The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis inCaenorhabditis elegans

Chase, Dan; Serafinas, Christina; Ashcroft, Neville; Kosinski, Mary; Longo, Dan L.; Ferris, Douglas K.; Golden, Andy

doi:10.1002/(sici)1526-968x(200001)26:1<26::aid-gene6>3.0.co;2-o

Cited by 128 publications

(145 citation statements)

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“…Recent studies suggest that MEX-5 affects PIE-1 localization in part by binding the polo kinases PLK-1 and PLK-2 (Nishi et al, 2008). PLK-1 is localized to the anterior of the one-cell embryo in a pattern that is similar to, and dependent on, MEX-5 (Chase et al, 2000;Nishi et al, 2008;Rivers et al, 2008). Both PLK-1 and PLK-2 bind a putative polo-docking site around residue Thr186 in MEX-5; an alanine substitution at Thr186 impairs, although it does not eliminate, MEX-5 function (Nishi et al, 2008).…”

Section: Introductionsupporting

confidence: 82%

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

et al. 2008

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Anteroposterior polarity in early C. elegans embryos is required for the specification of somatic and germline lineages, and is initiated by a sperm-induced reorganization of the cortical cytoskeleton and PAR polarity proteins. Through mechanisms that are not understood, the kinases PAR-1 and PAR-4, and other PAR proteins cause the cytoplasmic zinc finger protein MEX-5 to accumulate asymmetrically in the anterior half of the one-cell embryo. We show that MEX-5 asymmetry requires neither vectorial transport to the anterior, nor protein degradation in the posterior. MEX-5 has a restricted mobility before fertilization and in the anterior of one-cell embryos. However, MEX-5 mobility in the posterior increases as asymmetry develops, presumably allowing accumulation in the anterior. The MEX-5 zinc fingers and a small, C-terminal domain are essential for asymmetry; the zinc fingers restrict MEX-5 mobility, and the C-terminal domain is required for the increase in posterior mobility. We show that a crucial residue in the C-terminus, Ser 458, is phosphorylated in vivo. PAR-1 and PAR-4 kinase activities are required for the phosphorylation of S458, providing a link between PAR polarity proteins and the cytoplasmic asymmetry of MEX-5.

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Section: Introductionsupporting

confidence: 82%

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

et al. 2008

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“…Depletion or inhibition of Plk1 causes a severe delay in the G2/M transition in different systems (15,16). In C. elegans, Plk1 was also proposed as a regulator for NEBD during meiosis (10). Our data are unique in providing direct evidence that Plk1 positively regulates NEBD through phosphorylation of p150 Glued during prophase.…”

Section: Discussionmentioning

confidence: 99%

Polo-like kinase 1 phosphorylation of p150 ^Glued facilitates nuclear envelope breakdown during prophase

Liu

Yang

et al. 2010

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

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Nuclear envelope breakdown (NEBD) is an essential step during the G2/M transition in higher eukaryotic cells. Increasing evidence supports the notion that both microtubules and microtubuleassociated motor proteins are critical regulators of NEBD. Although it has been described that p150 Glued , the major component of the dynein/dynactin complex, localizes in the nuclear envelope during prophase, the exact role of p150 Glued and its regulation during NEBD are largely elusive. Polo-like kinase 1 (Plk1), the best characterized Ser/Thr kinase, is involved in mitotic entry in several systems; however, the targets of Plk1 during NEBD are unknown. Herein, we show that in mammalian cells both Plk1 and p150 Glued regulate NEBD and that Plk1 interacts with and phosphoryates p150 Glued during NEBD at prophase. Using various approaches, we showed that Plk1 phosphorylates p150 Glued at Ser-179 and that the pS179 epitope is generated at the nuclear envelope of prophase cells. Significantly, Plk1-mediated phosphorylation of p150 Glued at Ser-179 positively regulates its accumulation at the nuclear envelope during prophase. Finally, we found that cells expressing the Plk1-unphosphorylatable mutant (p150 Glued -S179A) arrest at G2, as indicated by reduced NEBD, increased levels of cyclin B and phospho-H3, but a decreased level of Cdc2 kinase activity. Taking these data together, we conclude that Plk1 phosphorylation of p150 Glued might be one major pathway of NEBD regulation. mitosis | microtubule dynamics | dynactin

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“…In C. elegans, there are three genes that encode polo-like kinases, plk-1, plk-2 and plk-3, with PLK-3 protein being significantly more diverged (Chase et al, 2000a;Chase et al, 2000b;Ouyang et al, 1999). Depletion of plk-1 by RNAi results in defects in nuclear envelope breakdown, meiotic chromosome segregation and cytokinesis, producing embryos arrested at the one-cell stage without cleavage, consistent with a role in cell division (Chase et al, 2000b).…”

