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Odorant-Binding Protein: Localization to Nasal Glands and Secretions (Olfaction/Mucus/Immunohistochemistry/Pyrazines) JONATHAN PEVSNER, PAMELA B

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Odorant-Binding Protein: Localization to Nasal Glands and Secretions (Olfaction/Mucus/Immunohistochemistry/Pyrazines) JONATHAN PEVSNER, PAMELA B Proc. Nail. Acad. Sci. USA Vol. 83, pp. 4942-4946, July 1986 Neurobiology Odorant-binding protein: Localization to nasal glands and secretions (olfaction/mucus/immunohistochemistry/pyrazines) JONATHAN PEVSNER, PAMELA B. SKLAR, AND SOLOMON H. SNYDER* Departments of Neuroscience, Pharmacology, and Experimental Therapeutics, Psychiatry, and Behavioral Sciences, Johns Hopkins University School of Medicine, 725 North Wolfe Street, Baltimore, MD 21205 Contributed by Solomon H. Snyder, January 6, 1986 ABSTRACT An odorant-binding protein (OBP) was iso- formed at an antiserum dilution of 1:8100 in 0.1 M Tris HCl, lated from bovine olfactory and respiratory mucosa. We have pH 8.0/0.5% Triton X-100, in a final vol of50 A.l. Incubations produced polyclonal antisera to this protein and report its were carried out at 370C for 90 min with 35,000 cpm of immunohistochemical localization to mucus-secreting glands of '251-labeled OBP per tube. Immunoprecipitation was accom- the olfactory and respiratory mucosa. Although OBP was plished by using 25 1LI of 5% Staphylococcus aureus cells originally isolated as a pyrazine binding protein, both rat and (Calbiochem) in 0.1 M Tris HCl (pH 8.0) at 370C for 30 min. bovine OBP also bind the odorants [3H]methyldihydrojasmon- Bound 1251I-labeled OBP was separated from free OBP by ate and 3,7-dimethyl-octan-1-ol as well as 2-isobutyl-3-[3HI filtration over glass fiber filters (No. 32, Schleicher & methoxypyrazine. We detect substantial odorant-binding ac- Schuell) pretreated with 10% fetal bovine serum, using a tivity attributable to OBP in secreted rat nasal mucus and tears Brandel cell harvester (Brandel, Gaithersburg, MD). In but not in saliva, suggesting a role for OBP in transporting or typical experiments, maximal and nonspecific binding were concentrating odorants. 30% and 2% of added radioactivity, respectively. Immunoblots. Whole bovine nasal epithelia were homog- In an effort to clarify molecular mechanisms of olfaction, enized in buffer A (50 mM Tris HCl, pH 7.6/1 mM EDTA) several groups have examined the binding of radioactive and filtered over cheesecloth. Samples of purified OBP, odorants to nasal mucosa (1-6). Recently, we purified to bovine serum albumin, and nasal homogenates prepared in homogeneity an odorant-binding protein based on its inter- buffer A were electrophoresed into 14% NaDodSO4/poly- actions with the potent odorant 2-isobutyl-3-[3H]methoxy- acrylamide gels. Transfer of proteins to nitrocellulose was pyrazine ([3H]IBMP) (7), a finding obtained independently by accomplished in 12 hr at 60 V (11). The nitrocellulose was Bignetti et al. (8). Odorant-binding protein (OBP) is a soluble incubated for 12 hr in buffer A supplemented with 0.1% dimeric protein with subunits of =19 kDa. OBP may have a gelatin and 0.1% Triton X-100 to decrease nonspecific staini- selective function in olfaction, since it occurs in nasal mucosa ing. Immunoblots were incubated with a 1:1000 dilution of and not in other tissues, and the relative potencies of a antisera for 2 hr as indicated in Fig. 2. Antisera were pre- homologous series of pyrazine derivatives in competing for adsorbed for 24 hr at 40C with either bovine serum albumin the binding sites parallels their potencies as odorants. or purified bovine OBP that had been further purified by We have produced antisera to bovine OBP and now report HPLC (see below). Immunoblots were developed by using the immunohistochemical localization ofOBP to bovine nasal the avidin/biotin/peroxidase technique (Vector Laborato- glands, which secrete mucus. Odorant-binding studies dem- ries, Burlingame, CA) with 4-chloro-1-naphthol and hydro- onstrate high levels of OBP in rat nasal mucus and tears, gen peroxide as substrates. suggesting a role for OBP in concentrating odorants from the Immunohistochemistry. Whole bovine nasal epithelia were air. obtained immediately after slaughter and were fixed in i% glutaraldehyde in 0.15 M sodium phosphate buffer (pH 7.4) MATERIALS AND METHODS for 2 hr. Tissue was embedded in a mixture of 50% brain Materials. [3H]IBMP (43.8 Ci/mmol; 1 Ci = 37 GBq), paste/50% Tissue-Tek (Miles Scientific, Naperville, IL) and 2-[3H]methoxypyrazine (63.6 Ci/mmol), and [pentyl-2,3- rapidly frozen. Cryostat tissue sections (8 ,um) were cut with 3H]methyldihydrojasmonate ([3H]MDHJ; 65.5 Ci/mmol) a microtome and immunohistochemically stained with the were prepared by New England Nuclear Dupont. 