Regulation of Cutaneous Immunity In Vivo by Calcitonin Gene-Related Peptide Signaling through Endothelial Cells

J Immunol. 2022 Feb 1;208(3):633-641. doi: 10.4049/jimmunol.2100139. Epub 2022 Jan 14.

Abstract

Calcitonin gene-related peptide (CGRP) can bias the outcome of Ag presentation to responsive T cells in vitro away from Th1-type immunity and toward the Th2 and Th17 poles through actions on endothelial cells (ECs). To test the in vivo significance of this observation, we engineered a mouse lacking functional CGRP receptors on ECs (EC receptor activity modifying protein 1 [RAMP1] knockout mice). On percutaneous immunization to 1-fluoro-2,4-dinitrobenzene, stimulated CD4+ T cells from draining lymph nodes showed significantly reduced IL-17A expression with significantly increased IFN-γ, IL-4, and IL-22 expression at the protein and mRNA levels compared with control mice. Retinoic acid receptor-related orphan receptor γ t mRNA was significantly reduced, while mRNAs for T-box expressed in T cells and GATA binding protein 3 were significantly increased. In addition, EC RAMP1 knockout mice had significantly reduced contact hypersensitivity responses, and systemic administration of a CGRP receptor antagonist similarly inhibited contact hypersensitivity in wild-type mice. These observations provide compelling evidence that CGRP is a key regulator of cutaneous immunity through effects on ECs and suggest a novel pathway for potential therapeutic manipulation.

Publication types

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

MeSH terms

  • Animals
  • Antigen Presentation / immunology
  • Calcitonin Gene-Related Peptide / genetics*
  • Calcitonin Gene-Related Peptide / metabolism
  • Dermatitis, Contact / immunology*
  • Dinitrofluorobenzene / immunology
  • Endothelial Cells / immunology*
  • GATA3 Transcription Factor / metabolism
  • Interferon-gamma / biosynthesis
  • Interleukin-17 / biosynthesis
  • Interleukin-22
  • Interleukin-4 / biosynthesis
  • Interleukins / biosynthesis
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nuclear Receptor Subfamily 1, Group F, Member 1 / genetics
  • Receptor Activity-Modifying Protein 1 / genetics*
  • Skin / immunology*
  • Th1 Cells / immunology
  • Th17 Cells / immunology
  • Th2 Cells / immunology

Substances

  • GATA3 Transcription Factor
  • Gata3 protein, mouse
  • IFNG protein, mouse
  • Il17a protein, mouse
  • Il4 protein, mouse
  • Interleukin-17
  • Interleukins
  • Nuclear Receptor Subfamily 1, Group F, Member 1
  • Ramp1 protein, mouse
  • Receptor Activity-Modifying Protein 1
  • Rora protein, mouse
  • Interleukin-4
  • Interferon-gamma
  • Dinitrofluorobenzene
  • Calcitonin Gene-Related Peptide