Naive T cells sense the cysteine protease allergen papain through protease-activated receptor 2 and propel TH2 immunity

J Allergy Clin Immunol. 2012 May;129(5):1377-1386.e13. doi: 10.1016/j.jaci.2012.02.035. Epub 2012 Mar 27.

Abstract

Background: Sensitization to protease allergens, such as papain, or helminth infection is associated with basophil recruitment to draining lymph nodes (LNs). Basophils have the capacity to present antigen to naive T cells and promote T(H)2 differentiation directly or indirectly through IL-4 production.

Objective: We studied how papain induces basophil migration to LNs and the contribution of various leukocytes to papain-induced immune responses.

Methods: We immunized mice in the footpad with papain and studied leukocyte recruitment and inflammatory cytokine and chemokine production in the draining popliteal LNs.

Results: Papain directly activated naive T cells through protease-activated receptor (PAR) 2 to initiate a chemokine/cytokine program that includes CCL17, CCL22, and IL-4. Papain-triggered innate immune responses were dependent on both CD4 T cells and PAR2 and were strongly reduced in the absence of CCR4, the primary receptor for CCL17/CCL22.

Conclusion: These results elucidate a novel innate allergen-recognition pathway mediated by naive T cells through PAR2, which provide an immediate source of chemokines and IL-4 upstream of basophils and antigen-restricted T(H)2 differentiation. PAR2 antagonism might thus hold promise for the treatment of allergic disease.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural

MeSH terms

  • Allergens / adverse effects
  • Allergens / immunology
  • Animals
  • Antigen Presentation
  • Basophils / immunology
  • Basophils / metabolism
  • Basophils / pathology
  • Cells, Cultured
  • Cysteine Proteases / immunology
  • Cysteine Proteases / metabolism*
  • Cytokines / genetics
  • Cytokines / immunology
  • Cytokines / metabolism
  • Hypersensitivity / immunology*
  • Immunity
  • Immunization
  • Immunologic Memory
  • Lymph Nodes / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Papain / immunology
  • Papain / metabolism*
  • Receptor, PAR-2 / genetics
  • Receptor, PAR-2 / immunology
  • Receptor, PAR-2 / metabolism*
  • Receptors, CCR4 / genetics
  • Receptors, CCR4 / metabolism
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*
  • T-Lymphocyte Subsets / pathology
  • Th2 Cells / immunology
  • Th2 Cells / metabolism*
  • Th2 Cells / pathology

Substances

  • Allergens
  • Ccr4 protein, mouse
  • Cytokines
  • Receptor, PAR-2
  • Receptors, CCR4
  • Cysteine Proteases
  • Papain