International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Detection, modulation, and transmission of sweet taste in regulation for energy homeostasis

  • Jyotaki, Masafumi (Section of Oral Neuroscience, Kyushu University, Graduate School of Dental Sciences) ;
  • Ninomiya, Yuzo (Section of Oral Neuroscience, Kyushu University, Graduate School of Dental Sciences)
  • Published : 2009.06.30
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Abstract

Perception of sweet compounds is important for animals to detect external carbohydrate source of calories and plays a crucial role in feeding behavior of animals. Recent progress in molecular genetic studies provides evidence for a candidate receptor (heterodimers with taste receptor type 1 member 2 and 3: T1R2/T1R3), and major downstream transduction molecules required for sweet taste signaling. Several studies demonstrated that the sweet taste signal can be modulated by a satiety hormone, leptin, through its receptors expressed in a subset of sweet-sensitive taste cells. Increase of internal energy storage in the adipose tissue leads to increase in the plasma leptin level which can reduce activities of sweet-sensitive cells. In human, thus, diurnal variation of plasma leptin level parallels variation of taste recognition thresholds for sweet compounds. This leptin modulation of sweet taste sensitivity may influence individuals' preference, ingestive behavior, and absorption of nutrients, thereby plays important roles in regulation of energy homeostasis.

Keywords

References

  1. Ahima RS, Prabakaran D, Mantzoros C, Qu D, Lowell B, MaratosFlier E, Flier JS. Role of leptin in the neuroendocrine response to fasting. Nature. 1996;382:250-2 https://doi.org/10.1038/382250a0
  2. Boden G, Chen X, Mozzoli M, Ryan I. Effect of fasting on serum leptin in normal human subjects. J Clin Endocrinol Metab. 1996;81:3419-23 https://doi.org/10.1210/jc.81.9.3419
  3. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ. T2Rs function as bitter taste receptors. Cell. 2000;100:703-11 https://doi.org/10.1016/S0092-8674(00)80706-0
  4. Finger TE, Danilova V, Barrows J, Bartel DL, Vigers AJ, Stone L, Hellekant G, Kinnamon SC. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science. 2005;310:1495-99 https://doi.org/10.1126/science.1118435
  5. Flier JS. Obesity wars: molecular progress confronts an expanding epidemic.Cell. 2004;116:337-50 https://doi.org/10.1016/S0092-8674(03)01081-X
  6. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM.Weightreducing effects of the plasma protein encoded by the obese gene. Science. 1995;269:543-6 https://doi.org/10.1126/science.7624777
  7. Heck GL, Mierson S, DeSimone JA. Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway. Science. 1984;223:403-5 https://doi.org/10.1126/science.6691151
  8. Hisatsune C, Yasumatsu K, Takahashi-Iwanaga H, Ogawa N, Kuroda Y, Yoshida R, Ninomiya Y, Mikoshiba K. Abnormal taste perception in mice lacking the type 3 inositol 1,4,5-trisphosphate receptor. J Biol Chem. 2007;282:37225-31 https://doi.org/10.1074/jbc.M705641200
  9. Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci. 2002;5:1169 -76 https://doi.org/10.1038/nn952
  10. Huang YJ, Maruyama Y, Dvoryanchikov G, Pereira E, Chaudhari N, Roper SD. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc Natl Acad Sci USA. 2007;104:6436-41 https://doi.org/10.1073/pnas.0611280104
  11. Ishimaru Y, Inada H, Kubota M, Zhuang H, Tominaga M, Matsunami H. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci USA. 2006;103:12569-74 https://doi.org/10.1073/pnas.0602702103
  12. Kawai K, Sugimoto K, Nakashima K, Miura H, Ninomiya Y: Leptin as a modulator of sweet taste sensitivities in mice. Proc Natl Acad Sci USA. 2000;97:11044-9 https://doi.org/10.1073/pnas.190066697