Section: Introductionmentioning

confidence: 99%

Polo kinases regulateC. elegansembryonic polarity via binding to DYRK2-primed MEX-5 and MEX-6

Nishi

Rogers

Robertson³

et al. 2008

Development

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During Caenorhabditis elegans embryogenesis, anteroposterior (AP) polarity is established by a hierarchy of PAR proteins (for a review, see Kemphues, 2000). Many of these PAR proteins are asymmetrically localized at the cortex along the AP axis. The asymmetric distribution of PAR proteins determines the position of the first mitotic spindle and the asymmetric localization of key cytoplasmic determinants (for reviews, see Cowan and Hyman, 2004;Lyczak et al., 2002). This results in two daughters that are different in both size and developmental fate: the larger anterior somatic cell, AB, and the smaller posterior germline blastomere, P1. P1 then undergoes a series of three more asymmetric divisions, each giving rise to a germline blastomere (sequentially P2 to P4, termed the P lineage) and a corresponding somatic cell (Fig. 1).PAR proteins regulate spindle position via a G-protein signaling pathway (Colombo et al., 2003;Hess et al., 2004), and cytoplasmic polarity via two maternally supplied proteins, MEX-5 and MEX-6 (Schubert et al., 2000). MEX-5 and MEX-6 are closely related proteins and are both preferentially localized toward the anterior cytoplasm of the one-cell embryo and are enriched in the somatic daughter after the division of each germline blastomere (Cuenca et al., 2003;Schubert et al., 2000). Whereas mex-5 mutants exhibit 100% embryonic lethality, mex-6 mutant embryos are 100% viable with no observable defects (Schubert et al., 2000). However, many molecular defects in mex-5 mutant embryos are dramatically enhanced when mex-6 is also mutated or depleted, suggesting partially redundant functions for these two genes (Schubert et al., 2000). For simplicity, unless specifically noted, we will use MEX-5/6 to refer to MEX-5 and MEX-6.One major function of MEX-5/6 is to restrict the localization of maternally supplied germline proteins, such as PIE-1, POS-1 and MEX-1, to germline blastomeres (Guedes and Priess, 1997;Mello et al., 1996;Schubert et al., 2000;Tabara et al., 1999). In the onecell embryo, as MEX-5/6 become asymmetrically localized anteriorly, PIE-1 becomes localized posteriorly (Cuenca et al., 2003;Mello et al., 1996;Schubert et al., 2000). After cell division, PIE-1 is enriched in P1, and this pattern reiterates in each subsequent Plineage division. The small amount of PIE-1 segregated to the somatic sister after each division is degraded by a ZIF-1-containing CUL-2 E3 ligase complex (DeRenzo et al., 2003;Reese et al., 2000). Both asymmetric distribution of PIE-1 before division, as well as asymmetric degradation after division, require the function of MEX-5/6 (DeRenzo et al., 2003;Schubert et al., 2000). MEX-5/6 are themselves also substrates for this ZIF-1-containing E3 ligase complex (DeRenzo et al., 2003).Before meiosis II, high levels of both PIE-1 and MEX-5/6 proteins are detected uniformly throughout the cytoplasm of oocytes and one-cell embryos ( Fig. 1) (Cuenca et al., 2003;Schubert et al., 2000). This suggests that localization of PIE-1 by MEX-5/6 is a developmentally regulated event ...

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The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis inCaenorhabditis elegans

Cited by 128 publications

References 50 publications

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

Polo-like kinase 1 phosphorylation of p150 ^Glued facilitates nuclear envelope breakdown during prophase

Polo kinases regulateC. elegansembryonic polarity via binding to DYRK2-primed MEX-5 and MEX-6

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The polo-like kinase PLK-1 is required for nuclear envelope breakdown and the completion of meiosis inCaenorhabditis elegans

Cited by 128 publications

References 50 publications

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

MEX-5 asymmetry in one-cellC. elegansembryos requires PAR-4-and PAR-1-dependent phosphorylation

Polo-like kinase 1 phosphorylation of p150 Glued facilitates nuclear envelope breakdown during prophase

Polo kinases regulateC. elegansembryonic polarity via binding to DYRK2-primed MEX-5 and MEX-6

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Polo-like kinase 1 phosphorylation of p150 ^Glued facilitates nuclear envelope breakdown during prophase