Molecular mechanisms for sweet-suppressing effect of gymnemic acids

Journal of Biological Chemistry

Volumn 289, Issue 37, 2014, Pages 25711-25720

  Sanematsu, Keisuke ^a   Kusakabe, Yuko ^b   Shigemura, Noriatsu ^a   Hirokawa, Takatsugu ^c   Nakamura, Seiji ^a   Imoto, Toshiaki ^d   Ninomiya, Yuzo ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^c NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^d TOTTORI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; MAMMALS;

AMINO ACID RESIDUES; DIRECTED MUTAGENESIS; MIXED-SPECIES PAIRINGS; MOLECULAR MECHANISM; REDUCED SENSITIVITY; SUPPRESSING EFFECTS; TRANS-MEMBRANE DOMAINS; TRITERPENE GLYCOSIDES;

ACTIVATION ANALYSIS;

GAMMA CYCLODEXTRIN; GLUCURONIC ACID; GYMNEMIC ACID; MEMBRANE PROTEIN; RECEPTOR SUBUNIT; BENZENE DERIVATIVE; G PROTEIN COUPLED RECEPTOR; LACTISOLE; SAPONIN; SWEETENING AGENT; TASTE RECEPTORS, TYPE 1; TRITERPENE;

ARTICLE; CHEMICAL STRUCTURE; CHIMERA; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; SENSITIVITY ANALYSIS; SITE DIRECTED MUTAGENESIS; SWEETNESS; TASTE ACUITY; TASTE BUD; TASTE TYPE 1 RECEPTOR 2; TASTE TYPE 1 RECEPTOR 3; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; TASTE;

AMINO ACID SEQUENCE; ANIMALS; BENZENE DERIVATIVES; BINDING SITES; HEK293 CELLS; HUMANS; MICE; RECEPTORS, G-PROTEIN-COUPLED; SAPONINS; SWEETENING AGENTS; TASTE; TASTE BUDS; TRITERPENES;

EID: 84907168726     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.560409     Document Type: Article

References (52)

