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PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Next, we evaluated the efficacy of 15–4P-stimulated ex vivo activated allogeneic B6 NK cells (H-2b) against Neuro2a (H-2a) murine NBL to evaluate the impact of Ly49 mismatch on cytotoxicity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Neuro2a NBL targets were co-cultured with either IL-15/IL-15Rα expanded allogeneic NK cells or 15–4P expanded allogeneic NK cells for 24 hours.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Apoptotic Neuro2a cells were selected by size and fluorescence intensity of caspase 3/7 and quantified using live-cell imaging by the IncuCyte system.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
15–4P-expanded allogeneic NK cells exhibited slightly increased target killing compared with IL-15-expanded allogeneic NK cells, despite showing a significant decrease in Fas-L expression (figure 2B).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Surface TIM-3 upregulation was confirmed on IL-15/IL-15Rα NK cells and 15–4P stimulated NK cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Results showed a significantly higher percentage of TIM-3 cells (20.78%±1.695) (p=0.0006) and TIM-3 expression by MFI in 15–4P stimulated NK cells relative to IL-15/IL-15Rα NK cells (4.134%±0.1592) (p=0.0012) (figure 2D, E).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
The elevated expression of TIM-3 on AgN2a-4P NK cells combined with elevated expression of putative TIM-3 ligands on NBL cells suggests this immune checkpoint may be a relevant axis governing NK cell function.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Initially, we measured IFN-γ and tumor necrosis factor (TNF)-α mRNA levels to determine the impact of TIM-3 blockade on NK cell cytokine production after ex vivo expansion.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
We co-cultured IL-15 B6 allogeneic NK cells or 15–4P stimulated B6 allogeneic NK cells with isotype control or anti-TIM-3 antibody in the presence of Neuro2a NBL cells at an effector-to-target (E:T) ratio of 10:1 and assessed cytokine production.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
TNF-α production was significantly increased in the 15–4P NK cells compared with IL-15 NK cells; however, there was no increase after 15–4P NK cell with TIM-3 blockade after exposure to Neuro2a NBL.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Similarly, we observed a notable increase in IFN-γ production in 15–4P stimulated NK cells compared with IL-15 NK cells, but 15–4P NK cells showed no further increase in IFN-γ (online supplemental figure 2D).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Then, to investigate whether blocking TIM-3 could enhance the killing potential of 15–4P stimulated NK cells, we co-cultured 15–4P stimulated NK cells with Neuro2a at an E:T ratio of 10:1 with isotype control or anti-TIM-3 and then assessed surface expression of activating receptors and death ligands as well as cytotoxicity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
There was a high percentage of NKG2D and NKp46 cells and elevated surface expression of NKG2D and NKp46 by MFI among 15–4P stimulated NK cells as seen in prior experiments, but these subsets were not enriched by TIM-3 blockade, suggesting NK cells were already maximally activated.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
After exposure to Neuro2a, 15–4P NK cells with TIM-3 blockade exhibited a higher percentage (p=0.004) but not MFI (p=0.05) of TRAIL than without the anti-TIM-3 antibody.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Compared with 15–4 P cells alone, TIM-3 blockade enhanced both the percentage (p=0.02) of Fas-L 15–4P NK cells, and Fas-L MFI (p=0.007) compared with 15–4P NK cells after Neuro2a exposure (figure 3A).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
This experiment was repeated with NXS2 NBL cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Interestingly, 15–4P NK cells treated with TIM-3 blockade showed no difference in NKG2D and NKp46 expression by MFI as compared with 15–4P NK cells (online supplemental figure 3A).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Additionally, in the presence of NXS2, we found no significant increase in TRAIL, Fas-L, granzyme B or perforin per cent or expression, suggesting that blockade of exposure to TIM-3 ligands on NBL is required to augment allogeneic NK cell activation (online supplemental figure 3B).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Next, we evaluated cytotoxicity by quantifying CD107a degranulation on allogeneic NK cells following exposure to NBL.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Interestingly, we found no discernible difference in degranulation between 15–4P stimulated NK cells with or without TIM-3 blockade in response to NXS2, which have lower expression of TIM-3 ligands (online supplemental figure 3C).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, TIM-3 blockade resulted in a significant increase in the percentage of CD107a+15–4P NK cells, as well as MFI of CD107a granules (figure 3B), in response to Neuro-2a.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Additionally, we observed a significant increase in the percentage of granzyme B-positive cells following TIM-3 blockade, as well as a significant increase in both granzyme B and perforin expression (figure 3C).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
