Mutant KRAS regulates transposable element RNA and innate immunity via KRAB zinc-finger genes.

CP: Molecular biology KRAS KZNF RAS signaling RNA biomarker cancer extracellular RNA extracellular vesicles interferon-stimulated genes noncoding RNA transposable element

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
19 07 2022
Historique:
received: 08 11 2020
revised: 04 04 2022
accepted: 27 06 2022
entrez: 20 7 2022
pubmed: 21 7 2022
medline: 23 7 2022
Statut: ppublish

Résumé

RAS genes are the most frequently mutated oncogenes in cancer, yet the effects of oncogenic RAS signaling on the noncoding transcriptome remain unclear. We analyzed the transcriptomes of human airway and bronchial epithelial cells transformed with mutant KRAS to define the landscape of KRAS-regulated noncoding RNAs. We find that oncogenic KRAS signaling upregulates noncoding transcripts throughout the genome, many of which arise from transposable elements (TEs). These TE RNAs exhibit differential expression, are preferentially released in extracellular vesicles, and are regulated by KRAB zinc-finger (KZNF) genes, which are broadly downregulated in mutant KRAS cells and lung adenocarcinomas in vivo. Moreover, mutant KRAS induces an intrinsic IFN-stimulated gene (ISG) signature that is often seen across many different cancers. Our results indicate that mutant KRAS remodels the repetitive noncoding transcriptome, demonstrating the broad scope of intracellular and extracellular RNAs regulated by this oncogenic signaling pathway.

Identifiants

pubmed: 35858545
pii: S2211-1247(22)00906-8
doi: 10.1016/j.celrep.2022.111104
pmc: PMC9374308
mid: NIHMS1824946
pii:
doi:

Substances chimiques

DNA Transposable Elements 0
KRAS protein, human 0
RNA 63231-63-0
Proto-Oncogene Proteins p21(ras) EC 3.6.5.2
Zinc J41CSQ7QDS

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

111104

Subventions

Organisme : NIDDK NIH HHS
ID : F99 DK131504
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA227807
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA230263
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA239604
Pays : United States

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests D.H.K. and R.E.R. are inventors on patent applications covering the methods and compositions to detect cancer using extracellular RNA submitted by the Regents of the University of California. D.H.K. and spouse are founders and shareholders in and D.H.K. is a board member of LincRNA Bio.

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Auteurs

Roman E Reggiardo (RE)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Sreelakshmi Velandi Maroli (SV)

Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Haley Halasz (H)

Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Mehmet Ozen (M)

Canary Center at Stanford for Cancer Early Detection, Department of Radiology, Stanford University School of Medicine, Palo Alto, CA 94305, USA.

Eva Hrabeta-Robinson (E)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Amit Behera (A)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Vikas Peddu (V)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

David Carrillo (D)

Department of Molecular, Cell, and Developmental Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Erin LaMontagne (E)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Lila Whitehead (L)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Eejung Kim (E)

Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA; Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA 02215, USA.

Shivani Malik (S)

Department of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA.

Jason Fernandes (J)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Georgi Marinov (G)

Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.

Eric Collisson (E)

Department of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA.

Angela Brooks (A)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Center for Molecular Biology of RNA, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.

Utkan Demirci (U)

Canary Center at Stanford for Cancer Early Detection, Department of Radiology, Stanford University School of Medicine, Palo Alto, CA 94305, USA.

Daniel H Kim (DH)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Canary Center at Stanford for Cancer Early Detection, Department of Radiology, Stanford University School of Medicine, Palo Alto, CA 94305, USA; Institute for the Biology of Stem Cells, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Genomics Institute, University of California, Santa Cruz, Santa Cruz, CA 95064, USA; Center for Molecular Biology of RNA, University of California, Santa Cruz, Santa Cruz, CA 95064, USA. Electronic address: daniel.kim@ucsc.edu.

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Classifications MeSH