PERIOD1 coordinates hippocampal rhythms and memory processing with daytime

被引:80
|
作者
Rawashdeh, Oliver [1 ]
Jilg, Antje [1 ]
Jedlicka, Peter [2 ]
Slawska, Jolanta [1 ]
Thomas, Lukas [1 ]
Saade, Anastasia [1 ]
Schwarzacher, Stephan W. [2 ]
Stehle, Joerg H. [1 ]
机构
[1] Goethe Univ Frankfurt, Inst Cellular & Mol Anat, D-60590 Frankfurt, Germany
[2] Goethe Univ Frankfurt, Inst Clin Neuroanat, D-60590 Frankfurt, Germany
关键词
circadian; chromatin; epigenetics; CREB; clock gene; LTP; learning; LONG-TERM POTENTIATION; ELEMENT-BINDING PROTEIN; CIRCADIAN MODULATION; HISTONE ACETYLATION; EPIGENETIC MECHANISMS; SYNAPTIC PLASTICITY; GENE-EXPRESSION; CLOCK GENE; REGULATES MEMORY; LATE-PHASE;
D O I
10.1002/hipo.22262
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
In species ranging from flies to mammals, parameters of memory processing, like acquisition, consolidation, and retrieval are clearly molded by time of day. However, mechanisms that regulate and adapt these temporal differences are elusive, with an involvement of clock genes and their protein products suggestive. Therefore, we analyzed initially in mouse hippocampus the daytime-dependent dynamics of parameters, known to be important for proper memory formation, like phosphorylation of the "memory molecule" cyclic adenosine monophosphate (cAMP) responsive element binding protein (CREB) and chromatin remodeling. Next, in an effort to characterize the mechanistic role of clock genes within hippocampal molecular dynamics, we compared the results obtained from wildtype (WT) -mice and mice deficient for the archetypical clock gene Period1 (Per1(-/-)-mice). We detected that the circadian rhythm of CREB phosphorylation in the hippocampus of WT mice disappeared completely in mice lacking Per1. Furthermore, we found that the here for the first time described profound endogenous day/night rhythms in histone modifications in the hippocampus of WT-mice are markedly perturbed in Per1(-/-)-mice. Concomitantly, both, in vivo recorded LTP, a cellular correlate for long-term memory, and hippocampal gene expression were significantly altered in the absence of Per1. Notably, these molecular perturbations in Per1(-/-)-mice were accompanied by the loss of daytime-dependent differences in spatial working memory performance. Our data provide a molecular blueprint for a novel role of PER1 in temporally shaping the daytime-dependency of memory performance, likely, by gating CREB signaling, and by coupling to downstream chromatin remodeling. (c) 2014 Wiley Periodicals, Inc.
引用
收藏
页码:712 / 723
页数:12
相关论文
共 50 条
  • [21] PINEAL MELATONIN SYNTHESIS IS ALTERED IN Period1 DEFICIENT MICE
    Christ, E.
    Pfeffer, M.
    Korf, H. W.
    von Gall, C.
    NEUROSCIENCE, 2010, 171 (02) : 398 - 406
  • [22] PTBP1 Positively Regulates the Translation of Circadian Clock Gene,Period1
    Kim, Wanil
    Shin, Jae-Cheon
    Lee, Kyung-Ha
    Kim, Kyong-Tai
    INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 2020, 21 (18) : 1 - 14
  • [23] The clock gene Period1 regulates innate routine behaviour in mice
    Bechstein, Philipp
    Rehbach, Nils-Joern
    Yuhasingham, Gowzekan
    Schuermann, Christoph
    Goepfert, Melanie
    Koessl, Manfred
    Maronde, Erik
    PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, 2014, 281 (1781)
  • [24] 节律基因Period1对吗啡依赖效应的影响
    王跃锜
    周薇
    刘延友
    刘英辉
    彭涛
    王正荣
    航天医学与医学工程, 2004, (05) : 383 - 385
  • [25] Glucocorticoids and Stress-Induced Changes in the Expression of PERIOD1 in the Rat Forebrain
    Al-Safadi, Sherin
    Branchaud, Marie
    Rutherford, Spencer
    Amir, Shimon
    PLOS ONE, 2015, 10 (06):
  • [26] Structural and functional analysis of 3′ untranslated region of mouse Period1 mRNA
    Kojima, S
    Hirose, M
    Tokunaga, K
    Sakaki, Y
    Tei, H
    BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 2003, 301 (01) : 1 - 7
  • [27] Uncoupling of promoter methylation and expression of Period1 in cervical cancer cells
    Hsu, Min-Chuan
    Huang, Chih-Cheng
    Choo, Kong-Bung
    Huang, Chiu-Jung
    BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS, 2007, 360 (01) : 257 - 262
  • [28] Expression of the circadian clock genes clock and period1 in human skin
    Zanello, SB
    Jackson, DM
    Holick, MF
    FASEB JOURNAL, 2000, 14 (08): : A1442 - A1442
  • [29] Hippocampal Processing of Ambiguity Enhances Fear Memory
    Amadi, Ugwechi
    Lim, Seh Hong
    Liu, Elizabeth
    Baratta, Michael V.
    Goosens, Ki A.
    PSYCHOLOGICAL SCIENCE, 2017, 28 (02) : 143 - 161
  • [30] The role of inhibitory circuits in hippocampal memory processing
    Topolnik, Lisa
    Tamboli, Suhel
    NATURE REVIEWS NEUROSCIENCE, 2022, 23 (08) : 476 - 492