To determine the impact of TIM-3 blockade on NK cell maturation, we assessed the expression of the transcription factors T-box expressed in T cells (T-bet) and Eomesodermin (Eomes) after exposure to NBL tumor cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
TIM-3 blockade did not impact T-bet per cent or expression as 15–4P NK, and 15–4P NK with TIM-3 blockade, cells showed similarly low levels of T-bet.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, we observed a significant rise in both the percentage (p=0.004) and MFI (p=0.004) of Eomes in 15–4P stimulated NK cells after exposure to TIM-3 blockade (47.05±1.607) compared with 15–4P NK cells alone (38.33±0.6756) (p=0.0018).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
This was consistent with Eomes MFI (figure 3D).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
We determined the ratio of Eomes positive cells relative to T-bet in 15–4P stimulated NK cells and 15–4P stimulated NK cells with anti-TIM-3 after Neuro2a NBL exposure; however, there was no significant difference between the two groups (figure 3E).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Interestingly, TIM-3 blockade did not enhance Eomes expression in 15–4P NK cells after exposure to NXS2 NBL cells which have lower expression of TIM-3 ligands (online supplemental figure 3D).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
These findings suggest that TIM-3 blockade enriches for NK cells in early maturation.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Following treatment with anti-TIM-3, 15–4P stimulated NK cells exhibited heightened expression of death ligands and increased markers of degranulation, indicating a phenotype conducive to antitumor activity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Allogeneic NK cells were incubated with Neuro2a NBL with anti-TIM-3 or an isotype control, and apoptotic NBL cells were quantified using IncuCyte live cell imaging of caspase 3/7 expression.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
For all groups, peak killing occurred after the 8-hour mark.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
15–4P NK cells treated with anti-TIM-3 antibody exhibited significantly higher killing compared with all other groups (figure 3F).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
The enhanced killing capacity of 15–4P NK cells was also observed in the presence of a second murine NBL cell line, 9464D (online supplemental figure 3E).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
This effect was not observed against NXS2 (figure 3G).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
We conducted a comparative evaluation of IL-15 allogeneic NK cells and 15–4P expanded allogeneic NK cells following exposure to the NBL TME to investigate whether TIM-3 blockade modulated NK cell gene expression.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Total RNA was isolated from 15 to 4P stimulated NK cells NK cells co-cultured with Neuro2a in the presence of isotype controls or anti-TIM-3 for 4 hours.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Using the NanoString/nCounter Mouse PanCancer Immune Profiling Panel, the expression of 760 genes was examined.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
The comparison between 15–4P stimulated NK cells and 15–4P stimulated NK cells treated with TIM-3 blockade showed 25 significantly upregulated genes, and 12 genes showed significant downregulation compared with 15–4P stimulated NK cells treated with an isotype control.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Within the upregulated subset of genes, numerous genes associated with NK cell trafficking and target cell recognition (CCL4, CCL3, CCL1, XCL1, CXCR6), and the non-canonical NF-κB pathway (LTA, LTB, TNFSF10, TNFSF14, TNFSF8, RELB, TNF, TRAF3) were observed.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Both ICAM1, which encodes CD54, and TNFSF10, which encodes TRAIL, exhibited a fold change of 2.4 (with false discovery rate p values of 0.003 and 0.0024, respectively).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Furthermore, genes encoding IL-15 and IL-21 receptors were upregulated.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Surprisingly, Prf1 (perforin) was downregulated in IL-15/AgN2a-4P/TIM-3 NK compared with 15–4P stimulated NK cells despite TRAIL upregulation (figure 4A, B; online supplemental table 1).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
This alteration may suggest functional impairment due to exhaustion.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Following the initial granule-mediated killing phase, NK cells may switch to death receptor signaling to sustain serial killing on granule depletion.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
NK cells use multiple cytotoxic pathways in tumor surveillance, transitioning between granule release and death receptor-mediated killing to initiate and sustain long-term cytotoxic activity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
To assess the impact of multiple NK cell cytotoxicity pathways on the killing efficiency of 15–4P stimulated NK cells in the presence of TIM-3 blockade, we exposed allogeneic NK cells to Neuro2a NBL in the presence of blocking antibodies targeting NKG2D, TRAIL, and Fas-L. The inhibition of all three targets resulted in a significant reduction in NK cell killing.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Notably, the blockade of Fas-L completely ameliorated NK cell cytotoxicity against NBL compared with NKG2D or TRAIL blockade, suggesting there is a hierarchy of pathways used to mediate NK cytotoxicity of NBL when TIM-3 is engaged (figure 4C).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
