Pellino-1 regulates the responses of the airway to viral infection

Journal article


Marsh, Elizabeth K, Prestwich, Elizabeth C, Marriott, Helen M, Williams, Lynne, Hart, Amber R, Muir, Claire F, Parker, Lisa C, Jonker, Marnix R, Heijink, Irene H, Timens, Wim, Fife, Mark, Hussell, Tracy, Hershenson, Marc B, Bentley, J Kelley, Sun, Shao-Cong, Barksby, Ben S, Borthwick, Lee A, Stewart, James P, Dockrell, David H and Sabroe, Ian 2020. Pellino-1 regulates the responses of the airway to viral infection. Frontiers in Cellular and Infection Microbiology. https://doi.org/10.3389/fcimb.2020.00456/full
AuthorsMarsh, Elizabeth K, Prestwich, Elizabeth C, Marriott, Helen M, Williams, Lynne, Hart, Amber R, Muir, Claire F, Parker, Lisa C, Jonker, Marnix R, Heijink, Irene H, Timens, Wim, Fife, Mark, Hussell, Tracy, Hershenson, Marc B, Bentley, J Kelley, Sun, Shao-Cong, Barksby, Ben S, Borthwick, Lee A, Stewart, James P, Dockrell, David H and Sabroe, Ian
Abstract

Exposure to respiratory pathogens is a leading cause of exacerbations of airway diseases such as asthma and chronic obstructive pulmonary disease (COPD). Pellino-1 is an E3 ubiquitin ligase known to regulate virally-induced inflammation. We wished to determine the role of Pellino-1 in the host response to respiratory viruses in health and disease. Pellino-1 expression was examined in bronchial sections from patients with GOLD stage 2 COPD and healthy controls. Primary bronchial epithelial cells (PBECs), in which Pellino-1 expression had been knocked down, were extracellularly challenged with the TLR3 agonist poly(I:C). C57BL/6 Peli1-/- mice and wild type littermates were subjected to intranasal infection with clinically-relevant respiratory viruses; rhinovirus (RV1B) and influenza A. We find that Pellino-1 is expressed in the airways of normal subjects and those with COPD, and that Pellino-1 regulates TLR3 signalling and responses to airways viruses. In particular we observed that knockout of
Pellino‐1 in the murine lung resulted in increased production of proinflammatory cytokines IL‐6 and TNFα upon viral infection, accompanied by enhanced recruitment of immune cells to the airways, without any change in viral replication. Pellino-1 therefore regulates inflammatory airway responses without altering replication of respiratory viruses.

KeywordsPellino-1, Influenza A virus, Rhinovirus, COPD, Asthma, Airway epithelia, Inflammation
Year2020
JournalFrontiers in Cellular and Infection Microbiology
PublisherFrontiers
ISSN2235-2988
Digital Object Identifier (DOI)https://doi.org/10.3389/fcimb.2020.00456/full
Web address (URL)http://hdl.handle.net/10545/625059
http://creativecommons.org/licenses/by-nc-nd/4.0/
hdl:10545/625059
Publication dates31 Aug 2020
Publication process dates
Deposited27 Jul 2020, 09:26
Accepted24 Jul 2020
Rights

Attribution-NonCommercial-NoDerivatives 4.0 International

ContributorsUniversity of Derby, University of Sheffield, University of Groningen, University of Manchester, University of Michigan, University of Texas MD Anderson Cancer Center, Newcastle University, University of Liverpool and University of Edinburgh
File
File Access Level
Open
File
File Access Level
Open
Permalink -

https://repository.derby.ac.uk/item/93684/pellino-1-regulates-the-responses-of-the-airway-to-viral-infection

Download files

  • 9
    total views
  • 0
    total downloads
  • 1
    views this month
  • 0
    downloads this month

