Physiological roles of dietary glutamate signaling via gut-brain axis due to efficient digestion and absorption

Journal of Gastroenterology

Volumn 48, Issue 4, 2013, Pages 442-451

  Torii, Kunio ^a,b   Uneyama, Hisayuki ^a   Nakamura, Eiji ^a  

^a AJINOMOTO CO INC   (Japan)

^b Torii Nutrient Stasis Institute Inc   (Japan)

Author keywords

Diet induced thermogenesis; Digestive juice secretion; Functional MRI; Gastric vagal afferent; Glutamate signaling; Gut brain axis

Indexed keywords

AMINO ACID; CARBOHYDRATE; ELECTROLYTE; GLUTAMATE SODIUM; GLUTAMIC ACID; MUCIN; NITRIC OXIDE; NITRITE;

AUTONOMIC NERVOUS SYSTEM FUNCTION; DIGESTION; ENTEROCHROMAFFIN CELL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GASTROINTESTINAL SECRETION; HUMAN; HYPOTHALAMUS; INTESTINE ABSORPTION; MEDIAL PREOPTIC AREA; MUCOSA CELL; NONHUMAN; PANCREAS JUICE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; VAGUS NERVE; VAGUS REFLEX; AUTONOMIC NERVE; BRAIN; DIET; GASTROINTESTINAL TRACT; HOMEOSTASIS; PHYSIOLOGY; STOMACH JUICE;

AUTONOMIC PATHWAYS; BRAIN; DIET; DIGESTION; GASTRIC JUICE; GASTROINTESTINAL TRACT; GLUTAMIC ACID; HOMEOSTASIS; HUMANS; INTESTINAL ABSORPTION; SIGNAL TRANSDUCTION; VAGUS NERVE;

EID: 84886577502     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-013-0778-1     Document Type: Review

References (60)

