The role of T1r3 and Trpm5 in carbohydrate-induced obesity in mice

Physiology and Behavior

Volumn 107, Issue 1, 2012, Pages 50-58

  Glendinning, John I ^a   Gillman, Jennifer ^a   Zamer, Haley ^a   Margolskee, Robert F ^b   Sclafani, Anthony ^c  

^a Program on US Russia Relations at Columbia s Harriman Institute   (United States)

^b MONELL CHEMICAL SENSES CENTER   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Carbohydrate; Diet induced obesity; Nutrient utilization; Palatability; Taste

Indexed keywords

CARBOHYDRATE; G PROTEIN COUPLED RECEPTOR; GLUCOSE POLYMER; INTRALIPID; PROTEIN TLR3; RECEPTOR PROTEIN; SUCROSE; SUGAR; TRANSIENT RECEPTOR POTENTIAL CHANNEL M5; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; MALE; MOUSE; NONHUMAN; NUTRIENT; OBESITY; OVERNUTRITION; PALATABILITY; PRIORITY JOURNAL; TASLR3 GENE; TASTE BUD; TRPM5 GENE; WEIGHT GAIN; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHT; CARBOHYDRATES; DISEASE MODELS, ANIMAL; EATING; FEMALE; FOOD PREFERENCES; GLUCANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OBESITY; RANDOM ALLOCATION; RECEPTORS, G-PROTEIN-COUPLED; SEX FACTORS; SUCROSE; SWEETENING AGENTS; TRPM CATION CHANNELS;

EID: 84862610589     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.05.023     Document Type: Article

References (79)

