Responsiveness to 6-n-propylthiouracil (PROP) is associated with salivary levels of two specific basic proline-rich proteins in humans

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Cabras, Tiziana ^a   Melis, Melania ^a   Castagnola, Massimo ^b   Padiglia, Alessandra ^a   Tepper, Beverly J ^c   Messana, Irene ^a   Barbarossa, Iole Tomassini ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROLINE RICH PROTEIN; PROPYLTHIOURACIL; PROTEIN II2; PROTEIN PS1; SALIVA PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG; 6 N PROPYLURACIL; 6-N-PROPYLURACIL; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE VI; DRUG DERIVATIVE; G PROTEIN COUPLED RECEPTOR; PROTEOME; TASTE RECEPTORS, TYPE 2; URACIL;

ADULT; AMINO ACID SEQUENCE; ARTICLE; BITTER TASTE; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; GENE; GENE FREQUENCY; GENE LOCUS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; GENOTYPE; GUSTIN GENE; HAPLOTYPE; HUMAN; MALE; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SALIVA LEVEL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; SALIVA LEVEL; SENSORY STIMULATION; TASTE DISCRIMINATION; CLINICAL TRIAL; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY; SALIVA; TASTE;

ADULT; CARBONIC ANHYDRASES; FEMALE; GENOTYPE; HUMANS; MALE; POLYMORPHISM, GENETIC; PROTEOME; RECEPTORS, G-PROTEIN-COUPLED; SALIVA; SALIVARY PROLINE-RICH PROTEINS; TASTE; TASTE PERCEPTION; URACIL; YOUNG ADULT;

EID: 84856479435     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030962     Document Type: Article

References (76)

1. Del Rio JA, Arcas MC, Benavente O, Sabater F, Ortuño A, (1998) Changes of polymethoxylated flavones levels during development of Citrus aurantium (cv. Sevillano) fruits. Planta Medica 64: 575-576.
2. Fenwick GR, Griffiths NM, Heaney RK, (1983) Bitterness in Brussels sprouts (Brassica oleracea L var gemnifera): the role of glucosinolates and their breakdown products. J Sci Food Agric 34: 73-80.
3. Fenwick GR, Heaney RK, Mullin WJ, (1983) Glucosinolates and their breakdown products in food and food plants. CRC Crit Rev Food Sci Nutr 18: 123-201.
4. Kingsbury JM, (1964) Poisonous Plants of the United States and Canada Englewood Cliffs, NJ Prentice-Hall.
5. Tepper BJ, (2008) Nutritional implications of genetic taste variation: the role of PROP sensitivity and other taste phenotypes. Annu Rev Nutr 28: 367-388.
6. Drewnowski A, Gomez-Carneros C, (2000) Bitter taste, phytonutrients, and the consumer: a review. Am J Clin Nutr 72: 1424-1435.
7. D'Archivio M, Filesi C, Di Benedetto R, Gargiulo R, Giovannini C, et al. (2007) Polyphenols, dietary sources and bioavailability. Ann Ist Super Sanità 43: 348-361.
8. Roper SD, (2007) Signal transduction and information processing in mammalian taste buds. Pflugers Arch 454: 759-776.
9. Behrens M, Reichling C, Batram C, Brockhoff A, Meyerhof W, (2009) Bitter taste receptors and their cells. Ann N Y Acad Sci 1170: 111-115.
10. Shi P, Zhang J, Yang H, Zhang YP, (2003) Adaptive diversification of bitter taste receptor genes in mammalian evolution. Mol Biol Evol 20: 805-814.
11. Wiener A, Shudler M, Levit A, Niv MY, (2011) BitterDB: a database of bitter compounds. Nucl Acids Res DOI 10.1093/nar/gkr755.
12. Behrens M, Meyerhof W, (2006) Bitter taste receptors and human bitter taste perception. Cell Mol Life Sci 63: 1501-1509.
13. Kim UK, Jorgenson E, Coon H, Leppert M, Risch N, et al. (2003) Positional cloning of the human quantitative trait locus underlying taste sensitivity to phenylthiocarbamide. Science 299: 1221-1225.
14. Meyerhof W, Batram C, Kuhn C, Brockhoff A, Chudoba E, et al. (2010) The Molecular Receptive Ranges of Human TAS2R Bitter Taste Receptors. Chem Senses 35: 157-170.
