Abstract
During meiosis, protein ensembles in the nuclear envelope (NE) containing SUN- and KASH-domain proteins, called linker nucleocytoskeleton and cytoskeleton (LINC) complex, promote the chromosome motion. Yeast SUN-domain protein, Mps3, forms multiple meiosis-specific ensembles on NE, which show dynamic localisation for chromosome motion; however, the mechanism by which these Mps3 ensembles are formed during meiosis remains largely unknown. Here, we showed that the cyclin-dependent protein kinase (CDK) and Dbf4-dependent Cdc7 protein kinase (DDK) regulate meiosis-specific dynamics of Mps3 on NE, particularly by mediating the resolution of Mps3 clusters and telomere clustering. We also found that the luminal region of Mps3 juxtaposed to the inner nuclear membrane is required for meiosis-specific localisation of Mps3 on NE. Negative charges introduced by meiosis-specific phosphorylation in the luminal region of Mps3 alter its interaction with negatively charged lipids by electric repulsion in reconstituted liposomes. Phospho-mimetic substitution in the luminal region suppresses the localisation of Mps3 via the inactivation of CDK or DDK. Our study revealed multi-layered phosphorylation-dependent regulation of the localisation of Mps3 on NE for meiotic chromosome motion and NE remodelling.
Highlights
During meiosis, homologous chromosomes pair with each other
In both mitotic and meiotic cells, Mps3 is a major component of a half-bridge as well as the spindle pole body (SPB) interacting network (SPIN)
Meiosis induces the localisation and motion of Mps3 on nuclear envelope (NE), which is accompanied by the formation of large protein ensembles of the linker nucleocytoskeleton and cytoskeleton (LINC) complex in NE, detected as foci/patches
Summary
Homologous chromosomes pair with each other. This pairing leads to juxtaposition of the chromosomes along their entire length, resulting in the formation of the synaptonemal complex (SC). Nuclear movement is driven by cytoplasmic microtubule cables, along which the spindle pole body (SPB), an yeast centrosome equivalent, embedded in NE moves together with the clustered telomeres This telomere-led movement promotes the pairing of homologous loci on chromosomes. Protein ensembles embedded in NE that connect telomeres in the nucleoplasm with the cytoskeleton in the cytoplasm, which are referred to as the linker of nucleocytoskeleton and cytoskeleton (LINC) complex, promote meiotic chromosome motion (Hiraoka & Dernburg, 2009; Starr & Fridolfsson, 2010). During meiotic prophase-I, in addition to SPB, Mps localises as a distinct protein ensemble on NE as a LINC complex (Conrad et al., 2007). Mps localisation to NE, thereby controlling the assembly of meiosis-specific canonical LINC complex for chromosome motion and NE remodelling during meiosis
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