CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy

© 2019, © 2019 The Author(s). Published with license by Taylor & Francis Group, LLC. Increasing life expectancy is associated with increased cancer incidence, yet the effect of cancer and anti-cancer treatment on elderly patients and their immune systems is not well understood. Declining T cel...

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Main Authors: Jackaman, Connie, Gardner, J., Tomay, F., Spowart, J., Crabb, Hannah, Dye, Danielle, Fox, Simon, Proksch, Stephen, Metharom, Pat, Dhaliwal, S., Nelson, Delia
Format: Journal Article
Published: Landes Bioscience 2019
Online Access:http://hdl.handle.net/20.500.11937/74358
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author Jackaman, Connie
Gardner, J.
Tomay, F.
Spowart, J.
Crabb, Hannah
Dye, Danielle
Fox, Simon
Proksch, Stephen
Metharom, Pat
Dhaliwal, S.
Nelson, Delia
author_facet Jackaman, Connie
Gardner, J.
Tomay, F.
Spowart, J.
Crabb, Hannah
Dye, Danielle
Fox, Simon
Proksch, Stephen
Metharom, Pat
Dhaliwal, S.
Nelson, Delia
author_sort Jackaman, Connie
building Curtin Institutional Repository
collection Online Access
description © 2019, © 2019 The Author(s). Published with license by Taylor & Francis Group, LLC. Increasing life expectancy is associated with increased cancer incidence, yet the effect of cancer and anti-cancer treatment on elderly patients and their immune systems is not well understood. Declining T cell function with aging in response to infection and vaccination is well documented, however little is known about aged T cell responses to tumor antigens during cancer progression or how these responses are modulated by standard chemotherapy. We examined T cell responses to cancer in aged mice using AE17sOVA mesothelioma in which ovalbumin (OVA) becomes a ‘spy’ tumor antigen containing one dominant (SIINFEKL) and two subdominant (KVVRFDKL and NAIVFKGL) epitopes. Faster progressing tumors in elderly (22–24 months, cf. 60–70 human years) relative to young (2–3 months, human 15–18 years) mice were associated with increased pro-inflammatory cytokines and worsened cancer cachexia. Pentamer staining and an in-vivo cytotoxic T lymphocyte (CTL) assay showed that whilst elderly mice generated a greater number of CD8+ T cells recognizing all epitopes, they exhibited a profound loss of function in their ability to lyse targets expressing the dominant, but not subdominant, epitopes compared to young mice. Chemotherapy was less effective and more toxic in elderly mice however, similar to young mice, chemotherapy expanded CTLs recognizing at least one subdominant epitope in tumors and draining lymph nodes, yet treatment efficacy still required CD8+ T cells. Given the significant dysfunction associated with elderly CTLs recognizing dominant epitopes, our data suggest that responses to subdominant tumor epitopes may become important when elderly hosts with cancer are treated with chemotherapy.
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spelling curtin-20.500.11937-743582023-08-02T06:39:14Z CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy Jackaman, Connie Gardner, J. Tomay, F. Spowart, J. Crabb, Hannah Dye, Danielle Fox, Simon Proksch, Stephen Metharom, Pat Dhaliwal, S. Nelson, Delia © 2019, © 2019 The Author(s). Published with license by Taylor & Francis Group, LLC. Increasing life expectancy is associated with increased cancer incidence, yet the effect of cancer and anti-cancer treatment on elderly patients and their immune systems is not well understood. Declining T cell function with aging in response to infection and vaccination is well documented, however little is known about aged T cell responses to tumor antigens during cancer progression or how these responses are modulated by standard chemotherapy. We examined T cell responses to cancer in aged mice using AE17sOVA mesothelioma in which ovalbumin (OVA) becomes a ‘spy’ tumor antigen containing one dominant (SIINFEKL) and two subdominant (KVVRFDKL and NAIVFKGL) epitopes. Faster progressing tumors in elderly (22–24 months, cf. 60–70 human years) relative to young (2–3 months, human 15–18 years) mice were associated with increased pro-inflammatory cytokines and worsened cancer cachexia. Pentamer staining and an in-vivo cytotoxic T lymphocyte (CTL) assay showed that whilst elderly mice generated a greater number of CD8+ T cells recognizing all epitopes, they exhibited a profound loss of function in their ability to lyse targets expressing the dominant, but not subdominant, epitopes compared to young mice. Chemotherapy was less effective and more toxic in elderly mice however, similar to young mice, chemotherapy expanded CTLs recognizing at least one subdominant epitope in tumors and draining lymph nodes, yet treatment efficacy still required CD8+ T cells. Given the significant dysfunction associated with elderly CTLs recognizing dominant epitopes, our data suggest that responses to subdominant tumor epitopes may become important when elderly hosts with cancer are treated with chemotherapy. 2019 Journal Article http://hdl.handle.net/20.500.11937/74358 10.1080/2162402X.2018.1564452 Landes Bioscience restricted
spellingShingle Jackaman, Connie
Gardner, J.
Tomay, F.
Spowart, J.
Crabb, Hannah
Dye, Danielle
Fox, Simon
Proksch, Stephen
Metharom, Pat
Dhaliwal, S.
Nelson, Delia
CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title_full CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title_fullStr CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title_full_unstemmed CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title_short CD8+ cytotoxic T cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
title_sort cd8+ cytotoxic t cell responses to dominant tumor-associated antigens are profoundly weakened by aging yet subdominant responses retain functionality and expand in response to chemotherapy
url http://hdl.handle.net/20.500.11937/74358