Sweet taste receptor gene variation and aspartame taste in primates and other species

Chemical Senses

Volumn 36, Issue 5, 2011, Pages 453-475

  Li, Xia ^a,d   Bachmanov, Alexander A ^a   Maehashi, Kenji ^a,e   Li, Weihua ^a,f   Lim, Raymond ^a,g   Brand, Joseph G ^a   Beauchamp, Gary K ^a   Reed, Danielle R ^a   Thai, Chloe ^b   Floriano, Wely B ^c  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

^c LAKEHEAD UNIVERSITY   (Canada)

^d AmeriPath Northeast   (United States)

^e TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Aspartame; Modeling; Primates; Sweet taste; T1R2; T1R3; Taste receptor

Indexed keywords

ASPARTAME; CELL PROTEIN; GENOMIC DNA; SWEET TASTE RECEPTOR PROTEIN T1R2; SWEET TASTE RECEPTOR PROTEIN T1R3; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALLITRICHINAE; CHIMPANZEE; COMPUTER MODEL; CONTROLLED STUDY; DNA SEQUENCE; ERYTHROCEBUS; GENE AMPLIFICATION; GENETIC VARIABILITY; GORILLA; MACACA MULATTA; MOLECULAR DOCKING; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; ORANG UTAN; ORTHOLOGY; PRIORITY JOURNAL; SANGUINUS LABIATUS; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; SQUIRREL MONKEY; SWEETNESS; TASTE BUD; TASTE DISCRIMINATION;

CERCOPITHECIDAE; MAMMALIA; PRIMATES;

EID: 79957502049     PISSN: 0379864X     EISSN: 14643553     Source Type: Journal    
DOI: 10.1093/chemse/bjq145     Document Type: Article

References (106)

