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. 2023 Nov 29;24(23):16901.
doi: 10.3390/ijms242316901.

Opaganib (ABC294640) Induces Immunogenic Tumor Cell Death and Enhances Checkpoint Antibody Therapy

Affiliations

Opaganib (ABC294640) Induces Immunogenic Tumor Cell Death and Enhances Checkpoint Antibody Therapy

Lynn W Maines et al. Int J Mol Sci. .

Abstract

Antibody-based cancer drugs that target the checkpoint proteins CTLA-4, PD-1 and PD-L1 provide marked improvement in some patients with deadly diseases such as lung cancer and melanoma. However, most patients are either unresponsive or relapse following an initial response, underscoring the need for further improvement in immunotherapy. Certain drugs induce immunogenic cell death (ICD) in tumor cells in which the dying cells promote immunologic responses in the host that may enhance the in vivo activity of checkpoint antibodies. Sphingolipid metabolism is a key pathway in cancer biology, in which ceramides and sphingosine 1-phosphate (S1P) regulate tumor cell death, proliferation and drug resistance, as well as host inflammation and immunity. In particular, sphingosine kinases are key sites for manipulation of the ceramide/S1P balance that regulates tumor cell proliferation and sensitivity to radiation and chemotherapy. We and others have demonstrated that inhibition of sphingosine kinase-2 by the small-molecule investigational drug opaganib (formerly ABC294640) kills tumor cells and increases their sensitivities to other drugs and radiation. Because sphingolipids have been shown to regulate ICD, opaganib may induce ICD and improve the efficacy of checkpoint antibodies for cancer therapy. This was demonstrated by showing that in vitro treatment with opaganib increases the surface expression of the ICD marker calreticulin on a variety of tumor cell types. In vivo confirmation was achieved using the gold standard immunization assay in which B16 melanoma, Lewis lung carcinoma (LLC) or Neuro-2a neuroblastoma cells were treated with opaganib in vitro and then injected subcutaneously into syngeneic mice, followed by implantation of untreated tumor cells 7 days later. In all cases, immunization with opaganib-treated cells strongly suppressed the growth of subsequently injected tumor cells. Interestingly, opaganib treatment induced crossover immunity in that opaganib-treated B16 cells suppressed the growth of both untreated B16 and LLC cells and opaganib-treated LLC cells inhibited the growth of both untreated LLC and B16 cells. Next, the effects of opaganib in combination with a checkpoint antibody on tumor growth in vivo were assessed. Opaganib and anti-PD-1 antibody each slowed the growth of B16 tumors and improved mouse survival, while the combination of opaganib plus anti-PD-1 strongly suppressed tumor growth and improved survival (p < 0.0001). Individually, opaganib and anti-CTLA-4 antibody had modest effects on the growth of LLC tumors and mouse survival, whereas the combination of opaganib with anti-CTLA-4 substantially inhibited tumor growth and increased survival (p < 0.001). Finally, the survival of mice bearing B16 tumors was only marginally improved by opaganib or anti-PD-L1 antibody alone but was nearly doubled by the drugs in combination (p < 0.005). Overall, these studies demonstrate the ability of opaganib to induce ICD in tumor cells, which improves the antitumor activity of checkpoint antibodies.

Keywords: ABC294640; checkpoint antibody; immunogenic cell death; immunotherapy; opaganib; sphingolipid.

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Conflict of interest statement

Lynn W. Maines, Staci N. Keller and Charles D. Smith are employees of and own stock in Apogee Biotechnology Corporation. Apogee Biotechnology Corporation owns patent rights to opaganib, and the value of these rights may be affected by the research reported in the enclosed paper. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Opaganib promotes ICD in multiple tumor types. B16 melanoma, Lewis lung carcinoma or Neuro-2a neuroblastoma cells were treated in vitro with 40 μM opaganib for 24 h and then injected subcutaneously into C57BL/6 (B16 and LLC) or A/J (Neuro-2a) mice. Control mice received subcutaneous injection of PBS. After 7 days, all mice were injected with 1/5 the number of untreated matched cells, and tumor growth was monitored until tumors reached ≥3000 mm3. N = 10/group for B16 and LLC tumors and N = 5/group for Neuro-2a tumors. The median tumor volume is indicated by the horizontal line in each bar; the range of the bar indicates the interquartile range; and the whiskers indicate the range between the smallest and largest tumors for each treatment group.
Figure 2
Figure 2
Opaganib promotes crossover immunity against tumors. (Left panel): Administration of opaganib-treated B16 melanoma or Lewis lung carcinoma (LLC) cells elicits immunity against subsequently injected untreated B16 tumor cells. (Right panel): Administration of opaganib-treated B16 melanoma or (LLC) cells elicits immunity against subsequently injected untreated LLC tumor cells.
Figure 3
Figure 3
Antitumor activity of opaganib in combination with anti-PD-1 antibody. B16 cells were grown as xenografts and treated with the vehicle; opaganib alone (50 mg/kg/day, 5 days/week); anti-PD-1 antibody (200 μg/mouse intraperitoneally, 3 times as indicated by the black arrows); or opaganib+anti-PD-1. (Left panel): The mean ± SD tumor volume for each treatment group (n = 10) is shown. (Right panel): Individual mice were sacrificed when tumors exceeded 3000 mm3 and survival for each group is shown.
Figure 4
Figure 4
Antitumor activity of opaganib in combination with anti-CTLA-4 antibody. LLC cells were grown as xenografts and treated with the vehicle; opaganib alone (50 mg/kg/day, 5 days/week); anti-CTLA-4 antibody (200 μg/mouse intraperitoneally, 6 times); or opaganib+anti-CTLA-4. (Left panel): The mean ± SD tumor volume for each treatment group (n = 5) is shown. (Right panel): Individual mice were sacrificed when tumors exceeded 3000 mm3 and survival for each group is shown.
Figure 5
Figure 5
Model for antitumor activity of opaganib. Opaganib acts as a sphingosine-competitive inhibitor of SK2 suppressing signaling through multiple pathways in tumor cells and thereby inhibiting proliferation, survival and inflammation. These pathways are also known to regulate PD-L1 expression allowing opaganib to also suppress antitumor immunity.

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