The sweet taste signalling pathways in the oral cavity and the gastrointestinal tract affect human appetite and food intake: a review

International Journal of Food Sciences and Nutrition

Volumn 70, Issue 2, 2019, Pages 125-135

  Han, Pengfei ^a   Bagenna, Bagenna ^b   Fu, Minghai ^b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b INNER MONGOLIA UNIVERSITY FOR NATIONALITIES   (China)

Author keywords

brain activation; caloric sugars; food intake; hormone; non nutritive sweeteners; Sweet taste receptor

Indexed keywords

HORMONE; SWEETENING AGENT;

APPETITE; CALORIC INTAKE; DRUG EFFECT; EATING; FOOD INTAKE; GASTROINTESTINAL TRACT; GENETIC PREDISPOSITION; HUMAN; METABOLISM; MOUTH; NERVOUS SYSTEM; PHYSIOLOGY; SATIETY RESPONSE; SIGNAL TRANSDUCTION; TASTE;

APPETITE; APPETITE REGULATION; EATING; ENERGY INTAKE; GASTROINTESTINAL TRACT; GENETIC PREDISPOSITION TO DISEASE; HORMONES; HUMANS; MOUTH; NERVOUS SYSTEM; SATIETY RESPONSE; SIGNAL TRANSDUCTION; SWEETENING AGENTS; TASTE; TASTE PERCEPTION;

EID: 85051926916     PISSN: 09637486     EISSN: 14653478     Source Type: Journal    
DOI: 10.1080/09637486.2018.1492522     Document Type: Article

References (111)

