Odorant-binding proteins and xenobiotic metabolizing enzymes: Implications in olfactory perireceptor events

Anatomical Record

Volumn 296, Issue 9, 2013, Pages 1333-1345

  Heydel, Jean Marie ^a   Coelho, Alexandra ^a   Thiebaud, Nicolas ^a   Legendre, Arièle ^a   Bon, Anne Marie Le ^a   Faure, Philippe ^a   Neiers, Fabrice ^a   Artur, Yves ^a   Golebiowski, Jérôme ^b   Briand, Loïc ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Chemoreception; Odorant binding protein; Olfaction; Xenobiotic metabolizing enzyme

Indexed keywords

ACETOIN; ANISALDEHYDE; ANISOLE; BINDING PROTEIN; CINEOLE; COUMARIN; ENZYME; EUGENOL; GUAIACOL; LIMONENE; LINALOOL; MENTHOL; ODORANT BINDING PROTEIN; PINENE; THYMOL; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; XENOBIOTIC METABOLIZING ENZYME;

AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME 9Q; ENZYME ACTIVITY; HUMAN; ISOELECTRIC POINT; LIGAND BINDING; MOLECULAR WEIGHT; NONHUMAN; OLFACTORY RECEPTOR; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SMELLING; VERTEBRATE;

VERTEBRATA;

CHEMORECEPTION; ODORANT-BINDING PROTEIN; OLFACTION; XENOBIOTIC METABOLIZING ENZYME;

AMINO ACID SEQUENCE; ANIMALS; ENZYMES; HUMANS; LIGANDS; METABOLIC DETOXICATION, DRUG; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; ODORS; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; PROTEIN CONFORMATION; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION; SMELL;

EID: 84882634316     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22735     Document Type: Article

References (79)

