miRNAs Related to Immune Checkpoint Inhibitor Response: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Screening and Eligibility Criteria
2.3. Data Extraction
3. Results
miRNA | Cancer | miRNA Target Gene | ICI | Experimental Model | Effect on ICI Response | Refs. |
---|---|---|---|---|---|---|
let-7a and let-7b | Head and neck squamous cell carcinoma | TCF-4 * | anti CTLA-4 | Overexpressing let-7a/b tumor cells inoculated into mice + anti CTLA-4 | H | [25] |
miR-15b-5p | Colorectal cancer | PD-L1 * | anti PD-1 | Overexpressing miR-15b-5p tumor cells inoculated into mice + anti PD-1. | H | [26] |
miR-16-5p | Lung cancer | anti PD-L1 | Tumor cell + overexpressing miR-16-5p exosomes + anti PD-L1 | H | [27] | |
miR-20b-5p | Lung cancer | PD-L1 * | anti PD-1 | Tumor cells transfected with miRNA mimic + Pembrolizumab | H | [28] |
Breast cancer | Tumor cells transfected with miRNA mimic + Pembrolizumab | H | ||||
miR-21 | Oral squamous cell carcinoma | PTEN | anti PD-L1 | Tumor cells inoculated into mice + miR-21 knockdown tumor-derived exosomes + anti-PD-L1 | L | [29] |
Melanoma | STAT1 * | anti PD-1 | Tumor cells and knocked down miR-21 tumor-associated macrophages (TAM) subcutaneously injected in mice + anti PD-1 | L | [30] | |
miR-128a | Laryngeal squamous cell carcinoma | BMI1 * | anti PD-1 | Overexpressing miR-128a tumor cells + Pembrolizumab | H | [31] |
miR-155 | Metastatic melanoma | anti PD-1 + anti PD-L1 + anti CTLA-4 | Tumor cells inoculated into modified mice for knockout of miR-155 in CD4/8 T cells + anti PD-1, anti PD-L1 and anti CTLA-4 | L | [32] | |
Diffuse large B-cell lymphoma | PD-L1 * | anti PD-L1 | Overexpressing miR-155 tumor cells inoculated into mice + anti PD-L1 | L | [33] | |
Breast cancer | SOCS1 | anti PD-L1 | Overexpressing miR-155 tumor cells inoculated into mice + anti PD-L1 | H | [34] | |
Melanoma | PD-L1 * | anti PD-L1 | Overexpressing miR-155 tumor cells co-cultured with peripheral blood mononuclear cells + anti PD-L1 | H | [22] | |
miR-340 | Pancreatic carcinoma | CD47 * | anti CD47 | Overexpressing miR-340 tumor cells inoculated into mice + anti CD47 | L | [35] |
miR-424 | Colorectal cancer | CD28 and CD80 * | anti PD-1 + anti CTLA-4 | Tumor cells inoculated into miR-424 knocked mice + anti PD-1 and anti CTLA-4 | L | [36] |
Mouse cecum orthotopic colorectal cancer + miR-424 knocked tumor cell-derived extracellular vesicles + anti PD-1 and anti CTLA-4 | L | |||||
Hepatocellular carcinoma | PD-L1 | anti PD-L1 | Tumor cells inoculated into mice + nanobubbles carrying miR-424 mimic and anti PD-L1 | H | [37] | |
miR-582 | B-cell precursor acute lymphoblastic leukemia | CD276 * | anti CD276 | Overexpressing miR-582 tumor cells co-cultured with NK cells + anti CD276 | H | [38] |
miR-708 | T-acute lymphoblastic leukemia | CD47 * | anti CD47 | Overexpressing miR-708 tumor cells + anti CD47. | H | [39] |
miR-4759 | Breast cancer | PD-L1 * | anti PD-L1 | Overexpressing miR-4759 tumor cells co-cultured with peripheral blood mononuclear cells + anti PD-L1 | H | [40] |
ICI | Experimental Model | miRNA | Experimental Effect on miRNA | Refs. |
---|---|---|---|---|
