Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy
Glioma is the most common primary brain tumor, characterized by a consistently high patient mortality rate and a dismal prognosis affecting both survival and quality of life. Substantial evidence underscores the vital role of the immune system in eradicating tumors effectively and preventing metasta...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1299064/full |
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| author | Tatiana A. Mishchenko Victoria D. Turubanova Victoria D. Turubanova Ekaterina N. Gorshkova Olga Krysko Maria V. Vedunova Maria V. Vedunova Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko |
| author_facet | Tatiana A. Mishchenko Victoria D. Turubanova Victoria D. Turubanova Ekaterina N. Gorshkova Olga Krysko Maria V. Vedunova Maria V. Vedunova Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko |
| author_sort | Tatiana A. Mishchenko |
| collection | DOAJ |
| description | Glioma is the most common primary brain tumor, characterized by a consistently high patient mortality rate and a dismal prognosis affecting both survival and quality of life. Substantial evidence underscores the vital role of the immune system in eradicating tumors effectively and preventing metastasis, underscoring the importance of cancer immunotherapy which could potentially address the challenges in glioma therapy. Although glioma immunotherapies have shown promise in preclinical and early-phase clinical trials, they face specific limitations and challenges that have hindered their success in further phase III trials. Resistance to therapy has been a major challenge across many experimental approaches, and as of now, no immunotherapies have been approved. In addition, there are several other limitations facing glioma immunotherapy in clinical trials, such as high intra- and inter-tumoral heterogeneity, an inherently immunosuppressive microenvironment, the unique tissue-specific interactions between the central nervous system and the peripheral immune system, the existence of the blood-brain barrier, which is a physical barrier to drug delivery, and the immunosuppressive effects of standard therapy. Therefore, in this review, we delve into several challenges that need to be addressed to achieve boosted immunotherapy against gliomas. First, we discuss the hurdles posed by the glioma microenvironment, particularly its primary cellular inhabitants, in particular tumor-associated microglia and macrophages (TAMs), and myeloid cells, which represent a significant barrier to effective immunotherapy. Here we emphasize the impact of inducing immunogenic cell death (ICD) on the migration of Th17 cells into the tumor microenvironment, converting it into an immunologically “hot” environment and enhancing the effectiveness of ongoing immunotherapy. Next, we address the challenge associated with the accurate identification and characterization of the primary immune profiles of gliomas, and their implications for patient prognosis, which can facilitate the selection of personalized treatment regimens and predict the patient’s response to immunotherapy. Finally, we explore a prospective approach to developing highly personalized vaccination strategies against gliomas, based on the search for patient-specific neoantigens. All the pertinent challenges discussed in this review will serve as a compass for future developments in immunotherapeutic strategies against gliomas, paving the way for upcoming preclinical and clinical research endeavors. |
| first_indexed | 2024-03-08T14:44:58Z |
| format | Article |
| id | doaj.art-671e1b3822144468a9b6f04b69832d42 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-08T14:44:58Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-671e1b3822144468a9b6f04b69832d422024-01-11T11:14:39ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-01-011410.3389/fimmu.2023.12990641299064Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapyTatiana A. Mishchenko0Victoria D. Turubanova1Victoria D. Turubanova2Ekaterina N. Gorshkova3Olga Krysko4Maria V. Vedunova5Maria V. Vedunova6Dmitri V. Krysko7Dmitri V. Krysko8Dmitri V. Krysko9Dmitri V. Krysko10Institute of Biology and Biomedicine, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaInstitute of Biology and Biomedicine, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaNeuroscience Research Institute, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaInstitute of Biology and Biomedicine, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaCell Death Investigation and Therapy Laboratory, Anatomy and Embryology Unit, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences, Ghent University, Ghent, BelgiumInstitute of Biology and Biomedicine, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaFaculty of Biology and Biotechnologies, National Research University Higher School of Economics, Moscow, RussiaInstitute of Biology and Biomedicine, National Research Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, RussiaCell Death Investigation and Therapy Laboratory, Anatomy and Embryology Unit, Department of Human Structure and Repair, Faculty of Medicine and Health Sciences, Ghent University, Ghent, BelgiumDepartment of Pathophysiology, Sechenov First Moscow State Medical University (Sechenov University), Moscow, RussiaCancer Research Institute Ghent, Ghent, BelgiumGlioma is the most common primary brain tumor, characterized by a consistently high patient mortality rate and a dismal prognosis affecting both survival and quality of life. Substantial evidence underscores the vital role of the immune system in eradicating tumors effectively and preventing metastasis, underscoring the importance of cancer immunotherapy which could potentially address the challenges in glioma therapy. Although glioma immunotherapies have shown promise in preclinical and early-phase clinical trials, they face specific limitations and challenges that have hindered their success in further phase III trials. Resistance to therapy has been a major challenge across many experimental approaches, and as of now, no immunotherapies have been approved. In addition, there are several other limitations facing glioma immunotherapy in clinical trials, such as high intra- and inter-tumoral heterogeneity, an inherently immunosuppressive microenvironment, the unique tissue-specific interactions between the central nervous system and the peripheral immune system, the existence of the blood-brain barrier, which is a physical barrier to drug delivery, and the immunosuppressive effects of standard therapy. Therefore, in this review, we delve into several challenges that need to be addressed to achieve boosted immunotherapy against gliomas. First, we discuss the hurdles posed by the glioma microenvironment, particularly its primary cellular inhabitants, in particular tumor-associated microglia and macrophages (TAMs), and myeloid cells, which represent a significant barrier to effective immunotherapy. Here we emphasize the impact of inducing immunogenic cell death (ICD) on the migration of Th17 cells into the tumor microenvironment, converting it into an immunologically “hot” environment and enhancing the effectiveness of ongoing immunotherapy. Next, we address the challenge associated with the accurate identification and characterization of the primary immune profiles of gliomas, and their implications for patient prognosis, which can facilitate the selection of personalized treatment regimens and predict the patient’s response to immunotherapy. Finally, we explore a prospective approach to developing highly personalized vaccination strategies against gliomas, based on the search for patient-specific neoantigens. All the pertinent challenges discussed in this review will serve as a compass for future developments in immunotherapeutic strategies against gliomas, paving the way for upcoming preclinical and clinical research endeavors.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1299064/fullgliomacancer immunotherapyimmunogenic cell deathICDtumor microenvironmentTh17 |
| spellingShingle | Tatiana A. Mishchenko Victoria D. Turubanova Victoria D. Turubanova Ekaterina N. Gorshkova Olga Krysko Maria V. Vedunova Maria V. Vedunova Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko Dmitri V. Krysko Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy Frontiers in Immunology glioma cancer immunotherapy immunogenic cell death ICD tumor microenvironment Th17 |
| title | Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy |
| title_full | Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy |
| title_fullStr | Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy |
| title_full_unstemmed | Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy |
| title_short | Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy |
| title_sort | glioma bridging the tumor microenvironment patient immune profiles and novel personalized immunotherapy |
| topic | glioma cancer immunotherapy immunogenic cell death ICD tumor microenvironment Th17 |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1299064/full |
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