1. Abdallah L, Chabert M, Louis-Sylvestre J. 1997. Cephalic phase responses to sweet taste. Am J Clin Nutr. 65:737–743
2. Antenucci RG, Hayes JE. 2015. Nonnutritive sweeteners are not supernormal stimuli. Int J Obes (Lond). 39:254–259
3. Anton SD, Martin CK, Han H, Coulon S, Cefalu WT, Geiselman P, Williamson DA. 2010. Effects of stevia, aspartame, and sucrose on food intake, satiety, and postprandial glucose and insulin levels. Appetite. 55:37–43
4. Bartoshuk LM, Duffy VB, Hayes JE, Moskowitz HR, Snyder DJ. 2006. Psychophysics of sweet and fat perception in obesity: problems, solutions and new perspectives. Philos Trans R Soc Lond B Biol Sci. 361:1137–1148
5. Bastaki S. 2015. Pharmacotherapy of nonnutritive sweeteners in diabetes mellitus. Int J Diabetes Metab. 23:11–22
6. Bellisle F, Louis-Sylvestre J, Demozay F, Blazy D, Le Magnen J. 1983. Reflex insulin response associated to food intake in human subjects. Physiol Behav. 31:515–521
7. Besnard P, Passilly-Degrace P, Khan NA. 2016. Taste of fat: a sixth taste modality? Physiol Rev. 96:151–176
8. Black RM, Leiter LA, Anderson GH. 1993. Consuming aspartame with and without taste: differential effects on appetite and food intake of young adult males. Physiol Behav. 53:459–466
9. Blundell JE, Hill AJ. 1986. Paradoxical effects of an intense sweetener (aspartame) on appetite. Lancet. 1:1092–1093
10. Boubaker J, Val-Laillet D, Guerin S, Malbert CH. 2012. Brain processing of duodenal and portal glucose sensing. J Neuroendocrinol. 24:1096–1105
11. Brown AW, Bohan Brown MM, Onken KL, Beitz DC. 2011. Short-term consumption of sucralose, a nonnutritive sweetener, is similar to water with regard to select markers of hunger signaling and short-term glucose homeostasis in women. Nutr Res. 31:882–888
12. Brown RJ, Rother KI. 2012. Non-nutritive sweeteners and their role in the gastrointestinal tract. J Clin Endocrinol Metab. 97:2597–2605
13. Burke MV, Small DM. 2015. Physiological mechanisms by which non-nutritive sweeteners may impact body weight and metabolism. Physiol Behav. 152:381–388
14. Calvo SS, Egan JM. 2015. The endocrinology of taste receptors. Nat Rev Endocrinol. 11:213–227
15. Cerf-Ducastel B, Van De Moortele PF, MacLeod P, Le Bihan D, Faurion A. 2001. Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chem Senses. 26:371–383
16. Chambers ES, Bridge MW, Jones DA. 2009. Carbohydrate sensing in the human mouth: effects on exercise performance and brain activity. J Physiol (Lond). 587:1779–1794
17. Cicerale S, Riddell LJ, Keast RS. 2012. The association between perceived sweetness intensity and dietary intake in young adults. J Food Sci. 77:H31–H35
18. Clouard C, Meunier-Salaun MC, Meurice P, Malbert CH, Val-Laillet D. 2014. Combined compared to dissociated oral and intestinal sucrose stimuli induce different brain hedonic processes. Front Psychol. 5:861
19. de Araujo IE, Rolls ET, Kringelbach ML, McGlone F, Phillips N. 2003. Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur J Neurosci. 18:2059–2068
20. Dhillon J, Lee JY, Mattes RD. 2017. The cephalic phase insulin response to nutritive and low-calorie sweeteners in solid and beverage form. Physiol Behav. 181:100–109
21. Drewnowski A, Henderson SA, Levine A, Hann C. 1999. Taste and food preferences as predictors of dietary practices in young women. Public Health Nutr. 2:513–519
22. DuBois GE. 2016. Molecular mechanism of sweetness sensation. Physiol Behav. 164:453–463
23. Duskova M, Macourek M, Sramkova M, Hill M, Starka L. 2013. The role of taste in cephalic phase of insulin secretion. Prague Med Rep. 114:222–230
24. Faurion A, Cerf B, Van De Moortele PF, Lobel E, Mac Leod P, Le Bihan D. 1999. Human taste cortical areas studied with functional magnetic resonance imaging: evidence of functional lateralization related to handedness. Neurosci Lett. 277:189–192
