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J Biol Chem, Vol. 273, Issue 32, 20300-20307, August 7, 1998

Ethidium Bromide-induced Inhibition of Mitochondrial Gene Transcription Suppresses Glucose-stimulated Insulin Release in the Mouse Pancreatic beta -Cell Line beta HC9

Takaki Hayakawaa, Mitsuhiko Nodaade, Kazuki Yasudaaf, Hiroshi Yorifujih, Shigeki Taniguchii, Ichitomo Miwai, Hiroshi Sakuraa, Yasuo Terauchia, Jun-ichi Hayashij, Geoffrey W. G. Sharpe, Yasunori Kanazawad, Yasuo Akanumaf, Yoshio Yazakia, and Takashi Kadowakia

From the a Third Department of Internal Medicine, Faculty of Medicine, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan, d Omiya Medical Center, Jichi Medical School, Omiya, Saitama 330, Japan, f The Institute for Diabetes Care and Research, Asahi Life Foundation, Chiyoda-ku, Tokyo 100, h Second Department of Anatomy, National Defense Medical College, Tokorozawa, Saitama 359, Japan, i Department of Pathobiochemistry, Faculty of Pharmacy, Meijo University, Tenpaku-ku, Nagoya, Aichi 468, Japan, j Institute of Biological Science, University of Tsukuba, Tsukuba, Ibaraki 305, Japan, and e Department of Pharmacology, College of Veterinary Medicine, Cornell University, Ithaca, New York 14853

Recently, a mitochondrial mutation was found to be associated with maternally inherited diabetes mellitus (Kadowaki, T., Kadowaki, H., Mori, Y., Tobe, K., Sakuta, R., Suzuki, Y., Tanabe, Y, Sakura, H., Awata, T., Goto, Y., Hayakawa, T., Matsuoka, K., Kawamori, R., Kamada, T., Horai, S., Nonaka, I., Hagura, R., Akanuma, Y., and Yazaki, Y. (1994) N. Engl. J. Med. 330, 962-968). In order to elucidate its etiology, we have investigated the involvement of mitochondrial function in insulin secretion. Culture of the pancreatic beta -cell line, beta HC9, with low dose ethidium bromide (EB) (0.4 µg/ml) for 2-6 days resulted in a substantial decrease in the transcription level of mitochondrial DNA (to 10-20% of the control cells) without changing its copy number, whereas the transcription of nuclear genes was grossly unaffected. Electron microscopic analysis revealed that treatment by EB caused morphological changes only in mitochondria and not in other organelles such as nuclei, endoplasmic reticula, Golgi bodies, or secretory granules. When the cells were treated with EB for 6 days, glucose (20 mM) could no longer stimulate insulin secretion, while glibenclamide (1 µM) still did. When EB was removed after 3- or 6-day treatment, mitochondrial gene transcription recovered within 2 days, and the profiles of insulin secretion returned to normal within 7 days. Studies with fura-2 indicated that in EB-treated cells, glucose (20 mM) failed to increase intracellular Ca2+, while the effect of glibenclamide (1 µM) was maintained. Our system provides a unique way to investigate the relationship between mitochondrial function and insulin secretion.

Copyright © 1998 by The American Society for Biochemistry and Molecular Biology, Inc.
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