Advertisement

Current Oral Health Reports

, Volume 4, Issue 2, pp 79–86 | Cite as

Taste Sensing Systems Influencing Metabolic Consequences

  • Noriatsu ShigemuraEmail author
Oral Disease and Nutrition (F Nishimura, Section Editor)
  • 73 Downloads
Part of the following topical collections:
  1. Topical Collection on Oral Disease and Nutrition

Abstract

Recent Findings

The taste information contributes to evaluate the quality and nutritional value of food before it is ingested, and thus, is essential for maintaining nutritive homeostasis within the body. Recent studies revealed that taste sensitivity is modulated by humoral factors such as hormones. Angiotensin II is a key hormone regulating sodium and water balance. Investigations of its involvement in the taste system revealed that angiotensin II suppresses the gustatory NaCl responses (amiloride-sensitive component) and enhances sweet taste sensitivity without affecting umami, sour, and bitter responses in mice.

Summary

These results suggest that taste modulation by angiotensin II may play important roles in maintaining electrolyte and glucose homeostasis.

Purpose of Review

This review focuses on the molecular mechanisms of salty taste perception and its modulation through the angiotensin II signaling to work out novel strategies to control food intake influencing metabolic consequences.

Keywords

Taste Taste modulation Angiotensin II ENaC T1r3 

Abbreviations

AngII

Angiotensin II

AT1 (AT2)

Angiotensin II receptor type 1 (type 2)

CB1

Cannabinoid receptor 1

CT

Chorda tympani

ENaC

Epithelial sodium channel

KCl

Potassium chloride

KO

Knockout

NaCl

Sodium chloride

Pkd2L1

Polycystic kidney disease 2-like 1

T1r3

Taste receptor family 1 member 3

Trpm5

Transient receptor potential cation channel subfamily M member 5

Trpv1

Transient receptor potential vanilloid 1

Notes

Acknowledgements

This research was supported in part by the Grants-in-Aid 24659828 and 15K11044 (N.S.) for Scientific Research from the Ministry of Education, Culture, Sports and Science, Japan.

