Helminth infection driven gastrointestinal hypermotility is independent of eosinophils and mediated by alterations in smooth muscle instead of enteric neurons

PLoS Pathog. 2024 Aug 14;20(8):e1011766. doi: 10.1371/journal.ppat.1011766. eCollection 2024 Aug.

Abstract

Intestinal helminth infection triggers a type 2 immune response that promotes a 'weep-and sweep' response characterised by increased mucus secretion and intestinal hypermotility, which function to dislodge the worm from its intestinal habitat. Recent studies have discovered that several other pathogens cause intestinal dysmotility through major alterations to the immune and enteric nervous systems (ENS), and their interactions, within the gastrointestinal tract. However, the involvement of these systems has not been investigated for helminth infections. Eosinophils represent a key cell type recruited by the type 2 immune response and alter intestinal motility under steady-state conditions. Our study aimed to investigate whether altered intestinal motility driven by the murine hookworm, Nippostrongylus brasiliensis, infection involves eosinophils and how the ENS and smooth muscles of the gut are impacted. Eosinophil deficiency did not influence helminth-induced intestinal hypermotility and hypermotility did not involve gross structural or functional changes to the ENS. Hypermotility was instead associated with a dramatic increase in smooth muscle thickness and contractility, an observation that extended to another rodent nematode, Heligmosomoides polygyrus. In summary our data indicate that, in contrast to other pathogens, helminth-induced intestinal hypermotility is driven by largely by myogenic, rather than neurogenic, alterations with such changes occurring independently of eosinophils. (<300 words).

MeSH terms

  • Animals
  • Enteric Nervous System* / immunology
  • Enteric Nervous System* / parasitology
  • Eosinophils* / immunology
  • Gastrointestinal Motility* / physiology
  • Helminthiasis / immunology
  • Helminthiasis / parasitology
  • Intestinal Diseases, Parasitic / immunology
  • Intestinal Diseases, Parasitic / parasitology
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Smooth* / parasitology
  • Nematospiroides dubius / immunology
  • Nematospiroides dubius / physiology
  • Neurons / metabolism
  • Neurons / parasitology
  • Nippostrongylus*
  • Strongylida Infections / immunology
  • Strongylida Infections / parasitology

Grants and funding

N.L.H received a salary from the National Health and Medical Research Council (NHMRC) of Australia, no. SRF-B 1140313. H. W. was financially supported by a Research Training Scholarship from Monash University. This work was additionally supported by a Discovery Project grant from the Australian Research Council (ARC), no DP210101500 awarded to N.L.H. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.