25. Fernstrom JD. 2015. Non-nutritive sweeteners and obesity. Annu Rev Food Sci Technol. 6:119–136
26. Fernstrom JD, Munger SD, Sclafani A, de Araujo IE, Roberts A, Molinary S. 2012. Mechanisms for sweetness. J Nutr. 142:1134S–1141S
27. Fogel A, Blissett J. 2014. Effects of sucrose detection threshold and weight status on intake of fruit and vegetables in children. Appetite. 83:309–316
28. Ford HE, Peters V, Martin NM, Sleeth ML, Ghatei MA, Frost GS, Bloom SR. 2011. Effects of oral ingestion of sucralose on gut hormone response and appetite in healthy normal-weight subjects. Eur J Clin Nutr. 65:508–513
29. Francis S, Rolls ET, Bowtell R, McGlone F, O'doherty J, Browning A, Clare S, Smith E. 1999. The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport. 10:453–459
30. Frank GK, Kaye WH, Carter CS, Brooks S, May C, Fissell K, Stenger VA. 2003. The evaluation of brain activity in response to taste stimuli–a pilot study and method for central taste activation as assessed by event-related fMRI. J Neurosci Methods. 131:99–105
31. Frank GK, Oberndorfer TA, Simmons AN, Paulus MP, Fudge JL, Yang TT, Kaye WH. 2008. Sucrose activates human taste pathways differently from artificial sweetener. NeuroImage. 39:1559–1569
32. Fushan AA, Simons CT, Slack JP, Drayna D. 2010. Association between common variation in genes encoding sweet taste signaling components and human sucrose perception. Chem Senses. 35:579–592
33. Fushan AA, Simons CT, Slack JP, Manichaikul A, Drayna D. 2009. Allelic polymorphism within the TAS1R3 promoter is associated with human taste sensitivity to sucrose. Curr Biol. 19:1288–1293
34. Gagnon L, Kupers R, Ptito M. 2015. Neural correlates of taste perception in congenital blindness. Neuropsychologia. 70:227–234
35. Geraedts MC, Troost FJ, Saris WH. 2011. Different tastants and low-caloric sweeteners induce differential effects on the release of satiety hormones. Food Chem. 129:731–738
36. Geraedts MC, Troost FJ, Saris WH. 2012. Addition of sucralose enhances the release of satiety hormones in combination with pea protein. Mol Nutr Food Res. 56:417–424
37. Green E, Murphy C. 2012. Altered processing of sweet taste in the brain of diet soda drinkers. Physiol Behav. 107:560–567
38. Gregersen S, Jeppesen PB, Holst JJ, Hermansen K. 2004. Antihyperglycemic effects of stevioside in type 2 diabetic subjects. Metab Clin Exp. 53:73–76
39. Grembecka M. 2015. Natural sweeteners in a human diet. Rocz Panstw Zakl Hig. 66:195–202
40. Haase L, Cerf-Ducastel B, Murphy C. 2009. Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety. NeuroImage. 44:1008–1021
41. Haase L, Green E, Murphy C. 2011. Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas. Appetite. 57:421–434
42. Han P, Keast RSJ, Roura E. 2017. Salivary leptin and TAS1R2/TAS1R3 polymorphisms are related to sweet taste sensitivity and carbohydrate intake from a buffet meal in healthy young adults. Br J Nutr. 118:763–770
43. Holt SHA, Cobiac L, Beaumont-Smith NE, Easton K, Best DJ. 2000. Dietary habits and the perception and liking of sweetness among Australian and Malaysian students: a cross-cultural study. Food Qual Prefer. 11:299–312
44. Hwang LD, Cuellar-Partida G, Ong JS, Breslin PA, Reed DR, MacGregor S, Gharahkhani P, Martin NG, Rentería ME. 2016. Sweet taste perception is associated with body mass index at the phenotypic and genotypic level. Twin Res Hum Genet. 19:465–471
45. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Zhou J, Kim HH, Xu X, Chan SL, Juhaszova M, et al. 2007. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc Natl Acad Sci USA. 104:15069–15074
46. Jayasinghe SN, Kruger R, Walsh DCI, Cao G, Rivers S, Richter M, Breier BH. 2017. Is sweet taste perception associated with sweet food liking and intake? Nutrients. 9:750
47. Joseph PV, Reed DR, Mennella JA. 2016. Individual differences among children in sucrose detection thresholds: relationship with age, gender, and bitter taste genotype. Nurs Res. 65:3–12
