Beef Protein-Derived Peptides as Bitter Taste Receptor T2R4 Blockers

Journal of Agricultural and Food Chemistry

Volumn 66, Issue 19, 2018, Pages 4902-4912

  Zhang, Chunlei ^a   Alashi, Adeola M ^a   Singh, Nisha ^a   Liu, Kun ^a   Chelikani, Prashen ^a   Aluko, Rotimi E ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

(T2R); bitter taste receptor; bitterness; electronic tongue; peptides; protein hydrolysates; quinine

Indexed keywords

AMINO ACIDS; BEEF; CALCIUM; HYDROLYSIS; PEPTIDES;

(T2R); BITTERNESS; PROTEIN HYDROLYSATE; QUININE; TASTE RECEPTORS;

ELECTRONIC TONGUES;

CALCIUM; CHYMOTRYPSIN; FLAVORING AGENT; FLAVOURZYME; G PROTEIN COUPLED RECEPTOR; PEPTIDE; PROTEIN; PROTEINASE; QUININE; SUBTILISIN; TASTE RECEPTORS, TYPE 2; TRYPSIN;

ANALYSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOCATALYSIS; BOVINE; CHEMISTRY; ELECTRONIC NOSE; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; RED MEAT;

ANIMALS; BIOCATALYSIS; CALCIUM; CATTLE; CHYMOTRYPSIN; ELECTRONIC NOSE; ENDOPEPTIDASES; FLAVORING AGENTS; HEK293 CELLS; HUMANS; PEPTIDES; PROTEINS; QUININE; RECEPTORS, G-PROTEIN-COUPLED; RED MEAT; SUBTILISINS; TRYPSIN;

EID: 85046531355     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.8b00830     Document Type: Article

References (62)

