Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity

Stressful conditions in the harsh tumor microenvironment induce autophagy in cancer cells as a mechanism to promote their survival. However, autophagy also causes post-translational modification of proteins that are recognized by the immune system. In particular, modified self-antigens can trigger C...

Full description

Bibliographic Details
Main Authors: Brentville, Victoria A., Metheringham, Rachael L., Gunn, Barbara, Symonds, Peter, Daniels, Ian, Gijon, Mohamed, Cook, Katherine, Xue, Wei, Durrant, Lindy
Format: Article
Published: American Association for Cancer Research 2016
Online Access:https://eprints.nottingham.ac.uk/49781/
_version_ 1848798075839053824
author Brentville, Victoria A.
Metheringham, Rachael L.
Gunn, Barbara
Symonds, Peter
Daniels, Ian
Gijon, Mohamed
Cook, Katherine
Xue, Wei
Durrant, Lindy
author_facet Brentville, Victoria A.
Metheringham, Rachael L.
Gunn, Barbara
Symonds, Peter
Daniels, Ian
Gijon, Mohamed
Cook, Katherine
Xue, Wei
Durrant, Lindy
author_sort Brentville, Victoria A.
building Nottingham Research Data Repository
collection Online Access
description Stressful conditions in the harsh tumor microenvironment induce autophagy in cancer cells as a mechanism to promote their survival. However, autophagy also causes post-translational modification of proteins that are recognized by the immune system. In particular, modified self-antigens can trigger CD4(+) T-cell responses that might be exploited to boost antitumor immune defenses. In this study, we investigated the ability of CD4 cells to target tumor-specific self-antigens modified by citrullination, which converts arginine residues in proteins to citrulline. Focusing on the intermediate filament protein vimentin, which is frequently citrullinated in cells during epithelial-to-mesenchymal transition of metastasizing epithelial tumors, we generated citrullinated vimentin peptides for immunization experiments in mice. Immunization with these peptides induced IFNγ- and granzyme B-secreting CD4 T cells in response to autophagic tumor targets. Remarkably, a single immunization with modified peptide, up to 14 days after tumor implant, resulted in long-term survival in 60% to 90% of animals with no associated toxicity. This antitumor response was dependent on CD4 cells and not CD8(+) T cells. These results show how CD4 cells can mediate potent antitumor responses against modified self-epitopes presented on tumor cells, and they illustrate for the first time how the citrullinated peptides may offer especially attractive vaccine targets for cancer therapy.
first_indexed 2025-11-14T20:14:01Z
format Article
id nottingham-49781
institution University of Nottingham Malaysia Campus
institution_category Local University
last_indexed 2025-11-14T20:14:01Z
publishDate 2016
publisher American Association for Cancer Research
recordtype eprints
repository_type Digital Repository
spelling nottingham-497812020-05-04T17:28:34Z https://eprints.nottingham.ac.uk/49781/ Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity Brentville, Victoria A. Metheringham, Rachael L. Gunn, Barbara Symonds, Peter Daniels, Ian Gijon, Mohamed Cook, Katherine Xue, Wei Durrant, Lindy Stressful conditions in the harsh tumor microenvironment induce autophagy in cancer cells as a mechanism to promote their survival. However, autophagy also causes post-translational modification of proteins that are recognized by the immune system. In particular, modified self-antigens can trigger CD4(+) T-cell responses that might be exploited to boost antitumor immune defenses. In this study, we investigated the ability of CD4 cells to target tumor-specific self-antigens modified by citrullination, which converts arginine residues in proteins to citrulline. Focusing on the intermediate filament protein vimentin, which is frequently citrullinated in cells during epithelial-to-mesenchymal transition of metastasizing epithelial tumors, we generated citrullinated vimentin peptides for immunization experiments in mice. Immunization with these peptides induced IFNγ- and granzyme B-secreting CD4 T cells in response to autophagic tumor targets. Remarkably, a single immunization with modified peptide, up to 14 days after tumor implant, resulted in long-term survival in 60% to 90% of animals with no associated toxicity. This antitumor response was dependent on CD4 cells and not CD8(+) T cells. These results show how CD4 cells can mediate potent antitumor responses against modified self-epitopes presented on tumor cells, and they illustrate for the first time how the citrullinated peptides may offer especially attractive vaccine targets for cancer therapy. American Association for Cancer Research 2016-02-01 Article PeerReviewed Brentville, Victoria A., Metheringham, Rachael L., Gunn, Barbara, Symonds, Peter, Daniels, Ian, Gijon, Mohamed, Cook, Katherine, Xue, Wei and Durrant, Lindy (2016) Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity. Cancer Research, 76 (3). pp. 548-560. ISSN 1538-7445 http://cancerres.aacrjournals.org/content/76/3/548 doi:10.1158/0008-5472.CAN-15-1085 doi:10.1158/0008-5472.CAN-15-1085
spellingShingle Brentville, Victoria A.
Metheringham, Rachael L.
Gunn, Barbara
Symonds, Peter
Daniels, Ian
Gijon, Mohamed
Cook, Katherine
Xue, Wei
Durrant, Lindy
Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title_full Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title_fullStr Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title_full_unstemmed Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title_short Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity
title_sort citrullinated vimentin presented on mhc-ii in tumor cells is a target for cd4+ t-cell-mediated antitumor immunity
url https://eprints.nottingham.ac.uk/49781/
https://eprints.nottingham.ac.uk/49781/
https://eprints.nottingham.ac.uk/49781/