Nuclear envelope buffering of cytoskeletal force stabilizes chromosome interactions in C. elegans meiosis

Abstract

Meiosis requires coordination between chromosome and nuclear envelope (NE) dynamics. Cytoskeletal forces transmitted through the NE via Linker of Nucleoskeleton and Cytoskeleton (LINC) complexes drive chromosome movement but can also compromise nuclear integrity if not properly balanced. Here, we identify the conserved inner nuclear membrane protein NEMP-1 as a key regulator that contributes to buffering of excessive force at the meiotic NE in Caenorhabditis elegans. NEMP-1 localizes to the NE throughout meiotic prophase and becomes enriched at the NE in nuclei with a weakened nuclear lamina. Simultaneous depletion of NEMP-1 and the lamin protein LMN-1 results in premature nuclear collapse and defects in chromosome synapsis and homolog pairing. These phenotypes depend on excessive dynein-mediated forces acting on a compromised NE. Furthermore, analysis of homolog pairing in the absence of synapsis revealed that NEMP-1 and LMN-1 contribute to the stabilization of synapsis-independent homolog interactions at the NE. Together, our findings reveal that excessive force at the NE can destabilize homolog interactions, and support a model in which NEMP-1 and LMN-1 cooperatively buffer cytoskeletal forces to maintain nuclear integrity while stabilizing chromosome interactions during meiosis. One-sentence summary Two nuclear envelope proteins synergize to maintain homolog interactions and meiotic nuclear integrity.