1. Levit, A.; Nowak, S.; Peters, M.; Wiener, A.; Meyerhof, W.; Behrens, M.; Niv, M. Y. The bitter pill: Clinical drugs that activate the human bitter taste receptor TAS2R14. FASEB J. 2014, 28, 1181-1197, 10.1096/fj.13-242594
2. Meyerhof, W. Elucidation of mammalian bitter taste. Rev. Physiol. Biochem. Pharmacol. 2005, 154, 37-72, 10.1007/s10254-005-0041-0
3. Upadhyaya, J.; Pydi, S. P.; Singh, N.; Aluko, R. E.; Chelikani, P. Bitter taste receptor T2R1 is activated by dipeptides and tripeptides. Biochem. Biophys. Res. Commun. 2010, 398, 331-335, 10.1016/j.bbrc.2010.06.097
4. Meyerhof, W.; Batram, C.; Kuhn, C.; Brockhoff, A.; Chudoba, E.; Bufe, B.; Appendino, G.; Behrens, M. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem. Senses 2010, 35, 157-170, 10.1093/chemse/bjp092
5. Lossow, K.; Hübner, S.; Roudnitzky, N.; Slack, J. P.; Pollastro, F.; Behrens, M.; Meyerhof, W. Comprehensive analysis of mouse bitter taste receptors reveals different molecular receptive ranges for orthologous receptors in mice and humans. J. Biol. Chem. 2016, 291, 15358-15377, 10.1074/jbc.M116.718544
6. Wiener, A.; Shudler, M.; Levit, A.; Niv, M. Y. BitterDB: a database of bitter compounds. Nucleic Acids Res. 2012, 40, D413-D419, 10.1093/nar/gkr755
7. Sainz, E.; Cavenagh, M. M.; Gutierrez, J.; Battey, J. F.; Northup, J. K.; Sullivan, S. L. Functional characterization of human bitter taste receptors. Biochem. J. 2007, 403, 537-43, 10.1042/BJ20061744
8. Pydi, S. P.; Sobotkiewicz, T.; Billakanti, R.; Bhullar, R. P.; Loewen, M. C.; Chelikani, P. Amino acid derivatives as bitter taste receptor (T2R) blockers. J. Biol. Chem. 2014, 289, 25054-25066, 10.1074/jbc.M114.576975
9. Pydi, S. P.; Jaggupilli, A.; Nelson, K. M.; Abrams, S. R.; Bhullar, R. P.; Loewen, M. C.; Chelikani, P. Abscisic acid acts as a blocker of the bitter taste G protein-coupled receptor T2R4. Biochemistry 2015, 54, 2622-2631, 10.1021/acs.biochem.5b00265
10. Roland, W. S. U.; Gouka, R. J.; Gruppen, H.; Driesse, M.; Van Buren, L.; Smit, G.; Vincken, J. P. 6-Methoxyflavanones as bitter taste receptor blockers for hTAS2R39. PLoS One 2014, 9 (4), e94451, 10.1371/journal.pone.0094451
11. Liszt, K. I.; Ley, J. P.; Lieder, B.; Behrens, M.; Stöger, B.; Reiner, A.; Hochkogler, C. M.; Köck, E.; Marchiori, A.; Hans, J.; Widder, S.; Krammer, G.; Sanger, G. J.; Somoza, M. M.; Meyerhof, W.; Somoza, V. Caffeine induces gastric acid secretion via bitter taste signaling in gastric parietal cells. Proc. Natl. Acad. Sci. U. S. A. 2017, 114, E6260-E6269, 10.1073/pnas.1703728114
12. Slack, J. P.; Brockhoff, A.; Batram, C.; Menzel, S.; Sonnabend, C.; Born, S.; Galindo, M. M.; Kohl, S.; Thalmann, S.; Ostopovici-Halip, L.; Simons, C. T.; Ungureanu, I.; Duineveld, K.; Bologa, C. G.; Behrens, M.; Furrer, S.; Oprea, T. I.; Meyerhof, W. Modulation of bitter taste perception by a small molecule hTAS2R antagonist. Curr. Biol. 2010, 20, 1104-1109, 10.1016/j.cub.2010.04.043
13. 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, 6236-6243, 10.1021/jf070503p
14. Jaggupilli, A.; Howard, R.; Upadhyaya, J. D.; Bhullar, R. P.; Chelikani, P. Bitter taste receptors: Novel insights into the biochemistry and pharmacology. Int. J. Biochem. Cell Biol. 2016, 77, 184-196, 10.1016/j.biocel.2016.03.005