Compliance with Ethical Standards

Conflict of Interest

The author declares that he has no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Lindemann B. Receptors and transduction in taste. Nature. 2001;413(6852):219–25.CrossRefPubMedGoogle Scholar
  2. 2.
    Chandrashekar J, et al. The receptors and cells for mammalian taste. Nature. 2006;444(7117):288–94.CrossRefPubMedGoogle Scholar
  3. 3.
    Shigemura N, Ninomiya Y. Recent advances in molecular mechanisms of taste signaling and modifying. Int Rev Cell Mol Biol. 2016;323:71–106.CrossRefPubMedGoogle Scholar
  4. 4.
    Richter CP. Increased salt appetite in adrenalectomized rats. Am J Phys. 1936;115:155–61.Google Scholar
  5. 5.
    Ten S, New M, Maclaren N. Clinical review 130: Addison’s disease 2001. J Clin Endocrinol Metab. 2001;86(7):2909–22.PubMedGoogle Scholar
  6. 6.
    Madias NE, Adrogue HJ. Hypo–hypernatraemia: disorders of water balance. In: Davidson AM, Cameron JS, Grünfeld J-P et al, editors. Oxford textbook of clinical nephrology, 3rd edn. Oxford University Press; 2005. p. 213–40.Google Scholar
  7. 7.
    He FJ, Burnier M, Macgregor GA. Nutrition in cardiovascular disease: salt in hypertension and heart failure. Eur Heart J. 2011;32(24):3073–80.CrossRefPubMedGoogle Scholar
  8. 8.
    Zhao D, et al. Dietary factors associated with hypertension. Nat Rev Cardiol. 2011;8(8):456–65.CrossRefPubMedGoogle Scholar
  9. 9.
    He J, et al. Premature deaths attributable to blood pressure in China: a prospective cohort study. Lancet. 2009;374(9703):1765–72.CrossRefPubMedGoogle Scholar
  10. 10.
    Murray RG. The ultrastructure of taste buds. In: Friedmann I, editor. The ultrastructure of sensory organs. Amsterdam: North Holland; 1973. p. 1–81.Google Scholar
  11. 11.
    Bartel DL, et al. Nucleoside triphosphate diphosphohydrolase-2 is the ecto-ATPase of type I cells in taste buds. J Comp Neurol. 2006;497(1):1–12.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Lawton DM, et al. Localization of the glutamate-aspartate transporter, GLAST, in rat taste buds. Eur J Neurosci. 2000;12(9):3163–71.CrossRefPubMedGoogle Scholar
  13. 13.
    Kitagawa M, et al. Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun. 2001;283(1):236–42.CrossRefPubMedGoogle Scholar
  14. 14.
    Montmayeur JP, et al. A candidate taste receptor gene near a sweet taste locus. Nat Neurosci. 2001;4(5):492–8.PubMedGoogle Scholar
  15. 15.
    Max M, et al. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet. 2001;28(1):58–63.PubMedGoogle Scholar
  16. 16.
    Sainz E, et al. Identification of a novel member of the T1R family of putative taste receptors. J Neurochem. 2001;77(3):896–903.CrossRefPubMedGoogle Scholar
  17. 17.
    Nelson G, et al. Mammalian sweet taste receptors. Cell. 2001;106(3):381–90.CrossRefPubMedGoogle Scholar
  18. 18.
    Bachmanov AA, et al. Positional cloning of the mouse saccharin preference (sac) locus. Chem Senses. 2001;26(7):925–33.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Chandrashekar J, et al. T2Rs function as bitter taste receptors. Cell. 2000;100(6):703–11.CrossRefPubMedGoogle Scholar
  20. 20.
    McLaughlin SK, McKinnon PJ, Margolskee RF. Gustducin is a taste-cell-specific G protein closely related to the transducins. Nature. 1992;357(6379):563–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Miyoshi MA, Abe K, Emori Y. IP(3) receptor type 3 and PLCbeta2 are co-expressed with taste receptors T1R and T2R in rat taste bud cells. Chem Senses. 2001;26(3):259–65.CrossRefPubMedGoogle Scholar
  22. 22.
    Clapp TR, et al. Immunocytochemical evidence for co-expression of Type III IP3 receptor with signaling components of bitter taste transduction. BMC Neurosci. 2001;2:6.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Pérez CA, et al. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci. 2002;5(11):1169–76.CrossRefPubMedGoogle Scholar
  24. 24.
    Talavera K, et al. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature. 2005;438(7070):1022–5.CrossRefPubMedGoogle Scholar
  25. 25.
    Taruno A, et al. CALHM1 ion channel mediates purinergic neurotransmission of sweet, bitter and umami tastes. Nature. 2013;495(7440):223–6.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Yang R, et al. Taste cells with synapses in rat circumvallate papillae display SNAP-25-like immunoreactivity. J Comp Neurol. 2000;424(2):205–15.CrossRefPubMedGoogle Scholar
