Nuclear and Division-Plane Positioning Revealed by Optical Micromanipulation

Tolić, Iva Marija; Sacconi, Leonardo; Stringari, Chiara; Raabe, Isabel; Pavone, Francesco S.

doi:10.1016/j.cub.2005.05.052

Cited by 85 publications

(66 citation statements)

References 29 publications

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“…It has been shown that the nucleus dynamically influences Mid1 and the cell division site positioning in fission yeast. 35,36 In kin1Δ cells, CAR formation 25 and septum synthesis 22 are only affected in their localization and Mid1 is properly localized around the nucleus (unpublished observations) as in Kin1 OFF cells (Suppl. Fig.…”

Section: Discussionmentioning

confidence: 82%

“…Since position of the CAR and the subsequent septum is specified in late G 2 and early mitosis by the position of the nucleus, [35][36][37] we monitored the position of the nucleus relative to the cell ends in late G 2 cells (≥10 μm) and we observed that a higher proportion of nuclei were misplaced towards the new cell end (according to the birthscar) in the Kin1 OFF (28 ± 1.1% with a short/long ratio <0.85, n = 206) compared to the Kin1 ON condition (16.4 ± 1.8%, n = 186). However, nuclear dynamics of interphase nuclei were not significantly different between Kin1 ON (Suppl.…”

Section: Resultsmentioning

confidence: 99%

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Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Cadou¹,

Carbona²,

Couturier³

et al. 2009

Cell Cycle

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Cytokinesis is the last step of the cell cycle, producing two daughter cells inheriting equal genetic information. This process involves the assembly of an actomyosin ring during mitosis. In the fission yeast Schizosaccharomyces pombe, cytokinesis occurs at the geometric cell centre, a position which is defined by the interphase nucleus and the anilin-related Mid1 protein. The pom1Δ, tea1Δ and tea4Δ mutants are defective in restricting Mid1 as a band around the nucleus and misplace the division site. We previously reported that inhibition of the protein kinase Kin1 promoted failure of cytokinesis in pom1Δ and tea1Δ cells but the mechanism involving Kin1 remained elusive. Here we investigated the contribution of Kin1 in cytokinesis. We show that Kin1-GFP has a dynamic cell cycle regulated distribution. Like pom1Δ and tea1Δ, tea4Δ exhibits a strong genetic interaction with kin1Δ. Using a conditional repressible kin1 allele that only alters interphase nuclear centering, we observed that Kin1 downregulation severely compromised actomyosin ring formation and septum synthesis in tea4Δ cells. In addition, nuclear displacement induced either by overexpression of a putative catalytically inactive Kin1 mutant, by chemically mediated microtubule depolymerization or by mutation in the par1Δ gene impaired cytokinesis in tea4Δ but not tea4 + cells. We propose that nuclear mispositioning exacerbates the tea4Δ, pom1Δ and tea1Δ cell division phenotype. Our work reveal that nuclear centering becomes essential when Pom1/Tea1/Tea4 function is compromised and that Kin1 expression level is a key regulatory element in this situation. Our results suggest the existence of distinct overlapping control mechanisms to ensure efficient cell division.

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Section: Discussionmentioning

confidence: 82%

Section: Resultsmentioning

confidence: 99%

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Cadou¹,

Carbona²,

Couturier³

et al. 2009

Cell Cycle

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“…4,5 In budding yeast, the position of the division plane is defined by the neck between the mother cell and the bud, whereas in fission yeast it is defined by the position of the interphase nucleus. 6,7 Cytoplasmic microtubules play an essential role in yeast nuclear positioning by both providing a link between the nucleus and the cell cortex, and by acting as the necessary purveyors of pushing and pulling forces. 8 Moreover, the regulation of microtubule dynamics, attachment and localization is crucial for the ability to generate asymmetric forces that orient and move the nucleus.…”

Section: Introductionmentioning

confidence: 99%

The Spindle Midzone Microtubule-Associated Proteins Ase1p and Cin8p Affect the Number and Orientation of Astral Microtubules in Saccharomyces cerevisiae

Gramont

Barbour²,

Ross³

et al. 2007

Cell Cycle

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“…In fact, this hypothesis was first formulated from the analysis of microtubule defective mutants displaying delocalized nuclei and septa [Toda et al, 1983;Radcliffe et al, 1998]. More recent studies, in the same spirit as the spindle displacement experiments developed by Ray Rappaport in marine eggs [Rappaport, 1985], have shown that displacing the nucleus from the cell middle by cell centrifugation in the absence of microtubules, or using optical tweezers, indeed results in the delocalization of contractile rings and septa to the new position occupied by the nucleus [Daga and Chang, 2005;Tolic-Norrelykke et al, 2005; see Fig. 2].…”

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confidence: 99%

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

Rincón

Paoletti

2012

Cytoskeleton

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Cell division is a critical and irreversible step in the cell cycle. The strategies that cells follow to regulate the position of the division plane must take into account the global geometry of the cell as well as position of the genetic material to ensure its accurate segregation into daughter cells of a given cell shape and size. Along the years, research on Schizosaccharomyces pombe, a wellrecognized model organism for cell division studies has allowed a detailed molecular understanding of the spatial mechanisms regulating cytokinesis. Division plane position in this unicellular rod-shaped organism, which divides by the assembly and constriction of a medially placed actomyosin ring, largely depends on the anillinlike protein Mid1. Therefore, the major pathways controlling the position of the division plane converge on Mid1. In this review, we make an overview of the studies that have deciphered how Mid1 localization and scaffolding activities are controlled over the cell cycle to ensure the symmetrical division of fission yeast cells. These studies have revealed new mechanisms generating spatial information based on nuclear shuttling of the division plane factor Mid1 and on the establishment of cortical inhibitory gradients of the cell polarity kinase Pom1. V C 2012 Wiley Periodicals, Inc Key Words: cytokinesis, fission yeast, contractile ring, Mid1, cell division Introduction C ytokinesis is the final step of cell division that physically separates the daughter cells at the end of the cell cycle. It is a universal process, essential for cell proliferation, for the survival of unicellular organisms or for the development of multicellular organisms, whose major features have been well conserved along evolution. As an irreversible event, cytokinesis is under tight spatial and temporal regulation. Defective cytokinesis can indeed alter cell geometry or size, perturb cellular organization within tissues or prevent the accurate transmission of the genetic material, producing aneuploid cells, which can affect the survival of unicellular species or favor cancer and tumor progression in animal species.Cytokinesis is first strictly coordinated with mitotic progression in order to successfully fulfill chromosome segregation. Checkpoint mechanisms monitoring the function of the mitotic apparatus can halt cells in metaphase, which prevents cytokinesis until actual chromosome segregation in anaphase.Second, spatial regulatory pathways define the position of the division plane according to the position of the nucleus at mitotic entry, or of the mitotic apparatus, perpendicular to the axis of chromosome segregation. This ensures the efficient segregation of the genetic material and allows to control the geometry of the daughter cells in response to morphogenetic programs. Cell division can indeed be symmetric or asymmetric to allow the generation of daughter cells of different sizes. Orientation of the division plane is also modulated to properly position the daughter cells inside embryos or tissues and to permit the asymm...

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Nuclear and Division-Plane Positioning Revealed by Optical Micromanipulation

Cited by 85 publications

References 29 publications

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

Role of the protein kinase Kin1 and nuclear centering in actomyosin ring formation in fission yeast

The Spindle Midzone Microtubule-Associated Proteins Ase1p and Cin8p Affect the Number and Orientation of Astral Microtubules in Saccharomyces cerevisiae

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

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