Receptor Polymorphism and Genomic Structure Interact to Shape Bitter Taste Perception

PLoS Genetics

Volumn 11, Issue 9, 2015, Pages

  Roudnitzky, Natacha ^a   Behrens, Maik ^a   Engel, Anika ^a   Kohl, Susann ^a   Thalmann, Sophie ^a   Hübner, Sandra ^a   Lossow, Kristina ^a   Wooding, Stephen P ^b   Meyerhof, Wolfgang ^a  

^a GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABSYNTHIN; AMAROGENTIN; CASCARILLIN; NATURAL PRODUCT; QUASSINOID; QUININE; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; GROSHEIMIN; IRIDOID; PHENYLTHIOUREA; QUASSIN; QUASSINOID DERIVATIVE; SESQUITERPENE; TAS2R1 PROTEIN, HUMAN;

ADULT; ARTICLE; BITTER TASTE; FEMALE; GENE; GENE LOCUS; GENE SEQUENCE; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENOTYPE; HAPLOTYPE; HUMAN; MALE; PHENOTYPIC VARIATION; TAS2R GENE; TASTE ACUITY; ALLELE; ANIMAL; CAUCASIAN; CHEMISTRY; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; SINGLE NUCLEOTIDE POLYMORPHISM; TASTE; TASTE BUD;

ALLELES; ANIMALS; EUROPEAN CONTINENTAL ANCESTRY GROUP; GENETIC ASSOCIATION STUDIES; GENOTYPE; HAPLOTYPES; HUMANS; IRIDOIDS; PHENYLTHIOUREA; POLYMORPHISM, SINGLE NUCLEOTIDE; QUASSINS; QUININE; RECEPTORS, G-PROTEIN-COUPLED; SESQUITERPENES; SESQUITERPENES, GUAIANE; TASTE BUDS; TASTE PERCEPTION;

EID: 84943564180     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005530     Document Type: Article

References (79)