3,7-Di- avidin/biotin/peroxidase complex technique (Vector Labo- methyl[6,7(N)-3H]octan-1-ol ([3H]DMO; 57 Ci/mmol), ratories) using diaminobenzidine and hydrogen peroxide as [amyl-3H]isoamyl acetate (49 Ci/mmol), and [3H]isovaleric substrates (12-14). Tissue sections were incubated with a acid (4-[2,3(n)3H]methylbutanoic acid; 52 Ci/mmol) were 1:20,000 dilution of antisera against either bovine OBP, prepared by Amersham. Unlabeled odorants were from bovine serum albumin (Sigma), or normal rabbit serum for 48 International Flavors and Fragrances (Union Beach, NJ) or hr at 4°C. Additional sections were counterstained with Pyrazine Specialties (Atlanta, GA). Protein molecular size toluidine blue. markers were obtained from Bio-Rad. All other reagents Purification and Characterization of Bovine OBP and Rat were from commercial sources. Mucus OBP. Bovine OBP was purified from bovine olfactory Preparation of Antibodies to OBP and Radioimmunoassays. and respiratory epithelium as described (7) by sequential Bovine OBP was purified as described (7), and antibodies to centrifugation; ammonium sulfate fractionation; and DEAE- this protein were raised by standard techniques (9). Bovine cellulose, hydroxylapatite, and gel filtration chromatogra- OBP was iodinated with lodo-Beads (Pierce) according to the method of Markwell (10). Radioimmunoassays were per- Abbreviations: IBMP, 2-isobutyl-3-methoxypyrazine; MDHJ, methyldihydrojasmonate (3-oxo-2-pentyl-cyclopentane-acetic acid The publication costs of this article were defrayed in part by page charge methyl ester); DMO, 3,7-dimethyl-octan-1-ol; OBP, odorant-binding payment. This article must therefore be hereby marked "advertisement" protein. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 4942 Downloaded by guest on September 25, 2021 Neurobiology: Pevsner et al. Proc. Natl. Acad. Sci. USA 83 (1986) 4943 phy. A single protein was purified from rat olfactory and respiratory epithelium by using the same purification proce- dure. Purified bovine OBP and proteins present in crude rat mucus were separated by HPLC on a Vydac C4 protein column (4.6 x 200 mm; 5-gim particle size) (15). The column was equilibrated with 0.1% (vol/vol) aqueous trifluoroacetic o 1: acid, and the samples were loaded in the same solvent. After x a 5-min wash, the proteins were eluted with a linear gradient E of 0-100% organic solvent over 40 min [0.1% (vol/vol) CL trifluoroacetic acid in acetonitrile/n-propanol (2:1)]. Proteins 0 were analyzed by NaDodSO4/PAGE (16) on 14% polyacryl- a E C- amide gels in the presence of 2-mercaptoethanol and were 0 ._-- .0 stained with Coomassie brilliant blue. Protein was deter- 0 mined according to the method of Bradford (17) using bovine 0- serum albumin as a standard. .0 Odorant Binding to Secretions from Rat. Male Sprague- Dawley rats (6-10 weeks old) were anesthetized with sodium Cu I pentobarbital (60 mg/kg, i.p.) and injected with isoproterenol ct (30 mg/kg, i.p.) to induce secretions (18-20). After 5 min, secreted nasal mucus, tears, and saliva were collected with 5-,41 or 100-gl glass micropipettes. Mucus was collected from the external nares and tears were collected from the puncta. Typically, 10 Al of nasal mucus, 20 Al of tears, and 200 A.l of saliva were obtained from a single rat in 1 hr. Fraction Binding assays were performed by filtration over polyeth- ylenimine-coated filters as described (7). Assay mixtures FIG. 1. Partial purification of OBP from bovine and rat nasal typically contain secretions (2-20 jig of protein), 3-25 nM epithelium by DEAE-cellulose chromatography. After ammonium radioactive odorant, and unlabeled odorants in a final vol of sulfate fractionation, bovine (A) or rat (B) protein was dialyzed and 100 ,ul, and they were incubated at 4°C for 1 hr. applied to a DEAE-cellulose column with a linear NaCl gradient In Vivo Binding of Individual male (0-400 mM NaCl; bovine OBP elutes at 330 mM NaCl; rat binding [3H]DMO. Sprague- protein elutes at 270 mM NaCl). All fractions were assayed for the Dawley rats were anesthetized and injected with isoproter- binding activities of [3H]DMO (8 nM), [3H]IBMP (10 nM), and enol as described above. Two minutes after the isoproterenol [3H]MDHJ (6 nM). All three odorants bind with a single major peak injection, a polypropylene test tube (1.5 ml capacity) con- of binding activity. Binding of [3H]amyl acetate and 2-[3H]methoxy- taining 50 ,Ci in 50 ,ul of [3H]DMO was positioned around the pyrazine also reveal single peaks of binding activity (not shown). animal's nose, eyes, or mouth for 3 min. Secretions were Data are from a single experiment. collected and assayed for protein content. Labeled odorant present in the mucus or saliva was measured by liquid DEAE-cellulose chromatography, column fractions were scintillation spectrometry. Radioactivity bound to protein assayed for the binding of four tritiated odorants. A single was measured by filtration (as described above) within 1 min major peak of activity was found (Fig. 1A). Using the same of collection of the secretions. techniques, we have purified an OBP from rat olfactory and respiratory epithelium. DEAE-cellulose chromatography re- RESULTS veals a single peak of binding activity (Fig. 1B) and the purified protein has an apparent subunit molecular size of 21 Odorant Binding to Purified Bovine OBP.
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