Wsh3/Tea4 Is a Novel Cell-End Factor Essential for Bipolar Distribution of Tea1 and Protects Cell Polarity under Environmental Stress in S. pombe

Tatebe, Hisashi; Shimada, Koji; Uzawa, Satoru; Morigasaki, Susumu; Shiozaki, Kazuhiro

doi:10.1016/j.cub.2005.04.061

Cited by 108 publications

(169 citation statements)

References 51 publications

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“…As shown on Figure 1B, Kin1-GFP was present predominantly at one cell end throughout interphase, this may correspond to the actively growing cell end, since tea4Δ cells show a monopolar growth pattern in interphase. 29,30 During mitosis, the tip signal was detected on the most distant cell end relative to the asymmetric ring (arrow, Fig. 1B).…”

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: Resultsmentioning

confidence: 99%

“…[22][23][24] Tea4 binds to Tea1 and regulates NETO and symmetry of cell division. 29,30 Kin1Δ tea4Δ cells showed a severe cytokinetic phenotype ( Fig. 2A), with aberrant septal material randomly deposited in a majority of cells (Fig.…”

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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“…Along the years, Pom1 has emerged as a critical factor regulating key processes such as polarized cell growth and cell division [Bahler and Nurse, 2001;Niccoli et al, 2003;Celton-Morizur et al, 2006;Padte et al, 2006;Tatebe et al, 2008;Martin and Berthelot-Grosjean, 2009;Moseley et al, 2009]. Pom1 localizes to the cell tip cortex where it forms a gradient which integrates spatial information on cell size and geometry, in a manner that depends indirectly on microtubules Tatebe et al, 2005].In fact, Hachet et al [2011] have proposed an elegant mechanism which explains the localization of Pom1 to the cell tips and the establishment of a gradient of the protein with decreasing concentrations from the cell tips to the cell middle. Pom1 binds directly to negatively charged phospholipids of the plasma membrane through a positively charged motif.…”

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confidence: 99%

“…Autophosphorylation of Pom1 in this region inhibits its membrane targeting. However, the PP1 phosphatase Dis2 [Ohkura et al, 1989], which is targeted to the cell tips through an interaction with Tea4 [Alvarez-Tabares et al, 2007], itself delivered to the cell tips together with Tea1 by microtubule plus ends [Martin et al, 2005;Tatebe et al, 2005], dephosphorylates Pom1 at the cell tips, favoring its association with the plasma membrane. When Pom1 diffuses laterally away from the cell tips, Dis2 can no longer dephosphorylate Pom1, which results in its gradual dissociation from the cortex.…”

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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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“…In these cells, microtubules are organized into three to four antiparallel bundles that are mechanically aligned along the long axis of the cells, thereby targeting growing microtubule tips to the cell poles (7). Microtubule plus-end-tracking proteins (+TIPs), such as the endbinding (EB) protein Mal3, mediate the active transport of polarity factors toward cell ends: the polarity factors Tea1 and Tea4, which control cell growth (6,8,9), interact with Mal3, the microtubule regulator Tip1 (homolog of CLIP-170), and the kinesin-7 Tea2 (10) at microtubule tips and are thus targeted to the cell poles. At the cell poles, Tea1 and Tea4 interact with the membrane-bound anchoring protein Mod5 (11), whose localization at cell poles is itself Tea1 dependent.…”

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confidence: 99%

Chimera proteins with affinity for membranes and microtubule tips polarize in the membrane of fission yeast cells

Recouvreux

Sokolowski

Γραμμουστιάνου

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Cell polarity refers to a functional spatial organization of proteins that is crucial for the control of essential cellular processes such as growth and division. To establish polarity, cells rely on elaborate regulation networks that control the distribution of proteins at the cell membrane. In fission yeast cells, a microtubule-dependent network has been identified that polarizes the distribution of signaling proteins that restricts growth to cell ends and targets the cytokinetic machinery to the middle of the cell. Although many molecular components have been shown to play a role in this network, it remains unknown which molecular functionalities are minimally required to establish a polarized protein distribution in this system. Here we show that a membrane-binding protein fragment, which distributes homogeneously in wild-type fission yeast cells, can be made to concentrate at cell ends by attaching it to a cytoplasmic microtubule end-binding protein. This concentration results in a polarized pattern of chimera proteins with a spatial extension that is very reminiscent of natural polarity patterns in fission yeast. However, chimera levels fluctuate in response to microtubule dynamics, and disruption of microtubules leads to disappearance of the pattern. Numerical simulations confirm that the combined functionality of membrane anchoring and microtubule tip affinity is in principle sufficient to create polarized patterns. Our chimera protein may thus represent a simple molecular functionality that is able to polarize the membrane, onto which additional layers of molecular complexity may be built to provide the temporal robustness that is typical of natural polarity patterns.

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Wsh3/Tea4 Is a Novel Cell-End Factor Essential for Bipolar Distribution of Tea1 and Protects Cell Polarity under Environmental Stress in S. pombe

Abstract: Wsh3/Tea4 is an essential component of the Tea1 cell-end complex. In addition to its role in bipolar growth during the normal cell cycle, the Wsh3-Tea1 complex, together with the stress-signaling MAPK cascade, contributes to cell-polarity maintenance under stress conditions.

Cited by 108 publications

References 51 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

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

Chimera proteins with affinity for membranes and microtubule tips polarize in the membrane of fission yeast cells

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