1. Allison D.B., Mattes R.D. Nutritively sweetened beverage consumption and obesity: the need for solid evidence on a fluid issue. JAMA 2009, 301:318-320.
2. Almind K., Manieri M., Sivitz W.I., Cinti S., Kahn C.R. Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice. PNAS 2007, 104:2366-2371.
3. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
4. Bermudez O.I., Gao X. Greater consumption of sweetened beverages and added sugars is associated with obesity among US young adults. Ann Nutr Metab 2010, 57:211-218.
5. Berridge K., Grill H.J., Norgren R. Relation of consummatory responses and preabsorptive insulin release to palatability and learned taste aversions. J Comp Physiol Psychol 1981, 95:363-382.
6. Berthoud H.-R., Trimble E.R., Siegel E.G., Bereiter D.A., Jeanrenaud B. Cephalic-phase insulin secretion in normal and pancreatic islet-transplanted rats. Am J Physiol 1980, 238:E336-E340.
7. Berthoud H.-R., Bereiter D.A., Trimble E.R., Siegel E.G., Jeanrenaud B. Cephalic phase, reflex insulin secretion: neuroanatomical and physiological characterization. Diabetologia 1981, 20:393-401.
8. Bezençon C., le Coutre J., Damak S. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem Senses 2007, 32:41-49.
9. Blednov Y.A., Walker D., Martinez M., Levine M., Damak S., Margolskee R.F. Perception of sweet taste is important for voluntary alcohol consumption in mice. Genes Brain Behav 2008, 1-13.
10. Brixel L.R., Monteilh-Zoller M.K., Ingenbrandt C.S., Fleig A., Penner R., Enklaar T., et al. TRPM5 regulates glucose-stimulated insulin secretion. Pflugers Arch 2010, 460:69-76.
11. Buddington R.K., Chen J.W., Diamond J.M. Dietary regulation of intestinal brush-border sugar and amino acid transport in carnivores. Am J Physiol 1991, 261:R793-R801.
12. Cao D., Lu H., Lewis T.L., Li L. Intake of sucrose-sweetened water induces insulin resistance and exacerbates memory deficits and amyloidosis in a transgenic mouse model of Alzheimer disease. J Biol Chem 2007, 282:36275-36282.
13. Cartoni C., Yasumatsu K., Ohkuri T., Shigemura N., Yoshida R., Godinot N., et al. Taste preference for fatty acids is mediated by GPR40 and GPR120. J Neurosci 2010, 30:8376-8382.
14. Chavez-Jauregui R.N., Mattes R.D., Parks E.J. Dynamics of fat absorption and effect of sham feeding on postprandial lipema. Gastroenterology 2010, 139:1538-1548.
15. 2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5-/- mice. PNAS 2010, 107:5208-5213.
16. Crystal S.R., Teff K.L. Tasting fat: cephalic phase hormonal responses and food intake in restrained and unrestrained eaters. Physiol Behav 2006, 89:213-220.
17. Cui M., Jiang P., Maillet E., Max M., Margolskee R.F., Osman R. The heterodimeric sweet taste receptor has multiple potential ligand binding sites. Curr Pharm Des 2006, 12:4591-4600.
18. Damak S., Rong M., Yasumatsu K., Kokrashvili Z., Varadarajan V., Zou S., et al. Detection of sweet and umami taste in the absence of taste receptor T1R3. Science 2003, 301:850-853.
19. Damak S., Rong M., Yasumatsu K., Kokrashvili K., Pérez C.A., Shigemura N., et al. Trpm5 null mice respond to bitter, sweet, and umami compounds. Chem Senses 2006, 31:253-264.
20. de Araujo I.E., Oliveira-Maia A.J., Sotnikova T.D., Gainetdinov R.R., Caron M.G., Nicolelis M.A.L., et al. Food reward in the absence of taste receptor signaling. Neuron 2008, 57:930-941.
21. Drewnowski A. Obesity and the food environment: dietary energy density and diet costs. Am J Prev Med 2004, 27(3S):154-162.
22. Edfalk S., Steneberg P., Edlund H. Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 2008, 57:2280-2287.
23. Forshee R.A., Anderson P.A., Storey M.L. Sugar-sweetened beverages and body mass index in children and adolescents: a metaanalysis. Am J Clin Nutr 2008, 87:1662-1671.
24. Glendinning J.I., Feld N., Goodman L., Bayor R. Contribution of orosensory stimulation to strain differences in oil intake by mice. Physiol Behav 2008, 95:476-483.
25. Glendinning J.I., Breinager L., Kyrillou E., Lacuna K., Rocha R., Sclafani A. Differential effects of sucrose and fructose on dietary obesity in four mouse strains. Physiol Behav 2010, 101:331-343.
26. Grill H.J., Berridge K.C., Ganster D.J. Oral glucose is the prime elicitor of preabsorptive insulin secretion. Am J Physiol 1984, 246:R88-R95.
27. Hesse D., Dunn M., Heldmaier G., Klingenspor M., Rozman J. Behavioural mechanisms affecting energy regulation in mice prone or resistant to diet-induced obesity. Physiol Behav 2010, 99:370-380.
