Comparative studies of a new subfamily of human Ste20-like kinases: homodimerization, subcellular localization, and selective activation of MKK3 and p38

Yustein, Jason T.; Xia, Liang; Kahlenburg, J Michelle; Robinson, Dan R.; Templeton, Dennis J.; Kung, Hsing-Jien

doi:10.1038/sj.onc.1206605

Cited by 40 publications

(49 citation statements)

References 50 publications

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“…This is consistent with the high levels of germline expression of TAO kinase in rat and human testis (Hutchison et al 1998;Yustein et al 2003). Moreover, work in tissue culture has established a role for TAO kinase in the DNA damage-signaling response.…”

Section: Mpk-1 Signaling and The Timing Of Meiotic Dsb Repair Eventssupporting

confidence: 69%

“…Second, mutants of all genes known to directly activate/deactivate MPK-1 lead to phenotypes that differ from that of kin-18 mutants (Church et al 1995;Hajnal and Berset 2002;Hsu et al 2002;Ohmachi et al 2002). Third, mammalian TAO kinases can activate the JNK (MAPK)-and p38 (MAPK)-signaling cascade but not ERK (MAPK) (Hutchison et al 1998;Chen et al 1999;Yustein et al 2003). Therefore, we propose that KIN-18 regulates MPK-1 activation in an indirect manner by the following two mechanisms.…”

Section: Mpk-1 Signaling and The Timing Of Meiotic Dsb Repair Eventsmentioning

confidence: 99%

“…TAOs were also shown to modulate actin cytoskeletal organization via JNK (MAPK) activation (Moore et al 2000). Mammalian TAO1 and TAO2 expression is enriched in the testis, suggesting potential roles in the germline (Hutchison et al 1998;Yustein et al 2003). However, while the role of TAOs has been studied extensively in tissue culture and in somatic tissues, little is known about the function of TAO kinases in the germline.…”

mentioning

confidence: 99%

“…Thousand And One (TAO) kinases were originally identified as mammalian homologs of Ste20 protein kinase in Saccharomyces cerevisiae (Hutchison et al 1998;Chen et al 1999). In mammalian tissue culture, TAO kinases function as a MAP3K that can activate p38 (MAPK) during stress response to trigger a cell cycle checkpoint (Hutchison et al 1998;Chen et al 1999Chen et al , 2003Chen and Cobb 2001;Yustein et al 2003;Raman et al 2007). TAOs were also shown to modulate actin cytoskeletal organization via JNK (MAPK) activation (Moore et al 2000).…”

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confidence: 99%

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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

Yin¹,

Donlevy²,

Smolikove

2015

Genetics

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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.KEYWORDS KIN-18; MPK-1; TAO; meiosis; recombination; genetics of sex T HE germline contains a multitude of cells that proliferate to form a population that will undergo two meiotic divisions, giving rise to gametes. In meiosis, one round of DNA replication is followed by two cell divisions reducing the ploidy of the germ cell by half. A large fraction of the cells encompassing the germline are found in meiotic prophase I. Many of the key evolutionarily conserved events that take place in this specialized prophase are aimed at preparing chromosomes for their segregation in meiosis I. One such essential and conserved event is the formation of crossovers between homologous chromosomes. During the initial stages of meiotic prophase I (leptotene/zygotene), a protein structure named the synaptonemal complex (SC) starts to assemble between homologs (MacQueen et al. 2002;Schild-Prufert et al. 2011). Concurrently, meiotic DNA double-strand breaks (DSBs) are introduced to initiate meiotic recombination (Keeney et al. 1997;Dernburg et al. 1998). As meiosis progresses, germ cells enter pachytene where the SC is fully formed and meiotic DSBs are processed and repaired. In the presence of a fully formed SC, meiotic DSBs are repaired, giving rise to crossovers by late pachytene. In most multicellular organisms, apoptosis is activated in late pachytene and reduces the number of germ cells in the developing germline (Gumienny et al. 1999). Apoptosis serves as a quality control...

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Section: Mpk-1 Signaling and The Timing Of Meiotic Dsb Repair Eventssupporting

confidence: 69%

Section: Mpk-1 Signaling and The Timing Of Meiotic Dsb Repair Eventsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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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

Yin¹,

Donlevy²,

Smolikove

2015

Genetics

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“…Thus, we speculate that Nos suppresses expression of effectors downstream of Tao-1. In mammals, Tao-1 and its related proteins signal through the p38 MAPK pathway by activating MKK3 (53,57,58). The p38 MAPK pathway contributes to a broad variety of cellular processes, including apoptosis, by regulating gene expression (59,60).…”

Section: Discussionmentioning

confidence: 99%

Maternal Nanos represses hid / skl -dependent apoptosis to maintain the germ line in Drosophila embryos

Sato

Hayashi

Ninomiya

et al. 2007

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

135

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Nanos (Nos) is an evolutionarily conserved protein essential for the survival of primordial germ cells. In Drosophila, maternal Nos partitions into pole cells and suppresses apoptosis to permit proper germ-line development. However, how this critical event is regulated by Nos has remained elusive. Here, we report that Nos represses apoptosis of pole cells by suppressing translation of head involution defective (hid), a member of the RHG gene family that is required for Caspase activation. In addition, we demonstrate that hid acts in concert with another RHG gene, sickle (skl), to induce apoptosis. Expression of skl is induced in pole cells by maternal tao-1, a ste20-like serine/threonine kinase. Tao-1-dependent skl expression is required to potentiate hid activity. However, skl expression is largely suppressed in normal pole cells. Once the pole cells lack maternal Nos, Tao-1-dependent skl expression is fully activated, suggesting that skl expression is also restricted by Nos. These findings provide the first evidence that the germ line is maintained through the regulated expression of RHG genes.germ cell ͉ pole cell ͉ germ plasm ͉ Tao-1

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Re-evaluating the role of Tao1 in the spindle checkpoint

et al. 2010

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The spindle checkpoint restrains anaphase onset and mitotic exit until all chromosomes are stably attached to the mitotic spindle via their kinetochores. The Tao1 protein kinase was recently reported as a novel spindle checkpoint component. When an siRNA was used to repress Tao1, the essential spindle checkpoint component Mad2 failed to localise to kinetochores, and cells rapidly exited mitosis. Tao1 was also shown to interact with BubR1, another essential checkpoint component, and be rapidly degraded after mitosis, a feature typical of many mitotic regulators. Here, we identify four different siRNAs that repress Tao1 protein levels as efficiently as the previously reported siRNA. However, these siRNAs do not override the spindle checkpoint. We also present data indicating that Tao1 does not interact with BubR1 and that it is not rapidly degraded after mitosis. We show that the previously reported siRNA not only represses Tao1 but also dramatically reduces Mad2 protein levels. Crucially, expression of exogenous Mad2, but not Tao1, rescued the spindle checkpoint phenotype induced by this siRNA. Thus, the key functional data implicating Tao1 in the spindle checkpoint can be explained by an off-target siRNA phenomenon that results in Mad2 inhibition. Taken together, our data do not support the notion that Tao1 is a component of the spindle checkpoint.

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Comparative studies of a new subfamily of human Ste20-like kinases: homodimerization, subcellular localization, and selective activation of MKK3 and p38

Cited by 40 publications

References 50 publications

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

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

Maternal Nanos represses hid / skl -dependent apoptosis to maintain the germ line in Drosophila embryos

Re-evaluating the role of Tao1 in the spindle checkpoint

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