  27. 27.
    Clapp TR, et al. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006;4:7.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Iwanaga T. Immunohistochemical localization of protein gene product 9.5 (PGP 9.5) in sensory paraneurons of the rat. Biomed Res. 1992;13(3):225–30.CrossRefGoogle Scholar
  29. 29.
    Tamamaki N, et al. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol. 2003;467(1):60–79.CrossRefPubMedGoogle Scholar
  30. 30.
    Nelson GM, Finger TE. Immunolocalization of different forms of neural cell adhesion molecule (NCAM) in rat taste buds. J Comp Neurol. 1993;336(4):507–16.CrossRefPubMedGoogle Scholar
  31. 31.
    Huang YJ, et al. Mouse taste buds use serotonin as a neurotransmitter. J Neurosci. 2005;25(4):843–7.CrossRefPubMedGoogle Scholar
  32. 32.
    Lopez-Jimenez ND, et al. Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem. 2006;98(1):68–77.CrossRefGoogle Scholar
  33. 33.
    Ishimaru Y, et al. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci U S A. 2006;103(33):12569–74.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Horio N, et al. Sour taste responses in mice lacking PKD channels. PLoS One. 2011;6(5):e20007.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Finger TE, Simon SA. Cell biology of taste epithelium. In: Finger TE, Silver WL, Restrepo D, editors. The neurobiology of taste and smell. New York: Wiley-Liss; 2000. p. 287–314.Google Scholar
  36. 36.
    Miura H, et al. Shh and Ptc are associated with taste bud maintenance in the adult mouse. Mech Dev. 2001;106(1–2):143–5.CrossRefPubMedGoogle Scholar
  37. 37.
    Hall JM, Bell ML, Finger TE. Disruption of sonic hedgehog signaling alters growth and patterning of lingual taste papillae. Dev Biol. 2003;255(2):263–77.CrossRefPubMedGoogle Scholar
  38. 38.
    Seta Y, et al. The bHLH transcription factors, Hes6 and Mash1, are expressed in distinct subsets of cells within adult mouse taste buds. Arch Histol Cytol. 2006;69(3):189–98.CrossRefPubMedGoogle Scholar
  39. 39.
    Nakayama A, et al. Expression of the basal cell markers of taste buds in the anterior tongue and soft palate of the mouse embryo. J Comp Neurol. 2008;509(2):211–24.CrossRefPubMedGoogle Scholar
  40. 40.
    Ren W, et al. Single Lgr5- or Lgr6-expressing taste stem/progenitor cells generate taste bud cells ex vivo. Proc Natl Acad Sci U S A. 2014;111(46):16401–6.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Schiffman SS, Lockhead E, Maes FW. Amiloride reduces the taste intensity of Na+ and Li+ salts and sweeteners. Proc Natl Acad Sci U S A. 1983;80(19):6136–40.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Heck GL, Mierson S, DeSimone JA. Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway. Science. 1984;223(4634):403–5.CrossRefPubMedGoogle Scholar
  43. 43.
    Jakinovich Jr W. Stimulation of gerbil’s gustatory receptors by methyl glycopyranosides. Chem Senses. 1985;10(4):591–604.CrossRefGoogle Scholar
  44. 44.
    Simon SA, Robb R, Garvin JL. Epithelial responses of rabbit tongues and their involvement in taste transduction. Am J Phys. 1986;251(3):R598–608.Google Scholar
  45. 45.
    Herness MS. Effect of amiloride on bulk flow and iontophoretic taste stimuli in the hamster. J Comp Physiol A. 1987;160(2):281–8.CrossRefPubMedGoogle Scholar
  46. 46.
    Ninomiya Y, Sako N, Funakoshi M. Strain differences in amiloride inhibition of NaCl responses in mice, Mus musculus. J Comp Physiol A. 1989;166(1):1–5.CrossRefPubMedGoogle Scholar
  47. 47.
    Hellekant G, Ninomiya Y. On the taste of umami in chimpanzee. Physiol Behav. 1991;49(5):927–34.CrossRefPubMedGoogle Scholar
  48. 48.
    Yoshida R, et al. NaCl responsive taste cells in the mouse fungiform taste buds. Neuroscience. 2009;159(2):795–803.CrossRefPubMedGoogle Scholar
  49. 49.
    Ninomiya Y, Funakoshi M. Amiloride inhibition of responses of rat single chorda tympani fibers to chemical and electrical tongue stimulations. Brain Res. 1988;451(1–2):319–25.CrossRefPubMedGoogle Scholar
  50. 50.
