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Accepted Manuscript

Non-neuronal cardiac cholinergic system influences CNS via the vagus nerve to acquire a stress-refractory propensity

Shino Oikawa, Yuko Kai, Masayuki Tsuda, Hisayuki Ohata, Asuka Mano, Naoko Mizoguchi, Shuei Sugama, Takahiro Nemoto, Kenji Suzuki, Atsushi Kurabayashi, Kazuyo Muramoto, Makoto Kaneda, Yoshihiko Kakinuma
Clinical Science Aug 15, 2016, CS20160277; DOI: 10.1042/CS20160277
Shino Oikawa
Nippon Medical School, Tokyo, Japan
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Yuko Kai
Nippon Medical School, Tokyo, Japan
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Masayuki Tsuda
Kochi University, Kochi, Japan
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Hisayuki Ohata
Nippon Medical School, Tokyo, Japan
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Asuka Mano
Nippon Medical School, Tokyo, Japan
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Naoko Mizoguchi
Meikai University, Saitama, Japan
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Shuei Sugama
Nippon Medical School, Tokyo, Japan
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Takahiro Nemoto
Nippon Medical School, Tokyo, Japan
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Kenji Suzuki
Nippon Medical School, Tokyo, Japan
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Atsushi Kurabayashi
Kochi University, Kochi, Japan
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Kazuyo Muramoto
Meikai University, Saitama, Japan
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Makoto Kaneda
Physiology, Nippon Medica School, Tokyo, Japan
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Yoshihiko Kakinuma
Physiology, Nippon Medical School, Tokyo, 113-8602, Japan
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  • For correspondence: k12417853@nms.ac.jp
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Abstract

We previously developed cardiac ventricle-specific choline acetyltransferase ( ChAT ) gene-overexpressing transgenic mice ( ChAT tgm), i.e., an in vivo model of the cardiac non-neuronal acetylcholine (NNA) system or non-neuronal cardiac cholinergic system (NNCCS). By using this murine model, we determined that this system was responsible for characteristics of resistance to ischemia, or hypoxia, via the modulation of cellular energy metabolism and angiogenesis. In line with our previous report, neuronal ChAT-immunoreactivity in the ChAT tgm brains was not altered from that in the WT mice brains; in contrast, the ChAT tgm hearts were the organs with the highest expression of the ChAT transgene. ChAT tgm showed specific traits in a central nervous system (CNS) phenotype, including decreased response to restraint stress, less depressive-like and anxiety-like behaviors, and anti-convulsive effects, all of which may benefit the heart. These phenotypes, induced by the activation of cardiac NNCCS, were dependent on the vagus nerve, because vagus nerve stimulation (VS) in wild-type (WT) mice also evoked phenotypes similar to those of ChAT tgm, which display higher vagus nerve discharge frequency; in contrast, lateral vagotomy attenuated these traits in ChAT tgm to levels observed in WT mice. Furthermore, ChAT tgm induced several biomarkers of VS responsible for anti-convulsive and anti-depressive-like effects. These results suggest that the augmentation of the NNCCS transduces an effective and beneficial signal to the afferent pathway, which mimics VS. Therefore, the present study supports our hypothesis that activation of the NNCCS modifies CNS to a more stress-resistant state through the vagus nerve activity.

  • acetylcholine
  • non-neuronal cholinergic system
  • central nervous system
  • vagal nerve
  • heart
  • ©2016 The Author(s)

This is an Accepted Manuscript; not the final Version of Record. Archiving permitted only in line with the archiving policy of Portland Press Limited. All other rights reserved.

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Non-neuronal cardiac cholinergic system influences CNS via the vagus nerve to acquire a stress-refractory propensity
Shino Oikawa, Yuko Kai, Masayuki Tsuda, Hisayuki Ohata, Asuka Mano, Naoko Mizoguchi, Shuei Sugama, Takahiro Nemoto, Kenji Suzuki, Atsushi Kurabayashi, Kazuyo Muramoto, Makoto Kaneda, Yoshihiko Kakinuma
Clinical Science Aug 2016, CS20160277; DOI: 10.1042/CS20160277
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Non-neuronal cardiac cholinergic system influences CNS via the vagus nerve to acquire a stress-refractory propensity
Shino Oikawa, Yuko Kai, Masayuki Tsuda, Hisayuki Ohata, Asuka Mano, Naoko Mizoguchi, Shuei Sugama, Takahiro Nemoto, Kenji Suzuki, Atsushi Kurabayashi, Kazuyo Muramoto, Makoto Kaneda, Yoshihiko Kakinuma
Clinical Science Aug 2016, CS20160277; DOI: 10.1042/CS20160277

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Keywords

acetylcholine
non-neuronal cholinergic system
central nervous system
vagal nerve
heart

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