Research Article: Restraint stress induced gut dysmotility is diminished by a milk oligosaccharide (2′-fucosyllactose) in vitro

Date Published: April 24, 2019

Publisher: Public Library of Science

Author(s): Sohana Farhin, Annette Wong, Thilini Delungahawatta, Jessica Y. Amin, John Bienenstock, Rachael Buck, Wolfgang A. Kunze, Yvette Tache.

http://doi.org/10.1371/journal.pone.0215151

Abstract

Stress causes severe dysmotility in the mammalian gut. Almost all research done to date has concentrated on prevention of stress-induced altered gut motility but not on treatment. We had previously shown that intraluminal 2′FL could acutely moderate propulsive motility in isolated mouse colonic segments. Because 2′FL appeared to modulate enteric nervous system dependent motility, we wondered if the oligosaccharide could reverse the effects of prior restraint stress, ex vivo. We tested whether 2′FL could benefit the dysmotility of isolated jejunal and colonic segments from animals subjected to prior acute restraint stress.

Jejunal and colonic segments were obtained from male Swiss Webster mice that were untreated or subjected to 1 hour of acute restraint stress. Segments were perfused with Krebs buffer and propagating contractile clusters (PCC) digitally video recorded. 2′FL or β-lactose were added to the perfusate at a concentration of 1 mg/ml. Spatiotemporal maps were constructed from paired before and after treatment recordings, each consisting of 20 min duration and PCC analyzed for frequency, velocity and amplitude.

Stress decreased propulsive motility in murine small intestine while increasing it in the colon. 2′FL in jejunum of previously stressed mice produced a 50% increase in PCC velocity (p = 0.0001), a 43% increase in frequency (p = 0.0002) and an insignificant decrease in peak amplitude. For stressed colon, 2′FL reduced the frequency by 23% (p = 0.017) and peak amplitude by 26% (p = 0.011), and was without effect on velocity. β-lactose had negligible or small treatment effects.

We show that the prebiotic 2′FL may have potential as a treatment for acute stress-induced gut dysmotility, ex vivo, and that, as is the case for certain beneficial microbes, the mechanism occurs in the gut, likely via action on the enteric nervous system.

Partial Text

Environmental stress is associated with disordered peristalsis and diarrhea [1]. Indeed, intestinal motility appears to be particularly sensitive to stress [2, 3]. These observations apply also to our everyday life, animal husbandry and experimental studies of animal behavior. In the experimental literature, prevention of stress effects on the gut has received considerable attention [4–11], whereas treatment of these (i.e. after stress) has received very little. There are few treatments available clinically for stress-induced gut dysmotility, but the one most used is loperamide, a μ-opioid receptor agonist, which inhibits peristalsis but does not restore normal oral to anal propulsive motility characterized by propagating contractile clusters (PCC) [12, 13]. We have reported that a neuroactive bacterium, Lactobacillus rhamnosus JB-1, could partially reverse in vitro the effects of prior acute restraint stress on murine gut dysmotility [14]. However, there are few additional substances with similar treatment effects.

We verified that 1 hour acute restraint stress affected motility as we have previously reported [14, 22] (Table 1). Namely, stress decreased PCC velocity and frequency while increasing amplitude for jejunum, but increased PCC velocity and frequency with negligible effects on amplitude for colon.

The present report demonstrates for the first time that a single oligosaccharide, 2′FL, rather than a live microbe [14] can have stress-reversing effects on intestinal motility. We have shown clear treatment effects of 2′FL relative to a control carbohydrate, β-lactose, on restraint stress-induced gut dysmotility. 2′FL largely reversed the slowed PCC velocity and frequency in jejunum, and increased frequency and peak amplitude in colon.

 

Source:

http://doi.org/10.1371/journal.pone.0215151

 

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