    Ninomiya Y. Reinnervation of cross-regenerated gustatory nerve fibers into amiloride-sensitive and amiloride-insensitive taste receptor cells. Proc Natl Acad Sci U S A. 1998;95(9):5347–50.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Formaker BK, Hill DL. Lack of amiloride sensitivity in SHR and WKY glossopharyngeal taste responses to NaCl. Physiol Behav. 1991;50:765–9.CrossRefPubMedGoogle Scholar
  52. 52.
    Yasumatsu K, et al. Recovery of amiloride-sensitive neural coding during regeneration of the gustatory nerve: behavioral-neural correlation of salt taste discrimination. J Neurosci. 2003;23(10):4362–8.PubMedGoogle Scholar
  53. 53.
    Lingueglia E, et al. Expression cloning of an epithelial amiloride-sensitive Na+ channel. A new channel type with homologies to Caenorhabditis elegans degenerins. FEBS Lett. 1993;318:95–9.CrossRefPubMedGoogle Scholar
  54. 54.
    Kretz O, et al. Differential expression of RNA and protein of the three pore-forming subunits of the amiloride-sensitive epithelial sodium channel in taste buds of the rat. J Histochem Cytochem. 1999;47(1):51–64.CrossRefPubMedGoogle Scholar
  55. 55.
    Lin W, et al. Epithelial Na+ channel subunits in rat taste cells: localization and regulation by aldosterone. J Comp Neurol. 1999;405(3):406–20.CrossRefPubMedGoogle Scholar
  56. 56.
    Shigemura N, et al. Expression of amiloride-sensitive epithelial sodium channels in mouse taste cells after chorda tympani nerve crush. Chem Senses. 2005;30(6):531–8.CrossRefPubMedGoogle Scholar
  57. 57.
    Chandrashekar J, et al. The cells and peripheral representation of sodium taste in mice. Nature. 2010;464(7286):297–301.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Shigemura N, et al. Amiloride-sensitive NaCl taste responses are associated with genetic variation of ENaC alpha-subunit in mice. Am J Physiol Regul Integr Comp Physiol. 2008;294(1):R66–75.CrossRefPubMedGoogle Scholar
  59. 59.
    Ambrosius WT, et al. Genetic variants in the epithelial sodium channel in relation to aldosterone and potassium excretion and risk for hypertension. Hypertension. 1999;34:631–7.CrossRefPubMedGoogle Scholar
  60. 60.
    Noh H, et al. Salty taste acuity is affected by the joint action of αENaC A663T gene polymorphism and available zinc intake in young women. Nutrients. 2013;5(12):4950–63.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Huque T, et al. Sour ageusia in two individuals implicates ion channels of the ASIC and PKD families in human sour taste perception at the anterior tongue. PLoS One. 2009;4(10):e7347.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lyall V, et al. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol. 2004;558(1):147–59.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Oka Y, et al. High salt recruits aversive taste pathways. Nature. 2013;494(7438):472–5.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Buggy J, Fisher AN. Evidence for a dual central role for angiotensin in water and sodium intake. Nature. 1974;250(5469):733–5.CrossRefPubMedGoogle Scholar
  65. 65.
    Avrith DB, Fitzsimons JT. Increased sodium appetite in the rat induced by intracranial administration of components of the renin-angiotensin system. J Physiol. 1980;301:349–64.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Avrith DB, Wiselka MJ, Fitzsimons JT. Increased sodium appetite in adrenalectomized or hypophysectomized rats after intracranial injection of renin or angiotensin II. J Endocrinol. 1980;87:109–12.CrossRefPubMedGoogle Scholar
  67. 67.
    Fitts DA, et al. Intravenous angiotensin and salt appetite in rats. Appetite. 2007;48(1):69–77.CrossRefPubMedGoogle Scholar
  68. 68.
    Dalhouse AD, et al. Angiotensin and salt appetite: physiological amounts of angiotensin given peripherally increase salt appetite in the rat. Behav Neurosci. 1986;100(4):597–602.CrossRefPubMedGoogle Scholar
  69. 69.
    Schoorlemmer GH, Johnson AK, Thunhorst RL. Circulating angiotensin II mediates sodium appetite in adrenalectomized rats. Am J Phys. 2001;281(3):R723–9.Google Scholar
  70. 70.
    Thunhorst RL, Fitts DA. Peripheral angiotensin causes salt appetite in rats. Am J Phys. 1994;267(1):R171–7.Google Scholar
  71. 71.
    de Gasparo M, et al. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev. 2000;52(3):415–72.PubMedGoogle Scholar
  72. 72.
