A Butter Aroma Recombinate Activates Human Class-I Odorant Receptors

Journal of Agricultural and Food Chemistry

Volumn 63, Issue 43, 2015, Pages 9410-9420

  Geithe, Christiane ^a   Andersen, Gaby ^a   Malki, Agne ^a   Krautwurst, Dietmar ^a  

^a DEUTSCHE FORSCHUNGSANSTALT FÜR LEBENSMITTELCHEMIE   (Germany)

Author keywords

chemoreception; chemotaxis; GPCR; key food odorants; neutrophils

Indexed keywords

BIOCHEMISTRY; BLOOD; CHEMICAL ACTIVATION; CHEMICAL CONTAMINATION;

CHEMORECEPTION; CHEMOTAXIS; GPCR; KEY FOOD ODORANTS; NEUTROPHILS;

ODORS;

BUTTER; FLAVORING AGENT; OLFACTORY RECEPTOR;

ANALYSIS; BUTTER; GENETICS; HUMAN; METABOLISM; ODOR; OLFACTORY RECEPTOR;

BUTTER; FLAVORING AGENTS; HUMANS; ODORS; RECEPTORS, ODORANT; SMELL;

EID: 84946595183     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.5b01884     Document Type: Article

References (73)

1. Buck, L.; Axel, R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition Cell 1991, 65 (1) 175-187 10.1016/0092-8674(91)90418-X
2. Levy, N. S.; Bakalyar, H. A.; Reed, R. R. Signal transduction in olfactory neurons J. Steroid Biochem. Mol. Biol. 1991, 39 (4B) 633-637 10.1016/0960-0760(91)90262-4
3. Mainland, J. D.; Keller, A.; Li, Y. R.; Zhou, T.; Trimmer, C.; Snyder, L. L.; Moberly, A. H.; Adipietro, K. A.; Liu, W. L.; Zhuang, H.; Zhan, S.; Lee, S. S.; Lin, A.; Matsunami, H. The missense of smell: functional variability in the human odorant receptor repertoire Nat. Neurosci. 2014, 17 (1) 114-120 10.1038/nn.3598
4. Olender, T.; Waszak, S. M.; Viavant, M.; Khen, M.; Ben-Asher, E.; Reyes, A.; Nativ, N.; Wysocki, C. J.; Ge, D.; Lancet, D. Personal receptor repertoires: olfaction as a model BMC Genomics 2012, 13, 414 10.1186/1471-2164-13-414
5. Nelson, G.; Chandrashekar, J.; Hoon, M. A.; Feng, L.; Zhao, G.; Ryba, N. J.; Zuker, C. S. An amino-acid taste receptor Nature 2002, 416 (6877) 199-202 10.1038/nature726
6. Nelson, G.; Hoon, M. A.; Chandrashekar, J.; Zhang, Y.; Ryba, N. J.; Zuker, C. S. Mammalian sweet taste receptors Cell 2001, 106 (3) 381-390 10.1016/S0092-8674(01)00451-2
7. Adler, E.; Hoon, M. A.; Mueller, K. L.; Chandrashekar, J.; Ryba, N. J.; Zuker, C. S. A novel family of mammalian taste receptors Cell 2000, 100 (6) 693-702 10.1016/S0092-8674(00)80705-9
8. Chandrashekar, J.; Mueller, K. L.; Hoon, M. A.; Adler, E.; Feng, L.; Guo, W.; Zuker, C. S.; Ryba, N. J. T2Rs function as bitter taste receptors Cell 2000, 100 (6) 703-711 10.1016/S0092-8674(00)80706-0
9. Shi, P.; Zhang, J.; Yang, H.; Zhang, Y. P. Adaptive diversification of bitter taste receptor genes in mammalian evolution Mol. Biol. Evol. 2003, 20 (5) 805-814 10.1093/molbev/msg083
10. Borowsky, B.; Adham, N.; Jones, K. A.; Raddatz, R.; Artymyshyn, R.; Ogozalek, K. L.; Durkin, M. M.; Lakhlani, P. P.; Bonini, J. A.; Pathirana, S.; Boyle, N.; Pu, X.; Kouranova, E.; Lichtblau, H.; Ochoa, F. Y.; Branchek, T. A.; Gerald, C. Trace amines: identification of a family of mammalian G protein-coupled receptors Proc. Natl. Acad. Sci. U. S. A. 2001, 98 (16) 8966-8971 10.1073/pnas.151105198
11. Liberles, S. D. Trace amine-associated receptors are olfactory receptors in vertebrates Ann. N. Y. Acad. Sci. 2009, 1170, 168-172 10.1111/j.1749-6632.2009.04014.x
12. Liberles, S. D.; Buck, L. B. A second class of chemosensory receptors in the olfactory epithelium Nature 2006, 442 (7103) 645-650 10.1038/nature05066
