Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

Abstract

The RNA cap methyltransferase CMTR1 methylates the first transcribed nucleotide of RNA polymerase II transcripts, impacting gene expression mechanisms, including during innate immune responses. Using mass spectrometry, we identify a multiply phosphorylated region of CMTR1 (phospho-patch [P-Patch]), which is a substrate for the kinase CK2 (casein kinase II). CMTR1 phosphorylation alters intramolecular interactions, increases recruitment to RNA polymerase II, and promotes RNA cap methylation. P-Patch phosphorylation occurs during the G1 phase of the cell cycle, recruiting CMTR1 to RNA polymerase II during a period of rapid transcription and RNA cap formation. CMTR1 phosphorylation is required for the expression of specific RNAs, including ribosomal protein gene transcripts, and promotes cell proliferation. CMTR1 phosphorylation is also required for interferon-stimulated gene expression. The cap-snatching virus, influenza A, utilizes host CMTR1 phosphorylation to produce the caps required for virus production and infection. We present an RNA cap methylation control mechanism whereby CK2 controls CMTR1, enhancing co-transcriptional capping.

People
Lukoszek, Radoslaw
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

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Inesta-Vaquera, Francisco
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

See full publications list
Brett, Natasha J.M.
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

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Liang, Shang
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

See full publications list
Hepburn, Lydia A.
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

See full publications list
Hughes, David J.
Author

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

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Pirillo, Chiara
Author

Hargrave, Kerrie E. and Worrell, Julie C. and Pirillo, Chiara and Brennan, Euan and Masdefiol Garriga, Andreu and Gray, Joshua I. and Purnell, Thomas and Roberts, Edward W. and MacLeod, Megan K.L. (2024) Lung influenza virus specific memory CD4 T cell location and optimal cytokine production are dependent on interactions with lung antigen-presenting cells. Mucosal Immunology, 17 (5). pp. 843-857. ISSN 1933-0219

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

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Roberts, Edward W.
Author

Samarakoon, Youhan and Yelland, Tamas and Garcia-Gonzalez, Esther and Justo-Junior, Amauri da Silva and Mahmood, Mahnoor and Manoharan, Anand and Patterson, Shaun and Serafin, Valentina and Gammage, Payam A. and Marmiroli, Sandra and Halsey, Christina and Ismail, Shehab and Roberts, Edward W. (2025) UNC119 regulates T-cell receptor signalling in primary T cells and T acute lymphocytic leukaemia. Life Science Alliance, 8 (3): e202403066. ISSN 2575-1077

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

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Cowling, Victoria H.
Author

Xavier, Vanessa and Martinelli, Silvia and Corbyn, Ryan and Pennie, Rachel and Rakovic, Kai and Powley, Ian R. and Officer-Jones, Leah and Ruscica, Vincenzo and Galloway, Alison and Carlin, Leo M. and Cowling, Victoria H. and Le Quesne, John and Martinou, Jean-Claude and MacVicar, Thomas (2024) Mitochondrial double-stranded RNA homeostasis depends on cell-cycle progression. Life Science Alliance, 7 (11): e202402764. ISSN 2575-1077

Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H. (2024) CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection. Cell Reports, 43 (7): 114405. ISSN 2639-1856

Knop, Katarzyna and Gomez-Moreira, Carolina and Galloway, Alison and Ditsova, Dimitrinka and Cowling, Victoria H. (2024) RAM is upregulated during T cell activation and is required for RNA cap formation and gene expression. Discovery Immunology, 3 (1): kyad021. ISSN 2754-2483

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Information
Title:
CK2 phosphorylation of CMTR1 promotes RNA cap formation and influenza virus infection
Creators:
Lukoszek, Radoslaw and Inesta-Vaquera, Francisco and Brett, Natasha J.M. and Liang, Shang and Hepburn, Lydia A. and Hughes, David J. and Pirillo, Chiara and Roberts, Edward W. and Cowling, Victoria H.
Identification Number:
10.1016/j.celrep.2024.114405
Date:
23 July 2024
Divisions:
College of Medical Veterinary and Life Sciences > School of Cancer Sciences
Publisher:
Cell Press
Additional Information:
This work was supported by Cancer Research UK core grant number A17196/A31287 to the CRUK Scotland Institute and CTRQQR-2021\100006 to the CRUK Scotland Centre. Research was funded by European Research Council Award 769080 TCAPS, Medical Research Council Senior Fellowship MR/K024213/1, a Lister Research Prize Fellowship, a Wellcome Trust PhD studentship 097462/Z/11/Z, Royal Society Wolfson Research Merit Award WRM\R1\180008, Wellcome Trust Investigator Award 219416/A/19/Z, and Wellcome Trust GRE Centre Award 097945/Z/11/Z.
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URI:
https://pub.demo35.eprints-hosting.org/id/eprint/191
Item Type:
Article
Depositing User:
Unnamed user with email ejo1f20@soton.ac.uk
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Date Deposited:
11 Jun 2025 16:35
Revision:
14
Last Modified:
12 Jun 2025 11:53
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