These data underscore the potential of TIM-3 blockade to enhance NK cell cytotoxicity against NBL, particularly in tumors with high expression of TIM-3 ligands, emphasizing the importance of considering the makeup of the NBL TME in therapeutic strategies.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Given our observations regarding the positive impact of TIM-3 blockade on the phenotype and function of 15–4P stimulated NK cells in vitro, we hypothesized that this therapy could yield therapeutic benefits in vivo.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, the intricate pro-inflammatory environment post-allo-HCT and the immunosuppressive NBL TME present additional challenges that could impede NK cell cytotoxic efficacy.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
To address this concern, we evaluated the potency of the combination allogeneic NK cell treatment against Neuro2a NBL following allo-HCT.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Initially, we established an MHC-mismatched haploidentical allo-HCT model wherein lethally irradiated B6AJF1 (H-2b × H-2a) recipients received 5×10 T cell-depleted (TCD) B6 (H-2b) bone marrow with 1×10 B6 T-cell add back on day+0 to simulate residual T cells present in the donor graft during clinical T-cell depletion protocols (eg, CD3 or αβ-TCR depletion).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
On day+7, mice were subcutaneously inoculated with Neuro2a (H-2a) cells to mimic relapse post-HCT.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Recipients then were infused with 3 weekly infusions of B6 IL-15 allogeneic NK cells or B6 15–4P stimulated allogeneic NK cells administered with either an isotype control or anti-TIM-3 treatment every 7 days starting on day+9 (figure 5A).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Although TIM-3 blockade has not been tested after haploidentical allo-HCT, despite the presence of residual T cells in the donor bone marrow graft, we did not observe significant differences in GVHD-associated weight loss (figure 5B).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
By day 35, mice treated with 15–4P NK cells and anti-TIM-3 exhibited the most substantial reduction in tumor growth compared with controls (figure 5C).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Treatment with 15–4P allogeneic NK cells combined with TIM-3 blockade significantly prolonged OS compared with mice treated with 15–4P stimulated NK cells and an isotype control, anti-TIM-3 alone, IL-15 NK cells alone, IL-15 NK cells alone with anti-TIM-3, or no treatment groups (figure 5D).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Given the known role of TIM-3 blockade in promoting T-cell responses and the presence of a low dose of T cells in the graft, we sought to delineate the contributions of NK cells and T cells to graft-versus-tumor (GVT) effects and OS in our allo-HCT model by depletion of these cell subsets prior to treatment.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
In our T-cell depletion studies, B6AJF1 mice received T-depleted B6 bone marrow without T-cell add-back.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
In NK depletion studies, B6AJF1 mice received NK-depleted B6 bone marrow with T-cell add-back.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Since NK cells typically are the first lymphocyte to reconstitute after allo-HCT, anti-NK1.1 antibody was administered intraperitoneally every 4 days to maintain NK cell depletion.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
NK1.1 depletion was performed to ensure the successful engraftment of allogeneic NK cells as endogenous NK cells can compete for space within the bone marrow niche and induce rejection of donor NK cells due to alloreactivity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Subsequently, mice were inoculated with Neuro2A cells and treated with anti-TIM-3 antibody alone or B6 15–4P stimulated allogeneic NK cells with anti-TIM-3 antibody (figure 6A).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Consistently, there were no noticeable differences concerning GVHD-associated weight loss (figure 6B).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
NK cell depletion led to a significant decrease in OS, while TCD mice exhibited significantly increased survival like that of mice treated with 15–4P stimulated NK cells and TIM-3 blockade (figure 6C).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Furthermore, NK cell depletion resulted in larger tumors in all mice, with no significant difference compared with the control, whereas T-cell depletion led to a significant decrease in tumor growth (figure 6D).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
These findings suggest that while T cells are present in the graft, NK cells may play a more substantial role in the survival benefit conferred by 15–4P stimulated NK cells, possibly due to the limited number of T cells compared with NK cells resulting from repeated adoptive transfers.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Moreover, these results underscore the crucial role of NK cells as the primary drivers of TIM-3-induced therapeutic benefits against NBL after allo-HCT, given that similar outcomes were not observed with anti-TIM-3 treatment alone (online supplemental figure 4A, B).
