Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs
The circadian rhythm is one of the most general and important rhythms in biological organisms. In this study, continuous 24-h video recordings showed that the cumulative movement distance and duration of the abalone, Haliotis discus hannai, reached their maximum values between 20:00–00:00, but both...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-01-01
|
| Series: | Computational and Structural Biotechnology Journal |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2001037022001921 |
| _version_ | 1797978226541199360 |
|---|---|
| author | Xiaolong Gao Mo Zhang Mingxin Lyu Shihui Lin Xuan Luo Weiwei You Caihuan Ke |
| author_facet | Xiaolong Gao Mo Zhang Mingxin Lyu Shihui Lin Xuan Luo Weiwei You Caihuan Ke |
| author_sort | Xiaolong Gao |
| collection | DOAJ |
| description | The circadian rhythm is one of the most general and important rhythms in biological organisms. In this study, continuous 24-h video recordings showed that the cumulative movement distance and duration of the abalone, Haliotis discus hannai, reached their maximum values between 20:00–00:00, but both were significantly lower between 08:00–12:00 than at any other time of day or night (P < 0.05). To investigate the causes of these diel differences in abalone movement behavior, their cerebral ganglia were harvested at 00:00 (group D) and 12:00 (group L) to screen for differentially expressed proteins using tandem mass tagging (TMT) quantitative proteomics. Seventy-five significantly different proteins were identified in group D vs. group L. The differences in acetylcholinesterase (AchE) expression levels between day- and nighttime and the key role in the cholinergic nervous system received particular attention during the investigation. A cosine rhythm analysis found that the concentration of acetylcholine (Ach) and the expression levels of AchE tended to be low during the day and high at night, and high during the day and low at night, respectively. However, the rhythmicity of the diel expression levels of acetylcholine receptor (nAchR) appeared to be insignificant (P > 0.05). Following the injection of three different concentrations of neostigmine methylsulfate, as an AchE inhibitor, the concentration of Ach in the hemolymph, and the expression levels of nAchR in the cerebral ganglia increased significantly (P < 0.05). Four hours after drug injection, the cumulative movement distance and duration of abalones were significantly higher than those in the uninjected control group, and the group injected with saline (P < 0.05). The expression levels of the core diurnal clock Bmal1 over a 24-h period also tended to be high during the day and low at night. First, a co-immunoprecipitation assay demonstrated the binding between Bmal1 and AchE or nAchR. A dual-luciferase gene test and electrophoretic mobility shift assay showed that Bmal1 bound to the promoter regions of AchE and nAchR. Twenty-four hours after silencing the Bmal1 gene, the expression levels of AchE and nAchR decreased significantly compared to those of the dsEGFP and PBS control groups, further showing that Bmal1 mediates the cholinergic system to regulate the behavioral rhythm of abalone. These findings shed light on the endocrine mechanism regulating the rhythmic behavior of abalone, and provide a reference for understanding the life history adaptation strategies of nocturnal organisms and the proliferation and protection of bottom dwelling economically important organisms. |
| first_indexed | 2024-04-11T05:19:37Z |
| format | Article |
| id | doaj.art-853128ea78774e7d85527ea3ac061780 |
| institution | Directory Open Access Journal |
| issn | 2001-0370 |
| language | English |
| last_indexed | 2024-04-11T05:19:37Z |
| publishDate | 2022-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Computational and Structural Biotechnology Journal |
| spelling | doaj.art-853128ea78774e7d85527ea3ac0617802022-12-24T04:52:37ZengElsevierComputational and Structural Biotechnology Journal2001-03702022-01-012028152830Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscsXiaolong Gao0Mo Zhang1Mingxin Lyu2Shihui Lin3Xuan Luo4Weiwei You5Caihuan Ke6State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China; Fujian Key Laboratory of Genetics and Breeding of Marine Organisms, Xiamen University, Xiamen, China; Corresponding author.The circadian rhythm is one of the most general and important rhythms in biological organisms. In this study, continuous 24-h video recordings showed that the cumulative movement distance and duration of the abalone, Haliotis discus hannai, reached their maximum values between 20:00–00:00, but both were significantly lower between 08:00–12:00 than at any other time of day or night (P < 0.05). To investigate the causes of these diel differences in abalone movement behavior, their cerebral ganglia were harvested at 00:00 (group D) and 12:00 (group L) to screen for differentially expressed proteins using tandem mass tagging (TMT) quantitative proteomics. Seventy-five significantly different proteins were identified in group D vs. group L. The differences in acetylcholinesterase (AchE) expression levels between day- and nighttime and the key role in the cholinergic nervous system received particular attention during the investigation. A cosine rhythm analysis found that the concentration of acetylcholine (Ach) and the expression levels of AchE tended to be low during the day and high at night, and high during the day and low at night, respectively. However, the rhythmicity of the diel expression levels of acetylcholine receptor (nAchR) appeared to be insignificant (P > 0.05). Following the injection of three different concentrations of neostigmine methylsulfate, as an AchE inhibitor, the concentration of Ach in the hemolymph, and the expression levels of nAchR in the cerebral ganglia increased significantly (P < 0.05). Four hours after drug injection, the cumulative movement distance and duration of abalones were significantly higher than those in the uninjected control group, and the group injected with saline (P < 0.05). The expression levels of the core diurnal clock Bmal1 over a 24-h period also tended to be high during the day and low at night. First, a co-immunoprecipitation assay demonstrated the binding between Bmal1 and AchE or nAchR. A dual-luciferase gene test and electrophoretic mobility shift assay showed that Bmal1 bound to the promoter regions of AchE and nAchR. Twenty-four hours after silencing the Bmal1 gene, the expression levels of AchE and nAchR decreased significantly compared to those of the dsEGFP and PBS control groups, further showing that Bmal1 mediates the cholinergic system to regulate the behavioral rhythm of abalone. These findings shed light on the endocrine mechanism regulating the rhythmic behavior of abalone, and provide a reference for understanding the life history adaptation strategies of nocturnal organisms and the proliferation and protection of bottom dwelling economically important organisms.http://www.sciencedirect.com/science/article/pii/S2001037022001921Haliotis discus hannaiMovement behaviourCholinergic systemAchE inhibitorBmal1 |
| spellingShingle | Xiaolong Gao Mo Zhang Mingxin Lyu Shihui Lin Xuan Luo Weiwei You Caihuan Ke Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs Computational and Structural Biotechnology Journal Haliotis discus hannai Movement behaviour Cholinergic system AchE inhibitor Bmal1 |
| title | Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| title_full | Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| title_fullStr | Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| title_full_unstemmed | Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| title_short | Role of Bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| title_sort | role of bmal1 in mediating the cholinergic system to regulate the behavioral rhythm of nocturnal marine molluscs |
| topic | Haliotis discus hannai Movement behaviour Cholinergic system AchE inhibitor Bmal1 |
| url | http://www.sciencedirect.com/science/article/pii/S2001037022001921 |
| work_keys_str_mv | AT xiaolonggao roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT mozhang roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT mingxinlyu roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT shihuilin roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT xuanluo roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT weiweiyou roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs AT caihuanke roleofbmal1inmediatingthecholinergicsystemtoregulatethebehavioralrhythmofnocturnalmarinemolluscs |