1. Andric SA, Kostic TS, Stojilkovic SS. 2006. Contribution of multidrug resistance protein MRP5 in control of cyclic guanosine 5′-monophosphate intracellular signaling in anterior pituitary cells. Endocrinology 147:3435-3445.
2. Anzenbacher P, Anzenbacherova E. 2001. Cytochromes P450 and metabolism of xenobiotics. Cell Mol Life Sci 58:737-747.
3. Benton R. 2006. On the ORigin of smell: odorant receptors in insects. Cell Mol Life Sci 63:1579-1585.
4. Bogdanffy MS. 1990. Biotransformation enzymes in the rodent nasal mucosa: The value of a histochemical approach. Environ Health Perspect 85:177-186.
5. Borysik AJ, Briand L, Taylor AJ, Scott DJ. 2010. Rapid odorant release in mammalian odour binding proteins facilitates their temporal coupling to odorant signals. J Mol Biol 404:372-380.
6. Briand L, Eloit C, Nespoulous C, Bezirard V, Huet JC, Henry C, Blon F, Trotier D, Pernollet JC. 2002. Evidence of an odorant-binding protein in the human olfactory mucus: location, structural characterization, and odorant-binding properties. Biochemistry 41:7241-7252.
7. Briand L, Nespoulous C, Perez V, Remy JJ, Huet JC, Pernollet JC. 2000. Ligand-binding properties and structural characterization of a novel rat odorant-binding protein variant. Eur J Biochem FEBS 267:3079-3089.
8. Brierley CH, Burchell B. 1993. Human UDP-glucuronosyl transferases: chemical defence, jaundice and gene therapy. Bioessays 15:749-754.
9. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-187.
10. Buck LB. 2005. Unraveling the sense of smell (Nobel lecture). Angew Chem (International ed) 44:6128-6140.
11. Charlier L, Cabrol-Bass D, Golebiowski J. 2009. How does human odorant binding protein bind odorants? The case of aldehydes studied by molecular dynamics. C R Chim 12:905-910.
12. Dahl AR. 1982. The inhibition of rat nasal cytochrome P-450-dependent mono-oxygenase by the essence heliotropin (piperonal). Drug Metab Dispos 10:553-554.
13. Debat H, Eloit C, Blon F, Sarazin B, Henry C, Huet JC, Trotier D, Pernollet JC. 2007. Identification of human olfactory cleft mucus proteins using proteomic analysis. J Proteome Res 6:1985-1996.
14. Ding X, Dahl A. 2003. Olfactory mucosa: composition, enzymatic localization and metabolism. Handbook of olfaction and gustation. New York: Marcel Dekker. p 51-73.
15. Ding XX, Porter TD, Peng HM, Coon MJ. 1991. cDNA and derived amino acid sequence of rabbit nasal cytochrome P450NMb (P450IIG1), a unique isozyme possibly involved in olfaction. Arch Biochem Biophys 285:120-125.
16. Flower DR. 1995. Multiple molecular recognition properties of the lipocalin protein family. J Mol Recognit 8:185-195.
17. Forstner M, Breer H, Krieger J. 2009. A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int J Biol Sci 5:745-757.
18. Genter MB, Krishan M, Augustine LM, Cherrington NJ. 2010. Drug transporter expression and localization in rat nasal respiratory and olfactory mucosa and olfactory bulb. Drug Metab Dispos 38:1644-1647.
19. Genter MB, Yost GS, Rettie AE. 2006. Localization of CYP4B1 in the rat nasal cavity and analysis of CYPs as secreted proteins. J Biochem Mol Toxicol 20:139-141.
20. Getchell ML, Chen Y, Ding X, Sparks DL, Getchell TV. 1993. Immunohistochemical localization of a cytochrome P-450 isozyme in human nasal mucosa: age-related trends. Ann Otol Rhinol Laryngol 102:368-374.
21. Golebiowski J, Antonczak S, Cabrol-Bass D. 2006. Molecular dynamics studies of odorant binding protein free of ligand and complexed to pyrazine and octenol. J Mol Struct Theochem 763:165-174.
22. Golebiowski J, Antonczak S, Fiorucci S, Cabrol-Bass D. 2007. Mechanistic events underlying odorant binding protein chemoreception. Proteins 67:448-458.
23. Golebiowski J, Topin J, Charlier L, Briand L. 2012. Interaction between odorants and proteins involved in the perception of smell: the case of odorant-binding proteins probed by molecular modelling and biophysical data. Flav Frag J 27:445-453.
24. Green N, Weech M, Walters E. 2005. Localization and characterization of glutathione-S-transferase isozymes alpha, mu, and pi within the mouse vomeronasal organ. Neurosci Lett 375:198-202.
25. Haberly LB. 2001. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551-576.
26. Hajjar E, Perahia D, Debat H, Nespoulous C, Robert CH. 2006. Odorant binding and conformational dynamics in the odorant-binding protein. J Biol Chem 281:29929-29937.
27. Hekmat-Scafe DS, Scafe CR, McKinney AJ, Tanouye MA. 2002. Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12:1357-1369.
28. Heydel JM, Holsztynska EJ, Legendre A, Thiebaud N, Artur Y, Le Bon AM. 2010. UDP-glucuronosyltransferases (UGTs) in neuro-olfactory tissues: expression, regulation, and function. Drug Metab Rev 42:71-94.
29. Heydel JM, Leclerc S, Bernard P, Pelczar H, Gradinaru D, Magdalou J, Minn A, Artur Y, Goudonnet H. 2001. Rat olfactory bulb and epithelium UDP-glucuronosyltransferase 2A1 (UGT2A1) expression: in situ mRNA localization and quantitative analysis. Brain Res 90:83-92.
