Adenocarcinoma of the Uterine Cervix Shows Impaired Recruitment of cDC1 and CD8+ T Cells and Elevated β-Catenin Activation Compared with Squamous Cell Carcinoma

Clin Cancer Res. 2020 Jul 15;26(14):3791-3802. doi: 10.1158/1078-0432.CCR-19-3826. Epub 2020 Mar 27.

Abstract

Purpose: Adenocarcinoma of the uterine cervix is the second most common type of cervical cancer after squamous cell carcinoma (SCC). Although both subtypes are treated similarly, patients with adenocarcinoma have a worse prognosis. In this study, immunologic features of the tumor microenvironment in these two subsets were pursued with potential therapeutic implications.

Experimental design: The immune microenvironment of primary tumors and nonmetastatic tumor-draining lymph nodes (TDLN) was compared between patients with cervical adenocarcinoma (n = 16) and SCC (n = 20) by polychromatic flow cytometry and by transcriptional profiling of the primary tumors (n = 299) using publicly available data from The Cancer Genome Atlas (TCGA).

Results: Flow cytometric analyses revealed intact T-cell differentiation in TDLNs, but hampered effector T-cell trafficking to the primary tumors in adenocarcinoma, as compared with SCC. TCGA analysis demonstrated higher expression of chemokines involved in effector T-cell homing (CXCL9/10/11) in SCC primary tumors as compared with adenocarcinoma primary tumors, which was highly correlated to a transcriptional signature for type I conventional dendritic cells (cDC1). This was consistent with elevated frequencies of CD141/BDCA3+cDC1 in primary tumor SCC samples relative to adenocarcinoma and correspondingly elevated levels of CXCL9 and CXCL10 in 24-hour ex vivo cultures. Hampered cDC1 recruitment in adenocarcinoma was in turn related to lower transcript levels of cDC1-recruiting chemokines and an elevated β-catenin activation score and was associated with poor overall survival.

Conclusions: Our data have identified an opportunity for the investigation of potentially novel therapeutic interventions in adenocarcinoma of the cervix, that is, β-catenin inhibition and cDC1 mobilization.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / immunology*
  • Adenocarcinoma / mortality
  • Adenocarcinoma / pathology
  • Adult
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Antineoplastic Combined Chemotherapy Protocols / therapeutic use
  • CD8-Positive T-Lymphocytes / immunology*
  • Carcinoma, Squamous Cell / drug therapy
  • Carcinoma, Squamous Cell / immunology*
  • Carcinoma, Squamous Cell / mortality
  • Carcinoma, Squamous Cell / pathology
  • Cervix Uteri / immunology
  • Cervix Uteri / pathology
  • Datasets as Topic
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology*
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / immunology
  • Female
  • Gene Expression Profiling
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Lymphocyte Activation
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Middle Aged
  • Tumor Microenvironment / immunology
  • Uterine Cervical Neoplasms / drug therapy
  • Uterine Cervical Neoplasms / immunology*
  • Uterine Cervical Neoplasms / mortality
  • Uterine Cervical Neoplasms / pathology
  • beta Catenin / antagonists & inhibitors
  • beta Catenin / metabolism

Substances

  • CTNNB1 protein, human
  • Immune Checkpoint Inhibitors
  • beta Catenin