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Allergen Expression of Procalin, a Major Triatomine Identification

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Allergen Expression of Procalin, a Major Triatomine Identification Identification, Cloning, and Recombinant Expression of Procalin, a Major Triatomine Allergen This information is current as Christopher D. Paddock, James H. McKerrow, Elizabeth of September 24, 2021. Hansell, K. W. Foreman, Ivy Hsieh and Neal Marshall J Immunol 2001; 167:2694-2699; ; doi: 10.4049/jimmunol.167.5.2694 http://www.jimmunol.org/content/167/5/2694 Downloaded from References This article cites 33 articles, 11 of which you can access for free at: http://www.jimmunol.org/content/167/5/2694.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 24, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2001 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Identification, Cloning, and Recombinant Expression of Procalin, a Major Triatomine Allergen1 Christopher D. Paddock,* James H. McKerrow,2†§ Elizabeth Hansell,† K. W. Foreman,‡ Ivy Hsieh,† and Neal Marshall¶ Among the most frequent anaphylactic reactions to insects are those attributed to reduviid bugs. We report the purification and identification of the major salivary allergen of these insects. This 20-kDa protein (procalin) is a member of the lipocalin family, which includes salivary allergens from other invertebrates and mammals. An expression system capable of producing reagent quantities of recombinant allergen was developed in Saccharomyces cerevisiae. Antisera produced against recombinant protein cross-reacts with ELISA with salivary allergen. Recombinant Ag is also shown to react with sera from an allergic patient but not with control sera. By immunolocalization, the source of the salivary Ag is the salivary gland epithelium and its secretions. The Journal of Immunology, 2001, 167: 2694–2699. Downloaded from mong the most frequently reported anaphylactic reac- indicate that ϳ89% of the allergenic activity in the saliva of this tions to biting insects are those attributed to a small but bug represents reaction to a 18- to 20-kDa protein (14). We now A medically important group of hematophagous bugs that report the purification of this major allergenic protein and isolation comprise the subfamily Triatominae (Heteroptera:Reduviidae) (1). of a cDNA clone. Successful expression of recombinant Ag in Although best known as arthropod vectors of Chagas disease, these yeast provides reagent quantities of Ag for subsequent investiga- http://www.jimmunol.org/ insects also inject salivary proteins during the acquisition of a tions of the serologic diagnosis, epidemiology, and desensitization blood meal that may initiate a variety of severe and occasionally therapy of individuals at risk of severe allergic reaction to the bite fatal allergic responses in sensitized individuals. Systemic reac- of T. protracta. We also predict the functional and primary aller- tions include generalized pruritis, gastrointestinal disturbances, fe- genic residues in procalin through sequence analysis and structural ver, dyspnea, syncope, hypotension, laryngeal and glossal edema, models. and convulsions (2–6). Extreme hypersensitivity resulting in death has been attributed to the bite of Triatoma protracta (6). Materials and Methods In the U.S., allergic reactions have been associated with T. pro- Ag purification and amino-terminal sequence analysis tracta, T. rubida, T. recurva, T. sanguisuga, T. gerstaekeri, and by guest on September 24, 2021 Paratriatoma hirsuta (6, 7). Allergic sensitization, demonstrated Paired salivary glands were dissected from 50 fourth-instar T. protracta nymphs and suspended in PBS (pH 7.4). Extracts were filtered through a by anti-Triatoma IgE Ab, may develop in as many as 7% of in- 0.2-␮m cellulose acetate membrane, dialyzed with a 6-kDa cutoff, and dividuals residing within the range of these insects (7). The ex- initially fractionated by fast protein liquid chromatography on a MonoQ pansion in both seasonal and perennial human incursions into HR5/5 (Pharmacia, Uppsala, Sweden) cationic exchange column. The sam- chaparral or woodland habitats of T. protracta in the western U.S. ple was loaded in 20 mM Tris-HCl (pH 7.4) and eluted with an NaCl gradient (0–1 M). One-milliliter fractions were collected from a flow rate has increased the number of persons at risk for Triatoma hyper- of 1 ml/min. Three immunologically active fractions were identified by sensitivity; it is estimated that as many as 30,000 persons in Cal- ELISA, using banked serum samples from patients with confirmed allergy ifornia are at risk for anaphylaxis from this insect (7). to T. protracta (7), and a goat anti-human IgG-HRP conjugate (Boehringer Isolation of proteins from the saliva