Oro-sensory perception of dietary lipids: New insights into the fat taste transduction

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 3, 2009, Pages 149-155

  Khan, Naim Akhtar ^a   Besnard, Philippe ^b  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b Chu   (France)

Author keywords

CD36; Gustatory perception; Lipid; Taste

Indexed keywords

CALCIUM ION; CD36 ANTIGEN; DELAYED RECTIFIER POTASSIUM CHANNEL; FATTY ACID; FATTY ACID TRANSPORTER; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 120; GLYCOPROTEIN; LIPID; LONG CHAIN FATTY ACID; NEUROTRANSMITTER; NORADRENALIN; POLYUNSATURATED FATTY ACID; PROTEIN TYROSINE KINASE; SEROTONIN; UNCLASSIFIED DRUG;

BITTER TASTE; DIETARY INTAKE; ENZYME PHOSPHORYLATION; FAT INTAKE; FOOD INTAKE; FOOD PREFERENCE; FOOD QUALITY; GUSTATORY NERVOUS SYSTEM; HUMAN; MOUTH CAVITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SWEETNESS; TASTE; TONGUE;

ANIMALS; ANTIGENS, CD36; DIETARY FATS; HUMANS; LIPIDS; SENSORY RECEPTOR CELLS; TASTE; TASTE BUDS;

MUS; RODENTIA;

EID: 60549103018     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.01.001     Document Type: Review

References (77)

