The conserved AAA ATPase PCH-2 distributes its regulation of meiotic prophase events through multiple meiotic HORMADs in C. elegans

Russo, Anna E; Giacopazzi, Stefani; Deshong, Alison J.; Menon, Malaika; Ortiz, Valery; Ego, Kaori M.; Corbett, K.D.; Bhalla, Needhi

doi:10.1371/journal.pgen.1010708

Cited by 5 publications

(1 citation statement)

References 91 publications

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“…The AAA+ ATPase Pch2/PCH-2 plays a conserved but enigmatic role in meiotic checkpoints (65)(66)(67)(68)(69)(70)(71)(72). Disruption of pch-2 did not perturb the retention of PLK-2 at PCs or lamin phosphorylation (Figure S11; Figure S12); however, the redistribution of PEZO-1 at the NE in response to asynapsis was abrogated (Figure S10; Figure 6A).…”

Section: Asynapsis Induces Pch-2-dependent Redistribution Of Pezo-1 A...mentioning

confidence: 99%

Chemically induced proximity reveals mechanotransduction of a meiotic checkpoint at the nuclear envelope

Liu,

Dernburg

2023

Preprint

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Successful sexual reproduction relies on robust quality control during meiosis. Assembly of the synaptonemal complex between homologous chromosomes (synapsis) regulates meiotic recombination and is crucial for accurate chromosome segregation in most eukaryotes. Synapsis defects can trigger cell cycle delays and, in some cases, apoptosis. Here, by developing and deploying a new chemically induced proximity system, we identify key players in this quality control pathway in Caenorhabditis elegans. We find that persistence of the Polo-like kinase PLK-2 at pairing centers, specialized chromosome regions that interact with the nuclear envelope to promote homolog pairing and synapsis, induces apoptosis of oocytes by phosphorylating and destabilizing the nuclear lamina. Unexpectedly, we find that a mechanosensitive Piezo1/PEZO-1 channel localizes to the nuclear envelope and is required to transduce this signal to promote apoptosis. Thus, mechanosensitive ion channels play essential roles in detecting nuclear events and triggering apoptosis during gamete production.

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Section: Asynapsis Induces Pch-2-dependent Redistribution Of Pezo-1 A...mentioning

confidence: 99%

Chemically induced proximity reveals mechanotransduction of a meiotic checkpoint at the nuclear envelope

Liu,

Dernburg

2023

Preprint

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TRIP13 localizes to synapsed chromosomes and functions as a dosage-sensitive regulator of meiosis

Chotiner,

Leu,

Yang

et al. 2023

Preprint

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Meiotic progression requires coordinated assembly and disassembly of protein complexes involved in chromosome synapsis and meiotic recombination. The AAA+ ATPase TRIP13 and its orthologue Pch2 are instrumental in remodeling HORMA domain proteins. Meiosis-specific HORMAD proteins are associated with unsynapsed chromosome axes but depleted from the synaptonemal complex (SC) of synapsed chromosome homologues. Here we report that TRIP13 localizes to the synapsed SC in early pachytene spermatocytes and to telomeres throughout meiotic prophase I. Loss of TRIP13 leads to meiotic arrest and thus sterility in both sexes.Trip13-null meiocytes exhibit abnormal persistence of HORMAD1 and HOMRAD2 on synapsed SC and chromosome asynapsis that preferentially affects XY and centromeric ends.Trip13heterozygous (Trip13+/-) mice also exhibit meiotic defects that are less severe than theTrip13-null mice, showing that TRIP13 is a dosage-sensitive regulator of meiosis. Localization of TRIP13 to the synapsed SC is independent of SC axial element proteins such as REC8 and SYCP2/SYCP3. The N- or C-terminal FLAG tagged TRIP13 proteins are functional and recapitulate the localization of native TRIP13 to SC and telomeres in knockin mice. Therefore, the evolutionarily conserved localization of TRIP13/Pch2 to the synapsed chromosomes provides a spatial explanation for dissociation of HORMA domain proteins upon chromosome synapsis in diverse organisms.

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TRIP13 localizes to synapsed chromosomes and functions as a dosage-sensitive regulator of meiosis

Chotiner,

Leu,

Yang

et al. 2024

Preprint

View full text Add to dashboard Cite

Meiotic progression requires coordinated assembly and disassembly of protein complexes involved in chromosome synapsis and meiotic recombination. The AAA+ ATPase TRIP13 and its orthologue Pch2 are instrumental in remodeling HORMA domain proteins. Meiosis-specific HORMAD proteins are associated with unsynapsed chromosome axes but depleted from the synaptonemal complex (SC) of synapsed chromosome homologues. Here we report that TRIP13 localizes to the synapsed SC in early pachytene spermatocytes and to telomeres throughout meiotic prophase I. Loss of TRIP13 leads to meiotic arrest and thus sterility in both sexes. Trip13-null meiocytes exhibit abnormal persistence of HORMAD1 and HOMRAD2 on synapsed SC and chromosome asynapsis that preferentially affects XY and centromeric ends. Trip13 heterozygous (Trip13+/-) mice also exhibit meiotic defects that are less severe than the Trip13-null mice, showing that TRIP13 is a dosage-sensitive regulator of meiosis. Localization of TRIP13 to the synapsed SC is independent of SC axial element proteins such as REC8 and SYCP2/SYCP3. The N- or C-terminal FLAG tagged TRIP13 proteins are functional and recapitulate the localization of native TRIP13 to SC and telomeres in knockin mice. Therefore, the evolutionarily conserved localization of TRIP13/Pch2 to the synapsed chromosomes provides a spatial explanation for dissociation of HORMA domain proteins upon chromosome synapsis in diverse organisms.

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The conserved AAA ATPase PCH-2 distributes its regulation of meiotic prophase events through multiple meiotic HORMADs in C. elegans

Cited by 5 publications

References 91 publications

Chemically induced proximity reveals mechanotransduction of a meiotic checkpoint at the nuclear envelope

Chemically induced proximity reveals mechanotransduction of a meiotic checkpoint at the nuclear envelope

TRIP13 localizes to synapsed chromosomes and functions as a dosage-sensitive regulator of meiosis

TRIP13 localizes to synapsed chromosomes and functions as a dosage-sensitive regulator of meiosis

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