anti PD-1 | miRNA analysis in peripheral lymphocytes from 21 good responders (complete response, partial response, or stable disease) with metastatic renal cell carcinoma before and after a 4-weeks period (2 cycles) of nivolumab administration | miR-99a, miR-708, miR-655, miR-582-3p, miR-492, miR-487a, miR-485-3p, miR-449a, miR-433, miR-431, miR-429, miR-376c, miR-342-5p, miR-340, miR-339-5p, miR-335, miR-324-5p, miR-25, miR-24, miR-22, miR-221, miR-214, miR-194, miR-18b, miR-152, miR-143, miR-100, miR-let-7ev | High levels of expression in peripheral lymphocytes after treatment compared to before treatment in good responders. | [41] |
miRNA analysis in peripheral lymphocytes from 17 good long-responders (complete response, partial response or stable disease and progression-free survival (PFS) > 18 months) with metastatic renal cell carcinoma before and after a 4-weeks period (2 cycles) of nivolumab administration | miR-22, miR-24, miR-99a, miR-194, miR-214, miR-335, miR-339, miR-708 | High expression levels in peripheral lymphocytes after treatment compared to before treatment in good responders. | ||
anti CTLA-4 + anti PD-1 | Plasma from stage IV melanoma non-responders (13 patients), partial response (4 patients) and complete response (5 patients) before and after Ipilimumab and Nivolumab/Pembrolizumab treatment | miR-4649-3p and miR-615-3p | Increased levels in post- vs. pre-treatment in non-responders. No changes post- vs. pre-treatment in patients with partial response. Decreased levels post- vs. pre-treatment in patients with complete response. | [42] |
ICI | miRNA | Immune-Related Adverse Events (irAEs) | Refs. |
---|---|---|---|
anti PD-1 | miR-34a | Anti PD-1 induced miR-34a-5p upregulation, modulating the miR-34a/Krüppel-like factor 4 (KLF4)-and miR-34a-5p/serine/threonine-protein phosphatase 1 regulatory subunit 10 (PNUTS) signaling pathway and inducing cardiac injury | [43,44] |
anti PD-1 + anti CTLA-4 | miR-146a | Downregulation of miR-146 increased the risk of developing irAE after ICI treatment. Toxicity was accompanied by increased infiltration of neutrophil and lymphocyte into the damaged organs. | [45] |
3.1. miRNAs That Modulate Response to ICIs
3.2. miRNAs Modulated after Response to ICIs
3.3. miRNAs That Regulate Immune-Related Adverse Events (irAEs)
3.4. miRNAs Related to ICIs Response
4. Discussion
4.1. miRNAs That Modulate Response to ICIs
4.2. miRNAs Modulated after Response to ICIs
4.3. miRNAs That Regulate Immune-Related Adverse Events (irAEs)
4.4. miRNAs Related to ICIs Response
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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García-Giménez, J.L.; Saadi, W.; Ortega, A.L.; Lahoz, A.; Suay, G.; Carretero, J.; Pereda, J.; Fatmi, A.; Pallardó, F.V.; Mena-Molla, S. miRNAs Related to Immune Checkpoint Inhibitor Response: A Systematic Review. Int. J. Mol. Sci. 2024, 25, 1737. https://doi.org/10.3390/ijms25031737
García-Giménez JL, Saadi W, Ortega AL, Lahoz A, Suay G, Carretero J, Pereda J, Fatmi A, Pallardó FV, Mena-Molla S. miRNAs Related to Immune Checkpoint Inhibitor Response: A Systematic Review. International Journal of Molecular Sciences. 2024; 25(3):1737. https://doi.org/10.3390/ijms25031737
Chicago/Turabian StyleGarcía-Giménez, José Luis, Wiam Saadi, Angel L. Ortega, Agustin Lahoz, Guillermo Suay, Julián Carretero, Javier Pereda, Ahlam Fatmi, Federico V. Pallardó, and Salvador Mena-Molla. 2024. "miRNAs Related to Immune Checkpoint Inhibitor Response: A Systematic Review" International Journal of Molecular Sciences 25, no. 3: 1737. https://doi.org/10.3390/ijms25031737