Translational profiling of clock cells reveals circadianly synchronized protein synthesis

PLoS Biology
Yanmei HuangF Rob Jackson

Abstract

Genome-wide studies of circadian transcription or mRNA translation have been hindered by the presence of heterogeneous cell populations in complex tissues such as the nervous system. We describe here the use of a Drosophila cell-specific translational profiling approach to document the rhythmic "translatome" of neural clock cells for the first time in any organism. Unexpectedly, translation of most clock-regulated transcripts--as assayed by mRNA ribosome association--occurs at one of two predominant circadian phases, midday or mid-night, times of behavioral quiescence; mRNAs encoding similar cellular functions are translated at the same time of day. Our analysis also indicates that fundamental cellular processes--metabolism, energy production, redox state (e.g., the thioredoxin system), cell growth, signaling and others--are rhythmically modulated within clock cells via synchronized protein synthesis. Our approach is validated by the identification of mRNAs known to exhibit circadian changes in abundance and the discovery of hundreds of novel mRNAs that show translational rhythms. This includes Tdc2, encoding a neurotransmitter synthetic enzyme, which we demonstrate is required within clock neurons for normal circadian locomoto...Continue Reading

Associated Datasets

References

May 5, 1983·Nature·M S Livingstone, B L Tempel
Jan 6, 1994·Nature·K A Hughes, B Charlesworth
Mar 1, 1994·Proceedings of the National Academy of Sciences of the United States of America·H SchenkK Schulze-Osthoff
Sep 30, 2000·European Journal of Biochemistry·E S Arnér, A Holmgren
Nov 24, 2001·Neuron·A Claridge-ChangM W Young
Feb 21, 2002·The Journal of Biological Chemistry·Hiroki R UedaSeiichi Hashimoto
Jun 29, 2002·Proceedings of the National Academy of Sciences of the United States of America·Yiing LinPaul H Taghert
Feb 26, 2003·Proceedings of the National Academy of Sciences of the United States of America·Bas van SteenselHarmen J Bussemaker
Jul 17, 2003·The Journal of Biological Chemistry·Katsutaka OishiNorio Ishida
Sep 10, 2004·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Yiing LinPaul H Taghert
Aug 19, 2005·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Gabriella B LundkvistGene D Block
Jan 13, 2006·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Michael N NitabachTodd C Holmes
Mar 3, 2006·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Dirk RiegerCharlotte Helfrich-Förster
Nov 11, 2006·Annual Review of Genetics·Herman Wijnen, Michael W Young
Feb 1, 2007·Proceedings of the National Academy of Sciences of the United States of America·Shihoko KojimaHajime Tei
May 31, 2007·Nature Genetics·Venkateswara R ChintapalliJulian A T Dow
Oct 5, 2007·The Journal of Neuroscience : the Official Journal of the Society for Neuroscience·Ania BuszaPatrick Emery
Jan 24, 2008·Current Biology : CB·Michael N Nitabach, Paul H Taghert
Apr 19, 2008·Cold Spring Harbor Symposia on Quantitative Biology·J BenitoP E Hardin
Mar 18, 2009·Bioinformatics·Cole TrapnellSteven L Salzberg
May 12, 2009·Nature Methods·Michael R MillerChris Q Doe
Jul 14, 2010·Proceedings of the National Academy of Sciences of the United States of America·Elzbieta Kula-EversoleMichael Rosbash
Sep 30, 2010·Journal of Biological Rhythms·Michael E HughesKarl Kornacker
Oct 29, 2010·Genome Biology·Simon Anders, Wolfgang Huber
Dec 4, 2010·Science·Joseph Bass, Joseph S Takahashi
Jan 29, 2011·Nature·John S O'Neill, Akhilesh B Reddy
Jan 29, 2011·Nature·John S O'NeillAndrew J Millar

