Mitotic Spindle Positioning in the EMS Cell of <i>Caenorhabditis elegans</i> Requires LET-99 and LIN-5/NuMA

Liro, Małgorzata J.; Rose, Lesilee S.

doi:10.1534/genetics.116.192831

Cited by 18 publications

(29 citation statements)

References 62 publications

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“…To score furrow ingression, differential interference contrast (DIC) or bright-field images of live embryos were captured using an Olympus BX60 compound microscope using a PlanApo N 60×/1.42 numerical aperture (NA) oil-immersion objective, Hamamatsu Orca 12-bit digital camera, and OpenLab software (Improvision/PerkinElmer, Waltham MA) or Micromanager ( Edelstein et al , 2001 ). Single-plane images were acquired every 10 s. Temperature shifts were performed using a Linkam PE95/T95 System Controller with EP Water Circulation Pump (Linkam Scientific Instruments, Tadworth, United Kingdom), and the actual slide temperature was determined using an Omega HH81 digital thermometer as in Liro and Rose (2016) . For zen-4(ts) , embryos were mounted and incubated at 16°C until NEB, when the embryos were shifted to the nonpermissive temperature (26°C).…”

Section: Methodsmentioning

confidence: 99%

LET-99 functions in the astral furrowing pathway, where it is required for myosin enrichment in the contractile ring

Rose

2017

MBoC

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Section: Methodsmentioning

confidence: 99%

LET-99 functions in the astral furrowing pathway, where it is required for myosin enrichment in the contractile ring

Rose

2017

MBoC

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“…Single-plane images in brightfield optics were acquired every 10 sec using Micromanager 1.4.22. EMS spindle positions were categorized as in Liro and Rose (2016): A/P, spindle initially formed on the A/P axis; late, spindle formed on the L/R or other non-A/P axis and then rotated onto the A/P axis; L/R D/V, the spindle formed on a non-A/P axis and never rotated. Phenotypes were grouped as normal (A/P) or abnormal (late or L/R D/V) and compared using Chi-squared analysis in Excel.…”

Section: Live Imagingmentioning

confidence: 99%

“…A subset of Wnt signaling components, such as the Wnt ligand (MOM-2 in C. elegans), the Frizzled receptor (MOM-5), and the Disheveled adaptor proteins (DSH-2 and MIG-5) are also partially required for timely spindle orientation. Embryos mutant for these components can exhibit a failure of nuclear rotation by NEB, but most embryos eventually orient their spindles onto the A/P axis in anaphase (Bei et al, 2002;Liro and Rose, 2016;Schlesinger et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

“…NMY-2 was shown to be upstream of SRC-1 in intestinal specification, but not spindle positioning (Liu et al, 2010). Recently, LET-99, a protein required for spindle positioning in the one-cell embryo (Krueger et al, 2010;Park and Rose, 2008;Rose and Kemphues, 1998;Tsou et al, 2002;Wu and Rose, 2007), has been shown to play a role in EMS spindle positioning, where it appears to act downstream of the MES-1/SRC-1 signal (Bei et al, 2002;Liro and Rose, 2016). In the one-cell embryo, LET-99 is asymmetrically localized by the PAR proteins at the cortex, where it then acts to localize the force generation complex that aligns the spindle on the PAR polarity axis.…”

Section: Introductionmentioning

confidence: 99%

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The kinases PIG-1 and PAR-1 act in redundant pathways to regulate asymmetric division in the EMS blastomere ofC. elegans

