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Gastrointestinal hormones (anorexigenic peptide YY and orexigenic ghrelin) influence neural tube development

Hideki Yuzuriha^*, Akio Inui^,1, Akihiro Asakawa^*, Naohiko Ueno^*, Masato Kasuga^*, Michael M. Meguid, Jun-ichi Miyazaki, Maiko Ninomiya^||, Herbert Herzog^¶ and Mineko Fujimiya^||

^* Division of Diabetes, Digestive and Kidney Diseases, Department of Clinical Molecular Medicine, Kobe University Graduate School of Medicine, Kobe, Japan;

Department of Behavioral Medicine, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan;

Department of Neuroscience and Surgery, SUNY Upstate Medical University, Syracuse, New York, USA;

Department of Nutrition and Physiological Chemistry, Osaka University Graduate School of Medicine, Osaka, Japan;

^|| Department of Anatomy, Shiga University of Medical Science, Otsu, Japan; and

^¶ Neurobiology Program, Garvan Institute of Medical Research, Sydney, Australia

¹Correspondence: Department of Behavioral and Internal Medicine, Kagoshima University Graduate School of Medical and Dental Sciences, 8–35-1 Sakuragaoka, Kagoshima 890-8520, Japan. E-mail: inui{at}m.kufm.kagoshima-u.ac.jp

Gastrointestinal (GI) hormones play an important role in GI secretion, motility, and eating behaviors. It was recently suggested that GI hormones may have a trophic role in GI tract. Here we demonstrate that two principal GI hormones, anorexigenic peptide YY (PYY) and orexigenic ghrelin, affect neural tube development. Chronic administration into the pregnant mice or transgenic overexpression of PYY led to a neural tube defect (NTD) in the embryos that was blocked by ghrelin. PYY Y1 receptor antagonist prevented the occurrence of NTD induced not only by PYY but also by vitamin A, a well-known teratogen in humans and animals. Y1 receptor deficiency also engendered NTDs, indicating the need to maintain normal Y1 receptor signaling. The present study is the first linking GI hormones to the leading cause of infant mortality and provides a novel insight for neurogenesis in which materno-fetal communication through GI hormones appears to be important.—Yuzuriha, H., Inui, A., Asakawa, A., Ueno, N., Kasuga, M., Meguid, M. M., Miyazaki, J-i., Ninomiya, M., Herzog, H., Fujimiya, M. Gastrointestinal hormones (anorexigenic peptide YY and orexigenic ghrelin) influence neural tube development.

Key Words: neural tube defect • transgenic mice • gut hormone