A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony

Whitfield, Zachary J.; Chisholm, Jennifer; Hawley, R. Scott; Orr‐Weaver, Terry L.

doi:10.1371/journal.pbio.1001648

Cited by 43 publications

(48 citation statements)

References 56 publications

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“…Furthermore, we previously showed that at least one of its substrates, the Polo kinase inhibitor Matrimony, must be removed for proper embryogenesis (46). By defining the proteome of cortex mutant eggs, we identified proteins dependent on the CORT form of the APC for removal at egg activation.…”

Section: Discussionmentioning

confidence: 99%

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Kronja

Whitfield

Yuan

et al. 2014

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

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The onset of development is marked by two major, posttranscriptionally controlled, events: oocyte maturation (release of the prophase I primary arrest) and egg activation (release from the secondary meiotic arrest). Using quantitative mass spectrometry, we previously described proteome remodeling during Drosophila egg activation. Here, we describe our quantitative mass spectrometry-based analysis of the changes in protein levels during Drosophila oocyte maturation. This study presents the first quantitative survey, to our knowledge, of proteome changes accompanying oocyte maturation in any organism and provides a powerful resource for identifying both key regulators and biological processes driving this critical developmental window. We show that Muskelin, found to be up-regulated during oocyte maturation, is required for timely nurse cell nuclei clearing from mature egg chambers. Other proteins up-regulated at maturation are factors needed not only for late oogenesis but also completion of meiosis and early embryogenesis. Interestingly, the down-regulated proteins are predominantly involved in RNA processing, translation, and RNAi. Integrating datasets on the proteome changes at oocyte maturation and egg activation uncovers dynamics in proteome remodeling during the change from oocyte to embryo. Notably, 66 proteins likely act uniquely during late oogenesis, because they are up-regulated at maturation and down-regulated at activation. We find down-regulation of this class of proteins to be mediated partially by APC/C CORT , a meiosis-specific form of the E3 ligase anaphase promoting complex/ cyclosome (APC/C).he change from oocyte to embryo marks the onset of development. Oocyte maturation is a prerequisite for the oocyte-toembryo transition. In most animals, oocytes undergo a prolonged arrest in prophase I to permit oocyte growth, differentiation, and stockpiling of maternal components. This arrest is released at oocyte maturation, commonly in response to hormonal cues. The nuclear envelope then breaks down, followed by assembly of the meiotic spindle. A secondary meiotic arrest ensues, occurring at metaphase II in most vertebrates and metaphase I in insects (1). The oocyte-to-embryo transition initiates with egg activation, which causes the release of the secondary arrest and the completion of meiosis. In many organisms, egg activation requires fertilization, but egg activation is independent of fertilization in Drosophila (1). In all cases, the onset of embryogenesis requires sperm entry, fusion of the male and female pronuclei, and the start of the mitotic embryonic divisions.How is this complex transition from differentiated oocyte into totipotent embryo regulated? Both oocyte maturation and egg activation occur in a transcriptionally silent context (2-4). These events are thus posttranscriptionally controlled, and translational regulation has been shown to play a crucial role. For example, resumption of meiosis in Xenopus depends on translational activation of cyclin B and mos mRNA by CPEB-mediated polyad...

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Section: Discussionmentioning

confidence: 99%

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Kronja

Whitfield

Yuan

et al. 2014

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

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“…Sequence conservation across lepidopterans and non-lepidopterans reveals a single binding site in cortex (Extended Data Fig. 9c) that probably binds the D box-like 18 degron LXEXXXN 19 . This degron binding capability is predicted for both of the full isoforms (1A (441 amino acids) and 1B (407 amino acids), although 1B apparently lacks the N-terminal C box that is usually required for APC/C binding) but not for the alternative isoforms (Extended Data Table 1).…”

Section: MMmentioning

confidence: 99%

The industrial melanism mutation in British peppered moths is a transposable element

Hof

Campagne

Rigden

et al. 2016

Nature

434

253

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Discovering the mutational events that fuel adaptation to environmental change remains an important challenge for evolutionary biology. The classroom example of a visible evolutionary response is industrial melanism in the peppered moth (Biston betularia): the replacement, during the Industrial Revolution, of the common pale typica form by a previously unknown black (carbonaria) form, driven by the interaction between bird predation and coal pollution. The carbonaria locus has been coarsely localized to a 200-kilobase region, but the specific identity and nature of the sequence difference controlling the carbonaria-typica polymorphism, and the gene it influences, are unknown. Here we show that the mutation event giving rise to industrial melanism in Britain was the insertion of a large, tandemly repeated, transposable element into the first intron of the gene cortex. Statistical inference based on the distribution of recombined carbonaria haplotypes indicates that this transposition event occurred around 1819, consistent with the historical record. We have begun to dissect the mode of action of the carbonaria transposable element by showing that it increases the abundance of a cortex transcript, the protein product of which plays an important role in cell-cycle regulation, during early wing disc development. Our findings fill a substantial knowledge gap in the iconic example of microevolutionary change, adding a further layer of insight into the mechanism of adaptation in response to natural selection. The discovery that the mutation itself is a transposable element will stimulate further debate about the importance of 'jumping genes' as a source of major phenotypic novelty.

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“…The faithful segregation of genetic material into daughter cells during cell division is crucial for the production of healthy progeny (Jin et al, 2010;Whitfield et al, 2013;Teixeira et al, 2014). Chromosome segregation is regulated by several mechanisms, including cohesion degradation and SAC-dependent surveillance (Musacchio and Ciliberto, 2012).…”

Section: A Potential Role Of Cdc201 In Meiotic Chromosome Segregationmentioning

confidence: 99%

Arabidopsis Cell Division Cycle 20.1 Is Required for Normal Meiotic Spindle Assembly and Chromosome Segregation

et al. 2015

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Cell division requires proper spindle assembly; a surveillance pathway, the spindle assembly checkpoint (SAC), monitors whether the spindle is normal and correctly attached to kinetochores. The SAC proteins regulate mitotic chromosome segregation by affecting CDC20 (Cell Division Cycle 20) function. However, it is unclear whether CDC20 regulates meiotic spindle assembly and proper homolog segregation. Here, we show that the Arabidopsis thaliana CDC20.1 gene is indispensable for meiosis and male fertility. We demonstrate that cdc20.1 meiotic chromosomes align asynchronously and segregate unequally and the metaphase I spindle has aberrant morphology. Comparison of the distribution of meiotic stages at different time points between the wild type and cdc20

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A Meiosis-Specific Form of the APC/C Promotes the Oocyte-to-Embryo Transition by Decreasing Levels of the Polo Kinase Inhibitor Matrimony

Abstract: During the oocyte-to-embryo transition in Drosophila, degradation of the Polo kinase inhibitor, Matrimony, depends on Cortex, a meiosis-specific form of the Anaphase Promoting Complex/Cyclosome that is required for the oocyte's normal transition from meiosis to mitosis.

Cited by 43 publications

References 56 publications

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

Quantitative proteomics reveals the dynamics of protein changes during Drosophila oocyte maturation and the oocyte-to-embryo transition

The industrial melanism mutation in British peppered moths is a transposable element

Arabidopsis Cell Division Cycle 20.1 Is Required for Normal Meiotic Spindle Assembly and Chromosome Segregation

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