Background
Patients diagnosed with diffuse midline glioma (DMG) have an overall survival of 9-11 months, with radiotherapy the only approved treatment. DMG is characterised by a cold tumour microenvironment (TME), with few tumour infiltrating lymphocytes (TILs) and inflammatory factors, likely explaining the failure of immune checkpoint inhibition (ICI). The cause of the cold TME remains uncertain, as the tumour does not harbour known immunosuppressive features. The cold TME seen in glioblastoma can be explained by systemic T cell lymphopenia.1 In glioblastoma, T cells are sequestered in the bone marrow due to loss of Sphingosine-1-phosphate receptor 1 (S1PR1) expression. S1PR1 internalization is driven by recruitment of β-arrestin, which is activated by Dopamine receptor D2 and D3 (DRD2, DRD3) signalling. ONC201 is a potent DRD2/DRD3 antagonist, showing some clinical efficacy as monotherapy for patients with DMG in the upfront setting. Work from our laboratory has informed the recently commenced DMG clinical trial NCT05009992, investigating radiotherapy, and ONC201 used in combination with the PI3K inhibitor paxalisib as maintenance. Importantly, PIK3CA knockout promotes expression of the major histocompatibility complex I (MHC I) increasing an adaptive immune response, with PI3K inhibitors working synergistically with ICIs highlighting the role of PI3K inhibition in immunomodulation.2,3
Aims
To determine whether T cell lymphopenia occurs in DMG patients/models and whether DRD2/DRD3 antagonism using ONC201 + paxalisib can warm the cold TME, sensitising DMG to immunotherapies.
Methods
Proteomic profiling was performed using DMG patient derived cells +/- ONC201. Western blot and immunohistochemistry analysis was performed on tumours from SU-DIPG-VI patient derived xenograft (PDX) NSG mouse models treated +/- ONC201 and in combination with paxalisib.
Results
ONC201 treatment increased the expression of members of the MHC I antigen presentation pathway, including B2M and HLA-A, illuminating DMG to the immune system. Increased B2M expression following ONC201 was confirmed in DMG-PDX models, also revealing further increase of B2M expression when combined with paxalisib. For the first time, we uncover a therapeutic means to promote recruitment of TILs through the combination of ONC201 and paxalisib. Preliminary mechanistic studies suggest that ONC201 and paxalisib increase MHC I activity, decrease dopamine signalling and promote the expression of EMILIN-3 a potent antagonist of immunosuppressive TGF-β, known to inhibit B2M expression.
Conclusion
Antagonism of DRD2/DRD3 with ONC201 primes DMG for an immune response, amplified with paxalisib. Work continues to understand T cell lymphopenia in DMG and whether DRD2/DRD3 antagonism can reverse the phenotype and sensitize DMG to immunotherapies.