48. Just T, Pau HW, Engel U, Hummel T. 2008. Cephalic phase insulin release in healthy humans after taste stimulation? Appetite. 51:622–627
49. Kareken DA, Dzemidzic M, Oberlin BG, Eiler WJ. 2013. A preliminary study of the human brain response to oral sucrose and its association with recent drinking. Alcohol Clin Exp Res. 37:2058–2065
50. Kato Y, Roth R. 2012. Relationship between taste sensitivity and eating style in Japanese Female University students. Food Nutr Sci. 3(3):302–309
51. Keast RS, Roper J. 2007. A complex relationship among chemical concentration, detection threshold, and suprathreshold intensity of bitter compounds. Chem Senses. 32:245–253
52. Kim UK, Wooding S, Riaz N, Jorde LB, Drayna D. 2006. Variation in the human TAS1R taste receptor genes. Chem Senses. 31:599–611
53. Kuhn C, Bufe B, Winnig M, Hofmann T, Frank O, Behrens M, Lewtschenko T, Slack JP, Ward CD, Meyerhof W. 2004. Bitter taste receptors for saccharin and acesulfame K. J Neurosci. 24:10260–10265
54. Kuhre RE, Gribble FM, Hartmann B, Reimann F, Windeløv JA, Rehfeld JF, Holst JJ. 2014. Fructose stimulates GLP-1 but not GIP secretion in mice, rats, and humans. Am J Physiol Gastrointest Liver Physiol. 306:G622–G630
55. Laffitte A, Neiers F, Briand L. 2014. Functional roles of the sweet taste receptor in oral and extraoral tissues. Curr Opin Clin Nutr Metab Care. 17:379–385
56. Lavin JH, French SJ, Ruxton CH, Read NW. 2002. An investigation of the role of oro-sensory stimulation in sugar satiety? Int J Obes Relat Metab Disord. 26:384–388
57. Lindemann B. 2001. Receptors and transduction in taste. Nature. 413:219–225
58. Little TJ, Gupta N, Case RM, Thompson DG, McLaughlin JT. 2009. Sweetness and bitterness taste of meals per se does not mediate gastric emptying in humans. Am J Physiol Regul Integr Comp Physiol. 297:R632–R639
59. Loper HB, La Sala M, Dotson C, Steinle N. 2015. Taste perception, associated hormonal modulation, and nutrient intake. Nutr Rev. 73:83–91
60. Low JY, Lacy KE, McBride R, Keast RS. 2016. The association between sweet taste function, anthropometry, and dietary intake in adults. Nutrients. 8:241
61. Ma J, Bellon M, Wishart JM, Young R, Blackshaw LA, Jones KL, Horowitz M, Rayner CK. 2009. Effect of the artificial sweetener, sucralose, on gastric emptying and incretin hormone release in healthy subjects. Am J Physiol Gastrointest Liver Physiol. 296:G735–G739
62. Ma J, Chang J, Checklin HL, Young RL, Jones KL, Horowitz M, Rayner CK. 2010. Effect of the artificial sweetener, sucralose, on small intestinal glucose absorption in healthy human subjects. Br J Nutr. 104:803–806
63. Mahar A, Duizer LM. 2007. The effect of frequency of consumption of artificial sweeteners on sweetness liking by women. J Food Sci. 72:S714–S718
64. Mainland JD, Matsunami H. 2009. Taste perception: how sweet it is (to be transcribed by you). Curr Biol. 19:R655–R656
65. Margolskee RF, Dyer J, Kokrashvili Z, Salmon KS, Ilegems E, Daly K, Maillet EL, Ninomiya Y, Mosinger B, Shirazi-Beechey SP. 2007. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci USA. 104:15075–15080
66. Martin LJ, Sollars SI. 2017. Contributory role of sex differences in the variations of gustatory function. J Neurosci Res. 95:594–603
67. Martinez-Cordero E, Malacara-Hernandez JM, Martinez-Cordero C. 2015. Taste perception in normal and overweight Mexican adults. Appetite. 89:192–195
68. Melanson KJ, Zukley L, Lowndes J, Nguyen V, Angelopoulos TJ, Rippe JM. 2007. Effects of high-fructose corn syrup and sucrose consumption on circulating glucose, insulin, leptin, and ghrelin and on appetite in normal-weight women. Nutrition. 23:103–112
69. Mennella I, Ferracane R, Zucco F, Fogliano V, Vitaglione P. 2015. Food Liking Enhances the Plasma Response of 2-Arachidonoylglycerol and of Pancreatic Polypeptide upon Modified Sham Feeding in Humans. J Nutr. 145:2169–2175