28. Hu F.B., Malik V.S. Sugar-sweetened beverages and risk of obesity and type 2 diabetes: epidemiologic evidence. Physiol Behav 2010, 100:47-54.
29. Jang H.-J., Kokrashvili Z., Theodorakis M.J., Carlson O.D., Kim B.-J., Zhou J., et al. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. PNAS 2007, 104:15069-15074.
30. Jürgens H., Haass W., Castaneda T.R., Schürmann A., Koebnick C., Dombrowski F., et al. Consuming fructose-sweetened beverages increases body adiposity in mice. Obes Res 2005, 13:1146-1156.
31. Kanarek R.B., Orthen-Gambill N. Differential effects of sucrose, fructose and glucose on carbohydrate-induced obesity in rats. J Nutr 1982, 112:1546-1554.
32. Kojima I., Nakagawa Y. The role of the sweet taste receptor in enteroendocrine cells and pancreatic β-cells. Diabetes Metab J 2011, 35:451-457.
33. Kokrashvili Z., Mosinger B., Margolskee R.F. T1r3 and α-gustducin in gut regulate secretion of glucagon-like peptide-1. Ann N Y Acad Sci 2009, 1170:91-94.
34. Kyriazis G.A., Soundarapandian M.M., Tyrberg B. Sweet taste receptor signaling in beta cells mediates fructose-induced potentiation of glucose-stimulated insulin secretion. PNAS 2012, 109(8):E524-E532.
35. Laugerette F., Passilly-Degrace P., Patris B., Niot I., Febbraio M., Montmayeur J.-P., et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest 2005, 115:3177-3184.
36. Le Gall M., Tobin V., Stolarczyk E., Dalet V., Leturque A., Brot-Laroche E. Sugar sensing by enterocytes combines polarity, membrane bound detectors and sugar metabolism. J Cell Physiol 2007, 213:834-843.
37. Lenard N.R., Berthoud H.-R. Central and peripheral regulation of food intake and physical activity: pathways and genes. Obesity 2008, 16(Supplement 3):S11-S22.
38. Li X., Li W., Wang H., Cao J., Maehashi K., Huang L., et al. Pseudogenization of a sweet-receptor gene accounts for cats' indifference toward sugar. PLoS Genet 2005, 1:e3.
39. Light H.R., Tsanzi E., Gigliotti J., Morgan K., Tou J.C. The type of caloric sweetener added to water influences weight gain, fat mass, and reproduction in growing Sprague-Dawley female rats. Exp Biol Med 2009, 234:651-661.
40. Lindqvist A., Baelemans A., Erlanson-Albertsson C. Effects of sucrose, glucose and fructose on peripheral and central appetite signals. Regul Pept 2008, 150:26-32.
41. Mace O.J., Affleck J., Nick Patel N., Kellett G.L. Sweet taste receptors in rat small intestine stimulate glucose absorption through apical GLUT2. J Physiol 2007, 582:379-392.
42. +-glucose cotransporter. PNAS 2007, 104:15075-15080.
43. Marks-Kaufman R., Hamm M.W., Barbato G.F. The effects of dietary sucrose on opiate receptor binding in genetically obese (ob/ob) and lean mice. J Am Coll Nutr 1989, 8:9-14.
44. Mucci L, Santilli F, Cuccurullo C, Davi G. Cardiovascular risk and dietary sugar intake: is the link so sweet? Intern Emerg Med in press.
45. Nakagawa Y., Nagasawa M., Yamada S., Hara A., Mogami H., Nikolaev V.O., et al. Sweet taste receptor expressed in pancreatic b-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion. PLoS One 2009, 4:e5106.
46. +-coupled glucose transporter SGLT1 by gum arabic (Acacia senegal). Cell Physiol Biochem 2010, 25:203-210.
47. Nelson G., Hoon M.A., Chadrashekar J., Zhang Y., Ryba N.J., Zuker C.S. Mammalian sweet receptors. Cell 2001, 106:381-390.
48. Nishikawa S., Yasoshima A., Doi K., Nakayama H., Uetsuka K. Involvement of sex, strain and age factors in high fat diet-induced obesity in C57BL/6J and BALB/cA mice. Exp Anim 2007, 56:263-272.
49. Parker H.E., Habib A.M., Rogers G.J., Gribble F.M., Reimann F. Nutrient-dependent secretion of glucose-dependent insulinotropic polypeptide from primary murine K cells. Diabetologia 2009, 52:289-298.
50. Picard F., Naïmi N., Richard D., Deshaies Y. Response of adipose tissue lipoprotein lipase to the cephalic phase of insulin secretion. Diabetes 1999, 48:452-459.
51. 2+]i. Proc Natl Acad Sci U S A 2003, 100:15166-15171.
52. Ruxton C.H.S., Garnder E.J., McNulty H.M. Is sugar consumption detrimental to health? A review of the evidence 1995-2006. Crit Rev Food Sci Nutr 2010, 50:1-19.
53. Sclafani A., Springer D. Dietary obesity in adult rats: similarities to hypothalamic and human obesity syndromes. Physiol Behav 1974, 17:461-471.
