Virtual Breakdown of the Nuclear Envelope in Fission Yeast Meiosis

Asymmetric localization of Ran regulators (RanGAP1 and RanGEF/RCC1) produces a gradient of RanGTP across the nuclear envelope [1]. In higher eukaryotes, the nuclear envelope breaks down as the cell enters mitosis (designated “open” mitosis). This nuclear envelope breakdown (NEBD) leads to collapse of the RanGTP gradient and the diffusion of nuclear and cytoplasmic macromolecules in the cell, resulting in irreversible progression of the cell cycle [2–7]. On the other hand, in many fungi, chromosome segregation takes place without NEBD (designated “closed” mitosis). Here we report that in the fission yeast Schizosaccharomyces pombe, despite the nuclear envelope and the nuclear pore complex remaining intact throughout both the meiotic and mitotic cell cycles, nuclear proteins diffuse into the cytoplasm transiently for a few minutes at the onset of anaphase of meiosis II. We also found that nuclear protein diffusion into the cytoplasm occurred coincidently with nuclear localization of Rna1, an S. pombe RanGAP1 homolog that is usually localized in the cytoplasm. These results suggest that nuclear localization of RanGAP1 and depression of RanGTP activity in the nucleus may be mechanistically tied to meiosis-specific diffusion of nuclear proteins into the cytoplasm. This nucleocytoplasmic shuffling of RanGAP1 and nuclear proteins represents virtual breakdown of the nuclear envelope. [Display omitted] ► Nuclear protein diffusion in meiosis II in the fission yeast S. pombe ► Nuclear envelope and nuclear pore complexes are intact in meiosis II ► Nuclear localization of RanGAP1 is coupled with nuclear protein diffusion ► Meiosis II-specific RanGAP1 nuclear localization is related to spore formation