Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells

Background How distinct methods of host preconditioning impact the efficacy of adoptively transferred antitumor T helper cells is unknown.Methods CD4+ T cells with a transgenic T-cell receptor that recognize tyrosinase-related peptide (TRP)-1 melanoma antigen were polarized to the T helper 17 (Th17)...

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Main Authors: Gregory B Lesinski, Chrystal M Paulos, Hannah M Knochelmann, Megan M Wyatt, Guillermo O Rangel Rivera, Anna C Cole, Megen C Wittling
Format: Article
Language:English
Published: BMJ Publishing Group 2024-06-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/12/6/e008715.full
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author Gregory B Lesinski
Chrystal M Paulos
Hannah M Knochelmann
Megan M Wyatt
Guillermo O Rangel Rivera
Anna C Cole
Megen C Wittling
author_facet Gregory B Lesinski
Chrystal M Paulos
Hannah M Knochelmann
Megan M Wyatt
Guillermo O Rangel Rivera
Anna C Cole
Megen C Wittling
author_sort Gregory B Lesinski
collection DOAJ
description Background How distinct methods of host preconditioning impact the efficacy of adoptively transferred antitumor T helper cells is unknown.Methods CD4+ T cells with a transgenic T-cell receptor that recognize tyrosinase-related peptide (TRP)-1 melanoma antigen were polarized to the T helper 17 (Th17) phenotype and then transferred into melanoma-bearing mice preconditioned with either total body irradiation or chemotherapy.Results We found that preconditioning mice with a non-myeloablative dose of total body irradiation (TBI of 5 Gy) was more effective than using an equivalently dosed non-myeloablative chemotherapy (cyclophosphamide (CTX) of 200 mg/kg) at augmenting therapeutic activity of antitumor TRP-1 Th17 cells. Antitumor Th17 cells engrafted better following preconditioning with TBI and regressed large established melanoma in all animals. Conversely, only half of mice survived long-term when preconditioned with CTX and infused with anti-melanoma Th17 cells. Interleukin (IL)-17 and interferon-γ, produced by the infused Th17 cells, were detected in animals given either TBI or CTX preconditioning. Interestingly, inflammatory cytokines (granulocyte colony stimulating factor, IL-6, monocyte chemoattractant protein-1, IL-5, and keratinocyte chemoattractant) were significantly elevated in the serum of mice preconditioned with TBI versus CTX after Th17 therapy. The addition of fludarabine (FLU, 200 mg/kg) to CTX (200 mg/kg) improved the antitumor response to the same degree mediated by TBI, whereas FLU alone with Th17 therapy was ineffective.Conclusions Our results indicate, for the first time, that the antitumor response, persistence, and cytokine profiles resulting from Th17 therapy are impacted by the specific regimen of host preconditioning. This work is important for understanding mechanisms that promote long-lived responses by adoptive cellular therapy, particularly as CD4+ based T-cell therapies are now emerging in the clinic.
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spelling doaj-art-fe2e22541bba40599235ed797c618c732025-08-20T03:07:02ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262024-06-0112610.1136/jitc-2023-008715Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cellsGregory B Lesinski0Chrystal M Paulos1Hannah M Knochelmann2Megan M Wyatt3Guillermo O Rangel Rivera4Anna C Cole5Megen C Wittling64Winship Cancer Institute of Emory University, Atlanta, GA, USA1Winship Cancer Institute of Emory University, Atlanta, GA, USAMedicine, Stanford University School of Medicine, Stanford, California, USA3Emory University, Stone Mountain, GA, USASurgery/Oncology & Microbiology/Immunology, Emory University, Atlanta, Georgia, USA4Emory University, Atlanta, GA, USADepartment of Surgery, Emory University, Atlanta, Georgia, USABackground How distinct methods of host preconditioning impact the efficacy of adoptively transferred antitumor T helper cells is unknown.Methods CD4+ T cells with a transgenic T-cell receptor that recognize tyrosinase-related peptide (TRP)-1 melanoma antigen were polarized to the T helper 17 (Th17) phenotype and then transferred into melanoma-bearing mice preconditioned with either total body irradiation or chemotherapy.Results We found that preconditioning mice with a non-myeloablative dose of total body irradiation (TBI of 5 Gy) was more effective than using an equivalently dosed non-myeloablative chemotherapy (cyclophosphamide (CTX) of 200 mg/kg) at augmenting therapeutic activity of antitumor TRP-1 Th17 cells. Antitumor Th17 cells engrafted better following preconditioning with TBI and regressed large established melanoma in all animals. Conversely, only half of mice survived long-term when preconditioned with CTX and infused with anti-melanoma Th17 cells. Interleukin (IL)-17 and interferon-γ, produced by the infused Th17 cells, were detected in animals given either TBI or CTX preconditioning. Interestingly, inflammatory cytokines (granulocyte colony stimulating factor, IL-6, monocyte chemoattractant protein-1, IL-5, and keratinocyte chemoattractant) were significantly elevated in the serum of mice preconditioned with TBI versus CTX after Th17 therapy. The addition of fludarabine (FLU, 200 mg/kg) to CTX (200 mg/kg) improved the antitumor response to the same degree mediated by TBI, whereas FLU alone with Th17 therapy was ineffective.Conclusions Our results indicate, for the first time, that the antitumor response, persistence, and cytokine profiles resulting from Th17 therapy are impacted by the specific regimen of host preconditioning. This work is important for understanding mechanisms that promote long-lived responses by adoptive cellular therapy, particularly as CD4+ based T-cell therapies are now emerging in the clinic.https://jitc.bmj.com/content/12/6/e008715.full
spellingShingle Gregory B Lesinski
Chrystal M Paulos
Hannah M Knochelmann
Megan M Wyatt
Guillermo O Rangel Rivera
Anna C Cole
Megen C Wittling
Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
Journal for ImmunoTherapy of Cancer
title Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
title_full Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
title_fullStr Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
title_full_unstemmed Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
title_short Distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred Th17 cells
title_sort distinct host preconditioning regimens differentially impact the antitumor potency of adoptively transferred th17 cells
url https://jitc.bmj.com/content/12/6/e008715.full
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