Meiosis I Is Established through Division-Specific Translational Control of a Cyclin

Carlile, Thomas M.; Amon, Angelika

doi:10.1016/j.cell.2008.02.032

Cited by 207 publications

(373 citation statements)

References 38 publications

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“…To test this we reversibly arrested cells at the end of prophase I, by placing NDT80, the gene encoding a transcription factor required for entry into the meiotic divisions, under the control of the GAL1-10 promoter. Upon addition of β-estradiol to the medium, cells also containing a GAL4-estrogen receptor (GAL4-ER) fusion exit the prophase I block and progress through the meiotic divisions (15). Cells overexpressing CDC5 from the CUP1 promoter underwent a single meiotic division.…”

Section: Resultsmentioning

confidence: 99%

Polo kinase Cdc5 is a central regulator of meiosis I

Attner

Miller

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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During meiosis, two consecutive rounds of chromosome segregation yield four haploid gametes from one diploid cell. The Polo kinase Cdc5 is required for meiotic progression, but how Cdc5 coordinates multiple cell-cycle events during meiosis I is not understood. Here we show that CDC5-dependent phosphorylation of Rec8, a subunit of the cohesin complex that links sister chromatids, is required for efficient cohesin removal from chromosome arms, which is a prerequisite for meiosis I chromosome segregation. CDC5 also establishes conditions for centromeric cohesin removal during meiosis II by promoting the degradation of Spo13, a protein that protects centromeric cohesin during meiosis I. Despite CDC5's central role in meiosis I, the protein kinase is dispensable during meiosis II and does not even phosphorylate its meiosis I targets during the second meiotic division. We conclude that Cdc5 has evolved into a master regulator of the unique meiosis I chromosome segregation pattern.P olo kinases are central regulators of chromosome segregation and control multiple mitotic events (1). Budding yeast contains a single Polo kinase, CDC5. Unlike in higher eukaryotes, budding yeast CDC5 primarily regulates postmetaphase events, its essential function being to trigger exit from mitosis (2). CDC5 also contributes to the efficient inactivation of cohesins, the protein complexes that hold sister chromatids together until the onset of chromosome segregation. Cdc5 phosphorylates the cohesin subunit Mcd1/Scc1 to facilitate its cleavage by the protease separase (3).CDC5 also regulates the specialized cell division that gives rise to gametes, known as meiosis (4). During meiosis, two consecutive rounds of chromosome segregation follow one round of DNA replication. During meiosis I, homologous chromosomes segregate; during meiosis II, sister chromatids separate (5). The chromosome segregation machinery is modified in three ways to facilitate the unusual meiosis I division. First, the combination of homologous recombination and cohesin complexes distal to the resulting cross-overs mediate the physical linkage of homologous chromosomes, which is essential for their accurate segregation during meiosis I. Second, sister chromatids of each homolog must be segregated to the same pole rather than to opposite poles, as they are during mitosis. The fusion of sister kinetochores by co-orientation factors (the monopolin complex in yeast) facilitates the attachment of microtubules emanating from one spindle pole. Third, cohesin complexes must be lost in a stepwise manner from chromosomes. During meiosis I cohesin complexes are lost from chromosome arms to bring about the segregation of homologous chromosomes (6). The residual cohesins at centromeres facilitate the accurate segregation of sister chromatids during meiosis II. Cdc5 has been implicated in the execution of all three meiosis I-specific events. CDC5 is required for the resolution of double Holliday junctions during homologous recombination (7,8). Cdc5 also controls the co-orientation of ...

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Section: Resultsmentioning

confidence: 99%

Polo kinase Cdc5 is a central regulator of meiosis I

Attner

Miller

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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“…ED addition induces NDT80 expression, and cells synchronously exit from pachytene and undergo meiotic nuclear divisions ( Fig. 1; Carlile and Amon 2008).…”

Section: Cdk Activity Is Not Required For Ndt80-dependent Jm Resolutimentioning

confidence: 99%

“…We combined cdc28-as1 with an estrogen-inducible NDT80 allele (NDT80-IN) (see Supplemental Material) that confers reversible pachytene arrest Carlile and Amon 2008). In the absence of inducer (␤-estradiol, ED), NDT80 is not expressed, and cells accumulate in pachytene with persistent JMs and full-length SC.…”

Section: Cdk Activity Is Not Required For Ndt80-dependent Jm Resolutimentioning

confidence: 99%

“…All but Clb2 are produced during meiosis (Chu and Herskowitz 1998). Clb5 (Sphase cyclin) is required for premeiotic DNA replication and meiotic DSB formation (Murakami and Keeney 2008), while Clb1, Clb3, Clb4, and Clb6 (M-phase cyclins), whose expression is Ndt80-dependent, promote meiotic divisions Marston and Amon 2004;Carlile and Amon 2008). Conditional cdc28-ts mutants arrest in meiosis I prophase with unseparated SPBs (Shuster and Byers 1989;Xu et al 1997), and meiosis I prophase arrest in response to defects in synapsis and/or recombination requires inhibition of CDK by the Swe1 protein (Leu and Roeder 1999).…”

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Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis

Sourirajan¹,

Lichten²

2008

Genes Dev.

