Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression

Abstract Background SIRT1 histone deacetylase acts on many epigenetic and non-epigenetic targets. It is thought that SIRT1 is involved in oocyte maturation; therefore, the importance of the ooplasmic SIRT1 pool for the further fate of mature oocytes has been strongly suggested. We hypothesised that...

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Main Authors: Jan Nevoral, Lukas Landsmann, Miriam Stiavnicka, Petr Hosek, Jiri Moravec, Sarka Prokesova, Hedvika Rimnacova, Eliska Koutna, Pavel Klein, Kristyna Hoskova, Tereza Zalmanova, Tereza Fenclova, Jaroslav Petr, Milena Kralickova
Format: Article
Language:English
Published: BMC 2019-08-01
Series:Journal of Animal Science and Biotechnology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40104-019-0372-3
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author Jan Nevoral
Lukas Landsmann
Miriam Stiavnicka
Petr Hosek
Jiri Moravec
Sarka Prokesova
Hedvika Rimnacova
Eliska Koutna
Pavel Klein
Kristyna Hoskova
Tereza Zalmanova
Tereza Fenclova
Jaroslav Petr
Milena Kralickova
author_facet Jan Nevoral
Lukas Landsmann
Miriam Stiavnicka
Petr Hosek
Jiri Moravec
Sarka Prokesova
Hedvika Rimnacova
Eliska Koutna
Pavel Klein
Kristyna Hoskova
Tereza Zalmanova
Tereza Fenclova
Jaroslav Petr
Milena Kralickova
author_sort Jan Nevoral
collection DOAJ
description Abstract Background SIRT1 histone deacetylase acts on many epigenetic and non-epigenetic targets. It is thought that SIRT1 is involved in oocyte maturation; therefore, the importance of the ooplasmic SIRT1 pool for the further fate of mature oocytes has been strongly suggested. We hypothesised that SIRT1 plays the role of a signalling molecule in mature oocytes through selected epigenetic and non-epigenetic regulation. Results We observed SIRT1 re-localisation in mature oocytes and its association with spindle microtubules. In mature oocytes, SIRT1 distribution shows a spindle-like pattern, and spindle-specific SIRT1 action decreases α-tubulin acetylation. Based on the observation of the histone code in immature and mature oocytes, we suggest that SIRT1 is mostly predestined for an epigenetic mode of action in the germinal vesicles (GVs) of immature oocytes. Accordingly, BML-278-driven trimethylation of lysine K9 in histone H3 in mature oocytes is considered to be a result of GV epigenetic transformation. Conclusions Taken together, our observations point out the dual spatiotemporal SIRT1 action in oocytes, which can be readily switched from the epigenetic to non-epigenetic mode of action depending on the progress of meiosis.
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spelling doaj.art-0e230c035bf14471bca8b2c951c9c4852022-12-21T23:52:41ZengBMCJournal of Animal Science and Biotechnology2049-18912019-08-0110111210.1186/s40104-019-0372-3Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progressionJan Nevoral0Lukas Landsmann1Miriam Stiavnicka2Petr Hosek3Jiri Moravec4Sarka Prokesova5Hedvika Rimnacova6Eliska Koutna7Pavel Klein8Kristyna Hoskova9Tereza Zalmanova10Tereza Fenclova11Jaroslav Petr12Milena Kralickova13Biomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityInstitute of Animal ScienceInstitute of Animal ScienceBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityInstitute of Animal ScienceBiomedical Center, Faculty of Medicine in Pilsen, Charles UniversityAbstract Background SIRT1 histone deacetylase acts on many epigenetic and non-epigenetic targets. It is thought that SIRT1 is involved in oocyte maturation; therefore, the importance of the ooplasmic SIRT1 pool for the further fate of mature oocytes has been strongly suggested. We hypothesised that SIRT1 plays the role of a signalling molecule in mature oocytes through selected epigenetic and non-epigenetic regulation. Results We observed SIRT1 re-localisation in mature oocytes and its association with spindle microtubules. In mature oocytes, SIRT1 distribution shows a spindle-like pattern, and spindle-specific SIRT1 action decreases α-tubulin acetylation. Based on the observation of the histone code in immature and mature oocytes, we suggest that SIRT1 is mostly predestined for an epigenetic mode of action in the germinal vesicles (GVs) of immature oocytes. Accordingly, BML-278-driven trimethylation of lysine K9 in histone H3 in mature oocytes is considered to be a result of GV epigenetic transformation. Conclusions Taken together, our observations point out the dual spatiotemporal SIRT1 action in oocytes, which can be readily switched from the epigenetic to non-epigenetic mode of action depending on the progress of meiosis.http://link.springer.com/article/10.1186/s40104-019-0372-3EpigeneticsHistone codeIn vitro maturationOocyteSIRT1Sirtuin 1
spellingShingle Jan Nevoral
Lukas Landsmann
Miriam Stiavnicka
Petr Hosek
Jiri Moravec
Sarka Prokesova
Hedvika Rimnacova
Eliska Koutna
Pavel Klein
Kristyna Hoskova
Tereza Zalmanova
Tereza Fenclova
Jaroslav Petr
Milena Kralickova
Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
Journal of Animal Science and Biotechnology
Epigenetics
Histone code
In vitro maturation
Oocyte
SIRT1
Sirtuin 1
title Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
title_full Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
title_fullStr Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
title_full_unstemmed Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
title_short Epigenetic and non-epigenetic mode of SIRT1 action during oocyte meiosis progression
title_sort epigenetic and non epigenetic mode of sirt1 action during oocyte meiosis progression
topic Epigenetics
Histone code
In vitro maturation
Oocyte
SIRT1
Sirtuin 1
url http://link.springer.com/article/10.1186/s40104-019-0372-3
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