Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes

Alsop, G. Bradley; Zhang, Dahong

doi:10.1242/jcs.01007

Cited by 30 publications

(26 citation statements)

References 100 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Furthermore, this localization is distinct from the ER, Golgi and lysosomes (Figure 3). Consistent with this, mitochondrial localization to the cleavage furrow has been noted at least twice previously in other somatic mammalian cells [27], [35], as well as in the first division of porcine oocytes [36] and in grasshopper spermatocytes [37]. In addition, we observed mitochondrial recruitment to the cleavage furrow in multiple mammalian cell lines (Figure 2) and in aberrant monopolar and multipolar divisions (Figure 4), suggesting that the mechanism of recruitment to the furrow is robust and conserved in mammals.…”

Section: Discussionsupporting

confidence: 85%

Mitochondria Localize to the Cleavage Furrow in Mammalian Cytokinesis

Lawrence

Mandato

2013

PLoS ONE

View full text Add to dashboard Cite

Mitochondria are dynamic organelles with multiple cellular functions, including ATP production, calcium buffering, and lipid biosynthesis. Several studies have shown that mitochondrial positioning is regulated by the cytoskeleton during cell division in several eukaryotic systems. However, the distribution of mitochondria during mammalian cytokinesis and whether the distribution is regulated by the cytoskeleton has not been examined. Using live spinning disk confocal microscopy and quantitative analysis of mitochondrial fluorescence intensity, we demonstrate that mitochondria are recruited to the cleavage furrow during cytokinesis in HeLa cells. After anaphase onset, the mitochondria are recruited towards the site of cleavage furrow formation, where they remain enriched as the furrow ingresses and until cytokinesis completion. Furthermore, we show that recruitment of mitochondria to the furrow occurs in multiple mammalian cells lines as well as in monopolar, bipolar, and multipolar divisions, suggesting that the mechanism of recruitment is conserved and robust. Using inhibitors of cytoskeleton dynamics, we show that the microtubule cytoskeleton, but not actin, is required to transport mitochondria to the cleavage furrow. Thus, mitochondria are specifically recruited to the cleavage furrow in a microtubule-dependent manner during mammalian cytokinesis. Two possible reasons for this could be to localize mitochondrial function to the furrow to facilitate cytokinesis and / or ensure accurate mitochondrial inheritance.

show abstract

Section: Discussionsupporting

confidence: 85%

Mitochondria Localize to the Cleavage Furrow in Mammalian Cytokinesis

Lawrence

Mandato

2013

PLoS ONE

View full text Add to dashboard Cite

show abstract

“…While mitotic chromosomes are thought to generate gradients of Ran GTP that selforganize the prometaphase spindle 3 , this cannot be the only self-organizing signal in anaphase because cytokinesis can occur in the absence of chromatin 4,5 . Instead, the location of the cleavage furrow is coupled to the position of the spindle midzone where the Chromosome *Correspondence to: PTS (e-mail pts7h@virginia.edu) or MAL (e-mail lampson@sas.upenn.edu).…”

