RAMP1 Signaling Mitigates Acute Lung Injury by Distinctively Regulating Alveolar and Monocyte-Derived Macrophages

Int J Mol Sci. 2024 Sep 20;25(18):10107. doi: 10.3390/ijms251810107.

Abstract

Acute respiratory distress syndrome (ARDS) is a life-threatening lung injury that induces cytokine hypersecretion. Receptor activity-modifying protein (RAMP) 1, a subunit of the calcitonin gene-related peptide (CGRP) receptor, regulates the production of cytokines. This study examined the role of RAMP1 signaling during lipopolysaccharide (LPS)-induced acute lung injury (ALI). LPS administration to wild-type (WT) mice depleted alveolar macrophages (AMs) and recruited monocyte-derived macrophages (MDMs) and neutrophils. RAMP1-deficient (RAMP1-/-) mice exhibited higher lung injury scores, cytokine levels, and cytokine-producing neutrophil infiltration. RAMP1-deficient AMs produced more cytokines in response to LPS than WT AMs. Adoptive transfer of RAMP1-deficient AMs to RAMP1-/- mice increased cytokine levels and neutrophil accumulation compared to the transfer of WT AMs. RAMP1-/- mice had reduced MDM recruitment and lower pro-inflammatory and reparative macrophage profiles. Cultured bone marrow (BM)-derived RAMP1-deficient macrophages stimulated with LPS showed decreased expression of pro-inflammatory and pro-repairing genes. CGRP administration to WT mice reduced cytokine production and neutrophil accumulation. These findings indicate that RAMP1 signaling mitigates LPS-induced ALI by inactivating AMs and promoting inflammatory and repair activities of MDMs. Targeting RAMP1 signaling presents a potential therapeutic approach for the treatment of ARDS.

Keywords: RAMP1; immunity; macrophage; nerve; neutrophil.

MeSH terms

  • Acute Lung Injury* / chemically induced
  • Acute Lung Injury* / genetics
  • Acute Lung Injury* / metabolism
  • Acute Lung Injury* / pathology
  • Animals
  • Cytokines* / metabolism
  • Lipopolysaccharides*
  • Macrophages / metabolism
  • Macrophages, Alveolar* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / metabolism
  • Receptor Activity-Modifying Protein 1* / genetics
  • Receptor Activity-Modifying Protein 1* / metabolism
  • Signal Transduction*

Substances

  • Receptor Activity-Modifying Protein 1
  • Lipopolysaccharides
  • Cytokines
  • Ramp1 protein, mouse

Grants and funding

This research was funded by grants from the Japanese Ministry of Education, Culture, Sports, Science, and Technology (MEXT) (22K06651), the Integrative Research Program of the Graduate School of Medical Science at Kitasato University, and the Parents’ Association Grant of the Kitasato University School of Medicine.