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
T cell-depleted (TCD) allo-HCT has recently gained traction as a safe alternative to standard unmanipulated allo-HCT in order to leverage the GVT effect mediated by donor-derived innate effector cells, like NK cells, while mitigating lethal GVHD.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
While graft manipulation techniques like CD3 or αβ-TCR depletion have achieved up to 5 log10 depletion of T cells, there are always depletion-resistant CD8+ or CD4+ T cells to consider toward impacting GVT or GVHD.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
A major limitation of TCD allo-HCT is the increased risk of infectious complications and relapse due to delayed immune reconstitution of T cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Preclinically, we have previously explored the use of TCD haploidentical allo-HCT in combination with adoptively transferred ex vivo activated NK cells and an anti-GD2 immunocytokine.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
In this study, we found that 15–4P ex vivo expanded NK cells have increased potency against NBL target cells, especially when combined with TIM-3 blockade.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
CD54 and CD137L co-stimulation have never been combined to activate murine NK cells ex vivo.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
While CD54CD137LAgN2 a-4P cells were initially designed as an in vivo vaccine for stimulating T cells, we demonstrate for the first time that combining IL-15/IL-15Ra with AgN2a-4P exposure ex vivo significantly boosts NK cell proliferation and activation, allowing for adoptive transfer of highly potent immune effector cells in the allo-HCT setting.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
AgN2a-4P stimulation increased both NKG2D and TRAIL expression on NK cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
15–4P-stimulated NK cells exhibited increased IFN-γ production compared with IL-15/IL-15RA stimulation alone.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Prior studies done in a syngeneic model by Jing et al demonstrated that AgN2a-4P vaccination enacted an anti-NBL response through CD8 and CD4 T cells mediated response, despite their tumor target being the parental line AgN2a, which does not express MHC class II.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
While studies have shown that CD4 T cells can kill tumor targets through an indirect mechanism involving IFN-γ directed elimination, the contribution of NK cells to the anti-NBL response cannot be ruled out.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
NK cell reconstitution occurs rapidly following HCT, and it is possible that AgN2a-4P vaccination induced an NK cell-mediated antitumor response and increased IFN-γ production, which indirectly facilitated CD8 T cell and macrophage antitumor responses.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Additionally, we found that 15–4P stimulation significantly enhanced NK cell-mediated lysis of Neuro2a NBL tumor compared with IL-15 NK cells in vitro.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
IL-15 exposure results in an upregulation of TIM-3 expression, where TIM-3 can act as a negative regulator of activation to limit autoreactivity in innate immune cells and maintain self-tolerance.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Although increased TIM-3 upregulation is associated with activated NK cells, cytotoxicity is significantly impaired on crosslinking of TIM-3 with cognate ligands.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
In addition to TIM-3 regulation of NK cell activation, inhibitory signals in the NBL TME can dampen the NK cell response through mechanisms including blockade of target cell adhesion and inhibition of LFA-1 activation, subjugating a weaker activating stimulus and tilting the NK cell response towards inactivation.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
