The influence of TAS2R38 bitter taste gene polymorphisms on obesity risk in three racially diverse groups

Chaowanee Chupeerach, Pradtana Tapanee, Nattira On-Nom, Piya Temviriyanukul, Boonrat Chantong, Nicole Reeder, Grace A Adegoye, Terezie Tolar-Peterson, Chaowanee Chupeerach, Pradtana Tapanee, Nattira On-Nom, Piya Temviriyanukul, Boonrat Chantong, Nicole Reeder, Grace A Adegoye, Terezie Tolar-Peterson

Abstract

Objectives: Bitter taste perception affects food preference, eating behavior, and nutrient intake. The purpose of this study was to investigate the contribution of bitter taste gene polymorphisms to body fatness as measured by percentage of body fat.

Method: Three common single nucleotide polymorphisms (SNPs) of the TAS2R38 gene which result in amino acid changes in the protein (A49P, V262A, and I296V), were studied in three racially diverse groups: European Americans n = 313, African Americans n = 109, and Asians n = 234.

Results: The allele frequencies of the three SNPs were similar to previous studies. The rare haplotypes, AAI and AAV, were found in high prevalence in the African American subgroup (22.94%) and European American subgroup (6.07%). The PROP non taster; AVI/AVI diplotype was associated with a higher risk of obesity in European American and Asian but not African American subjects after age adjustment.

Conclusions: TAS2R38 polymorphisms could be associated with obesity development. In addition to taste perception, nutrient sensing and energy metabolism should be studied in relation to bitter taste receptors to confirm the association between genetic polymorphisms and body fatness. Genetic polymorphisms, race, gender, and environmental factors such as dietary patterns could all contribute to body fat.

Keywords: Bitter taste receptor; Body fat; Genetic polymorphism; Obesity; TAS2R38.

© the Author(s).

