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Evaluation of Fumagilin-B® and Other Potential Alternative Chemotherapies Against Nosema Ceranae-Infected Honeybees (Apis Mellifera) in Cage Trial Assays Johan P

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Evaluation of Fumagilin-B® and Other Potential Alternative Chemotherapies Against Nosema Ceranae-Infected Honeybees (Apis Mellifera) in Cage Trial Assays Johan P View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Archive Ouverte en Sciences de l'Information et de la Communication Evaluation of Fumagilin-B® and other potential alternative chemotherapies against Nosema ceranae-infected honeybees (Apis mellifera) in cage trial assays Johan P. van den Heever, Thomas S. Thompson, Simon J. G. Otto, Jonathan M. Curtis, Abdullah Ibrahim, Stephen F. Pernal To cite this version: Johan P. van den Heever, Thomas S. Thompson, Simon J. G. Otto, Jonathan M. Curtis, Abdullah Ibrahim, et al.. Evaluation of Fumagilin-B® and other potential alternative chemotherapies against Nosema ceranae-infected honeybees (Apis mellifera) in cage trial assays. Apidologie, Springer Verlag, 2016, 47 (5), pp.617-630. 10.1007/s13592-015-0409-3. hal-01532347 HAL Id: hal-01532347 https://hal.archives-ouvertes.fr/hal-01532347 Submitted on 2 Jun 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2016) 47:617–630 Original article * INRA, DIB and Springer-Verlag France, 2015 DOI: 10.1007/s13592-015-0409-3 Evaluation of Fumagilin-B® and other potential alternative chemotherapies against Nosema ceranae -infected honeybees (Apis mellifera ) in cage trial assays 1 1 1,2 Johan P. VA N D EN HEEVER , Thomas S. THOMPSON , Simon J. G. OTTO , 3 4 4 Jonathan M. CURTIS , Abdullah IBRAHIM , Stephen F. PERNAL 1Alberta Agriculture and Forestry, Food Safety Division, Agri-Food Laboratories Branch, 6909-116 Street, Edmonton, Alberta T6H 4P2, Canada 2School of Public Health, University of Alberta, Edmonton, Alberta T6G 1C9, Canada 3Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta T6G 2P5, Canada 4Agriculture and Agri-Food Canada, Beaverlodge Research Farm, P.O. Box 29, Beaverlodge, Alberta T0H 0C0, Canada Received 5 May 2015 – Revised 30 September 2015 – Accepted 5 November 2015 Abstract – Fumagilin-B® is the only currently registered chemical treatment available to combat nosema disease in apiculture. Fumagillol, the basic hydrolysis product of fumagillin, two semisynthetic fumagillin analogues, and four in-house purely synthetic compounds which were designed to mimic the mode of action of fumagillin against the methionine aminopeptidase type 2 (MetAP-2) enzyme, was observed to exhibit statistically significant biological activity against Nosema ceranae -infected caged bees. None of these compounds were, however, as effective as Fumagilin-B®. The commercially available thymol and enilconazole also exhibited activity against N. ceranae , with thymol being the most promising chemical treatment other than Fumagilin-B®.Highcumulativebeemortalitywas associated with the therapeutic dosage of Fumagilin-B® during our study, suggesting the need for continued investigation. Fumagilin-B® / fumagillin / dicyclohexylamine / DCH / analogues / apiculture 1. INTRODUCTION Hernández et al. 2007; Higes et al. 2008, 2009; vanEngelsdorp et al. 2009). Fumagilin-B® is the Nosema disease of honeybees, Apis mellifera only currently available registered chemotherapy L., is caused by infection from two distinct species available to treat nosema disease in North America of single-cellular microsporidian fungal parasites, (Williams et al. 2011) and is reportedly allowed for Nosema apis (Zander 1909)andNosema ceranae use in special circumstances in Spain, the Balkans, (Fries et al. 1996). Infections of N. ceranae have and other parts of Europe (Stevanović et al. 2013). been shown to cause high levels of colony loss in The commercial products (Fumagilin-B® and some regions, while both species have been im- Fumidil-B®) both contain the therapeutic plicated as part of the pathogen complex associ- fumagillin as the dicyclohexylamine (DCH) salt. ated with the colony collapse disorder (CCD) This results in both compounds (fumagillin and phenomenon (Cox-Foster et al. 2007; Martín- DCH) being administered in equimolar quantities when using either of the commercial formulations. DCH is reportedly five times as toxic to mice as fumagillin, and the reader is referred to a recent Corresponding author: J. van den Heever, review where the relative toxicities of these two [email protected] compounds are discussed in greater detail (van den Manuscript editor: David Tarpy Heever et al. 2014). Fumagilin-B® (and the 618 J.P. van den Heever et al. equivalent Fumidil-B®) has been