Role of IL-33 receptor (ST2) deletion in diaphragm contractile and mitochondrial function in the Sugen5416/hypoxia model of pulmonary hypertension

Respir Physiol Neurobiol. 2022 Jan:295:103783. doi: 10.1016/j.resp.2021.103783. Epub 2021 Sep 8.

Abstract

Pulmonary arterial hypertension (PAH) is a progressive disease of the pulmonary vasculature that leads to right ventricular failure. Skeletal muscle maladaptations limit physical activity and may contribute to disease progression. The role of alarmin/inflammatory signaling in PAH respiratory muscle dysfunction is unknown. We hypothesized that diaphragm mitochondrial and contractile functions are impaired in SU5416/hypoxia-induced pulmonary hypertension due to increased systemic IL-33 signaling. We induced pulmonary hypertension in adult C57Bl/6 J (WT) and ST2 (IL1RL1) gene ablated mice by SU5416/hypoxia (SuHx). We measured diaphragm fiber mitochondrial respiration, inflammatory markers, and contractile function ex vivo. SuHx reduced coupled and uncoupled permeabilized myofiber respiration by ∼40 %. During coupled respiration with complex I substrates, ST2-/- attenuated SuHx inhibition of mitochondrial respiration (genotype × treatment interaction F[1,67] = 3.3, p = 0.07, η2 = 0.04). Flux control ratio and coupling efficiency were not affected by SuHx or genotype. A higher substrate control ratio for succinate was observed in SuHx fibers and attenuated in ST2-/- fibers (F[1,67] = 5.3, p < 0.05, η2 = 0.07). Diaphragm TNFα, but not IL-33 or NFkB, was increased in SuHx vs. DMSO in both genotypes (F[1,43] = 4.7, p < 0.05, η2 = 0.1). Diaphragm force-frequency relationships were right-shifted in SuHx vs. WT (F[3,440] = 8.4, p < 0.05, η2 = 0.0025). There was no effect of ST2-/- on the force-frequency relationship. Force decay during a fatigue protocol at 100 Hz, but not at 40 Hz, was attenuated by SuHx vs. DMSO in both genotypes (F[1,41] = 5.6, p < 0.05, η2 = 0.11). SuHx mice exhibit a modest compensation in diaphragm contractility and mitochondrial dysfunction during coupled respiration; the latter partially regulated through ST2 signaling.

Keywords: Diaphragm; Mitochondria; Pulmonary hypertension; Respirometry; SU5416.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Diaphragm / physiopathology*
  • Disease Models, Animal
  • Hypertension, Pulmonary / physiopathology*
  • Hypoxia / chemically induced
  • Hypoxia / physiopathology*
  • Indoles / pharmacology
  • Interleukin-1 Receptor-Like 1 Protein / genetics
  • Interleukin-1 Receptor-Like 1 Protein / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mitochondria / physiology*
  • Mitochondrial Diseases / genetics
  • Mitochondrial Diseases / physiopathology*
  • Muscle Contraction / physiology*
  • Protein Kinase Inhibitors / pharmacology
  • Pulmonary Arterial Hypertension / physiopathology*
  • Pyrroles / pharmacology

Substances

  • Il1rl1 protein, mouse
  • Indoles
  • Interleukin-1 Receptor-Like 1 Protein
  • Protein Kinase Inhibitors
  • Pyrroles
  • Semaxinib