Childhood brain tumours instruct cranial haematopoiesis and immunotolerance

Kavli Affiliate: Arnold R. Kriegstein

| Authors: Elizabeth Alexandra Cooper, David A Posner, Colin Y. C Lee, Linda Hu, Sigourney Bonner, Jessica T Taylor, Oscar Baldwin, Rocio Jimenez-Guerrero, Katherine E Masih, Katherine Wickham Rahrmann, Jason Eigenbrood, Gina Ngo, Valar Nila Roamio Franklin, Clive D’Santos, Richard Mair, Thomas Santarius, Claudia Craven, Ibrahim Jalloh, Julia Moreno-Vicente, Timotheus Halim, Li Wang, Arnold Kriegstein, Fredrik J Swartling, Javed Khan, Menna R Clatworthy and Richard J Gilbertson

| Summary:

Recent research has revealed a remarkable role for immunosurveillance in healthy and diseased brains, dispelling the notion that this organ is a passive immune-privileged site1–3. Better understanding of how this immunosurveillance operates could improve the treatment of neurological diseases. Here, using a novel genetically engineered mouse model of ZFTA-RELA ependymoma4–a childhood brain tumour–we characterised an immune circuit between the tumour and antigen presenting, haematopoietic stem/progenitor cells (HSPCs) in the skull bone marrow. The presentation of antigens in the cerebrospinal fluid (CSF) by HSPCs to CD4+ T cells, biased HSPC lineages toward myelopoiesis and polarised CD4+ T-cells to regulatory T cells (T- regs), culminating in tumour immunotolerance. Remarkably, a single infusion of antibodies directed against cytokines enriched in the CSF of mice bearing ZFTA-RELA ependymomas, choroid plexus carcinomas or Group-3 medulloblastoma–all aggressive childhood brain tumours–disrupted this process and caused profound tumour regression. These data unmask a mechanism by which skull bone marrow-derived HSPCs and CD4+ T cells cooperate to promote the immunotolerance of childhood brain tumours. Antibodies that disrupt this immunosurveillance could prove an effective therapy for these cancers that are less toxic than current treatments.

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