Transient and Partial Nuclear Lamina Disruption Promotes Chromosome Movement in Early Meiotic Prophase

Meiotic chromosome movement is important for the pairwise alignment of homologous chromosomes, which is required for correct chromosome segregation. Movement is driven by cytoplasmic forces, transmitted to chromosome ends by nuclear membrane-spanning proteins. In animal cells, lamins form a prominent scaffold at the nuclear periphery, yet the role lamins play in meiotic chromosome movement is unclear. We show that chromosome movement correlates with reduced lamin association with the nuclear rim, which requires lamin phosphorylation at sites analogous to those that open lamina network crosslinks in mitosis. Failure to remodel the lamina results in delayed meiotic entry, altered chromatin organization, unpaired or interlocked chromosomes, and slowed chromosome movement. The remodeling kinases are delivered to lamins via chromosome ends coupled to the nuclear envelope, potentially enabling crosstalk between the lamina and chromosomal events. Thus, opening the lamina network plays a role in modulating contacts between chromosomes and the nuclear periphery during meiosis. The onset of chromosome movement within meiotic prophase nuclei is accompanied by lamina structural changes resembling those associated with mitotic nuclear envelope breakdown. Link, Paouneskou et al. show that meiotic lamina crosslink remodeling, through phosphorylation by kinases delivered via chromosome ends coupled to the nuclear envelope, ensures chromosome integrity.