Microbiota-specific T follicular helper cells drive tertiary lymphoid structures and anti-tumor immunity against colorectal cancer

Immunity. 2021 Dec 14;54(12):2812-2824.e4. doi: 10.1016/j.immuni.2021.11.003. Epub 2021 Dec 2.

Abstract

The composition of the intestinal microbiota is associated with both the development of tumors and the efficacy of anti-tumor immunity. Here, we examined the impact of microbiota-specific T cells in anti-colorectal cancer (CRC) immunity. Introduction of Helicobacter hepaticus (Hhep) in a mouse model of CRC did not alter the microbial landscape but increased tumor infiltration by cytotoxic lymphocytes and inhibited tumor growth. Anti-tumor immunity was independent of CD8+ T cells but dependent upon CD4+ T cells, B cells, and natural killer (NK) cells. Hhep colonization induced Hhep-specific T follicular helper (Tfh) cells, increased the number of colon Tfh cells, and supported the maturation of Hhep+ tumor-adjacent tertiary lymphoid structures. Tfh cells were necessary for Hhep-mediated tumor control and immune infiltration, and adoptive transfer of Hhep-specific CD4+ T cells to Tfh cell-deficient Bcl6fl/flCd4Cre mice restored anti-tumor immunity. Thus, introduction of immunogenic intestinal bacteria can promote Tfh-associated anti-tumor immunity in the colon, suggesting therapeutic approaches for the treatment of CRC.

Keywords: T cells; T follicular helper cell; colorectal cancer; microbiome; microbiota-specific T cells; tertiary lymphoid structure; tumor microenvironment.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocyte Subsets / immunology*
  • CD4-Positive T-Lymphocytes / immunology*
  • Colon / pathology*
  • Colorectal Neoplasms / immunology*
  • Disease Models, Animal
  • Gastrointestinal Microbiome / immunology*
  • Helicobacter Infections / immunology*
  • Helicobacter hepaticus / physiology*
  • Humans
  • Killer Cells, Natural / immunology*
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Mice
  • Proto-Oncogene Proteins c-bcl-6 / genetics
  • Proto-Oncogene Proteins c-bcl-6 / metabolism
  • T Follicular Helper Cells / immunology*
  • Tertiary Lymphoid Structures / immunology*

Substances

  • Bcl6 protein, mouse
  • Proto-Oncogene Proteins c-bcl-6