Microdomains bounded by endoplasmic reticulum segregate cell cycle calcium transients in syncytial Drosophila embryos

Abstract

Cell cycle calcium signals are generated by the inositol trisphosphate (InsP3)–mediated release of calcium from internal stores (Ciapa, B., D. Pesando, M. Wilding, and M. Whitaker. 1994. Nature. 368:875–878; Groigno, L., and M. Whitaker. 1998. Cell. 92:193–204). The major internal calcium store is the endoplasmic reticulum (ER); thus, the spatial organization of the ER during mitosis may be important in shaping and defining calcium signals. In early Drosophila melanogaster embryos, ER surrounds the nucleus and mitotic spindle during mitosis, offering an opportunity to determine whether perinuclear localization of ER conditions calcium signaling during mitosis. We establish that the nuclear divisions in syncytial Drosophila embryos are accompanied by both cortical and nuclear localized calcium transients. Constructs that chelate InsP3 also prevent nuclear division. An analysis of nuclear calcium concentrations demonstrates that they are differentially regulated. These observations demonstrate that mitotic calcium signals in Drosophila embryos are confined to mitotic microdomains and offer an explanation for the apparent absence of detectable global calcium signals during mitosis in some cell types.

Nucleoplasmic Calcium Is Required for Cell Proliferation

“…The significance of this machinery within the nucleus has long been a question. Both growth factors (12) and integrins (36) InsP3 (16,37), plus temporally related increases in Ca 2ϩ in the perinuclear region (26,38,39), have been associated with breakdown of the nuclear envelope and entry into mitosis. In addition, nuclear Ca 2ϩ activates transcription factors such as CREB (9,11), Elk-1 (10), and DREAM (40), but cytosolic Ca 2ϩ activates other transcription factors such as SRE (9), plus phosphatases such as calcineurin that are important for transcription (41).…”

Breaking up is hard to do – membrane traffic in cytokinesis

“…So why should this reorganisation take place? One possibility, supported by evidence from cellularisation in Drosophila, is that the ER acts as a Ca signals are confined to so-called mitotic microdomains, which are, in turn, enclosed by the ER (Parry et al, 2005). The ER tubules that are arranged around the spindle might therefore contribute a signalling capacity to the cytokinesis machinery.…”

The Cytoskeleton and Its Regulation by Calcium and Protons

“…It is additionally pertinent that, even though the nuclear envelope has broken down, the mitotic/meiotic apparatus in different plant and animal cells remains surrounded by the ER ( Fig. 2A; Hepler, 1980;Hepler and Wolniak, 1984;Bobinnec et al, 2003;Parry et al, 2005;Whitaker, 2006Whitaker, , 2008, with some elements interpenetrating the mitotic apparatus specifically along the kinetochore MTs (Fig. 2, B and C ;Hepler, 1980).…”

“…For example, in Drosophila embryos, convincing images show prominent elements of ER surrounding the spindle apparatus (Bobinnec et al, 2003;Parry et al, 2005Parry et al, , 2006; it seems plausible that these membranes locally control the uptake and release of calcium. While some imaging studies show changes in calcium, particularly associated with nuclear envelope breakdown (Parry et al, 2005) and again at the onset of anaphase (Groigno and Whitaker, 1998), overall there are relatively few data, and moreover, the calcium changes observed are small and spatially localized (Parry et al, 2005). This is particularly true in plants, where robust images of calcium transients associated with the stages of cell division are rare, even though these same methods reveal striking ion gradients when applied to pollen tubes.…”