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THE TRANSCRIPTIONAL RESPONSE TO OXIDATIVE STRESS IS INDEPENDENT OF STRESS-GRANULE FORMATION

Amanjot Singh, Arvind Reddy Kandi, Deepa Jayaprakashappa, G. Thuery, Devam J Purohit, Joern Huelsmeier, R. Singh, Sai Shruti Pothapragada, M. Ramaswami, B. Bakthavachalu
Published 2021 · Biology

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Cells respond to stress with translational arrest, robust transcriptional changes, and transcription-independent formation of mRNP assemblies termed stress granules (SGs). Despite considerable interest in the role of SGs in oxidative, unfolded-protein, and viral stress responses, whether and how SGs contribute to stress-induced transcription has not been rigorously examined. To address this issue, we characterized transcriptional changes in Drosophila S2 cells induced by acute oxidative-stress and assessed how these were altered under conditions that disrupted SG assembly. Sodium-arsenite stress for 3 hours predominantly resulted in the induction or upregulation of stress-responsive mRNAs whose levels peaked during cell recovery after stress cessation. The stress-transcriptome is enriched in mRNAs coding for protein chaperones, including HSP70 and low molecular-weight heat shock proteins, glutathione transferases, and several non-coding RNAs. Oxidative stress also induced prominent cytoplasmic stress granules that disassembled 3-hours after stress cessation. As expected, RNAi-mediated knockdown of the conserved G3BP1/ Rasputin protein inhibited stress-granule assembly. However, this disruption had no significant effect on the stress-induced transcriptional response or stress-induced translational arrest. Thus, SG assembly and stress-induced effects on gene expression appear to be driven by distinctive signaling processes. We suggest that while SG assembly represents a fast, transient mechanism, the transcriptional response enables a slower, longer-lasting mechanism for adaptation to and recovery from cell stress.
This paper references
10.1007/PL00000572
Regulation of heat shock gene induction and expression during Drosophila development
S. Michaud (1997)
10.1007/s004010050923
RNA sequestration to pathological lesions of neurodegenerative diseases
S. Ginsberg (1998)
10.1101/GAD.12.24.3788
Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators.
R. Morimoto (1998)
10.1083/JCB.147.7.1431
RNA-Binding Proteins Tia-1 and Tiar Link the Phosphorylation of Eif-2α to the Assembly of Mammalian Stress Granules
N. Kedersha (1999)
10.1093/emboj/18.5.1321
Regulation of JNK signaling by GSTp
V. Adler (1999)
10.1038/70532
Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70
J. Warrick (1999)
10.1073/PNAS.260496697
Genome-wide study of aging and oxidative stress response in Drosophila melanogaster.
S. Zou (2000)
Rasputin, the Drosophila homologue of the RasGAP SH3 binding protein, functions in ras- and Rho-mediated signaling.
C. Pázmán (2000)
10.1093/HMG/9.19.2811
Mechanisms of chaperone suppression of polyglutamine disease: selectivity, synergy and modulation of protein solubility in Drosophila.
H. Chan (2000)
10.1074/jbc.M111548200
Distinct Roles for Glutathione S-Transferases in the Oxidative Stress Response in Schizosaccharomyces pombe *
E. Veal (2002)
10.1042/BST0300963
Stress granules: sites of mRNA triage that regulate mRNA stability and translatability.
N. Kedersha (2002)
10.1172/JCI16784
Translational control in the endoplasmic reticulum stress response.
D. Ron (2002)
10.1242/jeb.00549
Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function
D. Kültz (2003)
10.1016/J.BBRC.2005.07.008
Dynamic regulation of molecular chaperone gene expression in polyglutamine disease.
N. Y. M. Huen (2005)
10.1379/CSC-128R1.1
Full genome gene expression analysis of the heat stress response in Drosophila melanogaster
J. G. Sørensen (2005)
10.1111/j.1420-9101.2005.00962.x
Environmental stress, adaptation and evolution: an overview
R. Bijlsma (2005)
10.1093/AOB/MCL128
Redox regulatory mechanisms in cellular stress responses.
