Ingestion of bacterial lipopolysaccharide inhibits peripheral taste responses to sucrose in mice

Abstract

A fundamental role of the taste system is to discriminate between nutritive and toxic foods. However, it is unknown whether bacterial pathogens that might contaminate food and water modulate the transmission of taste input to the brain. We hypothesized that exogenous, bacterially-derived lipopolysaccharide (LPS), modulates neural responses to taste stimuli. Neurophysiological responses from the chorda tympani nerve, which innervates taste cells on the anterior tongue, were unchanged by acute exposure to LPS. Instead, neural responses to sucrose were selectively inhibited in mice that drank LPS during a single overnight period. Decreased sucrose sensitivity appeared 7 days after LPS ingestion, in parallel with decreased lingual expression of Tas1r2 and Tas1r3 transcripts, which are translated to T1R2+T1R3 subunits forming the sweet taste receptor. Tas1r2 and Tas1r3 mRNA expression levels and neural responses to sucrose were restored by 14 days after LPS consumption. Ingestion of LPS, rather than contact with taste receptor cells, appears to be necessary to suppress sucrose responses. Furthermore, mice lacking the Toll-like receptor (TLR) 4 for LPS were resistant to neurophysiological changes following LPS consumption. These findings demonstrate that ingestion of LPS during a single period specifically and transiently inhibits neural responses to sucrose. We suggest that LPS drinking initiates TLR4-dependent hormonal signals that downregulate sweet taste receptor genes in taste buds. Delayed inhibition of sweet taste signaling may influence food selection and the complex interplay between gastrointestinal bacteria and obesity.

Behavioral and neurophysiological taste responses to sweet and salt are diminished in a model of subclinical intestinal inflammation

“…inflammatory bowel disease) in susceptible patients or animal models 19 – 21 , and a high-fat diet 22 – 26 . We previously demonstrated reduced neurophysiological sweet responses in mice that ingested LPS 27 . Specifically, sucrose responses recorded from the chorda tympani nerve (CT), which transmits peripheral signals from taste buds on the anterior tongue to the brain, transiently decreased seven days after a single overnight period of LPS ingestion.…”

The effect of imiquimod on taste bud calcium transients and transmitter secretion

“…Activating TLRs up‐regulates the expression of cytokines, such as IFNs, which induces apoptosis and causes abnormal cell turnover in taste buds (Wang et al , ; Cohn et al , ; Feng et al , ). Notably, inflammation appears to play a role in many of the conditions and diseases associated with taste impairments (Zhu et al , ; Kumarhia et al , ). These studies suggest that immune responses may play a role for maintaining structural integrity of taste buds (Kim et al , ; Feng et al , ); however, little information has been generated regarding inflammation–taste interactions.…”

The gut microbiota to the brain axis in the metabolic control

“…The receptors TLR binding to LPS and some bacterial DNA and RNA fragments [94,95], the FFAR binding to SCFA [96] or TGR5 binding secondary biliary acids LCA and DCA [97] to cite a few are expressed by these tissues. Interestingly, inside the taste buds of the tongue, TLR and TGR5 are expressed also [98,99].…”

“…NOD2 as TLR4 are critical for the ENS sensitivity to the intestinal neuro-hormone as GLP-1 [14]. In the tongue level, LPS, through TLR4, decrease the neuronal response of taste buds to saccharose [99].…”