1. Mela D.J., and Rogers P.J. Food, eating and obesity?. The Psychological Basis of Appetite and Weight Control (1998), Chapman & Hall, London
2. Kaiyala K.J., Prigeon R.L., Kahn S.E., Woods S.C., and Schwartz M.W. Obesity induced by a high-fat diet is associated with reduced brain insulin transport in dogs. Diabetes 49 (2000) 1525-1533
3. Havel P.J., Townsend R., Chaump L., and Teff K. High-fat meals reduce 24-h circulating leptin concentrations in women. Diabetes 48 (1999) 334-341
4. Wild S.H., and Byrne C.D. ABC of obesity. Risk factors for diabetes and coronary heart disease. Br. Med. J. 333 (2006) 1009-1011
5. Colditz G.A., Willett W.C., Rotnitzky A., and Manson J.E. Weight gain as a risk factor for clinical diabetes mellitus in women. Ann. Intern. Med. 122 (1995) 481-486
6. Murphy N.F., MacIntyre K., Stewart S., Hart C.L., Hole D., and McMurray J.J. Long-term cardiovascular consequences of obesity: 20-year follow-up of more than 15 000 middle-aged men and women (Renfrew-Paisley study). Eur. Heart J. 27 (2006) 96-106
7. Peeters A., Barendregt J.J., Willekens F., Mackenbach J.P., Al Mamun A., and Bonneux L. Obesity in adulthood and its consequences for life expectancy: a life-table analysis. Ann. Intern. Med. 138 (2003) 24-32
8. Gaillard D., Passilly-Degrace P., and Besnard P. Molecular mechanisms of fat preference and overeating. Ann. N.Y. Acad. Sci. 1141 (2008) 163-175
9. Sclafani A. Psychobiology of food preferences. Int. J. Obes. Relat. Metab. Disord. 5 (2001) S13-S16
10. Smith J.C., Fisher E.M., Maleszewski V., and McClain B. Orosensory factors in the ingestion of corn oil/sucrose mixtures by the rat. Physiol. Behav. 69 (2000) 135-146
11. Warwick Z.S. Dietary fat dose dependently increases spontaneous caloric intake in rat. Obes. Res. 11 (2003) 859-864
12. Tsuruta M., Kawada T., Fukuwatari T., and Fushiki T. The orosensory recognition of long-chain fatty acids in rats. Physiol. Behav. 66 (1999) 285-288
13. Takeda M., Imaizumi M., and Fushiki T. Preference for vegetable oils in the two-bottle choice test in mice. Life Sci. 67 (2000) 197-204
14. Takeda M., Sawano S., Imaizumi M., and Fushiki T. Preference for corn oil in olfactory-blocked mice in the conditioned place preference test and the two-bottle choice test. Life Sci. 69 (2001) 847-854
15. Fukuwatari T., Shibata K., Iguchi K., Saeki T., Iwata A., Tani K., Sugimoto E., and Fushiki T. Role of gustation in the recognition of oleate and triolein in anosmic rats. Physiol. Behav. 78 (2003) 579-583
16. McCormack D.N., Clyburn V.L., and Pittman D.W. Detection of free fatty acids following a conditioned taste aversion in rats. Physiol. Behav. 87 (2006) 582-594
17. Kawai T., and Fushiki T. Importance of lipolysis in oral cavity for orosensory detection of fat. Am. J. Physiol. Regul., Integr. Comp. Physiol. 285 (2003) R447-454
18. Mela D.J., and Mattes R.D. The chemical senses and nutrition. Nutr. Today 23 (1988) 4-9
19. Oakley B. The gustatory competence of the lingual epithelium requires neonatal innervation. Brain Res. Dev. Brain Res. 72 (1993) 259-264
20. Gilbertson T.A., and Boughter Jr. J.D. Taste transduction: appetizing times in gestation. NeuroReport 14 (2003) 905-911
21. Sugita M. Taste perception and coding in the periphery. Cell. Mol. Life Sci. 63 (2006) 2000-2015
22. Gilbertson T.A., Fontenot D.T., Liu L., Zhang H., and Monroe W.T. Fatty acid modulation of K+ channels in taste receptor cells: gustatory cues for dietary fat. Am. J. Physiol. 272 (1997) C1203-C1210
23. Gilbertson T.A., Liu L., Kim I., Burks C.A., and Hansen D.R. Fatty acid responses in taste cells from obesity-prone and -resistant rats. Physiol. Behav. 86 (2005) 681-690
24. Liu L., Hansen D.R., Kim I., and Gilbertson T.A. Expression and characterization of delayed rectifying K+ channels in anterior rat taste buds. Am. J. Physiol., Cell Physiol. 289 (2005) C868-C880
25. Honore E., Barhanin J., Attali B., Lesage F., and Lazdunski M. External blockade of the major cardiac delayed-rectifier K+ channel (Kv1.5) by polyunsaturated fatty acids. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 1937-1941
26. Fredriksson R., Hoglund P.J., Gloriam D.E., Lagerstrom M.C., and Schioth H.B. Seven evolutionarily conserved human rhodopsin G protein-coupled receptors lacking close relatives. FEBS Lett. 554 (2003) 381-388