1. Berridge KC, Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev. 2000; 24(2): 173–98. 10714382
2. Pfaffmann C, Norgren R, Sensory affect and motivation. Ann N Y Acad Sci. 1977; 290(1): 18–34.
3. Rosenstein D, Oster H, Differential facial responses to four basic tastes in newborns. Child Dev. 1988; 59: 1555–68. 3208567
4. Schwartz C, Issanchou S, Nicklaus S, Developmental changes in the acceptance of the five basic tastes in the first year of life. Br J Nutr. 2009; 102(9): 1375–85. doi: 10.1017/S0007114509990286 19505346
5. Steiner JE, Weiffenbach JM, Facial expressions of the neonate infant indicating the hedonics of foodrelated chemical stimuli. In: Taste and Development: the genesis of sweet preference. Washington DC, USA: Government Printing Office; 1977. p. 173–89.
6. Brown PD, Morra MJ, Donald LS, Control of Soil-Borne Plant Pests Using Glucosinolate-Containing Plants. In: Advances in Agronomy. Volume 61. New York, USA: Academic Press; 1997. p. 167–231.
7. Garcia J, Hankins WG. The evolution of bitter and the acquisition of toxiphobia. In: Denton DA, Coghlan JP, editors. Proceedings of the 5th International Symposium on Olfaction and Taste. Melbourne, Australia: Academic Press; 1975. p. 39.
8. Mauricio R, Rausher MD, Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution. 1997; 51(5): 1435–44.
9. Whittaker RH, Feeny PP, Allelochemics: Chemical Interactions between Species. Science. 1971; 171(3973): 757–70. 5541160
10. Glendinning JI, Is the bitter rejection response always adaptive? Physiol Behav. 1994; 56(6): 1217–27. 7878094
11. Koshimizu K, Ohigashi H, Huffman MA, Use of Veronia-amygdalina by wild chimpanzee—possible roles of its bitter and related constituents. Physiol Behav. 1994; 56(6): 1209–16. 7878093
12. Faiz MA, Bin Yunus E, Rahman MR, Islam F, Hoque MG, et al.; South East Asian Quinine Artesunate Malaria Trial (SEAQUAMAT) group. Artesunate versus quinine for treatment of severe falciparum malaria: a randomised trial. Lancet. 2005; 366(9487): 717–25.
13. Drewnowski A, Gomez-Carneros C, Bitter taste, phytonutrients, and the consumer: a review. Am J Clin Nutr. 2000; 72(6): 1424–35. 11101467
14. Tepper BJ, Nutritional Implications of Genetic Taste Variation: The Role of PROP Sensitivity and Other Taste Phenotypes. Annu Rev Nutr. 2008; 28(1): 367–88.
15. Ventura AK, Worobey J, Early Influences on the Development of Food Preferences. Curr Biol. 2013; 23(9): R401–R8. doi: 10.1016/j.cub.2013.02.037 23660363
16. Adler E, Hoon MA, Mueller KL, Chandrashekar J, Ryba NJP, Zuker CS, A novel family of mammalian taste receptors. Cell. 2000; 100(6): 693–702. 10761934
17. Bufe B, Breslin PAS, 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(4): 322–7. 15723792
18. Chandrashekar J, Mueller KL, Hoon MA, Adler E, Feng LX, Guo W, et al. T2Rs function as bitter taste receptors. Cell. 2000; 100(6): 703–11. 10761935
19. Matsunami H, Montmayeur JP, Buck LB, A family of candidate taste receptors in human and mouse. Nature. 2000; 404(6778): 601–6. 10766242
20. Shi P, Zhang JZ, Yang H, Zhang YP, Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol Biol Evol. 2003; 20(5): 805–14. 12679530
21. 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(5610): 1221–5. 12595690
22. Kim U, Wooding S, Ricci D, Jorde LB, Drayna D, Worldwide haplotype diversity and coding sequence variation at human bitter taste receptor loci. Hum Mutat. 2005; 26(3): 199–204. 16086309
23. Bufe B, Hofmann T, Krautwurst D, Raguse JD, Meyerhof W, The human TAS2R16 receptor mediates bitter taste in response to beta-glucopyranosides. Nat Genet. 2002; 32(3): 397–401. 12379855
24. Dotson CD, Zhang L, Xu H, Shin YK, Vigues S, Ott SH, et al. Bitter Taste Receptors Influence Glucose Homeostasis. PLoS One. 2008; 3(12).
25. Pronin AN, Xu H, Tang H, Zhang L, Li Q, Li X, Specific Alleles of Bitter Receptor Genes Influence Human Sensitivity to the Bitterness of Aloin and Saccharin. Curr Biol. 2007; 17(16): 1403–8. 17702579
26. Roudnitzky N, Bufe B, Thalmann S, Kuhn C, Gunn HC, Xing C, et al. Genomic, genetic and functional dissection of bitter taste responses to artificial sweeteners. Hum Mol Genet. 2011; 20(17): 3437–49. doi: 10.1093/hmg/ddr252 21672920
27. Soranzo N, Bufe B, Sabeti PC, Wilson JF, Weale ME, Marguerie R, et al. Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr Biol. 2005; 15(14): 1257–65. 16051168
28. Allen AL, McGeary JE, Hayes JE, Polymorphisms in TRPV1 and TAS2Rs Associate with Sensations from Sampled Ethanol. Alcohol Clin Exp Res. 2014; 38(10): 2550–60. doi: 10.1111/acer.12527 25257701
29. Dotson CD, Wallace MR, Bartoshuk LM, Logan HL, Variation in the Gene TAS2R13 is Associated with Differences in Alcohol Consumption in Patients with Head and Neck Cancer. Chem Senses. 2012; 37(8): 737–44. doi: 10.1093/chemse/bjs063 22824251