70. Meyers B, Brewer MS. 2008. Sweet taste in man: a review. J Food Sci. 73:R81–R90
71. Mitchel H. 2006. Sweeteners and sugar alternatives in food technology. Oxford (UK): Blackwell Publishing Ltd
72. Monsivais P, Perrigue MM, Drewnowski A. 2007. Sugars and satiety: does the type of sweetener make a difference? Am J Clin Nutr. 86:116–123
73. Morini G, Bassoli A, Temussi PA. 2005. From small sweeteners to sweet proteins: anatomy of the binding sites of the human T1R2_T1R3 receptor. J Med Chem. 48:5520–5529
74. Nakamura Y, Sanematsu K, Ohta R, Shirosaki S, Koyano K, Nonaka K, Shigemura N, Ninomiya Y. 2008. Diurnal variation of human sweet taste recognition thresholds is correlated with plasma leptin levels. Diabetes. 57:2661–2665
75. Oberndorfer TA, Frank GK, Simmons AN, Wagner A, McCurdy D, Fudge JL, Yang TT, Paulus MP, Kaye WH. 2013. Altered insula response to sweet taste processing after recovery from anorexia and bulimia nervosa. Am J Psychiatry. 170:1143–1151
76. O'Doherty J, Rolls ET, Francis S, Bowtell R, McGlone F. 2001. Representation of pleasant and aversive taste in the human brain. J Neurophysiol. 85:1315–1321
77. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ. 2002. Neural responses during anticipation of a primary taste reward. Neuron. 33:815–826
78. Pepino MY, Finkbeiner S, Beauchamp GK, Mennella JA. 2010. Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women. Obesity (Silver Spring). 18:959–965
79. Power ML, Schulkin J. 2008. Anticipatory physiological regulation in feeding biology: cephalic phase responses. Appetite. 50:194–206
80. Purnell JQ, Klopfenstein BA, Stevens AA, Havel PJ, Adams SH, Dunn TN, Krisky C, Rooney WD. 2011. Brain functional magnetic resonance imaging response to glucose and fructose infusions in humans. Diabetes Obes Metab. 13:229–234
81. Ripken D, van der Wielen N, Wortelboer HM, Meijerink J, Witkamp RF, Hendriks HF. 2014. Steviol glycoside rebaudioside A induces glucagon-like peptide-1 and peptide YY release in a porcine ex vivo intestinal model. J Agric Food Chem. 62:8365–8370
82. Rogers PJ. 2017. The role of low-calorie sweeteners in the prevention and management of overweight and obesity: evidence v. conjecture. Proc Nutr Soc. 1–9
83. Rogers PJ, Carlyle JA, Hill AJ, Blundell JE. 1988. Uncoupling sweet taste and calories: comparison of the effects of glucose and three intense sweeteners on hunger and food intake. Physiol Behav. 43:547–552
84. Rudenga KJ, Small DM. 2012. Amygdala response to sucrose consumption is inversely related to artificial sweetener use. Appetite. 58:504–507
85. Rudenga KJ, Small DM. 2013. Ventromedial prefrontal cortex response to concentrated sucrose reflects liking rather than sweet quality coding. Chem Senses. 38:585–594
86. Sadler MJ, McNulty H, Gibson S. 2015. Sugar-fat seesaw: a systematic review of the evidence. Crit Rev Food Sci Nutr. 55:338–356
87. Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J. 2005. Functional magnetic resonance imaging of human hypothalamic responses to sweet taste and calories. Am J Clin Nutr. 82:1011–1016
88. Smeets PA, Weijzen P, de Graaf C, Viergever MA. 2011. Consumption of caloric and non-caloric versions of a soft drink differentially affects brain activation during tasting. NeuroImage. 54:1367–1374
89. Spetter MS, de Graaf C, Mars M, Viergever MA, Smeets PA. 2014. The sum of its parts-effects of gastric distention, nutrient content and sensory stimulation on brain activation. PLoS One. 9:e90872
90. Steinert RE, Frey F, Topfer A, Drewe J, Beglinger C. 2011. Effects of carbohydrate sugars and artificial sweeteners on appetite and the secretion of gastrointestinal satiety peptides. Br J Nutr. 105:1320–1328
91. Tarragon E, Moreno JJ. 2017. Role of endocannabinoids on sweet taste perception, food preference, and obesity-related disorders. Chem Senses. 43:3–16