1. Ariyasu T, Matsumoto S, Kyono F, Hanaya T, Arai S, Ikeda M, Kurimoto M. 2003. Taste receptor T1R3 is an essential molecule for the cellular recognition of the disaccharide trehalose. In Vitro Cell Dev Biol Anim. 39:80-88.
2. Bachmanov AA, Li X, Reed DR, Ohmen JD, Li S, Chen Z, Tordoff MG, de Jong PJ, Wu C, West DB, et al. 2001. Positional cloning of the mouse saccharin preference (Sac) locus. Chem Senses. 26:925-933.
3. Bachmanov AA, Tordoff MG, Beauchamp GK. 2001. Sweetener preference of C57BL/6ByJ and 129P3/J mice. Chem Senses. 26: 905-913.
4. Bosetti C, Gallus S, Talamini R, Montella M, Franceschi S, Negri E, La Vecchia C. 2009. Artificial sweeteners and the risk of gastric, pancreatic, and endometrial cancers in Italy. Cancer Epidemiol Biomarkers Prev. 18:2235-2238.
5. Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, Slack JP, Kim UK, Drayna D, Meyerhof W. 2005. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol. 15:322-327.
6. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng L, Guo W, Zuker CS, Ryba NJ. 2000. T2Rs function as bitter taste receptors. Cell. 100: 703-711.
7. Conn PJ, Christopoulos A, Lindsley CW. 2009. Allosteric modulators of GPCRs: a novel approach for the treatment of CNS disorders. Nat Rev Drug Discov. 8:41-54.
8. Crocker L, Algina J. 1986. Introduction to classical and modern test theory. New York: Harcourt Brace Jovanovich College Publishers.
9. Cui M, Jiang P, Maillet E, Max M, Margolskee RF, Osman R. 2006. The heterodimeric sweet taste receptor has multiple potential ligand binding sites. Curr Pharm Des. 12:4591-4600.
10. Damak S, Rong M, Yasumatsu K, Kokrashvili Z, Varadarajan V, Zou S, Jiang P, Ninomiya Y, Margolskee RF. 2003. Detection of sweet and umami taste in the absence of taste receptor T1r3. Science. 301:850-853.
11. Danilova V, Danilov Y, Roberts T, Tinti JM, Nofre C, Hellekant G. 2002. Sense of taste in a new world monkey, the common marmoset: recordings from the chorda tympani and glossopharyngeal nerves. J Neurophysiol. 88:579-594.
12. Danilova V, Hellekant G, Roberts T, Tinti JM, Nofre C. 1998. Behavioral and single chorda tympani taste fiber responses in the common marmoset, Callithrix jacchus jacchus. Ann N Y Acad Sci. 855:160-164.
13. Danilova V, Hellekant G, Tinti JM, Nofre C. 1998. Gustatory responses of the hamster Mesocricetus auratus to various compounds considered sweet by humans. J Neurophysiol. 80:2102-2112.
14. De Francisco JC, Dess NK. 1998. Aspartame consumption in rats selectively bred for high versus low saccharin intake. Physiol Behav. 65:393-396.
15. Dubois GE. 2008. Chemistry of gustatory stimuli. In: Firestein S, Beauchamp GK, editors. The senses: a comprehensive reference. San Diego, CA: Academic Press. p. 27-74.
16. Ferrari AM, Degliesposti G, Sgobba M, Rastelli G. 2007. Validation of an automated procedure for the prediction of relative free energies of binding on a set of aldose reductase inhibitors. Bioorg Med Chem. 15:7865-7877.
17. Floriano WB, Vaidehi N, Zamanakos G, Goddard WA 3rd. 2004. HierVLS hierarchical docking protocol for virtual ligand screening of largemolecule databases. J Med Chem. 47:56-71.
18. Fratev F, Benfenati E. 2008. A combination of 3D-QSAR, docking, local-binding energy (LBE) and GRID study of the species differences in the carcinogenicity of benzene derivatives chemicals. J Mol Graph Model. 27:147-160.
19. Gallus S, Scotti L, Negri E, Talamini R, Franceschi S, Montella M, Giacosa A, Dal Maso L, La Vecchia C. 2007. Artificial sweeteners and cancer risk in a network of case-control studies. Ann Oncol. 18:40-44.
20. Gasteiger J, Marsili M. 1980. Iterative partial equalization of orbital electronegativity- a rapid access to atomic charges. Tetrahedron. 36:3219-3228.
21. Gilson MK, Zhou HX. 2007. Calculation of protein-ligand binding affinities. Annu Rev Biophys Biomol Struct. 36:21-42.
22. Glaser D. 2002. Specialization and phyletic trends of sweetness reception in animals. Pure Appl Chem. 74:1153-1158.
23. Glaser D, Tinti JM, Nofre C. 1995. Evolution of the sweetness receptor in primates. I. Why does alitame taste sweet in all Prosimians and Simians, and aspartame only in Old World Simians? Chem Senses. 20:573-584.
24. Glaser D, Tinti J-M, Nofre C. 1996. Gustatory responses of non-human primates to dipeptide derivatives or analogues, sweet in man. Food Chem. 56:313-321.
25. Glaser D, van der Wel H, Brouwer JN, Dubois GE, Hellekant G. 1992. Gustatory responses in primates to the sweetener aspartame and their phylogenetic implications. Chem Senses. 17:325-335.
