Crosstalk between keratinocytes and T cells in a 3D microenvironment: a model to study inflammatory skin diseases

J Invest Dermatol. 2014 Mar;134(3):719-727. doi: 10.1038/jid.2013.417. Epub 2013 Oct 11.

Abstract

The interaction between keratinocytes and immune cells plays a major role in the development of inflammatory skin diseases like psoriasis and atopic dermatitis. Pharmacological intervention to inhibit T cell-derived proinflammatory mediators is an effective therapy in the treatment of psoriasis. Here, we present a model to study the interaction between keratinocytes and T cells in a three-dimensional (3D) microenvironment, based on human skin equivalents populated with CD4+ T cells. T cell migration into the dermis initiated keratinocyte activation within 2 days, with hallmarks of a psoriasiform inflammation after 4 days. Expression of epidermal psoriasis marker genes was upregulated, and proinflammatory cytokines and chemokines were highly expressed. Disturbed epidermal differentiation was shown by downregulated filaggrin expression and involucrin expression in the spinous layer. These effects were mediated via soluble factors produced by the T cells. The psoriasiform inflammation was also observed using T helper type 1 (Th1)- and Th17-polarized CD4+ T cells. We validated our model by treatment with anti-inflammatory drugs that reduced the expression of proinflammatory cytokines and chemokines and suppressed the psoriasiform inflammation. We propose that our T cell-driven inflammatory skin equivalent model has potential to study the pathogenesis of inflammatory skin diseases and may serve as a preclinical screening tool for anti-inflammatory drugs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Inflammatory Agents / pharmacology
  • CD4-Positive T-Lymphocytes / cytology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • Cell Communication / drug effects
  • Cell Communication / immunology*
  • Cell Culture Techniques / methods
  • Cell Movement / drug effects
  • Cell Movement / immunology
  • Dermatitis, Atopic / immunology*
  • Dermatitis, Atopic / metabolism
  • Dermatitis, Atopic / pathology
  • Dermis / cytology
  • Dermis / immunology
  • Dermis / metabolism
  • Filaggrin Proteins
  • Humans
  • Keratinocytes / cytology
  • Keratinocytes / immunology*
  • Keratinocytes / metabolism
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / immunology
  • Primary Cell Culture
  • Psoriasis / immunology*
  • Psoriasis / metabolism
  • Psoriasis / pathology
  • Receptor Cross-Talk / immunology*
  • Th1 Cells / cytology
  • Th1 Cells / immunology
  • Th1 Cells / metabolism
  • Th17 Cells / cytology
  • Th17 Cells / immunology
  • Th17 Cells / metabolism

Substances

  • Anti-Inflammatory Agents
  • FLG protein, human
  • Filaggrin Proteins