The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus

Melatonin is a highly conserved hormone in evolutionary history. It occurs in numerous organisms and plays a role in the endocrine and immune systems. Locomotor behavior is a basic behavior in animals and is an important indicator of circadian rhythms, which are coordinated by the nervous and endocr...

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Main Authors: Kui Ding, Libin Zhang, Tao Zhang, Hongsheng Yang, Richard Brinkman
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-03-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2019.00221/full
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author Kui Ding
Kui Ding
Kui Ding
Kui Ding
Libin Zhang
Libin Zhang
Libin Zhang
Libin Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Richard Brinkman
spellingShingle Kui Ding
Kui Ding
Kui Ding
Kui Ding
Libin Zhang
Libin Zhang
Libin Zhang
Libin Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Richard Brinkman
The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
Frontiers in Physiology
melatonin
sea cucumber
locomotor behavior
physiological mechanism
fatty acid oxidation
oxidative phosphorylation
author_facet Kui Ding
Kui Ding
Kui Ding
Kui Ding
Libin Zhang
Libin Zhang
Libin Zhang
Libin Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Tao Zhang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Hongsheng Yang
Richard Brinkman
author_sort Kui Ding
title The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
title_short The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
title_full The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
title_fullStr The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
title_full_unstemmed The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicus
title_sort effect of melatonin on locomotor behavior and muscle physiology in the sea cucumber apostichopus japonicus
publisher Frontiers Media S.A.
series Frontiers in Physiology
issn 1664-042X
publishDate 2019-03-01
description Melatonin is a highly conserved hormone in evolutionary history. It occurs in numerous organisms and plays a role in the endocrine and immune systems. Locomotor behavior is a basic behavior in animals and is an important indicator of circadian rhythms, which are coordinated by the nervous and endocrine systems. To date, the effect of melatonin on locomotor behavior has been studied in vertebrates, including syrian hamsters, sparrows, rats, zebrafish, goldfish, and flatworms. However, there have been few studies of the effects of melatonin on locomotor behavior in marine invertebrates. The goals of present study were to show the existence of melatonin in the sea cucumber Apostichopus japonicus and to evaluate its effect on locomotor activity. In addition, muscle tissues from control and melatonin-treated sea cucumbers were tested using ultra performance liquid chromatography and quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF-MS) to determine the changes of metabolic activity in muscle. Melatonin was present in the coelomic fluid of A. japonicus at a concentration of ∼135.0 ng/L. The total distance traveled and number steps taken over 9 h after melatonin administration decreased with increasing concentration of the melatonin dose. Mean and maximum velocity of movement and stride length and stride frequency also decreased, but their differences were not statistically significant. Overall, these results suggest that melatonin administration had a sedative effect on A. japonicus. The levels of 22 different metabolites were altered in the muscle tissues of melatonin-treated sea cucumbers. Serotonin, 9-cis retinoic acid, all-trans retinoic acid, flavin mononucleotide in muscles were downregulated after melatonin administration. Moreover, a high free fatty acid (FFA) concentration and a decrease in the adenosine 5′-triphosphate (ATP) concentration in the muscle tissues of the melatonin-treated group were detected as well. These results suggest that the sedative effect of melatonin involves some other metabolic pathways, and the reduced locomotor modulator—serotonin, inhibited fatty acid oxidation and disturbed oxidative phosphorylation are potential physiological mechanisms that result in the inhibitory effect of melatonin on locomotion in sea cucumbers.
topic melatonin
sea cucumber
locomotor behavior
physiological mechanism
fatty acid oxidation
oxidative phosphorylation
url https://www.frontiersin.org/article/10.3389/fphys.2019.00221/full
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spelling doaj-ab026ffb6b5c4dc9b1475348082f81f02020-11-25T02:56:37ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-03-011010.3389/fphys.2019.00221422978The Effect of Melatonin on Locomotor Behavior and Muscle Physiology in the Sea Cucumber Apostichopus japonicusKui Ding0Kui Ding1Kui Ding2Kui Ding3Libin Zhang4Libin Zhang5Libin Zhang6Libin Zhang7Tao Zhang8Tao Zhang9Tao Zhang10Tao Zhang11Hongsheng Yang12Hongsheng Yang13Hongsheng Yang14Hongsheng Yang15Richard Brinkman16CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaCAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaLaboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaCenter for Ocean Mega-Science, Chinese Academy of Sciences, Qingdao, ChinaAustralian Institute of Marine Science, Townsville, QLD, AustraliaMelatonin is a highly conserved hormone in evolutionary history. It occurs in numerous organisms and plays a role in the endocrine and immune systems. Locomotor behavior is a basic behavior in animals and is an important indicator of circadian rhythms, which are coordinated by the nervous and endocrine systems. To date, the effect of melatonin on locomotor behavior has been studied in vertebrates, including syrian hamsters, sparrows, rats, zebrafish, goldfish, and flatworms. However, there have been few studies of the effects of melatonin on locomotor behavior in marine invertebrates. The goals of present study were to show the existence of melatonin in the sea cucumber Apostichopus japonicus and to evaluate its effect on locomotor activity. In addition, muscle tissues from control and melatonin-treated sea cucumbers were tested using ultra performance liquid chromatography and quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF-MS) to determine the changes of metabolic activity in muscle. Melatonin was present in the coelomic fluid of A. japonicus at a concentration of ∼135.0 ng/L. The total distance traveled and number steps taken over 9 h after melatonin administration decreased with increasing concentration of the melatonin dose. Mean and maximum velocity of movement and stride length and stride frequency also decreased, but their differences were not statistically significant. Overall, these results suggest that melatonin administration had a sedative effect on A. japonicus. The levels of 22 different metabolites were altered in the muscle tissues of melatonin-treated sea cucumbers. Serotonin, 9-cis retinoic acid, all-trans retinoic acid, flavin mononucleotide in muscles were downregulated after melatonin administration. Moreover, a high free fatty acid (FFA) concentration and a decrease in the adenosine 5′-triphosphate (ATP) concentration in the muscle tissues of the melatonin-treated group were detected as well. These results suggest that the sedative effect of melatonin involves some other metabolic pathways, and the reduced locomotor modulator—serotonin, inhibited fatty acid oxidation and disturbed oxidative phosphorylation are potential physiological mechanisms that result in the inhibitory effect of melatonin on locomotion in sea cucumbers.https://www.frontiersin.org/article/10.3389/fphys.2019.00221/fullmelatoninsea cucumberlocomotor behaviorphysiological mechanismfatty acid oxidationoxidative phosphorylation