Abstract
Monosodium L-glutamate (MSG) elicits a unique taste termed umami and is widely used as a flavor enhancer in various cuisines. In addition, recent studies suggest the existence of sensors for L-glutamate (Glu) and transduction molecules in the gut mucosa as well as in the oral cavity. The vagal gastric afferent responds specifically to the luminal stimulation of Glu in the stomach and regulates the autonomic reflexes. The intragastric infusion of Glu also activates several brain areas (insular cortex, limbic system, and hypothalamus) and is able to induce flavor-preference learning in rats. These results suggest that umami signaling via gustatory and visceral pathways plays an important role in the processes of digestion, absorption, metabolism, and other physiological functions via activation of the brain.
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References
1.
Giacometti T: Free and bound glutamate in natural products; in Filer LJ Jr, Garattini MR, Kare MR, Reynolds WA, Wurtman RJ (eds): Glutamic Acid: Advances in Biochemistry and Physiology. New York, Raven Press, 1979, pp 25–34.
2.
Young VR, Ajami AM: Glutamate: an amino acid of particular distinction. J Nutr 2000; 130:892S–900S.
[PubMed]
3.
Uematsu A, Tsurugizawa T, Kondoh T, Torii K: Conditioned flavor preference learning by intragastric administration of L-glutamate in rats. Neurosci Lett 2009;451:190–193.
[PubMed]
4.
Uematsu A, Tsurugizawa T, Uneyama H, Torii K: Brain-gut communication via vagus nerve modulates conditioned flavor preference. Eur J Neurosci 2010;31:1136–1143.
[PubMed]
5.
Hector MP: Reflexes of salivary secretion; in Garrett JR, Ekström J, Anderson LC (eds): Neural Mechanisms of Salivary Gland Secretion. Basel, Karger, 1999, pp 196–217.
6.
Hodson NA, Linden RA: The effect of monosodium glutamate on parotid salivary flow in comparison to the response to representatives of the other four basic tastes. Physiol Behav 2006;89:711–717.
[PubMed]
7.
Niijima A: Control of liver function and neuroendocrine regulation of blood glucose levels; in Brooks CMcC, Koizumi K, Sato A (eds): Integrative Functions of the Autonomic Nervous System. Tokyo, University of Tokyo Press/Amsterdam, Elsevier/North-Holland Biomedical Press, 1979, pp 68–83.
8.
Niijima A: Effects of taste stimulation on the efferent activity of the pancreatic vagus nerve in the rat. Brain Res Bull 1991;26:161–164.
[PubMed]
9.
Niijima A: Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat. Brain Res Bull 1991;26:165–167.
[PubMed]
10.
Niijima A: Effect of umami taste stimulations on vagal efferent activity in the rat. Brain Res Bull 1991;27:393–396.
[PubMed]
11.
Louis-Sylvestre J: Preabsorptive insulin release and hypoglycemia in rats. Am J Physiol 1976;230:56–60.
[PubMed]
12.
Steffens AB: Influence of the oral cavity on insulin release in the rat. Am J Physiol 1976;230:1411–1415.
[PubMed]
13.
Strubbe JH, Steffens AB: Rapid insulin release after ingestion of a meal in the unanesthetized rat. Am J Physiol 1975;229:1019–1022.
[PubMed]
14.
Jiang ZY, Niijima A: Effects of taste stimuli on the efferent activity of the gastric vagus nerve in rats. Neurosci Lett 1986;69:42–46.
[PubMed]
15.
Ikuno H, Sakaguchi T: Gastric vagal functional distribution in the secretion of gastric acid produced by sweet taste. Brain Res Bull 1990;25:429–431.
[PubMed]
16.
Niijima A: Effects of oral and intestinal stimulation with umami substance on gastric vagus activity. Physiol Behav 1991;49:1025–1028.
[PubMed]
17.
Niijima A: Reflex effects of oral, gastrointestinal and hepatoportal glutamate sensors on vagal nerve activity. J Nutr 2000;130:971S–973S.
[PubMed]
18.
Niijima A, Togiyama T, Adachi A: Cephalic-phase insulin release induced by taste stimulus of monosodium glutamate (umami taste). Physiol Behav 1990;48:905–908.
[PubMed]
19.
