Leukocyte infiltrate in gastrointestinal adenocarcinomas is strongly associated with tumor microsatellite instability but not with tumor immunogenicity

Cancer Immunol Immunother. 2011 Jun;60(6):869-82. doi: 10.1007/s00262-011-0999-1. Epub 2011 Mar 13.

Abstract

Purpose: To analyze the correlation of genomic instability with leukocyte infiltrate in gastrointestinal carcinomas (GIACs) and with tumor immunogenicity, e.g., HLA class I cell surface expression defects and galectin-3 and PDL-1 expression.

Experimental design: Lymphocyte and macrophage infiltrations were immunohistochemically studied in HLA class I negative GIACs with sporadic high-level microsatellite instability (MSI-H) or microsatellite stability (MSS).

Results: Tumors with MSI-H were associated with the following: dense infiltration (CD45, P < 0.001); cytotoxic CD8-positive lymphocytes (P < 0.001); and a complete absence of HLA class I cell surface expression, due to inactivating β2-microglobulin (β2-m) mutation in 50% of cases. In contrast, HLA class I negative tumors with MSS were significantly associated with fewer CD8-positive lymphocytes. There was no association between microsatellite instability and other molecular features of the tumor cells, including expression of galectin-3. Finally, macrophage infiltrate in the tumors was not correlated with microsatellite instability or HLA class I cell surface expression (CD64, P = 0.63; CD163, P = 0.51).

Conclusions: Microsatellite instability appears to be the most important factor determining the composition, density, and localization of leukocyte infiltrate, which is independent of other molecular features such expression of HLA class I cells, galectin-3, or programmed death ligand-1. Accordingly, the strong intratumoral CD8+ T infiltration of MSI-H tumors may be produced by elevated levels of specific inflammatory chemokines in the tumor microenvironment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / genetics*
  • Adenocarcinoma / immunology*
  • Adenocarcinoma / pathology
  • Adult
  • Aged
  • Aged, 80 and over
  • Antigens, CD / genetics
  • Antigens, CD / immunology
  • B7-H1 Antigen
  • Down-Regulation
  • Female
  • Galectin 3 / genetics
  • Galectin 3 / immunology
  • Gastrointestinal Neoplasms / genetics*
  • Gastrointestinal Neoplasms / immunology*
  • Gastrointestinal Neoplasms / pathology
  • Histocompatibility Antigens Class I / genetics
  • Histocompatibility Antigens Class I / immunology
  • Humans
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Male
  • Microsatellite Instability*
  • Middle Aged
  • Neoplasm Staging
  • Treatment Outcome
  • beta 2-Microglobulin / genetics
  • beta 2-Microglobulin / immunology

Substances

  • Antigens, CD
  • B7-H1 Antigen
  • CD274 protein, human
  • Galectin 3
  • Histocompatibility Antigens Class I
  • beta 2-Microglobulin