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Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole
The American bullfrog (Lithobates catesbeianus) is a eurythermal amphibian that is naturally distributed from subarctic to subtropical areas. The tadpoles of this species overwinter, in water, in cold environments. Therefore, they may have adapted to a wide range of temperatures in an active state....
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Published in: | Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2019-04, Vol.230, p.39-48 |
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description | The American bullfrog (Lithobates catesbeianus) is a eurythermal amphibian that is naturally distributed from subarctic to subtropical areas. The tadpoles of this species overwinter, in water, in cold environments. Therefore, they may have adapted to a wide range of temperatures in an active state. To understand the adaptation mechanisms to cope with low or high temperatures, we investigated global epigenetic modifications, histone variants, transcript levels of related genes, and the cellular acetyl coenzyme A (acetyl-CoA) and free CoA (CoA-SH) levels, in the livers of tadpoles collected in summer and winter and of those acclimated to 4 °C and 21 °C. Among epigenetic marks tested, the levels of acetylated histones and the histone variant H2A.Z were influenced by different temperature conditions. Histone acetylation levels were higher in summer than in winter and increased within 3 days of warm acclimation, whereas histone H2A.Z levels were higher in winter than in summer and decreased within 2 weeks of warm acclimation. Transcript analysis revealed that decreased expression of histone H2A.Z in warm acclimation was regulated at the transcriptional level. Acetyl-CoA levels were not correlated with those of the acetylated histones, indicating that cellular acetyl-CoA levels may not directly influence the state of histone acetylation in the tadpole liver. Such epigenetic and metabolic changes in the tadpole liver may contribute to the maintenance of energy balance during seasonal acclimatization and thermal acclimation.
•Histone acetylation and variant levels changed in response to seasonal acclimatization and thermal acclimation.•Histone acetylation levels changed within 3 days of acclimation, not through transcriptional control.•Histone H2A.Z levels changed within 2 weeks of acclimation through transcriptional activation.•Cellular acetyl-CoA content or ratio of acetyl-CoA to CoA-SH was not correlated with the amounts of acetylated histones. |
doi_str_mv | 10.1016/j.cbpa.2018.12.014 |
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•Histone acetylation and variant levels changed in response to seasonal acclimatization and thermal acclimation.•Histone acetylation levels changed within 3 days of acclimation, not through transcriptional control.•Histone H2A.Z levels changed within 2 weeks of acclimation through transcriptional activation.•Cellular acetyl-CoA content or ratio of acetyl-CoA to CoA-SH was not correlated with the amounts of acetylated histones.</description><identifier>ISSN: 1095-6433</identifier><identifier>EISSN: 1531-4332</identifier><identifier>DOI: 10.1016/j.cbpa.2018.12.014</identifier><identifier>PMID: 30590112</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acclimation ; Acclimatization ; Acetylation ; Animals ; Epigenesis, Genetic ; Gene expression ; Histone ; Histones - metabolism ; Larva - metabolism ; Liver - metabolism ; Rana catesbeiana - genetics ; Rana catesbeiana - growth & development ; Rana catesbeiana - physiology ; Seasons ; Temperature ; Transcriptional Activation ; Variant</subject><ispartof>Comparative biochemistry and physiology. Part A, Molecular & integrative physiology, 2019-04, Vol.230, p.39-48</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c466t-35e2610a1773238d8a5d9fe4a0bb3167c725c6c12efed27058560a02e88ba37c3</citedby><cites>FETCH-LOGICAL-c466t-35e2610a1773238d8a5d9fe4a0bb3167c725c6c12efed27058560a02e88ba37c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30590112$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ishihara, Akinori</creatorcontrib><creatorcontrib>Sapon, Mohammad