of several species of Tri- Mannheim, Mannheim, Germany). Sera were obtained from four patients atominae, and characterization of the antihemostatic properties of all of whom had at least three life-threatening episodes of anaphylaxis. Ag-containing fractions were purified by using an HPLC system (Rainin these proteins, has been the subject of many recent investigations Instruments, Emeryville, CA) with a variable wavelength monitor (Knauer, (8–13). However, little is known about the molecular identity of Berlin, Germany). Ag-containing fractions were applied to a C8 peptide salivary allergens of these insects. Initial studies with T. protracta reverse-phase column (4.6 ϫ 250 mm; Vydac, Hesperia, CA) in 0.05% trifluoroacetic acid (TFA3; Sigma, St. Louis, MO) and eluted with a 50% methanol/50% water/0.5% TFA gradient (0–100% in 30 min). One-milli- liter fractions were collected and analyzed by ELISA and SDS-PAGE. The *Viral and Rickettsial Zoonoses Branch, Centers for Disease Control and Prevention, Atlanta, GA 30333; Departments of †Pathology and ‡Pharmaceutical Chemistry, Uni- purified 20-kDa Ag was stored at 4°C for 24 h to allow the TFA to evap- versity of California, and §Department of Veterans Affairs Medical Center, San Fran- orate before Edman degradation for N-terminal sequence analysis by using cisco, CA 94121; and ¶Department of Natural Sciences, Notre Dame de Namur Uni- a 470A protein sequencer (Applied Biosystems, Foster City, CA) with an versity, Belmont, CA 94002 on-line 120A phenylthiohydantoin analyzer (Applied Biosystems). Received for publication November 22, 2000. Accepted for publication June 20, 2001. Isolation and cloning of Triatoma allergen cDNA The costs of publication of this article were defrayed in part by the payment of page A 32-fold degenerate oligonucleotide primer (5Ј-ACAGAATTCCA(A/G) charges. This article must therefore be hereby marked advertisement in accordance AA(A/G)CC(T/G)AA(A/G)CC(T/G)ATGGA-3Ј) was deduced from with 18 U.S.C. Section 1734 solely to indicate this fact. amino acid residues 4–10 of the amino-terminal sequence of the purified 1 C.D.P. was supported in this work by a Research Training Fellowship provided by Ag. RNA from two pairs of nymphal T. protracta salivary glands was the Department of Pathology, University of California (San Francisco, CA). J.H.M. is extracted in RNAzol B (Biotecx Laboratories, Houston, TX) and reverse supported by a Burroughs Wellcome Scholar Award in Molecular Parasitology. 2 Address correspondence and reprint requests to Dr. James H. McKerrow, Depart- ment of Pathology, University of California, Box 0506, San Francisco, CA 94143. 3 Abbreviations used in this paper: TFA, trifluoroacetic acid; BLAST, basic local E-mail address: [email protected] alignment search tool. Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 The Journal of Immunology 2695 transcribed by using 400 U Moloney murine leukemia virus reverse tran- ELISA with human sera scriptase (Life Technologies, Gaithersburg, MD) and the primer 5Ј- ACAATCGATAAGCTTTTTTTTTTTTTTTTT-3Ј. First-strand cDNA Recombinant procalin (Tpa-2) was coated onto 96-well polystyrene en- ␮ was amplified by using PCR. One micromolar of each of the above primers zyme immunoassay plates (Costar, Cambridge, MA) at 1 or 10 ng/ lin50 ␮ were used in a 50-␮l reaction mixture containing 10 mM Tris-HCl (pH l of PBS (0.001 M KH2PO4,0.01MNa2HPO4, 0.137 M NaCl, 0.0027 M KCl (pH 7.4)) at 4°C overnight. The wells were rinsed, and then the re- 8.3), 50 mM KCl, 1.5 mM MgCl2, 0.2 mM of each dNTP, and 1.25 U Taq DNA polymerase (Boehringer Mannheim). A total of 45 cycles were per- maining sites were blocked by incubation at room temperature for 2 h with ␮ formed by using a DNA thermal cycler (PerkinElmer Cetus, Norwalk, CT). 100 l 0.05% Tween 20, 1% BSA in PBS. Serial dilutions of human sera The first two cycles were performed with annealing at 35°C for 2 min, from a known allergic patient (positive toward T. protracta extract) and control human sera were made in blocking buffer (after clearing sera by denaturing at 94°C for 1 min, and extension at 72°C for 2 min. For the ϫ ␮ subsequent 43 cycles, annealing occurred at 50°C for 2 min, denaturing at centrifugation for 4 min at 16,000 g). Then 50 l of each dilution was 94°C for 1 min, and extension at 72°C for 2 min. The amplified product incubated with the recombinant Tpa-2-coated wells for1hatroom tem- perature. The rinsed wells were then incubated for1hatroom temperature was gel-purified, electro-eluted in a Spectra/Por molecular porous dialysis ␮ membrane (Spectrum Medical Industries, Houston, TX), and subcloned with 100 l of an alkaline phosphatase-labeled secondary Ab to human into the EcoRI and HindIII sites of pBluescript (Stratagene, La Jolla, CA).
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