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. 2005 Nov;115(11):3177-84.
doi: 10.1172/JCI25299.

CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions

Fabienne Laugerette  1 , Patricia Passilly-Degrace, Bruno Patris, Isabelle Niot, Maria Febbraio, Jean-Pierre Montmayeur, Philippe Besnard
Affiliations

CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions

Fabienne Laugerette et al. J Clin Invest. 2005 Nov.

Abstract

Rats and mice exhibit a spontaneous attraction for lipids. Such a behavior raises the possibility that an orosensory system is responsible for the detection of dietary lipids. The fatty acid transporter CD36 appears to be a plausible candidate for this function since it has a high affinity for long-chain fatty acids (LCFAs) and is found in lingual papillae in the rat. To explore this hypothesis further, experiments were conducted in rats and in wild-type and CD36-null mice. In mice, RT-PCR experiments with primers specific for candidate lipid-binding proteins revealed that only CD36 expression was restricted to lingual papillae although absent from the palatal papillae. Immunostaining studies showed a distribution of CD36 along the apical side of circumvallate taste bud cells. CD36 gene inactivation fully abolished the preference for LCFA-enriched solutions and solid diet observed in wild-type mice. Furthermore, in rats and wild-type mice with an esophageal ligation, deposition of unsaturated LCFAs onto the tongue led to a rapid and sustained rise in flux and protein content of pancreatobiliary secretions. These findings demonstrate that CD36 is involved in oral LCFA detection and raise the possibility that an alteration in the lingual fat perception may be linked to feeding dysregulation.

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Figures

Figure 1
Figure 1
Expression pattern of various lipid-binding proteins and α-gustducin throughout the tongue and palatal epithelium in the mouse. Circumvallate, foliate, and fungiform papillae and respective surrounding nongustatory epithelium (negative control) were isolated under a microscope, and total RNA was prepared as described in Methods. (A) Quantification of CD36 and α-gustducin mRNA by the SYBR Green method. Each value corresponds to a pool of total RNA from 3–5 mice. Data represent mean + SEM; n = 5. *P < 0.05; #P < 0.001. The expression levels relative to fungiform papillae are indicated above the bars. (B) RT-PCR analysis of α-gustducin, CD36, FATP-4, L-FABP, I-FABP, and ACBP mRNA. Each experiments is representative of 3 independent experiments performed on a pool of total RNA from 3–5 mice. C, control; CV, circumvallate papillae; Fol., foliate papillae; Fun., fungiform papillae; +RT–RT, RT-PCR without reverse transcriptase; Surr. epith., surrounding nongustatory epithelium.
Figure 2
Figure 2
Immunolocalization of CD36 and α-gustducin in the mouse circumvallate papillae and palate. CD36 immunoreactivity was confined to the apical side of taste bud cells in the lingual epithelium (A and B), while α-gustducin was found throughout the taste buds in spindle-shaped cells (C and D). (E) Coexpression of CD36 and α-gustducin was found in some lingual taste receptor cells. Palatal taste buds were positive for α-gustducin (F) but negative for CD36 (G).
Figure 3
Figure 3
CD36 gene inactivation suppresses the spontaneous lipid preference in mice subjected to 48-hour 2-bottle preference test. Comparison of fluid intake in wild-type and FAT/CD36-null mice. Xanthan gum was used to emulsify linoleic acid (LA) in water and to mimic the lipid texture. The control solutions were water alone or with xanthan gum added. Data represent mean ± SEM; n = 12. #P < 0.001.
Figure 4
Figure 4
The short-term preference for lipid-enriched beverages and meals found in the wild-type mice is CD36 dependent. (A) Fluid intake in 1-hour-water-restricted wild-type and FAT/CD36-null mice subjected for 0.5 hours to a 2-bottle preference test. Xanthan gum (0.3%) was used to emulsify 2% linoleic acid in water and to mimic the lipid texture. The control solution was water with 0.3% xanthan gum added. (B) Food intake in 12-hour-fasted wild-type and FAT/CD36-null mice subjected to a choice between a 5% linoleic acid– or paraffin oil–enriched diet for 1 hour. *P < 0.05.
Figure 5
Figure 5
Effect of lingual fatty acid load on bile flux in rats. Anesthetized rats with bile diversion and esophageal ligation to prevent any lipid ingestion were subjected to an oral load of different purified fatty acids (0.2 ml). Controls received 0.2 ml water by the same route. Filled circles and open squares correspond to control solution and fatty acids tested, respectively. Data represent mean ± SEM; n = 9. *P < 0.05; **P < 0.01.
Figure 6
Figure 6
Lingual fatty acid deposition increases the protein content of pancreatic juice in rats. Anesthetized rats with pancreatic juice diversion and esophageal ligation to prevent any lipid ingestion were subjected to an oral load of different purified fatty acids (0.2 ml). Controls received 0.2 ml water by the same route. Black and white bars correspond to control solution and fatty acids, respectively. Data represent mean ± SEM; n = 9. *P < 0.05; **P < 0.01; #P < 0.001.
Figure 7
Figure 7
Impact of CD36 gene invalidation on the changes in pancreato-biliary flux (A) and protein levels (A) triggered by a lingual linoleic acid deposition. Anesthetized wild-type and CD36-null mice with pancreato-biliary diversion and esophageal ligation to prevent any lipid ingestion were subjected to an oral load with linoleic acid (0.2 ml). Controls received 0.2 ml water by the same route. Black and white bars correspond to pancreato-biliary flux before and after lingual linoleic acid deposition, respectively. The functional validity of preparations was assessed by a duodenal HCl infusion (gray bars). Data represent mean ± SEM; n = 9. *P < 0.05; **P < 0.01; #P < 0.001.
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