Central Insulin Action Activates Kupffer Cells by Suppressing Hepatic Vagal Activation via the Nicotinic Alpha 7 Acetylcholine Receptor
Kumi Kimura,
Mamoru Tanida,
Naoto Nagata,
Yuka Inaba,
Hitoshi Watanabe,
Mayumi Nagashimada,
Tsuguhito Ota,
Shun-ichiro Asahara,
Yoshiaki Kido,
Michihiro Matsumoto,
Koji Toshinai,
Masamitsu Nakazato,
Toshishige Shibamoto,
Shuichi Kaneko,
Masato Kasuga,
Hiroshi Inoue
Affiliations
Kumi Kimura
Department of Physiology and Metabolism, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Mamoru Tanida
Department of Physiology II, Kanazawa Medical University, Uchinada, Ishikawa 920-0293, Japan
Naoto Nagata
Department of Cell Metabolism and Nutrition, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Yuka Inaba
Department of Physiology and Metabolism, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Hitoshi Watanabe
Department of Physiology and Metabolism, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Mayumi Nagashimada
Department of Cell Metabolism and Nutrition, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Tsuguhito Ota
Department of Cell Metabolism and Nutrition, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Shun-ichiro Asahara
Division of Diabetes and Endocrinology, Department of Internal Medicine, Kobe University Graduate School of Medicine, Kobe, Hyogo 650-0017, Japan
Yoshiaki Kido
Division of Diabetes and Endocrinology, Department of Internal Medicine, Kobe University Graduate School of Medicine, Kobe, Hyogo 650-0017, Japan
Michihiro Matsumoto
Department of Molecular Metabolic Regulation, Diabetes Research Center, Research Institute, National Center for Global Health and Medicine, Tokyo 162-8655, Japan
Koji Toshinai
Department of Neurology, Respirology, Endocrinology, and Metabolism, Faculty of Internal Medicine, University of Miyazaki, Miyazaki, Miyazaki 889-1692, Japan
Masamitsu Nakazato
Department of Neurology, Respirology, Endocrinology, and Metabolism, Faculty of Internal Medicine, University of Miyazaki, Miyazaki, Miyazaki 889-1692, Japan
Toshishige Shibamoto
Department of Physiology II, Kanazawa Medical University, Uchinada, Ishikawa 920-0293, Japan
Shuichi Kaneko
Department of Disease Control and Homeostasis, Graduate School of Medical Sciences, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Masato Kasuga
National Center for Global Health and Medicine, Tokyo 162-8655, Japan
Hiroshi Inoue
Department of Physiology and Metabolism, Brain/Liver Interface Medicine Research Center, Kanazawa University, Kanazawa, Ishikawa 920-8641, Japan
Central insulin action activates hepatic IL-6/STAT3 signaling, which suppresses the gene expression of hepatic gluconeogenic enzymes. The vagus nerve plays an important role in this centrally mediated hepatic response; however, the precise mechanism underlying this brain-liver interaction is unclear. Here, we present our findings that the vagus nerve suppresses hepatic IL-6/STAT3 signaling via α7-nicotinic acetylcholine receptors (α7-nAchR) on Kupffer cells, and that central insulin action activates hepatic IL-6/STAT3 signaling by suppressing vagal activity. Indeed, central insulin-mediated hepatic IL-6/STAT3 activation and gluconeogenic gene suppression were impeded in mice with hepatic vagotomy, pharmacological cholinergic blockade, or α7-nAchR deficiency. In high-fat diet-induced obese and insulin-resistant mice, control of the vagus nerve by central insulin action was disturbed, inducing a persistent increase of inflammatory cytokines. These findings suggest that dysregulation of the α7-nAchR-mediated control of Kupffer cells by central insulin action may affect the pathogenesis of chronic hepatic inflammation in obesity.