Coordination of Recombination with Meiotic Progression in the Caenorhabditis elegans Germline by KIN-18, a TAO Kinase That Regulates the Timing of MPK-1 Signaling

Yizhi Yin; Sean Donlevy; Sarit Smolikove

doi:10.1534/genetics.115.177295

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Coordination of Recombination with Meiotic Progression in the Caenorhabditis elegans Germline by KIN-18, a TAO Kinase That Regulates the Timing of MPK-1 Signaling

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Coordination of Recombination with Meiotic Progression in the Caenorhabditis elegans Germline by KIN-18, a TAO Kinase That Regulates the Timing of MPK-1 Signaling

Yizhi Yin, Sean Donlevy and Sarit Smolikove

Genetics (Austin), Vol.202(1), pp.45-59

01/2016

DOI: 10.1534/genetics.115.177295

PMCID: PMC4701101

PMID: 26510792

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Abstract

Meiosis is a tightly regulated process requiring coordination of diverse events. A conserved ERK/MAPK-signaling cascade plays an essential role in the regulation of meiotic progression. The Thousand And One kinase (TAO) kinase is a MAPK kinase kinase, the meiotic role of which is unknown. We have analyzed the meiotic functions of KIN-18, the homolog of mammalian TAO kinases, in Caenorhabditis elegans. We found that KIN-18 is essential for normal meiotic progression; mutants exhibit accelerated meiotic recombination as detected both by analysis of recombination intermediates and by crossover outcome. In addition, ectopic germ-cell differentiation and enhanced levels of apoptosis were observed in kin-18 mutants. These defects correlate with ectopic activation of MPK-1 that includes premature, missing, and reoccurring MPK-1 activation. Late progression defects in kin-18 mutants are suppressed by inhibiting an upstream activator of MPK-1 signaling, KSR-2. However, the acceleration of recombination events observed in kin-18 mutants is largely MPK-1-independent. Our data suggest that KIN-18 coordinates meiotic progression by modulating the timing of MPK-1 activation and the progression of recombination events. The regulation of the timing of MPK-1 activation ensures the proper timing of apoptosis and is required for the formation of functional oocytes. Meiosis is a conserved process; thus, revealing that KIN-18 is a novel regulator of meiotic progression in C. elegans would help to elucidate TAO kinase's role in germline development in higher eukaryotes.

Animals

Apoptosis

Caenorhabditis elegans - enzymology

Caenorhabditis elegans - genetics

Caenorhabditis elegans - physiology

Caenorhabditis elegans Proteins - genetics

Caenorhabditis elegans Proteins - metabolism

Enzyme Activation

Germ Cells - enzymology

Germ Cells - physiology

MAP Kinase Signaling System

Meiosis - physiology

Mitogen-Activated Protein Kinase 1 - metabolism

Mutation

Oocytes - cytology

Prophase - genetics

Protein Kinases - genetics

Protein Kinases - metabolism

Recombination, Genetic

Details

Title: Subtitle: Coordination of Recombination with Meiotic Progression in the Caenorhabditis elegans Germline by KIN-18, a TAO Kinase That Regulates the Timing of MPK-1 Signaling
Creators: Yizhi Yin - Department of Biology, University of Iowa, Iowa City, Iowa 52242
Sean Donlevy - Department of Biology, University of Iowa, Iowa City, Iowa 52242
Sarit Smolikove - Department of Biology, University of Iowa, Iowa City, Iowa 52242 sarit-smolikove@uiowa.edu
Resource Type: Journal article
Publication Details: Genetics (Austin), Vol.202(1), pp.45-59
DOI: 10.1534/genetics.115.177295
PMID: 26510792
PMCID: PMC4701101
ISSN: 0016-6731
eISSN: 1943-2631
Grant note: R01 GM112657 / NIGMS NIH HHS P40-OD010440 / NIH HHS P40 OD010440 / NIH HHS R01GM112657 / NIGMS NIH HHS
Language: English
Date published: 01/2016
Academic Unit: Biology
Record Identifier: 9984217428802771

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