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The Effect of Tas1r3 Gene Polymorphism on Preference and Consumption of Sucrose and Low-Calorie Sweeteners in Interstrain Hybrid Mice of the First Filial Generation

  • Comparative and Ontogenic Physiology
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Abstract

Inter- and intra-species differences in consumption of sweet tastants formed during the evolution of vertebrates are thought to be due to polymorphism of the Tas1r3 gene encoding T1R3, a sweet taste receptor subunit. The aim of the study was to assess the effect of Tas1r3 polymorphism on nutritional behavior of laboratory mice using the first filial generation (F1) hybrids produced by crossing inbred strains with different sensitivity to sweet: 129P3/J males (129, carriers of a recessive SacD sweet taste receptor allele) and C57BL/6 females (B6, dominant SacB allele) or females of the Tas1r3 gene knockout strain, C57BL/6-Tas1r3KO (B6-Tas1r3KO). SacD/B and SacD/0 hybrids, sharing identical background genotypes, differed only by sets of Sac alleles. In a briefaccess test (BAT) or a 48-h two-bottle free choice test, the presence of the dominant SacD allele in SacD/B hybrids determined increased preference for low sucrose concentrations (1–4%) and higher concentrations of nonmetabolized sweeteners (saccharin Na, sucralose, acesulfame K). A comparison between the 129 parental strain and SacD/0 hybrids or between the B6 parental strain and hybrids from crossing B6 × B6-Tas1r3KO revealed no influence of hemizygosity of SacD or SacB on preference for sweeteners in BAT. A small decrease in sucrose and saccharin preference associated with the lack of the SacB allele was observed during long-term exposure to solutions with low concentrations of these substances. The data obtained indicate the relevance of studying the Tas1r3 polymorphism effects on preference and consumption of sweet tastants using F1 interstrain hybrids and BAT.

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References

  1. Bachmanov, A.A., Bosak, N.P., Lin, C., Matsumoto, I., Ohmoto, M., Reed, D.R., and Nelson, T.M., Genetics of taste receptors, Curr. Pharm. Des., 2014, vol. 20, no. 16, pp. 2669–2683.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J., and Zuker, C.S., The receptors for mammalian sweet and umami taste, Cell, 2003, vol. 115, no. 3, pp. 255–266.

    Article  PubMed  CAS  Google Scholar 

  3. Shi, P. and Zhang, J., Contrasting modes of evolution between vertebrate sweet/umami receptor genes and bitter receptor genes, Mol. Biol. Evol., 2006, vol. 23, no. 2, pp. 292–300.

    Article  PubMed  CAS  Google Scholar 

  4. Bachmanov, A.A., Bosak, N.P., Floriano, W.B., Inoue, M., Li, X., Lin, C., Murovets, V.O., Reed, D.R., Zolotarev, V.A., and Beauchamp, G.K., Genetics of sweet taste preferences, Flavour. Fragr. J., 2011, vol. 26, no. 4, pp. 286–294.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Kim, U.K., Wooding, S., Riaz, N., Jorde, L.B., and Drayna, D., Variation in the human TAS1R taste receptor genes, Chem. Senses, 2006, vol. 31, p.599.

    Article  PubMed  CAS  Google Scholar 

  6. Liu, S. and Manson, J.E., Dietary carbohydrates, physical inactivity, obesity, and the “metabolic syndrome” as predictors of coronary heart disease, Curr. Opin. Lipidol., 2001, vol. 12, no. 4, pp. 395–404.

    Article  PubMed  CAS  Google Scholar 

  7. Fuller, J.L., Single-locus control of saccharin preference in mice, J. Hered., 1974, vol. 65, no. 1, pp. 33–36.

    Article  PubMed  CAS  Google Scholar 

  8. Bachmanov, A.A., Li, X., Reed, D.R., Ohmen, J.D., Li, S., Chen, Z., Tordoff, M.G., de Jong, P.J., Wu, C., West, D.B., Chatterjee, A., Ross, D.A., and Beauchamp, G.K., Positional cloning of the mouse saccharin preference (Sac) locus, Chem. Senses, 2001, vol. 26, no. 7, pp. 925–933.

    Article  PubMed  CAS  Google Scholar 

  9. Nelson, G., Hoon, M.A., Chandrashekar, J., Zhang, Y., Ryba, N.J., and Zuker, C.S., Mammalian sweet taste receptors, Cell, 2001, vol. 106, no. 3, pp. 381–390.

    Article  PubMed  CAS  Google Scholar 

  10. Inoue, M., Glendinning, J.I., Theodorides, M.L., Harkness, S., Li, X., Bosak, N., Beauchamp, G.K, and Bachmanov, A.A., Allelic variation of the Tas1r3 taste receptor gene selectively affects taste responses to sweeteners: evidence from 129.B6-Tas1r3 congenic mice, Physiol. Genomics, 2007, vol. 32, no. 1, pp. 82–94.