15. Reed DR, Zhu G, Breslin PA, Duke FF, Henders AK, et al. (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.
16. Pronin AN, Xu H, Tang H, Zhang L, Li Q, et al. (2007) Specific alleles of bitter receptor genes influence human sensitivity to the bitterness of aloin and saccharin. Curr Biol 17: 1403-1408.
17. Roudnitzky N, Bufe B, Thalmann S, Kuhn C, Gunn HC, et al. (2011) Genomic, genetic and functional dissection of bitter taste responses to artificial sweeteners. Hum Mol Genet 20: 3437-3449.
18. Hayes JE, Wallace MR, Knopik VS, Herbstman DM, Bartoshuk LM, et al. (2011) Allelic variation in TAS2R bitter receptor genes associates with variation in sensations from and ingestive behaviors toward common bitter beverages in adults. Chem Senses 36: 311-319.
19. Guo SW, Reed DR, (2001) The genetics of phenylthiocarbamide perception. Ann Hum Biol 28: 111-142.
20. Bell KI, Tepper BJ, (2006) Short-term vegetable intake by young children classified by 6-n-propylthoiuracil bitter-taste phenotype. Am J Clin Nutr 84: 245-251.
21. Dinehart ME, Hayes JE, Bartoshuk LM, Lanier SL, Duffy VB, (2006) Bitter taste markers explain variability in vegetable sweetness, bitterness, and intake. Physiol Behav 87: 304-313.
22. Duffy VB, Bartoshuk LM, (2000) Food acceptance and genetic variation in taste. J Am Diet Assoc 100: 647-655.
23. Hayes J, Duffy VB, (2007) Revisiting sucrose-fat mixtures: sweetness and creaminess vary with phenotypic markers of oral sensation. Chem Senses 32: 225-236.
24. Keller KL, Steinmann L, Nurse RJ, Tepper BJ, (2002) Genetic taste sensitivity to 6-n-prophylthiouracil influences food preference and reported food intake in preschool children. Appetite 38: 3-12.
25. Tepper BJ, White EA, Koelliker Y, Lanzara C, d'Adamo P, et al. (2009) Genetic variation in taste sensitivity to 6-n-propylthiouracil and its relationship to taste perception and food selection. Ann N Y Acad Sci 1170: 126-139.
26. Tepper BJ, Nurse RJ, (1998) PROP taster status is related to the perception and preference for fat. Ann N Y Acad Sci 855: 802-804.
27. Bartoshuk LM, (1993) The biological basis of food perception and acceptance. Food Qual Prefer 4: 21-32.
28. Bartoshuk LM, Duffy VB, Miller IJ, (1994) PTC/PROP tasting: anatomy, psychophysics, and sex effects. Physiol Behav 56: 1165-1171.
29. Wooding S, Kim UK, Bamshad MJ, Larsen J, Jorde LB, et al. (2004) Natural selection and molecular evolution in PTC, a bitter-taste receptor gene. Am J Hum Genet 74: 637-646.
30. Bufe B, Breslin PA, Kuhn C, Reed DR, Tharp CD, et al. (2005) The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15: 322-327.
31. Duffy VB Davidson AC, Kidd JR, Kidd KK, Speed WC, et al. (2004) Bitter receptor gene (TAS2R38), 6-n-propylthiouracil (PROP) bitterness and alchohol intake. Alcohol Clin Exp Res 28: 1629-1637.
32. Hayes JE, Bartoshuk LM, Kidd JR, Duffy VB, (2008) Supertasting and PROP bitterness depends on more than the TAS2R38 gene. Chem Senses 33: 255-265.
33. Biarnés X, Marchiori A, Giorgetti A, Lanzara C, Gasparini P, et al. (2010) Insights into the binding of phenyltiocarbamide (PTC) agonist to its target human TAS2R38 bitter receptor. PLoS One 25: e12394.
34. Mennella JA, Pepino MY, Duke FF, Reed DR, (2011) Psychophysical dissection of genotype effects on human bitter perception. Chem Senses 36: 161-167.
35. Olson JM, Boehnke M, Neiswanger K, Roche AF, Siervogel RM, (1989) Alternative genetic models for the inheritance of the phenylthiocarbamide taste deficiency. Genet Epidemiol 6: 423-434.