13. Rodriguez, I.; Greer, C. A.; Mok, M. Y.; Mombaerts, P. A putative pheromone receptor gene expressed in human olfactory mucosa Nat. Genet. 2000, 26 (1) 18-19 10.1038/79124
14. Rodriguez, I.; Mombaerts, P. Novel human vomeronasal receptor-like genes reveal species-specific families Curr. Biol. 2002, 12 (12) R409-R411 10.1016/S0960-9822(02)00909-0
15. Abdoul-Azize, S.; Selvakumar, S.; Sadou, H.; Besnard, P.; Khan, N. A. Ca2+ signaling in taste bud cells and spontaneous preference for fat: unresolved roles of CD36 and GPR120 Biochimie 2014, 96, 8-13 10.1016/j.biochi.2013.06.005
16. Dunkel, A.; Steinhaus, M.; Kotthoff, M.; Nowak, B.; Krautwurst, D.; Schieberle, P.; Hofmann, T. Nature's chemical signatures in human olfaction: a foodborne perspective for future biotechnology Angew. Chem., Int. Ed. 2014, 53, 7124-7143 10.1002/anie.201309508
17. 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 (2) 157-170 10.1093/chemse/bjp092
18. Zhuang, H.; Matsunami, H. Evaluating cell-surface expression and measuring activation of mammalian odorant receptors in heterologous cells Nat. Protoc. 2008, 3 (9) 1402-1413 10.1038/nprot.2008.120
19. Schieberle, P.; Gassenmeier, K.; Guth, H.; Sen, A.; Grosch, W. Character impact odor compounds of different kinds of butter Food Sci. Technol. (London) 1993, 26 (4) 347-356 10.1006/fstl.1993.1070
20. Cui, T.; Tsolakis, A. V.; Li, S. C.; Cunningham, J. L.; Lind, T.; Oberg, K.; Giandomenico, V. Olfactory receptor 51E1 protein as a potential novel tissue biomarker for small intestine neuroendocrine carcinomas Eur. J. Endocrinol. 2013, 168 (2) 253-261 10.1530/EJE-12-0814
21. Deshpande, D. A.; Wang, W. C. H.; McIlmoyle, E. L.; Robinett, K. S.; Schillinger, R. M.; An, S. S.; Sham, J. S. K.; Liggett, S. B. Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction Nat. Med. 2010, 16 (11) 1299-1304 10.1038/nm.2237
22. Feldmesser, E.; Olender, T.; Khen, M.; Yanai, I.; Ophir, R.; Lancet, D. Widespread ectopic expression of olfactory receptor genes BMC Genomics 2006, 7, 121 10.1186/1471-2164-7-121
23. Flegel, C.; Manteniotis, S.; Osthold, S.; Hatt, H.; Gisselmann, G., Expression profile of ectopic olfactory receptors determined by deep sequencing. PLoS One 2013, 8 (2), e55368 10.1371/journal.pone.0055368
24. Foster, S. R.; Roura, E.; Thomas, W. G. Extrasensory perception: odorant and taste receptors beyond the nose and mouth Pharmacol. Ther. 2014, 142 (1) 41-61 10.1016/j.pharmthera.2013.11.004
25. Goto, T.; Adjaye, J.; Rodeck, C. H.; Monk, M. Identification of genes expressed in human primordial germ cells at the time of entry of the female germ line into meiosis Mol. Hum. Reprod. 1999, 5 (9) 851-860 10.1093/molehr/5.9.851
26. Iwatsuki, K.; Uneyama, H. Sense of Taste in the Gastrointestinal Tract J. Pharmacol. Sci. 2012, 118 (2) 123-128 10.1254/jphs.11R08CP
27. Lee, R. J.; Kofonow, J. M.; Rosen, P. L.; Siebert, A. P.; Chen, B.; Doghramji, L.; Xiong, G.; Adappa, N. D.; Palmer, J. N.; Kennedy, D. W.; Kreindler, J. L.; Margolskee, R. F.; Cohen, N. A. Bitter and sweet taste receptors regulate human upper respiratory innate immunity J. Clin. Invest. 2014, 124, 1393-1405 10.1172/JCI72094
28. 2+ and cAMP concentrations in spermatozoa PLoS One 2012, 7 (2) e32354 10.1371/journal.pone.0032354
