PUS10-induced tRNA fragmentation impacts retrotransposon-driven inflammation
(2025) In Cell Reports 44(6).- Abstract
Pseudouridine synthases (PUSs) catalyze the isomerization of uridine (U)-to-pseudouridine (Ψ) and have emerging roles in development and disease. How PUSs adapt gene expression under stress remains mostly unexplored. We identify an unconventional role for the Ψ "writer" PUS10 impacting intracellular innate immunity. Using Pus10 knockout mice, we uncover cell-intrinsic upregulation of interferon (IFN) signaling, conferring resistance to inflammation in vivo. Pus10 loss alters tRNA-derived small RNAs (tdRs) abundance, perturbing translation and endogenous retroelements expression. These alterations promote proinflammatory RNA-DNA hybrids accumulation, potentially activating cyclic GMP-AMP synthase (cGAS)-stimulator of interferon gene... (More)
Pseudouridine synthases (PUSs) catalyze the isomerization of uridine (U)-to-pseudouridine (Ψ) and have emerging roles in development and disease. How PUSs adapt gene expression under stress remains mostly unexplored. We identify an unconventional role for the Ψ "writer" PUS10 impacting intracellular innate immunity. Using Pus10 knockout mice, we uncover cell-intrinsic upregulation of interferon (IFN) signaling, conferring resistance to inflammation in vivo. Pus10 loss alters tRNA-derived small RNAs (tdRs) abundance, perturbing translation and endogenous retroelements expression. These alterations promote proinflammatory RNA-DNA hybrids accumulation, potentially activating cyclic GMP-AMP synthase (cGAS)-stimulator of interferon gene (STING). Supplementation with selected tdR pools partly rescues these effects through interactions with RNA processing factors that modulate immune responses, revealing a regulatory circuit that counteracts cell-intrinsic inflammation. By extension, we define a PUS10-specific molecular fingerprint linking its dysregulation to human autoimmune disorders, including inflammatory bowel diseases. Collectively, these findings establish PUS10 as a viral mimicry modulator, with broad implications for innate immune homeostasis and autoimmunity.
(Less)
- author
- organization
-
- LUCC: Lund University Cancer Centre
- StemTherapy: National Initiative on Stem Cells for Regenerative Therapy
- Division of Molecular Hematology (DMH)
- RNA and Stem Cell Biology (research group)
- Stem Cell Center
- Breastcancer-genetics
- Mucosal Immunology (research group)
- Proteomic Hematology (research group)
- LU Profile Area: Light and Materials
- NanoLund: Centre for Nanoscience
- Cell mechanobiology
- Epigenetics and Chromatin Dynamics (research group)
- LTH Profile Area: Photon Science and Technology
- LTH Profile Area: Nanoscience and Semiconductor Technology
- WCMM-Wallenberg Centre for Molecular Medicine
- Developmental Hematopoiesis (research group)
- publishing date
- 2025
- type
- Contribution to journal
- publication status
- published
- subject
- in
- Cell Reports
- volume
- 44
- issue
- 6
- article number
- 115735
- publisher
- Cell Press
- external identifiers
-
- scopus:105005368837
- pmid:40402745
- ISSN
- 2211-1247
- DOI
- 10.1016/j.celrep.2025.115735
- language
- English
- LU publication?
- yes
- additional info
- Copyright © 2025 The Author(s). Published by Elsevier Inc. All rights reserved.
- id
- 95dd49f1-77aa-4012-9452-be901fa6e1f8
- date added to LUP
- 2025-05-27 14:04:14
- date last changed
- 2025-07-09 07:46:16
@article{95dd49f1-77aa-4012-9452-be901fa6e1f8, abstract = {{<p>Pseudouridine synthases (PUSs) catalyze the isomerization of uridine (U)-to-pseudouridine (Ψ) and have emerging roles in development and disease. How PUSs adapt gene expression under stress remains mostly unexplored. We identify an unconventional role for the Ψ "writer" PUS10 impacting intracellular innate immunity. Using Pus10 knockout mice, we uncover cell-intrinsic upregulation of interferon (IFN) signaling, conferring resistance to inflammation in vivo. Pus10 loss alters tRNA-derived small RNAs (tdRs) abundance, perturbing translation and endogenous retroelements expression. These alterations promote proinflammatory RNA-DNA hybrids accumulation, potentially activating cyclic GMP-AMP synthase (cGAS)-stimulator of interferon gene (STING). Supplementation with selected tdR pools partly rescues these effects through interactions with RNA processing factors that modulate immune responses, revealing a regulatory circuit that counteracts cell-intrinsic inflammation. By extension, we define a PUS10-specific molecular fingerprint linking its dysregulation to human autoimmune disorders, including inflammatory bowel diseases. Collectively, these findings establish PUS10 as a viral mimicry modulator, with broad implications for innate immune homeostasis and autoimmunity.</p>}}, author = {{Madej, Magdalena and Ngoc, Phuong Cao Thi and Muthukumar, Sowndarya and Konturek-Cieśla, Anna and Tucciarone, Silvia and Germanos, Alexandre and Ashworth, Christian and Kotarsky, Knut and Ghosh, Sudip and Fan, Zhimeng and Fritz, Helena and Pascual-Gonzalez, Izei and Huerta, Alain and Guzzi, Nicola and Colazzo, Anita and Beneventi, Giulia and Lee, Hang-Mao and Cieśla, Maciej and Douse, Christopher and Kato, Hiroki and Swaminathan, Vinay and Agace, William W and Castellanos-Rubio, Ainara and Salomoni, Paolo and Bryder, David and Bellodi, Cristian}}, issn = {{2211-1247}}, language = {{eng}}, number = {{6}}, publisher = {{Cell Press}}, series = {{Cell Reports}}, title = {{PUS10-induced tRNA fragmentation impacts retrotransposon-driven inflammation}}, url = {{http://dx.doi.org/10.1016/j.celrep.2025.115735}}, doi = {{10.1016/j.celrep.2025.115735}}, volume = {{44}}, year = {{2025}}, }