N. Fedoroff (2006)
10.1534/genetics.105.048793
Loss of Hsp70 in Drosophila Is Pleiotropic, With Effects on Thermotolerance, Recovery From Heat Shock and Neurodegeneration
Wei-Jie Gong (2006)
10.1126/SCIENCE.1118265
The snoRNA HBII-52 Regulates Alternative Splicing of the Serotonin Receptor 2C
S. Kishore (2006)
10.1016/S0076-6879(07)31005-7
Mammalian stress granules and processing bodies.
N. Kedersha (2007)
10.1073/pnas.0808480105
Exploring RNA transcription and turnover in vivo by using click chemistry
Cindy Y. Jao (2008)
10.1016/j.gde.2009.09.007
From elements to modules: regulatory evolution in Ascomycota fungi.
Dana J. Wohlbach (2009)
10.1261/rna.1684009
Metazoan stress granule assembly is mediated by P-eIF2alpha-dependent and -independent mechanisms.
Natalie G. Farny (2009)
10.1016/j.mrgentox.2008.09.021
Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells.
R. Ruiz-Ramos (2009)
10.1038/cdd.2010.80
Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death
E. Laborde (2010)
10.1093/hmg/ddp585
The snoRNA MBII-52 (SNORD 115) is processed into smaller RNAs and regulates alternative splicing.
S. Kishore (2010)
10.1001/archneurol.2010.254
Pathological 43-kDa transactivation response DNA-binding protein in older adults with and without severe mental illness.
F. Geser (2010)
10.1016/j.ibmb.2010.03.002
Gene and protein expression of Drosophila Starvin during cold stress and recovery from chill coma.
H. Colinet (2010)
10.1111/j.1742-4658.2009.07470.x
Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster
H. Colinet (2010)
10.1016/j.devcel.2011.11.006
Crosstalk in cellular signaling: background noise or the real thing?
G. Vert (2011)
10.1101/cshperspect.a009704
The stress of protein misfolding: from single cells to multicellular organisms.
T. Gidalevitz (2011)
10.1038/nbt.1861
Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells
M. Rabani (2011)
10.1016/j.cmet.2011.04.009
Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress.
Carlos I. Michel (2011)
10.1242/jcs.107029
Arsenite interferes with protein folding and triggers formation of protein aggregates in yeast
Therese Jacobson (2012)
10.1534/genetics.111.128033
The Response to Heat Shock and Oxidative Stress in Saccharomyces cerevisiae
K. Morano (2012)
10.1002/dneu.20957
Oxidative stress in synapse development and function
Valerie J Milton (2012)
10.1128/MMBR.05018-11
Biology of the Heat Shock Response and Protein Chaperones: Budding Yeast (Saccharomyces cerevisiae) as a Model System
J. Verghese (2012)
10.1371/journal.pone.0040899
Genome-Wide Transcriptional Profiles during Temperature and Oxidative Stress Reveal Coordinated Expression Patterns and Overlapping Regulons in Rice
Dheeraj K Mittal (2012)
10.1002/wrna.1135
Long non‐coding RNAs coordinate cellular responses to stress
S. C. Lakhotia (2012)
Genome-wide transcriptional profiles
D Mittal (2012)
10.1371/journal.pgen.1003598
The RNA-binding Proteins FMR1, Rasputin and Caprin Act Together with the UBA Protein Lingerer to Restrict Tissue Growth in Drosophila melanogaster
R. Baumgartner (2013)
10.1371/journal.pone.0079546
Production of a Dominant-Negative Fragment Due to G3BP1 Cleavage Contributes to the Disruption of Mitochondria-Associated Protective Stress Granules during CVB3 Infection
G. Fung (2013)
10.1101/gr.138628.112
Linking the signaling cascades and dynamic regulatory networks controlling stress responses.
A. Gitter (2013)
10.1016/j.tibs.2013.09.001
Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics.