continuously cyclohexane skeleton of fumagillin with the intact employed to treat both N. apis and N. ceranae spiro-epoxide was used as a template for the de- ever since the discovery (Hanson and Eble 1949) sign and synthesis of several semisynthetic com- of fumagillin, when it was found to be effective in pounds and synthetic compounds aimed at controlling N. apis infections in honeybees targeting the MetAP-2 enzyme in N. ceranae . (Katznelson and Jamieson 1952;Bailey1953). These compounds, as well as other commercially Fumagillin and its analogues inhibit the forma- available chemicals that reportedly exhibited ac- tion of new blood vessels around tumors (angio- tivity against nosema disease, were evaluated for genesis), thereby limiting the blood supply to disease suppression and adult bee survival using tumors and thus impeding their growth (Ingber cage trial assays. et al. 1990). Fumagillin covalently binds to a histidine moiety (His231) within the enzymatic 2. MATERIALS AND METHODS active site of the methionine aminopeptidase type 2 (MetAP-2) enzyme (Griffith et al. 1997; Sin 2.1. Reagents and materials et al. 1997; Liu et al. 1998; Zhang et al. 2002). resulting in the irreversible opening of the spiro- Trimethylsulfoxonium iodide (catalog no. T80500), epoxide group on the core cyclohexane skeleton N ,N ′-dicyclohexylcarbodiimide (catalog no. D80002), of fumagillin. This spiro-epoxide is reportedly 4-(dimethylamino) pyridine (catalog no. 107700), ace- responsible for the biological activity of tyl salicylic acid (catalog no. A5376), piperonylic acid fumagillin, since opening of the epoxide by ther- (catalog no. P49805), thymol (catalog no. T0501), mal decomposition leads to the loss of biological carbendazim (catalog no. 378674), toltrazuril (catalog activity (Griffith et al. 1997, 1998; Kochansky no. 34000), thiabendazole (catalog no. T8904), and and Nasr 2004). enilconazole (also known as imazalil or chloramizole, MetAP-2 enzymes are ubiquitous in eukaryotic catalog no. Y0000136) were all purchased from Sigma- organisms, including the host honeybee and the Aldrich (St. Louis, MO, USA). Nozevit solution, a disease-causative N. apis and N. ceranae (Zhang natural plant polyphenol extract, was obtained from et al. 2002; Huang et al. 2013). Comparison of the Complete Bee (AK, USA). Fumagilin-B® was obtained MetAP-2 enzyme binding site amino acid se- from Medivet Pharmaceuticals Ltd. (High River, AB, quences among humans and A. mellifera shows Canada). identical protein sequences, while sequences dif- fer by only two amino acids when comparing 2.2. General synthetic methodology N. apis and N. ceranae (Huang et al. 2013). Numerous research efforts have been aimed at Fumagillol was prepared by basic hydrolysis of modulating the mode of action of fumagillin by Fumagilin-B® (Figure 1) according to Assil and Sporns synthesizing analogues that replace the alkene (1991). Oxidation of alcohols to their corresponding side chain (Han et al. 2000; Baldwin et al. 2002; ketone compounds was performed using established Chen et al. 2009; Balthaser et al. 2011) in attempts methodology (Dess and Martin 1991). The esterifica- to reduce the cytotoxicity of fumagillin while tion of alcohols with carboxylic acids (Figure 2), as well retaining its beneficial properties. The alkene side as epoxidation of ketones (Figure 3), is described below. chain can be removed by basic hydrolysis, yield- The identity of all the synthesized compounds was ing the alcohol, fumagillol (Tarbell et al. 1961; verified by high-resolution mass spectrometry on an Gochnauer and Furgala 1962; Assil and Sporns Agilent 6224 time of flight (TOF) mass spectrometer 1991). Chemical moieties such as carboxylic (Table I). acids can then be coupled to fumagillol, resulting in new semisynthetic fumagillin analogues. 2.2.1. Ester synthesis We postulated that the known mode of action of fumagillin against the MetAP-2 enzyme in The Steglich esterification (Figure 2) was used to humans is similar for MetAP-2 enzymes found prepare esters from the corresponding carboxylic in N. apis and in N. ceranae .Assuch,thecore acids and alcohols (Neises and Steglich 1978). The Evaluation of Fumagilin-B® and other potential alternative chemotherapies 619 O O O OH OMe O H N H O O OMe O OH O a b c Figure 1. The commercial Fumagilin-B®, consisting of fumagillin (a ) as the dicyclohexylamine (b ) salt, which can be hydrolyzed to afford the alcohol, fumagillol (c ). general procedure involved stirring a solution of the 2.2.2. Epoxide formation from ketones carboxylic acid (10 mmol) in anhydrous CH2Cl2 (10 mL). The catalyst, dimethylaminopyridine A modified version of the Corey-Chaykovsky
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