Export as

Related outputs

Study to investigate the prevalence of human papillomavirus in Barrett’s oesophagus using a novel screening methodology
Marsh, E.K., White, J.R., Ragunath, K., Whitton, A., Kaye, P. and Knight, G.L. 2022. Study to investigate the prevalence of human papillomavirus in Barrett’s oesophagus using a novel screening methodology. BMJ Open Gastroenterology. 9, pp. 1-5. https://doi.org/10.1136/bmjgast-2021-000840
Human Papillomavirus as a Risk Factor for Oropharyngeal Squamous Cell Carcinoma
Marsh, E. 2022. Human Papillomavirus as a Risk Factor for Oropharyngeal Squamous Cell Carcinoma. in: Harding, J. J. (ed.) Care of Head and Neck Cancer Patients for Dental Hygienists and Dental Therapists Oxford Wiley. pp. 36-43
Airway epithelial cells generate pro-inflammatory tenascin-C and small extracellular vesicles in response to TLR3 stimuli and rhinovirus infection
Mills, Jake, Schwenzer, Anja, Marsh, Elizabeth, Edwards, Michael, Midwood, Kim, Sabroe, Ian and Parker, Lisa 2019. Airway epithelial cells generate pro-inflammatory tenascin-C and small extracellular vesicles in response to TLR3 stimuli and rhinovirus infection. Frontiers in Immunology. https://doi.org/10.3389/fimmu.2019.01987
Pellino-1 regulates immune responses to Haemophilus influenzae in models of inflammatory lung disease.
Hughes, Bethany, Burton, Charlotte, Reese, Abigail, Jabeen, Maisha, Wright, Carl, Khoshaein, Nika, Marsh, Elizabeth, Peachell, Peter, Sun, Shao-Cong, Dockrell, David, Marriott, Helen, Sabroe, Ian, Condliffe, Alison, Prince, Lynne and Willis, Jessica 2019. Pellino-1 regulates immune responses to Haemophilus influenzae in models of inflammatory lung disease. Frontiers in Immunology.
Caenorhabditis elegans, a model organism for investigating immunity.
Marsh, Elizabeth K and May, Robin C 2012. Caenorhabditis elegans, a model organism for investigating immunity. Applied and Environmental Microbiology. https://doi.org/10.1128/AEM.07486-11
The role of protein kinase A regulation of the E6 PDZ-binding domain during the differentiation-dependent life cycle of human papillomavirus type 18.
Delury, Craig P, Marsh, Elizabeth K, James, Claire D, Boon, Siaw Shi, Banks, Lawrence, Knight, Gillian L and Roberts, Sally 2013. The role of protein kinase A regulation of the E6 PDZ-binding domain during the differentiation-dependent life cycle of human papillomavirus type 18. Journal of Virology. https://doi.org/10.1128/JVI.01234-13
Targeted transgene integration overcomes variability of position effects in zebrafish.
Roberts, Jennifer Anne, Miguel-Escalada, Irene, Slovik, Katherine Joan, Walsh, Kathleen Theodora, Hadzhiev, Yavor, Sanges, Remo, Stupka, Elia, Marsh, Elizabeth Kate, Balciuniene, Jorune, Balciunas, Darius and Müller, Ferenc 2014. Targeted transgene integration overcomes variability of position effects in zebrafish. Development. https://doi.org/10.1242/dev.100347
A two-gene balance regulates Salmonella typhimurium tolerance in the nematode Caenorhabditis elegans.
Marsh, Elizabeth K, van den Berg, Maaike C W and May, Robin C 2011. A two-gene balance regulates Salmonella typhimurium tolerance in the nematode Caenorhabditis elegans. PLos ONE. https://doi.org/10.1371/journal.pone.0016839
DUSP10 negatively regulates the inflammatory response to Rhinovirus through IL-1β signalling.
Manley, Grace C. A, Stokes, Clare A, Marsh, Elizabeth K., Sabroe, Ian and Parker, Lisa C 2018. DUSP10 negatively regulates the inflammatory response to Rhinovirus through IL-1β signalling. Journal of Virology. https://doi.org/10.1128/JVI.01659-18
Mitotic control of human papillomavirus genome-containing cells is regulated by the function of the PDZ-binding motif of the E6 oncoprotein.
Marsh, Elizabeth K., Delury, Craig P., Davies, Nicholas J., Weston, Christopher J., Miah, Mohammed A. L., Banks, Lawrence, Parish, Joanna L., Higgs, Martin R. and Roberts, Sally 2017. Mitotic control of human papillomavirus genome-containing cells is regulated by the function of the PDZ-binding motif of the E6 oncoprotein. Oncotarget. https://doi.org/10.18632/oncotarget.14469