Deciphering the longitudinal trajectories of glioblastoma ecosystems by integrative single-cell genomics

Avishay Spitzer, Kevin C. Johnson, Masashi Nomura, Luciano Garofano, Djamel Nehar-belaid, Noam Galili Darnell, Alissa C. Greenwald, Lillian Bussema, Young Taek Oh, Frederick S. Varn, Fulvio D’Angelo, Simon Gritsch, Kevin J. Anderson, Simona Migliozzi, L. Nicolas Gonzalez Castro, Tamrin Chowdhury, Nicolas Robine, Catherine Reeves, Jong Bae Park, Anuja LipsaFrank Hertel, Anna Golebiewska, Simone P. Niclou, Labeeba Nusrat, Sorcha Kellet, Sunit Das, Hyo Eun Moon, Sun Ha Paek, Franck Bielle, Alice Laurenge, Anna Luisa Di Stefano, Bertrand Mathon, Alberto Picca, Marc Sanson, Shota Tanaka, Nobuhito Saito, David M. Ashley, Stephen T. Keir, Keith L. Ligon, Jason T. Huse, W. K.Alfred Yung, Anna Lasorella*, Antonio Iavarone*, Roel G.W. Verhaak*, Itay Tirosh*, Mario L. Suvà*

*Corresponding author for this work

Research output: Contribution to journalArticleResearchpeer-review

1 Citation (Scopus)

Abstract

The evolution of isocitrate dehydrogenase (IDH)-wildtype glioblastoma (GBM) after standard-of-care therapy remains poorly understood. Here we analyzed matched primary and recurrent GBMs from 59 patients using single-nucleus RNA sequencing and bulk DNA sequencing, assessing the longitudinal evolution of the GBM ecosystem across layers of cellular and molecular heterogeneity. The most consistent change was a lower malignant cell fraction at recurrence and a reciprocal increase in glial and neuronal cell types in the tumor microenvironment (TME). The predominant malignant cell state differed between most matched pairs, but no states were exclusive or highly enriched in either time point, nor was there a consistent longitudinal trajectory across the cohort. Nevertheless, specific trajectories were enriched in subsets of patients. Changes in malignant state abundances mirrored changes in TME composition and baseline profiles, reflecting the co-evolution of the GBM ecosystem. Our study provides a blueprint of GBM’s diverse longitudinal trajectories and highlights the treatment and TME modifiers that shape them.

Original languageEnglish
Article number1088
Pages (from-to)1168-1178
Number of pages28
JournalNature Genetics
Volume57
Issue number5
DOIs
Publication statusPublished - 9 May 2025

Keywords

  • Humans
  • Glioblastoma/genetics
  • Tumor Microenvironment/genetics
  • Single-Cell Analysis/methods
  • Brain Neoplasms/genetics
  • Genomics/methods
  • Isocitrate Dehydrogenase/genetics
  • Male
  • Longitudinal Studies
  • Female
  • Neoplasm Recurrence, Local/genetics
  • Middle Aged

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