Review
Preference for dietary fat: From detection to disease

https://doi.org/10.1016/j.plipres.2020.101032Get rights and content

Highlights

In this review, we discuss the following points:

  • Is fat taste a “basic” or “alimentary” taste modality?

  • Do different dieting habits impact fat taste perception?

  • The interaction of microbiota and olfaction with fat taste.

  • Can the lipid sensors be the target of anti-obesity strategy?

Abstract

Recent advances in the field of taste physiology have clarified the role of different basic taste modalities and their implications in health and disease and proposed emphatically that there might be a distinct cue for oro-sensory detection of dietary long-chain fatty acids (LCFAs). Hence, fat taste can be categorized as a taste modality. During mastication, LCFAs activate tongue lipid sensors like CD36 and GPR120 triggering identical signaling pathways as the basic taste qualities do; however, the physico-chemical perception of fat is not as distinct as sweet or bitter or other taste sensations. The question arises whether “fat taste” is a basic or “alimentary” taste. There is compelling evidence that fat-rich dietary intervention modulates fat taste perception where an increase or a decrease in lipid contents in the diet results, respectively, in downregulation or upregulation of fat taste sensitivity. Evidently, a decrease in oro-sensory detection of LCFAs leads to high fat intake and, consequently, to obesity. In this article, we discuss recent relevant advances made in the field of fat taste physiology with regard to dietary fat preference and lipid sensors that can be the target of anti-obesity strategies.

Introduction

The sense of taste plays a key role in food choice, either to like or dislike at the first contact with it. There are five taste qualities, i.e., bitter, salt, sour, sweet and umami [1]. It has been considered that sweet taste allows the detection of energetic high calorie and pleasant (hedonic) substances, whereas bitter taste perception leads to avoid or reject toxic or noxious substances. The salty taste governs the intake of Na+ and it is essential for maintaining body's water balance and blood circulation [2]. Umami taste allows the recognition of amino acids, particularly of glutamate [3]. The sour taste is an important sensory input to inform on the ingestion of acidic food sources [4].

Taste perception is brought about by specialized cells that are grouped in taste buds which, in turn, are assembled in papillae, distributed principally throughout the tongue epithelium. There are three principal gustatory papillae on the tongue: circumvallate, fungiform and foliate which are localized, respectively, on posterior, dorsal and lateral regions. The taste buds form a cauliflower like structure whose apical part, containing microvilli, is bathed with salivary/buccal secretions and is in direct contact with sapid agents. The tuned gustatory message is sent to the brain, particular to the nucleus tractus solitaris (NTS), via afferent VII and/or IX cranial nerves. The NTS, central relay for gustatory and visceral information, further sends gustatory information to different regions of the brain which, in turn, modulates eating behavior of the organism. A detailed account of the morphology of taste system and its communication with NTS can be seen be consulted elsewhere [5].

Section snippets

Fat taste: Basic or alimentary?

The generalized definition of a basic taste modality should follow, at least, 4 criteria: 1) a taste receptor on the taste bud cells (TBCs), 2) its coupling to Ca2+ signaling, 3) transfer of the gustatory message from tongue to brain, and 4) activation of gut-brain-axis, responsible for anticipatory physiological mechanisms. According to these 4 criteria, fat taste might be considered as a basic taste as the mechanisms of fat taste transduction from tongue to brain (and to gut) follow the same

Tongue lipid sensors

In this article, we will employ the term lipid sensors for lipido-receptors like CD36 and GPR120 or other G-protein coupled receptors (GPCR) involved in fat taste perception. CD36, also known as FAT (fatty acid translocase) and discovered by the team of Nada Abumrad, has been largely studied for its implication in lipid metabolism [14]. CD36 is also known as scavenger receptor because it is expressed by a number of cells where it assures a number of diverse functions [15]. CD36 can be

Fat taste activates tongue-brain-gut axis

As far as the activation of different brain areas are concerned, most of the studies have been conducted by employing fMRI technique. Eldeghaidy et al. [47] observed that fat activated cortex insula, frontal operculum and secondary somatosensory cortex, anterior cingulate cortex, and amygdala in human volunteers. In another study again on humans, the same team reported that a high-fat food inhibited the activation of amygdala if the subjects had a previous experience with fatty food [48].

Oral microbiota

It is now well demonstrated that gut microbiota plays a key role in the pathogenies of obesity [57]. The transplantation of gut microbiota from obese individuals to lean subjects and vice versa can trigger or decrease obesity. Generally, obesity in animals (diet- or genetically-induced obesity in ob/ob mice) and humans, is marked with high number of Firmicutes and low number of Bacteroidetes bacteria in the gut [58]. As regards the changes in oral microbiota in obesity, Goodson et al. [59]

Dietary intervention impacts fat taste

Dietary fat modulates fat taste sensitivity: increasing fat intake causes decreasing fat taste sensitivity, viz., an increase in fat taste thresholds. Multiple cross-sectional studies have shown negative associations between fat intake and fat taste sensitivity [74,75], meaning individuals who consume high levels of dietary fat were found to have reduced taste sensitivity to fat. Intervention studies have conclusively demonstrated that modifications to long-term dietary fat intake mediate a

Fat taste sensitivity is decreased in obesity

There are more than 1.9 billion adults, 18 years and older, who are overweight on the globe. Of these, over 650 million are clinically obese [80]. Though there are several factors like genetic trait or socio-economic environment that are responsible for its incidence, high dietary fat intake that exceeds more than 40% daily ingested calories, in most of the advanced countries, remains a factor. Besides, the repeated exposure to palatable food increases hedonic pleasure, leading to obesity [81].

Tongue taste signaling: the target of anti-obesity strategy

Many humans have trouble limiting dietary fat. The management of obesity costs a lot for governmental or private organizations all over the world. The products like inulin, maltodextrin and plant fibres that mimic “fat-like’ texture are not very successful as they do not trigger “fat-like taste” [94]. Moreover, their prolonged use may cause a number of gastro-intestinal complications. Since physiological mechanisms of fat taste perception are evident and increased thresholds for LCFAs detection

Conclusions and perspectives

The second messenger cascade, coupled to lingual lipid sensors like CD36 and GPR120 has been well explored. However, there still remains some gaps. During receptor activation, the PLC-catalysed hydrolysis of PIP2 gives rise to IP3 and diacylgycerol (DAG); the former triggers an increase in free Ca2+, but the role of DAG in fat taste signal transduction is not known. Do taste bud cells also express other Ca2+channels that can be activated by endogenous DAG? DAG is known to open transient

Declaration of Competing Interest

All the authors declare that they do not have any conflict of interest.

Acknowledgements

This work was supported by a grant from Labex LIPSTIC (ANR-11-LABEX-002-01)/Region Bourgogne-Franche Comté, France.

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