scholarly journals Spatial and temporal control of targeting Polo-like kinase during meiotic prophase

2020 ◽  
Vol 219 (11) ◽  
Author(s):  
James N. Brandt ◽  
Katarzyna A. Hussey ◽  
Yumi Kim
Keyword(s):  
Chromosome Segregation ◽  
Meiotic Prophase ◽  
Meiotic Chromosome ◽  
Holocentric Chromosomes ◽  
Cyclin Dependent Kinase ◽  
Chromosome Dynamics ◽  
C Elegans ◽  
Meiotic Progression ◽  
Crossover Site ◽  
Meiosis I

Polo-like kinases (PLKs) play widely conserved roles in orchestrating meiotic chromosome dynamics. However, how PLKs are targeted to distinct subcellular localizations during meiotic progression remains poorly understood. Here, we demonstrate that the cyclin-dependent kinase CDK-1 primes the recruitment of PLK-2 to the synaptonemal complex (SC) through phosphorylation of SYP-1 in C. elegans. SYP-1 phosphorylation by CDK-1 occurs just before meiotic onset. However, PLK-2 docking to the SC is prevented by the nucleoplasmic HAL-2/3 complex until crossover designation, which constrains PLK-2 to special chromosomal regions known as pairing centers to ensure proper homologue pairing and synapsis. PLK-2 is targeted to crossover sites primed by CDK-1 and spreads along the SC by reinforcing SYP-1 phosphorylation on one side of each crossover only when threshold levels of crossovers are generated. Thus, the integration of chromosome-autonomous signaling and a nucleus-wide crossover-counting mechanism partitions holocentric chromosomes relative to the crossover site, which ultimately defines the pattern of chromosome segregation during meiosis I.

scholarly journals Shugoshin protects centromere pairing and promotes segregation of non-exchange partner chromosomes in meiosis

2018 ◽  
Author(s):  
Luciana Previato de Almeida ◽  
Jared M. Evatt ◽  
Hoa H. Chuong ◽  
Emily L. Kurdzo ◽  
Craig A. Eyster ◽  
...  
Keyword(s):  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Meiotic Prophase ◽  
Single Unit ◽  
Meiotic Chromosome ◽  
Model Systems ◽  
Meiotic Spindle ◽  
Homologous Chromosomes ◽  
Meiosis I

ABSTRACTFaithful chromosome segregation during meiosis I depends upon the formation of connections between homologous chromosomes. Crossovers between homologs connect the partners allowing them to attach to the meiotic spindle as a unit, such that they migrate away from one another at anaphase I. Homologous partners also become connected by pairing of their centromeres in meiotic prophase. This centromere pairing can promote proper segregation at anaphase I of partners that have failed to become joined by a crossover. Centromere pairing is mediated by synaptonemal complex (SC) proteins that persist at the centromere when the SC disassembles. Here, using mouse spermatocyte and yeast model systems, we tested the role of shugoshin in promoting meiotic centromere pairing by protecting centromeric synaptonemal components from disassembly. The results show that shugoshin protects centromeric SC in meiotic prophase and, in anaphase, promotes the proper segregation of partner chromosomes that are not linked by a crossover.SIGNIFICANCEMeiotic crossovers form a connection between homologous chromosomes that allows them to attach to the spindle as a single unit in meiosis I. In humans, failures in this process are a leading cause of aneuploidy. A recently described process, called centromere pairing, can also help connect meiotic chromosome partners in meiosis. Homologous chromosomes become tightly joined by a structure called the synaptonemal complex (SC) in meiotic prophase. After the SC disassembles, persisting SC proteins at the centromeres mediate their pairing. Here, studies in mouse spermatocytes and yeast are used to show that the shugoshin protein helps SC components persist at centromeres and helps centromere pairing promote the proper segregation of yeast chromosomes that fail to become tethered by crossovers.

scholarly journals Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis

2012 ◽  
Vol 196 (1) ◽  
pp. 47-64 ◽  
Author(s):  
David J. Wynne ◽  
Ofer Rog ◽  
Peter M. Carlton ◽  
Abby F. Dernburg
Keyword(s):  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Search Rate ◽  
Homologous Pairing ◽  
Chromosome Dynamics ◽  
C Elegans ◽  
Diverse Species ◽  
And Function ◽  
Chromosome Motion ◽  
Chromosome Regions