References

    1. Dotson CD, Babich J, Steinle NI. Genetic Predisposition and Taste Preference: Impact on Food Intake and Risk of Chronic Disease. Curr Nutr Rep. 2012;1:175–83.
    1. Sandell M, Hoppu U, Mikkilä V, Mononen N, Kähönen M, Männistö S, et al. Genetic variation in the hTAS2R38 taste receptor and food consumption among Finnish adults. Genes Nutr. 2014;9:433.
    1. Guo SW, Reed DR. The genetics of phenylthiocarbamide perception. Ann Hum Biol. 2001;28:111–42.
    1. Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, Slack JP, et al. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol. 2005;15:1–20.
    1. Drayna D. Human taste genetics. Annu Rev Genomics Hum Genet. 2005;6:217–35.
    1. Garneau NL, Nuessle TM, Sloan MM, Santorico SA, Coughlin BC, Hayes JE. Crowdsourcing taste research: genetic and phenotypic predictors of bitter taste perception as a model. Front Integr Neurosci. 2014;8:33.
    1. Campbell MC, Ranciaro A, Froment A, Hirbo J, Omar S, Bodo JM, et al. Evolution of functionally diverse alleles associated with PTC bitter taste sensitivity in Africa. Mol Biol Evol. 2012;29:1141–53.
    1. Behrens M, Gunn HC, Ramos PC, Meyerhof W, Wooding SP. Genetic, functional, and phenotypic diversity in TAS2R38-mediated bitter taste perception. Chem Senses. 2013;38:475–84.
    1. Risso DS, Mezzavilla M, Pagani L, Robino A, Morini G, Tofanelli S, et al. Global diversity in the TAS2R38 bitter taste receptor: revisiting a classic evolutionary PROPosal. Sci Rep. 2016;3:25506.
    1. Duffy VB, Davidson AC, Kidd JR, Kidd KK, Speed WC, Pakstis AJ, et al. Bitter receptor gene (TAS2R38), 6-n-propylthiouracil (PROP) bitterness and alcohol intake. Alcohol Clin Exp Res. 2004;28:1629–37.
    1. Ooi SX, Lee PL, Law HY, Say YH. Bitter receptor gene (TAS2R38) P49A genotypes and their associations with aversion to vegetables and sweet/fat foods in Malaysian subjects. Asia Pac J Clin Nutr. 2010;19:491–8.
    1. Melis M, Sollai G, Muroni P, Crnjar R, Barbarossa IT. Associations between orosensory perception of oleic acid, the common single nucleotide polymorphisms (rs1761667 and rs1527483) in the CD36 gene, and 6-n-propylthiouracil (PROP) tasting. Nutrients. 2015;20:2068–84.
    1. Donaldson LF, Bennett L, Baic S, Melichar JK. Taste and weight: is there a link? Am J Clin Nutr. 2009;90:800S–3S.
    1. Park H, Shin Y, Kwon O, Kim Y. Association of Sensory Liking for Fat with Dietary Intake and Metabolic Syndrome in Korean Adults. Nutrients. 2018;10:877.
    1. Jang HJ, Kokrashvili Z, Theodorakis MJ, Carlson OD, Kim BJ, Kim HH, et al. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. PNAS. 2007;104:15069–74.
    1. Furness JB, Rivera LR, Cho HJ, Bravo DM, Callaghan B. The gut as a sensory organ. Nat Rev Gastroenterol Hepatol. 2013;10:729–40.
    1. Janssen S, Depoortere I. Nutrient sensing in the gut: new roads to therapeutics? Trends Endocrinol Metab. 2013;24:92–100.
    1. Bartoshuk LM, Duffy VB, Green BG, Hoffman HJ, Ko CW, Lucchina LA, et al. Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching. Physiol Behav. 2004;82:109–14.
    1. Bartoshuk LM, Duffy VB, Hayes JE, Moskowitz HR, Snyder DJ. Psychophysics of sweet and fat perception in obesity: problems, solutions and new perspectives. Philos Trans R Soc Lond B Biol Sci. 2006;361:1137–48.
    1. Deshaware S, Singhal R. Genetic variation in bitter taste receptor gene TAS2R38, PROP taster status and their association with body mass index and food preferences in Indian population. Gene. 2017;627:363–8.
    1. Prescott J, Soo J, Campbell H, Roberts C. Responses of PROP taster groups to variations in sensory qualities within foods and beverages. Physiol Behav. 2004;15:459–69.
    1. Dinehart ME, Hayes JE, Bartoshuk LM, Lanier SL, Duffy VB. Bitter taste markers explain variability in vegetable sweetness, bitterness, and intake. Physiol Behav. 2006;28:304–13.
