Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer

Immunity. 2013 Oct 17;39(4):782-95. doi: 10.1016/j.immuni.2013.10.003.

Abstract

The complex interactions between tumors and their microenvironment remain to be elucidated. Combining large-scale approaches, we examined the spatio-temporal dynamics of 28 different immune cell types (immunome) infiltrating tumors. We found that the immune infiltrate composition changed at each tumor stage and that particular cells had a major impact on survival. Densities of T follicular helper (Tfh) cells and innate cells increased, whereas most T cell densities decreased along with tumor progression. The number of B cells, which are key players in the core immune network and are associated with prolonged survival, increased at a late stage and showed a dual effect on recurrence and tumor progression. The immune control relevance was demonstrated in three endoscopic orthotopic colon-cancer mouse models. Genomic instability of the chemokine CXCL13 was a mechanism associated with Tfh and B cell infiltration. CXCL13 and IL21 were pivotal factors for the Tfh/B cell axis correlating with survival. This integrative study reveals the immune landscape in human colorectal cancer and the major hallmarks of the microenvironment associated with tumor progression and recurrence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / pathology
  • Carcinoma / genetics
  • Carcinoma / immunology*
  • Carcinoma / mortality
  • Carcinoma / pathology
  • Cell Movement
  • Chemokine CXCL13 / genetics
  • Chemokine CXCL13 / immunology*
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Humans
  • Immunity, Innate
  • Interleukins / genetics
  • Interleukins / immunology*
  • Lymphocyte Count
  • Mice
  • Neoplasm Recurrence, Local / genetics
  • Neoplasm Recurrence, Local / immunology*
  • Neoplasm Recurrence, Local / mortality
  • Neoplasm Recurrence, Local / pathology
  • Neoplasm Staging
  • Protein Stability
  • Survival Analysis
  • T-Lymphocytes, Helper-Inducer / immunology*
  • T-Lymphocytes, Helper-Inducer / pathology
  • Tumor Microenvironment / immunology

Substances

  • CXCL13 protein, human
  • Chemokine CXCL13
  • Interleukins
  • interleukin-21