54. Sclafani A. Carbohydrate-induced hyperphagia and obesity in the rat: effects of saccharide type, form, and taste. Neurosci Biobehav Rev 1987, 11:155-162.
55. Sclafani A., Lucas F., Ackroff K. The importance of taste and palatability in carbohydrate-induced overeating in rats. Am J Physiol 1996, 270:R1197-R1202.
56. Sclafani A. Oral and postoral determinants of food reward. Physiol Behav 2004, 81:773-779.
57. Sclafani A., Glendinning J.I. Sugar and fat conditioned flavor preferences in C57BL/6J and 129 mice: oral and postoral interactions. Am J Physiol 2005, 289:R712-R720.
58. Sclafani A., Zukerman S., Glendinning J.I., Margolskee R.F. Fat and carbohydrate preferences in mice: the contribution of alpha-gustducin and Trpm5 taste-signaling proteins. Am J Physiol 2007, 293:R1504-R1513.
59. Sclafani A., Glass D.S., Margolskee R.F., Glendinning J.I. Gut T1R3 sweet taste receptors do not mediate sucrose-conditioned flavor preferences in mice. Am J Physiol 2010, 299:R1643-R1650.
60. Sclafani A., Ackroff K. The role of gut nutrient sensing in stimulating appetite and conditioning food preferences. Am J Physiol 2012, 302:R1119-R1133.
61. Shinozaki K., Shimizu Y., Shiina T., Morita H., Takewaki T. Relationship between taste-induced physiological reflexes and temperature of sweet taste. Physiol Behav 2008, 93:1000-1004.
62. Shirazi-Beechey S.P., Moran A.W., Batchelor D.J., Daly K., Al-Rammahi M. Session 3: influences of food constituents on gut health. Glucose sensing and signalling; regulation of intestinal glucose transport. Proc Nutr Soc 2011, 70:185-193.
63. Smeets P.A.M., Erkner A., de Graaf C. Cephalic phase responses and appetite. Nutr Rev 2010, 68:643-655.
64. Steinert R.E., Gerspach A.C., Gutmann H., Asarian L., Drewe J., Beglinger C. The functional involvement of gut-expressed sweet taste receptors in glucose-stimulated secretion of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY). Clin Nutr 2011, 30:524-532.
65. Takeda M., Imaizumi M., Sawano S., Manabe Y., Fushiki T. Long-term optional ingestion of corn oil induces excessive caloric intake and obesity in mice. Nutrition 2001, 17:117-120.
66. Tonosaki K., Hori Y., Shimizu Y., Tonosaki K. Relationship between insulin release and taste. Biomed Res 2007, 28:79-83.
67. Tonosaki K. Relationships between cephalic phase insulin release and taste modalities. The cephalic/neural phase in nutrition 2009, 83-92. Research Signpost, Kerala, India. M.A. Zafra, F. Molina, A. Puerto (Eds.).
68. Treesukosol Y., Blonde G.D., Spector A.C. T1R2 and T1R3 subunits are individually unnecessary for normal affective licking responses to Polycose: implications for saccharide taste receptors in mice. Am J Physiol 2009, 296:R855-R865.
69. Treesukosol Y., Smith K.R., Spector A.C. Behavioral evidence for a glucose polymer taste receptor that is independent of the T1R2+3 heterodimer in a mouse model. J Neurosci 2011, 31:13527-13534.
70. Wang P.Y.T., Caspi L., Lam C.K.L., Chari M., Li X., Light P.E., et al. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 2008, 452:1012-1016.
71. Warwick Z.S., Weingarten H.P. Determinants of high-fat diet hyperphagia: experimental dissection of orosensory and postingestive effects. Am J Physiol 1995, 269:R30-R37.
72. West D.B., Boozer C.N., Moody D.L., Atkinson R.L. Dietary obesity in nine inbred mouse strains. Am J Physiol 1992, 262:R1025-R1032.
73. Woods S.C., Gotoh K., Clegg D.J. Gender differences in the control of energy homeostasis. Exp Biol Med 2003, 228:1175-1180.
74. Yoder S.M., Yang Q., Kindel T.L., Tso P. Stimulation of incretin secretion by dietary lipid: is it dose dependent?. Am J Physiol 2009, 297:G299-G305.
75. Zhang Y., Hoon M.A., Chandrashekar J., Mueller K.L., Cook B., Wu D., et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 2003, 112:293-301.
76. Zhang Z., Zhao Z., Margolskee R.F., Liman E. The transduction channel TRPM5 is gated by intracellular calcium in taste cells. J Neurosci 2007, 27:5777-5786.
77. Zhao G.Q., Zhang Y., Hoon M.A., Chandrashekar J., Erlenbach I., Ryba N.J.P., et al. The receptors for mammalian sweet and umami taste. Cell 2003, 115:255-266.
78. Zukerman S., Glendinning J.I., Margolskee R.F., Sclafani A. T1R3 taste receptor is critical for sucrose but not Polycose taste. Am J Physiol 2009, 296:R866-R876.
79. Zukerman S., Touzani K., Margolskee R.F., Sclafani A. Role of olfaction in the conditioned sucrose preference of sweet-ageusic T1R3 knockout mice. Chem Senses 2009, 34:685-694.