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[Preprint]. 2023 Mar 25:2023.03.24.534105. [Version 1] doi: 10.1101/2023.03.24.534105

Glioblastoma induces the recruitment and differentiation of hybrid neutrophils from skull bone marrow

By Meeki Lad, Angad S Beniwal, Saket Jain, Poojan Shukla, Jangham Jung, Sumedh S Shah, Garima Yagnik, Husam Babikir, Alan T Nguyen, Sabraj Gill, Jacob S Young, Austin Lui, Diana Salha, Aaron Diaz, Manish K Aghi
PMCID: PMC10055347  PMID: 36993266

SUMMARY

Tumor-associated neutrophil (TAN) effects on glioblastoma biology remain under-characterized. We show here that ‘hybrid’ neutrophils with dendritic features – including morphological complexity, expression of antigen presentation genes, and the ability to process exogenous peptide and stimulate MHCII-dependent T cell activation – accumulate intratumorally and suppress tumor growth in vivo . Trajectory analysis of patient TAN scRNA-seq identifies this phenotype as a polarization state which is distinct from canonical cytotoxic TANs and differentiates intratumorally from immature precursors absent in circulation. Rather, these hybrid-inducible immature neutrophils – which we identified in patient and murine glioblastomas – arise from local skull marrow. Through labeled skull flap transplantation and targeted ablation, we characterize calvarial marrow as a potent contributor of antitumoral myeloid APCs, including hybrid TANs and dendritic cells, which elicit T cell cytotoxicity and memory. As such, agents augmenting neutrophil egress from skull marrow – such as intracalvarial AMD3100 whose survival prolonging-effect in GBM we demonstrate – present therapeutic potential.

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