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      Optogenetic perturbation and bioluminescence imaging to analyze cell-to-cell transfer of oscillatory information

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          Abstract

          Isomura et al. developed an integrated approach that combines optogenetic perturbations and single-cell bioluminescence imaging to visualize and reconstitute synchronized oscillatory gene expression in signal-sending and signal-receiving processes.

          Abstract

          Cells communicate with each other to coordinate their gene activities at the population level through signaling pathways. It has been shown that many gene activities are oscillatory and that the frequency and phase of oscillatory gene expression encode various types of information. However, whether or how such oscillatory information is transmitted from cell to cell remains unknown. Here, we developed an integrated approach that combines optogenetic perturbations and single-cell bioluminescence imaging to visualize and reconstitute synchronized oscillatory gene expression in signal-sending and signal-receiving processes. We found that intracellular and intercellular periodic inputs of Notch signaling entrain intrinsic oscillations by frequency tuning and phase shifting at the single-cell level. In this way, the oscillation dynamics are transmitted through Notch signaling, thereby synchronizing the population of oscillators. Thus, this approach enabled us to control and monitor dynamic cell-to-cell transfer of oscillatory information to coordinate gene expression patterns at the population level.

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          Single cell RNA Seq reveals dynamic paracrine control of cellular variation

          High-throughput single-cell transcriptomics offers an unbiased approach for understanding the extent, basis, and function of gene expression variation between seemingly identical cells. Here, we sequence single-cell RNA-Seq libraries prepared from over 1,700 primary mouse bone marrow derived dendritic cells (DCs) spanning several experimental conditions. We find substantial variation between identically stimulated DCs, in both the fraction of cells detectably expressing a given mRNA and the transcript’s level within expressing cells. Distinct gene modules are characterized by different temporal heterogeneity profiles. In particular, a “core” module of antiviral genes is expressed very early by a few “precocious” cells, but is later activated in all cells. By stimulating cells individually in sealed microfluidic chambers, analyzing DCs from knockout mice, and modulating secretion and extracellular signaling, we show that this response is coordinated via interferon-mediated paracrine signaling. Surprisingly, preventing cell-to-cell communication also substantially reduces variability in the expression of an early-induced “peaked” inflammatory module, suggesting that paracrine signaling additionally represses part of the inflammatory program. Our study highlights the importance of cell-to-cell communication in controlling cellular heterogeneity and reveals general strategies that multicellular populations use to establish complex dynamic responses.
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            Encoding and decoding cellular information through signaling dynamics.

            A growing number of studies are revealing that cells can send and receive information by controlling the temporal behavior (dynamics) of their signaling molecules. In this Review, we discuss what is known about the dynamics of various signaling networks and their role in controlling cellular responses. We identify general principles that are emerging in the field, focusing specifically on how the identity and quantity of a stimulus is encoded in temporal patterns, how signaling dynamics influence cellular outcomes, and how specific dynamical patterns are both shaped and interpreted by the structure of molecular networks. We conclude by discussing potential functional roles for transmitting cellular information through the dynamics of signaling molecules and possible applications for the treatment of disease. Copyright © 2013 Elsevier Inc. All rights reserved.
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              Detection ofn:mPhase Locking from Noisy Data: Application to Magnetoencephalography

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                Author and article information

                Journal
                Genes Dev
                Genes Dev
                genesdev
                genesdev
                GAD
                Genes & Development
                Cold Spring Harbor Laboratory Press
                0890-9369
                1549-5477
                1 March 2017
                1 March 2017
                : 31
                : 5
                : 524-535
                Affiliations
                [1 ]Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto 606-8507, Japan;
                [2 ]Japan Science and Technology Agency, PRESTO (Precursory Research for Embryonic Science and Technology), Saitama 332-0012, Japan;
                [3 ]Department of Information Sciences, Ochanomizu University, Tokyo 112-8610, Japan;
                [4 ]Institute for Integrated Cell-Material Sciences (World Premier International research Center [WPI]-iCeMS), Kyoto University, Kyoto 606-8501, Japan;
                [5 ]Graduate School of Medicine, Kyoto University, Kyoto 606-8501, Japan;
                [6 ]Graduate School of Biostudies, Kyoto University, Kyoto 606-8501, Japan
                Author notes
                Article
                8711660
                10.1101/gad.294546.116
                5393066
                28373207
                acfd9373-a7df-4c76-85f3-f07144d93701
                © 2017 Isomura et al.; Published by Cold Spring Harbor Laboratory Press

                This article, published in Genes & Development, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.

                History
                : 4 December 2016
                : 28 February 2017
                Page count
                Pages: 12
                Funding
                Funded by: Japan Science and Technology Agency http://dx.doi.org/10.13039/501100002241
                Funded by: Precursory Research for Embryonic Science and Technology
                Funded by: Core Research for Evolutional Science and Technology http://dx.doi.org/10.13039/501100003382
                Funded by: Ministry of Education, Culture, Sports, Science, and Technology http://dx.doi.org/10.13039/501100001700
                Award ID: 26119708
                Award ID: 16H06480
                Funded by: Japan Society for the Promotion of Science http://dx.doi.org/10.13039/501100001691
                Award ID: 24240049
                Funded by: JSPS http://dx.doi.org/10.13039/501100001691
                Award ID: 15H05326
                Categories
                Resource/Methodology

                optogenetics,oscillatory expression,synchronization,frequency tuning,phase shifting,notch signaling,live imaging

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