Cytoplasmic fluidization contributes to breaking spore dormancy in fission yeast

• 成果类型: Article
• 署名作者: Sakai, Keiichiro; Kondo, Yohei; Goto, Yuhei; Aoki, Kazuhiro
• 署名单位: National Institutes of Natural Sciences (NINS) - Japan; The Exploratory Research Center on Life & Living Systems (ExCELLS); National Institutes of Natural Sciences (NINS) - Japan; National Institute for Basic Biology (NIBB); Graduate University for Advanced Studies - Japan; Kyoto University; Kyoto University
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-9774
• DOI: 10.1073/pnas.2405553121
• 发表日期: 2024-06-25
• 关键词: schizosaccharomyces-pombe; neutral trehalase; physical-properties; signaling pathway; glass-formation; protein-kinase; pka1 gene; germination; glucose; diffusion

摘要

The cytoplasm is a complex, crowded environment that influences myriad cellular processes including protein folding and metabolic reactions. Recent studies have suggested that changes in the biophysical properties of the cytoplasm play a key role in cellular homeostasis and adaptation. However, it still remains unclear how cells control their cytoplasmic properties in response to environmental cues. Here, we used fission yeast spores as a model system of dormant cells to elucidate the mechanisms underlying regulation of the cytoplasmic properties. By tracking fluorescent tracer particles, we found that particle mobility decreased in spores compared to vegetative cells and rapidly increased at the onset of dormancy breaking upon glucose addition. This cytoplasmic fluidization depended on glucose - sensing via the cyclic adenosine monophosphate - protein kinase A pathway. PKA activation led to trehalose degradation through trehalase Ntp1, thereby increasing particle mobility as the amount of trehalose decreased. In contrast, the rapid cytoplasmic fluidization did not require de novo protein synthesis, cytoskeletal dynamics, or cell volume increase. Furthermore, the measurement of diffusion coefficients with tracer particles of different sizes suggests that the spore cytoplasm impedes the movement of larger protein complexes (40 to 150 nm) such as ribosomes, while allowing free diffusion of smaller molecules ( similar to 3 nm) such as second messengers and signaling proteins. Our experiments have thus uncovered a series of signaling events that enable cells to quickly fluidize the cytoplasm at the onset of dormancy breaking.