Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells

<h3>Background</h3><p dir="ltr">The pleiotropic cytokine, transforming growth factor (TGF)-β, and CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> regulatory T cells (Tregs) play a critical role in actively suppressing antitumor immune...

وصف كامل

محفوظ في:
التفاصيل البيبلوغرافية
المؤلف الرئيسي: Magdalena J. Polanczyk (14153283) (author)
مؤلفون آخرون: Edwin Walker (4705993) (author), Daniel Haley (14153286) (author), Bella S. Guerrouahen (14153289) (author), Emmanuel T. Akporiaye (8335038) (author)
منشور في: 2019
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_version_ 1864513555881000960
author Magdalena J. Polanczyk (14153283)
author2 Edwin Walker (4705993)
Daniel Haley (14153286)
Bella S. Guerrouahen (14153289)
Emmanuel T. Akporiaye (8335038)
author2_role author
author
author
author
author_facet Magdalena J. Polanczyk (14153283)
Edwin Walker (4705993)
Daniel Haley (14153286)
Bella S. Guerrouahen (14153289)
Emmanuel T. Akporiaye (8335038)
author_role author
dc.creator.none.fl_str_mv Magdalena J. Polanczyk (14153283)
Edwin Walker (4705993)
Daniel Haley (14153286)
Bella S. Guerrouahen (14153289)
Emmanuel T. Akporiaye (8335038)
dc.date.none.fl_str_mv 2019-07-09T06:00:00Z
dc.identifier.none.fl_str_mv 10.1186/s12967-019-1967-3
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Blockade_of_TGF-_signaling_to_enhance_the_antitumor_response_is_accompanied_by_dysregulation_of_the_functional_activity_of_CD4_CD25_Foxp3_and_CD4_CD25_Foxp3_T_cells/21598446
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Immunology
Medical biochemistry and metabolomics
Oncology and carcinogenesis
TGF-β
SM16
Mice
Treg subsets
Anti-tumor response
dc.title.none.fl_str_mv Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <h3>Background</h3><p dir="ltr">The pleiotropic cytokine, transforming growth factor (TGF)-β, and CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> regulatory T cells (Tregs) play a critical role in actively suppressing antitumor immune responses. Evidence shows that TGF-β produced by tumor cells promotes tolerance via expansion of Tregs. Our group previously demonstrated that blockade of TGF-β signaling with a small molecule TGF-β receptor I antagonist (SM16) inhibited primary and metastatic tumor growth in a T cell dependent fashion. In the current study, we evaluated the effect of SM16 on Treg generation and function. </p><h3>Methods</h3><p dir="ltr">Using BALB/c, FoxP3eGFP and Rag<sup>−/−</sup> mice, we performed FACS analysis to determine if SM16 blocked de novo TGF-β-induced Treg generation in vitro and in vivo. CD4<sup>+</sup> T cells from lymph node and spleen were isolated from control mice or mice maintained on SM16 diet, and flow cytometry analysis was used to detect the frequency of CD4<sup>+</sup>CD25<sup>−</sup>FoxP3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>+</sup>FoxP3<sup>+</sup> T cells. In vitro suppression assays were used to determine the ability to suppress naive T cell proliferation in vitro of both CD4<sup>+</sup>CD25<sup>+</sup>FoxP3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>FoxP3<sup>+</sup> T cell sub-populations. We then examined whether SM16 diet exerted an inhibitory effect on primary tumor growth and correlated with changes in FoxP3<sup>+</sup>expression. ELISA analysis was used to measure IFN-γ levels after 72 h co-culture of CD4<sup>+</sup>CD25<sup>+</sup> T cells from tumor-bearing mice on control or SM16 diet with CD4<sup>+</sup>CD25<sup>−</sup> T cells from naive donors. </p><h3>Results</h3><p dir="ltr">SM16 abrogates TGF-β-induced Treg generation in vitro but does not prevent global homeostatic expansion of CD4<sup>+</sup>T cell sub-populations in vivo. Instead, SM16 treatment causes expansion of a population of CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> Treg-like cells without significantly altering the overall frequency of Treg in lymphoreplete naive and tumor-bearing mice. Importantly, both the CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells and the CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> Tregs in mice receiving SM16 diet exhibited diminished ability to suppress naive T cell proliferation in vitro compared to Treg from mice on control diet. </p><h3>Conclusions</h3><p dir="ltr">These findings suggest that blockade of TGF-β signaling is a potentially useful strategy for blunting Treg function to enhance the anti-tumor response. Our data further suggest that the overall dampening of Treg function may involve the expansion of a quiescent Treg precursor population, which is CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup>.</p><h2>Other Information</h2><p dir="ltr">Published in: Journal of Translational Medicine<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="http://dx.doi.org/10.1186/s12967-019-1967-3" target="_blank">http://dx.doi.org/10.1186/s12967-019-1967-3</a></p>
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network_acronym_str Manara2
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oai_identifier_str oai:figshare.com:article/21598446