92. Teff KL, Devine J, Engelman K. 1995. Sweet taste: effect on cephalic phase insulin release in men. Physiol Behav. 57:1089–1095
93. Teff KL, Mattes RD, Engelman K, Mattern J. 1993. Cephalic-phase insulin in obese and normal-weight men: relation to postprandial insulin. Metab Clin Exp. 42:1600–1608
94. Temizkan S, Deyneli O, Yasar M, Arpa M, Gunes M, Yazici D, Sirikci O, Haklar G, Imeryuz N, Yavuz DG. 2015. Sucralose enhances GLP-1 release and lowers blood glucose in the presence of carbohydrate in healthy subjects but not in patients with type 2 diabetes. Eur J Clin Nutr. 69:162–166
95. Tordoff MG, Alleva AM. 1990. Oral stimulation with aspartame increases hunger. Physiol Behav. 47:555–559
96. Tsurugizawa T, Uematsu A, Nakamura E, Hasumura M, Hirota M, Kondoh T, Uneyama H, Torii K. 2009. Mechanisms of neural response to gastrointestinal nutritive stimuli: the gut-brain axis. Gastroenterology. 137:262–273
97. Tsurugizawa T, Uneyama H. 2014. Differences in BOLD responses to intragastrically infused glucose and saccharin in rats. Chem Senses. 39:683–691
98. Turner CE, Byblow WD, Stinear CM, Gant N. 2014. Carbohydrate in the mouth enhances activation of brain circuitry involved in motor performance and sensory perception. Appetite. 80:212–219
99. Umabiki M, Tsuzaki K, Kotani K, Nagai N, Sano Y, Matsuoka Y, Kitaoka K, Okami Y, Sakane N, Higashi A. 2010. The improvement of sweet taste sensitivity with decrease in serum leptin levels during weight loss in obese females. Tohoku J Exp Med. 220:267–271
100. van Avesaat M, Troost FJ, Ripken D, Peters J, Hendriks HF, Masclee AA. 2015. Intraduodenal infusion of a combination of tastants decreases food intake in humans. Am J Clin Nutr. 102:729–735
101. van Rijn I, de Graaf C, Smeets PA. 2015. Tasting calories differentially affects brain activation during hunger and satiety. Behav Brain Res. 279:139–147
102. Webb J, Bolhuis DP, Cicerale S, Hayes JE, Keast R. 2015. The relationships between common measurements of taste function. Chemosens Percept. 8:11–18
103. Wise PM, Nattress L, Flammer LJ, Beauchamp GK. 2016. Reduced dietary intake of simple sugars alters perceived sweet taste intensity but not perceived pleasantness. Am J Clin Nutr. 103:50–60
104. Wolnerhanssen BK, Meyer-Gerspach AC, Schmidt A, Zimak N, Peterli R, Beglinger C, Borgwardt S. 2015. Dissociable behavioral, physiological and neural effects of acute glucose and fructose ingestion: a pilot study. PLoS One. 10:e0130280
105. Wong GT, Gannon KS, Margolskee RF. 1996. Transduction of bitter and sweet taste by gustducin. Nature. 381:796–800
106. Wu T, Zhao BR, Bound MJ, Checklin HL, Bellon M, Little TJ, Young RL, Jones KL, Horowitz M, Rayner CK. 2012. Effects of different sweet preloads on incretin hormone secretion, gastric emptying, and postprandial glycemia in healthy humans. Am J Clin Nutr. 95:78–83
107. Xu H, Staszewski L, Tang H, Adler E, Zoller M, Li X. 2004. Different functional roles of T1R subunits in the heteromeric taste receptors. Proc Natl Acad Sci USA. 101:14258–14263
108. Yarmolinsky DA, Zuker CS, Ryba NJ. 2009. Common sense about taste: from mammals to insects. Cell. 139:234–244
109. Young RL, Sutherland K, Pezos N, Brierley SM, Horowitz M, Rayner CK, Blackshaw LA. 2009. Expression of taste molecules in the upper gastrointestinal tract in humans with and without type 2 diabetes. Gut. 58:337–346
110. Yoshinaka M, Ikebe K, Uota M, Ogawa T, Okada T, Inomata C, Takeshita H, Mihara Y, Gondo Y, Masui Y, et al. 2016. Age and sex differences in the taste sensitivity of young adult, young-old and old-old Japanese. Geriatr Gerontol Int. 16:1281–1288
111. Zhang F, Klebansky B, Fine RM, Liu H, Xu H, Servant G, Zoller M, Tachdjian C, Li X. 2010. Molecular mechanism of the sweet taste enhancers. Proc Natl Acad Sci USA. 107:4752–4757