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Anti-Inflammatory Remedy Frankincense the Functional Target

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Anti-Inflammatory Remedy Frankincense the Functional Target The Journal of Immunology Identification of Human Cathepsin G As a Functional Target of Boswellic Acids from the Anti-Inflammatory Remedy Frankincense1 Lars Tausch,* Arne Henkel,† Ulf Siemoneit,† Daniel Poeckel,† Nicole Kather,‡ Lutz Franke,§ Bettina Hofmann,§ Gisbert Schneider,§ Carlo Angioni,¶ Gerd Geisslinger,¶ Carsten Skarke,¶ Wolfgang Holtmeier,ʈ Tobias Beckhaus,* Michael Karas,* Johann Jauch,‡ and Oliver Werz2† Frankincense preparations, used in folk medicine to cure inflammatory diseases, showed anti-inflammatory effectiveness in animal models and clinical trials. Boswellic acids (BAs) constitute major pharmacological principles of frankincense, but their targets and the underlying molecular modes of action are still unclear. Using a BA-affinity Sepharose matrix, a 26-kDa protein was selectively precipitated from human neutrophils and identified as the lysosomal protease cathepsin G (catG) by mass spectrometry (MALDI- TOF) and by immunological analysis. In rigid automated molecular docking experiments BAs tightly bound to the active center of catG, occupying the same part of the binding site as the synthetic catG inhibitor JNJ-10311795 (2-[3-{methyl[1-(2-naphthoyl)pi- peridin-4-yl]amino}carbonyl)-2-naphthyl]-1-(1-naphthyl)-2-oxoethylphosphonic acid). BAs potently suppressed the proteolytic ac- ϳ tivity of catG (IC50 of 600 nM) in a competitive and reversible manner. Related serine proteases were significantly less sensitive against BAs (leukocyte elastase, chymotrypsin, proteinase-3) or not affected (tryptase, chymase). BAs inhibited chemoinvasion but not chemotaxis of challenged neutrophils, and they suppressed Ca2؉ mobilization in human platelets induced by isolated catG or by catG released from activated neutrophils. Finally, oral administration of defined frankincense extracts significantly reduced catG activities in human blood ex vivo vs placebo. In conclusion, we show that catG is a functional and pharmacologically relevant target of BAs, and interference with catG could explain some of the anti-inflammatory properties of frankincense. The Journal of Immunology, 2009, 183: 3433–3442. rankincense, the gum resin derived from Boswellia spe- Whereas 11-keto-␤-BA (KBA) and 3-O-acetyl-11-keto-␤-BA cies, is frequently used in folk medicine to cure inflam- (AKBA) were shown to exhibit numerous biological activities in F matory diseases. Data from animal models of inflam- vitro, the corresponding BAs lacking the 11-oxo moiety (i.e., mation and from clinical trials suggest a therapeutic value of ␤-BA and A␤-BA) are considered as less relevant. In particular, frankincense in the treatment of acute and chronic inflammatory AKBA is thought to be mainly responsible for the pharmacological and allergic disorders (1, 2). The pentacyclic triterpenes boswellic actions of frankincense (2). In search for a molecular basis of the acids (BAs)3 (see Fig. 1A) are major ingredients of frankincense. anti-inflammatory effectiveness, 5- and 12-lipoxygenase (1), cy- clooxygenase-1 (3), human leukocyte elastase (HLE) (4), and I␬B kinases (5) have been identified as possible targets of AKBA in *Institute of Pharmaceutical Chemistry, Johann Wolfgang Goethe-University Frank- biochemical and cellular in vitro models. However, due to the high furt, Frankfurt, Germany; †Department of Pharmaceutical Analytics, Pharmaceutical Institute, Eberhard-Karls-University Tuebingen, Tuebingen, Germany; ‡Organic concentrations required to interfere with these targets (IC50 of Chemistry II, University of Saarland, Saarbru¨cken, Germany; §Institut fu¨r Organische 1–50 ␮M) and the low maximal plasma levels of AKBA (Ͻ0.1 Chemie und Chemische Biologie/Zentrum fur Arzneimittelforschung, -Entwicklung ␮M) obtained after oral administration of standard doses of frank- und -Sicherheit, Johann Wolfgang Goethe-University Frankfurt, Frankfurt am Main, Germany; ¶Pharmazentrum Frankfurt, Zentrum fur Arzneimittelforschung, -Entwick- incense extracts (6), the pharmacological relevance of the pro- lung und -Sicherheit, Institut fu¨r Klinische Pharmakologie, Klinikum der Johann posed targets and mechanisms remain questionable (7). Wolfgang Goethe-Universita¨t, Frankfurt, Germany; and ʈDepartment of Gastroenter- ology, Medizinische Klinik 1, University Hospital, Frankfurt, Germany An elegant technique for the identification of a high-affinity Received for publication October 24, 2008. Accepted for publication July 6, 2009. small molecule (ligand)-protein (target) interaction is the protein- fishing approach, using an affinity matrix composed of the small The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance molecule covalently linked