Ashrafuzzaman</creatorcontrib><creatorcontrib>Yamauchi, Kiyoshi</creatorcontrib><title>Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole</title><title>Comparative biochemistry and physiology. Part A, Molecular & integrative physiology</title><addtitle>Comp Biochem Physiol A Mol Integr Physiol</addtitle><description>The American bullfrog (Lithobates catesbeianus) is a eurythermal amphibian that is naturally distributed from subarctic to subtropical areas. The tadpoles of this species overwinter, in water, in cold environments. Therefore, they may have adapted to a wide range of temperatures in an active state. To understand the adaptation mechanisms to cope with low or high temperatures, we investigated global epigenetic modifications, histone variants, transcript levels of related genes, and the cellular acetyl coenzyme A (acetyl-CoA) and free CoA (CoA-SH) levels, in the livers of tadpoles collected in summer and winter and of those acclimated to 4 °C and 21 °C. Among epigenetic marks tested, the levels of acetylated histones and the histone variant H2A.Z were influenced by different temperature conditions. Histone acetylation levels were higher in summer than in winter and increased within 3 days of warm acclimation, whereas histone H2A.Z levels were higher in winter than in summer and decreased within 2 weeks of warm acclimation. Transcript analysis revealed that decreased expression of histone H2A.Z in warm acclimation was regulated at the transcriptional level. Acetyl-CoA levels were not correlated with those of the acetylated histones, indicating that cellular acetyl-CoA levels may not directly influence the state of histone acetylation in the tadpole liver. Such epigenetic and metabolic changes in the tadpole liver may contribute to the maintenance of energy balance during seasonal acclimatization and thermal acclimation.
•Histone acetylation and variant levels changed in response to seasonal acclimatization and thermal acclimation.•Histone acetylation levels changed within 3 days of acclimation, not through transcriptional control.•Histone H2A.Z levels changed within 2 weeks of acclimation through transcriptional activation.•Cellular acetyl-CoA content or ratio of acetyl-CoA to CoA-SH was not correlated with the amounts of acetylated histones.</description><subject>Acclimation</subject><subject>Acclimatization</subject><subject>Acetylation</subject><subject>Animals</subject><subject>Epigenesis, Genetic</subject><subject>Gene expression</subject><subject>Histone</subject><subject>Histones - metabolism</subject><subject>Larva - metabolism</subject><subject>Liver - metabolism</subject><subject>Rana catesbeiana - genetics</subject><subject>Rana catesbeiana - growth & development</subject><subject>Rana catesbeiana - physiology</subject><subject>Seasons</subject><subject>Temperature</subject><subject>Transcriptional Activation</subject><subject>Variant</subject><issn>1095-6433</issn><issn>1531-4332</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNp9kc1u1DAUhS0Eoj_wAiyQl2WR4GsnTiKxQRVQpJG6oF1bjnMz45HHDrZTqTxFHxmPpiBWWPLv_c6RfA8h74DVwEB-3NdmXHTNGfQ18JpB84KcQyugaoTgL8uZDW0ly-WMXKS0Z2U00LwmZ4K1AwPg5-TpB-oUvHZUG-PsQWf7q8zgqfYTzTuMh39r5d36aTVIty6MpbKzKQePFBe7RY_ZGmp22m8xFZA6-4CRhpmOq3NzDFt6tbF5V5S5AOa4jmi1X9MHmvW0BIdvyKtZu4Rvn_dLcv_1y931TbW5_fb9-vOmMo2UuRItcglMQ9cJLvqp1-00zNhoNo4CZGc63hppgOOME-9Y27eSacax70ctOiMuydXJd4nh54opq4NNBp3THsOaFAcJchg6LgvKT6iJIaWIs1pi6UZ8VMDUMQm1V8ck1DEJBVyVJIro_bP_Oh5w-iv50_oCfDoBWH75YDGqZCx6g5ONaLKagv2f_2-6o5x_</recordid><startdate>201904</startdate><enddate>201904</enddate><creator>Ishihara, Akinori</creator><creator>Sapon, Mohammad Ashrafuzzaman</creator><creator>Yamauchi, Kiyoshi</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201904</creationdate><title>Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole</title><author>Ishihara, Akinori ; Sapon, Mohammad Ashrafuzzaman ; Yamauchi, Kiyoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c466t-35e2610a1773238d8a5d9fe4a0bb3167c725c6c12efed27058560a02e88ba37c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Acetylation</topic><topic>Animals</topic><topic>Epigenesis, Genetic</topic><topic>Gene expression</topic><topic>Histone</topic><topic>Histones - metabolism</topic><topic>Larva - metabolism</topic><topic>Liver - metabolism</topic><topic>Rana catesbeiana - genetics</topic><topic>Rana catesbeiana - growth & development</topic><topic>Rana catesbeiana - physiology</topic><topic>Seasons</topic><topic>Temperature</topic><topic>Transcriptional Activation</topic><topic>Variant</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ishihara, Akinori</creatorcontrib><creatorcontrib>Sapon, Mohammad Ashrafuzzaman</creatorcontrib><creatorcontrib>Yamauchi, Kiyoshi</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Comparative biochemistry and physiology. Part A, Molecular & integrative physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ishihara, Akinori</au><au>Sapon, Mohammad Ashrafuzzaman</au><au>Yamauchi, Kiyoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole</atitle><jtitle>Comparative biochemistry and physiology. Part A, Molecular & integrative physiology</jtitle><addtitle>Comp Biochem Physiol A Mol Integr Physiol</addtitle><date>2019-04</date><risdate>2019</risdate><volume>230</volume><spage>39</spage><epage>48</epage><pages>39-48</pages><issn>1095-6433</issn><eissn>1531-4332</eissn><abstract>The American bullfrog (Lithobates catesbeianus) is a eurythermal amphibian that is naturally distributed from subarctic to subtropical areas. The tadpoles of this species overwinter, in water, in cold environments. Therefore, they may have adapted to a wide range of temperatures in an active state. To understand the adaptation mechanisms to cope with low or high temperatures, we investigated global epigenetic modifications, histone variants, transcript levels of related genes, and the cellular acetyl coenzyme A (acetyl-CoA) and free CoA (CoA-SH) levels, in the livers of tadpoles collected in summer and winter and of those acclimated to 4 °C and 21 °C. Among epigenetic marks tested, the levels of acetylated histones and the histone variant H2A.Z were influenced by different temperature conditions. Histone acetylation levels were higher in summer than in winter and increased within 3 days of warm acclimation, whereas histone H2A.Z levels were higher in winter than in summer and decreased within 2 weeks of warm acclimation. Transcript analysis revealed that decreased expression of histone H2A.Z in warm acclimation was regulated at the transcriptional level. Acetyl-CoA levels were not correlated with those of the acetylated histones, indicating that cellular acetyl-CoA levels may not directly influence the state of histone acetylation in the tadpole liver. Such epigenetic and metabolic changes in the tadpole liver may contribute to the maintenance of energy balance during seasonal acclimatization and thermal acclimation.
•Histone acetylation and variant levels changed in response to seasonal acclimatization and thermal acclimation.•Histone acetylation levels changed within 3 days of acclimation, not through transcriptional control.•Histone H2A.Z levels changed within 2 weeks of acclimation through transcriptional activation.•Cellular acetyl-CoA content or ratio of acetyl-CoA to CoA-SH was not correlated with the amounts of acetylated histones.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30590112</pmid><doi>10.1016/j.cbpa.2018.12.014</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acclimation Acclimatization Acetylation Animals Epigenesis, Genetic Gene expression Histone Histones - metabolism Larva - metabolism Liver - metabolism Rana catesbeiana - genetics Rana catesbeiana - growth & development Rana catesbeiana - physiology Seasons Temperature Transcriptional Activation Variant |
title | Seasonal acclimatization and thermal acclimation induce global histone epigenetic changes in liver of bullfrog (Lithobates catesbeianus) tadpole |
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