❮ Previous
Next ❯

Citations

Sep 19, 2014·ELife·Jorge Ruiz-OreraM Mar Alba
Nov 12, 2015·Frontiers in Molecular Neuroscience·Denise R Cook-SnyderLeon G Reijmers
Jun 30, 2015·Current Opinion in Insect Science·Ozgur Tataroglu, Patrick Emery
Nov 18, 2014·Frontiers in Molecular Neuroscience·Laurel DraneLeon G Reijmers
Oct 1, 2016·Cellular and Molecular Life Sciences : CMLS·Lucia Mendoza-ViverosHai-Ying Mary Cheng
Jul 30, 2014·Nature Communications·Joshua A AinsleyLeon G Reijmers
Oct 21, 2018·Behavior Genetics·Susan T HarbisonTrudy F C Mackay
Jul 5, 2017·Biochemical Society Transactions·Minnie Fu, Xiaoyong Yang
Nov 4, 2017·RNA Biology·Sarah Catherine MillsAlbrecht G von Arnim
Apr 3, 2020·The Journal of Experimental Biology·Thomas Roeder
Jun 3, 2020·Nature Communications·Chenwei WangLuoying Zhang
May 11, 2019·International Journal of Molecular Sciences·Ellen PaatelaNobuaki Kikyo
Feb 6, 2015·G3 : Genes - Genomes - Genetics·Yanmei HuangF Rob Jackson
Oct 3, 2019·Physical Review. E·Paula S Nieto, C A Condat
Aug 13, 2017·Genetics·Esteban J BeckwithMarcelo J Yanovsky
Feb 5, 2021·CNS Neuroscience & Therapeutics·Nurul Atiqah ZulazmiMohd Farooq Shaikh
Nov 15, 2020·Nature Communications·Nathan C BalukoffStephen Lee
Feb 21, 2021·Glia·Tina SmoličNina Vardjan
Mar 2, 2021·Journal of Biological Rhythms·Myra AhmadDeniz Top
Mar 12, 2021·Wiley Interdisciplinary Reviews. RNA·J J David HoPhilip A Marsden
Dec 27, 2017·Free Radical Biology & Medicine·Markus DagnellElias S J Arnér
Sep 21, 2021·PLoS Genetics·Samantha YouF Rob Jackson

❮ Previous
Next ❯

Methods Mentioned

BETA
Fluorescence-Activated Cell Sorting
dissection
PCR
RNA-seq
GTPases
Transgenic
affinity purification
immunoprecipitation
Illumina

Software Mentioned

Image J
ARSER
HTseq
CYCLE
JTK
DESeq package for R
FlyAtlas
_ CYCLE
Bowtie
Bowtie2

Related Concepts

Trending Feeds

COVID-19

Coronaviruses encompass a large family of viruses that cause the common cold as well as more serious diseases, such as the ongoing outbreak of coronavirus disease 2019 (COVID-19; formally known as 2019-nCoV). Coronaviruses can spread from animals to humans; symptoms include fever, cough, shortness of breath, and breathing difficulties; in more severe cases, infection can lead to death. This feed covers recent research on COVID-19.

Blastomycosis

Blastomycosis fungal infections spread through inhaling Blastomyces dermatitidis spores. Discover the latest research on blastomycosis fungal infections here.

Nuclear Pore Complex in ALS/FTD

Alterations in nucleocytoplasmic transport, controlled by the nuclear pore complex, may be involved in the pathomechanism underlying multiple neurodegenerative diseases including Amyotrophic Lateral Sclerosis and Frontotemporal Dementia. Here is the latest research on the nuclear pore complex in ALS and FTD.

Applications of Molecular Barcoding

The concept of molecular barcoding is that each original DNA or RNA molecule is attached to a unique sequence barcode. Sequence reads having different barcodes represent different original molecules, while sequence reads having the same barcode are results of PCR duplication from one original molecule. Discover the latest research on molecular barcoding here.

Chronic Fatigue Syndrome

Chronic fatigue syndrome is a disease characterized by unexplained disabling fatigue; the pathology of which is incompletely understood. Discover the latest research on chronic fatigue syndrome here.

Evolution of Pluripotency

Pluripotency refers to the ability of a cell to develop into three primary germ cell layers of the embryo. This feed focuses on the mechanisms that underlie the evolution of pluripotency. Here is the latest research.

Position Effect Variegation

Position Effect Variagation occurs when a gene is inactivated due to its positioning near heterochromatic regions within a chromosome. Discover the latest research on Position Effect Variagation here.

STING Receptor Agonists

Stimulator of IFN genes (STING) are a group of transmembrane proteins that are involved in the induction of type I interferon that is important in the innate immune response. The stimulation of STING has been an active area of research in the treatment of cancer and infectious diseases. Here is the latest research on STING receptor agonists.

Microbicide

Microbicides are products that can be applied to vaginal or rectal mucosal surfaces with the goal of preventing, or at least significantly reducing, the transmission of sexually transmitted infections. Here is the latest research on microbicides.