  13. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. Human receptors for sweet and umami taste. Proc Natl Acad Sci USA. 2002;99:4692-6 https://doi.org/10.1073/pnas.072090199
  14. Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, DeSimone JA.The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol. 2004; 558:147-59 https://doi.org/10.1113/jphysiol.2004.065656
  15. Margolskee RF. Molecular mechanisms of bitter and sweet taste transduction. J Biol Chem. 2002;277:1-4 https://doi.org/10.1074/jbc.R100054200
  16. Margolskee RF, Dyer J, Kokrashvili Z, Salmon KSH, Ilegems E, Daly K, Maillet EL, Ninomiya Y, Mosinger B, Shirazi-Beechey SP. T1R3 and gustducin in gut sense sugars to regulate expression of $Na^{+}$-glucose cotranspoter 1. Proc Natl Acad Sci USA. 2007;104:15075-81 https://doi.org/10.1073/pnas.0706678104
  17. Medler KF, Margolskee RF, Kinnamon SC. Electrophysiological characterization of voltage-gated currents in defined taste cell types of mice. J Neurosci. 2003;23:2608-17
  18. Nakamura Y, Sanematsu K, Ohta R, Shirosaki S, Koyano K, Nonaka K, Shigemura N, Ninomiya Y. Diurnal variation of human sweet taste recognition thresholds is correlated with plasma leptin level. Diabetes. 2008;57:2661-65 https://doi.org/10.2337/db07-1103
  19. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. Mammalian sweet taste receptors. Cell. 2001;106: 381-90 https://doi.org/10.1016/S0092-8674(01)00451-2
  20. Ninomiya Y, Shigemura N, Yasumatsu K, Ohta R, Sugimoto K, Nakashima K, Lindemann B. . Vitam Horm. 2002;64:221-48 https://doi.org/10.1016/S0083-6729(02)64007-5
  21. Romanov RA, Rogachevskaja OA, Bystrova MF, Jiang P, Margolskee RF, Kolesnikov SS. Afferent neurotransmission mediated by hemichannels in mammalian taste cells. EMBO J. 2007;26:657-67 https://doi.org/10.1038/sj.emboj.7601526
  22. Saladin R, Vos DP, Guerre-Millo M, Leturque A, Girard J, Staels B, Auwerx J. Transient increase in obese gene expression after food intake or insulin administration. Nature. 1995;377:527-9 https://doi.org/10.1038/377527a0
  23. Schoeller DA, Cella LK, Sinha MK, Caro JF. Entrainment of the diurnal rhythm of plasma leptin to meal timing. J Clin Invest. 1997;100:1882-87 https://doi.org/10.1172/JCI119717
  24. Shigemura N, Ohta R, Kusakabe Y, Miura H, Hino A, Koyano K, Ninomiya Y. Leptin modulates behavioral responses to sweet substances by influencing peripheral taste structures. Endocrinology. 2004;145:839-43 https://doi.org/10.1210/en.2003-0602
  25. Sinha MK, Sturis J, Ohannesian J, Magosin S, Thomas S, Heiman ML, Polonsky KS, Caro JF. Ultradian oscillations of leptin secretion in humans. Biochem Biophys Res Commun. 1996;228:733-8 https://doi.org/10.1006/bbrc.1996.1724
  26. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature. 2005;438:1022-25 https://doi.org/10.1038/nature04248
  27. Tomchik SM, Berg S, Kim JW, Chaudhari N, Roper SD. Breadth of tuning and taste coding in mammalian taste buds. J Neurosci. 2007;27:10840-48 https://doi.org/10.1523/JNEUROSCI.1863-07.2007
  28. Ugawa S, Minami Y, Gup W, Saishin Y, Takatsuji K, Yamamoto T, Tohyama M, Shimada S. Receptor that leaves a sour taste in the mouth. Nature. 1998;395:555-6 https://doi.org/10.1038/26882
  29. Wong GT, Gannon KS, Margolskee RF. Transduction of bitter and sweet taste by gustducin. Nature. 1996;381:796-800 https://doi.org/10.1038/381796a0
  30. Yoshida R, Shigemura N, Sanematsu K, Yasumatsu K, Ishizuka S, Ninomiya Y. Taste responsiveness of fungiform taste cells with action potentials. J Neurophysiol. 2006;96:3088-95 https://doi.org/10.1152/jn.00409.2006
  31. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM: Positional cloning of the mouse obese gene and its human homologue. Nature. 1994;372:425-32 https://doi.org/10.1038/372425a0