29. Rozengurt, E. Taste receptors in the gastrointestinal tract. I. Bitter taste receptors and alpha-gustducin in the mammalian gut Am. J. Physiol.-Gastrointest. Liver Physiol. 2006, 291 (2) G171-G177 10.1152/ajpgi.00073.2006
30. Spehr, M.; Schwane, K.; Riffell, J. A.; Zimmer, R. K.; Hatt, H. Odorant receptors and olfactory-like signaling mechanisms in mammalian sperm Mol. Cell. Endocrinol. 2006, 250 (1-2) 128-136 10.1016/j.mce.2005.12.035
31. Thomas, M. B.; Haines, S. L.; Akeson, R. A. Chemoreceptors expressed in taste, olfactory and male reproductive tissues Gene 1996, 178 (1-2) 1-5 10.1016/0378-1119(96)00311-3
32. Foster, S. R.; Blank, K.; See Hoe, L. E.; Behrens, M.; Meyerhof, W.; Peart, J. N.; Thomas, W. G. Bitter taste receptor agonists elicit G-protein-dependent negative inotropy in the murine heart FASEB J. 2014, 28 (10) 4497-4508 10.1096/fj.14-256305
33. Prandi, S.; Bromke, M.; Hubner, S.; Voigt, A.; Boehm, U.; Meyerhof, W.; Behrens, M. A subset of mouse colonic goblet cells expresses the bitter taste receptor Tas2r131 PLoS One 2013, 8 (12) e82820 10.1371/journal.pone.0082820
34. Feingold, E. A.; Penny, L. A.; Nienhuis, A. W.; Forget, B. G. An olfactory receptor gene is located in the extended human beta-globin gene cluster and is expressed in erythroid cells Genomics 1999, 61 (1) 15-23 10.1006/geno.1999.5935
35. Zhao, W.; Ho, L.; Varghese, M.; Yemul, S.; Dams-O'Connor, K.; Gordon, W.; Knable, L.; Freire, D.; Haroutunian, V.; Pasinetti, G. M. Decreased level of olfactory receptors in blood cells following traumatic brain injury and potential association with tauopathy J. Alzheimer's Dis. 2013, 34 (2) 417-429 10.3233/JAD-121894
36. Malki, A.; Fiedler, J.; Fricke, K.; Ballweg, I.; Pfaffl, M. W.; Krautwurst, D. Class I odorant receptors, TAS1R and TAS2R taste receptors, are markers for subpopulations of circulating leukocytes J. Leukocyte Biol. 2015, 97, 533-545 10.1189/jlb.2A0714-331RR
37. Colburn, W. A.; Bekersky, I.; Blumenthal, H. P. Dietary saccharin kinetics Clin. Pharmacol. Ther. 1981, 30 (4) 558-563 10.1038/clpt.1981.203
38. Desage, M.; Schaal, B.; Soubeyrand, J.; Orgeur, P.; Brazier, J. L. Gas chromatographic-mass spectrometric method to characterise the transfer of dietary odorous compounds into plasma and milk J. Chromatogr., Biomed. Appl. 1996, 678 (2) 205-210 10.1016/0378-4347(95)00527-7
39. Zeller, A.; Horst, K.; Rychlik, M. Study of the metabolism of estragole in humans consuming fennel tea Chem. Res. Toxicol. 2009, 22 (12) 1929-1937 10.1021/tx900236g
40. Krautwurst, D.; Yau, K. W.; Reed, R. R. Identification of ligands for olfactory receptors by functional expression of a receptor library Cell 1998, 95 (7) 917-926 10.1016/S0092-8674(00)81716-X
41. HORDE, The Human Olfactory Receptor Data Exploratorium (HORDE). The Weizmann Institute, 2011; http://bioportal.weizmann.ac.il/HORDE/.
42. Olender, T.; Nativ, N.; Lancet, D. HORDE: comprehensive resource for olfactory receptor genomics Methods Mol. Biol. 2013, 1003, 23-38 10.1007/978-1-62703-377-0-2
43. Hamprecht, B. Structural, electrophysiological, biochemical, and pharmacological properties of neuroblastoma-glioma cell hybrids in cell culture Int. Rev. Cytol. 1977, 49, 99-170 10.1016/S0074-7696(08)61948-8
44. Jones, D. T.; Reed, R. R. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction Science (Washington, DC, U. S.) 1989, 244 (4906) 790-795 10.1126/science.2499043
