Mid1p-dependent regulation of the M–G1 transcription wave in fission yeast

Agarwal, Monica; Papadopoulou, Kyriaki; Mayeux, Adeline; Vajrala, Vasanthi; Quintana, Daniela M.; Paoletti, Anne; McInerny, Christopher

doi:10.1242/jcs.073049

Cited by 7 publications

(8 citation statements)

References 25 publications

(62 reference statements)

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“…The coupling between the mitotic and transcription control machineries may in fact be mediated by physical interactions. In support of this idea, the anillin-like protein Mid1, which is involved in division plane positioning (3), has recently been shown to control the transcription of mitotic genes (1) and to interact in vivo with both Fkh2 and Wee1 (1,37). In future studies, we plan to investigate whether Mid1 is part of a machinery that connects the transcription and mitotic control networks.…”

Section: Discussionmentioning

confidence: 89%

Cyclin-Dependent Kinase 8 Regulates Mitotic Commitment in Fission Yeast

Szilágyi

Bányai

López

et al. 2012

Molecular and Cellular Biology

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Temporal changes in transcription programs are coupled to control of cell growth and division. We here report that Mediator, a conserved coregulator of eukaryotic transcription, is part of a regulatory pathway that controls mitotic entry in fission yeast. The Mediator subunit cyclin-dependent kinase 8 (Cdk8) phosphorylates the forkhead 2 (Fkh2) protein in a periodic manner that coincides with gene activation during mitosis. Phosphorylation prevents degradation of the Fkh2 transcription factor by the proteasome, thus ensuring cell cycle-dependent variations in Fkh2 levels. Interestingly, Cdk8-dependent phosphorylation of Fkh2 controls mitotic entry, and mitotic entry is delayed by inactivation of the Cdk8 kinase activity or mutations replacing the phosphorylated serine residues of Fkh2. In addition, mutations in Fkh2, which mimic protein phosphorylation, lead to premature mitotic entry. Therefore, Fkh2 regulates not only the onset of mitotic transcription but also the correct timing of mitotic entry via effects on the Wee1 kinase. Our findings thus establish a new pathway linking the Mediator complex to control of mitotic transcription and regulation of mitotic entry in fission yeast. Signaling pathways can control the activation of gene expression programs and thereby regulate cell fate determination. In embryonic stem cells, certain gene expression programs allow the cells to self-renew whereas other programs trigger differentiation into specific cell types as a response to developmental signaling (58). Elucidation of how temporal changes in transcription programs are coupled to control of cell growth and division is therefore of fundamental importance for our understanding of developmental processes.Global gene transcription analysis in yeasts and higher eukaryotes has revealed that a significant proportion of the genome is transcribed in a periodic manner during cell cycle progression (5,15,34,49,55). Correct periodic regulation is believed to play a critical role in normal cell proliferation, and the genes are often deregulated in different forms of cancer (6). Depending on the organism, the number of periodically expressed genes ranges from ϳ400 to more than 1,000 (5, 6, 56). These include genes with well-established roles in cell cycle progression, such as those encoding cyclins, transcription factors and protein kinases.A cluster named CLB2 in budding yeast (35 genes) or cluster 1 in fission yeast (87 genes) is periodically expressed and activated at mitosis and repressed in G 1 of the next cell cycle (4,5,34,56). In budding yeast, transcription of the CLB2 cluster is controlled by the forkhead proteins Fkh1 and Fkh2, which cooperate with Mcm1 (a MADS box protein) and the Ndd1 coactivator (27, 28). In fission yeast, forkhead proteins Sep1 and Fkh2 and the MADS box protein Mbx1 regulate mitotic transcription (12,13,49,53). Deletion of the sep1 gene results in reduced transcription, whereas overexpression of sep1 induces expression of the same genes. In contrast, deletion of fkh2 causes elevated levels of g...

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Section: Discussionmentioning

confidence: 89%

Cyclin-Dependent Kinase 8 Regulates Mitotic Commitment in Fission Yeast

Szilágyi

Bányai

López

et al. 2012

Molecular and Cellular Biology

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“…An interesting possibility is that precocious Mid1-dependent ring assembly may have arisen in S. pombe lineage to compensate for deregulation of the conventional, late mitotic pathway. An unrelated nuclear function in regulation of gene expression [ 41 ] could have promoted evolutionary co-option of Mid1 in instructive division site positioning in addition to its structural role in scaffolding cell division machinery.…”

Section: Resultsmentioning

confidence: 99%

Rewiring of Cellular Division Site Selection in Evolution of Fission Yeasts

Yam

Oliferenko

2015

Current Biology

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SummaryStrategies to position the division apparatus exhibit a bewildering diversity [1], but how these mechanisms evolve remains virtually unknown. Here, we explore the plasticity of division site positioning in fission yeasts Schizosaccharomyces pombe and Schizosaccharomyces japonicus. We demonstrate that, whereas both species divide in the middle, only S. pombe uses the anillin Mid1 as a primary nucleus-derived cue to assemble the actomyosin ring at the equatorial cortex. We trace this variance to the divergence in subcellular targeting of Mid1 and show that duplication of an ancestral anillin early in the Schizosaccharomyces lineage may have led to subfunctionalization of the Mid1 orthologs. In contrast to S. pombe, medial assembly of the actomyosin ring in mitotic S. japonicus relies on the cortical anchor protein Cdc15 regulated by the tip-localized kinase Pom1. Our data suggest that division site placement is determined by cortical positioning of the actomyosin-plasma membrane linkers and that both identity of the linker and control of its subcellular targeting are highly modular.

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“…The second paper explores the role of Mid1p (Dmf1p), an anillin-like protein with known function in controlling the deposition of actin ring that predicts the site of cleavage of the daughter two cells. 10 Here it is shown 4 that Mid1p binds to Fkh2p and possibly to Sep1p, and to gene promoters, to control cell cycle gene expression ( Fig. 1).…”

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confidence: 81%

“…Two recently published papers address this issue. 3,4 Both analyze gene expression in fission yeast that occurs at the end the cell cycle, the M-G 1 interval, with the encoded proteins having important roles in cytokinesis and cell separation, which occur at this cell cycle time. Such gene expression is controlled by the PBF (PCB binding factor) transcription factor complex that contains at least three components: two forkhead transcription factors Fkh2p and Sep1p, and a MADS box protein Mbx1p.…”

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confidence: 99%