Function-Blocking RHAMM Peptides Attenuate Fibrosis and Promote Antifibrotic Adipokines in a Bleomycin-Induced Murine Model of Systemic Sclerosis

J Invest Dermatol. 2021 Jun;141(6):1482-1492.e4. doi: 10.1016/j.jid.2019.11.032. Epub 2020 Nov 23.

Abstract

Systemic sclerosis a chronic, fibrotic disorder associated with high disease-specific mortality and morbidity. Cutaneous manifestations include dermal thickening and obliteration of dermal adipose tissue. Accumulation of low-molecular-weight hyaluronan, which signals through the receptor for hyaluronan-mediated motility, RHAMM, leads to progressive fibrosis and is correlated with increased severity of systemic sclerosis. The purpose of this study is to test the efficacy of two function-blocking RHAMM peptides, NPI-110 and NPI-106, in reducing skin fibrosis in a bleomycin-induced mouse model of systemic sclerosis. NPI-110 reduced visible measures of fibrosis (dermal thickness and collagen production, deposition, and organization) and profibrotic gene expression (Tgfb1, c-Myc, Col1a1, Col3a1). NPI-110 treatment also increased the expression of the antifibrotic adipokines perilipin and adiponectin. Both RHAMM peptides strongly reduced dermal RHAMM expression, predicting that dermal fibroblasts are peptide targets. Transcriptome and cell culture analyses using Rhamm-/- and Rhamm-rescued dermal fibroblasts reveal a TGFβ1/RHAMM/MYC signaling axis that promotes fibrogenic gene expression and myofibroblast differentiation. RHAMM function‒blocking peptides suppress this signaling and prevent TGFβ1-induced myofibroblast differentiation. These results suggest that inhibiting RHAMM signaling will offer a treatment method for cutaneous fibrosis in systemic sclerosis.

MeSH terms

  • Adipokines / metabolism*
  • Animals
  • Bleomycin / administration & dosage
  • Bleomycin / toxicity
  • Cell Differentiation / drug effects
  • Disease Models, Animal
  • Extracellular Matrix Proteins / antagonists & inhibitors*
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism
  • Female
  • Fibrosis
  • Humans
  • Hyaluronan Receptors / antagonists & inhibitors*
  • Hyaluronan Receptors / genetics
  • Hyaluronan Receptors / metabolism
  • Mice
  • Mice, Knockout
  • Peptides / pharmacology*
  • Peptides / therapeutic use
  • Proto-Oncogene Proteins c-myc / metabolism
  • Scleroderma, Systemic / chemically induced
  • Scleroderma, Systemic / drug therapy*
  • Scleroderma, Systemic / pathology
  • Signal Transduction / drug effects
  • Skin / drug effects
  • Skin / pathology*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Adipokines
  • Extracellular Matrix Proteins
  • Hyaluronan Receptors
  • Myc protein, mouse
  • Peptides
  • Proto-Oncogene Proteins c-myc
  • Tgfb1 protein, mouse
  • Transforming Growth Factor beta1
  • hyaluronan-mediated motility receptor
  • Bleomycin