27. Rayasam G.V., Tulasi V.K., Davis J.A., and Bansal V.S. Fatty acid receptors as new therapeutic targets for diabetes. Expert Opin. Ther. Targets 11 (2007) 661-671
28. Hirasawa A., Tsumaya K., Awaji T., Katsuma S., Adachi T., Yamada M., Sugimoto Y., Miyazaki S., and Tsujimoto G. Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat. Med. 11 (2005) 90-94
29. Tanaka T., Katsuma S., Adachi T., Koshimizu T.A., Hirasawa A., and Tsujimoto G. Free fatty acids induce cholecystokinin secretion through GPR120. Naunyn-Schmiedebergs Arch. Pharmacol. 377 (2008) 523-527
30. Matsumura S., Mizushige T., Yoneda T., Iwanaga T., Tsuzuki S., Inoue K., and Fushiki T. GPR expression in the rat taste bud relating to fatty acid sensing. Biomed. Res. 28 (2007) 49-55
31. Dyer J., Salmon K.S., Zibrik L., and Shirazi-Beechey S.P. Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem. Soc. Trans. 33 (2005) 302-305
32. Wu S.V., Rozengurt N., Yang M., Young S.H., Sinnett-Smith J., and Rozengurt E. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2392-2397
33. Saitoh O., Hirano A., and Nishimura Y. Intestinal STC-1 cells respond to five basic taste stimuli. NeuroReport 18 (2007) 1991-1995
34. Abumrad N.A., el-Maghrabi M.R., Amri E.Z., Lopez E., and Grimaldi P.A. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268 (1993) 17665-17668
35. Fukuwatari T., Kawada T., Tsuruta M., Hiraoka T., Iwanaga T., Sugimoto E., and Fushiki T. Expression of the putative membrane fatty acid transporter (FAT) in taste buds of the circumvallate papillae in rats. FEBS Lett. 414 (1997) 461-464
36. Laugerette F., Passilly-Degrace P., Patris B., Niot I., Febbraio M., Montmayeur J.P., and Besnard P. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J. Clin. Invest. 115 (2005) 3177-3184
37. Rac M.E., Safranow K., and Poncyljusz W. Molecular basis of human CD36 gene mutations. Mol. Med. 13 (2007) 288-296
38. Baillie A.G., Coburn C.T., and Abumrad N.A. Reversible binding of long-chain fatty acids to purified FAT, the adipose CD36 homolog. J. Membr. Biol. 153 (1996) 75-81
39. Ibrahimi A., Sfeir Z., Magharaie H., Amri E.Z., Grimaldi P., and Abumrad N.A. Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 2646-2651
40. Huang M.M., Bolen J.B., Barnwell J.W., Shattil S.J., and Brugge J.S. Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 7844-7848
41. Sclafani A., Ackroff K., and Abumrad N.A. CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice. Am. J. Physiol., Regul. Integr. Comp. Physiol. 293 (2007) R1823-1832
42. Chandrashekar J., Hoon M.A., Ryba N.J., and Zuker C.S. The receptors and cells for mammalian taste. Nature 444 (2006) 288-294
43. Gaillard D., Laugerette F., Darcel N., El-Yassimi A., Passilly-Degrace P., Hichami A., Khan N.A., Montmayeur J.P., and Besnard P. The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 22 (2008) 1458-1468
44. El-Yassimi A., Hichami A., Besnard P., and Khan N.A. Linoleic acid induces calcium signaling, SRC-kinase phosphorylation and neurotransmitters release in mouse CD36-positive gustatory cells. J. Biol. Chem. 283 (2008) 12949-12959
45. Harmon C.M., Luce P., Beth A.H., and Abumrad N.A. Labeling of adipocyte membranes by sulfo-N-succinimidyl derivatives of long-chain fatty acids: inhibition of fatty acid transport. J. Membr. Biol. 121 (1991) 261-268
46. Bernhardt S.J., Naim M., Zehavi U., and Lindemann B. Changes in IP3 and cytosolic Ca2+ in response to sugars and non-sugar sweeteners in transduction of sweet taste in the rat. J. Physiol. 490 (1996) 325-336
47. Gousset K., Tsvetkova N.M., Crowe J.H., and Tablin F. Important role of raft aggregation in the signaling events of cold-induced platelet activation. Biochem. Biophys. Acta 1660 (2004) 7-15
48. Yang R., Crowley H.H., Rock M.E., and Kinnamon J.C. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J. Comp. Neurol. 424 (2000) 205-215
49. Pérez C.A., Robert F., Margolskee S., Kinnamon S.C., and Ogura T. Making sense with TRP channels: store-operated calcium entry and the ion channel Trpm5 in taste receptor cells. Cell Calcium 33 (2003) 541-549
50. Babnigg G., Bowersox S.R., and Villereal M.L. The role of pp60c-src in the regulation of calcium entry via store-operated calcium channels. J. Biol. Chem. 272 (1997) 29434-29437
