Glycolytic regulation in aestivation of the sea cucumber Apostichopus japonicus: evidence from metabolite quantification and rate-limiting enzyme analyses

Xiang, Xiaowei; Chen, Muyan; Wu, Changwen; Zhu, Aiyi; Yang, Jingwen; Lv, Zhenming; Wang, Tianming

doi:10.1007/s00227-016-2936-5

Cited by 14 publications

(5 citation statements)

References 43 publications

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“…As reported previously, strong depression of the metabolic rate is a vital adaptive strategy targeting the energy budget during hypometabolism; hence, a decline in catabolism usually occurs during estivation (Storey and Storey, 1990;Storey and Storey, 2010). In this study, obvious decreases in the contents of carbohydrates and lipids were found in the DA group, consistent with previous results in A. japonicus during estivation (Xiang et al, 2016;Yang et al, 2021), suggesting that some necessary controls might be implemented for energy reorganization during dormancy.…”

Section: Lc-ms Metabolomic Profilessupporting

confidence: 91%

“…For A. japonicus, similar depression of glycolytic rates also occurs in the hypometabolic state. Xiang et al (2016) found significant decreases in glucose and pyruvic acid concentrations in the intestines of estivating A. japonicus, along with reduced enzymatic activity and transcription levels of the rate-limiting enzyme hexokinase. In our study, the levels of the glycolysis precursor or the intermediate metabolites D-galactose, fructose 1,6-bisphosphate, and D-glyceraldehyde 3-phosphate were all significantly decreased in the DA group in comparison with the NA and AA groups, verifying that profound glycolytic suppression occurred in estivating A. japonicus.…”

Section: Glycolysis Tca Cycle and Pentose Phosphate Pathwaymentioning

confidence: 90%

“…Since A. japonicus is one of the most important economic species that is widely cultured in Asia, mainly due to its high nutritional and pharmaceutical value, estivation obviously shortens the growth cycle and drives down the production efficiency in the sea cucumber aquaculture industry (Yuan et al, 2007a). Recently, accumulating studies have focused on the physiological and biochemical strategies of sea cucumber in dealing with estivation, including metabolic rate depression (Yang et al, 2006;Xiang et al, 2016), energetic reorganization (Yuan et al, 2007b), and degeneration of intestinal structure and function (Gao et al, 2008). With the rapid development of omics technology, the molecular regulation mechanisms underpinning estivation have been further elucidated, mainly focusing on global transcriptional and translational regulation (Zhao et al, 2014;Chen et al, 2016a;Li et al, 2018), miRNA-targeted posttranscriptional modifications (Chen et al, 2013;Chen et al, 2018), reversible protein phosphorylation (Chen et al, 2016b) and epigenetic modifications (Zhao et al, 2015;Yang et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Metabolic response of the sea cucumber Apostichopus japonicus during the estivation-arousal cycles

Zhao

Wang

et al. 2022

Front. Mar. Sci.

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Estivation is a widespread survival strategy for dealing with adverse environmental conditions such as high temperature, low oxygen and lack of water or food, which has been reported across multiple vertebrate and invertebrate species. The sea cucumber Apostichopus japonicus is an excellent model organism to investigate the adaptive mechanism of estivation in marine invertebrates. In this study, a metabolomics approach based on ultraperformance liquid chromatography coupled with electrospray ionization time-of-flight mass spectrometry (UPLC-ESI-Q-TOF/MS) was performed to reveal the metabolic response of intestines from adult A. japonicus over the annual estivation-arousal cycle: nonestivation (NA), deep-estivation (DA) and arousal from estivation (AA). A total of 424 metabolites were identified, and among them, 243, 238 and 37 significant differentially metabolites (DMs) were further screened in the comparisons of DA vs. NA, AA vs. DA, and AA vs. NA. Specifically, the levels of metabolites involved in glycolysis and the tricarboxylic acid cycle were significantly decreased, while higher amounts of long-chain fatty acids, phospholipids and free amino acids were found in A. japonicus during estivation, implying that sea cucumbers might reorganize metabolic priorities for ATP production by depressing carbohydrate metabolism and promoting lipid and amino acid catabolism. Interestingly, elevated relative carbon flow entry into the pentose phosphate pathway and accumulation of various nonenzymatic antioxidant molecules (e.g., tocotrienols, folic acid, catechin, genistein and resveratrol) were observed in estivating sea cucumbers, which suggested that enhancement of the reactive oxygen species defense system might promote long-term viability in the hypometabolic state in an energy-efficient manner. Thus, this research provides new insights into the adaptation mechanisms of marine invertebrates to estivation at the metabolic level.

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Section: Lc-ms Metabolomic Profilessupporting

confidence: 91%

Section: Glycolysis Tca Cycle and Pentose Phosphate Pathwaymentioning

confidence: 90%

Section: Introductionmentioning

confidence: 99%

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Metabolic response of the sea cucumber Apostichopus japonicus during the estivation-arousal cycles

Zhao

Wang

et al. 2022

Front. Mar. Sci.

