Extranuclear Structural Components that Mediate Dynamic Chromosome Movements in Yeast Meiosis

Lee, Chih Ying; Bisig, C. Gastón; Conrad, Michael M.; Ditamo, Yanina; Almeida, Luciana Previato de; Dresser, Michael E.; Pezza, Roberto J.

doi:10.1016/j.cub.2020.01.054

Cited by 23 publications

(47 citation statements)

References 65 publications

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“…We note that a recent work also suggests that Mps2 acts as a member of the t-LINC (Lee et al, 2020). In budding yeast, the combined action of Mps2 and Csm4 is needed to carry out the function of the canonical KASH protein at the t-LINC.…”

Section: Reconstituted T-linc Can Tether Telomeresmentioning

confidence: 60%

Mps2 links Csm4 and Mps3 to form a telomere-associated LINC complex in budding yeast

Fan

Jin

Koch

et al. 2020

Preprint

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The linker of the nucleoskeleton and cytoskeleton (LINC) protein complex is composed of a pair of transmembrane proteins: the KASH-domain protein localized to the outer nuclear membrane and the SUN-domain protein to the inner nuclear membrane. In budding yeast, the sole SUN-domain protein, Mps3, is thought to pair with either Csm4 or Mps2, two KASH-like proteins, to form two separate LINC complexes. Here we show that Mps2 mediates the interaction between Csm4 and Mps3 to form a heterotrimeric telomere-associated LINC (t-LINC) in budding yeast meiosis. Mps2 binds to Csm4 and Mps3, and all three are localized to the telomere. Telomeric localization of Csm4 depends on both Mps2 and Mps3; in contrast,Mps2's localization depends on Mps3 but not Csm4. Mps2-mediated t-LINC regulates telomere movement and meiotic recombination. By ectopically expressing CSM4 in vegetative yeast cells, we reconstitute the heterotrimeric t-LINC and demonstrate its ability to tether telomeres. Our findings therefore reveal the heterotrimeric composition of t-LINC in budding yeast and have implications for understanding LINC variant formation.

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Section: Reconstituted T-linc Can Tether Telomeresmentioning

confidence: 60%

Mps2 links Csm4 and Mps3 to form a telomere-associated LINC complex in budding yeast

Fan

Jin

Koch

et al. 2020

Preprint

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“…In contrast, the meiotically induced Csm4 protein forms LINC complexes with Mps3 along the NE. A recent report has shown that, during meiotic prophase, Mps2 also interacts with Csm4 at the NE mediating the coupling with the Myo2 microfilament motor associated to the actin cytoskeleton (Lee et al, 2020). During meiotic prophase, telomeres are anchored to the nucleoplasmic N-terminal domain of Mps3 by the mediation of the meiosis-specific Ndj1 protein.…”

Section: Introductionmentioning

confidence: 99%

SWR1-independent association of H2A.Z to the LINC complex promotes meiotic chromosome motion

González-Arranz

Gardner

et al. 2020

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ABSTRACTThe H2A.Z histone variant is deposited into chromatin by the SWR1 complex affecting multiple aspects of meiosis. Here we describe a SWR1-independent localization of H2A.Z at meiotic telomeres and the centrosome. We demonstrate that H2A.Z colocalizes and interacts with Mps3, the SUN component of the LINC complex that spans the nuclear envelope and links meiotic telomeres to the cytoskeleton promoting meiotic chromosome movement. H2A.Z also interacts with the meiosis-specific Ndj1 protein that anchors telomeres to the nuclear periphery via Mps3. Telomeric localization of H2A.Z depends on Ndj1 and the N-terminal domain of Mps3. Although telomeric attachment to the nuclear envelope is maintained in the absence of H2A.Z, the distribution of Mps3 is altered. The velocity of chromosome movement during meiotic prophase I is reduced in the htz1Δ mutant lacking H2A.Z, but it is unaffected in swr1Δ cells. We reveal that H2A.Z is an additional LINC-associated factor that contributes to promote telomere-driven chromosome motion critical for error-free gametogenesis.

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“…whereas Csm4 is a meiosis-specific ONM protein (Conrad et al, 2007;Kosaka et al, 2008;Wanat et al, 2008), which interacts with a unique class of KASH protein, Mps2 (Chen et al, 2019;Lee et al, 2020). Second, the formation of actin cables is specifically induced in the cytoplasm of meiotic cells (Koszul et al, 2008;Taxis et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

“…Third, NE dynamics including NE remodeling and movement occur prominently in meiotic prophase I (Conrad et al 2007;this paper). NE remodeling is accompanied by NE localization of a yeast SUN-domain protein, Mps3/Nep98 (Conrad et al, 2007) as well as Mps2 (Lee et al, 2020). In mitosis, Mps3 and Mps2 predominantly localizes to SPB as a component of the halfbridge as well as SPB-interacting network (SPIN) (Chen et al, 2019) and play an essential role in SPB duplication (Jaspersen et al, 2002;Nishikawa et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…Here we described the multilayered control of the dynamics of a NE protein with SUN domain, Mps3, during yeast meiosis. In both mitotic and meiotic cells, Mps3 is a major component of a half bridge as well as SPIN (SPB interacting network)(Chen et al, 2019;Lee et al, 2020) (Li et al, 2017). Meiosis induces the localization and motion of Mps3 on NE, which are accompanied with the formation of a large protein ensembles in NE as the LINC complex detected as foci/patches.…”

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confidence: 99%

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Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis

Rao

Sato

Challa

et al. 2020

Preprint

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SummaryDuring meiosis, protein ensembles in the nuclear envelope (NE) containing SUN- and KASH-domain proteins, called linker nucleocytoskeleton and cytoskeleton (LINC) complex, promote chromosome motion. How LINC complexes acquire the meiotic property is largely unknown. Here we showed that cyclin-dependent protein kinase (CDK) and Dbf4-dependent Cdc7 protein kinase (DDK) promote proper meiosis-specific localization of yeast SUN-domain protein Mps3 on NE and control force-dependent movement of chromosomes during meiosis. We also found a NE luminal region of Mps3 juxtaposed to inner nuclear membrane (INM) is required for meiosis-specific localization of Mps3 on NE. Negative charges introduced by meiosis-specific non-canonical phosphorylation of the luminal region of Mps3 changes its interaction with INM, which may induce NE localization by promoting the formation of a canonical LINC complex with Mps3. Our study reveals unique phosphorylation-dependent regulation on the localization and function of Mps3 protein in meiotic NE remodeling.

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Extranuclear Structural Components that Mediate Dynamic Chromosome Movements in Yeast Meiosis

Abstract: Highlights d Mps2 connects the LINC complex to the cytoskeleton d Myo2 interacts with Mps2 and connects the telomer to cytoskeleton actin filaments d Csm4 works together with Mps2 and Myo2 to regulate rapidprophase movements

Cited by 23 publications

References 65 publications

Mps2 links Csm4 and Mps3 to form a telomere-associated LINC complex in budding yeast

Mps2 links Csm4 and Mps3 to form a telomere-associated LINC complex in budding yeast

SWR1-independent association of H2A.Z to the LINC complex promotes meiotic chromosome motion

Phosphorylation of luminal region of the SUN-domain protein Mps3 promotes nuclear envelope localization during meiosis

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