A Phosphorylation Cycle Shapes Gradients of the DYRK Family Kinase Pom1 at the Plasma Membrane

Hachet, Olivier; Berthelot-Grosjean, Martine; Kokkoris, Kyriakos; Vincenzetti, Vincent; Moosbrugger, Josselin

doi:10.1016/j.cell.2011.05.014

Cited by 112 publications

(210 citation statements)

References 39 publications

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“…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.…”

Section: Cell Tips Inhibit Mid1 Cortical Localizationmentioning

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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Section: Cell Tips Inhibit Mid1 Cortical Localizationmentioning

confidence: 99%

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

Rincón

Paoletti

2012

Cytoskeleton

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“…Pom1 autophosphorylates and phosphorylated Pom1 is unable to bind to the membrane. The landmark protein Tea4, which localizes to the tips [39], recruits Pom1 and the protein phosphatase Dis2 [40], which locally dephosphorylates Pom1 [41]. This allows binding of Pom1 to membranes at the cell tips.…”

Section: Reviewmentioning

confidence: 99%

“…This allows binding of Pom1 to membranes at the cell tips. Lateral diffusion of Pom1 away from the Tea4 domain results in autophosphorylation and membrane detachment [41]. Intracellular gradients such as this are crucial for the regulation of mitotic events in many cells [42].…”

Section: Reviewmentioning

confidence: 99%

Coordinating cell polarity with cell division in space and time

Panbianco

Gotta

2011

Trends in Cell Biology

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Decisions of when and where to divide are crucial for cell survival and fate, and for tissue organization and homeostasis. The temporal coordination of mitotic events during cell division is essential to ensure that each daughter cell receives one copy of the genome. The spatial coordination of these events is also crucial because the cytokinetic furrow must be aligned with the axis of chromosome segregation and, in asymmetrically dividing cells, the polarity axis. Several recent papers describe how cell shape and polarity are coordinated with cell division in single cells and tissues and begin to unravel the underlying molecular mechanisms, revealing common principles and molecular players. Here, we discuss how cells regulate the spatial and temporal coordination of cell polarity with cell division

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“…For the ability to associate with the membrane, we chose the membrane binding fragment of Pom1, Pom1-305-510, which cannot be phosphorylated and does not polarize significantly on its own, even in the presence of full-length Pom1 (14). To assess the distribution of this membrane-binding fragment in the absence of any Mal3-mediated interaction with microtubules, we analyzed the cortical distribution of the GFP-tagged Pom1-305-510 fragment in otherwise WT cells.…”

Section: A Chimera Protein That Combines Membrane Binding With Microtmentioning

confidence: 99%

“…1, Left): the DYRK-family member kinase Pom1, which links cell length to mitotic commitment, displays a polar cortical gradient (12,13). Local long-lived Tea1-Tea4 complexes trigger the association of Pom1 with the plasma membrane by recruiting the protein phosphatase 1 (PP1) Dis2, which dephosphorylates Pom1, thereby locally increasing Pom1 affinity for the membrane (14). Diffusion on the membrane of dephosphorylated Pom1, followed by autophosphorylation and detachment from the membrane, then establishes a cortical gradient (14).…”

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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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A Phosphorylation Cycle Shapes Gradients of the DYRK Family Kinase Pom1 at the Plasma Membrane

Cited by 112 publications

References 39 publications

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

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

Coordinating cell polarity with cell division in space and time

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

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