    Article  PubMed  CAS  Google Scholar 

  11. Reed, D.R., Li, S., Li, X., Huang, L., Tordoff, M.G., Starling-Roney, R., Taniguchi, K., West, D.B., Ohmen, J.D., Beauchamp, G.K., and Bachmanov, A.A., Polymorphisms in the taste receptor gene (Tas1r3) region are associated with saccharin preference in 30 mouse strains, J. Neurosci., 2004, vol. 24, no. 4, pp. 938–946.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Nie, Y., Vigues, S., Hobbs, J.R., Conn, G.L., and Munger, S.D., Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli, Curr. Biol., 2005, vol. 15, no. 21, pp. 1948–1952.

    Article  PubMed  CAS  Google Scholar 

  13. Fushan, A.A., Simons, C.T., Slack, J.P., Manichaikul, A., and Drayna, D., Allelic polymorphism within the TAS1R3 promoter is associated with human taste sensitivity to sucrose, Curr. Biol., 2009, vol. 19, no. 15, pp. 1288–1293.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Eny, K.M., Wolever, T.M., Corey, P.N., and El-Sohemy, A., Genetic variation in TAS1R2 (Ile191Val) is associated with consumption of sugars in overweight and obese individuals in 2 distinct populations, Am. J. Clin. Nutr., 2010, vol. 92, no. 6, pp. 1501–1510.

    Article  PubMed  CAS  Google Scholar 

  15. Dias, A.G., Eny, K.M., Cockburn, M., Chiu, W., Nielsen, D.E., Duizer, L., and El-Sohemy, A., Variation in the TAS1R2 gene, sweet taste perception and intake of sugars, J. Nutrigen. Nutrigenomics, 2015, vol. 8, no. 2, pp. 81–90.

    Article  CAS  Google Scholar 

  16. Robino, A., Bevilacqua, L., Pirastu, N., Situlin, R., Di Lenarda, R., Gasparini, P., and Navarra, C.O., Polymorphisms in sweet taste genes (TAS1R2 and GLUT2), sweet liking, and dental caries prevalence in an adult Italian population, Genes Nutr., 2015, vol. 10, no. 5, Article 37. doi: 10.1007/S12263-015-0448-9

    Google Scholar 

  17. Fushan, A.A., Simons, C.T., Slack, J.P., and Drayna, D., Association between common variation in genes encoding sweet taste signaling components and human sucrose perception, Chem. Senses, 2010, vol. 35, no. 7, pp. 579–592.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Keskitalo, K., Tuorila, H., Spector, T.D., Cherkas, L.F., Knaapila, A., Kaprio, J., Silventoinen, K., and Perola, M., The Three-factor eating questionnaire, body mass index, and responses to sweet and salty fatty foods: a twin study of genetic and environmental associations, Am. J. Clin. Nutr., 2008, vol. 88, no. 2, pp. 263–271.

    Article  PubMed  CAS  Google Scholar 

  19. Shigemura, N., Yasumatsu, K., Yoshida, R., Sako, N., Katsukawa, H., Nakashima, K., Imoto, T., and Ninomiya, Y., The role of the dpa locus in mice, Chem. Senses, 2005, vol. 30, Suppl. no. 1, pp. 84–85.

    Article  CAS  Google Scholar 

  20. Yee, K.K., Sukumaran, S.K., Kotha, R., Gilbertson, T.A., and Margolskee, R.F., Glucose transporters and ATP-gated K+ (KATP) metabolic sensors are present in type 1 taste receptor 3 (T1r3)-expressing taste cells, Proc. Natl. Acad. Sci. USA, 2011, vol. 108, no. 13, pp. 5431–5436.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Yoshida, R., Noguchi, K., Shigemura, N., Jyotaki, M., Takahashi, I., Margolskee, R.F., and Ninomiya, Y., Leptin suppresses mouse taste cell responses to sweet compounds, Diabetes, 2015, vol. 64, pp. 3751–3762.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Calvo, S.S. and Egan, J.M., The endocrinology of taste receptors, Nat. Rev. Endocrinol., 2015, vol. 11, no. 4, pp. 213–227.

    Article  PubMed  CAS  Google Scholar 

  23. Murovets, V.O., Bachmanov, A.A., Travnikov, S.V., Churikova, A.A., and Zolotarev, V.A., The involvement of the T1R3 receptor protein in the control of glucose metabolism in mice at different levels of Glycemia, J. Evol. Biochem. Physiol., 2014, vol. 50, no. 4, pp. 334–344. doi: 10.1134/S0022093014040061

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Murovets, V.O., Bachmanov, A.A., and Zolotarev, V.A., Impaired glucose metabolism in mice lacking the Tas1r3 taste receptor gene, PLoS ONE, 2015, vol. 10, no. 6. e0130997

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Murovets, V.O., Sozontov, E.A., Andreeva, Yu.V., Khropycheva, R.P., and Zolotarev, V.A., Influence of T1R3 receptor protein on gluconeogenesis and fat metabolism in mice, Ross. Fiziol. Zh., 2016, vol. 102, no. 6, pp. 668–679.