TIM-3 ligands such as Gal-9, CEACAM-1, HMGB1, and PtdSer are expressed at different levels on and within NBL cells and are present in the TME as they are ancillary to pathogenesis.3436 Our results showed that multiple TIM-3 ligands were expressed at a higher proportion on Neuro2a, but not NXS2, suggesting that TIM-3 ligand exposure is cell line dependent and may only be upregulated in a subset of patients with NBL.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, exposure to inhibitory signals from TIM-3 ligands can originate from tumor-associated macrophages as well as other immune cell types within the TME.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
To better understand the mechanisms driving 15–4P NK cells treated with TIM-3 blockade against NBL, we analyzed upregulation of 25 genes and downregulation of 12 genes in 15–4P stimulated NK cells compared with 15–4P stimulated NK cells alone, including ICAM1 and TNFSF10 encoding CD54 and TRAIL, respectively.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Within the upregulated subset of genes, numerous genes were found to be associated with NK cell trafficking and target cell recognition (CCL4, CCL3, CCL1, XCL1, CXCR6) in 15–4P stimulated NK cells with TIM-3 blockade compared to 15–4P NK cells alone.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Modulating chemokine receptors may contribute to increased NK cell motility, thereby allowing 15–4P NK cells enhanced ability to track Neuro2a NBL cells in the absence of TIM-3 inhibition.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Interestingly, we saw increased expression of multiple genes involved in the TNFR2 non-canonical NF-kB pathway (LTA, LTB, TNFSF10, TNFSF14, TNFSF8, RELB, TNF, TRAF3) and in DAP12 signaling (H2-Aa, KLRC2), which suggests the involvement of NKG2D activation in anti-TIM-3 15–4P NK cell mediated killing.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Functional cytotoxicity studies confirmed the ability of 15–4P NK cells treated with TIM-3 blockade to kill Neuro2A targets, which were reversed when blocking NKG2D, TRAIL, or Fas-L. Interestingly, we observed a downregulation of Prf1 (perforin) in 15–4P NK cells treated with TIM-3 blockade compared with 15–4P stimulated NK cells, while TNFSF10 (TRAIL) showed upregulation.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
This may suggest functional impairment in 15–4P NK cells treated with TIM-3 blockade, potentially due to exhaustion.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
The upregulation of TRAIL and the non-canonical Nuclear Factor kappa-light-chain-enhancer of activated B cells (NF-κB) pathway intermediates suggests a compensatory mechanism, where NK cells engage the death receptor pathway for killing on granule depletion, thereby sustaining serial killing of target cells.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, NK cells are regulated by a complex interplay of activating and inhibitory co-receptors which contribute to a dynamic response.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Therefore, it cannot be ruled out that unidentified alternative signaling pathways may influence TIM-3 induced NK cell activation.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Further investigation is required to understand how TIM-3 engagement mobilizes FAS-L and TRAIL in the context of NK cell biology.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
Several studies have indicated that blocking TIM-3 interactions during hepatitis B virus infection, as well as in melanoma, acute myelogenous leukemia and multiple myeloma, resulted in enhanced NK cell cytotoxicity.3942 Conversely, other studies have reported enhanced IFN-γ production without a corresponding improvement in NK cell degranulation, suggesting that TIM-3 engagement can shift the NK cell response between positive and negative signaling events through differential tyrosine phosphorylation of the cytoplasmic tail.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
We observed increased IFN-γ production in 15–4P stimulated NK cells, which indicated that exposure to AgN2a-4P during ex vivo expansion shifts NK cells to a more immature phenotype that is still capable of robust cytotoxicity.
PMC12699621
TIM-3 blockade enhances ex vivo stimulated allogeneic NK cell therapy for relapsed murine neuroblastoma after hematopoietic cell transplant
However, the addition of TIM-3 blockade did not further enhance IFN-γ and TNF-α production in 15–4P NK cells.