Tonosaki K, Hori Y, Shimizu Y, Tonosaki K: Relationships between insulin release and taste. Biomed Res 2007;28:79–83.
[PubMed]
20.
DeFonseka A, Kaunitz J: Gut sensing mechanisms. Curr Gastroenterol Rep 2009;11:442–447.
[PubMed]
21.
Kitamura A, Niijima A, Torii K, Uneyama H: Amino acid-sensing by the abdominal vagus; in Costa A, Villalba E (eds): Horizons in Neuroscience Research. New York, Nova Science, 2010, vol 1, pp 367–377.
22.
Raybould HE, Glatzle J, Freeman SL, Whited K, Dracel N, Liou A, Bohan D: Detection of macronutrients in the intestinal wall. Auton Neurosci 2006;125:28–33.
[PubMed]
23.
Rozengurt E, Sternini C: Taste receptor signaling in the mammalian gut. Curr Opin Pharmacol 2007;7:557–562.
[PubMed]
24.
Uneyama H, Niijima A, San Gabriel A, Torii K: Luminal amino acid sensing in the rat gastric mucosa. Am J Physiol Gastrointest Liver Physiol 2006;291:G1163–G1170.
[PubMed]
25.
Uneyama H, Niijima A, Kitamura A, Torii K: Existence of NO-triggered vagal afferent activation in the rat gastric mucosa. Life Sci 2009;85:782–787.
[PubMed]
26.
Fujita T, Kobayashi S, Yui R: Paraneuron concept and its current implications. Adv Biochem Psychopharmacol 1980;25:321–325.
[PubMed]
27.
Höfer D, Püschel B, Drenckhahn D: Taste receptor-like cells in the rat gut identified by expression of α-gustducin. Proc Natl Acad Sci USA 1996;93:6631–6634.
[PubMed]
28.
Kitamura A, Sato W, Uneyama H, Torii K, Niijima A: Effects of intragastric infusion of inosine monophosphate and L-glutamate on vagal gastric afferent activity and subsequent autonomic reflexes. J Physiol Sci 2011;61: 65–71.
[PubMed]
29.
Sharma KN, Nasset ES: Electrical activity in mesenteric nerves after perfusion of gut lumen. Am J Physiol 1962;202:725–730.
[PubMed]
30.
Jeanningros R, Mei N: Données préliminaires sur la réponse des chémorécepteurs intestinaux acides aminés. Reprod Nutr Dev 1980;20:1615–1619.
[PubMed]
31.
Jeanningros R: Vagal unitary responses to intestinal amino acid infusions in the anesthetized cat: a putative signal for protein induced satiety. Physiol Behav 1982;28:9–21.
[PubMed]
32.
Niijima A, Torii K, Uneyama H: Role played by vagal chemical sensors in the hepato-portal region and duodeno-intestinal canal: an electrophysiological study. Chem Senses 2005;30(suppl 1):i178–i179.
[PubMed]
33.
Eastwood C, Maubach K, Kirkup AJ, Grundy D: The role of endogenous cholecystokinin in the sensory transduction of luminal nutrient signals in the rat jejunum. Neurosci Lett 1998;254:145–148.
[PubMed]
34.
Schwartz GJ, Moran TH: Duodenal nutrient exposure elicits nutrient-specific gut motility and vagal afferent signals in rat. Am J Physiol 1998;274:R1236–R1242.
[PubMed]
35.
Raybould HE: Sensing of glucose in the gastrointestinal tract. Auton Neurosci 2007;133:86–90.
[PubMed]
36.
Mei N: Intestinal chemosensitivity. Physiol Rev 1985;65:211–237.
[PubMed]
37.
Schwartz GJ: The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition 2000;16:866–873.
[PubMed]
38.
Tsurugizawa T, Kondoh T, Torii K: Forebrain activation induced by postoral nutritive substances in rats. Neuroreport 2008;19:1111–1115.
[PubMed]
39.
Tsurugizawa T, Uematsu A, Nakamura E, Hasumura M, Hirota M, Kondoh T, Uneyama H, Torii K: Mechanisms of neural response to gastrointestinal nutritive stimuli: the gut-brain axis. Gastroenterology 2009;137:262–273.
[PubMed]
40.
Tsurugizawa T, Uematsu A, Uneyama H, Torii K: Blood oxygenation level-dependent response to intragastric load of corn oil emulsion in conscious rats. Neuroreport 2009;20:1625–1629.
