Cdc14 Early Anaphase Release, FEAR, Is Limited to the Nucleus and Dispensable for Efficient Mitotic Exit
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{"title"=>"Cdc14 Early Anaphase Release, FEAR, is limited to the nucleus and dispensable for efficient mitotic exit", "type"=>"journal", "authors"=>[{"first_name"=>"Christopher M.", "last_name"=>"Yellman", "scopus_author_id"=>"6507324640"}, {"first_name"=>"G. Shirleen", "last_name"=>"Roeder", "scopus_author_id"=>"7006794016"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84939136622", "pmid"=>"26090959", "sgr"=>"84939136622", "doi"=>"10.1371/journal.pone.0128604", "issn"=>"19326203", "pui"=>"605585530"}, "id"=>"7befec92-ead4-3d52-bb24-e13309fcc3c7", "abstract"=>"© 2015 Yellman, Roeder. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Cdc14 phosphatase is a key regulator of exit from mitosis, acting primarily through antagonism of cyclin-dependent kinase, and is also thought to be important for meiosis. Cdc14 is released from its sequestration site in the nucleolus in two stages, first by the non-essential Cdc Fourteen Early Anaphase Release (FEAR) pathway and later by the essential Mitotic Exit Network (MEN), which drives efficient export of Cdc14 to the cytoplasm. We find that Cdc14 is confined to the nucleus during early mitotic anaphase release, and during its meiosis I release. Proteins whose degradation is directed by Cdc14 as a requirement for mitotic exit (e.g. the B-type cyclin, Clb2), remain stable during mitotic FEAR, a result consistent with Cdc14 being restricted to the nucleus and not participating directly in mitotic exit. Cdc14 released by the FEAR pathway has been proposed to have a wide variety of activities, all of which are thought to promote passage through anaphase. Proposed functions of FEAR include stabilization of anaphase spindles, resolution of the rDNA to allow its segregation, and priming of the MEN so that mitotic exit can occur promptly and efficiently. We tested the model for FEAR functions using the FEAR-deficient mutation net1-6cdk. Our cytological observations indicate that, contrary to the current model, FEAR is fully dispensable for timely progression through a series of anaphase landmarks and mitotic exit, although it is required for timely rDNA segregation. The net1-6cdk mutation suppresses temperature-sensitive mutations in MEN genes, suggesting that rather than activating mitotic exit, FEAR either inhibits the MEN or has no direct effect upon it. One interpretation of this result is that FEAR delays MEN activation to ensure that rDNA segregation occurs before mitotic exit. Our findings clarify the distinction between FEAR and MEN-dependent Cdc14 activities and will help guide emerging quantitative models of this cell cycle transition.", "link"=>"http://www.mendeley.com/research/cdc14-early-anaphase-release-fear-limited-nucleus-dispensable-efficient-mitotic-exit", "reader_count"=>14, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>2, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>6, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>6}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2127340"], "description"=>"<p>Cdc14-7Myc cells undergoing meiotic nuclear divisions. Images show the most representative Cdc14 localization at each stage of meiosis I and meiosis II. Fractions represent the number of cells with that localization divided by the total number of cells imaged at that stage. Images show Cdc14-7Myc (red), tubulin (green) and DNA (blue). The white bar represents 5 μm.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455309, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cdc14_7Myc_localization_during_meiosis_I_and_II_/1455309", "title"=>"Cdc14-7Myc localization during meiosis I and II.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127339"], "description"=>"<p>Wild-type cells in log-phase mitosis were stained with DAPI to reveal DNA (in blue) and by indirect immunofluorescence to localize α-tubulin (green) and Cdc14-7Myc (red). Cell cycle stages were identified as described in Materials and Methods. Cell outlines are shown in solid white, and dashed white lines outline the region of strong DAPI-staining (i.e., the nucleus minus the nucleolus, see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#sec002\" target=\"_blank\">Materials and Methods</a>). The white bar represents 5 μm. (A) A metaphase cell with Cdc14 sequestered in the nucleolus. (B) An early anaphase cell with Cdc14 released to the nucleus. (C) A late anaphase cell with Cdc14 exported to the cytoplasm.