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Opposing actions of septins and Sticky on Anillin promote the transition from contractile to midbody ring.

El Amine N, Kechad A, Jananji S, Hickson GR - J. Cell Biol. (2013)

Bottom Line: During cytokinesis, closure of the actomyosin contractile ring (CR) is coupled to the formation of a midbody ring (MR), through poorly understood mechanisms.The septin cytoskeleton acts on the C terminus of Anillin to locally trim away excess membrane from the late CR/nascent MR via internalization, extrusion, and shedding, whereas the citron kinase Sticky acts on the N terminus of Anillin to retain it at the mature MR.Simultaneous depletion of septins and Sticky not only disrupted MR formation but also caused earlier CR oscillations, uncovering redundant mechanisms of CR stability that can partly explain the essential role of Anillin in this process.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre de Cancérologie Charles Bruneau, Centre Hospitalier Universitaire Sainte-Justine Centre de Recherche, Montréal, Québec H3T 1C5, Canada.

ABSTRACT
During cytokinesis, closure of the actomyosin contractile ring (CR) is coupled to the formation of a midbody ring (MR), through poorly understood mechanisms. Using time-lapse microscopy of Drosophila melanogaster S2 cells, we show that the transition from the CR to the MR proceeds via a previously uncharacterized maturation process that requires opposing mechanisms of removal and retention of the scaffold protein Anillin. The septin cytoskeleton acts on the C terminus of Anillin to locally trim away excess membrane from the late CR/nascent MR via internalization, extrusion, and shedding, whereas the citron kinase Sticky acts on the N terminus of Anillin to retain it at the mature MR. Simultaneous depletion of septins and Sticky not only disrupted MR formation but also caused earlier CR oscillations, uncovering redundant mechanisms of CR stability that can partly explain the essential role of Anillin in this process. Our findings highlight the relatedness of the CR and MR and suggest that membrane removal is coordinated with CR disassembly.

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Model for the maturation of the CR and MR. (top) At the CR stage, Anillin links the plasma membrane–associated septin cytoskeleton to actomyosin, stabilizing the furrow. Anillin also stabilizes the furrow via a separate Sticky-dependent action of its N terminus. (middle) At the nascent MR, Sticky, myosin, and the Anillin N terminus are retained at the midbody, where they will form a mature MR structure. Septins act on the C terminus of Anillin to remove membrane-associated Anillin molecules, whose N termini are liberated upon disassembly of the F-actin ring. Note that this removal does not only occur at the center of the midbody as depicted. (bottom) Septins and the C termini of Anillin molecules that are retained also act as membrane anchors for the mature MR that persists beyond ∼1 h after furrowing.
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fig9: Model for the maturation of the CR and MR. (top) At the CR stage, Anillin links the plasma membrane–associated septin cytoskeleton to actomyosin, stabilizing the furrow. Anillin also stabilizes the furrow via a separate Sticky-dependent action of its N terminus. (middle) At the nascent MR, Sticky, myosin, and the Anillin N terminus are retained at the midbody, where they will form a mature MR structure. Septins act on the C terminus of Anillin to remove membrane-associated Anillin molecules, whose N termini are liberated upon disassembly of the F-actin ring. Note that this removal does not only occur at the center of the midbody as depicted. (bottom) Septins and the C termini of Anillin molecules that are retained also act as membrane anchors for the mature MR that persists beyond ∼1 h after furrowing.

Mentions: The organization of the cell cortex during closure of the CR and formation of a stable MR remains poorly defined. We show in Drosophila S2 cells that the late CR/nascent MR thins via a maturation process that lasts ∼1 h and that involves a molecular tug of war between stable retention and dynamic removal of the membrane- and cytoskeleton-associated scaffold Anillin. Retention requires a scaffold function of the Cit-K Sticky and the N terminus of Anillin, whereas removal requires septins and the C terminus of Anillin and includes dramatic extrusion and shedding of membranes. Simultaneous perturbation of these antagonistic processes disrupts not only MR maturation but also CR stability, supporting our previous proposal that the CR and MR represent different stages of the same structure (Kechad et al., 2012). The work provides novel insight into the elusive mechanisms of CR closure and its maturation to the MR (Fig. 9).


