ArticleMolecular cell2023
Nuclear RNA catabolism controls endogenous retroviruses, gene expression asymmetry, and dedifferentiation.
Open access · hybridAbstract read
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Article in Molecular cell, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 16 papers.
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0cells of the map it votes in
16citing papers in PubMed
2.8field-weighted citation impact, top 9% of its field
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Who cites it
16 citing papers in PubMed, 18 citations in OpenAlex.
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- The expression, regulation, and function of human endogenous retroviruses in genitourinary cancers.Cell death discovery · 2025Review
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Corrections and comments
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Authors and funding
46 authors at 12 institutions in 4 countries.
Denis TorreDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Center for OncoGenomics and Innovative Therapeutics (COGIT), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Yesai S FstkchyanDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Jessica Sook Yuin HoDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore 169857, Singapore.
Youngseo CheonDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, South Korea; Department of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Roosheel S PatelDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Emma J DegraceDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Slim MzoughiCenter for OncoGenomics and Innovative Therapeutics (COGIT), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Megan SchwarzCenter for OncoGenomics and Innovative Therapeutics (COGIT), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Kevin MohammedCenter for OncoGenomics and Innovative Therapeutics (COGIT), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Ji-Seon SeoDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Raquel Romero-BuenoDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Deniz DemirciogluDepartment of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Bioinformatics for Next Generation Sequencing (BiNGS) Shared Resource Facility, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Dan HassonDepartment of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Bioinformatics for Next Generation Sequencing (BiNGS) Shared Resource Facility, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Weijing TangDepartment of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Sameehan U MahajaniDepartment of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Laura CampisiDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Simin ZhengDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Won-Suk SongDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Ying-Chih WangDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Hardik ShahDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Nancy FrancoeurDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Juan SotoDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Zelda SalfatiDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Matthew T WeirauchDepartment of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45229, USA.
Peter WarburtonDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Kristin BeaumontDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Melissa L SmithDepartment of Biochemistry and Molecular Genetics, University of Louisville School of Medicine, Louisville, KY 40202, USA.
Lubbertus MulderDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
S Armando VillaltaDepartment of Physiology and Biophysics, University of California Irvine, Irvine, CA 92697, USA.
Kai KessenbrockDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA.
Cholsoon JangDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Daeyoup LeeDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, South Korea.
Silvia De RubeisSeaver Autism Center for Research and Treatment, Department of Psychiatry, The Mindich Child Health and Development Institute, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Inma CobosDepartment of Pathology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Oliver TamCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Molly Gale HammellCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Marcus SeldinDepartment of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA.
Yongsheng ShiCenter for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA; Department of Microbiology and Molecular Genetics, School of Medicine, University of California Irvine, Irvine, CA 92697, USA.
Uttiya BasuDepartment of Microbiology & Immunology, Columbia University Medical Center, New York, NY 10032, USA.
Vittorio SebastianoInstitute for Stem Cell Biology and Regenerative Medicine and the Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, CA 94305, USA.
Minji ByunDepartment of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Robert SebraDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Brad R RosenbergDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Chris BennerDepartment of Medicine, University of California, San Diego, San Diego, CA 92093, USA.
Ernesto GuccioneCenter for OncoGenomics and Innovative Therapeutics (COGIT), Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Pharmacological Sciences and Mount Sinai Center for Therapeutics Discovery, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Black Family Stem Cell Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: ernesto.guccione@mssm.edu.
Ivan MarazziDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Biological Chemistry, University of California Irvine, Irvine, CA 92697, USA; Center for Epigenetics and Metabolism, University of California Irvine, Irvine, CA 92697, USA; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: imarazzi@uci.edu.