15. Wu, S. V.; Rozengurt, N.; Yang, M.; Young, S. H.; 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. U. S. A. 2002, 99, 2392-2397, 10.1073/pnas.042617699
16. Clark, A. A.; Liggett, S. B.; Munger, S. D. Extraoral bitter taste receptors as mediators of off-target drug effects. FASEB J. 2012, 26, 4827-4831, 10.1096/fj.12-215087
17. Avau, B.; Rotondo, A.; Thijs, T.; Andrews, C. N.; Janssen, P.; Tack, J.; Depoortere, I. Targeting extra-oral bitter taste receptors modulates gastrointestinal motility with effects on satiation. Sci. Rep. 2015, 5, 15985, 10.1038/srep15985
18. Clark, A. A.; Dotson, C. D.; Elson, A. E. T.; Voigt, A.; Boehm, U.; Meyerhof, W.; Steinle, N. I.; Munger, S. D. TAS2R bitter taste receptors regulate thyroid function. FASEB J. 2015, 29, 164-172, 10.1096/fj.14-262246
19. Wölfle, U.; Elsholz, F. A.; Kersten, A.; Haarhaus, B.; Müller, W. E.; Schempp, C. M. Expression and functional activity of the bitter taste receptors TAS2R1 and TAS2R38 in human keratinocytes. Skin Pharmacol. Physiol 2015, 28, 137-146, 10.1159/000367631
20. Deshpande, D. A.; Wang, W. C. H.; McIlmoyle, E. L.; Robinett, K. S.; Schillinger, R. M.; An, S. S.; Liggett, S. B. Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat. Med. 2010, 16, 1299-1304, 10.1038/nm.2237
21. Zhang, C. H.; Lifshitz, L. M.; Uy, K. F.; Ikebe, M.; Fogarty, K. E.; ZhuGe, R. The cellular and molecular basis of bitter tastant-induced bronchodilation. PLoS Biol. 2013, 11, e1001501, 10.1371/journal.pbio.1001501
22. Shaik, F. A.; Singh, N.; Arakawa, M.; Duan, K.; Bhullar, R. P.; Chelikani, P. Bitter taste receptors: Extraoral roles in pathophysiology. Int. J. Biochem. Cell Biol. 2016, 77, 197-204, 10.1016/j.biocel.2016.03.011
23. Kannan, A.; Hettiarachchy, N. S.; Marshall, M.; Raghavan, S.; Kristinsson, H. Shrimp shell peptide hydrolysates inhibit human cancer cell proliferation. J. Sci. Food Agric. 2011, 91, 1920-1924, 10.1002/jsfa.4464
24. Ryu, B.; Qian, Z. J.; Kim, S. K. SHP-1, a novel peptide isolated from seahorse inhibits collagen release through the suppression of collagenases 1 and 3, nitric oxide products regulated by NF-B/p38 kinase. Peptides 2010, 31, 79-87, 10.1016/j.peptides.2009.10.019
25. Udenigwe, C. C.; Aluko, R. E. Food protein-derived bioactive peptides: Production, processing, and potential health benefits. J. Food Sci. 2012, 77, R11-R24, 10.1111/j.1750-3841.2011.02455.x
26. Karametsi, K.; Kokkinidou, S.; Ronningen, I.; Peterson, D. G. Identification of bitter peptides in aged Cheddar cheese. J. Agric. Food Chem. 2014, 62, 8034-8041, 10.1021/jf5020654
27. Fuller, W.; Qurtz, R. J. Composition comprising bitter- or metallic-tasting eatable and tastand-comprising (hydroxy-, amino- or mercapto)-substituted di:carboxylic acid or derivatives, especially di:peptide containing aspartic acid. US Patent 5643955, 1997.
28. Ley, J. P. Masking bitter taste by molecules. Chemosens. Percept. 2008, 1, 58-77, 10.1007/s12078-008-9008-2
29. Akitomi, H.; Tahara, Y.; Yasuura, M.; Kobayashi, Y.; Ikezaki, H.; Toko, K. Quantification of tastes of amino acids using taste sensors. Sens. Actuators, B 2013, 179, 276-281, 10.1016/j.snb.2012.09.014
30. Williams, P. G. Nutritional composition of red meat. Nutr. Dietetics 2007, 64 (Suppl. 4), S113-S119, 10.1111/j.1747-0080.2007.00197.x