36. Drayna D, Coon H, Kim UK, Elsner T, Cromer K, et al. (2003) Genetic analysis of a complex trait in the Utah Genetic Reference Project: a major locus for PTC taste ability on chromosome 7q and a secondary locus on chromosome 16p. Hum Genet 112: 567-572.
37. Padiglia A, Zonza A, Atzori E, Chillotti C, Calo' MC, et al. (2010) Sensitivity to 6-n-propylthiouracil (PROP) is associated with gustin (CA6) gene polymorphism, salivary zinc and BMI in humans. Am J Clin Nutr 92: 539-545.
38. Henkin RI, Martin BM, Agarwal RP, (1999) Decreased parotid saliva gustin/carbonic anhydrase isoenzyme VI secretion: an enzyme disorder manifested by gustatory and olfactory dysfunction. Am J Med Sci 318: 380-391.
39. Henkin RI, Martin BM, Agarwal RP, (1999) Efficacy of exogenous oral zinc in treatment of patients with carbonic anhydrase VI deficiency. Am J Med Sci 318: 392-405.
40. Calò C, Padiglia A, Zonza A, Corrias L, Contu P, et al. (2011) Polymorphisms in TAS2R38 and the taste bud trophic factor, gustin gene co-operate in modulating PROP taste phenotype. Physiol Behav 104: 1065-1071.
41. Fox AF, (1932) The relationship between chemical constitution and taste. Proc Natl Acad Sci USA 18: 115-20.
42. Blakeslee AF, (1932) Genetics of Sensory Thresholds: Taste for Phenyl Thio Carbamide. Proc Natl Acad Sci U S A 18: 120-130.
43. Bennick A, (2002) Interaction of plant polyphenols with salivary proteins. Crit Rev Oral Biol Med 13: 184-196.
44. Williamson MP, (1994) The structure and function of proline-rich regions in proteins. Biochem J 297: 249-260.
45. Yan QY, Bennick A, (1995) Identification of histatins as tannin binding proteins in human saliva. Biochem J 311: 341-347.
46. Lush IE, Holland G, (1988) The genetics of tasting in mice. V. Glycine and cycloheximide. Genet Res 52: 207-212.
47. Azen EA, Davisson MT, Cherry M, Taylor BA, (1989) Prp (proline-rich protein) genes linked to markers Es-12 (esterase-12), Ea-10 (erythrocyte alloantigen) and loci on distal mouse chromosome 6. Genomics 5: 415-422.
48. Azen EA, (1991) Linkage studies of genes for salivary proline-rich proteins and bitter taste in mouse and humans. In: Wysocki CI, Kare MR, editors. Chemical senses Vol 3. Genetics of perception and communication New York Marcel Dekker pp. 279-290.
49. Capeless CG, Whitney G, Azen EA, (1992) Chromosome mapping of Soa, a gene influencing gustatory sensitivity to sucrose octaacetate in mice. Behav Genet 22: 655-663.
50. Quintana M, Palicki O, Lucchi G, Ducoroy P, Chambon C, et al. (2009) Short-Term Modification of Human Salivary Proteome Induced by Two Bitter Tastants, Urea and Quinine. Chem Percept 2: 133-142.
51. Neyraud E, Sayd T, Morzel M, Dransfield E, (2006) Proteomic analysis of human whole and parotid salivas following stimulation by different tastes. J Proteome Res 5: 2474-2480.
52. Cabras T, Pisano E, Boi R, Olianas A, Manconi B, et al. (2009) Age-Dependent Modifications of the Human Salivary Secretory Protein Complex. J Proteome Res 8: 4126-4134.
53. Azen EA, Latreille P, Niece RL, (1993) PRBI gene variants coding for length and null polymorphisms among human salivary Ps, PmF, PmS, and Pe proline-rich proteins (PRPs). Am J Hum Genet 53: 264-278.
54. Stubbs M, Chan J, Kwan A, So J, Barchynsky U, et al. (1998) Encoding of human basic and glycosylated proline-rich proteins by the PRB gene complex and proteolytic processing of their precursor proteins. Arch Oral Biol 43: 753-770.
