Th17 cells inhibit CD8+ T cell migration by systematically downregulating CXCR3 expression via IL-17A/STAT3 in advanced-stage colorectal cancer patients

J Hematol Oncol. 2020 Jun 5;13(1):68. doi: 10.1186/s13045-020-00897-z.

Abstract

Background: CD8+ T cell trafficking to the tumor site is essential for effective colorectal cancer (CRC) immunotherapy. However, the mechanism underlying CD8+ T cell infiltration in colorectal tumor tissues is not fully understood. In the present study, we investigated CD8+ T cell infiltration in CRC tissues and the role of chemokine-chemokine receptor signaling in regulation of T cell recruitment.

Methods: We screened chemokines and cytokines in healthy donor and CRC tissues from early- and advanced-stage patients using multiplex assays and PCR screening. We also utilized transcription factor activation profiling arrays and established a xenograft mouse model.

Results: Compared with tumor tissues of early-stage CRC patients, CD8+ T cell density was lower in advanced-stage tumor tissues. PCR screening showed that CXCL10 levels were significantly increased in advanced-stage tumor tissues. CXCR3 (the receptor of CXCL10) expression on CD8+ T cells was lower in the peripheral blood of advanced-stage patients. The migratory ability of CD8+ T cells to CXCL10 depended on CXCR3 expression. Multiplex arrays showed that IL-17A was increased in advanced-stage patient sera, which markedly downregulated CXCR3 expression via activating STAT3 signaling and reduced CD8+ T cell migration. Similar results were found after CD8+ T cells were treated with Th17 cell supernatant. Adding anti-IL-17A or the STAT3 inhibitor, Stattic, rescued these effects in vitro and in vivo. Moreover, survival analysis showed that patients with low CD8 and CXCR3 expression and high IL-17A levels had significantly worse prognosis.

Conclusions: CD8+ T cell infiltration in advanced-stage tumor was systematically inhibited by Th17 cells via IL-17A/STAT3/CXCR3 axis. Our findings indicate that the T cell infiltration in the tumor microenvironment may be improved by inhibiting STAT3 signaling.

Keywords: CD8; CXCR3; Colorectal cancer; IL-17A; Th17 cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / immunology
  • Adenocarcinoma / pathology
  • Adult
  • Aged
  • Animals
  • CD8 Antigens / biosynthesis
  • CD8 Antigens / genetics
  • CD8-Positive T-Lymphocytes / immunology*
  • Cell Movement
  • Chemokine CXCL10 / physiology
  • Colorectal Neoplasms / immunology*
  • Colorectal Neoplasms / pathology
  • Cyclic S-Oxides / pharmacology
  • Down-Regulation
  • Female
  • Humans
  • Interleukin-17 / physiology*
  • Kaplan-Meier Estimate
  • Lymphocytes, Tumor-Infiltrating / immunology*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Middle Aged
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / physiology*
  • Random Allocation
  • Receptors, CXCR3 / biosynthesis
  • Receptors, CXCR3 / genetics
  • Receptors, CXCR3 / physiology*
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / physiology*
  • Th17 Cells / physiology*
  • Xenograft Model Antitumor Assays

Substances

  • CD8 Antigens
  • CXCL10 protein, human
  • CXCR3 protein, human
  • Chemokine CXCL10
  • Cyclic S-Oxides
  • IL17A protein, human
  • Interleukin-17
  • Neoplasm Proteins
  • Receptors, CXCR3
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • stattic