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455308, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nuclear_limited_Cdc14_release_during_mitosis_/1455308", "title"=>"Nuclear-limited Cdc14 release during mitosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127357", "https://ndownloader.figshare.com/files/2127359", "https://ndownloader.figshare.com/files/2127360", "https://ndownloader.figshare.com/files/2127361"], "description"=>"<div><p>Cdc14 phosphatase is a key regulator of exit from mitosis, acting primarily through antagonism of cyclin-dependent kinase, and is also thought to be important for meiosis. Cdc14 is released from its sequestration site in the nucleolus in two stages, first by the non-essential Cdc <u>F</u>ourteen <u>E</u>arly <u>A</u>naphase <u>R</u>elease (FEAR) pathway and later by the essential <u>M</u>itotic <u>E</u>xit <u>N</u>etwork (MEN), which drives efficient export of Cdc14 to the cytoplasm. We find that Cdc14 is confined to the nucleus during early mitotic anaphase release, and during its meiosis I release. Proteins whose degradation is directed by Cdc14 as a requirement for mitotic exit (e.g. the B-type cyclin, Clb2), remain stable during mitotic FEAR, a result consistent with Cdc14 being restricted to the nucleus and not participating directly in mitotic exit. Cdc14 released by the FEAR pathway has been proposed to have a wide variety of activities, all of which are thought to promote passage through anaphase. Proposed functions of FEAR include stabilization of anaphase spindles, resolution of the rDNA to allow its segregation, and priming of the MEN so that mitotic exit can occur promptly and efficiently. We tested the model for FEAR functions using the FEAR-deficient mutation <i>net1-6cdk</i>. Our cytological observations indicate that, contrary to the current model, FEAR is fully dispensable for timely progression through a series of anaphase landmarks and mitotic exit, although it is required for timely rDNA segregation. The <i>net1-6cdk</i> mutation suppresses temperature-sensitive mutations in MEN genes, suggesting that rather than activating mitotic exit, FEAR either inhibits the MEN or has no direct effect upon it. One interpretation of this result is that FEAR delays MEN activation to ensure that rDNA segregation occurs before mitotic exit. Our findings clarify the distinction between FEAR and MEN-dependent Cdc14 activities and will help guide emerging quantitative models of this cell cycle transition.</p></div>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455322, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0128604.s001", "https://dx.doi.org/10.1371/journal.pone.0128604.s002", "https://dx.doi.org/10.1371/journal.pone.0128604.s003", "https://dx.doi.org/10.1371/journal.pone.0128604.s004"], "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cdc14_Early_Anaphase_Release_FEAR_Is_Limited_to_the_Nucleus_and_Dispensable_for_Efficient_Mitotic_Exit_/1455322", "title"=>"Cdc14 Early Anaphase Release, FEAR, Is Limited to the Nucleus and Dispensable for Efficient Mitotic Exit", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127351"], "description"=>"<p>Interactions of FEAR mutations with <i>lte1Δ</i> were determined by the viability of double-mutant haploid spores germinated at 30°C. To assay interactions with high-temperature-sensitive MEN mutations, cells with the indicated genotypes were grown to saturation in YPD liquid medium at 23°C and a 10-fold dilution series was plated on YPD agar. The plates were incubated at the indicated temperatures for 24–48 before being photographed. (A) Interactions of <i>slk19Δ</i> and <i>spo12Δ</i> with MEN mutations. (B) Interactions of <i>net1-6cdk</i> and <i>cdc55Δ</i> with MEN mutations. The W303 strain background carries a dominant suppressor of <i>mob1-77</i> temperature-sensitivity at an unknown locus, which we refer to as <i>DSM</i>. We backcrossed the recessive (non-suppressing) allele <i>dsm</i> along with <i>mob1-77</i> into our W303 strains a minimum of five times to eliminate the suppressor.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455316, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_interactions_between_FEAR_and_MEN_mutations_/1455316", "title"=>"Genetic interactions between FEAR and MEN mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127348"], "description"=>"<p>Cells were synchronized and arrested in mitosis as described for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.g003\" target=\"_blank\">Fig 3</a> (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.s002\" target=\"_blank\">S2 Fig</a> for cell synchrony data). (A) Cdc20-13Myc protein stability in wild-type, <i>mad2Δ</i>, <i>cdc55Δ</i> and <i>bub2Δ</i> cells. β-tubulin loading controls are indicated with arrows. (B) Stability of Clb2-9Myc, Cdc5-9Myc and Ipl1-13Myc proteins in wild-type and <i>cdc55Δ</i> cells. (C) β-actin loading controls for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.g003\" target=\"_blank\">Fig 3B</a>.