55. Bennick A, (1982) Salivary proline-rich proteins. Mol Cell Biochem 45: 83-99.
56. Messana I, Cabras T, Pisano E, Sanna MT, Olianas A, et al. (2008) Trafficking and postsecretory events responsible for the formation of secreted human salivary peptides: a proteomics approach. Mol Cell Proteomics 7: 911-926.
57. Rayment SA, Liu B, Soares RV, Offner GD, Oppenheim FG, et al. (2001) The Effects of Duration and Intensity of Stimulation on Total Protein and Mucin Concentrations in Resting and Stimulated Whole Saliva. J Dent Res 80: 1584-1587.
58. Dinnella C, Recchia A, Fia G, Bertuccioli M, Monteleone E, (2009) Saliva characteristics and individual sensitivity to phenolic astringent stimuli. Chem Senses 34: 295-304.
59. Dinella C, Recchia A, Vincenzi S, Tuorila H, Monteleone E, (2010) Temporary Modification of salivary protein profile and individual responses to repeated phenolic astringent stimuli. Chem Senses 35: 75-85.
60. Dinella C, Recchia A, Tuorila H, Monteleone E, (2011) Individual astringency responsiveness affects the acceptance of phenol-rich foods. Appetite 56: 633-642.
61. Soares S, Vitorino R, Osorio H, Fernandes A, Venancio A, et al. (2011) Reactivity of human salivary proteins families toward food polyphenols. J Agric Food Chem 59: 5535-5547.
62. Stunkard A, Messick S, (1985) The three-factor eating questionnaire to measure dietary restraint, disinhibition, and hunger. J Psychosom Res 29: 71-83.
63. Tepper BJ, Cao J, Christensen CM, (2001) Development of brief methods to classify individuals by PROP taster status. Physiol Behav 73: 571-577.
64. Rankin KM, Godinot N, Christensen CM, Tepper BJ, Kirkmeyer SV, (2004) Assessment of different methods for 6-n-propylthiouracil status classification. In: Prescott J, Tepper BJ, editors. Genetic variation in taste sensitivity New York Marcel Dekker pp. 63-88.
65. Zhang Z, Marshall GA, (1998) A universal algorithm for fast and automated charge state deconvolution of electrospray mass-to-charge ratio spectra. J Am Soc Mass Spectrom 9: 225-233.
66. Lupi A, Messana I, Denotti G, Schininà ME, Gambarini G, et al. (2003) Identification of the human salivary Cystatin complex by the coupling of high-performance liquid chromatography and ion-trap mass spectrometry. Proteomics 3: 461-467.
67. Messana I, Cabras T, Inzitari R, Lupi A, Zuppi C, et al. (2004) Characterization of the human salivary basic proline-rich protein complex by a proteomic approach. J Proteome Res 3: 792-800.
68. Castagnola M, Inzitari R, Rossetti DV, Olmi C, Cabras T, et al. (2004) A cascade of 24 Histatins (Histatin 3 fragments) in human saliva: suggestions for a pre-secretory sequential cleavage pathway. J Biol Chem 279: 41436-41443.
69. Inzitari R, Cabras T, Onnis G, Olmi C, Mastinu A, et al. (2005) Different isoforms and post-translational modifications of human salivary acidic proline-rich proteins. Proteomics 5: 805-815.
70. Inzitari R, Cabras T, Rossetti DV, Fanali C, Vitali A, et al. (2006) Detection in human saliva of different Statherin and P-B fragments and derivatives. Proteomics 6: 6370-6379.
71. Ong SE, Mann M, (2005) Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 1: 252-262.
72. Messana I, Inzitari R, Fanali C, Cabras T, Castagnola M, (2008) Facts and artifacts in proteomics of body fluids. What proteomics of saliva is telling us? J Sep Sci 31: 1948-1963.
73. Glanville EV, Kaplan AR, (1965) Taste perception and the menstrual cycle. Nature 205: 930-931.
74. Green BG, Shaffer GS, Gilmore MM, (1993) Derivation and evaluation of a semantic scale of oral sensation magnitude with apparent ratio properties. Chem Senses 18: 683-702.
75. Tepper BJ, Ullrich NV, (2002) Influence of genetic taste sensitivity to 6-n-propylthiouracil (PROP), dietary restraint and disinhibition on body mass index in middle-age women. Physiol Behav 75: 305-312.
76. Rousset F, (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resources 8: 103-106.