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“…For qRT-PCR, β-actin (ACTB) and β-tubulin (TUBB) were chosen as the internal control (housekeeping) genes and gene-specific primers were designed based on the ORF sequences6364. Specific qRT-PCR primers for Aj5-HT4R and AjPFK were designed based on CDS (Table 1).…”

Section: Methodsmentioning

confidence: 99%

Identification and functional characterisation of 5-HT4 receptor in sea cucumber Apostichopus japonicus (Selenka)

Wang

Yang

Zhou

et al. 2017

Sci Rep

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Serotonin (5-HT) is an important neurotransmitter and neuromodulator that controls a variety of sensory and motor functions through 5-HT receptors (5-HTRs). The 5-HT4R subfamily is linked to Gs proteins, which activate adenylyl cyclases (ACs), and is involved in many responses in peripheral organs. In this study, the 5-HT4R from Apostichopus japonicus (Aj5-HT4R) was identified and characterised. The cloned full-length Aj5-HT4R cDNA is 1,544 bp long and contains an open reading frame 1,011 bp in length encoding 336 amino acid proteins. Bioinformatics analysis of the Aj5-HT4R protein indicated this receptor was a member of class A G protein coupled receptor (GPCR) family. Further experiments using Aj5-HT4R-transfected HEK293 cells demonstrated that treatment with 5-HT triggered a significant increase in intracellular cAMP level in a dose-dependent manner and induced a rapid internalisation of Aj5-HT4R fused with enhanced green fluorescent protein (Aj5-HT4R-EGFP) from the cell surface into the cytoplasm. In addition, the transcriptional profiles of Aj5-HT4R in aestivating A. japonicas and phosphofructokinase (AjPFK) in 5-HT administrated A. japonicus have been analysed by real-time PCR assays. Results have led to a basic understanding of Aj5-HT4R in A. japonicus, and provide a foundation for further exploration of the cell signaling and regulatory functions of this receptor.

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“…In terms of the physiological and metabolic characteristics of A. japonicus during aestivation, Yang et al studied their oxygen consumption rate (OCR) and ammonia excretion rate (AER) under laboratory conditions, demonstrating that mature sea cucumber individuals have a peak OCR and AER at 20 °C, which subsequently decrease after entering aestivation [ 135 ]. Xiang et al quantitatively analyzed the activity and metabolites of two rate-limiting enzymes, hexokinase (Aj-HK) and pyruvate kinase (Aj-PK), to verify the inhibition of the glycolytic pathway in the intestine of aestivating A. japonicus and showed that transcriptional and post-transcriptional modifications might play a role in regulating glycolytic inhibition [ 136 ]. Furthermore, Xu et al identified the distribution of fatty acids (FAs) in aestivating A. japonicus and discovered that FAs may be synthesized from heterotrophic bacteria during early aestivation stages, and the sea cucumber may digest long-chain FAs such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) from intestinal degradation during deep aestivation stages [ 137 ].…”

Section: Characteristics and Research Progress Of Invertebrate Aestiv...mentioning

confidence: 99%

Aestivation in Nature: Physiological Strategies and Evolutionary Adaptations in Hypometabolic States

Jiang,

Storey,

Yang

et al. 2023

IJMS

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Aestivation is considered to be one of the “purest” hypometabolic states in nature, as it involves aerobic dormancy that can be induced and sustained without complex factors. Animals that undergo aestivation to protect themselves from environmental stressors such as high temperatures, droughts, and food shortages. However, this shift in body metabolism presents new challenges for survival, including oxidative stress upon awakening from aestivation, accumulation of toxic metabolites, changes in energy sources, adjustments to immune status, muscle atrophy due to prolonged immobility, and degeneration of internal organs due to prolonged food deprivation. In this review, we summarize the physiological and metabolic strategies, key regulatory factors, and networks utilized by aestivating animals to address the aforementioned components of aestivation. Furthermore, we present a comprehensive overview of the advancements made in aestivation research across major species, including amphibians, fish, reptiles, annelids, mollusks, and echinoderms, categorized according to their respective evolutionary positions. This approach offers a distinct perspective for comparative analysis, facilitating an understanding of the shared traits and unique features of aestivation across different groups of organisms.

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Glycolytic regulation in aestivation of the sea cucumber Apostichopus japonicus: evidence from metabolite quantification and rate-limiting enzyme analyses

Cited by 14 publications

References 43 publications

Metabolic response of the sea cucumber Apostichopus japonicus during the estivation-arousal cycles

Metabolic response of the sea cucumber Apostichopus japonicus during the estivation-arousal cycles

Identification and functional characterisation of 5-HT4 receptor in sea cucumber Apostichopus japonicus (Selenka)

Aestivation in Nature: Physiological Strategies and Evolutionary Adaptations in Hypometabolic States

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