Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation in<i>Tetrahymena thermophila</i>

Yan, Guangwu; Dang, Huai; Tian, Miao; Zhang, Jing; Shodhan, Anura; Ning, Yingzhi; Xiong, Jie; Miao, Wei

doi:10.1080/15384101.2016.1188238

Cited by 19 publications

(22 citation statements)

References 55 publications

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“…Tetrahymena thermophila cells lacking Cyc2 and Cyc17 are arrested at early crescent (∼2–3.5 h postmixing) and diakinesis-like metaphase I (∼5 h postmeiotic induction) stages of meiosis, respectively (Xu et al. 2016; Yan et al. 2016).…”

Section: Discussionmentioning

confidence: 99%

Proteomic Analysis of Histones H2A/H2B and Variant Hv1 in Tetrahymena thermophila Reveals an Ancient Network of Chaperones

Ashraf

Nabeel‐Shah

Garg

et al. 2019

Molecular Biology and Evolution

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Epigenetic information, which can be passed on independently of the DNA sequence, is stored in part in the form of histone posttranslational modifications and specific histone variants. Although complexes necessary for deposition have been identified for canonical and variant histones, information regarding the chromatin assembly pathways outside of the Opisthokonts remains limited. Tetrahymena thermophila , a ciliated protozoan, is particularly suitable to study and unravel the chromatin regulatory layers due to its unique physical separation of chromatin states in the form of two distinct nuclei present within the same cell. Using a functional proteomics pipeline, we carried out affinity purification followed by mass spectrometry of endogenously tagged T. thermophila histones H2A, H2B and variant Hv1.We identified a set of interacting proteins shared among the three analyzed histones that includes the FACT-complex, as well as H2A- or Hv1-specific chaperones. We find that putative subunits of T. thermophila versions of SWR- and INO80-complexes, as well as transcription-related histone chaperone Spt6 Tt specifically copurify with Hv1. We also identified importin β6 and the T. thermophila ortholog of nucleoplasmin 1 (cNpl1 Tt ) as H2A–H2B interacting partners. Our results further implicate Poly [ADP-ribose] polymerases in histone metabolism. Molecular evolutionary analysis, reciprocal affinity purification coupled to mass spectrometry experiments, and indirect immunofluorescence studies using endogenously tagged Spt16 Tt (FACT-complex subunit), cNpl1 Tt , and PARP6 Tt underscore the validity of our approach and offer mechanistic insights. Our results reveal a highly conserved regulatory network for H2A (Hv1)–H2B concerning their nuclear import and assembly into chromatin.

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Section: Discussionmentioning

confidence: 99%

Proteomic Analysis of Histones H2A/H2B and Variant Hv1 in Tetrahymena thermophila Reveals an Ancient Network of Chaperones

Ashraf

Nabeel‐Shah

Garg

et al. 2019

Molecular Biology and Evolution

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“…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%

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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“…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%

“…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]. Figure 3(A) showed a heatmap representation of the fold change in expression for these genes.…”

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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Cyc17, a meiosis-specific cyclin, is essential for anaphase initiation and chromosome segregation inTetrahymena thermophila

Cited by 19 publications

References 55 publications

Proteomic Analysis of Histones H2A/H2B and Variant Hv1 in Tetrahymena thermophila Reveals an Ancient Network of Chaperones

Proteomic Analysis of Histones H2A/H2B and Variant Hv1 in Tetrahymena thermophila Reveals an Ancient Network of Chaperones

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

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

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