R. Mailloux (2013)
10.1073/pnas.1309543111
FMRP and Ataxin-2 function together in long-term olfactory habituation and neuronal translational control
Indulekha P Sudhakaran (2013)
10.1038/nchembio.1140
Activation of Hsp70 reduces neurotoxicity by promoting polyglutamine protein degradation
Adrienne M. Wang (2013)
10.1016/j.cub.2014.03.034
ROS Function in Redox Signaling and Oxidative Stress
Michael Schieber (2014)
10.1038/nature12962
Diversity and dynamics of the Drosophila transcriptome
James B. Brown (2014)
10.1016/j.freeradbiomed.2014.08.012
Regulation of protein turnover by heat shock proteins.
Perinur Bozaykut (2014)
10.1371/journal.pgen.1004763
Stress Granule-Defective Mutants Deregulate Stress Responsive Transcripts
Xiaoxue Yang (2014)
10.1146/annurev-virology-031413-085505
Cytoplasmic RNA Granules and Viral Infection.
W. Tsai (2014)
10.3389/fpls.2014.00754
The role of ROS signaling in cross-tolerance: from model to crop
Ilse Barrios Perez (2014)
10.1146/annurev-biochem-060614-034316
Mechanisms and Regulation of Alternative Pre-mRNA Splicing.
Yeon J. Lee (2015)
10.1039/C4RA14600J
Transcriptome analysis reveals the oxidative stress response in Saccharomyces cerevisiae
H. Zhao (2015)
10.1371/journal.pone.0128976
The Role of Inducible Hsp70, and Other Heat Shock Proteins, in Adaptive Complex of Cold Tolerance of the Fruit Fly (Drosophila melanogaster)
T. Štětina (2015)
dFoxo Dependent Transcription of the Heat Shock Proteins
M. Donovan (2015)
10.1261/rna.053116.115
Differential effects of Ydj1 and Sis1 on Hsp70-mediated clearance of stress granules in Saccharomyces cerevisiae.
R. Walters (2015)
10.1016/j.jmb.2015.02.014
Protein quality control under oxidative stress conditions.
Jan-Ulrik Dahl (2015)
10.1007/s00401-015-1487-z
PERK inhibition prevents tau-mediated neurodegeneration in a mouse model of frontotemporal dementia
H. Radford (2015)
10.1016/j.molcel.2016.07.021
A Surveillance Function of the HSPB8-BAG3-HSP70 Chaperone Complex Ensures Stress Granule Integrity and Dynamism.
M. Ganassi (2016)
10.1073/pnas.1519292113
Dual function of C/D box small nucleolar RNAs in rRNA modification and alternative pre-mRNA splicing
M. Falaleeva (2016)
10.1083/jcb.201508028
G3BP–Caprin1–USP10 complexes mediate stress granule condensation and associate with 40S subunits
N. Kedersha (2016)
10.1126/science.aac4354
In vivo aspects of protein folding and quality control
D. Balchin (2016)
10.7554/eLife.18413
Distinct stages in stress granule assembly and disassembly
Joshua R. Wheeler (2016)
10.1172/JCI88069
Rpl13a small nucleolar RNAs regulate systemic glucose metabolism.
Jiyeon Lee (2016)
10.1146/annurev-biochem-060815-014124
Experimental Milestones in the Discovery of Molecular Chaperones as Polypeptide Unfolding Enzymes.
Andrija Finka (2016)
10.1111/acel.12422
Specific protein homeostatic functions of small heat‐shock proteins increase lifespan
M. Vos (2016)
10.1016/j.cell.2015.12.038
ATPase-Modulated Stress Granules Contain a Diverse Proteome and Substructure
Saumya Jain (2016)
10.1002/9781119004813
Stress and environmental regulation of gene expression and adaptation in bacteria
F. J. Bruijn (2016)
A Surveillance Function
O Pansarasa (2016)
Experimental Milestones in the Discovery
A doi10.1093aobmcl128 Finka (2016)
10.1038/nri.2017.63
Translation inhibition and stress granules in the antiviral immune response
C. McCormick (2017)
10.3389/fnmol.2017.00084
Granulostasis: Protein Quality Control of RNP Granules
S. Alberti (2017)
10.1038/s41467-017-00151-0
Transcriptional response to stress is pre-wired by promoter and enhancer architecture
Anniina Vihervaara (2017)
10.1016/j.celrep.2017.06.042
Phospho-Rasputin Stabilization by Sec16 Is Required for Stress Granule Formation upon Amino Acid Starvation.
