TLR4 expression and functionality are downregulated in glioblastoma cells and in tumor-associated macrophages: A new mechanism of immune evasion?

Biochim Biophys Acta Mol Basis Dis. 2021 Aug 1;1867(8):166155. doi: 10.1016/j.bbadis.2021.166155. Epub 2021 Apr 28.

Abstract

Glioblastoma (GB) is the most common and aggressive form of primary brain tumor, in which the presence of an inflammatory environment, composed mainly by tumor-associated macrophages (TAMs), is related to its progression and development of chemoresistance. Toll-Like Receptors (TLRs) are key components of the innate immune system and their expression in both tumor and immune-associated cells may impact the cell communication in the tumor microenvironment (TME), further modeling cancer growth and response to therapy. Here, we investigated the participation of TLR4-mediated signaling as a mechanism of induced-immune escape in GB. Initially, bioinformatics analysis of public datasets revealed that TLR4 expression is lower in GB tumors when compared to astrocytomas (AST), and in a subset of TAMs. Further, we confirmed that TLR4 expression is downregulated in chemoresistant GB, as well as in macrophages co-cultured with GB cells. Additionally, TLR4 function is impaired in those cells even following stimulation with LPS, an agonist of TLR4. Finally, experiments performed in a cohort of clinical primary and metastatic brain tumors indicated that the immunostaining of TLR4 and CD45 are inversely proportional, and confirmed the low TLR4 expression in GBs. Interestingly, the cytoplasmic/nuclear pattern of TLR4 staining in cancer tissues suggests additional roles of this receptor in carcinogenesis. Overall, our data suggest the downregulation of TLR4 expression and activity as a strategy for GB-associated immune escape. Additional studies are necessary to better understand TLR4 signaling in TME in order to improve the benefits of immunotherapy based on TLR signaling.

Keywords: Chemoresistance; Glioblastoma; Immune evasion; Macrophages; TLR4.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Brain Neoplasms / immunology*
  • Brain Neoplasms / metabolism
  • Cell Line
  • Cell Line, Tumor
  • Cell Proliferation / physiology
  • Down-Regulation / immunology*
  • Female
  • Glioblastoma / immunology*
  • Glioblastoma / metabolism*
  • Humans
  • Immune Evasion / immunology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Signal Transduction / immunology
  • Toll-Like Receptor 4 / immunology*
  • Toll-Like Receptor 4 / metabolism
  • Tumor Microenvironment / immunology
  • Tumor-Associated Macrophages / immunology*
  • Tumor-Associated Macrophages / metabolism

Substances

  • TLR4 protein, human
  • Toll-Like Receptor 4