30. 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 and Nutrition. 2014; 9(3).
31. Meyerhof W, Batram C, Kuhn C, Brockhoff A, Chudoba E, Bufe B, et al. The Molecular Receptive Ranges of Human TAS2R Bitter Taste Receptors. Chem Senses. 2010; 35(2): 157–70. doi: 10.1093/chemse/bjp092 20022913
32. Ledda M, Kutalik Z, Souza Destito MC, Souza MM, Cirillo CA, Zamboni A, et al. GWAS of human bitter taste perception identifies new loci and reveals additional complexity of bitter taste genetics. Hum Mol Genet. 2014; 23(1): 259–67. doi: 10.1093/hmg/ddt404 23966204
33. Reed DR, Zhu G, Breslin PAS, Duke FF, Henders AK, Campbell MJ, et al. The perception of quinine taste intensity is associated with common genetic variants in a bitter receptor cluster on chromosome 12 Hum Mol Genet. 2010; 19(21): 4278–85. doi: 10.1093/hmg/ddq324 20675712
34. Hayes JE, Wallace MR, Knopik VS, Herbstman DM, Bartoshuk LM, Duffy VB, Allelic Variation in TAS2R Bitter Receptor Genes Associates with Variation in Sensations from and Ingestive Behaviors toward Common Bitter Beverages in Adults. Chem Senses. 2011; 36(3): 311–9. doi: 10.1093/chemse/bjq132 21163912
35. International Standing Committee on Human Cytogenetic Nomenclature. ISCN 2009: An International System for Human Cytogenetic Nomenclature. 1st ed. Shaffer LG, Slovak ML, Campbell LJ, editors. Basel, Switzerland: Karger; 2009. 138 p.
36. Altshuler DM, Durbin RM, Abecasis GR, Bentley DR, Chakravarti A, Clark AG, 1000 Genomes Project Consortiumet al.; An integrated map of genetic variation from 1,092 human genomes. Nature. 2012; 491(7422): 56–65. doi: 10.1038/nature11632 23128226
37. Campbell MC, Ranciaro A, Zinshteyn D, Rawlings-Goss R, Hirbo J, Thompson S, et al. Origin and Differential Selection of Allelic Variation at TAS2R16 Associated with Salicin Bitter Taste Sensitivity in Africa. Mol Biol Evol. 2013; 31(2): 288–302. doi: 10.1093/molbev/mst211 24177185
38. Altshuler D, Brooks LD, Chakravarti A, Collins FS, Daly MJ, Donnelly P, International Haplotype Map (HapMap) Consortiumet al.; A haplotype map of the human genome. Nature. 2005; 437(7063): 1299–320. 16255080
39. Thalmann S, Behrens M, Meyerhof W, Major haplotypes of the human bitter taste receptor TAS2R41 encode functional receptors for chloramphenicol. Biochem Biophys Res Commun. 2013; 435(2): 267–73. doi: 10.1016/j.bbrc.2013.04.066 23632330
40. Wooding S, Kim UK, Bamshad MJ, Larsen J, Jorde LB, Drayna D, Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. Am J Hum Genet. 2004; 74(4): 637–46. 14997422
41. Born S, Levit A, Niv MY, Meyerhof W, Behrens M, The Human Bitter Taste Receptor TAS2R10 Is Tailored to Accommodate Numerous Diverse Ligands. J Neurosci. 2013; 33(1): 201–13. doi: 10.1523/JNEUROSCI.3248-12.2013 23283334
42. Brockhoff A, Behrens M, Niv MY, Meyerhof W, Structural requirements of bitter taste receptor activation. Proc Natl Acad Sci USA. 2010; 107(24): 11110–5. doi: 10.1073/pnas.0913862107 20534469
43. Campa D, De Rango F, Carrai M, Crocco P, Montesanto A, Canzian F, et al. Bitter Taste Receptor Polymorphisms and Human Aging. PLoS One. 2012; 7(11): e45232. doi: 10.1371/journal.pone.0045232 23133589
44. Wall JD, Pritchard JK, Haplotype blocks and linkage disequilibrium in the human genome. Nat Rev Genet. 2003; 4(8): 587–97. 12897771
45. Altshuler D, Brooks LD, Chakravarti A, Collins FS, Daly MJ, Donnelly P, et al.; International Haplotype Map (HapMap) Consortium. A second generation human haplotype map of over 3.1 million SNPs. Nature. 2007; 449(7164): 851–61. 17943122
46. Wooding S, Gunn H, Ramos P, Thalmann S, Xing C, Meyerhof W, Genetics and Bitter Taste Responses to Goitrin, a Plant Toxin Found in Vegetables. Chem Senses. 2010; 35(8): 685–92. doi: 10.1093/chemse/bjq061 20551074
47. Wooding S, Phenylthiocarbamide: A 75-Year Adventure in Genetics and Natural Selection. Genetics. 2006; 172(4): 2015–23. 16636110
48. Hayes JE, Feeney EL, Allen AL, Do polymorphisms in chemosensory genes matter for human ingestive behavior? Food Quality and Preference. 2013; 30(2): 202–16. 23878414
49. Stephens JC, Schneider JA, Tanguay DA, Choi J, Acharya T, Stanley SE, et al. Haplotype Variation and Linkage Disequilibrium in 313 Human Genes. Science. 2001; 293(5529): 489–93. 11452081
50. Witherspoon DJ, Wooding S, Rogers AR, Marchani EE, Watkins WS, Batzer MA, et al. Genetic Similarities Within and Between Human Populations. Genetics. 2007; 176(1): 351–9. 17339205
51. Fushan AA, Simons CT, Slack JP, Manichaikul A, Drayna D, Allelic Polymorphism within the TAS1R3 Promoter Is Associated with Human Taste Sensitivity to Sucrose. Curr Biol. 2009; 19(15): 1288–93. doi: 10.1016/j.cub.2009.06.015 19559618