to an insoluble resin (8). Application of with 18 U.S.C. Section 1734 solely to indicate this fact. this strategy revealed human histone deacetylase as target for trap- 1 The financial support for this study by Pharmasan (Freiburg, Germany), Medeon oxin (9) or mTOR as target for the immunosuppressant rapamycin (Berlin, Germany), and by the Deutsche Forschungsgemeinschaft is acknowledged. (10). Using a BA-affinity Sepharose matrix and neutrophil lysates 2 Address correspondence and reprint requests to Dr. Oliver Werz, Department of as source of targets, we identified cathepsin G (catG) as a selected, Pharmaceutical Analytics, Pharmaceutical Institute, Eberhard-Karls-University Tu- ebingen, Auf der Morgenstelle 8, 72076 Tuebingen, Germany. E-mail address: high-affinity target for BAs. CatG, a neutral serine protease, is [email protected] mainly expressed in neutrophils, stored in azurophilic granules, 3 Abbreviations used in this paper: BA, ␤-boswellic acid; A␤-BA, 3-O-acetyl-␤- and released upon degranulation (11, 12). After release into the boswellic acid; AKBA, 3-O-acetyl-11-keto-␤-boswellic acid; catG, cathepsin G; JNJ-10311795, 2-[3-{methyl[1-(2-naphthoyl)piperidin-4-yl]amino}carbonyl)-2-naph- plasma, it cleaves extracellular matrix proteins, including laminin, thyl]-1-(1-naphthyl)-2-oxoethylphosphonic acid; HLE, human leukocyte elastase; proteoglycans, collagen, fibronectin, and elastin (13, 14), implying KBA, 11-keto-␤-boswellic acid; RMSD, root mean square deviation; SPR, surface a role in local destruction of connective tissue at sites of injury. plasmon resonance. CatG also processes chemokines (11, 15, 16), functioning as che- Copyright © 2009 by The American Association of Immunologists, Inc. 0022-1767/09/$2.00 moattractant for T cells and other leukocytes (17), and modulates www.jimmunol.org/cgi/doi/10.4049/jimmunol.0803574 3434 IDENTIFICATION OF CATHEPSIN G AS TARGET OF BOSWELLIC ACIDS integrin clustering on neutrophils (18). Moreover, catG stimulates In-gel digestion and MALDI-TOF-MS platelets via the protease-activated receptor-4 for aggregation and Protein bands were manually cut out and dissected gel pieces were sub- secretion (19) and acts as chemotactic agonist for the formyl pep- jected to in-gel digestion (24, 25), adapted for use on a Microlab STAR tide receptor on phagocytic leukocytes (20). Accordingly, catG digestion robot (26). Samples were reduced, alkylated, digested overnight inhibitors have been proposed to exhibit potential in treating cer- by trypsin, extracted, and the extracts were dried in a vacuum centrifuge. tain inflammatory disorders such as asthma, chronic obstructive MALDI-TOF-MS experiments were performed on an Ultraflex TOF/TOF mass spectrometer (Bruker Daltonics). The samples were dissolved in 5 ␮l pulmonary disease, emphysema, reperfusion injury, psoriasis, and of water/acetonitrile/TFA (29.5/70/0.5, v/v/v), and ␣-cyano-4-hydroxycin- rheumatoid arthritis (21). Since frankincense extracts showed ben- namic acid (3 mg/ml) was used as matrix. Analyte and matrix were spotted eficial effects in several of these disorders, interference of BAs consecutively in a 1:1 ratio on a stainless steel target and dried under with catG may possess pharmacological relevance. ambient conditions. The dried sample was washed with ice-cold 5% formic acid to reduce salt contamination. Spectra were externally calibrated with a Sequazyme peptide mass standards kit (Applied Biosystems) and inter- Materials and Methods nally calibrated on a tryptic auto digestion peptide (m/z of 2163.0564). The spectra were processed in flexAnalysis version 2.2 (Bruker Daltonics) us- Materials ing the SNAP algorithm (signal to noise threshold, 3; maximal number of BAs were prepared as described previously (22). ␣-Amyrin was from Ex- peaks, 150; quality factor threshold, 40). Proteins were identified by Mas- trasynthe`se; Boswellia serrata gum extract PS0201Bo was standardized to cot (Matrix Science) (peptide mass tolerance, 100 ppm; maximum missed at least 1% KBA and 1% AKBA (quantified by reversed phase HPLC) and cleavages using the NCBInr database: 2,314,886 sequences, 1,066,605,192 was provided by Pharmasan; EAH-Sepharose 4B, GE Healthcare Bio-Sci- total letters, date Jan. 26, 2005). Proteins with a score of 76 or higher were Ͻ ences; Abs against catG, BIOMOL; human catG, human tryptase, human considered significant ( p 0.05). chymase, human chymotrypsin, elastase inhibitor IV (N-(2-(4-(2,2-dimeth- ylpropionyloxy)phenylsulfonylamino)benzoyl)aminoacetic acid) and 2-[3- Purification of catG from neutrophils {methyl[1-(2-naphthoyl)piperidin-4-yl]amino}carbonyl)-2-naphthyl]-1-(1- Human neutrophils (2 ϫ 109) were suspended in ice-cold 0.15 M NaCl and naphthyl)-2-oxoethylphosphonic acid (JNJ-10311795), Calbiochem; human sonicated (five times for 30 s, 65%).
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