Nitric oxide-producing myeloid-derived suppressor cells inhibit vascular E-selectin expression in human squamous cell carcinomas

J Invest Dermatol. 2012 Nov;132(11):2642-51. doi: 10.1038/jid.2012.190. Epub 2012 Jun 21.

Abstract

Squamous cell carcinomas (SCCs) are sun-induced skin cancers that are particularly numerous and aggressive in immunosuppressed individuals. SCCs evade immune detection at least in part by downregulating E-selectin on tumor vessels, thereby restricting entry of skin-homing T cells into tumors. We find that nitric oxide (NO) potently suppresses E-selectin expression on human endothelial cells and that SCCs are infiltrated by NO-producing iNOS(+) CD11b(+) CD33(+) CD11c(-) HLA-DR(-) myeloid-derived suppressor cells (MDSCs). MDSCs from SCCs produced NO, transforming growth factor-β (TGF-β), and arginase, and inhibited endothelial E-selectin expression in vitro. MDSCs from SCCs expressed the chemokine receptor CCR2 (chemokine (C-C motif) receptor 2) and tumors expressed the CCR2 ligand human β-defensin 3 (HBD3), suggesting that CCR2/HBD3 interactions may contribute to MDSC recruitment to SCCs. Treatment of SCCs in vitro with the inducible nitric oxide synthase (iNOS) inhibitor N(ω)-nitro-L-arginine(L-NNA) induced E-selectin expression at levels comparable to imiquimod-treated SCCs undergoing immunologic destruction. Our results suggest that local production of NO in SCCs may impair vascular E-selectin expression. We show that MDSCs are critical producers of NO in SCCs and that NO inhibition restores vascular E-selectin expression, potentially enhancing T-cell recruitment. The iNOS inhibitors and other therapies that reduce NO production may therefore be effective in the treatment of SCCs and their premalignant precursor lesions, actinic keratoses.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antigens, Differentiation, T-Lymphocyte / metabolism
  • Arginase / genetics
  • Arginase / metabolism
  • CD11b Antigen / metabolism
  • CD11c Antigen / metabolism
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism*
  • Carcinoma, Squamous Cell / pathology
  • Dermis / cytology
  • E-Selectin / genetics
  • E-Selectin / metabolism*
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation, Neoplastic / physiology
  • HLA-DR Antigens / metabolism
  • Human Umbilical Vein Endothelial Cells
  • Humans
  • Membrane Glycoproteins / metabolism
  • Myeloid Cells / metabolism*
  • Myeloid Cells / pathology
  • Nitric Oxide / metabolism*
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / metabolism
  • Nitroarginine / pharmacology
  • Receptors, CCR2 / genetics
  • Receptors, CCR2 / metabolism
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism*
  • Skin Neoplasms / pathology
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology

Substances

  • Antigens, Differentiation, T-Lymphocyte
  • CCR2 protein, human
  • CD11b Antigen
  • CD11c Antigen
  • CTAGE1 protein, human
  • E-Selectin
  • Enzyme Inhibitors
  • HLA-DR Antigens
  • ITGAM protein, human
  • Membrane Glycoproteins
  • Receptors, CCR2
  • Nitroarginine
  • Nitric Oxide
  • NOS2 protein, human
  • Nitric Oxide Synthase Type II
  • ARG1 protein, human
  • Arginase