51. Roper S.D. Cell communication in taste buds. Cell. Mol. Life Sci. 63 (2006) 1494-1500
52. Seta Y., Kataoka S., Toyono T., and Toyoshima K. Immunohistochemical localization of aromatic L-amino acid decarboxylase in mouse taste buds and developing taste papillae. Histochem. Cell Biol. 127 (2007) 415-422
53. Ortiz-Alvarado R., Guzman-Quevedo O., Mercado-Camargo R., Haertle T., Vignes C., and Bolanos-Jimenez F. Expression of tryptophan hydroxylase in developing mouse taste papillae. FEBS Lett. 580 (2006) 5371-5376
54. Huang Y.J., Maruyama Y., Lu K.S., Pereira E., Plonsky I., Baur J.E., Wu D., and Roper S.D. Using biosensors to detect the release of serotonin from taste buds during taste stimulation. Arch. Ital. Biol. 143 (2005) 87-96
55. Ren Y., Shimada K., Shirai Y., Fujimiya M., and Saito N. Immunocytochemical localization of serotonin and serotonin transporter (SET) in taste buds of rat. Brain Res. Mol. Brain Res. 74 (1999) 221-224
56. Gilbertson T.A. Gustatory mechanisms for the detection of fat. Curr. Opin. Neurobiol. 8 (1998) 447-452
57. Khan N.A., Gaillard D., El-Yassimi A., Passilly-Degrace P., Hichami A., and Besnard P. Unraveling the downstream signalling of gustatory perception of lipids. Med. Sci. (Paris) 24 (2008) 692-693
58. Liu D., and Liman E.R. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 15160-15165
59. Liman E.R. TRPM5 and taste transduction. Handb. Exp. Pharmacol. 179 (2007) 287-298
60. Sclafani A., Zukerman S., Glendinning J.I., and Margolskee R.F. Fat and carbohydrate preferences in mice: the contribution of alpha-gustducin and Trpm5 taste-signaling proteins. Am. J. Physiol., Regul. Integr. Comp. Physiol. 293 (2007) R1504-1513
61. Sugita M. Taste perception and coding in the periphery. Cell. Mol. Life Sci. 63 (2006) 2000-2015
62. Oike H., Wakamori M., Mori Y., Nakanishi H., Taguchi R., Misaka T., Matsumoto I., and Abe K. Arachidonic acid can function as a signaling modulator by activating the TRPM5 cation channel in taste receptor cells. Biochim. Biophys. Acta 1761 (2006) 1078-1084
63. Dotson C.D., Roper S.D., and Spector A.C. PLCbeta2-independent behavioral avoidance of prototypical bitter-tasting ligands. Chem. Senses 30 (2005) 593-600
64. Hisatsune C., Yasumatsu K., Takahashi-Iwanaga H., Ogawa N., Kuroda Y., Yoshida R., Ninomiya Y., and Mikoshiba K. Abnormal taste perception in mice lacking the type 3 inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 282 (2007) 37225-37231
65. Roper S.D. Signal transduction and information processing in mammalian taste buds. Pflugers Arch. 454 (2007) 759-776
66. Khan N.A., and Besnard P. Sensing of lipids via receptor signalling in taste buds. Eur. J. Lipid Sci. Technol. 110 (2008) 379-380
67. Drewnowski A., Brunzell J.D., Sande K., Iverius P.H., and Greenwood M.R. Sweet tooth reconsidered: taste responsiveness in human obesity. Physiol. Behav. 35 (1985) 617-622
68. Mela D.J., and Sacchetti D.A. Sensory preferences for fats: relationships with diet and body composition. Am. J. Clin. Nutr. 53 (1991) 908-915
69. Mela D.J. Determinants of food choice: relationships with obesity and weight control. Obes. Res. 9 (2001) 249S-255S
70. Wang G.J., Volkow N.D., Felder C., Fowler J.S., Levy A.V., Pappas N.R., Wong C.T., Zhu W., and Netusil N. Enhanced resting activity of the oral somatosensory cortex in obese subjects. NeuroReport 13 (2002) 1151-1155
71. Chale-Rush A., Burgess J.R., and Mattes R.D. Evidence for human orosensory (taste?) sensitivity to free fatty acids. Chem. Senses 32 (2007) 423-431
72. Schiffman S.S., Graham B.G., Sattely-Miller E.A., and Warwick Z.S. Orosensory perception of dietary fat. Curr. Dir. Psychol. Sci. 7 (1998) 137-143
73. Mattes R.D. Fat taste and lipid metabolism in humans. Physiol. Behav. 86 (2005) 691-697
74. Moreau H., Laugier R., Gargouri Y., Ferrato F., and Verger R. Human preduodenal lipase is entirely of gastric fundic origin. Gastroenterology 95 (1988) 1221-1226
75. Hamosh M. Lingual and gastric lipases. Nutrition 6 (1990) 421-428
76. Benton R., Vannice K.S., and Vosshall L.B. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450 (2007) 289-293
77. Greenwalt D.E., Lipsky R.H., Ockenhouse C.F., Ikeda H., Tandon N.N., and Jamieson G.A. Membrane glycoprotein CD36: a review of its roles in adherence, signal transduction, and transfusion medicine. Blood 80 (1992) 1105-1115