Preference for linoleic acid in obesity-prone and obesity-resistant rats is attenuated by the reduction of CD36 on the tongue

Abstract

Chen CS, Bench EM, Allerton TD, Schreiber AL, Arceneaux KP 3rd, Primeaux SD. Preference for linoleic acid in obesity-prone and obesityresistant rats is attenuated by the reduction of CD36 on the tongue. Am J Physiol Regul Integr Comp Physiol 305: R1346-R1355, 2013. First published October 23, 2013 doi:10.1152/ajpregu.00582.2012.-Differential sensing of dietary fat and fatty acids by the oral cavity is proposed to regulate the susceptibility to obesity. In the current experiments, animals that differ in their susceptibility to obesity were used to investigate the influence of the oral cavity on the preference for the polyunsaturated fatty acid, linoleic acid. In experiment 1, the preference for differing concentrations of linoleic acid was determined in obesity-prone Osborne-Mendel (OM) and obesity-resistant S5B/Pl (S5B) rats. The preference threshold for linoleic acid was lower in S5B rats, compared with OM rats. To determine whether differences in linoleic acid preference threshold were related to innate strain differences in the fatty acid receptors on the tongue, the expression of GPR120, GPR40, and CD36 on the circumvallate papillae were assessed in OM and S5B rats. Results indicated that the expression of CD36, GPR40, and GPR120 did not differ between these two strains. Numerous studies have examined the role of CD36 on fat intake; therefore, in experiment 3, RNA interference was used to decrease the expression of CD36 on the tongues of OM and S5B rats, and the effect of decreased CD36 expression on linoleic acid preference was determined. CD36 siRNA attenuated linoleic acid preference for the most preferred concentration in both OM and S5B rats. Overall, these data indicate that there are innate differences in the preference threshold for linoleic acid in obesity-prone and obesity-resistant rats. Experimentally reducing the expression of CD36 on the circumvallate papillae attenuated the preference for linoleic acid in both strains. preference threshold; obesity-prone; obesity-resistant; CD36; taste CONSUMPTION OF AN ENERGY-DENSE, high-fat diet has been associated with an increased risk for developing obesity (23). The detection of dietary fat and subsequent fat intake are mediated by input from the oral cavity and by postingestive effects (12). The ability to sense dietary fat in the oral cavity has two main functions: 1) mediation of the cephalic phase response and 2) regulation of food intake (12, 31). Differences in fat/fatty acid sensors in the oral cavity have been proposed as potential mechanisms contributing to the susceptibility of becoming obese. This is characterized by a subset of individuals who become obese on a high-fat diet (HFD) and another subset of individuals that are resistant to becoming obese when consuming a HFD (15,24,31,33). Understanding the detection and regulation of fat intake by fat/fatty acid sensors in the oral cavity may elucidate the mechanisms by which individuals develop preferences for high-fat foods, overconsume dietary fat, and subsequently become obese.Demonstration...

Taste of Fat: A Sixth Taste Modality?

“…This preference response was also reproduced when CD36-null mice were subjected to brief-access licking tests, suggesting that lingual CD36 can play a significant role in this phenomenon (122). The fact that a specific depletion of CD36 in CVP with CD36 siRNA attenuates the preference for LA in rats is consistent with this interpretation (29). Nevertheless, whether naive CD36 Ϫ/Ϫ mice failed to detect properly fat sources during two bottle preference tests, oil-experienced animals displayed near similar attraction for oil emulsion than wild-type controls (187).…”

Linoleic acid and the pathogenesis of obesity

“…Additionally, in this study FAT/CD36 knock-out obese mice consumed less of an LA solution than their wild type controls [68]. In humans this has been found to result from the rs1761667-AA allele which decreases FAT/CD36 expression, with those who are unable to orally sense LA having a higher fat intake and total EI than those who can [69].…”

“…In contrast to these results, when the same LA EI was combined into an isoenergetic high protein diet, there was insignificant weight gain, with the differences found to be dependent on cyclic adenosine monophosphate (cAMP) activation [67]. Oral sensing may also play a role in LA induced adipogenesis, with obese mice having been shown to have a preference for higher concentrations of oral LA, found to occur due to increased lingual expression of FAT/CD36 (fatty acid translocase cluster of differentiation 36), which has been shown to have a role in fat sensing and tolerance [68].…”

Recent advances in the modification of taste and food preferences following bariatric surgery

“…Taste receptors that are present on the tongue, do allow for the perception of taste and the importance of the oral cavity in the detection of highly palatable foods has led to a number of studies demonstrating the importance of sweet taste receptors and fatty acid receptors on the tongue. Lingual taste receptors modulate the preference for palatable foods and are regulated by the consumption of palatable foods [92][93][94][95][96][97][98][99][100][101][102][103][104][105][106]. Our laboratory has demonstrated that consumption of a high fat diet increases lingual and duodenal expression of the fatty acid receptor, CD36, in obesity-prone rats [102].…”

“…The detection of tastants by lingual taste receptors leads to the induction of signaling cascades which activate gustatory nerves to transmit sensory information to brain regions associated with the regulation of gustatory information, food intake and reward [107][108][109][110]. Obese animal models and human patients with T2D demonstrate alterations in fat and sucrose preferences and patients with T2D crave higher carbohydrate (sweet taste) foods, which is associated with poor glycemic control [81,94,103,111,112].…”