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455313, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Substrates_of_APC_Cdh1_are_stable_during_FEAR_/1455313", "title"=>"Substrates of APC<sup>Cdh1</sup> are stable during FEAR.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127346"], "description"=>"<p>See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#sec002\" target=\"_blank\">Materials and Methods</a> for the mitotic growth, synchronization and nocodazole-induced arrest procedure. Images of arrested cells were collected 3.5 hours after release from G<sub>1</sub> arrest into nocodazole. Nuclear-localized GFP is shown in green and Cdc14-7Myc protein in red; the white bar represents 5 μm. Cell outlines are shown in solid white, and nuclei in dashed white lines. Cdc14 was scored as nucleolar (filled circles), nuclear (open circles) or cytoplasmic (triangles). (A) Wild-type cells with Cdc14 sequestered in the nucleolus. (B) <i>mad2Δ</i> cells with Cdc14 in the nucleolus. (C) <i>cdc55Δ</i> cells with Cdc14 released into the nucleus only. (D) <i>bub2Δ</i> cells with Cdc14 exported to the cytoplasm. (E) <i>net1-6cdk</i> cells with Cdc14 in the nucleolus. (F) <i>cdc55Δ net1-6cdk</i> cells with Cdc14 in the nucleolus.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455311, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mitotic_arrest_reveals_nuclear_limited_Cdc14_release_by_the_FEAR_pathway_/1455311", "title"=>"Mitotic arrest reveals nuclear-limited Cdc14 release by the FEAR pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127356"], "description"=>"<p><sup>a</sup> Values represent the means +/- SD.</p><p>Mitotic doubling times.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455321, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mitotic_doubling_times_/1455321", "title"=>"Mitotic doubling times.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127355"], "description"=>"<p>Synchronized cells growing at 25°C. (A) Quantitative analysis of landmarks of mitotic progression. B) Indirect immunofluorescence of Cdc14-3Myc protein in red, spindle staining in green and DAPI-stained DNA in blue. At 90 minutes, an early anaphase wild-type cell undergoing FEAR (arrow) and two <i>net1-6cdk</i> cells that have not released Cdc14 (arrows); at 110 minutes, a wild-type cell undergoing MEN release of Cdc14 (arrow) and three net1-6cdk cells undergoing MEN release; at 130 minutes both wild-type and <i>net1-6cdk</i> cells with Cdc14 returned to the nucleolus.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455320, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g008", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_net1_6cdk_cells_progress_efficiently_through_anaphase_and_mitotic_exit_/1455320", "title"=>"<i>net1-6cdk</i> cells progress efficiently through anaphase and mitotic exit.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127353"], "description"=>"<p>MEN proteins in red had mutations that interacted negatively with the indicated FEAR mutation, enhancing temperature-sensitivity. MEN proteins in green had mutations that interacted positively with the FEAR mutation, suppressing temperature-sensitivity. MEN proteins in blue had mutations that did not significantly interact with the indicated FEAR mutation. The interactions of proteins in black were not determined in this study.</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455318, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_interactions_between_FEAR_and_MEN_mutations_/1455318", "title"=>"Summary of interactions between FEAR and MEN mutations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/2127349"], "description"=>"<p>Cells were synchronized and arrested in mitosis as described for Figs <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.g003\" target=\"_blank\">3</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.g004\" target=\"_blank\">4</a> (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0128604#pone.0128604.s002\" target=\"_blank\">S2 Fig</a> for synchrony data). Cdc14 protein was scored as nucleolar (black circles), nuclear (gray circles) or cytoplasmic (triangles).</p>", "links"=>[], "tags"=>["mitotic exit", "Cdc 14", "Mitotic Exit Network", "rDNA segregation", "Anaphase Release", "delays MEN activation", "Efficient Mitotic Exit Cdc 14 phosphatase", "cell cycle transition", "mitotic anaphase release"], "article_id"=>1455314, "categories"=>["Biological Sciences"], "users"=>["Christopher M. Yellman", "G. Shirleen Roeder"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0128604.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_Cdc55_bypasses_FEAR_loss_of_function_mutants_/1455314", "title"=>"Deletion of Cdc55 bypasses FEAR loss-of-function mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-19 03:48:22"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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