Challenges in glioblastoma immunotherapy: mechanisms of resistance and therapeutic approaches to overcome them

Habashy, Karl John; Mansour, Rana; Moussalem, Charbel; Sawaya, Raymond; Massaad, Michel J.

doi:10.1038/s41416-022-01864-w

Cited by 96Glioma Diagnosis and TreatmentCancer Immunotherapy and BiomarkersImmunotherapy and Immune Responses

Challenges in glioblastoma immunotherapy: mechanisms of resistance and therapeutic approaches to overcome them

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Habashy, Karl John, Mansour, Rana, Moussalem, Charbel, Sawaya, Raymond, Massaad, Michel J.·2022·British Journal of Cancer

DOI 10.1038/s41416-022-01864-wPMC PMC9470562

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Abstract

Glioblastoma is the most common and aggressive primary malignant brain tumour. The prognosis of patients with glioblastoma is poor, and their overall survival averages at 1 year, despite advances made in cancer therapy. The emergence of immunotherapy, a strategy that targets the natural mechanisms of immune evasion by cancerous cells, has revolutionised the treatment of melanoma, lung cancer and other solid tumours; however, immunotherapy failed to improve the prognosis of patients with glioblastoma. This is attributed to the fact that glioblastoma is endowed with numerous mechanisms of resistance that include the intrinsic resistance, which refers to the location of the tumour within the brain and the nature of the blood-brain barrier, as well as the adaptive and acquired resistance that result from the tumour heterogeneity and its immunosuppressive microenvironment. Glioblastoma is notorious for its inter and intratumoral heterogeneity, which, coupled with its spatial and temporal evolution, limits its immunogenicity. In addition, the tumour microenvironment is enriched with immunosuppressive cells and molecules that hinder the reactivity of cytotoxic immune cells and the success of immunotherapies. In this article, we review the mechanisms of resistance of glioblastoma to immunotherapy and discuss treatment strategies to overcome them worthy of further exploration.

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Tumour cell heterogeneity and an immunosuppressive microenvironment contribute to primary GBM immunoresistance, which dampens anti-tumour responses by macrophages and T cells.
“Tumour cell heterogeneity and an immunosuppressive microenvironment contribute to primary GBM immunoresistance, which dampens anti-tumour responses by macrophages and T cells [7, 10].”
From Preclinical development of an mRNA-based multiepitope immunotherapeutic for glioblastoma (2025) · cites this paper as [7]
Checkpoint inhibitors against CTLA-4 and PD-1/PD-L1 have shown only very limited benefits in patients with GBM.
“Immunotherapies such as checkpoint inhibitors against cytotoxic T-lymphocyte-associated protein 4 (CTLA-4) and programmed death-1 (PD-1)/PD ligand 1 (PD-L1) have represented a major advancement in the treatment of several types of solid tumour; however, these treatments have shown only very limited benefits in patients with GBM [7–9].”
From Preclinical development of an mRNA-based multiepitope immunotherapeutic for glioblastoma (2025) · cites this paper as [7]