Meiotic chromosome segregation requires homologue pairing, synapsis, and crossover recombination, which occur during meiotic prophase. Telomere-led chromosome motion has been observed or inferred to occur during this stage in diverse species, but its mechanism and function remain enigmatic. In Caenorhabditis elegans, special chromosome regions known as pairing centers (PCs), rather than telomeres, associate with the nuclear envelope (NE) and the microtubule cytoskeleton. In this paper, we investigate chromosome dynamics in living animals through high-resolution four-dimensional fluorescence imaging and quantitative motion analysis. We find that chromosome movement is constrained before meiosis. Upon prophase onset, constraints are relaxed, and PCs initiate saltatory, processive, dynein-dependent motions along the NE. These dramatic motions are dispensable for homologous pairing and continue until synapsis is completed. These observations are consistent with the idea that motions facilitate pairing by enhancing the search rate but that their primary function is to trigger synapsis. This quantitative analysis of chromosome dynamics in a living animal extends our understanding of the mechanisms governing faithful genome inheritance.

scholarly journals Saccharomyces cerevisiaedeficient in the early anaphase release of Cdc14 can traverse anaphase I without ribosomal DNA disjunction and successfully complete meiosis

2021 ◽  
Author(s):  
Christopher M. Yellman
Keyword(s):  
Chromosome Segregation ◽  
Ribosomal Dna ◽  
Meiotic Chromosome ◽  
Spindle Pole ◽  
Cyclin Dependent Kinase ◽  
Binding Partner ◽  
Meiotic Progression ◽  
Nuclear Domain ◽  
Early Anaphase ◽  
Mutant Cells

ABSTRACTEukaryotic meiosis is a specialized cell cycle involving two successive nuclear divisions that lead to the formation of haploid gametes. The phosphatase Cdc14 plays an essential role in meiosis as revealed in studies of the yeastSaccharomyces cerevisiae. Cdc14 is stored in the nucleolus, a sub-nuclear domain containing the ribosomal DNA, and its release is regulated by two distinct pathways, one acting in early anaphase I of meiosis and a second at the exit from meiosis II. The early anaphase release is thought to be important for disjunction of the ribosomal DNA, disassembly of the anaphase I spindle, spindle pole re-duplication and the counteraction of CDK, all of which are required for progression into meiosis II. The release of Cdc14 from its nucleolar binding partner Net1 is stimulated by phosphorylation of cyclin-dependent kinase sites in Net1, but the importance of that phospho-regulation in meiosis is not well understood. We inducednet1-6cdkmutant cells to enter meiosis and examined the localization of Cdc14 and various indicators of meiotic progression. Thenet1-6cdkmutations inhibit, but don’t fully prevent Cdc14 release, and they almost completely prevent disjunction of the ribosomal DNA during meiosis I. Failure to disjoin the ribosomal DNA is lethal in mitosis, and we expected the same to be true in meiosis. However, the cells were able to complete meiosis II, yielding the expected four meiotic products as viable spores. Therefore, all ribosomal DNA disjunction required for meiosis can occur in meiosis II. We discuss the implications of these findings for our understanding of meiotic chromosome segregation.

scholarly journals Double or nothing: a Drosophila mutation affecting meiotic chromosome segregation in both females and males.

Genetics ◽  
1994 ◽  
Vol 136 (3) ◽  
pp. 953-964 ◽  
Author(s):  
D P Moore ◽  
W Y Miyazaki ◽  
J E Tomkiel ◽  
T L Orr-Weaver
Keyword(s):  
Cell Death ◽  
Chromosome Segregation ◽  
Sister Chromatid ◽  
Meiotic Chromosome ◽  
Sister Chromatid Cohesion ◽  
Aberrant Chromosome ◽  
Chromatid Cohesion ◽  
Meiotic Nondisjunction ◽  
Lethal Allele ◽  
Meiosis I

Abstract We describe a Drosophila mutation, Double or nothing (Dub), that causes meiotic nondisjunction in a conditional, dominant manner. Previously isolated mutations in Drosophila specifically affect meiosis either in females or males, with the exception of the mei-S332 and ord genes which are required for proper sister-chromatid cohesion. Dub is unusual in that it causes aberrant chromosome segregation almost exclusively in meiosis I in both sexes. In Dub mutant females both nonexchange and exchange chromosomes undergo nondisjunction, but the effect of Dub on nonexchange chromosomes is more pronounced. Dub reduces recombination levels slightly. Multiple nondisjoined chromosomes frequently cosegregate to the same pole. Dub results in nondisjunction of all chromosomes in meiosis I of males, although the levels are lower than in females. When homozygous, Dub is a conditional lethal allele and exhibits phenotypes consistent with cell death.

scholarly journals Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

2017 ◽  
Author(s):  
Aya Sato-Carlton ◽  
Chihiro Nakamura-Tabuchi ◽  
Stephane Kazuki Chartrand ◽  
Tomoki Uchino ◽  
Peter Mark Carlton
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
C Elegans ◽  
Chromosome Domains ◽  
Chromatid Cohesion ◽  
Complex Protein ◽  
Chromosomal Passenger ◽  
Synaptonemal Complex Protein ◽  
A Site ◽  
Meiosis I