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spelling Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cellsMagdalena J. Polanczyk (14153283)Edwin Walker (4705993)Daniel Haley (14153286)Bella S. Guerrouahen (14153289)Emmanuel T. Akporiaye (8335038)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesImmunologyMedical biochemistry and metabolomicsOncology and carcinogenesisTGF-βSM16MiceTreg subsetsAnti-tumor response<h3>Background</h3><p dir="ltr">The pleiotropic cytokine, transforming growth factor (TGF)-β, and CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> regulatory T cells (Tregs) play a critical role in actively suppressing antitumor immune responses. Evidence shows that TGF-β produced by tumor cells promotes tolerance via expansion of Tregs. Our group previously demonstrated that blockade of TGF-β signaling with a small molecule TGF-β receptor I antagonist (SM16) inhibited primary and metastatic tumor growth in a T cell dependent fashion. In the current study, we evaluated the effect of SM16 on Treg generation and function. </p><h3>Methods</h3><p dir="ltr">Using BALB/c, FoxP3eGFP and Rag<sup>−/−</sup> mice, we performed FACS analysis to determine if SM16 blocked de novo TGF-β-induced Treg generation in vitro and in vivo. CD4<sup>+</sup> T cells from lymph node and spleen were isolated from control mice or mice maintained on SM16 diet, and flow cytometry analysis was used to detect the frequency of CD4<sup>+</sup>CD25<sup>−</sup>FoxP3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>+</sup>FoxP3<sup>+</sup> T cells. In vitro suppression assays were used to determine the ability to suppress naive T cell proliferation in vitro of both CD4<sup>+</sup>CD25<sup>+</sup>FoxP3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>FoxP3<sup>+</sup> T cell sub-populations. We then examined whether SM16 diet exerted an inhibitory effect on primary tumor growth and correlated with changes in FoxP3<sup>+</sup>expression. ELISA analysis was used to measure IFN-γ levels after 72 h co-culture of CD4<sup>+</sup>CD25<sup>+</sup> T cells from tumor-bearing mice on control or SM16 diet with CD4<sup>+</sup>CD25<sup>−</sup> T cells from naive donors. </p><h3>Results</h3><p dir="ltr">SM16 abrogates TGF-β-induced Treg generation in vitro but does not prevent global homeostatic expansion of CD4<sup>+</sup>T cell sub-populations in vivo. Instead, SM16 treatment causes expansion of a population of CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> Treg-like cells without significantly altering the overall frequency of Treg in lymphoreplete naive and tumor-bearing mice. Importantly, both the CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells and the CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> Tregs in mice receiving SM16 diet exhibited diminished ability to suppress naive T cell proliferation in vitro compared to Treg from mice on control diet. </p><h3>Conclusions</h3><p dir="ltr">These findings suggest that blockade of TGF-β signaling is a potentially useful strategy for blunting Treg function to enhance the anti-tumor response. Our data further suggest that the overall dampening of Treg function may involve the expansion of a quiescent Treg precursor population, which is CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup>.</p><h2>Other Information</h2><p dir="ltr">Published in: Journal of Translational Medicine<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="http://dx.doi.org/10.1186/s12967-019-1967-3" target="_blank">http://dx.doi.org/10.1186/s12967-019-1967-3</a></p>2019-07-09T06:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1186/s12967-019-1967-3https://figshare.com/articles/journal_contribution/Blockade_of_TGF-_signaling_to_enhance_the_antitumor_response_is_accompanied_by_dysregulation_of_the_functional_activity_of_CD4_CD25_Foxp3_and_CD4_CD25_Foxp3_T_cells/21598446CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/215984462019-07-09T06:00:00Z
spellingShingle Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
Magdalena J. Polanczyk (14153283)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Immunology
Medical biochemistry and metabolomics
Oncology and carcinogenesis
TGF-β
SM16
Mice
Treg subsets
Anti-tumor response
status_str publishedVersion
title Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
title_full Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
title_fullStr Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
title_full_unstemmed Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
title_short Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
title_sort Blockade of TGF-β signaling to enhance the antitumor response is accompanied by dysregulation of the functional activity of CD4<sup>+</sup>CD25<sup>+</sup>Foxp3<sup>+</sup> and CD4<sup>+</sup>CD25<sup>−</sup>Foxp3<sup>+</sup> T cells
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Immunology
Medical biochemistry and metabolomics
Oncology and carcinogenesis
TGF-β
SM16
Mice
Treg subsets
Anti-tumor response