Cargando…

Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies

Accumulating evidence suggests that transcriptional regulation is required for maintenance of long-term memories (LTMs). Here we characterize global transcriptional and epigenetic changes that occur during LTM storage in the Drosophila mushroom bodies (MBs), structures important for memory. Although...

Descripción completa

Detalles Bibliográficos
Autores principales: Hirano, Yukinori, Ihara, Kunio, Masuda, Tomoko, Yamamoto, Takuya, Iwata, Ikuko, Takahashi, Aya, Awata, Hiroko, Nakamura, Naosuke, Takakura, Mai, Suzuki, Yusuke, Horiuchi, Junjiro, Okuno, Hiroyuki, Saitoe, Minoru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5114576/
https://www.ncbi.nlm.nih.gov/pubmed/27841260
http://dx.doi.org/10.1038/ncomms13471
_version_ 1782468364112756736
author Hirano, Yukinori
Ihara, Kunio
Masuda, Tomoko
Yamamoto, Takuya
Iwata, Ikuko
Takahashi, Aya
Awata, Hiroko
Nakamura, Naosuke
Takakura, Mai
Suzuki, Yusuke
Horiuchi, Junjiro
Okuno, Hiroyuki
Saitoe, Minoru
author_facet Hirano, Yukinori
Ihara, Kunio
Masuda, Tomoko
Yamamoto, Takuya
Iwata, Ikuko
Takahashi, Aya
Awata, Hiroko
Nakamura, Naosuke
Takakura, Mai
Suzuki, Yusuke
Horiuchi, Junjiro
Okuno, Hiroyuki
Saitoe, Minoru
author_sort Hirano, Yukinori
collection PubMed
description Accumulating evidence suggests that transcriptional regulation is required for maintenance of long-term memories (LTMs). Here we characterize global transcriptional and epigenetic changes that occur during LTM storage in the Drosophila mushroom bodies (MBs), structures important for memory. Although LTM formation requires the CREB transcription factor and its coactivator, CBP, subsequent early maintenance requires CREB and a different coactivator, CRTC. Late maintenance becomes CREB independent and instead requires the transcription factor Bx. Bx expression initially depends on CREB/CRTC activity, but later becomes CREB/CRTC independent. The timing of the CREB/CRTC early maintenance phase correlates with the time window for LTM extinction and we identify different subsets of CREB/CRTC target genes that are required for memory maintenance and extinction. Furthermore, we find that prolonging CREB/CRTC-dependent transcription extends the time window for LTM extinction. Our results demonstrate the dynamic nature of stored memory and its regulation by shifting transcription systems in the MBs.
format Online
Article
Text
id pubmed-5114576
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-51145762016-11-29 Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies Hirano, Yukinori Ihara, Kunio Masuda, Tomoko Yamamoto, Takuya Iwata, Ikuko Takahashi, Aya Awata, Hiroko Nakamura, Naosuke Takakura, Mai Suzuki, Yusuke Horiuchi, Junjiro Okuno, Hiroyuki Saitoe, Minoru Nat Commun Article Accumulating evidence suggests that transcriptional regulation is required for maintenance of long-term memories (LTMs). Here we characterize global transcriptional and epigenetic changes that occur during LTM storage in the Drosophila mushroom bodies (MBs), structures important for memory. Although LTM formation requires the CREB transcription factor and its coactivator, CBP, subsequent early maintenance requires CREB and a different coactivator, CRTC. Late maintenance becomes CREB independent and instead requires the transcription factor Bx. Bx expression initially depends on CREB/CRTC activity, but later becomes CREB/CRTC independent. The timing of the CREB/CRTC early maintenance phase correlates with the time window for LTM extinction and we identify different subsets of CREB/CRTC target genes that are required for memory maintenance and extinction. Furthermore, we find that prolonging CREB/CRTC-dependent transcription extends the time window for LTM extinction. Our results demonstrate the dynamic nature of stored memory and its regulation by shifting transcription systems in the MBs. Nature Publishing Group 2016-11-14 /pmc/articles/PMC5114576/ /pubmed/27841260 http://dx.doi.org/10.1038/ncomms13471 Text en Copyright © 2016, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Hirano, Yukinori
Ihara, Kunio
Masuda, Tomoko
Yamamoto, Takuya
Iwata, Ikuko
Takahashi, Aya
Awata, Hiroko
Nakamura, Naosuke
Takakura, Mai
Suzuki, Yusuke
Horiuchi, Junjiro
Okuno, Hiroyuki
Saitoe, Minoru
Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title_full Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title_fullStr Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title_full_unstemmed Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title_short Shifting transcriptional machinery is required for long-term memory maintenance and modification in Drosophila mushroom bodies
title_sort shifting transcriptional machinery is required for long-term memory maintenance and modification in drosophila mushroom bodies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5114576/
https://www.ncbi.nlm.nih.gov/pubmed/27841260
http://dx.doi.org/10.1038/ncomms13471
work_keys_str_mv AT hiranoyukinori shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT iharakunio shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT masudatomoko shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT yamamototakuya shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT iwataikuko shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT takahashiaya shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT awatahiroko shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT nakamuranaosuke shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT takakuramai shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT suzukiyusuke shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT horiuchijunjiro shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT okunohiroyuki shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies
AT saitoeminoru shiftingtranscriptionalmachineryisrequiredforlongtermmemorymaintenanceandmodificationindrosophilamushroombodies