Nuclei are the defining feature of the eukaryotic cell
In this paper we show that the nuclear envelope of neuroblasts undergoes an asymmetric remodeling during mitosis, so that the genome is partitioned into daughter nuclei that differ by more than 30-fold in volume and in envelope composition
The nuclear envelope of fly neuroblasts is maintained during mitosis and remodeled to generate two sibling nuclei that differ in size and envelope composition To characterize nuclear division in Drosophila neuroblasts, we used markers to label plasma and nuclear membranes (CD8),[20] the INM (Klaroid), ONM (Klarsicht) and the ER (BipSfGFP::HDEL)
Summary
Nuclei are the defining feature of the eukaryotic cell. nuclear division—the process by which a nucleus divides into two—was one of the first subjects studied by Walther Flemming and other pioneers of cell biology, it remains one of the most poorly understood aspects of the division process. The nuclear envelope is disassembled during mitosis in Drosophila cells in culture,[12] but is maintained in the syncytial fly embryo.[9,13,14] To further investigate the mechanism of nuclear division in an intermediate ‘‘semi-closed mitosis,’’ we sought to study the process in Drosophila neural stem cells (neuroblasts), which divide asymmetrically to generate a large self-renewing neuroblast containing a large nucleus and a smaller differentiating ganglion mother cell (GMC) with a small nucleus.[15,16,17] it is not known how the nuclear compartment is partitioned during these stem cell divisions, nor how nuclear division might contribute to the formation of sibling nuclei with different transcriptional profiles/identities.[18,19] In this paper we show that the nuclear envelope of neuroblasts undergoes an asymmetric remodeling during mitosis, so that the genome is partitioned into daughter nuclei that differ by more than 30-fold in volume and in envelope composition This analysis reveals the emergence of differences in chromatin organization between the two daughter nuclei that precede the cortical release and nuclear
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