    1. Keller KL, Steinmann L, Nurse RJ, Tepper BJ. Genetic taste sensitivity to 6-n-propylthiouracil influences food preference and reported intake in preschool children. Appetite. 2002;38:3–12.
    1. Robino A, Mezzavilla M, Pirastu N, Dognini M, Tepper BJ, Gasparini P. A population-based approach to study the impact of PROP perception on food liking in populations along the Silk Road. PLoS One. 2014;9:e91716.
    1. Tepper BJ, Koelliker Y, Zhao L, Ullrich NV, Lanzara C, d'Adamo P, et al. Variation in the bitter-taste receptor gene TAS2R38, and adiposity in a genetically isolated population in Southern Italy. Obesity (Silver Spring) 2008;16:2289–95.
    1. Tepper BJ, Neilland M, Ullrich NV, Koelliker Y, Belzer LM. Greater energy intake from a buffet meal in lean, young women is associated with the 6-n-propylthiouracil (PROP) non-taster phenotype. Appetite. 2011;56:104–10.
    1. Carta G, Melis M, Pintus S, Pintus P, Piras CA, Muredda L, et al. Participants with normal weight or with obesity show different relationships of 6-n-propylthiouracil (PROP) taster status with bmi and plasma endocannabinoids. Sci Rep. 2017;7:1361.
    1. Melis M, Sollai G, Muroni P, Crnjar R, Tomassini Barbarossa I. Associations between orosensory perception of oleic acid, the common single nucleotide polymorphisms (rs1761667 and rs1527483) in the CD36 gene, and 6-n-propylthiouracil (PROP) tasting. Nutrients. 2015;7:2068–84.
    1. Tepper BJ, Banni S, Melis M, Crnjar R, Tomassini Barbarossa I. Genetic sensitivity to the bitter taste of 6-n-propylthiouracil (PROP) and its association with physiological mechanisms controlling body mass index (BMI) Nutrients. 2014;6:3363–81.
    1. Tomassini Barbarossa I, Carta G, Murru E, Melis M, Zonza A, Vacca C, et al. Taste sensitivity to 6-n-propylthiouracil is associated with endocannabinoid plasma levels in normal-weight individuals. Nutrition. 2013;29:531–6.
    1. Tepper BJ, Williams TZ, Burgess JR, Antalis CJ, Mattes RD. Genetic variation in bitter taste and plasma markers of anti-oxidant status in college women. Int J Food Sci Nutr. 2009;60:35–45.
    1. Basson MD, Bartoshuk LM, Dichello SZ, Panzini L, Weiffenbach JM, Duffy VB. Association between 6-n-propylthiouracil (PROP) bitterness and colonic neoplasms. Dig Dis Sci. 2005;50(3):483–9.
    1. Risso D, Morini G, Pagani L, Quagliariello A, Giuliani C, De Fanti S, et al. Genetic signature of differential sensitivity to stevioside in the Italian population. Genes Nutr. 2014;9:401.
    1. Adappa ND, Farquhar D, Palmer JN, Kennedy DW, Doghramji L, Morris SA, et al. TAS2R38 genotype predicts surgical outcome in nonpolypoid chronic rhinosinus. International forum of allergy & rhinology. 2016
    1. Adappa ND, Zhang Z, Palmer JN, Kennedy DW, Doghramji L, Lysenko A, et al. The bitter taste receptor T2R38 is an independent risk factor for chronic rhinosinusitis requiring sinus surgery. Int Forum Allergy Rhinol. 2014;4:3–7.
    1. Lee RJ, Cohen NA. Role of the bitter taste receptor T2R38 in upper respiratory infection and chronic rhinosinusitis. Curr Opin Allergy Clin Immunol. 2015;15:14–20.
    1. Melis M, Grzeschuchna L, Sollai G, Hummel T, Tomassini Barbarossa I. Taste disorders are partly genetically determined: Role of the TAS2R38 gene, a pilot study. Laryngoscope. 2019;129:E307–12.
    1. Melis M, Errigo A, Crnjar R, Pes GM, Tomassini Barbarossa I. TAS2R38 bitter taste receptor and attainment of exceptional longevity. Sci Rep. 2019;9:18047.
    1. Brewer WJ, Lin A, Moberg PJ, Smutzer G, Nelson B, Yung AR, et al. Phenylthiocarbamide (PTC) perception in ultrahigh risk for psychosis participants who develop schizophrenia: testing the evidence for an endophenotypic marker. Psychiatr Res. 2012;199:8–11.
    1. Cossu G, Melis M, Sarchioto M, Melis M, Melis M, Morelli M, Tomassini Barbarossa I. 6-n-propylthiouracil taste disruption and TAS2R38 nontasting form in Parkinson's disease. Mov Disord. 2018;33:1331–9.
