Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy

Oncolytic viruses often face challenges in achieving optimal antitumor immunity as standalone therapies. The penton base RGD-integrin interactions play a significant role in wild-type adenovirus-induced innate immune responses. To modify these responses, we present ISC301, a novel oncolytic adenovir...

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Main Authors: Alvaro Morales-Molina, Miguel Angel Rodriguez-Milla, Patricia Garcia-Rodriguez, Laura Hidalgo, Ramon Alemany, Javier Garcia-Castro
Format: Article
Language:English
Published: Elsevier 2024-09-01
Series:Molecular Therapy: Oncology
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Online Access:http://www.sciencedirect.com/science/article/pii/S295032992400105X
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author Alvaro Morales-Molina
Miguel Angel Rodriguez-Milla
Patricia Garcia-Rodriguez
Laura Hidalgo
Ramon Alemany
Javier Garcia-Castro
author_facet Alvaro Morales-Molina
Miguel Angel Rodriguez-Milla
Patricia Garcia-Rodriguez
Laura Hidalgo
Ramon Alemany
Javier Garcia-Castro
author_sort Alvaro Morales-Molina
collection DOAJ
description Oncolytic viruses often face challenges in achieving optimal antitumor immunity as standalone therapies. The penton base RGD-integrin interactions play a significant role in wild-type adenovirus-induced innate immune responses. To modify these responses, we present ISC301, a novel oncolytic adenovirus engineered by deleting the natural RGD motifs in the penton base while incorporating artificial RGD motifs in the fiber knobs. ISC301 demonstrated comparable in vitro infectivity, cytotoxic effects, and signaling profiles across various cell types to its parental ICOVIR-5, which retains the penton base RGD motif. In immunodeficient and immunocompetent mouse models, ISC301 exhibited similar in vivo antitumor efficacy to ICOVIR-5. However, ISC301 induced higher intratumoral inflammation through NF-κB activation, leading to increased levels of tumor-infiltrating leukocytes and higher proportion of cytotoxic CD8+ T cells. In addition, ISC301 elicits a heightened pro-inflammatory response in peripheral blood. Importantly, when combined with CAR T cell therapy, ISC301 exhibited superior antitumor efficacy, surpassing monotherapy outcomes. These findings emphasize the impact of adenoviral modifications on antitumor immune responses. The deletion of penton base RGD motifs enhances ISC301’s pro-inflammatory profile and boosts CAR T cell therapy efficacy. This study enhances understanding of oncolytic virus engineering strategies, positioning ISC301 as a promising candidate for combined immunotherapeutic approaches in cancer treatment.
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spelling doaj-art-f889f634fb8d45d19137a418f077a9bb2024-11-24T04:15:47ZengElsevierMolecular Therapy: Oncology2950-32992024-09-01323200863Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapyAlvaro Morales-Molina0Miguel Angel Rodriguez-Milla1Patricia Garcia-Rodriguez2Laura Hidalgo3Ramon Alemany4Javier Garcia-Castro5Cellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, SpainCellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, SpainCellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, Spain; Universidad Nacional de Educación a Distancia, UNED, 28015 Madrid, SpainCellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, SpainOncobell and ProCure Programs, IDIBELL-Institut Català d’Oncologia, L’Hospitalet de Llobregat, 08908 Barcelona, SpainCellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, Spain; Instituto de Investigación de Enfermedades Raras (IIER) & Departamento de Desarrollo de Medicamentos de Terapias Avanzadas (DDMTA), Instituto de Salud Carlos III, 28220 Madrid, Spain; Corresponding author: Javier Garcia-Castro, Cellular Biotechnology Unit, Instituto de Salud Carlos III, 28220 Madrid, Spain.Oncolytic viruses often face challenges in achieving optimal antitumor immunity as standalone therapies. The penton base RGD-integrin interactions play a significant role in wild-type adenovirus-induced innate immune responses. To modify these responses, we present ISC301, a novel oncolytic adenovirus engineered by deleting the natural RGD motifs in the penton base while incorporating artificial RGD motifs in the fiber knobs. ISC301 demonstrated comparable in vitro infectivity, cytotoxic effects, and signaling profiles across various cell types to its parental ICOVIR-5, which retains the penton base RGD motif. In immunodeficient and immunocompetent mouse models, ISC301 exhibited similar in vivo antitumor efficacy to ICOVIR-5. However, ISC301 induced higher intratumoral inflammation through NF-κB activation, leading to increased levels of tumor-infiltrating leukocytes and higher proportion of cytotoxic CD8+ T cells. In addition, ISC301 elicits a heightened pro-inflammatory response in peripheral blood. Importantly, when combined with CAR T cell therapy, ISC301 exhibited superior antitumor efficacy, surpassing monotherapy outcomes. These findings emphasize the impact of adenoviral modifications on antitumor immune responses. The deletion of penton base RGD motifs enhances ISC301’s pro-inflammatory profile and boosts CAR T cell therapy efficacy. This study enhances understanding of oncolytic virus engineering strategies, positioning ISC301 as a promising candidate for combined immunotherapeutic approaches in cancer treatment.http://www.sciencedirect.com/science/article/pii/S295032992400105Xoncolytic virusRGDpenton baseadenovirusNKG2DT cell
spellingShingle Alvaro Morales-Molina
Miguel Angel Rodriguez-Milla
Patricia Garcia-Rodriguez
Laura Hidalgo
Ramon Alemany
Javier Garcia-Castro
Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
Molecular Therapy: Oncology
oncolytic virus
RGD
penton base
adenovirus
NKG2D
T cell
title Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
title_full Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
title_fullStr Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
title_full_unstemmed Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
title_short Deletion of the RGD motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined CAR T cell therapy
title_sort deletion of the rgd motif from the penton base in oncolytic adenoviruses enhances antitumor efficacy of combined car t cell therapy
topic oncolytic virus
RGD
penton base
adenovirus
NKG2D
T cell
url http://www.sciencedirect.com/science/article/pii/S295032992400105X
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