Liro

Morton

Rose

2017

Preprint

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The PAR-1 kinase of C. elegans is localized to the posterior of the one-cell embryo and its mutations affect asymmetric spindle placement and partitioning of cytoplasmic components in the first cell cycle. However, unlike mutations in the posteriorly localized PAR-2 protein, par-1 mutations do not cause failure to restrict the anterior PAR polarity complex. Further, it has been difficult to examine the role of PAR-1 in subsequent divisions due to the early defects in par-1 mutant embryos. Here we show that the PIG-1 kinase acts redundantly with PAR-1 to restrict the anterior PAR-3 protein for polarity maintenance in the one-cell embryo. By using a weak allele of par-1 that exhibits enhanced lethality when combined with a pig-1 mutation we have further explored roles for these genes in subsequent divisions. We find that both PIG-1 and PAR-1 regulate spindle orientation in the EMS blastomere of the four-cell stage embryo to ensure that it undergoes an asymmetric division. In this cell, PIG-1 and PAR-1 act in parallel pathways for spindle positioning, PIG-1 in the MES-1/SRC-1 pathway and PAR-1 in the Wnt pathway.

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“…We next focus our attention on the mechanism by which dividing cells assume their correct position inside the developing embryo. Specific rotations of the spindle (termed spindle skews) are thought to be a key mechanism by which dividing cells reposition themselves in the embryo [33,45,46]. One hypothesis is that spindle skews are driven by spindle elongation [32].…”

Section: Introductionmentioning

confidence: 99%

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early development

Pimpale

Middelkoop

Mietke

et al. 2019

Preprint

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Proper positioning of cells is important for many aspects of embryonic development, tissue homeostasis, and regeneration. A simple mechanism by which cell positions can be specified is via orienting the cell division axis. This axis is specified at the onset of cytokinesis, but can be reoriented as cytokinesis proceeds.Rotatory actomyosin flows have been implied in specifying and reorienting the cell division axis in certain cases, but how general such reorientation events are, and how they are controlled, remains unclear. In this study, we set out to address these questions by investigating early Caenorhabditis elegans development.In particular, we determined which of the early embryonic cell divisions exhibit chiral counter-rotating actomyosin flows, and which do not. We follow the first nine divisions of the early embryo, and discover that chiral counter-rotating flows arise systematically in the early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify specific properties of the actomyosin cortex in the symmetric AB lineage divisions that favor chiral counter-rotating actomyosin flows of the two halves of the dividing cell. Finally, we show that these counter-rotations are the driving force of both the AB lineage spindle skew and cell reorientation events. In conclusion, we here have shed light on the physical basis of lineage-specific actomyosin-based processes that drive chiral morphogenesis during development.Proper positioning of cells is instrumental for many aspects of early embryonic development [1][2][3]. One way to achieve proper cell positioning is via migration [4,5]. Another way by which cell positions can be specified is via the orientation of the cell division axis [6][7][8]. Since the orientation of the mitotic spindle dictates the cell division axis, the orientation of the mitotic spindle at cleavage is instrumental for determining daughter cell positions [9][10][11][12]. This axis can be set at the beginning of cytokinesis, by assembling the mitotic spindle in the correct orientation from the start, or during cytokinesis by reorientation of the mitotic spindle [13][14][15][16][17][18] While several studies highlight the mechanisms that determine the initial orientation of the mitotic spindle at the onset of cytokinesis [15-17, 19, 20] the mechanisms controlling reorientation remain not very well understood. We here set out to investigate cell repositioning during cytokinesis in the early development of the C. elegans nematode. The fully grown hermaphrodite worm consists of exactly 959 somatic cells that are essentially invariant both in terms of position and lineage [21][22][23][24]. Development is deterministic from the start: the one-cell embryo undergoes an asymmetric cell division that gives rise to the AB (somatic) lineage and the P lineage [22,25]. While the anterior daughter cell, AB, undergoes a symmetric cell division into ABa and ABp, the posterior daughter cell, P 1 , divides asymmetrically into...

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Mitotic Spindle Positioning in the EMS Cell of Caenorhabditis elegans Requires LET-99 and LIN-5/NuMA

Cited by 18 publications

References 62 publications

LET-99 functions in the astral furrowing pathway, where it is required for myosin enrichment in the contractile ring

LET-99 functions in the astral furrowing pathway, where it is required for myosin enrichment in the contractile ring

The kinases PIG-1 and PAR-1 act in redundant pathways to regulate asymmetric division in the EMS blastomere ofC. elegans

Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early development

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