AbstractChromosomes that have undergone crossing-over in meiotic prophase must maintain sister chromatid cohesion somewhere along their length between the first and second meiotic divisions. While many eukaryotes use the centromere as a site to maintain cohesion, the holocentric organism C. elegans instead creates two chromosome domains of unequal length termed the short arm and long arm, which become the first and second site of cohesion loss at meiosis I and II. The mechanisms that confer distinct functions to the short and long arm domains remain poorly understood. Here, we show that phosphorylation of the synaptonemal complex protein SYP-1 is required to create these domains. Once crossovers are made, phosphorylated SYP-1 and PLK-2 become cooperatively confined to short arms and guide phosphorylated histone H3 and the chromosomal passenger complex to the site of meiosis I cohesion loss. Our results show that PLK-2 and phosphorylated SYP-1 ensure creation of the short arm subdomain, promoting disjunction of chromosomes in meiosis I.

scholarly journals Increased Expression of Maturation Promoting Factor Components Speeds Up Meiosis in Oocytes from Aged Females

2018 ◽  
Vol 19 (9) ◽  
pp. 2841 ◽  
Author(s):  
Marketa Koncicka ◽  
Anna Tetkova ◽  
Denisa Jansova ◽  
Edgar Del Llano ◽  
Lenka Gahurova ◽  
...  
Keyword(s):  
Chromosome Segregation ◽  
Maternal Age ◽  
Germ Line ◽  
Nuclear Lamina ◽  
Nuclear Envelope Breakdown ◽  
Meiotic Progression ◽  
Translational Activity ◽  
Female Germ Line ◽  
Mammalian Female ◽  
Meiosis I

The rate of chromosome segregation errors that emerge during meiosis I in the mammalian female germ line are known to increase with maternal age; however, little is known about the underlying molecular mechanism. The objective of this study was to analyze meiotic progression of mouse oocytes in relation to maternal age. Using the mouse as a model system, we analyzed the timing of nuclear envelope breakdown and the morphology of the nuclear lamina of oocytes obtained from young (2 months old) and aged females (12 months old). Oocytes obtained from older females display a significantly faster progression through meiosis I compared to the ones obtained from younger females. Furthermore, in oocytes from aged females, lamin A/C structures exhibit rapid phosphorylation and dissociation. Additionally, we also found an increased abundance of MPF components and increased translation of factors controlling translational activity in the oocytes of aged females. In conclusion, the elevated MPF activity observed in aged female oocytes affects precocious meiotic processes that can multifactorially contribute to chromosomal errors in meiosis I.

Regulation of chromosome dynamics by Hsk1/Cdc7 kinase

2013 ◽  
Vol 41 (6) ◽  
pp. 1712-1719 ◽  
Author(s):  
Seiji Matsumoto ◽  
Hisao Masai
Keyword(s):  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Centromeric Heterochromatin ◽  
Minichromosome Maintenance ◽  
Replicative Helicase ◽  
Heterochromatin Formation ◽  
Chromosome Dynamics ◽  
Essential Components ◽  
Cdc7 Kinase ◽  
Cell Division Cycle 7

Hsk1 (homologue of Cdc7 kinase 1) of the fission yeast is a member of the conserved Cdc7 (cell division cycle 7) kinase family, and promotes initiation of chromosome replication by phosphorylating Mcm (minichromosome maintenance) subunits, essential components for the replicative helicase. Recent studies, however, indicate more diverse roles for Hsk1/Cdc7 in regulation of various chromosome dynamics, including initiation of meiotic recombination, meiotic chromosome segregation, DNA repair, replication checkpoints, centromeric heterochromatin formation and so forth. Hsk1/Cdc7, with its unique target specificity, can now be regarded as an important modulator of various chromosome transactions.

scholarly journals Intertwined Functions of Separase and Caspase in Cell Division and Programmed Cell Death

2019 ◽  
Author(s):  
Pan-Young Jeong ◽  
Ashish Kumar ◽  
Pradeep Joshi ◽  
Joel H. Rothman
Keyword(s):  
Cell Proliferation ◽  
Cell Division ◽  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Cysteine Proteases ◽  
Embryonic Lethality ◽  
Substrate Specificities ◽  
C Elegans ◽  
Cell Suicide ◽  
Chromosome Disjunction

