Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori.
Our previous study demonstrated that predominant feeding inhibitory effects were found in the crude extracts of foregut and midgut of the silkworm Bombyx mori larvae. To address the entero-intestinal control crucial for the regulation of insect feeding behavior, the present study identified and func...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0219050 |
| _version_ | 1819148328915435520 |
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| author | Sumihiro Matsumoto Natsumaro Kutsuna Ivana Daubnerová Ladislav Roller Dušan Žitňan Hiromichi Nagasawa Shinji Nagata |
| author_facet | Sumihiro Matsumoto Natsumaro Kutsuna Ivana Daubnerová Ladislav Roller Dušan Žitňan Hiromichi Nagasawa Shinji Nagata |
| author_sort | Sumihiro Matsumoto |
| collection | DOAJ |
| description | Our previous study demonstrated that predominant feeding inhibitory effects were found in the crude extracts of foregut and midgut of the silkworm Bombyx mori larvae. To address the entero-intestinal control crucial for the regulation of insect feeding behavior, the present study identified and functionally characterized feeding inhibitory peptides from the midgut of B. mori larvae. Purification and structural analyses revealed that the predominant inhibitory factors in the crude extracts were allatotropin (AT) and GSRYamide after its C-terminal sequence. In situ hybridization revealed that AT and GSRYamide were expressed in enteroendocrine cells in the posterior and anterior midgut, respectively. Receptor screening using Ca2+-imaging technique showed that the B. mori neuropeptide G protein-coupled receptor (BNGR)-A19 and -A22 acted as GSRYamide receptors and BNGR-A5 acted as an additional AT receptor. Expression analyses of these receptors and the results of the peristaltic motion assay indicated that these peptides participated in the regulation of intestinal contraction. Exposure of pharynx and ileum to AT and GSRYamide inhibited spontaneous contraction in ad libitum-fed larvae, while exposure of pharynx to GSRYamide did not inhibit contraction in non-fed larvae, indicating that the feeding state changed their sensitivity to inhibitory peptides. These different responses corresponded to different expression levels of their receptors in the pharynx. In addition, injection of AT and GSRYamide decreased esophageal contraction frequencies in the melamine-treated transparent larvae. These findings strongly suggest that these peptides exert feeding inhibitory effects by modulating intestinal contraction in response to their feeding state transition, eventually causing feeding termination. |
| first_indexed | 2024-12-22T13:43:59Z |
| format | Article |
| id | doaj.art-89dec09305094f9cba26ca84d2c53e74 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-22T13:43:59Z |
| publishDate | 2019-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-89dec09305094f9cba26ca84d2c53e742022-12-21T18:23:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-01147e021905010.1371/journal.pone.0219050Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori.Sumihiro MatsumotoNatsumaro KutsunaIvana DaubnerováLadislav RollerDušan ŽitňanHiromichi NagasawaShinji NagataOur previous study demonstrated that predominant feeding inhibitory effects were found in the crude extracts of foregut and midgut of the silkworm Bombyx mori larvae. To address the entero-intestinal control crucial for the regulation of insect feeding behavior, the present study identified and functionally characterized feeding inhibitory peptides from the midgut of B. mori larvae. Purification and structural analyses revealed that the predominant inhibitory factors in the crude extracts were allatotropin (AT) and GSRYamide after its C-terminal sequence. In situ hybridization revealed that AT and GSRYamide were expressed in enteroendocrine cells in the posterior and anterior midgut, respectively. Receptor screening using Ca2+-imaging technique showed that the B. mori neuropeptide G protein-coupled receptor (BNGR)-A19 and -A22 acted as GSRYamide receptors and BNGR-A5 acted as an additional AT receptor. Expression analyses of these receptors and the results of the peristaltic motion assay indicated that these peptides participated in the regulation of intestinal contraction. Exposure of pharynx and ileum to AT and GSRYamide inhibited spontaneous contraction in ad libitum-fed larvae, while exposure of pharynx to GSRYamide did not inhibit contraction in non-fed larvae, indicating that the feeding state changed their sensitivity to inhibitory peptides. These different responses corresponded to different expression levels of their receptors in the pharynx. In addition, injection of AT and GSRYamide decreased esophageal contraction frequencies in the melamine-treated transparent larvae. These findings strongly suggest that these peptides exert feeding inhibitory effects by modulating intestinal contraction in response to their feeding state transition, eventually causing feeding termination.https://doi.org/10.1371/journal.pone.0219050 |
| spellingShingle | Sumihiro Matsumoto Natsumaro Kutsuna Ivana Daubnerová Ladislav Roller Dušan Žitňan Hiromichi Nagasawa Shinji Nagata Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. PLoS ONE |
| title | Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. |
| title_full | Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. |
| title_fullStr | Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. |
| title_full_unstemmed | Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. |
| title_short | Enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm Bombyx mori. |
| title_sort | enteroendocrine peptides regulate feeding behavior via controlling intestinal contraction of the silkworm bombyx mori |
| url | https://doi.org/10.1371/journal.pone.0219050 |
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