Cargando…

Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function

TCR-gene-transfer is an efficient strategy to produce therapeutic T cells of defined antigen specificity. However, there are substantial variations in the cell surface expression levels of human TCRs, which can impair the function of engineered T cells. Here we demonstrate that substitutions of 3 am...

Descripción completa

Detalles Bibliográficos
Autores principales: Thomas, Sharyn, Mohammed, Fiyaz, Reijmers, Rogier M., Woolston, Annemarie, Stauss, Theresa, Kennedy, Alan, Stirling, David, Holler, Angelika, Green, Louisa, Jones, David, Matthews, Katherine K., Price, David A., Chain, Benjamin M., Heemskerk, Mirjam H. M., Morris, Emma C., Willcox, Benjamin E., Stauss, Hans J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773850/
https://www.ncbi.nlm.nih.gov/pubmed/31575864
http://dx.doi.org/10.1038/s41467-019-12441-w
_version_ 1783455969266630656
author Thomas, Sharyn
Mohammed, Fiyaz
Reijmers, Rogier M.
Woolston, Annemarie
Stauss, Theresa
Kennedy, Alan
Stirling, David
Holler, Angelika
Green, Louisa
Jones, David
Matthews, Katherine K.
Price, David A.
Chain, Benjamin M.
Heemskerk, Mirjam H. M.
Morris, Emma C.
Willcox, Benjamin E.
Stauss, Hans J.
author_facet Thomas, Sharyn
Mohammed, Fiyaz
Reijmers, Rogier M.
Woolston, Annemarie
Stauss, Theresa
Kennedy, Alan
Stirling, David
Holler, Angelika
Green, Louisa
Jones, David
Matthews, Katherine K.
Price, David A.
Chain, Benjamin M.
Heemskerk, Mirjam H. M.
Morris, Emma C.
Willcox, Benjamin E.
Stauss, Hans J.
author_sort Thomas, Sharyn
collection PubMed
description TCR-gene-transfer is an efficient strategy to produce therapeutic T cells of defined antigen specificity. However, there are substantial variations in the cell surface expression levels of human TCRs, which can impair the function of engineered T cells. Here we demonstrate that substitutions of 3 amino acid residues in the framework of the TCR variable domains consistently increase the expression of human TCRs on the surface of engineered T cells.The modified TCRs mediate enhanced T cell proliferation, cytokine production and cytotoxicity, while reducing the peptide concentration required for triggering effector function up to 3000-fold. Adoptive transfer experiments in mice show that modified TCRs control tumor growth more efficiently than wild-type TCRs. Our data indicate that simple variable domain modifications at a distance from the antigen-binding loops lead to increased TCR expression and improved effector function. This finding provides a generic platform to optimize the efficacy of TCR gene therapy in humans.
format Online
Article
Text
id pubmed-6773850
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-67738502019-10-03 Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function Thomas, Sharyn Mohammed, Fiyaz Reijmers, Rogier M. Woolston, Annemarie Stauss, Theresa Kennedy, Alan Stirling, David Holler, Angelika Green, Louisa Jones, David Matthews, Katherine K. Price, David A. Chain, Benjamin M. Heemskerk, Mirjam H. M. Morris, Emma C. Willcox, Benjamin E. Stauss, Hans J. Nat Commun Article TCR-gene-transfer is an efficient strategy to produce therapeutic T cells of defined antigen specificity. However, there are substantial variations in the cell surface expression levels of human TCRs, which can impair the function of engineered T cells. Here we demonstrate that substitutions of 3 amino acid residues in the framework of the TCR variable domains consistently increase the expression of human TCRs on the surface of engineered T cells.The modified TCRs mediate enhanced T cell proliferation, cytokine production and cytotoxicity, while reducing the peptide concentration required for triggering effector function up to 3000-fold. Adoptive transfer experiments in mice show that modified TCRs control tumor growth more efficiently than wild-type TCRs. Our data indicate that simple variable domain modifications at a distance from the antigen-binding loops lead to increased TCR expression and improved effector function. This finding provides a generic platform to optimize the efficacy of TCR gene therapy in humans. Nature Publishing Group UK 2019-10-01 /pmc/articles/PMC6773850/ /pubmed/31575864 http://dx.doi.org/10.1038/s41467-019-12441-w Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Thomas, Sharyn
Mohammed, Fiyaz
Reijmers, Rogier M.
Woolston, Annemarie
Stauss, Theresa
Kennedy, Alan
Stirling, David
Holler, Angelika
Green, Louisa
Jones, David
Matthews, Katherine K.
Price, David A.
Chain, Benjamin M.
Heemskerk, Mirjam H. M.
Morris, Emma C.
Willcox, Benjamin E.
Stauss, Hans J.
Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title_full Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title_fullStr Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title_full_unstemmed Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title_short Framework engineering to produce dominant T cell receptors with enhanced antigen-specific function
title_sort framework engineering to produce dominant t cell receptors with enhanced antigen-specific function
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773850/
https://www.ncbi.nlm.nih.gov/pubmed/31575864
http://dx.doi.org/10.1038/s41467-019-12441-w
work_keys_str_mv AT thomassharyn frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT mohammedfiyaz frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT reijmersrogierm frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT woolstonannemarie frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT stausstheresa frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT kennedyalan frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT stirlingdavid frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT hollerangelika frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT greenlouisa frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT jonesdavid frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT matthewskatherinek frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT pricedavida frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT chainbenjaminm frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT heemskerkmirjamhm frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT morrisemmac frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT willcoxbenjamine frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction
AT stausshansj frameworkengineeringtoproducedominanttcellreceptorswithenhancedantigenspecificfunction