Leptin as a modulator of sweet taste sensitivities in mice

Kawai, Kirio; Sugimoto, Kumiko; Nakashima, Kenichiro; Miura, Hirohito; Ninomiya, Yuzo

doi:10.1073/pnas.190066697

Cited by 294 publications

(306 citation statements)

References 34 publications

(39 reference statements)

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“…Whole nerve responses to lingual application of tastants were recorded from the CT and the GL nerve as described (9,15,16). Responses to tastants were normalized to responses to NH 4 Cl.…”

Section: Methodsmentioning

confidence: 99%

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Endocannabinoids selectively enhance sweet taste

Yoshida

Ohkuri

Jyotaki

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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175

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Endocannabinoids such as anandamide [N-arachidonoylethanolamine (AEA)] and 2-arachidonoyl glycerol (2-AG) are known orexigenic mediators that act via CB 1 receptors in hypothalamus and limbic forebrain to induce appetite and stimulate food intake. Circulating endocannabinoid levels inversely correlate with plasma levels of leptin, an anorexigenic mediator that reduces food intake by acting on hypothalamic receptors. Recently, taste has been found to be a peripheral target of leptin. Leptin selectively suppresses sweet taste responses in wild-type mice but not in leptin receptor-deficient db/db mice. Here, we show that endocannabinoids oppose the action of leptin to act as enhancers of sweet taste. We found that administration of AEA or 2-AG increases gustatory nerve responses to sweeteners in a concentration-dependent manner without affecting responses to salty, sour, bitter, and umami compounds. The cannabinoids increase behavioral responses to sweet-bitter mixtures and electrophysiological responses of taste receptor cells to sweet compounds. Mice genetically lacking CB 1 receptors show no enhancement by endocannnabinoids of sweet taste responses at cellular, nerve, or behavioral levels. In addition, the effects of endocannabinoids on sweet taste responses of taste cells are diminished by AM251, a CB 1 receptor antagonist, but not by AM630, a CB 2 receptor antagonist. Immunohistochemistry shows that CB 1 receptors are expressed in type II taste cells that also express the T1r3 sweet taste receptor component. Taken together, these observations suggest that the taste organ is a peripheral target of endocannabinoids. Reciprocal regulation of peripheral sweet taste reception by endocannabinoids and leptin may contribute to their opposing actions on food intake and play an important role in regulating energy homeostasis.energy homeostasis | gustation | reciprocal regulation E ndocannabinoids such as anandamide [N-arachidonoylethanolamine (AEA)] and 2-arachidonoyl glycerol (2-AG) are known orexigenic mediators that act via CB 1 receptors in hypothalamus and limbic forebrain to induce appetite (1, 2) and stimulate food intake (3). Systemic administration of exogenous cannabinoids or endocannabinoids in rodents causes hyperphagia (4) and increases the preference for palatable substances such as sucrose solution or food pellets (5, 6). These effects are mediated by the CB 1 receptor: pretreatment with the CB 1 antagonist SR141716 inhibited hyperphagia and reduced consumption of both bland and palatable foods (4-6). The natural "liking" reactions of rats to sweet compounds were amplified by endogenous cannabinoid signals in nucleus accumbens (7). Thus, endocannabinoids may be related to hedonic aspects of sweet taste.There is growing evidence that taste function can be modulated by hormones or other factors that act on receptors present in the peripheral gustatory system. Leptin, an anorexigenic mediator that reduces food intake by acting on hypothalamic receptors (8), selectively suppresses sweet taste responses and th...

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“…Whole nerve responses to lingual application of tastants were recorded from the CT and the GL nerve as described (9,15,16). Responses to tastants were normalized to responses to NH 4 Cl.…”

Section: Methodsmentioning

confidence: 99%

“…RT-PCR and immunostaining were as described previously (9,10). Primer sequences for each PCR are listed in Table S2.…”

Section: Methodsmentioning

confidence: 99%

Endocannabinoids selectively enhance sweet taste

Yoshida

Ohkuri

Jyotaki

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

175

162

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“…Leptin modulates sweet taste sensation via actions on sweet taste receptor cells via the leptin receptor. Increased leptin decreases firing of sweet taste cells in mice (Kawai et al, 2000).…”

Section: A Role For Cephalic Phase Responses In Appetite and Satiety?mentioning

confidence: 98%

Anticipatory physiological regulation in feeding biology: Cephalic phase responses

2008

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Anticipatory physiological regulation is an adaptive strategy that enables animals to respond faster to physiologic and metabolic challenges. The cephalic phase responses are anticipatory responses that prepare animals to digest, absorb and metabolize nutrients. They enable the sensory aspects of the food to interact with the metabolic state of the animal to influence feeding behavior. The anticipatory digestive secretions and metabolic adjustments in response to food cues are key adaptations that affect digestive and metabolic efficiency and aid in controlling the resulting elevation of metabolic fuels in the blood. Cephalic phase responses enable digestion, metabolism and appetite to be regulated in a coordinated fashion. These responses have significant effects on meal size. For example, if the cephalic phase insulin response is blocked the result is poor glucose control and smaller meals. Cephalic phase responses also are linked to motivation to feed, and may play a more direct role in regulating meal size beyond the permissive one of ameliorating negative consequences of feeding. For example, the orexigenic peptide ghrelin appears to display a cephalic phase response, rising before expected meal times. This anticipatory ghrelin response increases appetite; interestingly it also enhances fat absorption, linking appetite with digestion and metabolism.

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“…Injection of leptin into lean mice resulted in suppressed response to sweet tastants in peripheral taste nerves without effect on other taste qualities. 80 Shigemura et al 81 demonstrated that the functional leptin receptor Ob-Rb messenger RNA is expressed in the fungiform and circumvallate taste buds in mice and that the presence or absence of Ob-Rb was associated with differences in leptin's effect on behavioral response to sweet substances. Leptin receptor-deficient obese mice showed increased gustatory neural response to sweet compounds.…”

Section: Leptinmentioning

confidence: 99%

Taste perception, associated hormonal modulation, and nutrient intake

et al. 2015

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It is well known that taste perception influences food intake. After ingestion, gustatory receptors relay sensory signals to the brain, which segregates, evaluates, and distinguishes the stimuli, leading to the experience known as "flavor." It is well accepted that five taste qualities -sweet, salty, bitter, sour, and umami -can be perceived by animals. In this review, the anatomy and physiology of human taste buds, the hormonal modulation of taste function, the importance of genetic chemosensory variation, and the influence of gustatory functioning on macronutrient selection and eating behavior are discussed. Individual genotypic variation results in specific phenotypes of food preference and nutrient intake. Understanding the role of taste in food selection and ingestive behavior is important for expanding our understanding of the factors involved in body weight maintenance and the risk of chronic diseases including obesity, atherosclerosis, cancer, diabetes, liver disease, and hypertension.

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Leptin as a modulator of sweet taste sensitivities in mice

Cited by 294 publications

References 34 publications

Endocannabinoids selectively enhance sweet taste

Endocannabinoids selectively enhance sweet taste

Anticipatory physiological regulation in feeding biology: Cephalic phase responses

Taste perception, associated hormonal modulation, and nutrient intake

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