178

299

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In budding yeast, exit from the pachytene stage of meiosis requires the mid-meiosis transcription factor Ndt80, which promotes expression of ∼200 genes. Ndt80 is required for meiotic function of polo-like kinase (PLK, Cdc5) and cyclin-dependent kinase (CDK), two cell cycle kinases previously implicated in pachytene exit. We show that ongoing CDK activity is dispensable for two events that accompany exit from pachytene: crossover formation and synaptonemal complex breakdown. In contrast, CDC5 expression in ndt80⌬ mutants efficiently promotes both events. Thus, Cdc5 is the only member of the Ndt80 transcriptome required for this critical step in meiotic progression. During meiosis, a single round of DNA replication is followed by two successive divisions (meiosis I and meiosis II), producing four haploid gametes. This is achieved by segregation of homologs, homologous chromosomes of different parental origin, during meiosis I, followed by segregation of sister chromatids in meiosis II. During the prophase of meiosis I, progressive chromosome condensation is accompanied by homolog pairing and recombination, which culminate at the pachytene stage, where homologs are paired along their entire lengths and connected by the synaptonemal complex (SC). Upon exit from pachytene, the SC disappears and chromosomes become diffuse, only to recondense at diplotene/diakinesis as visible homologs connected by crossovers.Meiotic recombination initiates in early meiosis I prophase by the formation of DNA double-strand breaks (DSBs), catalyzed by the Spo11 endonuclease (Keeney and Neale 2006). As cells progress toward pachytene, DSBs are repaired to form either noncrossover (NCO) recombinants or joint molecule (JM) intermediates, many of which contain parental homologs connected by double Holliday junctions (Bishop and Zickler 2004). JMs are resolved, primarily as crossover recombinants (COs), at the end of pachytene. Crossovers provide the interhomolog connections that later ensure proper homolog alignment on the metaphase I spindle and thus their accurate segregation at anaphase I.The exit from pachytene is a crucial transition, since it is associated with the resolution of JMs as COs, SC disassembly, and kinetochore modification so that sister kinetochores orient toward the same spindle pole (monoorientation), and the separation of duplicated spindle pole bodies (SPBs), the fungal centrosome equivalents (Shuster and Byers 1989;Xu et al. 1995Xu et al. , 1997Clyne et al. 2003;Lee and Amon 2003b). Failure in any of these processes can result in chromosome nondisjunction and the production of aneuploid progeny. Consequently, checkpoint systems monitor synapsis and recombination and prevent exit from pachytene unless these processes are complete (Roeder and Bailis 2000).Ndt80, a transcription factor first expressed in late pachytene, is a central target of these checkpoint systems (Xu et al. 1995;Tung et al. 2000). Ndt80 activates expression of more than 200 genes at mid-meiosis, including those required for meiotic divisions and spor...

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“…In S. cerevisiae, translation of one of four mitotic Cyclins, Clb3, needs to be repressed until meiosis II, otherwise its premature translation causes defective meiosis I chromosome segregation [40].…”

Section: Developmental Control Of the Cell Cycle Via Translational Rementioning

confidence: 99%

Translational regulation of the cell cycle: when, where, how and why?

Kronja

Orr‐Weaver

2011

Phil. Trans. R. Soc. B

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Translational regulation contributes to the control of archetypal and specialized cell cycles, such as the meiotic and early embryonic cycles. Late meiosis and early embryogenesis unfold in the absence of transcription, so they particularly rely on translational repression and activation of stored maternal mRNAs. Here, we present examples of cell cycle regulators that are translationally controlled during different cell cycle and developmental transitions in model organisms ranging from yeast to mouse. Our focus also is on the RNA-binding proteins that affect cell cycle progression by recognizing special features in untranslated regions of mRNAs. Recent research highlights the significance of the cytoplasmic polyadenylation element-binding protein (CPEB). CPEB determines polyadenylation status, and consequently translational efficiency, of its target mRNAs in both transcriptionally active somatic cells as well as in transcriptionally silent mature Xenopus oocytes and early embryos. We discuss the role of CPEB in mediating the translational timing and in some cases spindle-localized translation of critical regulators of Xenopus oogenesis and early embryogenesis. We conclude by outlining potential directions and approaches that may provide further insights into the translational control of the cell cycle.

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Meiosis I Is Established through Division-Specific Translational Control of a Cyclin

Cited by 207 publications

References 38 publications

Polo kinase Cdc5 is a central regulator of meiosis I

Polo kinase Cdc5 is a central regulator of meiosis I

Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis

Translational regulation of the cell cycle: when, where, how and why?

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