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
  • [41] Enhancing of hippocampal theta rhythms correlates with propofol-induced memory suppression
    Han, Linlin
    Zhao, Shuai
    Chen, Xiangdong
    ANESTHESIA AND ANALGESIA, 2021, 133 (3S_SUPPL): : 1390 - 1391
  • [42] The cortisol awakening response is related with PERIOD1 clock gene expression in older women
    Olbrich, Denise
    Dittmar, Manuela
    EXPERIMENTAL GERONTOLOGY, 2012, 47 (07) : 527 - 533
  • [43] A comparative study on the regulatory region of the PERIOD1 gene among diurnal/nocturnal primates
    Takafumi Katsumura
    Yukiko Fukuyo
    Shoji Kawamura
    Hiroki Oota
    Journal of Physiological Anthropology, 35
  • [44] Effects of Antisense-induced Downregulation of Circadian Gene Period1 in the Basolateral Amygdala on Spontaneous Sleep-Wakefulness and Consolidation of Traumatic Memory
    Parikh, Meet
    Sharma, R.
    Chischolm, A.
    Whittle, A.
    Sahota, P.
    Thakkar, M.
    ANNALS OF NEUROLOGY, 2024, 96 : S295 - S295
  • [45] Similar profiles in human period1 gene expression in peripheral mononuclear and polymorphonuclear cells
    Kusanagi, H
    Mishima, K
    Satoh, K
    Echizenya, M
    Katoh, T
    Shimizu, T
    NEUROSCIENCE LETTERS, 2004, 365 (02) : 124 - 127
  • [46] PERIOD1 is an Anti-apoptotic Factor in Human Pancreatic and Hepatic Cancer Cells
    Sato, Fuyuki
    Nagata, Chihiro
    Liu, Yang
    Suzuki, Takahiro
    Kondo, Jun
    Morohashi, Satoko
    Imaizumi, Tadaatsu
    Kato, Yukio
    Kijima, Hiroshi
    JOURNAL OF BIOCHEMISTRY, 2009, 146 (06): : 833 - 838
  • [47] Period1 mediates rhythmic metabolism of toxins by interacting with CYP2E1
    Wenhao Ge
    Tao Wang
    Yang Zhao
    Yunxia Yang
    Qi Sun
    Xiao Yang
    Yan Gao
    Xi Xu
    Jianfa Zhang
    Cell Death & Disease, 12
  • [48] Separate roles for hippocampal β-adrenoceptors in memory processing.
    Gibbs, Marie
    Summers, Roger
    ACTA PHARMACOLOGICA SINICA, 2006, 27 : 112 - 112
  • [49] Hippocampal function in memory processing and its deterioration in aging
    Siancas, Aguirre
    Ernesto, Elias
    REVISTA MEXICANA DE NEUROCIENCIA, 2015, 16 (04): : 21 - 30
  • [50] A meeting of two chronobiological systems: Period1 and BMAL1 modulate the human hair cycle
    Al-Nuaimi, Y.
    Hardman, J. A.
    Haslam, I. S.
    Biro, T.
    Toth, B. I.
    Farjo, N.
    Farjo, B.
    Philpott, M.
    Watson, R.
    Grimaldi, B.
    Kloepper, J. E.
    Paus, R.
    JOURNAL OF INVESTIGATIVE DERMATOLOGY, 2013, 133 (05) : 1416 - 1416