45. Kerr, D. S.; Von Dannecker, L. E.; Davalos, M.; Michaloski, J. S.; Malnic, B., Ric-8B interacts with G alpha olf and G gamma 13 and co-localizes with G alpha olf, G beta 1 and G gamma 13 in the cilia of olfactory sensory neurons. Mol. Cell. Neurosci. 2008, 38 (3), 341-348 (Epub 2008 Apr 1). 10.1016/j.mcn.2008.03.006
46. Saito, H.; Kubota, M.; Roberts, R. W.; Chi, Q.; Matsunami, H. RTP family members induce functional expression of mammalian odorant receptors Cell 2004, 119 (5) 679-691 10.1016/j.cell.2004.11.021
47. Binkowski, B.; Fan, F.; Wood, K. Engineered luciferases for molecular sensing in living cells Curr. Opin. Biotechnol. 2009, 20 (1) 14-18 10.1016/j.copbio.2009.02.013
48. Babusyte, A.; Kotthoff, M.; Fiedler, J.; Krautwurst, D. Biogenic amines activate blood leukocytes via trace amine-associated receptors TAAR1 and TAAR2 J. Leukocyte Biol. 2013, 93, 387-394 10.1189/jlb.0912433
49. Saito, H.; Chi, Q.; Zhuang, H.; Matsunami, H.; Mainland, J. D. Odor coding by a mammalian receptor repertoire Sci. Signaling 2009, 2 (60) ra9 10.1126/scisignal.2000016
50. Lehmann, D.; Maas, B.; Mosandl, A. Stereoisomeric flavor compounds. Part 69. Stereodifferentiation of δ(γ)-lactones C8-C18 in dairy products, margarine, and coconut Z. Lebensm.-Unters. Forsch. 1995, 201 (1) 55-61 10.1007/BF01193201
51. Glusman, G.; Bahar, A.; Sharon, D.; Pilpel, Y.; White, J.; Lancet, D. The olfactory receptor gene superfamily: data mining, classification, and nomenclature Mamm. Genome 2000, 11 (11) 1016-1023 10.1007/s003350010196
52. Niimura, Y.; Nei, M. Evolution of olfactory receptor genes in the human genome Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (21) 12235-12240 10.1073/pnas.1635157100
53. Sanz, G.; Schlegel, C.; Pernollet, J. C.; Briand, L. Comparison of odorant specificity of two human olfactory receptors from different phylogenetic classes and evidence for antagonism Chem. Senses 2005, 30 (1) 69-80 10.1093/chemse/bji002
54. Kolaczkowska, E.; Kubes, P. Neutrophil recruitment and function in health and inflammation Nat. Rev. Immunol. 2013, 13 (3) 159-175 10.1038/nri3399
55. Katada, T. The inhibitory G protein G(i) identified as pertussis toxin-catalyzed ADP-ribosylation Biol. Pharm. Bull. 2012, 35 (12) 2103-2111 10.1248/bpb.b212024
56. Cubillos, S.; Norgauer, J.; Lehmann, K. Toxins-useful biochemical tools for leukocyte research Toxins 2010, 2 (4) 428-452 10.3390/toxins2040428
57. Nijssen, L. M.; Ingen-Visscher, C. A. v.; Donders, J. J. H., Eds. VCF Volatile Compounds in Food: Database; TNO Triskelion: Zeist, The Netherlands, 1963- 2014; Vol. Version 15.2.
58. Krautwurst, D.; Kotthoff, M. A hit map-based statistical method to predict best ligands for orphan olfactory receptors: natural key odorants versus lock picks Methods Mol. Biol. 2013, 1003, 85-97 10.1007/978-1-62703-377-0-6
59. Jaeger, S. R.; McRae, J. F.; Bava, C. M.; Beresford, M. K.; Hunter, D.; Jia, Y.; Chheang, S. L.; Jin, D.; Peng, M.; Gamble, J. C.; Atkinson, K. R.; Axten, L. G.; Paisley, A. G.; Tooman, L.; Pineau, B.; Rouse, S. A.; Newcomb, R. D. A mendelian trait for olfactory sensitivity affects odor experience and food selection Curr. Biol. 2013, 23 (16) 1601-1605 10.1016/j.cub.2013.07.030