    •• Shigemura N, et al. Angiotensin II modulates salty and sweet taste sensitivities. J Neurosci. 2013;33(15):6267–77. This manuscript represents the first description of salty and sweet taste modulation by angiotensin II signaling in the peripheral taste organs CrossRefPubMedGoogle Scholar
  73. 73.
    Kinugawa K, et al. Effects of a nonpeptide angiotensin II receptor antagonist (CV-11974) on [Ca2+]i and cell motion in cultured ventricular myocytes. Eur J Pharmacol. 1993;235(2–3):313–6.CrossRefPubMedGoogle Scholar
  74. 74.
    Murata Y, et al. Gurmarin suppression of licking responses to sweetener-quinine mixtures in C57BL mice. Chem Senses. 2003;28(3):237–43.CrossRefPubMedGoogle Scholar
  75. 75.
    Shigemura N, et al. Leptin modulates behavioral responses to sweet substances by influencing peripheral taste structures. Endocrinology. 2004;145(2):839–47.CrossRefPubMedGoogle Scholar
  76. 76.
    Lingueglia E, et al. Different homologous subunits of the amiloride-sensitive Na+ channel are differently regulated by aldosterone. J Biol Chem. 1994;269(19):13736–9.PubMedGoogle Scholar
  77. 77.
    Loffing J, et al. Aldosterone induces rapid apical translocation of ENaC in early portion of renal collecting system: possible role of SGK. Am J Physiol Renal Physiol. 2001;280(4):F675–82.PubMedGoogle Scholar
  78. 78.
    Jamshidi N, Taylor DA. Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br J Pharmacol. 2001;134(6):1151–4.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Cota D, et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest. 2003;112(3):423–31.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    • Yoshida R, et al. Endocannabinoids selectively enhance sweet taste. Proc Natl Acad Sci U S A. 2010;107(2):935–9. This manuscript represents the first description of sweet taste enhancing effect by endocannabinoid signaling in the peripheral taste organs CrossRefPubMedGoogle Scholar
  81. 81.
    Rozenfeld R, et al. AT1R-CB1R heteromerization reveals a new mechanism for the pathogenic properties of angiotensin II. EMBO J. 2011;30(12):2350–63.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Turu G, et al. Paracrine transactivation of the CB1 cannabinoid receptor by AT1 angiotensin and other Gq/11 protein-coupled receptors. J Biol Chem. 2009;284(25):16914–21.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Ledent C, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science. 1999;283(5400):401–4.CrossRefPubMedGoogle Scholar
  84. 84.
    Araki K, et al. Telmisartan prevents obesity and increases the expression of uncoupling protein 1 in diet-induced obese mice. Hypertension. 2006;48(1):51–7.CrossRefPubMedGoogle Scholar
  85. 85.
    McMurray JJ, et al. Effect of valsartan on the incidence of diabetes and cardiovascular events. N Engl J Med. 2010;362(16):1477–90.CrossRefPubMedGoogle Scholar
  86. 86.
    Fallis N, Lasagna L, Tetreault L. Gustatory thresholds in patients with hypertension. Nature. 1962;196:74–5.CrossRefGoogle Scholar
  87. 87.
    Mattes RD. The taste for salt in humans. Am J Clin Nutr. 1997;65(2):692S–7S.PubMedGoogle Scholar
  88. 88.
    Boyd I. Captopril-induced taste disturbance. Lancet. 1993;342(8866):304–5.CrossRefPubMedGoogle Scholar
  89. 89.
    McNeil JJ, et al. Taste loss associated with captopril treatment. Br Med J. 1979;2(6204):1555–6.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Gradman AH, et al. A randomized, placebo-controlled, double-blind, parallel study of various doses of losartan potassium compared with enalapril maleate in patients with essential hypertension. Hypertension. 1995;25(6):1345–50.CrossRefPubMedGoogle Scholar
  91. 91.
    Schlienger RG, Saxer M, Haefeli WE. Reversible ageusia associated with losartan. Lancet. 1996;347(8999):471–2.CrossRefPubMedGoogle Scholar
  92. 92.
    Tsuruoka S, et al. Angiotensin II receptor blocker-induces blunted taste sensitivity: comparison of candesartan and valsartan. Br J Clin Pharmacol. 2005;60(2):204–7.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Section of Oral Neuroscience, Graduate School of Dental ScienceKyushu UniversityFukuokaJapan
  2. 2.Division of Sensory Physiology, Research and Development Center for Taste and Odor SensingKyushu UniversityFukuokaJapan

Personalised recommendations