30. Jedlitschky G, Burchell B, Keppler D. 2000. The multidrug resistance protein 5 functions as an ATP-dependent export pump for cyclic nucleotides. J Biol Chem 275:30069-30074.
31. Jedlitschky G, Cassidy AJ, Sales M, Pratt N, Burchell B. 1999. Cloning and characterization of a novel human olfactory UDP-glucuronosyltransferase. Biochem J 340 (Part 3):837-843.
32. Jones PM, George AM. 2004. The ABC transporter structure and mechanism: perspectives on recent research. Cell Mol Life Sci 61:682-699.
33. Kaissling KE. 2009. Olfactory perireceptor and receptor events in moths: a kinetic model revised. J Comp Physiol 195:895-922.
34. Kaler G, Truong DM, Sweeney DE, Logan DW, Nagle M, Wu W, Eraly SA, Nigam SK. 2006. Olfactory mucosa-expressed organic anion transporter, Oat6, manifests high affinity interactions with odorant organic anions. Biochem Biophys Res Commun 351:872-876.
35. Kudo H, Doi Y, Fujimoto S. 2010. Expressions of the multidrug resistance-related proteins in the rat olfactory epithelium: a possible role in the phase III xenobiotic metabolizing function. Neurosci Lett 468:98-101.
36. Kurosaki M, Terao M, Barzago MM, Bastone A, Bernardinello D, Salmona M, Garattini E. 2004. The aldehyde oxidase gene cluster in mice and rats. Aldehyde oxidase homologue 3, a novel member of the molybdo-flavoenzyme family with selective expression in the olfactory mucosa. J Biol Chem 279:50482-50498.
37. Laughlin JD, Ha TS, Jones DN, Smith DP. 2008. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133:1255-1265.
38. Lazard D, Zupko K, Poria Y, Nef P, Lazarovits J, Horn S, Khen M, Lancet D. 1991. Odorant signal termination by olfactory UDP glucuronosyl transferase. Nature 349:790-793.
39. Leclerc S, Heydel JM, Amosse V, Gradinaru D, Cattarelli M, Artur Y, Goudonnet H, Magdalou J, Netter P, Pelczar H, Minn A. 2002. Glucuronidation of odorant molecules in the rat olfactory system: activity, expression and age-linked modifications of UDP-glucuronosyltransferase isoforms, UGT1A6 and UGT2A1, and relation to mitral cell activity. Brain Res 107:201-213.
40. Lobel D, Jacob M, Volkner M, Breer H. 2002. Odorants of different chemical classes interact with distinct odorant binding protein subtypes. Chem Senses 27:39-44.
41. Lobel D, Marchese S, Krieger J, Pelosi P, Breer H. 1998. Subtypes of odorant-binding proteins-heterologous expression and ligand binding. Eur J Biochem FEBS 254:318-324.
42. Lobel D, Strotmann J, Jacob M, Breer H. 2001. Identification of a third rat odorant-binding protein (OBP3). Chem Senses 26:673-680.
43. Mayer U, Kuller A, Daiber PC, Neudorf I, Warnken U, Schnolzer M, Frings S, Mohrlen F. 2009. The proteome of rat olfactory sensory cilia. Proteomics 9:322-334.
44. Millery J, Briand L, Bezirard V, Blon F, Fenech C, Richard-Parpaillon L, Quennedey B, Pernollet JC, Gascuel J. 2005. Specific expression of olfactory binding protein in the aerial olfactory cavity of adult and developing Xenopus. Eur J Neurosci 22:1389-1399.
45. Minn AL, Leclerc S, Heydel JM, Minn AL, Denizcot C, Cattarelli M, Netter P, Gradinaru D. 2002. Drug transport into the mammalian brain: the nasal pathway and its specific metabolic barrier. J Drug Target 10:285-296.
46. Minn AL, Pelczar H, Denizot C, Martinet M, Heydel JM, Walther B, Minn A, Goudonnet H, Artur Y. 2005. Characterization of microsomal cytochrome P450-dependent monooxygenases in the rat olfactory mucosa. Drug Metab Dispos 33:1229-1237.
47. Monte JC, Nagle MA, Eraly SA, Nigam SK. 2004. Identification of a novel murine organic anion transporter family member, OAT6, expressed in olfactory mucosa. Biochem Biophys Res Commun 323:429-436.
48. Mori K, Nagao H, Yoshihara Y. 1999. The olfactory bulb: coding and processing of odor molecule information. Science 286:711-715.
49. Nagashima A, Touhara K. 2010. Enzymatic conversion of odorants in nasal mucus affects olfactory glomerular activation patterns and odor perception. J Neurosci 30:16391-16398.
50. Nagnan-Le Meillour P, Le Danvic C, Brimau F, Chemineau P, Michalski JC. 2009. Phosphorylation of native porcine olfactory binding proteins. J Chem Ecol 35:752-760.
51. Nef P, Heldman J, Lazard D, Margalit T, Jaye M, Hanukoglu I, Lancet D. 1989. Olfactory-specific cytochrome P-450. cDNA cloning of a novel neuroepithelial enzyme possibly involved in chemoreception. J Biol Chem 264:6780-6785.
52. Nespoulous C, Briand L, Delage MM, Tran V, Pernollet JC. 2004. Odorant binding and conformational changes of a rat odorant-binding protein. Chem Senses 29:189-198.
53. Neve EP, Ingelman-Sundberg M. 2000. Molecular basis for the transport of cytochrome P450 2E1 to the plasma membrane. J Biol Chem 275:17130-17135.
54. Pelosi P. 2001. The role of perireceptor events in vertebrate olfaction. Cell Mol Life Sci 58:503-509.
