Coordinate Activation of Maternal Protein Degradation during the Egg-to-Embryo Transition in C. elegans

Pellettieri, Jason; Reinke, V; Kim, Stuart K.; Seydoux, Géraldine

doi:10.1016/s1534-5807(03)00231-4

Cited by 138 publications

(161 citation statements)

References 51 publications

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“…These effects were seen in two nontransformed cell types, Mv1Lu lung epithelial cells and C2C12 myoblasts. A related Dyrk family kinase, MBK-2, has been shown to coordinate the degradation of several maternal proteins, which is essential for Caenorhabditis elegans zygotes to complete cytokinesis (24). Depletion of MBK-2 by RNA interference arrested the development at the one-cell stage with multiple nuclei.…”

Section: Discussionmentioning

confidence: 99%

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Mirk/dyrk1B Kinase Destabilizes Cyclin D1 by Phosphorylation at Threonine 288

Zou

Ewton

Deng

et al. 2004

Journal of Biological Chemistry

110

128

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The phosphorylation of cyclin D1 at threonine 286 by glycogen synthase kinase 3␤ (GSK3␤) has been shown to be required for the ubiquitination and nuclear export of cyclin D1 and its subsequent degradation in the proteasome. The mutation of the nearby residue, threonine 288, to nonphosphorylatable alanine has also been shown to reduce the ubiquitination of cyclin D1, suggesting that phosphorylation at threonine 288 may also lead to degradation of cyclin D1. We now demonstrate that the G 0 /G 1 -active arginine-directed protein kinase Mirk/dyrk1B binds to cyclin D1 and phosphorylates cyclin D1 at threonine 288 in vivo and that the cyclin D1-T288A construct is more stable than wild-type cyclin Cell cycle progression in eukaryotic cells is mediated by cyclin-dependent kinases (CDKs). 1 The D-type cyclins, D1, D2, and D3, increase in nuclear abundance in G 1 in response to mitogens, facilitate the import of CDK4 into the nucleus (1), and assemble combinatorially with CDK4 or CDK6 into complexes that phosphorylate the retinoblastoma protein, releasing factors needed for the progression into S phase. Cyclin D1 is translocated into the cytoplasm during S phase where it is destroyed by the proteasome following phosphorylation at threonine 286 by GSK3␤ (2, 3). Mutant cyclin D1-T286A, which cannot be phosphorylated by GSK3␤, is stabilized in the nucleus and is capable of transforming murine fibroblasts, whereas overexpression of wild-type cyclin D1 cannot act alone to transform such cells (4). A cyclin D1 isoform derived by alternative splicing was shown to lack threonine 286, enabling this cyclin D1 isoform to remain nuclear throughout the cell cycle, remain highly expressed, and function to facilitate transformation of NIH3T3 cells (5). This cyclin D1 splice variant was also found in tumor-derived cells and primary human esophageal tumors (5). Overexpression of cyclin D1 occurs in several cancers including breast, pancreatic, and esophageal (6), suggesting that either increased transcription, transcription of stable splice variants, or dysregulation of cyclin D1 turnover may frequently occur in cancer.In this study, we have studied the interaction of the ubiquitously expressed protein kinase Mirk/dyrk1B with cyclin D1. Mirk/dyrk1B is an arginine-directed serine/threonine kinase (7), which functions as a transcriptional co-activator and is activated through the stress-activated mitogen-activated protein kinase kinase MKK3 (8). We have shown recently that Mirk stabilizes the CDK inhibitor p27kip1 in the G 0 phase of the cell cycle in NIH3T3 fibroblasts, whereas depletion of Mirk by RNA interference increases cell cycling as measured by increased PCNA expression (9). Mirk expression is decreased by mitogen activation of the MEK-ERK pathway during G 1 (10), restricting Mirk function primarily to G 0 and early G 1 . We now confirm that transient overexpression of Mirk in nontransformed Mv1Lu lung epithelial cells increases the length of G 0 /G 1 by FACS analysis and that Mirk targets the G 1 cell cycle regulator, cyclin D1, t...

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Section: Discussionmentioning

confidence: 99%

“…The mechanism of MBK-2 action is not known, but MBK-2 was not a general activator of protein degradation by the proteasome. MBK-2 was postulated to target some unknown factor but not an E3 ubiquitin ligase common to the specific group of maternal proteins, which were degraded (24).…”

Section: Discussionmentioning

confidence: 99%

Mirk/dyrk1B Kinase Destabilizes Cyclin D1 by Phosphorylation at Threonine 288

Zou

Ewton

Deng

et al. 2004

Journal of Biological Chemistry

110

128

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“…Strains bearing these mutations produce and lay eggs that fail to undergo pronuclear fusion and/or have no shells. The strains studied included egg-3, simultaneous mutation of egg-4 and egg-5, mei-1, mbk-2, and chs-1 (25)(26)(27)(28)(29). We also studied pos-1, a strain that exhibits completely normal fertilization but whose embryos fail soon thereafter (30).…”

