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NDR Kinase Sid2 Drives Anillin-like Mid1 from the Membrane to Promote Cytokinesis and Medial Division Site Placement
Alaina H Willet1, Ashley K DeWitt2, Janel R Beckley1
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN 37232, USA.
Abstract:
In animals and fungi, cytokinesis is facilitated by the constriction of an actomyosin contractile ring (CR) [1]. In Schizosaccharomyces pombe, the CR forms mid-cell during mitosis from clusters of proteins at the medial cell cortex called nodes [2]. The anillin-like protein Mid1 localizes to nodes and is required for CR assembly at mid-cell [3]. When CR constriction begins, Mid1 leaves the division site. How Mid1 disassociates and whether this step is important for cytokinetic progression has been unknown. The septation initiation network (SIN), analogous to the Hippo pathway of multicellular organisms, is a signaling cascade that triggers node dispersal, CR assembly and constriction, and septum formation [4, 5]. We report that the terminal SIN kinase, Sid2 [6], phosphorylates Mid1 to drive its removal from the cortex at CR constriction onset. A Mid1 mutant that cannot be phosphorylated by Sid2 remains cortical during cytokinesis, over-accumulates in interphase nodes following cell division in a manner dependent on the SAD kinase Cdr2, advances the G2/M transition, precociously recruits other CR components to nodes, pulls Cdr2 aberrantly into the CR, and reduces rates of CR maturation and constriction. When combined with cdr2 mutants that affect node assembly or disassembly, gross defects in division site positioning result. Our findings identify Mid1 as a key Sid2 substrate for SIN-mediated remodeling of the division site for efficient cytokinesis and provide evidence that nodes serve to integrate signals coordinating cell cycle progression and cytokinesis.
Insights
The study reveals that Sid2 kinase phosphorylates Mid1, a key protein, to ensure its timely removal from the cell division site, crucial for efficient cytokinesis and cell cycle coordination.
Area of Science:
- Cell Biology
- Molecular Biology
- Genetics
Background:
- Cytokinesis, the process of cell division, relies on an actomyosin contractile ring (CR) in animals and fungi.
- In Schizosaccharomyces pombe, the CR assembles at the cell's midpoint from protein clusters called nodes.
- The anillin-like protein Mid1 is essential for CR assembly but its dissociation mechanism and importance were unclear.
Purpose of the Study:
- To investigate the mechanism and significance of Mid1 dissociation from the division site during cytokinesis.
- To elucidate the role of the septation initiation network (SIN) in regulating Mid1 dynamics.
- To understand how Mid1 contributes to the coordination of cell cycle progression and cytokinesis.
Main Methods:
- Utilized Schizosaccharomyces pombe as a model organism.
- Investigated protein phosphorylation using kinase assays and mutant analysis.
- Observed protein localization and dynamics using microscopy.
- Analyzed cell cycle progression and cytokinesis defects in wild-type and mutant strains.
Main Results:
- The terminal SIN kinase, Sid2, phosphorylates Mid1, promoting its removal from the cortex at the onset of CR constriction.
- A non-phosphorylatable Mid1 mutant exhibits persistent cortical localization, aberrant accumulation in interphase nodes, and premature G2/M transition.
- This mutant also precociously recruits CR components, mislocalizes Cdr2, and impairs CR maturation and constriction.
- Combined mutations in Mid1 and Cdr2 lead to severe defects in division site positioning.
Conclusions:
- Mid1 is a critical substrate of Sid2, essential for SIN-mediated remodeling of the division site during cytokinesis.
- Nodes integrate signals that coordinate cell cycle progression with cytokinesis.
- Proper Mid1 dissociation is vital for efficient cell division and accurate division site placement.
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