26. Glaser D, Wanner M, Tinti JM, Nofre C. 2000. Gustatory responses of pigs to various natural and artificial compounds known to be sweet in man. Food Chem. 68:375-385.
27. Gordesky-Gold B, Rivers N, Ahmed OM, Breslin PA. 2008. Drosophila melanogaster prefers compounds perceived sweet by humans. Chem Senses. 33:301-309.
28. Grigoriev FV, Luschekina SV, Romanov AN, Sulimov VB, Nikitina EA. 2007. Computation of entropy contribution to protein-ligand binding free energy. Biochemistry (Mosc). 72:785-792.
29. Hard af Segerstad C, Hellekant G. 1989a. The sweet taste in the calf. I. Chorda tympani proper nerve responses to taste stimulation of the tongue. Physiol Behav. 45:633-638.
30. Hard af Segerstad CH, Hellekant G. 1989b. The sweet taste in the calf. II. Glossopharyngeal nerve responses to taste stimulation of the tongue. Physiol Behav. 45:1043-1047.
31. Hellekant G, Danilova V. 1996. Species differences toward sweetness. Food Chem. 56:323-328.
32. Hellekant G, Danilova V, Ninomiya Y. 1997. Primate sense of taste: behavioral and single chorda tympani and glossopharyngeal nerve fiber recordings in the rhesus monkey, Macaca mulatta. J Neurophysiol. 77:978-993.
33. Hellekant G, Glaser D, Brouwer JN, Van der Wel H. 1981. Gustatory response of three prosimian and two simian primate species (Tupaia glis, Nycticebus cou cang, Galago senegalensis, Callithrix jacchus jacchus and Saguinus midas niger) to six sweeteners and miraculin and their phylogenetic implications. Chem Senses. 6:165-173.
34. Hellekant G, Glaser D, Brower J, van der Wel H. 1980. Study of behavioural and neurophysiological experiments on the sweet taste of five primates. In: Van der Starre H, editor. Olfaction and taste VII. Oxford: IRL Press Ltd. p. 183-186.
35. Hellekant G, Hard af Segerstad C, Roberts TW. 1994. Sweet taste in the calf: III. Behavioral responses to sweeteners. Physiol Behav. 56:555-562.
36. Hellekant G, Hladik CM, Dennys V, Simmen B, Roberts TW, Glaser D, DuBois G, Walters DE. 1993. On the sense of taste in two Malagasy primates (Microcebus murinus and Eulemur mongoz). Chem Senses. 18:307-320.
37. Hellekant G, Ninomiya Y, Danilova V. 1997. Taste in chimpanzees II: single chorda tympani fibers. Physiol Behav. 61:829-841.
38. Hellekant G, Ninomiya Y, Danilova V. 1998. Taste in chimpanzees. III: labeled-line coding in sweet taste. Physiol Behav. 65:191-200.
39. Hellekant G, Ninomiya Y, DuBois GE, Danilova V, Roberts TW. 1996. Taste in chimpanzee: I. The summated response to sweeteners and the effect of gymnemic acid. Physiol Behav. 60:469-479.
40. Hellekant G, Roberts T, Elmer D, Cragin T, Danilova V. 2010. Responses of single chorda tympani taste fibers of the calf (Bos taurus). Chem Senses. 35:383-394.
41. Hellekant G, Walters DE. 1993. An example of phylogenetic differences in sweet taste: sweetness of five high potency sweeteners in rats. In: Mathlouthi M, Kanters JA, Birch G, editors. Sweet-taste chemoreception. London: Elsevier Applied Science. p. 373-386.
42. Henrich S, Feierberg I, Wang T, Blomberg N, Wade RC. 2010. Comparative binding energy analysis for binding affinity and target selectivity prediction. Proteins. 78:135-153.
43. Hnizdo V, Tan J, Killian BJ, Gilson MK. 2008. Efficient calculation of configurational entropy from molecular simulations by combining the mutual-information expansion and nearest-neighbor methods. J Comput Chem. 29:1605-1614.
44. Inoue M, McCaughey SA, Bachmanov AA, Beauchamp GK. 2001. Wholenerve chorda tympani responses to sweeteners in C57BL/6ByJ and 129P3/J mice. Chem Senses. 26:915-923.
45. Irudayam SJ, Henchman RH. 2009. Entropic cost of protein-ligand binding and its dependence on the entropy in solution. J Phys Chem B. 113:5871-5884.
46. Jakinovich W. 1981. Stimulation of the gerbil's gustatory receptors by artificial sweeteners. Brain Res. 210:69-81.
47. Jiang P, Cui M, Ji Q, Snyder L, Liu Z, Benard L, Margolskee RF, Osman R, Max M. 2005. Molecular mechanisms of sweet receptor function. Chem Senses. 30(Suppl 1):i17-i18.
48. Jiang P, Cui M, Zhao B, Liu Z, Snyder LA, Benard LM, Osman R, Margolskee RF, Max M. 2005. Lactisole interacts with the transmembrane domains of human T1R3 to inhibit sweet taste. J Biol Chem. 280:15238-15246.
49. Jiang P, Cui M, Zhao B, Snyder LA, Benard LM, Osman R, Max M, Margolskee RF. 2005. Identification of the cyclamate interaction site within the transmembrane domain of the human sweet taste receptor subunit T1R3. J Biol Chem. 280:34296-34305.