Section: Significancementioning

confidence: 99%

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Leighton

Choe

et al. 2014

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

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Males of the androdioecious species Caenorhabditis elegans are more likely to attempt to mate with and successfully inseminate C. elegans hermaphrodites that do not concurrently harbor sperm. Although a small number of genes have been implicated in this effect, the mechanism by which it arises remains unknown. In the context of the battle of the sexes, it is also unknown whether this effect is to the benefit of the male, the hermaphrodite, or both. We report that successful contact between mature sperm and oocyte in the C. elegans gonad at the start of fertilization causes the oocyte to release a signal that is transmitted to somatic cells in its mother, with the ultimate effect of reducing her attractiveness to males. Changes in hermaphrodite attractiveness are tied to the production of a volatile pheromone, the first such pheromone described in C. elegans.fertilization | sex pheromones | egg-soma communication I ts properties of self-fertilization and rapid generation, along with its extensive library of mutants, make Caenorhabditis elegans an excellent system in which to study reproductive events. The generation time of C. elegans is under 3 d, and a single hermaphroditic worm can use its sperm to fertilize its own eggs, without the need for mating (1). C. elegans and related nematodes have a robust sperm sensation pathway that limits unfruitful oocyte maturation and ovulation (2). Both self-sperm and nonself-sperm secrete protein ligands, known as major sperm proteins (MSPs), that activate signal transduction pathways in both unfertilized oocytes, leading to activation of mitogen-activated protein kinase (MPK-1), and the somatic gonad, involving transcription factor CEH-18. The result of this signaling is the release of oocytes from prophase I arrest and the ovulation of unarrested oocytes into the uterus (3, 4).Several behaviors of female and hermaphroditic nematodes have been demonstrated to correlate with either the presence of sperm or the recentness of mating. C. elegans hermaphrodites that have exhausted their supply of self-sperm are more likely to elicit a mating response from males of their species, and less likely to resist an attempted mating. Mutant C. elegans hermaphrodites that develop without self-sperm also elicit more mating attempts, and this increase in attractiveness vanishes after a successful mating (5, 6). In the gonochoristic species Caenorhabditis brenneri and Caenorhabditis remanei, males are attracted to a volatile pheromone produced only by females that have not recently mated (7). The mechanisms that link these behaviors to sperm status remain unknown.Pheromones have been shown to exist in dozens of nematode species (8-10) and have been positively identified in several, including C. elegans (11-14). Although HPLC-MS studies have led to the identification of more than 140 pheromones and pheromone-related metabolites in C. elegans (15), little is known about how production of such pheromones is regulated. Life stage and environmental conditions have been shown to affect pheromone o...

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“…In C. elegans, protein degradation is necessary for the meiosis-to-mitosis transition and the establishment of polarity. For instance, the katanin complex MEI-1/ MEI-2 is necessary for meiotic spindle assembly, but its persistence during mitosis causes defects in mitotic spindle elongation and rotation (Pellettieri et al, 2003;Quintin et al, 2003). Furthermore, localization of a protein required for germline specification, PIE-1, occurs through regulated degradation: PIE-1 is initially ubiquitous, but then is degraded in somatic blastomeres (Pang et al, 2004).…”

Section: Maternal Protein Degradation and Phosphorylationmentioning

confidence: 99%

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

Horner

Wolfner

2008

Developmental Dynamics

181

177

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The transition from mature oocyte to developing embryo requires a coordinated series of events, collectively known as egg activation. Egg activation includes changes to egg coverings to prevent polyspermy, release of oocyte meiotic arrest, generation of haploid female and male pronuclei, changes in maternal mRNAs and protein populations, and cytoskeletal rearrangements. In many animals, egg activation is triggered by fertilization, which increases intracellular calcium within the oocyte and thereby regulates molecular events of egg activation. In other animals, fertilization-independent external signals, including mechanical stimulation of eggs and/or changes in ionic milieu, trigger activation. Recent studies have clarified the upstream portion of pathways leading to eggshell changes and cell cycle resumption and have identified activation-induced changes in maternal mRNA and protein profiles that can identify molecular players in the downstream events of egg activation. We review signals that trigger activation and how they link to subsequent molecular events of egg activation. Developmental Dynamics 237:527-544, 2008.

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Coordinate Activation of Maternal Protein Degradation during the Egg-to-Embryo Transition in C. elegans

Cited by 138 publications

References 51 publications

Mirk/dyrk1B Kinase Destabilizes Cyclin D1 by Phosphorylation at Threonine 288

Mirk/dyrk1B Kinase Destabilizes Cyclin D1 by Phosphorylation at Threonine 288

Communication between oocytes and somatic cells regulates volatile pheromone production in Caenorhabditis elegans

Transitioning from egg to embryo: Triggers and mechanisms of egg activation

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