52. Lipchock SV, Mennella JA, Spielman AI, Reed DR, Human bitter perception correlates with bitter receptor messenger RNA expression in taste cells. Am J Clin Nutr. 2013; 98(4): 1136–43. doi: 10.3945/ajcn.113.066688 24025627
53. Fushan A, Simons C, Slack J, Drayna D, Association between common variation in genes encoding sweet taste signaling components and human sucrose perception. Chem Senses. 2010; 35(7): 579–92. doi: 10.1093/chemse/bjq063 20660057
54. Loper HB, La Sala M, Dotson C, Steinle N, Taste perception, associated hormonal modulation, and nutrient intake. Nutr Rev. 2015; 73(2): 83–91. doi: 10.1093/nutrit/nuu009 26024495
55. Faas MM, Melgert BN, de Vos P, A Brief Review on How Pregnancy and Sex Hormones Interfere with Taste and Food Intake. Chemosens Percept. 2010; 3(1): 51–6. 20352054
56. Brockhoff A, Behrens M, Massarotti A, Appendino G, Meyerhof W, Broad tuning of the human bitter taste receptor hTAS2R46 to various sesquiterpene lactones, clerodane and labdane diterpenoids, strychnine, and denatonium. J Agric Food Chem. 2007; 55(15): 6236–43. 17595105
57. Levy S, Sutton G, Ng PC, Feuk L, Halpern AL, Walenz BP, et al. The Diploid Genome Sequence of an Individual Human. PLoS Biol. 2007; 5(10): 2113–44.
58. Feng DF, Doolittle RF, Progressive sequence alignment as a prerequisitetto correct phylogenetic trees. J Mol Evol. 1987; 25(4): 351–60. 3118049
59. Reichling C, Meyerhof W, Behrens M, Functions of human bitter taste receptors depend on N-glycosylation. J Neurochem. 2008; 106(3): 1138–48. doi: 10.1111/j.1471-4159.2008.05453.x 18466324
60. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ, Multiple sequence alignment with Clustal X. Trends Biochem Sci. 1998; 23(10): 403–5. 9810230
61. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden T, Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinform. 2012; 13(1): 134–44.
62. Stephens M, Donnelly P, A Comparison of Bayesian Methods for Haplotype Reconstruction from Population Genotype Data. Am J Hum Genet. 2003; 73(5): 1162–9. 14574645
63. Stephens M, Smith NJ, Donnelly P, A new statistical method for haplotype reconstruction from population data. Am J Hum Genet. 2001; 68(4): 978–89. 11254454
64. Weir BS, Cockerham CC, Testing hypotheses about linkage disequilibrium with multiple alleles. Genetics. 1978; 88(3): 633–42. 17248813
65. Zaykin DV, Pudovkin A, Weir BS, Correlation-Based Inference for Linkage Disequilibrium With Multiple Alleles. Genetics. 2008; 180(1): 533–45. doi: 10.1534/genetics.108.089409 18757931
66. Barrett JC, Fry B, Maller J, Daly MJ, Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005; 21(2): 263–5. 15297300
67. Wang N, Akey JM, Zhang K, Chakraborty R, Jin L, Distribution of Recombination Crossovers and the Origin of Haplotype Blocks: The Interplay of Population History, Recombination, and Mutation. Am J Hum Genet. 2002; 71(5): 1227–34. 12384857
68. Cai JJ, PGEToolbox: A Matlab Toolbox for Population Genetics and Evolution. J Hered. 2008; 99(4): 438–40. doi: 10.1093/jhered/esm127 18310616
69. ISO 6658:2005. Sensory analysis—Methodology—General guidance. Vernier, Geneva (Switzerland): International Organization for Standardization; 2005. p. 1–20.
70. Lawless HT, Heymann H, Sensory Evaluation of Food: Principles and Practices: Springer US; 1999. 819 p.
71. ISO 13301:2002. Sensory analysis—Methodology—General guidance for measuring odour, flavour and taste detection thresholds by a three-alternative forced-choice (3-AFC) procedure. Vernier, Geneva (Switzerland): International Organization for Standardization; 2005. p. 1–27.
72. Green BG, Dalton P, Cowart B, Shaffer G, Rankin K, Higgins J, Evaluating the ‘Labeled Magnitude Scale’ for Measuring Sensations of Taste and Smell. Chem Senses. 1996; 21(3): 323–34. 8670711
73. Green BG, Shaffer GS, Gilmore MM, Derivation and evaluation of a semantic scale of oral sensation magnitude with apparent ratio properties. Chem Senses. 1993; 18(6): 683–702.
74. 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(1): 109–14. 15234598
75. Gould BA, On Peirce's Criterion for the Rejection of Doubtful Observations, with tables for facilitating its application. Astron J. 1855; 4(83): 81–7.
76. Peirce B, Criterion for the rejection of doubtful observations. Astron J. 1852; 2(45): 161–3.
77. Nyholt DR, A Simple Correction for Multiple Testing for Single-Nucleotide Polymorphisms in Linkage Disequilibrium with Each Other. Am J Hum Genet. 2004; 74(4): 765–9. 14997420
78. Ueda T, Ugawa S, Yamamura H, Imaizumi Y, Shimada S, Functional Interaction between T2R Taste Receptors and G-Protein α Subunits Expressed in Taste Receptor Cells. J Neurosci. 2003; 23(19): 7376–80. 12917372
79. Hill AV, The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol. 1910; 40(Suppl): iv–vii.