A sodium-dependent trehalose transporter contributes to anhydrobiosis in insect cell line, Pv11

Author:

Mizutani Kosuke1ORCID,Yoshida Yuki2,Nakanishi Eita1,Miyata Yugo3,Tokumoto Shoko24,Fuse Hiroto1,Gusev Oleg4,Kikuta Shingo5,Kikawada Takahiro12ORCID

Affiliation:

1. Department of Integrated Biosciences, Graduate School of Frontier Science, The University of Tokyo, Kashiwa, Chiba 277-8562, Japan

2. Division of Biomaterial Sciences, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8634, Japan

3. Department of Medical Chemistry, Medical Research Institute, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8510, Japan

4. Intractable Disease Research Center, Graduate School of Medicine, Juntendo University, Bunkyo-ku, Tokyo 113-8421, Japan

5. Department of Regional and Comprehensive Agriculture, College of Agriculture, Ibaraki University, Ami, Ibaraki 300-0393, Japan

Abstract

Pv11 is the only animal cell line that, when preconditioned with a high concentration of trehalose, can be preserved in the dry state at room temperature for more than one year while retaining the ability to resume proliferation. This extreme desiccation tolerance is referred to as anhydrobiosis. Here, we identified a transporter that contributes to the recovery of Pv11 cells from anhydrobiosis. In general, the solute carrier 5 (SLC5)-type secondary active transporters cotransport Na + and carbohydrates including glucose. The heterologous expression systems showed that the transporter belonging to the SLC5 family, whose expression increases upon rehydration, exhibits Na + -dependent trehalose transport activity. Therefore, we named it STRT1 (sodium-ion trehalose transporter 1). We report an SLC5 family member that transports a naturally occurring disaccharide, such as trehalose. Knockout of the Strt1 gene significantly reduced the viability of Pv11 cells upon rehydration after desiccation. During rehydration, when intracellular trehalose is no longer needed, Strt1 -knockout cells released the disaccharide more slowly than the parental cell line. During rehydration, Pv11 cells became roughly spherical due to osmotic pressure changes, but then returned to their original spindle shape after about 30 min. Strt1 -knockout cells, however, required about 50 min to adopt their normal morphology. STRT1 probably regulates intracellular osmolality by releasing unwanted intracellular trehalose with Na + , thereby facilitating the recovery of normal cell morphology during rehydration. STRT1 likely improves the viability of dried Pv11 cells by rapidly alleviating the significant physical stresses that arise during rehydration.

Funder

MEXT | Japan Society for the Promotion of Science

MEXT | Japan Science and Technology Agency

Publisher

Proceedings of the National Academy of Sciences

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