Ingestion of bacterial lipopolysaccharide inhibits peripheral taste responses to sucrose in mice.
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 7days 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.
Institute of Molecular Medicine and Genetics, Georgia Regents University, Augusta, GA, United States; Department of Orthopedic Surgery, Zhongnan Hospital of Wuhan University, Wuhan 430071, China.
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Institute of Molecular Medicine and Genetics, Georgia Regents University, Augusta, GA, United States.
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Institute of Molecular Medicine and Genetics, Georgia Regents University, Augusta, GA, United States. Electronic address: lmccluskey@gru.edu.
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D000818:Animals; D002814:Chorda Tympani Nerve / Q000187:drug effects / Q000502:physiology; D004326:Drinking; D004848:Epithelium / Q000187:drug effects / Q000502:physiology; D005260:Female; D008070:Lipopolysaccharides / Q000494:pharmacology*; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects; D051379:Mice; D008810:Mice, Inbred C57BL; D009474:Neurons / Q000187:drug effects / Q000502:physiology; D018373:Peripheral Nervous System Agents / Q000494:pharmacology*; D012333:RNA, Messenger / Q000378:metabolism; D043562:Receptors, G-Protein-Coupled / Q000378:metabolism; D013045:Species Specificity; D013395:Sucrose / Q000378:metabolism*; D013649:Taste / Q000187:drug effects* / Q000502:physiology*; D013997:Time Factors; D051197:Toll-Like Receptor 4 / Q000378:metabolism; D014059:Tongue / Q000187:drug effects / Q000502:physiology
D008070:Lipopolysaccharides; D018373:Peripheral Nervous System Agents; D012333:RNA, Messenger; D043562:Receptors, G-Protein-Coupled; C493487:Tlr4 protein, mouse; D051197:Toll-Like Receptor 4; C431926:taste receptors, type 1; D013395:Sucrose
ANOVAs; CT; GLP; LPS; MPG; QHCl; SCCs; SPF; TLR; TRP; Tas1r1; Tas1r2; Tas1r3; Toll-like receptor; aceK; analyses of variance; chorda tympani; chorda tympani nerve; glucagon-like peptide; l-glutamic acid monopotassium salt; lipopolysaccharide; neuro-immune interactions; potassium acesulfame; qRT-PCR; quantitative reverse transcriptase-polymerase chain reaction; quinine hydrochloride dehydrate; solitary chemosensory cells; specified pathogen-free; taste receptor cell; transient receptor potential