[PubMed]
41.
Ackroff K, Sclafani A: Flavor preferences conditioned by intragastric infusions of dilute polycose solutions. Physiol Behav 1994;55:957–962.
[PubMed]
42.
Sclafani A: Fat and sugar flavor preference and acceptance in C57BL/6J and 129 mice: experience attenuates strain differences. Physiol Behav 2007;90:602–611.
[PubMed]
43.
Ackroff K, Sclafani A: Flavor preferences conditioned by intragastric infusion of ethanol in rats. Pharmacol Biochem Behav 2001;68:327–338.
[PubMed]
44.
Touzani K, Sclafani A: Lateral hypothalamic lesions impair flavour-nutrient and flavour-toxin trace learning in rats. Eur J Neurosci 2002;16:2425–2433.
[PubMed]
45.
Mark GP, Smith SE, Rada PV, Hoebel BG: An appetitively conditioned taste elicits a preferential increase in mesolimbic dopamine release. Pharmacol Biochem Behav 1994;48:651–660.
[PubMed]
46.
Shibata R, Kameishi M, Kondoh T, Torii K: Bilateral dopaminergic lesions in the ventral tegmental area of rats influence sucrose intake, but not umami and amino acid intake. Physiol Behav 2009;96:667–674.
[PubMed]
47.
Rozengurt E: Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and α-gustducin in the mammalian gut. Am J Physiol Gastrointest Liver Physiol 2006;291:G171–G177.
[PubMed]
48.
Dyer J, Salmon KS, Zibrik L, Shirazi-Beechey SP: Expression of sweet taste receptors of the T1R family in the intestinal tract and enteroendocrine cells. Biochem Soc Trans 2005;33:302–305.
[PubMed]
49.
Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, Sugimoto Y, Miyazaki S, Tsujimoto G: Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 2005;11:90–94.
[PubMed]
50.
Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fujii R, Fukusumi S, Ogi K, Hosoya M, Tanaka Y, Uejima H, Tanaka H, Maruyama M, Satoh R, Okubo S, Kizawa H, Komatsu H, Matsumura F, Noguchi Y, Shinohara T, Hinuma S, Fujisawa Y, Fujino M: Free fatty acids regulate insulin secretion from pancreatic β cells through GPR40. Nature 2003;422:173–176.
[PubMed]
51.
Beardshall K, Frost G, Morarji Y, Domin J, Bloom SR, Calam J: Saturation of fat and cholecystokinin release: implications for pancreatic carcinogenesis. Lancet 1989;2:1008–1010.
[PubMed]
52.
Viltart O, Sartor DM, Verberne AJ: Chemical stimulation of visceral afferents activates medullary neurones projecting to the central amygdala and periaqueductal grey. Brain Res Bull 2006;71:51–59.
[PubMed]
53.
Wang L, Martinez V, Barrachina MD, Tache Y: Fos expression in the brain induced by peripheral injection of CCK or leptin plus CCK in fasted lean mice. Brain Res 1998;791:157–166.
[PubMed]
54.
Baggio LL, Huang Q, Brown TJ, Drucker DJ: A recombinant human glucagon-like peptide (GLP)-1-albumin protein (albugon) mimics peptidergic activation of GLP-1 receptor-dependent pathways coupled with satiety, gastrointestinal motility, and glucose homeostasis. Diabetes 2004;53:2492–2500.
[PubMed]
55.
Mei N, Garnier L: Osmosensitive vagal receptors in the small intestine of the cat. J Auton Nerv Syst 1986;16:159–170.
[PubMed]
56.
Randich A, Tyler WJ, Cox JE, Meller ST, Kelm GR, Bharaj SS: Responses of celiac and cervical vagal afferents to infusions of lipids in the jejunum or ileum of the rat. Am J Physiol Regul Integr Comp Physiol 2000;278:R34–R43.
[PubMed]
57.
Niijima A, Meguid MM: An electrophysiological study on amino acid sensors in the hepato-portal system in the rat. Obes Res 1995;3(suppl 5):741S–745S.
[PubMed]
58.
Sclafani A, Lucas F: Abdominal vagotomy does not block carbohydrate-conditioned flavor preferences in rats. Physiol Behav 1996;60:447–453.
[PubMed]
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