50. Jiang P, Ji Q, Liu Z, Snyder LA, Benard LM, Margolskee RF, Max M. 2004. The cysteine-rich region of T1R3 determines responses to intensely sweet proteins. J Biol Chem. 279:45068-45075.
51. Jordt SE, Julius D. 2002. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell. 108:421-430.
52. Kare MR, Beauchamp GK. 1984. Taste, smell, and hearing. In: Swenson MJ, editor. Dukes' physiology of domestic animals. Ithaca (NY): Cornell University Press. p. 742-760.
53. Kim U, Jorgenson E, Coon H, Leppert M, Risch N, Drayna D. 2003. Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science. 299:1221-1225.
54. Kitagawa M, Kusakabe Y, Miura H, Ninomiya Y, Hino A. 2001. Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem Biophys Res Commun. 283:236-242.
55. Kunishima N, Shimada Y, Tsuji Y, Sato T, Yamamoto M, Kumasaka T, Nakanishi S, Jingami H, Morikawa K. 2000. Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature. 407:971-977.
56. Li X, Glaser D, Li W, Johnson WE, O'Brien SJ, Beauchamp GK, Brand JG. 2009. Analyses of sweet receptor gene (Tas1r2) and preference for sweet stimuli in species of Carnivora. J Hered. 100(Suppl 1): S90-S100.
57. Li X, Li W, Wang H, Cao J, Maehashi K, Huang L, Bachmanov AA, Reed DR, Legrand-Defretin V, Beauchamp GK, et al. 2005. Pseudogenization of a sweet-receptor gene accounts for cats' indifference toward sugar. PLoS Genet. 1:27-35.
58. Li X, Staszewski L, Xu H, Durick K, Zoller M, Adler E. 2002. Human receptors for sweet and umami taste. Proc Natl Acad Sci U S A. 99:4692-4696.
59. Liu T, Whitten ST, Hilser VJ. 2006. Ensemble-based signatures of energy propagation in proteins: a new view for an old phenomenon. Proteins. 62:728-738.
60. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, et al. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B. 102:3586-3616.
61. Max M, Shanker YG, Huang L, Rong M, Liu Z, Campagne F, Weinstein H, Damak S, Margolskee RF. 2001. Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat Genet. 28:58-63.
62. May LT, Christopoulos A. 2003. Allosteric modulators of G-protein-coupled receptors. Curr Opin Pharmacol. 3:551-556.
63. Mayo SL, Olafson BD, Goddard WA. 1990. Dreiding-a generic force-field for molecular simulations. J Phys Chem. 94:8897-8909.
64. Meliska CJ, Bartke A, McGlacken G, Jensen RA. 1995. Ethanol, nicotine, amphetamine, and aspartame consumption and preferences in C57BL/6 and DBA/2 mice. Pharmacol Biochem Behav. 50: 619-626.
65. Mojet J, Christ-Hazelhof E, Heidema J. 2001. Taste perception with age: generic or specific losses in threshold sensitivity to the five basic tastes? Chem Senses. 26:845-860.
66. Mojet J, Heidema J, Christ-Hazelhof E. 2003. Taste perception with age: generic or specific losses in supra-threshold intensities of five taste qualities? Chem Senses. 28:397-413.
67. Mojet J, Heidema J, Christ-Hazelhof E. 2004. Effect of concentration on taste-taste interactions in foods for elderly and young subjects. Chem Senses. 29:671-681.
68. Montmayeur JP, Liberles SD, Matsunami H, Buck LB. 2001. A candidate taste receptor gene near a sweet taste locus. Nat Neurosci. 4:492-498.
69. 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.
70. Murcia M, Morreale A, Ortiz AR. 2006. Comparative binding energy analysis considering multiple receptors: a step toward 3D-QSAR models for multiple targets. J Med Chem. 49:6241-6253.
71. Naim M, Rogatka H, Yamamoto T, Zehavi U. 1982. Taste responses to neohesperidin dihydrochalcone in rats and baboon monkeys. Physiol Behav. 28:979-986.
72. Nelson G, Chandrashekar J, Hoon MA, Feng L, Zhao G, Ryba NJP, Zuker CS. 2002. An amino acid taste receptor. Nature. 416:199-202.
73. Nelson G, Hoon MA, Chandrashekar J, Zhang Y, Ryba NJ, Zuker CS. 2001. Mammalian sweet taste receptors. Cell. 106:381-390.
74. Nie Y, Vigues S, Hobbs JR, Conn GL, Munger SD. 2005. Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli. Curr Biol. 15:1948-1952.
75. Nofre C, Tinti JM. 2000. Neotame: discovery, properties, utility. Food Chem. 69:245-257.
76. Nofre C, Tinti JM, Glaser D. 1996. Evolution of the sweetness receptor in primates. II. Gustatory responses of non-human primates to nine compounds known to be sweet in man. Chem Senses. 21:747-762.
77. Nowlis GH, Frank ME, Pfaffman C. 1980. Specificity of acquired aversions to taste qualities in hamsters and rats. J Comp Physiol Psychol. 94:932-942.
78. Pin JP, Kniazeff J, Liu J, Binet V, Goudet C, Rondard P, Prezeau L. 2005. Allosteric functioning of dimeric class C G-protein-coupled receptors. Febs J. 272:2947-2955.
