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Modulatory effect of ionizing radiation on food-NaCl associative learning: the role of subunit of G protein in Caenorhabditis elegans

Tetsuya Sakashita^*,1, Nobuyuki Hamada^*,, Daisuke D. Ikeda, Sumino Yanase, Michiyo Suzuki^*, Naoaki Ishii^|| and Yasuhiko Kobayashi^*,

^* Microbeam Radiation Biology Group, Japan Atomic Energy Agency, Takasaki, Gunma, Japan;

Department of Quantum Biology, Gunma University Graduate School of Medicine, Maebashi, Gunma, Japan;

Molecular Genetics Research Laboratory and Graduate Program in Biophysics and Biochemistry, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo, Japan;

School of Sports and Health Science, Daito Bunka University, Higashi-Matsuyama, Saitama, Japan; and

^|| Department of Molecular Life Science, Tokai University School of Medicine, Isehara, Kanagawa, Japan

¹Correspondence: Microbeam Radiation Biology Group, Quantum Beam Science Directorate, Japan Atomic Energy Agency, 1233 Watanuki-machi, Takasaki, Gunma 370-1292, Japan. E-mail: sakashita.tetsuya{at}jaea.go.jp

Ionizing radiation (IR) is known to impair learning by suppressing adult neurogenesis in the hippocampus. However, in a mature nervous system, IR-induced functional alterations that are independent of neurogenesis remain largely unknown. In the present study, we analyzed the effects of IR on a food-NaCl associative learning paradigm of adult Caenorhabditis elegans that does not undergo neurogenesis. We observed that a decrease in chemotaxis toward NaCl occurs only after combined starvation and exposure to NaCl. Exposure to IR induced an additional decrease in chemotaxis immediately after an acute dose in the transition stage of the food-NaCl associative learning. Strikingly, chronic irradiation induced negative chemotaxis in the exposed animals, i.e., the primary avoidance response. IR-induced additional decreases in chemotaxis after acute and chronic irradiation were significantly suppressed in the gpc-1 mutant, which was defective in GPC-1 (one of the two subunits of the heterotrimeric G-protein). Chemotaxis to cAMP, but not to lysine and benzaldehyde, was influenced by IR during the food-NaCl associative learning. Our novel findings suggest that IR behaves as a modulator in the food-NaCl associative learning via C. elegans GPC-1 and a specific neuronal network and may shed light on the modulatory effect of IR on learning.—Sakashita, T., Hamada, N., Ikeda, D. D., Yanase, S., Suzuki, M., Ishii, N., Kobayashi, Y. Modulatory effect of ionizing radiation on food-NaCl associative learning: the role of subunit of G protein in Caenorhabditis elegans.

Key Words: learning behavior • irradiation • nematode • GPC-1