Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial

Background Natural killer (NK) cells are one of the main effector populations of immunotherapy with monoclonal antibody and cytokines, used in combination with chemotherapy to treat children with high-risk neuroblastoma on this phase II trial. However, the impact of chemoimmunotherapy on NK cell kin...

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Main Authors: Rosa Nguyen, David Cullins, Barbara Rooney, Natasha Sahr, April Sykes, Mary Beth McCarville, Sara M Federico, Amanda Sooter, William E Janssen, Gwendolyn Anthony, Michael A Dyer, Alberto S Pappo, Wing H Leung, Wayne L Furman
Format: Article
Language:English
Published: BMJ Publishing Group 2020-05-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/8/1/e000176.full
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author Rosa Nguyen
David Cullins
Barbara Rooney
Natasha Sahr
April Sykes
Mary Beth McCarville
Sara M Federico
Amanda Sooter
William E Janssen
Gwendolyn Anthony
Michael A Dyer
Alberto S Pappo
Wing H Leung
Wayne L Furman
author_facet Rosa Nguyen
David Cullins
Barbara Rooney
Natasha Sahr
April Sykes
Mary Beth McCarville
Sara M Federico
Amanda Sooter
William E Janssen
Gwendolyn Anthony
Michael A Dyer
Alberto S Pappo
Wing H Leung
Wayne L Furman
author_sort Rosa Nguyen
collection DOAJ
description Background Natural killer (NK) cells are one of the main effector populations of immunotherapy with monoclonal antibody and cytokines, used in combination with chemotherapy to treat children with high-risk neuroblastoma on this phase II trial. However, the impact of chemoimmunotherapy on NK cell kinetics, phenotype, and function is understudied.Methods We prospectively examined NK cell properties from 63 children with newly diagnosed neuroblastoma enrolled in a phase II trial (NCT01857934) and correlated our findings with tumor volume reduction after 2 courses of chemoimmunotherapy. NK cell studies were conducted longitudinally during chemoimmunotherapy and autologous hematopoietic cell transplantation (autoHCT) with optional haploidentical NK cell infusion and additional immunotherapy.Results Chemoimmunotherapy led to significant NK cytopenia, but complete NK cell recovery reliably occurred by day 21 of each therapy course as well as after autoHCT. Haploidentical NK cell infusion elevated the NK cell count transiently during autoHCT. NK cell cytotoxicity increased significantly during treatment compared with diagnosis. In addition, NK cells maintained their ability to respond to cytokine stimulation in culture longitudinally. Unsupervised cluster analysis of CD56bright NK cell count and tumor volume at diagnosis and after two courses of chemoimmunotherapy identified two patient groups with distinct primary tumor sizes and therapy responses.Conclusion After profound NK cytopenia due to chemoimmunotherapy, endogenously reconstituted NK cells exhibit enhanced NK cytotoxicity compared with pretherapy measurements. Our data suggest a relationship between CD56bright expression and tumor size before and after two courses of chemoimmunotherapy; however, future studies are necessary to confirm this relationship and its predictive significance.Trial registration number NCT01857934.
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spelling doaj-art-61aa4de3291f4f04b11f55638ec3891c2025-08-20T02:49:52ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262020-05-018110.1136/jitc-2019-000176Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trialRosa Nguyen0David Cullins1Barbara Rooney2Natasha Sahr3April Sykes4Mary Beth McCarville5Sara M Federico6Amanda Sooter7William E Janssen8Gwendolyn Anthony9Michael A Dyer10Alberto S Pappo11Wing H Leung12Wayne L Furman131Department of Pediatrics, University of Maryland, USA5 Department of Bone Marrow Transplantation & Cellular Therapy, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA5 Department of Bone Marrow Transplantation & Cellular Therapy, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA3 Department of Biostatistics, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA3 Department of Biostatistics, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA4 Department of Radiological Sciences, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA1 Oncology Department, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA5 Department of Bone Marrow Transplantation & Cellular Therapy, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA5 Department of Bone Marrow Transplantation & Cellular Therapy, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA1 Oncology Department, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA6 Developmental Neurobiology, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA1 Oncology Department, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA5 Department of Bone Marrow Transplantation & Cellular Therapy, St. Jude Children`s Research Hospital, Memphis, Tennessee, USA1 Oncology Department, St. Jude Children`s Research Hospital, Memphis, Tennessee, USABackground Natural killer (NK) cells are one of the main effector populations of immunotherapy with monoclonal antibody and cytokines, used in combination with chemotherapy to treat children with high-risk neuroblastoma on this phase II trial. However, the impact of chemoimmunotherapy on NK cell kinetics, phenotype, and function is understudied.Methods We prospectively examined NK cell properties from 63 children with newly diagnosed neuroblastoma enrolled in a phase II trial (NCT01857934) and correlated our findings with tumor volume reduction after 2 courses of chemoimmunotherapy. NK cell studies were conducted longitudinally during chemoimmunotherapy and autologous hematopoietic cell transplantation (autoHCT) with optional haploidentical NK cell infusion and additional immunotherapy.Results Chemoimmunotherapy led to significant NK cytopenia, but complete NK cell recovery reliably occurred by day 21 of each therapy course as well as after autoHCT. Haploidentical NK cell infusion elevated the NK cell count transiently during autoHCT. NK cell cytotoxicity increased significantly during treatment compared with diagnosis. In addition, NK cells maintained their ability to respond to cytokine stimulation in culture longitudinally. Unsupervised cluster analysis of CD56bright NK cell count and tumor volume at diagnosis and after two courses of chemoimmunotherapy identified two patient groups with distinct primary tumor sizes and therapy responses.Conclusion After profound NK cytopenia due to chemoimmunotherapy, endogenously reconstituted NK cells exhibit enhanced NK cytotoxicity compared with pretherapy measurements. Our data suggest a relationship between CD56bright expression and tumor size before and after two courses of chemoimmunotherapy; however, future studies are necessary to confirm this relationship and its predictive significance.Trial registration number NCT01857934.https://jitc.bmj.com/content/8/1/e000176.full
spellingShingle Rosa Nguyen
David Cullins
Barbara Rooney
Natasha Sahr
April Sykes
Mary Beth McCarville
Sara M Federico
Amanda Sooter
William E Janssen
Gwendolyn Anthony
Michael A Dyer
Alberto S Pappo
Wing H Leung
Wayne L Furman
Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
Journal for ImmunoTherapy of Cancer
title Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
title_full Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
title_fullStr Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
title_full_unstemmed Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
title_short Longitudinal NK cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase II trial
title_sort longitudinal nk cell kinetics and cytotoxicity in children with neuroblastoma enrolled in a clinical phase ii trial
url https://jitc.bmj.com/content/8/1/e000176.full
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