31. Hou, H.; Li, B.; Zhao, X. Enzymatic hydrolysis of defatted mackerel protein with low bitter taste. J. Ocean Univ. China 2011, 10, 85-92, 10.1007/s11802-011-1785-6
32. Lin, S.; Tian, W.; Li, H.; Cao, J.; Jiang, W. Improving antioxidant activities of whey protein hydrolysates obtained by thermal preheat treatment of pepsin, trypsin, alcalase and flavourzyme. Int. J. Food Sci. Technol. 2012, 47, 2045-2051, 10.1111/j.1365-2621.2012.03068.x
33. Nchienzia, H. A.; Morawicki, R. O.; Gadang, V. P. Enzymatic hydrolysis of poultry meal with endo- and exopeptidases. Poult. Sci. 2010, 89, 2273-2280, 10.3382/ps.2008-00558
34. Charoenphun, N.; Cheirsilp, B.; Sirinupong, N.; Youravong, W. Calcium-binding peptides derived from tilapia (Oreochromis niloticus) protein hydrolysate. Eur. Food Res. Technol. 2013, 236, 57-63, 10.1007/s00217-012-1860-2
35. Nielsen, P. M.; Petersen, D.; Dambmann, C. Improved method for determining food protein degree of hydrolysis. J. Food Sci. 2001, 66, 642-646, 10.1111/j.1365-2621.2001.tb04614.x
36. Bidlingmeyer, B. A.; Cohen, S. A.; Tarvin, T. L. Rapid analysis of amino acids using pre-column derivatization. J. Chromatogr., Biomed. Appl. 1984, 336, 93-104, 10.1016/S0378-4347(00)85133-6
37. Gehrke, C. W.; Wall, L. L.; Absheer, J. S.; Kaiser, F. E.; Zumwalt, R. W. Sample preparation for chromatography of amino-acids: acid hydrolysis of proteins. J. Assoc. Official Anal. Chem. 1985, 68, 811-821
38. Landry, J.; Delhaye, S. Simplified procedure for the determination of tryptophan of foods and feedstuffs from barytic hydrolysis. J. Agric. Food Chem. 1992, 40, 776-779, 10.1021/jf00017a014
39. He, R.; Alashi, A.; Malomo, S. A.; Girgih, A. T.; Chao, D.; Ju, X.; Aluko, R. E. Antihypertensive and free radical scavenging properties of enzymatic rapeseed protein hydrolysates. Food Chem. 2013, 141, 153-159, 10.1016/j.foodchem.2013.02.087
40. Alpha MOS. Astree electrochemical sensor technology-Technical note: T-SAS-04; 2004.
41. Girgih, A. T.; Udenigwe, C. C.; Aluko, R. E. Reverse-phase HPLC separation of hemp seed (Cannabis sativa L.) protein hydrolysate produced peptide fractions with enhanced antioxidant capacity. Plant Foods Hum. Nutr. 2013, 68, 39-46, 10.1007/s11130-013-0340-6
42. Chuesiang, P.; Sanguandeekul, R. Protein hydrolysate from tilapia frame: antioxidant and angiotensin I converting enzyme inhibitor properties. Int. J. Food Sci. Technol. 2015, 50, 1436-1444, 10.1111/ijfs.12762
43. Wanasundara, P. K. J. P. D.; Amarowicz, R.; Pegg, R.; Shand, P. J. Preparation and characterization of hydrolyzed proteins from defibrinated bovine plasma. J. Food Sci. 2002, 67, 623-630, 10.1111/j.1365-2621.2002.tb10649.x
44. Kane, L. E.; Davis, J. P.; Oakes, A. J.; Dean, L. L.; Sanders, T. H. Value-added processing of peanut meal: enzymatic hydrolysis to improve functional and nutritional properties of water soluble extracts. J. Food Biochem. 2012, 36, 520-531, 10.1111/j.1745-4514.2011.00566.x
45. Kohl, S.; Behrens, M.; Dunkel, A.; Hofmann, T.; Meyerhof, W. Amino acids and peptides activate at least five members of the human bitter taste receptor family. J. Agric. Food Chem. 2013, 61, 53-60, 10.1021/jf303146h
46. Maehashi, K.; Huang, L. Bitter peptides and bitter taste receptors. Cell. Mol. Life Sci. 2009, 66, 1661-1671, 10.1007/s00018-009-8755-9