Angelica Aguilera-Gomez (2017)
10.15252/embj.201695957
An aberrant phase transition of stress granules triggered by misfolded protein and prevented by chaperone function
Daniel Matějů (2017)
10.1016/j.molcel.2017.10.015
The Stress Granule Transcriptome Reveals Principles of mRNA Accumulation in Stress Granules.
A. Khong (2017)
10.1038/emm.2016.157
Oxidative stress and calcium dysregulation by palmitate in type 2 diabetes
L. Ly (2017)
10.1038/emm.2016.143
Therapeutic effect of the immunomodulatory drug lenalidomide, but not pomalidomide, in experimental models of rheumatoid arthritis and inflammatory bowel disease
B. López-Millán (2017)
10.1016/j.cell.2017.08.009
In Situ Architecture and Cellular Interactions of PolyQ Inclusions
F. J. Bäuerlein (2017)
10.1093/nar/gkw977
FlyRNAi.org—the database of the Drosophila RNAi screening center and transgenic RNAi project: 2017 update
Yanhui Hu (2017)
10.1093/brain/awx074
Repurposed drugs targeting eIF2α-P-mediated translational repression prevent neurodegeneration in mice
M. Halliday (2017)
10.1242/dev.154047
Shep regulates Drosophila neuronal remodeling by controlling transcription of its chromatin targets
Dahong Chen (2018)
10.1038/s41389-017-0025-3
Glutathione transferases: substrates, inihibitors and pro-drugs in cancer and neurodegenerative diseases
N. Allocati (2018)
10.1016/j.neuron.2018.04.032
RNP-Granule Assembly via Ataxin-2 Disordered Domains Is Required for Long-Term Memory and Neurodegeneration
B. Bakthavachalu (2018)
10.1038/s41576-018-0001-6
Molecular mechanisms driving transcriptional stress responses
Anniina Vihervaara (2018)
10.1126/scisignal.aat6409
Cells alter their tRNA abundance to selectively regulate protein synthesis during stress conditions
M. Torrent (2018)
10.1016/j.molcel.2017.12.021
Maintaining a Healthy Proteome during Oxidative Stress.
D. Reichmann (2018)
10.1093/jxb/ery130
Redox-dependent control of nuclear transcription in plants.
Huaming He (2018)
10.1093/icb/icz055
Stress-free evolution: the Nrf-coordinated oxidative stress response in early diverging metazoans.
Liam B. Doonan (2019)
10.1101/cshperspect.a032813
Stress Granules and Processing Bodies in Translational Control.
P. Ivanov (2019)
10.3389/fphar.2019.01047
Small Heat Shock Proteins, Big Impact on Protein Aggregation in Neurodegenerative Disease
J. M. Webster (2019)
10.1016/j.celrep.2018.12.034
Heat Shock Factor 1 Drives Intergenic Association of Its Target Gene Loci upon Heat Shock
Surabhi Chowdhary (2019)
10.1093/nar/gkz1140
Functional diversity of small nucleolar RNAs
T. Bratkovič (2019)
10.1038/s41598-019-47424-w
Extensive post-transcriptional buffering of gene expression in the response to severe oxidative stress in baker’s yeast
William R Blevins (2019)
10.1146/annurev-micro-020518-115515
Cellular Functions and Mechanisms of Action of Small Heat Shock Proteins.