1. Li, X., Inoue, M., Reed, D. R., Huque, T., Puchalski, R. B., Tordoff, M. G., Ninomiya, Y., Beauchamp, G. K., and Bachmanov, A. A. (2001) Highresolution genetic mapping of the saccharin preference locus (Sac) and the putative sweet taste receptor (T1R1) gene (Gpr70) to mouse distal chromosome 4. Mamm. Genome 12, 13-16
2. Nelson, G., Hoon, M. A., Chandrashekar, J., Zhang, Y., Ryba, N. J., and Zuker, C. S. (2001) Mammalian sweet taste receptors. Cell 106, 381-390
3. Hoon, M. A., Adler, E., Lindemeier, J., Battey, J. F., Ryba, N. J., and Zuker, C. S. (1999) Putative mammalian taste receptors: a class of taste-specific GPCRs with distinct topographic selectivity. Cell 96, 541-551
4. Max, M., Shanker, Y. G., Huang, L., Rong, M., Liu, Z., Campagne, F., Weinstein, H., Damak, S., and Margolskee, R. F. (2001) Tas1r3, encoding a new candidate taste receptor, is allelic to the sweet responsiveness locus Sac. Nat. Genet. 28, 58-63
5. Sainz, E., Korley, J. N., Battey, J. F., and Sullivan, S. L. (2001) Identification of a novel member of the T1R family of putative taste receptors. J. Neurochem. 77, 896-903
6. Montmayeur, J. P., Liberles, S. D., Matsunami, H., and Buck, L. B. (2001) A candidate taste receptor gene near a sweet taste locus. Nat. Neurosci. 4, 492-498
7. Kitagawa, M., Kusakabe, Y., Miura, H., Ninomiya, Y., and Hino, A. (2001) Molecular genetic identification of a candidate receptor gene for sweet taste. Biochem. Biophys. Res. Commun. 283, 236-242
8. Pin, J. P., Galvez, T., and Prézeau, L. (2003) Evolution, structure, and activation mechanism of family 3/C G-protein-coupled receptors. Pharmacol. Ther. 98, 325-354
9. Kunishima, N., Shimada, Y., Tsuji, Y., Sato, T., Yamamoto, M., Kumasaka, T., Nakanishi, S., Jingami, H., and Morikawa, K. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977
10. Muto, T., Tsuchiya, D., Morikawa, K., and Jingami, H. (2007) Structures of the extracellular regions of the group II/III metabotropic glutamate receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 3759-3764
11. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G proteincoupled receptor. Science 289, 739-745
12. Xu, H., Staszewski, L., Tang, H., Adler, E., Zoller, M., and Li, X. (2004) Different functional roles of T1R subunits in the heteromeric taste receptors. Proc. Natl. Acad. Sci. U.S.A. 101, 14258-14263
13. Masuda, K., Koizumi, A., Nakajima, K., Tanaka, T., Abe, K., Misaka, T., and Ishiguro, M. (2012) Characterization of the modes of binding between human sweet taste receptor and low-molecular-weight sweet compounds. PLoS ONE 7, e35380
14. Koizumi, A., Nakajima, K., Asakura, T., Morita, Y., Ito, K., Shmizu-Ibuka, A., Misaka, T., and Abe, K. (2007) Taste-modifying sweet protein, neoculin, is received at human T1R3 amino terminal domain. Biochem. Biophys. Res. Commun. 358, 585-589
15. Jiang, P., Ji, Q., Liu, Z., Snyder, L. A., Benard, L. M., Margolskee, R. F., and Max, M. (2004) The cysteine-rich region of T1R3 determines responses to intensely sweet proteins. J. Biol. Chem. 279, 45068-45075
16. Assadi-Porter, F. M., Maillet, E. L., Radek, J. T., Quijada, J., Markley, J. L., and Max, M. (2010) Key amino acid residues involved in multi-point binding interactions between brazzein, a sweet protein, and the T1R2-T1R3 human sweet receptor. J. Mol. Biol. 398, 584-599
17. Jiang, P., Cui, M., Zhao, B., Snyder, L. A., Benard, L. M., Osman, R., Max, M., and Margolskee, R. F. (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
18. Jiang, P., Cui, M., Zhao, B., Liu, Z., Snyder, L. A., Benard, L. M., Osman, R., Margolskee, R. F., and Max, M. (2005) Lactisole interacts with the transmembrane domains of human T1R3 to inhibit sweet taste. J. Biol. Chem. 280, 15238-15246
19. Winnig, M., Bufe, B., Kratochwil, N. A., Slack, J. P., and Meyerhof, W. (2007) The binding site for neohesperidin dihydrochalcone at the human sweet taste receptor. BMC Struct. Biol. 7, 66
20. Suttisri, R., Lee, I. S., and Kinghorn, A. D. (1995) Plant-derived triterpenoid sweetness inhibitors. J. Ethnopharmacol. 47, 9-26
21. Warren, R. M., and Pfaffmann, C. (1959) Suppression of sweet sensitivity by potassium gymnemate. J. Appl. Physiol. 14, 40-42
22. Kurihara, Y. (1969) Antisweet activity of gymnemic acid A1 and its derivatives. Life Sci. 8, 537-543
23. Diamant, H., Oakley, B., Stroem, L., Wells, C., and Zotterman, Y. (1965) A comparison of neural and psychophysical responses to taste stimuli in man. Acta Physiol. Scand. 64, 67-74
24. Hellekant, G., and Gopal, V. (1976) On the effects of gymnemic acid in the hamster and rat. Acta Physiol. Scand. 98, 136-142