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Profiling of patients with glioma reveals the dominant immunosuppressive axis is refractory to immune function restoration
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Self-citation
Inability of mitogen-activated lymphocytes obtained from patients with malignant primary intracranial tumors to express high affinity interleukin 2 receptors.
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Blockade of CD73 delays glioblastoma growth by modulating the immune environment
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Temozolomide antagonizes oncolytic immunovirotherapy in glioblastoma
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Radiation with STAT3 Blockade Triggers Dendritic Cell–T cell Interactions in the Glioma Microenvironment and Therapeutic Efficacy
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Management of Glioblastoma, Present and Future
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Self-citation
Inhibition of Colony-Stimulating Factor-1 Receptor Enhances the Efficacy of Radiotherapy and Reduces Immune Suppression in Glioblastoma
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Poor survival in glioblastoma patients is associated with early signs of immunosenescence in the CD4 T-cell compartment after surgery
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Systemic Anti–PD-1 Immunotherapy Results in PD-1 Blockade on T Cells in the Cerebrospinal Fluid
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HMGB1 in Radiotherapy: A Two Headed Signal Regulating Tumor Radiosensitivity and Immunity
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Replication stress response defects are associated with response to immune checkpoint blockade in nonhypermutated cancers
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New somatic TERT promoter variants enhance the Telomerase activity in Glioblastoma
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Aging- and Tumor-Mediated Increase in CD8+CD28− T Cells Might Impose a Strong Barrier to Success of Immunotherapy in Glioblastoma
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Human Astrocytomas Co-expressing Fas and Fas Ligand also Produce TGFβ2 and Bcl-2
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mRNA-based precision targeting of neoantigens and tumor-associated antigens in malignant brain tumors
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Intracavitary Spraying of Nanoregulator‐Encased Hydrogel Modulates Cholesterol Metabolism of Glioma‐Supportive Macrophage for Postoperative Glioblastoma Immunotherapy
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synNotch-programmed iPSC-derived NK cells usurp TIGIT and CD73 activities for glioblastoma therapy
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Fc-enhanced anti-CTLA-4, anti-PD-1, doxorubicin, and ultrasound-mediated blood–brain barrier opening: A novel combinatorial immunotherapy regimen for gliomas
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Self-citation
Glioma: bridging the tumor microenvironment, patient immune profiles and novel personalized immunotherapy
Mishchenko, T. A., Turubanova, V. D., Gorshkova, E. N., Krysko, O., Vedunova, M. V., & Krysko, D. V. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1299064 · Cited by 35 · see citing works
Harnessing type I interferon-mediated immunity to target malignant brain tumors
Lim, J., Kang, I., La, J., Ku, K. B., Kang, B. H., Kim, Y., Park, W. H., & Lee, H. K. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1203929 · Cited by 35 · see citing works
Single-Cell Transcriptomics Reveals the Heterogeneity of the Immune Landscape of IDH–Wild-Type High-Grade Gliomas
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Photodynamic therapy for glioblastoma: A light at the end of the tunnel
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Exploring the Multi-Faceted Role of Sirtuins in Glioblastoma Pathogenesis and Targeting Options
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STING stimulation via supramolecular prodrug hydrogel boosts innate-adaptive immune cross-talk to prevent glioblastoma recurrence
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ATR inhibition using gartisertib enhances cell death and synergises with temozolomide and radiation in patient-derived glioblastoma cell lines
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In situ administration of STING-activating hyaluronic acid conjugate primes anti-glioblastoma immune response
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Unlocking the Gates: Therapeutic Agents for Noninvasive Drug Delivery Across the Blood-Brain Barrier
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CHI3L1-targeted small molecules as glioblastoma therapies: Virtual screening-based discovery, biophysical validation, pharmacokinetic profiling, and evaluation in glioblastoma spheroids
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Exosomal DNA: Role in Reflecting Tumor Genetic Heterogeneity, Diagnosis, and Disease Monitoring
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Spatial transcriptomics and multi-omics reveal relapse and resistance mechanisms of EndMT-derived CAFs mediated by TNC and FLNC in glioblastoma
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Normofractionated irradiation and not temozolomide modulates the immunogenic and oncogenic phenotype of human glioblastoma cell lines
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Small Molecule Immunomodulators as Next-Generation Therapeutics for Glioblastoma
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Dendritic cell vaccine for glioblastoma: an updated meta-analysis and trial sequential analysis
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Repurposing FDA‐Approved Drugs for Temozolomide‐Resistant IDH1 Mutant Glioma Using High‐Throughput Miniaturized Screening on Droplet Microarray Chip
Cui, H., Sun, X., Schilling, M. P., Herold‐Mende, C. C., Reischl, M., Levkin, P. A., Popova, A. A., & Turcan, Ş. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300591 · Cited by 14 · see citing works
Human gamma-delta (γδ) T cell therapy for glioblastoma: A novel alternative to overcome challenges of adoptive immune cell therapy
Choi, H., Kim, T., Jeun, S., & Ahn, S. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216335 · Cited by 14 · see citing works
Pediatric gliomas immunity challenges and immunotherapy advances
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Endoplasmic reticulum stress on glioblastoma: Tumor growth promotion and immunosuppression
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Applications of nanotechnology in remodeling the tumour microenvironment for glioblastoma treatment
Mu, Y., Zhang, Z., Zhou, H., Ma, L., & Wang, D. (2024) · Biomaterials Science · doi:10.1039/d4bm00665h · Cited by 12 · see citing works
NR2F6, a new immune checkpoint that acts as a potential biomarker of immunosuppression and contributes to poor clinical outcome in human glioma
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Authors: Habashy, K. J., Mansour, R., Moussalem, C., Sawaya, R., & Massaad, M. J.
Affiliations: American University of Beirut (LB)
American University of Beirut Medical Center (LB)
Corresponding author: Massaad, Michel J.
ORCID: Habashy, Karl John
Moussalem, Charbel
Sawaya, Raymond
Massaad, Michel J.
Venue: British Journal of Cancer
Publisher: Springer Science and Business Media LLC
Published: 2022-06-04
Volume: 127
Issue: 6
Pages: 976-987
ISSN: 0007-0920 (ISSN-L)
1532-1827
DOI: 10.1038/s41416-022-01864-w
PMC: PMC9470562
OpenAlex: W4281661874
Cited by: 95
References: 197
Citations by year: 2026: 29 · 2025: 23 · 2024: 27 · 2023: 13 · 2022: 3
FWCI: 2.82
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: British Journal of Cancer (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: glioblastoma, cancer immunotherapy, immunotherapy resistance, blood-brain barrier, tumor heterogeneity, tumor microenvironment, immunosuppression, immune evasion, brain tumors
MeSH terms: Brain Neoplasms, Glioblastoma, Humans, Immunologic Factors, Immunotherapy, Tumor Microenvironment

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Challenges in glioblastoma immunotherapy: mechanisms of resistance and therapeutic approaches to overcome them

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