A. Mogk (2019)
10.1016/j.bbamcr.2018.09.001
Rasputin a decade on and more promiscuous than ever? A review of G3BPs
U. Alam (2019)
10.1016/j.tig.2018.11.005
Small Nucleolar RNAs Tell a Different Tale.
J. Kufel (2019)
Stress-Free Evolution: The NrfCoordinated Oxidative Stress Response in Early Diverging MetazoansIntegrative and Comparative Biology
LB Doonan (2019)
10.1101/2020.06.08.140319
On the evolution of chaperones and co-chaperones and the exponential expansion of proteome complexity
Mathieu E. Rebeaud (2020)
10.1105/tpc.19.00214
Metabolic Labeling of RNAs Uncovers Hidden Features and Dynamics of the Arabidopsis Transcriptome[CC-BY]
E. Szabo (2020)
10.1038/s41594-020-0399-3
Hsp27 chaperones FUS phase separation under the modulation of stress-induced phosphorylation
Zhenying Liu (2020)
10.3389/fonc.2020.00285
Long Non-coding RNAs: Major Regulators of Cell Stress in Cancer
Patrick Connerty (2020)
10.1101/2020.04.13.039677
Small molecule cognitive enhancer reverses age-related memory decline in mice
K. Krukowski (2020)
10.1007/s12192-020-01101-4
Small heat shock proteins in neurodegenerative diseases
Leen Vendredy (2020)
10.1126/science.aax3072
Sequencing metabolically labeled transcripts in single cells reveals mRNA turnover strategies
Nico Battich (2020)
10.1007/s00018-020-03565-0
Stress granule subtypes: an emerging link to neurodegeneration
Vivek M. Advani (2020)
10.1093/nar/gkaa376
G3BP1-linked mRNA partitioning supports selective protein synthesis in response to oxidative stress
Syam Prakash Somasekharan (2020)
10.1101/2020.06.30.179986
RNA degradation sculpts the maternal transcriptome during Drosophila oogenesis
Patrick Blatt (2020)
10.1126/science.abb6502
Do us a favor
H. Thorp (2020)
10.1016/j.celrep.2020.02.066
The RNA-Binding Protein Rasputin/G3BP Enhances the Stability and Translation of Its Target mRNAs.
J. Laver (2020)
10.1016/j.cell.2020.03.049
RNA-Induced Conformational Switching and Clustering of G3BP Drive Stress Granule Assembly by Condensation
J. Guillén-Boixet (2020)
10.1016/j.molcel.2020.06.037
Translational Repression of G3BP in Cancer and Germ Cells Suppresses Stress Granules and Enhances Stress Tolerance.
Anna K. Lee (2020)
10.1016/j.cell.2020.03.050
Competing Protein-RNA Interaction Networks Control Multiphase Intracellular Organization
David W. Sanders (2020)
10.1242/jcs.243451
Canonical nucleators are dispensable for stress granule assembly in intestinal progenitors.
K. Buddika (2020)
10.1101/2020.01.08.899146
An interaction network of RNA-binding proteins involved in Drosophila oogenesis
Prashali Bansal (2020)
10.1126/science.aat5314
The integrated stress response: From mechanism to disease
M. Costa-Mattioli (2020)
10.1016/j.cell.2020.03.046
G3BP1 Is a Tunable Switch that Triggers Phase Separation to Assemble Stress Granules
Peiguo Yang (2020)
10.1126/science.abb4309
HSP70 chaperones RNA-free TDP-43 into anisotropic intranuclear liquid spherical shells
Haiyang Yu (2021)
10.1101/2021.06.21.449212
Identification of the stress granule transcriptome via RNA-editing in single cells and in vivo
W. van Leeuwen (2021)
10.1242/dmm.048983
(Dis)Solving the problem of aberrant protein states
C. Fare (2021)
10.15252/embj.2020106183
Dual roles of HSP70 chaperone HSPA1 in quality control of nascent and newly synthesized proteins
Guiyou Tian (2021)
10.1261/rna.078738.121
The role of stress-activated RNA-protein granules in surviving adversity.
Leah E. Escalante (2021)
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