1. Giacometti T. Free and bound glutamate in natural products. In: Filer Jr LJ, Garattini MR, Kare MR, Reynolds WA, Wurtman RJ, editors. Glutamic acid: advances in biochemistry and physiology. New York: Raven Press; 1979. p. 25-34.
2. Young VR, Ajami AM. Glutamate: an amino acid of particular distribution. J Nutr. 2000;130(Suppl 4S):892S-900S.
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: 190-3.
4. Uematsu A, Tsurugizawa T, Uneyama H, Torii K. Brain-gut communication via vagus nerve modulates conditioned flavor preference. Eur J Neurosci. 2010;31: 1136-43.
5. Hector MP. Reflexes of salivary secretion. In: Garrett JR, Ekstro ̈m J, Anderson LC, editors. Neural mechanisms of salivary gland secretion. Basel: Karger; 1999. p. 196-217.
6. Hodson NA, Linden RWA. 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: 711-7.
7. Niijima A. Control of liver function and neuroendocrine regulation of blood glucose levels. In: Brooks CMcC, Koizumi K, Sato A, editors. Integrative functions of the autonomic nervous system. Tokyo/Elsevier: University of Tokyo Press and Amsterdam/ North-Holland Biomedical Press; 1979. p. 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: 161-4.
9. Niijima A. Effects of taste stimulation on the efferent activity of the autonomic nerves in the rat. Brain Res Bull. 1991;26: 165-7.
10. Niijima A. Effect of umami taste stimulations on vagal efferent activity in the rat. Brain Res Bull. 1991;27: 393-6.
11. Louis-Sylvestre J. Preabsorptive insulin release and hypoglycemia in rats. Am J Physiol. 1976;230: 56-60.
12. Steffens AB. Influence of the oral cavity on insulin release in the rat. Am J Physiol. 1976;230: 1411-5.
13. Strubbe JH, Steffens AB. Rapid insulin release after ingestion of a meal in the unanesthetized rat. Am J Physiol. 1975;229: 1019-22.
14. Jiang ZY, Niijima A. Effects of taste stimuli on the efferent activity of the gastric vagus nerve in rats. Neurosci Lett. 1986;69: 42-6.
15. Ikuno H, Sakaguchi T. Gastric vagal functional distribution in the secretion of gastric acid produced by sweet taste. Brain Res Bull. 1990;25: 429-31.
16. Niijima A. Effects of oral and intestinal stimulation with umami substance on gastric vagus activity. Physiol Behav. 1991;49: 1025-8.
17. Niijima A. Reflex effects of oral, gastrointestinal and hepatoportal glutamate sensors on vagal nerve activity. J Nutr. 2000; 130:971S-3S.
18. Niijima A, Togiyama T, Adachi A. Cephalic-phase insulin release induced by taste stimulus of monosodium glutamate (umami taste). Physiol Behav. 1990;48: 905-8.
19. Tonosaki K, Hori Y, Shimizu Y, Tonosaki K. Relationships between insulin release and taste. Biomed Res. 2007;28: 79-83.
20. deFonseka A, Kaunitz J. Gut sensing mechanisms. Curr Gastroenterol Rep. 2009;11: 442-7.
21. Kitamura A, Niijima A, Torii K, Uneyama H. Amino acidsensing by the abdominal vagus. In: Costa A, Villalba E (eds) Horizons in neuroscience research, vol. 1. New York: Nova Science Publishers, Inc.; 2010. p. 367-77.
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.
23. Rozengurt E, Sternini C. Taste receptor signaling in the mammalian gut. Curr Opin Pharmacol. 2007;7: 557-62.
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:G1163-70.
25. Fujita T, Kobayashi S, Yui R. Paraneuron concept and its current implications. Adv Biochem Psychopharmacol. 1980;25: 321-5.
26. Höfer D, Püschel B, Drenckhahn D. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc Natl Acad Sci USA. 1996;93: 6631-4.
27. Kitamura A, Sato W, Uneyama H, Torii K, Niijima A. Effects of the intragastric infusion of inosine monophosphate and L-glutamate on the vagal gastric afferent activity and subsequent autonomic reflexes. J Physiol Sci. 2011;61(1): 65-71.
28. Sharma KN, Nasset ES. Electrical activity in mesenteric nerves after perfusion of gut lumen. Am J Physiol. 1962;202: 725-30.
29. Jeanningros R, Mei N. Données préliminaires sur la réponse des chémorécepteurs intestinaux acides aminés. Reprod Nutr Dév. 1980;20: 1615-9.
30. 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.
31. 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): i178-9.
32. 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: 145-8.
33. Schwartz GJ, Moran TH. Duodenal nutrient exposure elicits nutrient-specific gut motility and vagal afferent signals in rat. Am J Physiol Regul Integr Comp Physiol. 1998;274:R1236-42.
34. Raybould HE. Sensing of glucose in the gastrointestinal tract. Auton Neurosci. 2007;133: 86-90.
35. Mei N. Intestinal chemosensitivity. Physiol Rev. 1985;65: 211-37.
36. Schwartz GJ. The role of gastrointestinal vagal afferents in the control of food intake: current prospects. Nutrition. 2000;16: 866-73.
37. Tsurugizawa T, Kondoh T, Torii K. Forebrain activation induced by postoral nutritive substances in rats. NeuroReport. 2008;19: 1111-5.
38. 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: 262-73.
39. 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: 1625-9.
40. Kondoh T, Torii K. MSG intake suppresses weight gain, fat deposition and plasma leptin levels in male Sprague-Dawley rats. Physiol Behav. 2008;95: 135-44.
41. Sclafani A. Fat and sugar flavor preference and acceptance in C57BL/6J and 129 mice: experience attenuates strain differences. Physiol Behav. 2007;90: 602-11.
42. Ackroff K, Sclafani A. Flavor preferences conditioned by intragastric infusion of ethanol in rats. Pharmacol Biochem Behav. 2001;68: 327-38.
43. Touzani K, Sclafani A. Lateral hypothalamic lesions impair flavour- nutrient and flavour-toxin trace learning in rats. Eur J Neurosci. 2002;16: 2425-33.
44. 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: 651-60.
45. 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: 667-74.
46. Rozengurt E. Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and alpha-gustducin in the mammalian gut. Am J Physiol Gastrointest Liver Physiol. 2006;291:G171-7.
47. 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: 302-5.
48. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, Yamada M, et al. Free fatty acids regulate gut incretin glucagon-like peptide- 1 secretion through GPR120. Nat Med. 2005;11: 90-4.
49. Itoh Y, Kawamata Y, Harada M, Kobayashi M, Fuji R, Fukusumi S, et al. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature. 2003;422: 173-6.
50. 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: 1008-10.
51. Viltart O, Sartor DM, Verberne AJ. Chemical stimulation of visceral afferents activates medullary neurones projecting to the central amygdale and periaqueductal grey. Brain Res Bull. 2006;71: 51-9.
52. 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: 157-66.
53. 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: 2492-500.
54. Mei N, Garnier L. Osmosensitive vagal receptors in the small intestine of the cat. J Auton Nerv Syst. 1986;16: 159-70.
55. 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:R34-43.
56. 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-5S.
57. Sclafani A, Lucas F. Abdominal vagotomy does not block carbohydrate- conditioned flavor preferences in rats. Physiol Behav. 1996;60: 447-53.
58. Otsubo H, Kondoh T, Shibata M, Torii K, Ueta Y. Induction of Fos expression in the rat forebrain after intragastric administration of monosodium L-glutamate, glucose and NaCl. Neuroscience. 2011;196: 97-103.
59. Murayama A, Uehara A, Yatsushiro S, Echigo N, Morimoto R, Morita M, et al. A novel variant of ionotropic glutamate receptor regulates somatostatin secretion from g-cell of islets of Langerhans. Diabetes. 2004;53: 1743-53.
60. Yamamoto S, Tomoe M, Toyama K, Kawai M, Uneyama H. Can dietary supplementation of monosodium glutamate improve the health of the elderly? Am J Clin Nutr. 2009;90(3): 97-103.