Microtubule severing by the katanin complex is activated by PPFR-1–dependent MEI-1 dephosphorylation

Gomes, José‐Eduardo; Tavernier, Nicolas; Richaudeau, Bénédicte; Formstecher, Étienne; Boulin, Thomas; Mains, Paul E.; Dumont, Julien; Pintard, Lionel

doi:10.1083/jcb.201304174

Cited by 22 publications

(38 citation statements)

References 33 publications

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“…Close inspection of the images from prior work showed that Drosophila katanin p60 was diffusely localized to the entire chromosome but was not specifically at the kinetochores (Zhang et al, 2007). (2) Some types of katanin p60 have been shown to be regulated by kinase activity (Gomes et al, 2013;Quintin, Mains, Zinke, & Hyman, 2003), specifically Aurora B kinase (Loughlin et al, 2011). (2) Some types of katanin p60 have been shown to be regulated by kinase activity (Gomes et al, 2013;Quintin, Mains, Zinke, & Hyman, 2003), specifically Aurora B kinase (Loughlin et al, 2011).…”

Section: Resultsmentioning

confidence: 99%

“…Thus, we reasoned that localizing katanin p60 to the kinetochores, where it could directly affect microtubule attachment to the chromosomes, could serve as a proofof-concept. (2) Some types of katanin p60 have been shown to be regulated by kinase activity (Gomes et al, 2013;Quintin, Mains, Zinke, & Hyman, 2003), specifically Aurora B kinase (Loughlin et al, 2011). The kinetochore is a location with high levels of Aurora B kinase activity (Tanaka et al, 2002;Cheeseman et al, 2002).…”

Section: Resultsmentioning

confidence: 99%

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Creation and testing of a new, local microtubule‐disruption tool based on the microtubule‐severing enzyme, katanin p60

2018

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Current methods to disrupt the microtubule cytoskeleton do not easily provide rapid, local control with standard cell manipulation reagents. Here, we develop a new microtubule-disruption tool based on katanin p60 severing activity and demonstrate proof-of-principle by targeting it to kinetochores in Drosophila melanogaster S2 cells. Specifically, we show that human katanin p60 can remove microtubule polymer mass in S2 cells and an increase in misaligned chromosomes when globally overexpressed. When katanin p60 was targeted to the kinetochores via Mis12, we were able to recapitulate the misalignment only when using a phosphorylation-resistant mutant katanin p60. Our results demonstrate that targeting an active version of katanin p60 to the kinetochore can reduce the fidelity of achieving full chromosome alignment in metaphase and could serve as a microtubule disruption tool for the future.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Creation and testing of a new, local microtubule‐disruption tool based on the microtubule‐severing enzyme, katanin p60

2018

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“…Contractile ring dynamics during meiosis I were more normal after mei-1 RNAi knockdown, but the furrows nevertheless often regressed and polar body extrusion usually failed. Previous studies have shown that partial loss of function mutations in mei-1 result in abnormally large second polar bodies that are produced after meiosis II, as a result of decreased microtubule severing that is required for complete disassembly of the oocyte meiosis II spindle (42, 43). Our results provide the first systematic examination of polar body extrusion during meiosis I after depletion of katanin/MEI-1, and it is possible that the late failures in polar body cytokinesis that we observed also reflect a requirement for microtubule severing.…”

Section: Discussionmentioning

confidence: 99%

“…Here we report our use of fluorescent protein fusions and live cell imaging to characterize polar body extrusion during meiosis I in mutants lacking the function of CLS-2, KLP-18 or MEI-1. Previous studies indicate that both CLS-2 and MEI-1 are involved in polar body extrusion, with oocytes lacking CLS-2 frequently failing to extrude polar bodies (27, 30, 41), and oocytes lacking MEI-1 forming very large polar bodies (16, 17, 42, 43). Furthermore, klp-18 mutants sometimes lack an oocyte pronucleus, suggesting that all oocyte chromosomes can be extruded (34).…”

Section: Introductionmentioning

confidence: 99%

C. elegansCLASP/CLS-2 negatively regulates membrane ingression throughout the oocyte cortex and is required for polar body extrusion