25. Hellekant, G., af Segerstad, C. H., Roberts, T., van der Wel, H., Brouwer, J. N., Glaser, D., Haynes, R., and Eichberg, J. W. (1985) Effects of gymnemic acid on the chorda tympani proper nerve responses to sweet, sour, salty and bitter taste stimuli in the chimpanzee. Acta Physiol. Scand. 124, 399-408
26. Hellekant, G., Ninomiya, Y., DuBois, G. E., Danilova, V., and Roberts, T. W. (1996) Taste in chimpanzee: I. The summated response to sweeteners and the effect of gymnemic acid. Physiol. Behav. 60, 469-479
27. Hellekant, G., Ninomiya, Y., and Danilova, V. (1998) Taste in chimpanzees. III: labeled-line coding in sweet taste. Physiol. Behav. 65, 191-200
28. Nagaoka, T., Hane, H., Yamashita, H., and Kensho, I. (1990) Taste improvement of extracts from the leaves of Gymnema sylvestre. Seitou Gijutsu Kenkyukai-Shi 38, 61-70
29. Imoto, T. (1990) Sugar discrimination and plant-originated glycosides, gymnemic acids. Seibutsu Butsuri 30, 146-150
30. Izutani, Y., Kanaori, K., Imoto, T., and Oda, M. (2005) Interaction of gymnemic acid with cyclodextrins analyzed by isothermal titration calorimetry, NMR and dynamic light scattering. FEBS J. 272, 6154-6160
31. Nakamura, Y., Tsumura, Y., Tonogai, Y., and Shibata, T. (1999) Fecal steroid excretion is increased in rats by oral administration of gymnemic acids contained in Gymnema sylvestre leaves. J. Nutr. 129, 1214-1222
32. Porchezhian, E., and Dobriyal, R. M. (2003) An overview on the advances of Gymnema sylvestre: chemistry, pharmacology and patents. Pharmazie 58, 5-12
33. Kanetkar, P., Singhal, R., and Kamat, M. (2007) Gymnema sylvestre: a memoir. J. Clin. Biochem. Nutr. 41, 77-81
34. Izutani, Y., Murai, T., Imoto, T., Ohnishi, M., Oda, M., and Ishijima, S. (2005) Gymnemic acids inhibit rabbit glyceraldehyde-3-phosphate dehydrogenase and induce a smearing of its electrophoretic band and dephosphorylation. FEBS Lett. 579, 4333-4336
35. Ballesteros, J. A., and Weinstein, H. (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G-protein-coupled receptors. Methods Neurosci. 25, 366-428
36. Shigemura, N., Shirosaki, S., Sanematsu, K., Yoshida, R., and Ninomiya, Y. (2009) Genetic and molecular basis of individual differences in human umami taste perception. PLoS ONE 4, e6717
37. Li, X., Staszewski, L., Xu, H., Durick, K., Zoller, M., and Adler, E. (2002) Human receptors for sweet and umami taste. Proc. Natl. Acad. Sci. U.S.A. 99, 4692-4696
38. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K., and Pease, L. R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77, 61-68
39. Zhang, F., Klebansky, B., Fine, R. M., Liu, H., Xu, H., Servant, G., Zoller, M., Tachdjian, C., and Li, X. (2010) Molecular mechanism of the sweet taste enhancers. Proc. Natl. Acad. Sci. U.S.A. 107, 4752-4757
40. Sánchez, R., and Sali, A. (2000) Comparative protein structure modeling. Introduction and practical examples with modeller. Methods Mol. Biol. 143, 97-129
41. Wu, H., Wang, C., Gregory, K. J., Han, G. W., Cho, H. P., Xia, Y., Niswender, C. M., Katritch, V., Meiler, J., Cherezov, V., Conn, P. J., and Stevens, R. C. (2014) Structure of a class C GPCR metabotropic glutamate receptor 1 bound to an allosteric modulator. Science 344, 58-64
42. Irwin, J. J., and Shoichet, B. K. (2005) ZINC-a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 45, 177-182
43. Suenaga, M. (2005) New computational chemistry environment for PC GAMESS. J. Comput. Chem. 4, 25-32
44. Suenaga, M. (2008) Development of GUI for GAMESS/FMO calculation. J. Comput. Chem. 7, 33-53
45. Schmidt, M. W., Baldridge, K. K., Boatz, J. A., Elbert, S. T., Gordon, M. S., Jensen, J. H., Koseki, S., Matsunaga, N., Nguyen, K. A., Su, S. J., Windus, T. L., Dupuis, M., and Montgomery, J. A. (1993) General atomic and molecular electronic-structure system. J. Comput. Chem. 14, 1347-1363
46. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J. Comput. Chem. 19, 1639-1662
47. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
48. Kurihara, Y. (1992) Characteristics of antisweet substances, sweet proteins, and sweetness-inducing proteins. Crit. Rev. Food Sci. Nutr. 32, 231-252
49. Li, S., and Purdy, W. C. (1992) Cyclodextrins and their applications in analytical chemistry. Chem. Rev. 92, 1457-1470
50. Inoue, Y., and Miyata, Y. (1981) Formation and molecular-dynamics of cycloamylose inclusion complexes with phenylalanine. Bull. Chem. Soc. 54, 809-816
51. Inoue, Y., Okuda, T., and Miyata, Y. (1981) Side-chain conformational changes of some amino-acids and dipeptides having aromatic side-chains induced by complexation with cycloamyloses. J. Am. Chem. Soc. 103, 7393-7394
52. Nie, Y., Vigues, S., Hobbs, J. R., Conn, G. L., and Munger, S. D. (2005) Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli. Curr. Biol. 15, 1948-1952