The G2-to-M Transition Is Ensured by a Dual Mechanism that Protects Cyclin B from Degradation by Cdc20-Activated APC/C

Lara-González, Pablo; Moyle, Mark W.; Budrewicz, Jacqueline; Mendoza-Lopez, Jose; Oegema, Karen; Desai, Arshad

doi:10.1016/j.devcel.2019.09.005

Cited by 56 publications

(47 citation statements)

References 90 publications

(124 reference statements)

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“…The germ cell cycle structure and regulation differs significantly from that of somatic cells. Germ cells have a very short or nonexistent G1 phase (Fox et al 2011;Seidel and Kimble 2015), which has been confirmed by live imaging showing the appearance of DNA replication foci immediately after telophase (Lara-Gonzalez et al 2019). In contrast, G1 is a prominent feature of the somatic cell cycle (Baugh and Sternberg 2006;Ruijtenberg and van den Heuvel 2015;van Rijnberk et al 2017;Kipreos and van den Heuvel 2019).…”

Section: Adult Germline Stem Cell System: Organization and Cell Biologymentioning

confidence: 71%

Biology of the Caenorhabditis elegans Germline Stem Cell System

Hubbard

Schedl

2019

Genetics

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Stem cell systems regulate tissue development and maintenance. The germline stem cell system is essential for animal reproduction, controlling both the timing and number of progeny through its influence on gamete production. In this review, we first draw general comparisons to stem cell systems in other organisms, and then present our current understanding of the germline stem cell system in Caenorhabditis elegans. In contrast to stereotypic somatic development and cell number stasis of adult somatic cells in C. elegans, the germline stem cell system has a variable division pattern, and the system differs between larval development, early adult peak reproduction and age-related decline. We discuss the cell and developmental biology of the stem cell system and the Notch regulated genetic network that controls the key decision between the stem cell fate and meiotic development, as it occurs under optimal laboratory conditions in adult and larval stages. We then discuss alterations of the stem cell system in response to environmental perturbations and aging. A recurring distinction is between processes that control stem cell fate and those that control cell cycle regulation. C. elegans is a powerful model for understanding germline stem cells and stem cell biology.

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Section: Adult Germline Stem Cell System: Organization and Cell Biologymentioning

confidence: 71%

Biology of the Caenorhabditis elegans Germline Stem Cell System

Hubbard

Schedl

2019

Genetics

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“…The underlying mechanism and whether it also occurs in other systems remain to be determined. However, CYB-3 plays roles in C. elegans that have not been detected for Cyclin B3 in flies or vertebrates, including a major role in mitotic entry, where CYB-3 mediates the inhibitory phosphorylation of Cdc20 (Lara-Gonzalez et al, 2019). In this regard, C. elegans CYB-3 may be more orthologous to Cyclin A.…”

Section: Mechanism and Conservation Of The Role Of Cyclin B3 In The Amentioning

confidence: 99%

Cyclin B3 activates the Anaphase-Promoting Complex/Cyclosome in meiosis and mitosis

Garrido

Bourouh

Bonneil

et al. 2020

Preprint

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In mitosis and meiosis, chromosome segregation is triggered by the Anaphase-Promoting Complex/Cyclosome (APC/C), a multi-subunit ubiquitin ligase that targets proteins for degradation, leading to the separation of chromatids. APC/C activation requires phosphorylation of its APC3 and APC1 subunits, which allows the APC/C to bind its Cdc20 co-activator. The identity of the kinase(s) responsible for APC/C activation in vivo is unclear. Cyclin B3 is required for meiotic anaphase in flies, worms and vertebrates, but whether it activates the APC/C is unclear. We found that Drosophila Cyclin B3 (CycB3) collaborates with PP2A-B55/Tws in embryonic development, indicating that CycB3 also promotes anaphase in mitosis. Moreover, CycB3 promotes APC/C activity and anaphase in cells in culture. We show that CycB3 physically associates with the APC/C, is required for phosphorylation of APC3, and promotes APC/C association with its co-activators. We propose that CycB3-Cdk1 directly phosphorylates the APC/C to activate it in both meiosis and mitosis.

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“…The slow cell cycle phenotype of the fbf-2(lf) mutant SPCs was rescued by introduction of a CYB-2.1 transgene with mutated FBE elements ( Figure 2D), suggesting that the levels of B-type cyclins are limiting for SPC progression through cell cycle in this genetic background. Among the B-type cyclins, CYB-3 has emerged as a major G2 regulator in C. elegans germline stem cells (Lara-Gonzalez et al, 2019). Since cyb-3 lacks canonical FBE elements in its 3'UTR, testing whether FBFs might regulate CYB-3 levels to control SPC division rate will require identification of the relevant non-canonical binding sites.…”

Section: Regulation Of Cyclin B By Puf-family Proteins In Stem Cellsmentioning

confidence: 99%

Antagonistic control of Caenorhabditis elegans germline stem cell proliferation and differentiation by PUF proteins FBF-1 and FBF-2

Wang

Ellenbecker

Hickey

et al. 2020

eLife

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Stem cells support tissue maintenance, but the mechanisms that coordinate the rate of stem cell self-renewal with differentiation at a population level remain uncharacterized. We find that two PUF family RNA-binding proteins FBF-1 and FBF-2 have opposite effects on C. elegans germline stem cell dynamics: FBF-1 restricts the rate of meiotic entry, while FBF-2 promotes both cell division and meiotic entry rates. Antagonistic effects of FBFs are mediated by their distinct activities towards the shared set of target mRNAs, where FBF-1-mediated post-transcriptional control requires the activity of CCR4-NOT deadenylase, while FBF-2 is deadenylase-independent and might protect the targets from deadenylation. These regulatory differences depend on protein sequences outside of the conserved PUF family RNA-binding domain. We propose that the opposing FBF-1 and FBF-2 activities serve to modulate stem cell division rate simultaneously with the rate of meiotic entry.

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The G2-to-M Transition Is Ensured by a Dual Mechanism that Protects Cyclin B from Degradation by Cdc20-Activated APC/C

Cited by 56 publications

References 90 publications

Biology of the Caenorhabditis elegans Germline Stem Cell System

Biology of the Caenorhabditis elegans Germline Stem Cell System

Cyclin B3 activates the Anaphase-Promoting Complex/Cyclosome in meiosis and mitosis

Antagonistic control of Caenorhabditis elegans germline stem cell proliferation and differentiation by PUF proteins FBF-1 and FBF-2

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