79. Reed DR, Li S, Li X, Huang L, Tordoff MG, Starling-Roney R, Taniguchi K, West DB, Ohmen JD, Beauchamp GK, et al. 2004. Polymorphisms in the taste receptor gene (Tas1r3) region are associated with saccharin preference in 30 mouse strains. J Neurosci. 24:938-946.
80. Reed DR, Zhu G, Breslin PA, Duke FF, Henders AK, Campbell MJ, Montgomery GW, Medland SE, Martin NG, Wright MJ. 2010. The perception of quinine taste intensity is associated with common genetic variants in a bitter receptor cluster on chromosome 12. Hum Mol Genet. 19:4278-4285.
81. Sainz E, Korley JN, Battey JF, Sullivan SL. 2001. Identification of a novel member of the T1R family of putative taste receptors. J Neurochem. 77:896-903.
82. Sato M, Hiji Y, Ito H. 1977. Taste discrimination in the money. In: Le Magnen VIJ, Mac Leod P, editors. Olfaction and taste. London: Information Retrieval Ltd. p. 233-240.
83. Schilling A, Danilova V, Hellekant G. 2004. Behavioral study in the gray mouse lemur (Microcebus murinus) using compounds considered sweet by humans. Am J Primatol. 62:43-48.
84. Sclafani A, Abrams M. 1986. Rats show only a weak preference for the artificial sweetener aspartame. Physiol Behav. 37:253-256.
85. Servant G, Tachdjian C, Tang XQ,Werner S, Zhang F, Li X, Kamdar P, Petrovic G, Ditschun T, Java A, et al. 2010. Positive allosteric modulators of the human sweet taste receptor enhance sweet taste. Proc Natl Acad Sci U S A. 107:4746-4751.
86. Shi P, Zhang J. 2006. Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes. Mol Biol Evol. 23:292-300.
87. Springael JY, Urizar E, Costagliola S, Vassart G, Parmentier M. 2007. Allosteric properties of G protein-coupled receptor oligomers. Pharmacol Ther. 115:410-418.
88. Tamamis P, Morikis D, Floudas CA, Archontis G. 2010. Species specificity of the complement inhibitor compstatin investigated by all-atom molecular dynamics simulations. Proteins. 78:2655-2667.
89. Temussi P. 2006. The history of sweet taste: not exactly a piece of cake. J Mol Recognit. 19:188-199.
90. Temussi P. 2007. The sweet taste receptor: a single receptor with multiple sites and modes of interaction. Adv Food Nutr Res. 53:199-239.
91. Temussi PA. 2002. Why are sweet proteins sweet? Interaction of brazzein, monellin and thaumatin with the T1R2-T1R3 receptor. FEBS Lett. 526: 1-4.
92. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
93. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
94. Thomsen MW, Dalton JM, Stewart CN. 1988. Comparison of aspartame and 4-chloroaspartame taste characteristics in rats and monkeys. Chem Senses. 13:397-405.
95. Tordoff MG, Shao H, Alarcon LK, Margolskee RF, Mosinger B, Bachmanov AA, Reed DR, McCaughey SA. 2008. Involvement of T1R3 in calcium-magnesium taste. Physiol Genomics. 34:338-348.
96. Walters DE. 2002. Homology-based model of the extracellular domain of the taste receptor T1R3. Pure Appl Chem. 47:1117-1123.
97. Walters DE, Cragin T, Jin Z, Rumbley JN, Hellekant G. 2009. Design and evaluation of new analogs of the sweet protein brazzein. Chem Senses. 34:679-683.
98. Wang T,Wade RC. 2001. Comparative binding energy (COMBINE) analysis of influenza neuraminidase-inhibitor complexes. J Med Chem. 44:961-971.
99. Weihrauch MR, Diehl V. 2004. Artificial sweeteners-do they bear a carcinogenic risk? Ann Oncol. 15:1460-1465.
100. Wellendorph P, Johansen LD, Brauner-Osborne H. 2009. Molecular pharmacology of promiscuous seven transmembrane receptors sensing organic nutrients. Mol Pharmacol. 76:453-465.
101. Winnig M, Bufe B, Kratochwil N, Slack JP, Meyerhof W. 2006. A newly identified neohesperidine dihydrochalcone binding site in the human sweet taste receptor overlaps with allosteric modulator binding sites for class 3 GPCRS. Chem Senses. 31:A103-A103.
102. Winnig M, Bufe B, Meyerhof W. 2005. Valine 738 and lysine 735 in the fifth transmembrane domain of rTas1r3 mediate insensitivity towards lactisole of the rat sweet taste receptor. BMC Neurosci. 6:22.
103. 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 U S A. 101:14258-14263.
104. Zamanakos G. 2002. A fast and accurate analytical method for the computation of solvent effects in molecular simulations. Pasadena (CA): California Institute of Technology.
105. 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 U S A. 107:4752-4757.
106. Zhao G, Zhang Y, Hoon MA, Chandrashekar J, Erlenbach I, Ryba NJ, Zuker CS. 2003. The receptors for mammalian sweet and umami taste. Cell. 115:255-266.