AbstractTimely sister chromatid separation, promoted by separase, is essential for faithful chromosome segregation. Separase is a member of the CD clan of cysteine proteases, which also includes the pro-apoptotic enzymes known as caspases. We report that the C. elegans separase SEP-1, primarily known for its role in cell division, is required for apoptosis when the predominant pro-apoptotic caspase CED-3 is compromised. Loss of SEP-1 results in extra surviving cells in a weak ced-3(−) mutant, and suppresses the embryonic lethality of a mutant defective for the apoptotic suppressor ced-9/Bcl-2. We also report apparent non-apoptotic roles for CED-3 in promoting germ cell proliferation and germline meiotic chromosome disjunction and the normal rate of embryonic development. Moreover, loss of the soma-specific (CSP-3) and germline-specific (CSP-2) caspase inhibitors results in CED-3-dependent suppression of embryonic lethality and meiotic chromosome non-disjunction respectively, when separase function is compromised. Thus, while caspases and separases have evolved different substrate specificities associated with their specialized functions in apoptosis and cell division respectively, they appear to have retained the residual ability to participate in both processes, supporting the view that co-option of components in cell division may have led to the innovation of programmed cell suicide early in metazoan evolution.

scholarly journals The MAP kinase pathway coordinates crossover designation with disassembly of synaptonemal complex proteins during meiosis

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Saravanapriah Nadarajan ◽  
Firaz Mohideen ◽  
Yonatan B Tzur ◽  
Nuria Ferrandiz ◽  
Oliver Crawley ◽  
...  
Keyword(s):  
Map Kinase ◽  
Synaptonemal Complex ◽  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Late Pachytene ◽  
C Elegans ◽  
Map Kinase Pathway ◽  
Rho Gef ◽  
Kinase Signaling Pathway ◽  
Kinase Pathway

Asymmetric disassembly of the synaptonemal complex (SC) is crucial for proper meiotic chromosome segregation. However, the signaling mechanisms that directly regulate this process are poorly understood. Here we show that the mammalian Rho GEF homolog, ECT-2, functions through the conserved RAS/ERK MAP kinase signaling pathway in the C. elegans germline to regulate the disassembly of SC proteins. We find that SYP-2, a SC central region component, is a potential target for MPK-1-mediated phosphorylation and that constitutively phosphorylated SYP-2 impairs the disassembly of SC proteins from chromosomal domains referred to as the long arms of the bivalents. Inactivation of MAP kinase at late pachytene is critical for timely disassembly of the SC proteins from the long arms, and is dependent on the crossover (CO) promoting factors ZHP-3/RNF212/Zip3 and COSA-1/CNTD1. We propose that the conserved MAP kinase pathway coordinates CO designation with the disassembly of SC proteins to ensure accurate chromosome segregation.

New B-type cyclin synthesis is required between meiosis I and II duringXenopusoocyte maturation

Development ◽  
2001 ◽  
Vol 128 (19) ◽  
pp. 3795-3807 ◽  
Author(s):  
Helfrid Hochegger ◽  
Andrea Klotzbücher ◽  
Jane Kirk ◽  
Mike Howell ◽  
Katherine le Guellec ◽  
...  
Keyword(s):  
Protein Synthesis ◽  
Translational Control ◽  
Antisense Oligonucleotides ◽  
Kinase Activity ◽  
Meiotic Spindle ◽  
Cyclin Dependent Kinase ◽  
Metaphase Arrest ◽  
Meiotic Progression ◽  
New Protein ◽  
Meiosis I

Progression through meiosis requires two waves of maturation promoting factor (MPF) activity corresponding to meiosis I and meiosis II. Frog oocytes contain a pool of inactive ‘pre-MPF’ consisting of cyclin-dependent kinase 1 bound to B-type cyclins, of which we now find three previously unsuspected members, cyclins B3, B4 and B5. Protein synthesis is required to activate pre-MPF, and we show here that this does not require new B-type cyclin synthesis, probably because of a large maternal stockpile of cyclins B2 and B5. This stockpile is degraded after meiosis I and consequently, the activation of MPF for meiosis II requires new cyclin synthesis, principally of cyclins B1 and B4, whose translation is strongly activated after meiosis I. If this wave of new cyclin synthesis is ablated by antisense oligonucleotides, the oocytes degenerate and fail to form a second meiotic spindle. The effects on meiotic progression are even more severe when all new protein synthesis is blocked by cycloheximide added after meiosis I, but can be rescued by injection of indestructible B-type cyclins. B-type cyclins and MPF activity are required to maintain c-mos and MAP kinase activity during meiosis II, and to establish the metaphase arrest at the end of meiotic maturation. We discuss the interdependence of c-mos and MPF, and reveal an important role for translational control of cyclin synthesis between the two meiotic divisions.

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