Opposing actions of septins and Sticky on Anillin promote the transition from contractile to midbody ring.

El Amine N, Kechad A, Jananji S, Hickson GR - J. Cell Biol. (2013)

Model for the maturation of the CR and MR. (top) At the CR stage, Anillin links the plasma membrane–associated septin cytoskeleton to actomyosin, stabilizing the furrow. Anillin also stabilizes the furrow via a separate Sticky-dependent action of its N terminus. (middle) At the nascent MR, Sticky, myosin, and the Anillin N terminus are retained at the midbody, where they will form a mature MR structure. Septins act on the C terminus of Anillin to remove membrane-associated Anillin molecules, whose N termini are liberated upon disassembly of the F-actin ring. Note that this removal does not only occur at the center of the midbody as depicted. (bottom) Septins and the C termini of Anillin molecules that are retained also act as membrane anchors for the mature MR that persists beyond ∼1 h after furrowing.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
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fig9: Model for the maturation of the CR and MR. (top) At the CR stage, Anillin links the plasma membrane–associated septin cytoskeleton to actomyosin, stabilizing the furrow. Anillin also stabilizes the furrow via a separate Sticky-dependent action of its N terminus. (middle) At the nascent MR, Sticky, myosin, and the Anillin N terminus are retained at the midbody, where they will form a mature MR structure. Septins act on the C terminus of Anillin to remove membrane-associated Anillin molecules, whose N termini are liberated upon disassembly of the F-actin ring. Note that this removal does not only occur at the center of the midbody as depicted. (bottom) Septins and the C termini of Anillin molecules that are retained also act as membrane anchors for the mature MR that persists beyond ∼1 h after furrowing.
Mentions: The organization of the cell cortex during closure of the CR and formation of a stable MR remains poorly defined. We show in Drosophila S2 cells that the late CR/nascent MR thins via a maturation process that lasts ∼1 h and that involves a molecular tug of war between stable retention and dynamic removal of the membrane- and cytoskeleton-associated scaffold Anillin. Retention requires a scaffold function of the Cit-K Sticky and the N terminus of Anillin, whereas removal requires septins and the C terminus of Anillin and includes dramatic extrusion and shedding of membranes. Simultaneous perturbation of these antagonistic processes disrupts not only MR maturation but also CR stability, supporting our previous proposal that the CR and MR represent different stages of the same structure (Kechad et al., 2012). The work provides novel insight into the elusive mechanisms of CR closure and its maturation to the MR (Fig. 9).

Bottom Line: During cytokinesis, closure of the actomyosin contractile ring (CR) is coupled to the formation of a midbody ring (MR), through poorly understood mechanisms.The septin cytoskeleton acts on the C terminus of Anillin to locally trim away excess membrane from the late CR/nascent MR via internalization, extrusion, and shedding, whereas the citron kinase Sticky acts on the N terminus of Anillin to retain it at the mature MR.Simultaneous depletion of septins and Sticky not only disrupted MR formation but also caused earlier CR oscillations, uncovering redundant mechanisms of CR stability that can partly explain the essential role of Anillin in this process.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre de Cancérologie Charles Bruneau, Centre Hospitalier Universitaire Sainte-Justine Centre de Recherche, Montréal, Québec H3T 1C5, Canada.

ABSTRACT
During cytokinesis, closure of the actomyosin contractile ring (CR) is coupled to the formation of a midbody ring (MR), through poorly understood mechanisms. Using time-lapse microscopy of Drosophila melanogaster S2 cells, we show that the transition from the CR to the MR proceeds via a previously uncharacterized maturation process that requires opposing mechanisms of removal and retention of the scaffold protein Anillin. The septin cytoskeleton acts on the C terminus of Anillin to locally trim away excess membrane from the late CR/nascent MR via internalization, extrusion, and shedding, whereas the citron kinase Sticky acts on the N terminus of Anillin to retain it at the mature MR. Simultaneous depletion of septins and Sticky not only disrupted MR formation but also caused earlier CR oscillations, uncovering redundant mechanisms of CR stability that can partly explain the essential role of Anillin in this process. Our findings highlight the relatedness of the CR and MR and suggest that membrane removal is coordinated with CR disassembly.

Show MeSH