High-fat diet in early life triggers both reversible and persistent epigenetic changes in the medaka fish (Oryzias latipes)

The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during thi...

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Published inBMC genomics Vol. 24; no. 1; pp. 472 - 19
Main Authors Inoue, Yusuke, Suzuki, Yuta, Kunishima, Yoshimi, Washio, Terumi, Morishita, Shinichi, Takeda, Hiroyuki
Format Journal Article
LanguageEnglish
Published England BioMed Central Ltd 21.08.2023
BioMed Central
BMC
Subjects
Analysis
Animals
Cell signaling
Chromatin
Chromatin accessibility
Developmental stages
Diabetes
Diet
Diet, High-Fat
DNA methylation
Epigenesis, Genetic
Epigenetic inheritance
Epigenetics
Fatty liver
Fertilization
Fetuses
Fibrosis
Gastrointestinal surgery
Gene expression
Gene Expression Regulation, Developmental
Genes
Genetic Loci
Genomes
Genomics
Hatching
Health aspects
Hepatocellular carcinoma
Hepatocytes
High fat diet
Histone modifications
Histones
Larvae
Lipids
Liver
Liver cancer
Liver diseases
Long-term effects
Mammals
Medaka
Metabolism
Nutrients
Nutrition
Nutritional programming
Nutritional status
Oryzias - genetics
Oryzias - growth & development
Physiological aspects
Steatosis
Transcriptomes
Transcriptomics
Type 2 diabetes
Vertebrates
Japan
Medaka
Chromatin accessibility
Histone modifications
Fatty liver
Nutritional programming
High-fat diet
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Abstract The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems. In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding. In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
AbstractList The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems. In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding. In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems. In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding. In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
BackgroundThe nutritional status during early life can have enduring effects on an animal’s metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems.ResultsIn this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding.ConclusionIn summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems.BACKGROUNDThe nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems.In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding.RESULTSIn this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding.In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.CONCLUSIONIn summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
Background The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems. Results In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding. Conclusion In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates. Keywords: Nutritional programming, High-fat diet, Fatty liver, Chromatin accessibility, Histone modifications, Medaka
Abstract Background The nutritional status during early life can have enduring effects on an animal’s metabolism, although the mechanisms underlying these long-term effects are still unclear. Epigenetic modifications are considered a prime candidate mechanism for encoding early-life nutritional memories during this critical developmental period. However, the extent to which these epigenetic changes occur and persist over time remains uncertain, in part due to challenges associated with directly stimulating the fetus with specific nutrients in viviparous mammalian systems. Results In this study, we used medaka as an oviparous vertebrate model to establish an early-life high-fat diet (HFD) model. Larvae were fed with HFD from the hatching stages (one week after fertilization) for six weeks, followed by normal chow (NC) for eight weeks until the adult stage. We examined the changes in the transcriptomic and epigenetic state of the liver over this period. We found that HFD induces simple liver steatosis, accompanied by drastic changes in the hepatic transcriptome, chromatin accessibility, and histone modifications, especially in metabolic genes. These changes were largely reversed after the long-term NC, demonstrating the high plasticity of the epigenetic state in hepatocytes. However, we found a certain number of genomic loci showing non-reversible epigenetic changes, especially around genes related to cell signaling, liver fibrosis, and hepatocellular carcinoma, implying persistent changes in the cellular state of the liver triggered by early-life HFD feeding. Conclusion In summary, our data show that early-life HFD feeding triggers both reversible and persistent epigenetic changes in medaka hepatocytes. Our data provide novel insights into the epigenetic mechanism of nutritional programming and a comprehensive atlas of the long-term epigenetic state in an early-life HFD model of non-mammalian vertebrates.
ArticleNumber 472
Audience Academic
Author Kunishima, Yoshimi
Morishita, Shinichi
Inoue, Yusuke
Suzuki, Yuta
Washio, Terumi
Takeda, Hiroyuki
Author_xml – sequence: 1
  givenname: Yusuke
  surname: Inoue
  fullname: Inoue, Yusuke
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  givenname: Yuta
  surname: Suzuki
  fullname: Suzuki, Yuta
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  givenname: Yoshimi
  surname: Kunishima
  fullname: Kunishima, Yoshimi
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  givenname: Terumi
  surname: Washio
  fullname: Washio, Terumi
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  surname: Morishita
  fullname: Morishita, Shinichi
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  givenname: Hiroyuki
  surname: Takeda
  fullname: Takeda, Hiroyuki
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37605229$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Medaka
Chromatin accessibility
Histone modifications
Fatty liver
Nutritional programming
High-fat diet
Language English
License 2023. BioMed Central Ltd., part of Springer Nature.
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  publication-title: Nature
  doi: 10.1038/nature24271
– volume: 10
  start-page: 2490
  year: 2019
  ident: 9557_CR80
  publication-title: Front Immunol
  doi: 10.3389/fimmu.2019.02490
– volume: 14
  start-page: 4217
  year: 2021
  ident: 9557_CR75
  publication-title: J Inflamm Res
  doi: 10.2147/JIR.S324336
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Snippet The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term effects are...
Background The nutritional status during early life can have enduring effects on an animal's metabolism, although the mechanisms underlying these long-term...
BackgroundThe nutritional status during early life can have enduring effects on an animal’s metabolism, although the mechanisms underlying these long-term...
Abstract Background The nutritional status during early life can have enduring effects on an animal’s metabolism, although the mechanisms underlying these...
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SubjectTerms Analysis
Animals
Cell signaling
Chromatin
Chromatin accessibility
Developmental stages
Diabetes
Diet
Diet, High-Fat
DNA methylation
Epigenesis, Genetic
Epigenetic inheritance
Epigenetics
Fatty liver
Fertilization
Fetuses
Fibrosis
Gastrointestinal surgery
Gene expression
Gene Expression Regulation, Developmental
Genes
Genetic Loci
Genomes
Genomics
Hatching
Health aspects
Hepatocellular carcinoma
Hepatocytes
High fat diet
Histone modifications
Histones
Larvae
Lipids
Liver
Liver cancer
Liver diseases
Long-term effects
Mammals
Medaka
Metabolism
Nutrients
Nutrition
Nutritional programming
Nutritional status
Oryzias - genetics
Oryzias - growth & development
Physiological aspects
Steatosis
Transcriptomes
Transcriptomics
Type 2 diabetes
Vertebrates
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Title High-fat diet in early life triggers both reversible and persistent epigenetic changes in the medaka fish (Oryzias latipes)
URI https://www.ncbi.nlm.nih.gov/pubmed/37605229
https://www.proquest.com/docview/2865361658
https://www.proquest.com/docview/2854967138
https://pubmed.ncbi.nlm.nih.gov/PMC10441761
https://doaj.org/article/ba5d2832bc5c47b4bed188ff848760be
Volume 24
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