Schlientz

Bowerman

2020

Preprint

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1 2 3 C. elegans CLASP/CLS-2 negatively regulates membrane ingression 4 throughout the oocyte cortex and is required for polar body extrusion 5 6 Aleesa 11 12 13 Short Title: Spindle structure and polar body extrusion 14 15 2 16 Abstract 17The requirements for oocyte meiotic cytokinesis during polar body extrusion are 18 not well understood. In particular, the relationship between the oocyte meiotic spindle 19 and polar body contractile ring dynamics remains largely unknown. We have used live 20 cell imaging and spindle assembly defective mutants lacking the function of 21 CLASP/CLS-2, kinesin-12/KLP-18, or katanin/MEI-1 to investigate the relationship 22 between meiotic spindle structure and polar body extrusion in C. elegans oocytes. We 23 show that spindle bipolarity and chromosome segregation are not required for polar 24 body contractile ring formation and chromosome extrusion in klp-18 mutants, but 25 oocytes with severe spindle assembly defects due to loss of CLS-2 or MEI-1 have 26 penetrant and distinct polar body extrusion defects: CLS-2 is required early for 27 contractile ring assembly or stability, while MEI-1 is required later for contractile ring 28 constriction. We also show that CLS-2 negatively regulates membrane ingression 29 throughout the oocyte cortex during meiosis I, and we explore the relationship between 30 global cortical dynamics and oocyte meiotic cytokinesis. 313 32 Author Summary 33The precursor cells that produce gametes-sperm and eggs in animals-have 34 two copies of each chromosome, one from each parent. These precursors undergo 35 specialized cell divisions that leave each gamete with only one copy of each 36 chromosome; defects that produce incorrect chromosome number cause severe 37 developmental abnormalities. In oocytes, these cell divisions are highly asymmetric, 38 with extra chromosomes discarded into small membrane bound polar bodies, leaving 39 one chromosome set within the much larger oocyte. How oocytes assemble the 40 contractile apparatus that pinches off polar bodies remains poorly understood. To better 41 understand this process, we have used the nematode Caenorhabditis elegans to 42 investigate the relationship between the bipolar structure that separates oocyte 43 chromosomes, called the spindle, and assembly of the contractile apparatus that 44 pinches off polar bodies. We used a comparative approach, examining this relationship 45 in three spindle assembly defective mutants. Bipolar spindle assembly and 46 chromosome separation were not required for polar body extrusion, as it occurred 47 normally in mutants lacking a protein called KLP-18. However, mutants lacking the 48 protein CLS-2 failed to assemble the contractile apparatus, while mutants lacking the 49 protein MEI-1 assembled a contractile apparatus that failed to fully constrict. We also 50 found that CLS-2 down-regulates membrane ingression throughout the oocyte surface, 51 and we explored the relationship between oocyte membrane dynamics and polar body 52 extrusion. 53 Introduction 54Oocyte meiosis co...

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“…In Xenopus, phosphorylation of p60 on Ser 131 inhibits its activity (Loughlin et al, 2011;Whitehead et al, 2013). In C. elegans, p60 is also regulated by phosphorylation; an MBK-2 kinase-dependent phosphorylation leads to an inactivation of p60 and its subsequent ubiquitination and degradation (Stitzel et al, 2006;Lu and Mains, 2007;Johnson et al, 2009), while dephosphorylation by PP4 phosphatase activates p60 (Han et al, 2009;Gomes et al, 2013). Destruction of katanin by ubiquitination-dependent degradation also takes place in mammalian cells (Cummings et al, 2009;Yang et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Regulation of katanin activity in the ciliate Tetrahymena thermophila

Wacławek

Joachimiak

Hall

et al. 2016

Molecular Microbiology

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SummaryKatanin is a microtubule severing protein that functions as a heterodimer composed of an AAA domain catalytic subunit, p60, and a regulatory subunit, a WD40 repeat protein, p80. Katanin-dependent severing of microtubules is important for proper execution of key cellular activities including cell division, migration, and differentiation. Published data obtained in Caenorhabditis elegans, Xenopus and mammals indicate that katanin is regulated at multiple levels including transcription, posttranslational modifications (of both katanin and microtubules) and degradation. Little is known about how katanin is regulated in unicellular organisms. Here we show that in the ciliated protist Tetrahymena thermophila, as in Metazoa, the localization and activity of katanin requires specific domains of both p60 and p80, and that the localization of p60, but not p80, is sensitive to the levels of microtubule glutamylation. A prolonged overexpression of either a full length, or a fragment of p80 containing WD40 repeats, partly phenocopies a knockout of p60, indicating that in addition to its activating role, p80 could also contribute to the inhibition of p60. We also show that the level of p80 depends on the 26S proteasome activity.

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Microtubule severing by the katanin complex is activated by PPFR-1–dependent MEI-1 dephosphorylation

Abstract: Dephosphorylation of MEI-1 activates katanin during meiosis, whereas ubiquitin-mediated degradation of both MEI-1 and its activator PPFR-1 ensure efficient katanin inactivation during mitosis.

Cited by 22 publications

References 33 publications

Creation and testing of a new, local microtubule‐disruption tool based on the microtubule‐severing enzyme, katanin p60

Creation and testing of a new, local microtubule‐disruption tool based on the microtubule‐severing enzyme, katanin p60

C. elegansCLASP/CLS-2 negatively regulates membrane ingression throughout the oocyte cortex and is required for polar body extrusion

Regulation of katanin activity in the ciliate Tetrahymena thermophila

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