Section: Introductionmentioning

confidence: 99%

Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient

Fuller

Lampson

Foley

et al. 2008

Nature

339

380

View full text Add to dashboard Cite

Proper partitioning of the contents of a cell between two daughters requires integration of spatial and temporal cues. The anaphase array of microtubules that self-organize at the spindle midzone contributes to positioning the cell division plane midway between the segregating chromosomes 1 . How this signaling occurs over micron length-scales, from the midzone to the cell cortex, is not known. Here we examine the anaphase dynamics of protein phosphorylation by Aurora B kinase, a key mitotic regulator, using FRET-based sensors in living cells and immunofluorescence of native Aurora B substrates. Quantitative analysis of phosphorylation dynamics, using chromosome and centromere targeted sensors, reveals that changes are due primarily to position along the division axis rather than time. These dynamics result in the formation of a spatial phosphorylation gradient early in anaphase that is centered at the spindle midzone. This gradient depends on Aurora B targeting to a subpopulation of microtubules that activate it. Aurora kinase activity organizes the targeted microtubules to generate a structure based feedback loop. We propose that feedback between Aurora B kinase activation and midzone microtubules generates a gradient of posttranslational marks that provides spatial information for events in anaphase and cytokinesis. Keywordsanaphase; gradient; FRET; Aurora B; INCENP; histone H3; serine 10; mitotic spindle; Hesperadin; monopolar It is believed that self-organizing systems position the cleavage furrow, since experimental displacement of the anaphase spindle results in repositioning of the cleavage furrow within minutes 2 . While mitotic chromosomes are thought to generate gradients of Ran GTP that selforganize the prometaphase spindle 3 , this cannot be the only self-organizing signal in anaphase because cytokinesis can occur in the absence of chromatin 4,5 . Instead, the location of the cleavage furrow is coupled to the position of the spindle midzone where the Chromosome *Correspondence to: PTS (e-mail pts7h@virginia.edu) or MAL (e-mail lampson@sas.upenn.edu). $ Both authors contributed equally to this work Author Information: Development of the Aurora B and Plk phosphorylation sensors and FRET imaging and analysis were done in the Kapoor lab by MA Lampson, together with EA Foley. BG Fuller performed immunofluorescence experiments. SR Nitcher and P Tobelman performed the kinase assays and P-Lisa experiments, respectively. KV Le performed live imaging of Aurora B-GFP. BG Fuller and MA Lampson wrote the paper. To examine spatial patterns of Aurora B signaling during anaphase, we developed a strategy using FRET-based sensors that report quantitative changes in substrate phosphorylation in living cells. We adapted a sensor design 6 in which changes in intramolecular CFP-YFP FRET depend on changes in phosphorylation of an Aurora B substrate peptide, which is conserved among members of the kinesin-13 family 7 (Fig. 1a). To mimic localizations of endogenous Aurora B substrates 8 , sensors were targeted to ce...

show abstract

“…[4–6]); however, the molecular bases of these signaling cascades are not well defined. The central spindle signals are mediated partly by kinesin-6-family motors complexed with two general sets of proteins, including MgcRacGap (in metazoans – the centralspindlin complex) or the chromosomal passenger proteins INCENP and Aurora kinase (in Dictyostelium protozoans and higher metazoans) [7–10].…”

Section: Introductionmentioning

confidence: 99%

14-3-3 Coordinates Microtubules, Rac, and Myosin II to Control Cell Mechanics and Cytokinesis

et al. 2010

View full text Add to dashboard Cite

Summary Background During cytokinesis, regulatory signals are presumed to emanate from the mitotic spindle. However, what these signals are and how they lead to the spatiotemporal changes in the cortex structure, mechanics, and regional contractility are not well understood in any system. Results To investigate pathways that link the microtubule network to the cortical changes that promote cytokinesis, we used chemical genetics in Dictyostelium to identify genetic suppressors of nocodazole, a microtubule depolymerizer. We identified 14-3-3 and found that it is enriched in the cortex, helps maintain steady state microtubule length, contributes to normal cortical tension, modulates actin wave formation, and controls the symmetry and kinetics of cleavage furrow contractility during cytokinesis. Furthermore, 14-3-3 acts downstream of a Rac small GTPase (RacE), associates with myosin II heavy chain and is needed to promote myosin II bipolar thick filament remodeling. Conclusion 14-3-3 connects microtubules, Rac and myosin II to control several aspects of cortical dynamics, mechanics, and cytokinesis cell shape change. Further, 14-3-3 interacts directly with myosin II heavy chain to promote bipolar thick filament remodeling and distribution. Overall, 14-3-3 appears to integrate several critical cytoskeletal elements that drive two important processes cytokinesis shape change and cell mechanics.

show abstract

Microtubules continuously dictate distribution of actin filaments and positioning of cell cleavage in grasshopper spermatocytes

Cited by 30 publications

References 100 publications

Mitochondria Localize to the Cleavage Furrow in Mammalian Cytokinesis

Mitochondria Localize to the Cleavage Furrow in Mammalian Cytokinesis

Midzone activation of aurora B in anaphase produces an intracellular phosphorylation gradient

14-3-3 Coordinates Microtubules, Rac, and Myosin II to Control Cell Mechanics and Cytokinesis

Contact Info

Product

Resources

About