60. Keller, A.; Zhuang, H.; Chi, Q.; Vosshall, L. B.; Matsunami, H. Genetic variation in a human odorant receptor alters odour perception Nature 2007, 449 (7161) 468-472 10.1038/nature06162
61. Noe, F.; Polster, J.; Schieberle, P.; Krautwurst, D., Structure-activity relationships of mercaptans on odorant receptor OR2M3 may explain the characteristic odour threshold trend across a homologous series of 3-mercapto-2-methylalkan-1-ols in humans. In Flavour Science-Proceedings of the XIV Weurman Flavour Research Symposium; Taylor, A. J.; Mottram, D. S., Eds.; Context Products: Leicestershire, UK, 2015; Vol. 14, pp 353-356.
62. Keeney, P. G.; Patton, S. The coconut-flavor defect of milk fat. I. Isolation of the flavor compound from butter oil and its identification as δ-decalactone J. Dairy Sci. 1956, 39, 1104-1113 10.3168/jds.S0022-0302(56)94825-1
63. Hague, C.; Uberti, M. A.; Chen, Z.; Bush, C. F.; Jones, S. V.; Ressler, K. J.; Hall, R. A.; Minneman, K. P. Olfactory receptor surface expression is driven by association with the beta2-adrenergic receptor Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (37) 13672-13676 10.1073/pnas.0403854101
64. Jiang, Y.; Li, Y. R.; Tian, H.; Ma, M.; Matsunami, H. Muscarinic acetylcholine receptor M3 modulates odorant receptor activity via inhibition of beta-arrestin-2 recruitment Nat. Commun. 2015, 6, 6448 10.1038/ncomms7448
65. Li, Y. R.; Matsunami, H. Activation state of the m3 muscarinic acetylcholine receptor modulates mammalian odorant receptor signaling Sci. Signaling 2011, 4 (155) ra1 10.1126/scisignal.2001230
66. Behrens, M.; Meyerhof, W. Gustatory and extragustatory functions of mammalian taste receptors Physiol. Behav. 2011, 105 (1) 4-13 10.1016/j.physbeh.2011.02.010
67. Nilsson, N. E.; Kotarsky, K.; Owman, C.; Olde, B. Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids Biochem. Biophys. Res. Commun. 2003, 303 (4) 1047-1052 10.1016/S0006-291X(03)00488-1
68. Nohr, M. K.; Pedersen, M. H.; Gille, A.; Egerod, K. L.; Engelstoft, M. S.; Husted, A. S.; Sichlau, R. M.; Grunddal, K. V.; Poulsen, S. S.; Han, S.; Jones, R. M.; Offermanns, S.; Schwartz, T. W. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes Endocrinology 2013, 154 (10) 3552-3564 10.1210/en.2013-1142
69. Spinsanti, G.; Zannolli, R.; Panti, C.; Ceccarelli, I.; Marsili, L.; Bachiocco, V.; Frati, F.; Aloisi, A. M. Quantitative real-time PCR detection of TRPV1-4 gene expression in human leukocytes from healthy and hyposensitive subjects Mol. Pain 2008, 4, 51 10.1186/1744-8069-4-51
70. Wenning, A. S.; Neblung, K.; Strauss, B.; Wolfs, M. J.; Sappok, A.; Hoth, M.; Schwarz, E. C. TRP expression pattern and the functional importance of TRPC3 in primary human T-cells Biochim. Biophys. Acta, Mol. Cell Res. 2011, 1813 (3) 412-423 10.1016/j.bbamcr.2010.12.022
71. Nei, M.; Niimura, Y.; Nozawa, M. The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity Nat. Rev. Genet. 2008, 9 (12) 951-963 10.1038/nrg2480
72. Freitag, J.; Ludwig, G.; Andreini, I.; Rössler, P.; Breer, H. Olfactory receptors in aquatic and terrestrial vertebrates J. Comp. Physiol., A 1998, 183 (5) 635-650 10.1007/s003590050287
73. Vinolo, M. A.; Ferguson, G. J.; Kulkarni, S.; Damoulakis, G.; Anderson, K.; Bohlooly, Y. M.; Stephens, L.; Hawkins, P. T.; Curi, R. SCFAs induce mouse neutrophil chemotaxis through the GPR43 receptor PLoS One 2011, 6 (6) e21205 10.1371/journal.pone.0021205