Pharmacological blockade of HDAC6 attenuates cancer progression by inhibiting IL-1β and modulating immunosuppressive response in OSCC

Int Immunopharmacol. 2024 May 10:132:111921. doi: 10.1016/j.intimp.2024.111921. Epub 2024 Mar 27.

Abstract

Interleukin-1-beta (IL-1β) one of the biomarkers for oral squamous cell carcinoma (OSCC), is upregulated in tumor-microenvironment (TME) and associated with poor patient survival. Thus, a novel modulator of IL-1β would be of great therapeutic value for OSCC treatment. Here we report regulation of IL-1β and TME by histone deacetylase-6 (HDAC6)-inhibitor in OSCC. We observed significant upregulation of HDAC6 in 4-nitroquniline (4-NQO)-induced OSCC in mice and 4-NQO & Lipopolysaccharide (LPS) stimulated OSCC and fibroblast cells. Tubastatin A (TSA)-attenuated the OSCC progression in mice as observed improvement in the histology over tongue and esophagus, with reduced tumor burden. TSA treatment to 4-NQO mice attenuated protein expression of HDAC6, pro-and-mature-IL-1β and pro-and-cleaved-caspase-1 and ameliorated acetylated-tubulin. In support of our experimental work, human TCGA analysis revealed HDAC6 and IL-1β were upregulated in the primary tumor, with different tumor stages and grades. We found TSA modulate TME, indicated by downregulation of CD11b+Gr1+-Myeloid-derived suppressor cells, CD11b+F4/80+CD206+ M2-macrophages and increase in CD11b+F4/80+MHCII+ M1-macrophages. TSA significantly reduced the gene expression of HDAC6, IL-1β, Arginase-1 and iNOS in isolated splenic-MDSCs. FaDu-HTB-43 and NIH3T3 cells stimulated with LPS and 4-NQO exhibit higher IL-1β levels in the supernatant. Interestingly, immunoblot analysis of the cell lysate, we observed that TSA does not alter the expression as well as activation of IL-1β and caspase-1 but the acetylated-tubulin was found to be increased. Nocodazole pre-treatment proved that TSA inhibited the lysosomal exocytosis of IL-1β through tubulin acetylation. In conclusion, HDAC6 inhibitors attenuated TME and cancer progression through the regulation of IL-1β in OSCC.

Keywords: HDAC6; IL-1β; OSCC; Tubastatin A.

MeSH terms

  • Animals
  • Carcinoma, Squamous Cell / drug therapy
  • Carcinoma, Squamous Cell / immunology
  • Carcinoma, Squamous Cell / pathology
  • Cell Line, Tumor
  • Disease Progression
  • Histone Deacetylase 6* / antagonists & inhibitors
  • Histone Deacetylase 6* / metabolism
  • Histone Deacetylase Inhibitors* / pharmacology
  • Histone Deacetylase Inhibitors* / therapeutic use
  • Humans
  • Hydroxamic Acids* / pharmacology
  • Hydroxamic Acids* / therapeutic use
  • Indoles*
  • Interleukin-1beta* / metabolism
  • Lipopolysaccharides
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mouth Neoplasms* / drug therapy
  • Mouth Neoplasms* / immunology
  • Mouth Neoplasms* / pathology
  • Myeloid-Derived Suppressor Cells / drug effects
  • Myeloid-Derived Suppressor Cells / immunology
  • Tubulin / metabolism
  • Tumor Microenvironment* / drug effects
  • Tumor Microenvironment* / immunology

Substances

  • Histone Deacetylase 6
  • Interleukin-1beta
  • Histone Deacetylase Inhibitors
  • tubastatin A
  • Hydroxamic Acids
  • HDAC6 protein, human
  • Hdac6 protein, mouse
  • Tubulin
  • Lipopolysaccharides
  • Indoles