    1. Moberg Paul J, Colleen McGue, Stephen J, Kanes, David R, et al. Phenylthiocarbamide (PTC) perception in patients with schizophrenia and first-degree family members: relationship to clinical symptomatology and psychophysical olfactory performance. Schizophr Res. 2007;90:221–8.
    1. Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y. Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr. 2000;72:694–701.
    1. Rousset F. genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecul Ecol Res. 2008;8:103e106.
    1. Choi JH, Lee J, Choi IJ, Kim YW, Ryu KW, Kim J. Genetic Variation in the TAS2R38 Bitter Taste Receptor and Gastric Cancer Risk in Koreans. Sci Rep. 2016;1:26904.
    1. Yamaki M, Saito H, Isono K, Goto T, Shirakawa H, Shoji N, Satoh-Kuriwada S, Sasano T, Okada R, Kudoh K, Motoi F, Unno M, Komai M. Genotyping Analysis of Bitter-Taste Receptor Genes TAS2R38 and TAS2R46 in Japanese Patients with Gastrointestinal Cancers. J Nutr Sci Vitaminol (Tokyo) 2017;63:148–54.
    1. Calò C, Padiglia A, Zonza A, Corrias L, Contu P, Tepper BJ, et al. Polymorphisms in TAS2R38 and the taste bud trophic factor, gustin gene co-operate in modulating PROP taste phenotype. Physiol Behav. 2011;24:1065–71.
    1. Goldstein GL, Daun H, Tepper BJ. Adiposity in middle-aged women is associated with genetic taste blindness to 6-n-propylthiouracil. Obes Res. 2005;13:1017–23.
    1. Tepper BJ, Nurse RJ. Fat perception is related to PROP taster status. Physiol Behav. 1997;61:949–54.
    1. Shafaie Y, Hoffman DJ, Tepper BJ. Consumption of a high-fat soup preload leads to differences in short-term energy and fat intake between PROP non-taster and super-taster women. Appetite. 2015;89:196–202.
    1. Keller M, Liu X, Wohland T, Rohde K, Gast MT, Stumvoll M, Kovacs P, Tönjes A, Böttcher Y. TAS2R38 and its influence on smoking behavior and glucose homeostasis in the German Sorbs. PLoS One. 2013;8:e80512.
    1. Overberg J, Hummel T, Krude H, Wiegand S. Differences in taste sensitivity between obese and non-obese children and adolescents. Archiv Dise Childhood. 2012;97:1048–52.
    1. Deurenberg P, Deurenberg M, Yap M, Wang J, Lin FP, Schmidt G. The impact of body build on the relationship between body mass index and percent body fat. Int J Obes Relat Metab Disord. 1999;23:537–42.
    1. Kim UK, Jorgenson E, Coon H, Leppert M, Risch N, Drayna D. Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science. 2003;299:1221–4.
    1. Douglas JE, Lin C, Mansfield CJ, Arayata CJ, Cowart BJ, Spielman AI, et al. Tissue-Dependent Expression of Bitter Receptor TAS2R38 mRNA. Chem Senses. 2019;44:33–40.
    1. Janssen S, Laermans J, Verhulst PJ, Thijs T, Tack J, Depoortere I. Bitter taste receptors and α-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. PNAS. 2012;108:2094–9.
    1. Latorre R, Huynh J, Mazzoni M, Gupta A, Bonora E, Clavenzani P, et al. Expression of the Bitter Taste Receptor, T2R38, in Enteroendocrine Cells of the Colonic Mucosa of Overweight/Obese vs. Lean Subjects. PLoS One. 2016;11:e0147468.
    1. Abrol R, Tan J, Hui H, Goddard WA, III, Pandol SJ. Structural Basis for a Bitter Taste Receptor Activation and its Potential Role in Targeting Diabetes. Func Food Health Dise. 2015;5:117–25.
    1. Wu SV, Rozengurt N, Yang M, Young SH, Sinnett-Smith J, Rozengurt E. Expression of bitter taste receptors of the T2R family in the gastrointestinal tract and enteroendocrine STC-1 cells. Proc Natl Acad Sci USA. 2002;99:2392–7.
    1. Padiglia A, Zonza A, Atzori E, Chillotti C, Calo MC, Tepper BJ, et al. Sensitivity to 6-npropylthiouracil (PROP) is associated with gustin (CA6) gene polymorphism, salivary zinc and BMI in humans. Am J Clin Nutr. 2010;92:539–45.
    1. Encyclopedic Reference of Genomics and Proteomics in Molecular Medicine. Berlin, Heidelberg: Springer; 2005. Population Stratification.

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