47. Kim, M. R.; Choi, S. Y.; Lee, C. H. Molecular characterization and bitter taste formation of tryptic hydrolysis of 11S glycinin. J. Microbiol. Biotechnol. 1999, 9, 509-513
48. Rachid, O.; Simons, F. E. R.; Rawas-Qalaji, M.; Simons, K. J. An electronic tongue: Evaluation of the masking efficacy of sweetening and/or flavoring agents on the bitter taste of epinephrine. AAPS PharmSciTech 2010, 11, 550-557, 10.1208/s12249-010-9402-3
49. Wu, X.; Onitake, H.; Haraguchi, T.; Tahara, Y.; Yatabe, R.; Yoshida, M.; Toko, K. Quantitative prediction of bitterness masking effect of high-potency sweeteners using taste sensor. Sens. Actuators, B 2016, 235, 11-17, 10.1016/j.snb.2016.05.009
50. Upadhyaya, J. D.; Chakraborty, J.; Shaik, F. A.; Jaggupilli, A.; Bhullar, R. P.; Chelikani, P. The pharmacochaperone activity of quinine on bitter taste receptors. PLoS One 2016, 11, e0156347, 10.1371/journal.pone.0156347
51. Sun, X. D. Enzymatic hydrolysis of soy proteins and the hydrolysates utilization. Int. J. Food Sci. Technol. 2011, 46, 2447-2459, 10.1111/j.1365-2621.2011.02785.x
52. Tamura, M.; Mori, N.; Miyoshi, T.; Koyama, S.; Kohri, H.; Okai, H. Practical debittering using model peptides and related compounds. Agric. Biol. Chem. 1990, 54, 41-51, 10.1080/00021369.1990.10869906
53. Humiski, L.; Aluko, R. E. Physicochemical and bitterness properties of enzymatic pea protein hydrolysates. J. Food Sci. 2007, 72, S605-S611, 10.1111/j.1750-3841.2007.00475.x
54. Geisenhoff, H. Bitterness of soy protein hydrolysates according to molecular weight of peptides, MSc thesis dissertaion, Iowa State University, 2009.
55. Miyanaga, Y.; Tanigake, A.; Nakamura, T.; Kobayashi, Y.; Ikezaki, H.; Taniguchi, A.; Uchida, T. Prediction of the bitterness of single, binary- and multiple-component amino acid solutions using a taste sensor. Int. J. Pharm. 2002, 248, 207-218, 10.1016/S0378-5173(02)00456-8
56. Rudnitskaya, A.; Nieuwoudt, H. H.; Muller, N.; Legin, A.; Du Toit, M.; Bauer, F. F. Instrumental measurement of bitter taste in red wine using an electronic tongue. Anal. Bioanal. Chem. 2010, 397, 3051-3060, 10.1007/s00216-010-3885-3
57. Sarmadi, B. H.; Ismail, A. Antioxidative peptides from food proteins: A review. Peptides 2010, 31, 1949-1956, 10.1016/j.peptides.2010.06.020
58. Edens, L.; Dekker, P.; Van Der Hoeven, R.; Deen, F.; De Roos, A.; Floris, R. Extracellular prolyl endoprotease from Aspergillus niger and its use in the debittering of protein hydrolysates. J. Agric. Food Chem. 2005, 53, 7950-7957, 10.1021/jf050652c
59. FitzGerald, R. J.; O'Cuinn, G. Enzymatic debittering of food protein hydrolysates. Biotechnol. Adv. 2006, 24, 234-237, 10.1016/j.biotechadv.2005.11.002
60. Singh, N.; Vrontakis, M.; Parkinson, F.; Chelikani, P. Functional bitter taste receptors are expressed in brain cells. Biochem. Biophys. Res. Commun. 2011, 406, 146-151, 10.1016/j.bbrc.2011.02.016
61. Xu, J.; Cao, J.; Iguchi, N.; Riethmacher, D.; Huang, L. Functional characterization of bitter-taste receptors expressed in mammalian testis. Mol. Hum. Reprod. 2013, 19, 17-28, 10.1093/molehr/gas040
62. Jaggupilli, A.; Singh, N.; Upadhyaya, J.; Sikarwar, A. S.; Arakawa, M.; Dakshinamurti, S.; Chelikani, P. Analysis of the expression of human bitter taste receptors in extraoral tissues. Mol. Cell. Biochem. 2017, 426, 137-147, 10.1007/s11010-016-2902-z