Icahn School of Medicine at Mount Sinai · USUniversity of California, Irvine · USStanford University · USCold Spring Harbor Laboratory · USKorea Advanced Institute of Science and Technology · KRCalifornia Institute for Regenerative Medicine · USChild Health and Development Institute · USColumbia University Irving Medical Center · USDuke-NUS Medical School · SGUniversity of California San Diego · USUniversity of Cincinnati Medical Center · USUniversity of Louisville · US
Funding
SARS-CoV adaptations through a Systems Biology Lens (SYBIL)U19AI135972 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI Adolfo Garcia-Sastre · 2018 to 2026
$27.2MTRAINING PROGRAM IN CANCER THERAPYT32CA078207 · NCI · MOUNT SINAI SCHOOL OF MEDICINE OF NYU · PI James J Manfredi · 1999 to 2026
$11.6MResearch Project 3: Role of Posttranslational Protein Modifications in the Pathogenesis of Ebola Virus DiseaseP01AI150585 · NIAID · UNIVERSITY OF TEXAS MED BR GALVESTON · PI BUKREYEV, ALEXANDER · 2021 to 2025
$11.3MDynamic regulatory network models of human response to influenza virusU01AI150748 · NIAID · UNIVERSITY OF CALIFORNIA-IRVINE · PI MARAZZI, IVAN, MIRALDI, EMILY · 2020 to 2024
$5.8MRegulation of inflammatory gene expression during SARS2 infectionR01AI168130 · NIAID · UNIVERSITY OF CALIFORNIA-IRVINE · PI Ivan Marazzi · 2022 to 2026
$3.7MAltered inflammatory response associated with acquired DNMT3A mutationsR01HL153974 · NHLBI · UNIVERSITY OF CALIFORNIA-IRVINE · PI BYUN, MINJI · 2021 to 2025
$3.3MT cell Immunity in a Rare Juvenile Form of Motor Neuron DiseaseR01NS123287 · NINDS · UNIVERSITY OF CALIFORNIA-IRVINE · PI Laura Campisi, Ivan Marazzi · 2023 to 2026
$2.6MA host-dependent mechanism controlling influenza virus infection by suppressing viral RNA synthesisR01AI143840 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI MARAZZI, IVAN · 2019 to 2023
$2.1MCOVID and Translational Science supercomputer (CATS)S10OD030463 · OD · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI KOVATCH, PATRICIA · 2021 to 2021
$2.0MBig Omics Data Engine 2 SupercomputerS10OD026880 · OD · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI KOVATCH, PATRICIA · 2019 to 2019
$2.0MUncovering how transcription and chromatin 3D structure impact one another during cellular activationR01GM134366 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI BENNER, CHRISTOPHER W · 2019 to 2023
$1.7MNCI NIH HHS T32 CA078207NHLBI NIH HHS R01 HL153974NIAID NIH HHS P01 AI150585NIAID NIH HHS R01 AI143840NIAID NIH HHS R01 AI168130NIAID NIH HHS U01 AI150748NIAID NIH HHS U19 AI135972NIGMS NIH HHS R01 GM134366NIH HHS S10 OD026880NIH HHS S10 OD030463NINDS NIH HHS R01 NS123287
Abstract
Endogenous retroviruses (ERVs) are remnants of ancient parasitic infections and comprise sizable portions of most genomes. Although epigenetic mechanisms silence most ERVs by generating a repressive environment that prevents their expression (heterochromatin), little is known about mechanisms silencing ERVs residing in open regions of the genome (euchromatin). This is particularly important during embryonic development, where induction and repression of distinct classes of ERVs occur in short temporal windows. Here, we demonstrate that transcription-associated RNA degradation by the nuclear RNA exosome and Integrator is a regulatory mechanism that controls the productive transcription of most genes and many ERVs involved in preimplantation development. Disrupting nuclear RNA catabolism promotes dedifferentiation to a totipotent-like state characterized by defects in RNAPII elongation and decreased expression of long genes (gene-length asymmetry). Our results indicate that RNA catabolism is a core regulatory module of gene networks that safeguards RNAPII activity, ERV expression, cell identity, and developmental potency.
Indexed as
Endogenous RetrovirusesEpigenesis, GeneticGene ExpressionHeterochromatinRNA, NuclearHeterochromatinRNA, Nuclear2CLCelongationendogenous retrovirusIntegratorMERVLnon-coding RNARNA catabolismstem celltotipotent-like cellstranscription-associated RNA degradation
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