Cdk3, a conjugation-specific cyclin-dependent kinase, is essential for the initiation of meiosis in Tetrahymena thermophila

Yan, Guangwu; Zhang, Jing; Shodhan, Anura; Tian, Miao; Miao, Wei

doi:10.1080/15384101.2016.1207838

Cited by 19 publications

(10 citation statements)

References 51 publications

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“…RNA was extracted, sequenced and mapped according to a method described previously (Yan et al, 2016a). Briefly, total RNA was extracted from WT cells at the starvation, co-stimulation and conjugation stages, and from ΔCDK19 and ΔCYC9 cells at the starvation (KO cells) and costimulation stages (KO cells and WT cells mixed in a ratio of 9:1 for 1 h) using the RNeasy Protect Cell Mini Kit (Qiagen), as previously described (TetraFGD: http://tfgd.ihb.ac.cn/) (Wuitschick et al, 2002).…”

Section: Transcriptome Analysismentioning

confidence: 99%

“…showed that T. thermophila has a total of 34 cyclins (Yan et al, 2016b), and only four standard CDKs with exact PSTAIRE-like cyclin-binding motifs (Yan et al, 2016a). Because of the divergence between the number of annotated cyclin and CDK genes in this organism, we searched for additional CDK family members and identified a total of 20 CDKs or CDK-like genes in the T. thermophila macronuclear genome (Table S1).…”

Section: Introductionmentioning

confidence: 99%

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Sexual cell cycle initiation is regulated by CDK19 and CYC9 in Tetrahymena thermophila

Yan

Han

et al. 2020

Journal of Cell Science

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To investigate the mechanisms underlying initiation of the sexual cell cycle in eukaryotes, we have focused on cyclins and cyclindependent kinases (CDKs) in the well-studied model ciliate, Tetrahymena thermophila. We identified two genes, CDK19 and CYC9, which are highly co-expressed with the mating-associated factors MTA, MTB and HAP2. Both CDK19 and CYC9 were found to be essential for mating in T. thermophila. Subcellular localization experiments suggested that these proteins are located at the oral area, including the conjugation junction area, and that CDK19 or CYC9 knockout prevents mating. We found that CDK19 and CYC9 form a complex, and also identified several additional subunits, which may have regulatory or constitutive functions. RNA sequencing analyses and cytological experiments showed that mating is abnormal in both ΔCDK19 and ΔCYC9, mainly at the entry to the co-stimulation stage. These results indicate that the CDK19-CYC9 complex initiates the sexual cell cycle in T. thermophila.

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Section: Transcriptome Analysismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Sexual cell cycle initiation is regulated by CDK19 and CYC9 in Tetrahymena thermophila

Yan

Han

et al. 2020

Journal of Cell Science

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“…In Tetrahymena , previous examples of genes required for meiotic initiation and DSBs included meiosis-specific cell cycle regulators such as cyclins and CDKs, which act upstream of the process (43,44), but co-factors that support DSB formation by Spo11 have not yet been found. Here, we report that Pars11 has functions in DSB initiation and restriction and in DNA damage sensing.…”

Section: Discussionmentioning

confidence: 99%

A chromatin-associated protein required for inducing and limiting meiotic DNA double-strand break formation

Tian

Loidl

2018

Nucleic Acids Research

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Programmed DNA double-strand breaks (DSBs) are required for meiotic recombination, but the number is strictly controlled because they are potentially harmful. Here we report a novel protein, Pars11, which is required for Spo11-dependent DSB formation in the protist Tetrahymena. Pars11 localizes to chromatin early in meiotic prophase in a Spo11-independent manner and is removed before the end of prophase. Pars11 removal depends on DSB formation and ATR-dependent phosphorylation. In the absence of the DNA damage sensor kinase ATR, Pars11 is retained on chromatin and excess DSBs are generated. Similar levels of Pars11 persistence and DSB overproduction occur in a non-phosphorylatable pars11 mutant. We conclude that Pars11 supports DSB formation by Spo11 until enough DSBs are formed; thereafter, DSB production stops in response to ATR-dependent degradation of Pars11 or its removal from chromatin. A similar DSB control mechanism involving a Rec114-Tel1/ATM-dependent negative feedback loop regulates DSB formation in budding yeast. However, there is no detectable sequence homology between Pars11 and Rec114, and DSB numbers are more tightly controlled by Pars11 than by Rec114. The discovery of this mechanism for DSB regulation in the evolutionarily distant protist and fungal lineages suggests that it is conserved across eukaryotes.

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“…We previously identified other important meiotic regulators in T. thermophila, including the Cyc2 and Cyc17 cyclin and the Tcdk3 cyclin-dependent kinase [27,28]. To investigate the function of E2fl1/Dpl2 complex during meiosis regulation, we tracked the expression of meiotic genes in dpl2D and e2fl1D cells (Figure 3(A)) and used these data to construct a meiotic regulatory network (Figure 3(B)).…”

Section: T Thermophila Dpl2 and E2fl1 Form A Transcription Factor Comentioning

confidence: 99%

“…Cyc2 and Tcdk3 may act together to initiate meiosis. They regulated the expression of genes important for early prophase that functioned in DSBs formation and repair [28]. Cyc17 was essential for initiating meiotic anaphase and mainly regulated the genes involved in meiotic anaphase, including those that functioned in chromosome condensation and segregation [27].…”

Section: T Thermophila Dpl2 and E2fl1 Form A Transcription Factor Comentioning

confidence: 99%

A DP-like transcription factor protein interacts with E2fl1 to regulate meiosis inTetrahymena thermophila

et al. 2018

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Evolutionarily conserved E2F family transcription factors regulate the cell cycle via controlling gene expression in a wide range of eukaryotes. We previously demonstrated that the meiosis-specific transcription factor E2fl1 had an important role in meiosis in the model ciliate Tetrahymena thermophila. Here, we report that expression of another E2F family transcription factor gene DPL2 correlates highly with that of E2FL1. Similar to e2fl1Δ cells, dpl2Δ cells undergo meiotic arrest prior to anaphase I, with the five chromosomes adopting an abnormal tandem arrangement. Immunofluorescence staining and immunoprecipitation experiments demonstrate that Dpl2 and E2fl1 form a complex during meiosis. We previously identified several meiotic regulatory proteins in T. thermophila. Cyc2 and Tcdk3 may cooperate to initiate meiosis and Cyc17 is essential for initiating meiotic anaphase. We investigate the relationship of these regulators with Dpl2 and E2fl1, and then construct a meiotic regulatory network by measuring changes in meiotic genes expression in knockout cells. We conclude that the E2fl1/Dpl2 complex plays a central role in meiosis in T. thermophila.

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Cdk3, a conjugation-specific cyclin-dependent kinase, is essential for the initiation of meiosis in Tetrahymena thermophila

Cited by 19 publications

References 51 publications

Sexual cell cycle initiation is regulated by CDK19 and CYC9 in Tetrahymena thermophila

Sexual cell cycle initiation is regulated by CDK19 and CYC9 in Tetrahymena thermophila

A chromatin-associated protein required for inducing and limiting meiotic DNA double-strand break formation

A DP-like transcription factor protein interacts with E2fl1 to regulate meiosis inTetrahymena thermophila

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