55. Pes D, Mameli M, Andreini I, Krieger J, Weber M, Breer H, Pelosi P. 1998. Cloning and expression of odorant-binding proteins Ia and Ib from mouse nasal tissue. Gene 212:49-55.
56. Rooney PH, Telfer C, McFadyen MC, Melvin WT, Murray GI. 2004. The role of cytochrome P450 in cytotoxic bioactivation: future therapeutic directions. Curr Cancer Drug Targets 4:257-265.
57. Sanz G, Schlegel C, Pernollet JC, Briand L. 2005. Comparison of odorant specificity of two human olfactory receptors from different phylogenetic classes and evidence for antagonism. Chem Senses 30:69-80.
58. Sassi Y, Lipskaia L, Vandecasteele G, Nikolaev VO, Hatem SN, Cohen Aubart F, Russel FG, Mougenot N, Vrignaud C, Lechat P, Lompre AM, Hulot JS. 2008. Multidrug resistance-associated protein 4 regulates cAMP-dependent signaling pathways and controls human and rat SMC proliferation. J Clin Invest 118:2747-2757.
59. Schilling B, Kaiser R, Natsch A, Gautschi M. 2010. Investigation of odors in the fragrance industry. Chemoecology 20:135-147.
60. Shepherd GM. 2004. The human sense of smell: are we better than we think? PLoS Biol 2:E146.
61. Shepherd GM. 2007. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad of Sci 1121:87-101.
62. Sten T, Bichlmaier I, Kuuranne T, Leinonen A, Yli-Kauhaluoma J, Finel M. 2009a. UDP-glucuronosyltransferases (UGTs) 2B7 and UGT2B17 display converse specificity in testosterone and epitestosterone glucuronidation, whereas UGT2A1 conjugates both androgens similarly. Drug Metab Dispos 37:417-423.
63. Sten T, Kurkela M, Kuuranne T, Leinonen A, Finel M. 2009b. UDP-glucuronosyltransferases in conjugation of 5alpha- and 5beta-androstane steroids. Drug Metab Dispos 37:2221-2227.
64. Stepanenko OV, Marabotti A, Kuznetsova IM, Turoverov KK, Fini C, Varriale A, Staiano M, Rossi M, D'Auria S. 2008. Hydrophobic interactions and ionic networks play an important role in thermal stability and denaturation mechanism of the porcine odorant-binding protein. Proteins 71:35-44.
65. Strotmann J, Breer H. 2011. Internalization of odorant-binding proteins into the mouse olfactory epithelium. Histochem Cell Biol 136:357-369.
66. Tamura HO, Harada Y, Miyawaki A, Mikoshiba K, Matsui M. 1998. Molecular cloning and expression of a cDNA encoding an olfactory-specific mouse phenol sulphotransferase. Biochem J 331 (Part 3):953-958.
67. Tcatchoff L, Nespoulous C, Pernollet JC, Briand L. 2006. A single lysyl residue defines the binding specificity of a human odorant-binding protein for aldehydes. FEBS Lett 580:2102-2108.
68. Tegoni M, Campanacci V, Cambillau C. 2004. Structural aspects of sexual attraction and chemical communication in insects. Trends Biochem Sci 29:257-264.
69. Tegoni M, Pelosi P, Vincent F, Spinelli S, Campanacci V, Grolli S, Ramoni R, Cambillau C. 2000. Mammalian odorant binding proteins. Biochim Biophy Acta 1482:229-240.
70. Tegoni M, Ramoni R, Bignetti E, Spinelli S, Cambillau C. 1996. Domain swapping creates a third putative combining site in bovine odorant binding protein dimer. Nat Struct Biol 3:863-867.
71. Thiebaud N, Menetrier F, Belloir C, Minn AL, Neiers F, Artur Y, Le Bon AM, Heydel JM. 2011. Expression and differential localization of xenobiotic transporters in the rat olfactory neuro-epithelium. Neurosci Lett 505:180-185.
72. Thiebaud N, Sigoillot M, Chevalier J, Artur Y, Heydel JM, Le Bon AM. 2010. Effects of typical inducers on olfactory xenobiotic-metabolizing enzyme, transporter, and transcription factor expression in rats. Drug Metab Dispos 38:1865-1875.
73. Thiebaud N, Veloso Da Silva S, Jakob I, Sicard G, Chevalier J, Ménétrier F, Berdeaux O, Artur Y, Heydel JM, Le Bon AM. 2013. Odorant metabolism catalyzed by olfactory mucosal enzymes influences peripheral olfactory responses in rats. PLoS ONE 8:e59547.
74. Thornton-Manning JR, Dahl AR. 1997. Metabolic capacity of nasal tissue interspecies comparisons of xenobiotic-metabolizing enzymes. Mutat Res 380:43-59.
75. Vidic J, Grosclaude J, Monnerie R, Persuy MA, Badonnel K, Baly C, Caillol M, Briand L, Salesse R, Pajot-Augy E. 2008. On a chip demonstration of a functional role for odorant binding protein in the preservation of olfactory receptor activity at high odorant concentration. Lab Chip 8:678-688.
76. Vincent F, Spinelli S, Ramoni R, Grolli S, Pelosi P, Cambillau C, Tegoni M. 2000. Complexes of porcine odorant binding protein with odorant molecules belonging to different chemical classes. J Mol Biol 300:127-139.
77. White SA, Briand L, Scott DJ, Borysik AJ. 2009. Structure of rat odorant-binding protein OBP1 at 1.6 A resolution. Acta Crystallogr 65:403-410.
78. Xu P, Atkinson R, Jones DN, Smith DP. 2005. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193-200.
79. Zupko K, Poria Y, Lancet D. 1991. Immunolocalization of cytochromes P-450olf1 and P-450olf2 in rat olfactory mucosa. Eur J Biochem 196:51-58.