    CAS  Google Scholar 

  26. Bachmanov, A.A., Reed, D.R., Ninomiya, Y., Inoue, M., Tordoff, M.G., Price, R.A., and Beauchamp, G.K., Sucrose consumption in mice: major influence of two genetic loci affecting peripheral sensory responses, Mamm. Genome, 1997, vol. 8, no. 8, pp. 545–548.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Inoue, M., Reed, D.R., Li, X., Tordoff, M.G., Beauchamp, G.K., and Bachmanov, A.A., Allelic variation of the Tas1r3 taste receptor gene selectively affects behavioral and neural taste responses to sweeteners in the F2 hybrids between C57BL/6ByJ and 129P3/J mice, J. Neurosci., 2004, vol. 24, no. 9, pp. 2296–2303.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Bachmanov, A.A., Tordoff, M.G., and Beauchamp, G.K., Sweetener preference of C57BL/6ByJ and 129P3/J mice, Chem. Senses, 2001, vol. 26, no. 7, pp. 905–913.

    Article  PubMed  CAS  Google Scholar 

  29. Damak, S., Rong, M., Yasumatsu, K., Kokrashvili, Z., Varadarajan, V., Zou, S., Jiang, P., Ninomiya, Y., and Margolskee, R.F., Detection of sweet and umami taste in the absence of taste receptor T1r3, Science, 2003, vol. 301, no. 5634, pp. 850–853.

    Article  PubMed  CAS  Google Scholar 

  30. Glendinning, J.I., Gresack, J., and Spector, A.C., A high-throughoutput screening procedure for identifying mice with aberrant taste and oromotor function, Chem. Senses, 2002, vol. 27, no. 5, pp. 461–474.

    Article  PubMed  Google Scholar 

  31. Spector, A.C., Psychophysical evaluation of taste function in non-human mammals, Handbook of Olfaction and Gustation, Doty, R.L., Ed., New York, 2003, pp. 869–879.

    Google Scholar 

  32. Glendinning, J.I., Chyou, S., Lin, I., Onishi, M., Patel, P., and Zheng, K.H., Initial licking responses of mice to sweeteners: effects of tas1r3 polymorphisms, Chem. Senses, 2005, vol. 30, no. 7, pp. 601–614.

    Article  PubMed  CAS  Google Scholar 

  33. Glendinning, J.I., Stano, S., Holter, M., Azenkot, T., Goldman, O., Margolskee, R.F., Vasselli, J.R., and Sclafani, A., Sugar-induced cephalicphase insulin release is mediated by a T1r2+T1r3-independent taste transduction pathway in mice, Am. J. Physiol. Regul. Integr. Comp. Physiol., 2015, vol. 309, no. 5, pp. 552–560.

    Article  CAS  Google Scholar 

  34. Sclafani, A., Gut-brain nutrient signaling. Appetition vs. satiation, Appetite, 2013, vol. 71, pp. 454–458.

    Article  PubMed  CAS  Google Scholar 

  35. Frank, G.K.W., Oberndorfer, T.A., Simmons, A.N., Paulus, M.P., Fudge, J.L., Yang, T.T., and Kayeb, W.H., Sucrose activates human taste pathways differently from artificial sweetener, NeuroImage, 2008, vol. 39, no. 4, pp. 1559–1569.

    Article  PubMed  Google Scholar 

  36. Huang, N., Lee, I., Marcotte, E.M., and Hurles, M.E., Characterizing and predicting haploinsufficiency in the human genome, PLoS Genet., 2010, vol. 6, no. 10. e1001154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Boughter, J.D., Jr., St.-John, S.J., Noel, D.T., Ndubuizu, O., and Smith, D.V., A brief-access test for bitter taste in mice, Chem. Senses, 2002, vol. 27, no. 2, pp. 133–142.

    Article  PubMed  Google Scholar 

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Correspondence to V. O. Murovets.

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Original Russian Text © V.O. Murovets, E.A. Lukina, V.A. Zolotarev, 2018, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2018, Vol. 54, No. 3, pp. 194–204.

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Murovets, V.O., Lukina, E.A. & Zolotarev, V.A. The Effect of Tas1r3 Gene Polymorphism on Preference and Consumption of Sucrose and Low-Calorie Sweeteners in Interstrain Hybrid Mice of the First Filial Generation. J Evol Biochem Phys 54, 221–233 (2018). https://doi.org/10.1134/S0022093018030079

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