Thermotolerance in S. cerevisiae as a model to study extracellular vesicle biology

IF 15.5 1区 医学 Q1 CELL BIOLOGY Journal of Extracellular Vesicles Pub Date : 2024-05-06 DOI:10.1002/jev2.12431
Curtis John Logan, Claire C. Staton, Joshua Thomas Oliver, Jeff Bouffard, Thomas David Daniel Kazmirchuk, Melissa Magi, Christopher Leonard Brett
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Abstract

The budding yeast Saccharomyces cerevisiae is a proven model organism for elucidating conserved eukaryotic biology, but to date its extracellular vesicle (EV) biology is understudied. Here, we show yeast transmit information through the extracellular medium that increases survival when confronted with heat stress and demonstrate the EV-enriched samples mediate this thermotolerance transfer. These samples contain vesicle-like particles that are exosome-sized and disrupting exosome biogenesis by targeting endosomal sorting complexes required for transport (ESCRT) machinery inhibits thermotolerance transfer. We find that Bro1, the yeast ortholog of the human exosome biomarker ALIX, is present in EV samples, and use Bro1 tagged with green fluorescent protein (GFP) to track EV release and uptake by endocytosis. Proteomics analysis reveals that heat shock protein 70 (HSP70) family proteins are enriched in EV samples that provide thermotolerance. We confirm the presence of the HSP70 ortholog stress-seventy subunit A2 (Ssa2) in EV samples and find that mutant yeast cells lacking SSA2 produce EVs but they fail to transfer thermotolerance. We conclude that Ssa2 within exosomes shared between yeast cells contributes to thermotolerance. Through this work, we advance Saccharomyces cerevisiae as an emerging model organism for elucidating molecular details of eukaryotic EV biology and establish a role for exosomes in heat stress and proteostasis that seems to be evolutionarily conserved.

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将麦角菌的耐热性作为研究细胞外囊泡生物学的模型
芽殖酵母(Saccharomyces cerevisiae)是一种成熟的模式生物,可用于阐明保守的真核生物生物学,但迄今为止,对其细胞外囊泡(EV)生物学的研究还很不够。在这里,我们展示了酵母通过细胞外介质传递信息,从而在面临热应激时提高存活率,并证明了富含 EV 的样本介导了这种耐热性传递。这些样本含有外泌体大小的囊泡状颗粒,通过靶向运输所需的内泌体分选复合物(ESCRT)机制来破坏外泌体的生物发生,会抑制耐热性的传递。我们发现人类外泌体生物标记物 ALIX 的酵母直向同源物 Bro1 存在于 EV 样本中,并利用标记有绿色荧光蛋白(GFP)的 Bro1 跟踪 EV 的释放和内吞摄取。蛋白质组学分析表明,热休克蛋白 70(HSP70)家族蛋白在提供耐热性的 EV 样品中富集。我们证实了 EV 样本中存在 HSP70 同源物应激-70 亚基 A2(Ssa2),并发现缺乏 SSA2 的突变酵母细胞会产生 EV,但它们无法转移耐热性。我们的结论是,酵母细胞之间共享的外泌体中的Ssa2有助于提高耐热性。通过这项工作,我们将酵母菌作为一种新兴的模式生物,用于阐明真核细胞外泌体生物学的分子细节,并确立了外泌体在热应激和蛋白稳态中的作用,这种作用似乎在进化过程中得到了保护。
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来源期刊
Journal of Extracellular Vesicles
Journal of Extracellular Vesicles Biochemistry, Genetics and Molecular Biology-Cell Biology
CiteScore
27.30
自引率
4.40%
发文量
115
审稿时长
12 weeks
期刊介绍: The Journal of Extracellular Vesicles is an open access research publication that focuses on extracellular vesicles, including microvesicles, exosomes, ectosomes, and apoptotic bodies. It serves as the official journal of the International Society for Extracellular Vesicles and aims to facilitate the exchange of data, ideas, and information pertaining to the chemistry, biology, and applications of extracellular vesicles. The journal covers various aspects such as the cellular and molecular mechanisms of extracellular vesicles biogenesis, technological advancements in their isolation, quantification, and characterization, the role and function of extracellular vesicles in biology, stem cell-derived extracellular vesicles and their biology, as well as the application of extracellular vesicles for pharmacological, immunological, or genetic therapies. The Journal of Extracellular Vesicles is widely recognized and indexed by numerous services, including Biological Abstracts, BIOSIS Previews, Chemical Abstracts Service (CAS), Current Contents/Life Sciences, Directory of Open Access Journals (DOAJ), Journal Citation Reports/Science Edition, Google Scholar, ProQuest Natural Science Collection, ProQuest SciTech Collection, SciTech Premium Collection, PubMed Central/PubMed, Science Citation Index Expanded, ScienceOpen, and Scopus.
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