Antibacterial activity of monoacetylated alkyl gallates against Xanthomonas citri subsp. citri

Archiv für Mikrobiologie - Tập 200 - Trang 929-937 - 2018
Abigail Savietto1, Carlos Roberto Polaquini2, Malgorzata Kopacz3, Dirk-Jan Scheffers3, Beatriz Carvalho Marques2, Luís Octavio Regasini2, Henrique Ferreira1
1Departamento de Bioquímica e Microbiologia, Instituto de Biociências, Universidade Estadual Paulista, Rio Claro, Brazil
2Departamento de Química e Ciências Ambientais, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista, São José do Rio Preto, Brazil
3Department of Molecular Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Groningen, The Netherlands

Tóm tắt

Asiatic citrus canker (ACC) is an incurable disease of citrus plants caused by the Gram-negative bacterium Xanthomonas citri subsp. citri (X. citri). It affects all the commercially important citrus varieties in the major orange producing areas around the world. Control of the pathogen requires recurrent sprays of copper formulations that accumulate in soil and water reservoirs. Here, we describe the improvement of the alkyl gallates, which are potent anti-X. citri compounds, intended to be used as alternatives to copper in the control of ACC. Acetylation of alkyl gallates increased their lipophilicity, which resulted in potentiation of the antibacterial activity. X. citri exposed to the acetylated compounds exhibited increased cell length that is consistent with the disruption of the cell division apparatus. Finally, we show that inhibition of cell division is an indirect effect that seemed to be caused by membrane permeabilization, which is apparently the primary target of the acetylated alkyl gallates.

Tài liệu tham khảo

Beaumont K, Webster R, Gardner I, Dack K (2003) Design of ester prodrugs to enhance oral absorption of poorly permeable compounds: challenges to the discovery scientist. Curr Drug Metab 4:461–485 Behlau F, Belasque J Jr, Bergamin Filho A, Graham JH, Leite RP Jr, Gottwald TR (2008) Copper sprays and windbreaks for control of citrus canker on young orange trees in southern. Braz Crop Prot 27:807–813. https://doi.org/10.1016/j.cropro.2007.11.008 Behlau F, Amorim L, Belasque J, Bergamin Filho A, Leite RP, Graham JH, Gottwald TR (2010) Annual and polyetic progression of citrus canker on trees protected with copper sprays. Plant Pathol 59:1031–1036. https://doi.org/10.1111/j.1365-3059.2010.02344.x Behlau F, Canteros BI, Jones JB, Graham JH (2012) Copper resistance genes from different xanthomonads and citrus epiphytic bacteria confer resistance to Xanthomonas citri subsp. citri. Eur J Plant Pathol 133:949–963. https://doi.org/10.1007/s10658-012-9966-8 Belasque J Jr, Behlau F (2011) Current status of citrus canker control in São Paulo state Brazil: a new chapter in a 50-year book? In: Ferreira H, Belasque J Jr (eds) Proceedings of the International Workshop on Xanthomonas citri/citrus canker. UNESP/Fundecitrus, Ribeirão Preto. http://lgb.rc.unesp.br/wxc/workshop_Xanthomonas_final.pdf Belasque J Jr, Fernandes NG, Massari CA (2009) The Success of erradication campaign os citrus canker in São Paulo States. Braz Summa Phytopathol 35:91–92 Biasutto L, Marotta E, De Marchi U, Zoratti M, Paradisi C (2007) Ester-based precursors to increase the bioavailability of quercetin. J Med Chem 50:241–253. https://doi.org/10.1021/jm060912x Bock CH, Parker PE, Gottwald TR (2005) Effect of simulated wind-driven rain on duration and distance of dispersal of Xanthomonas axonopodis pv. citri from canker-infected citrus trees. Plant Dis 89:71–80 Brunetto G et al (2016) Copper accumulation in vineyard soils: Rhizosphere processes and agronomic practices to limit its toxicity. Chemosphere 162:293–307. https://doi.org/10.1016/j.chemosphere.2016.07.104 Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4:141–157. https://doi.org/10.1046/j.1364-3703.2003.00163.x Canteros BI (1999) Copper resistance in Xanthomonas campestris pv. citri. In: Mahadevan A (ed) Plant pathogenic bacteria. Proceedings of the International Society of Bacteriology, Centre for Advanced Study in Botany. University of Madras, Chennai, India, pp 455–459 Changtam C, Hongmanee P, Suksamrarn A (2010) Isoxazole analogs of curcuminoids with highly potent multidrug-resistant antimycobacterial activity. Eur J Med Chem 45:4446–4457. https://doi.org/10.1016/j.ejmech.2010.07.003 Cornu JY, Huguenot D, Jezequel K, Lollier M, Lebeau T (2017) Bioremediation of copper-contaminated soils by bacteria. World J Microbiol Biotechnol 33:26. https://doi.org/10.1007/s11274-016-2191-4 da Silva AC et al (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–463. https://doi.org/10.1038/417459a Dahan A, Beig A, Lindley D, Miller JM (2016) The solubility-permeability interplay and oral drug formulation design: two heads are better than one. Adv Drug Deliv Rev 101:99–107. https://doi.org/10.1016/j.addr.2016.04.018 del Campo R, Russi P, Mara P, Mara H, Peyrou M, de Leon IP, Gaggero C (2009) Xanthomonas axonopodis pv. citri enters the VBNC state after copper treatment and retains its virulence FEMS. Microbiol Lett 298:143–148 (Epub 2009 Jun 2026) Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74:504–528 Ettmayer P, Amidon GL, Clement B, Testa B (2004) Lessons learned from marketed and investigational prodrugs. J Med Chem 47:2393–2404. https://doi.org/10.1021/jm0303812 Fones H, Preston GM (2013) The impact of transition metals on bacterial plant disease. FEMS Microbiol Rev 37:495–519. https://doi.org/10.1111/1574-6976.12004 Gottwald TR, Graham JH, Schubert TS (2002) Citrus canker: the pathogen and its impact. Online Plant Health Progress. https://doi.org/10.1094/PHP-2002-0812-01-RV Han HK, Amidon GL (2000) Targeted prodrug design to optimize drug delivery. AAPS PharmSci 2:E6 Hurley KA, Santos TMA, Nepomuceno GM, Huynh V, Shaw JT, Weibel DB (2016) Targeting the bacterial division protein FtsZ. J Med Chem. https://doi.org/10.1021/acs.jmedchem.5b01098 Krol E, de Sousa Borges A, da Silva I, Polaquini CR, Regasini LO, Ferreira H, Scheffers DJ (2015) Antibacterial activity of alkyl gallates is a combination of direct targeting of FtsZ and permeabilization of bacterial membranes. Front Microbiol 6:390. https://doi.org/10.3389/fmicb.2015.00390 Król E, de Sousa Borges A, da Silva I, Polaquini CR, Regasini LO, Ferreira H, Scheffers DJ (2015) Antibacterial activity of alkyl gallates is a combination of direct targeting of FtsZ and permeabilization of bacterial membranes. Front Microbiol 6:1–12. https://doi.org/10.3389/fmicb.2015.00390 Leite RP Jr, Mohan SK (1990) Integrated management of the citrus bacterial canker disease caused by Xanthomonas campestris pv. citri in the State of Paraná. Braz Crop Prot 9:3–7. https://doi.org/10.1016/0261-2194(90)90038-9 Lipinski CA (2000) Drug-like properties and the causes of poor solubility and poor permeability. J Pharmacol Toxicol Methods 44:235–249 Martins PM, Lau IF, Bacci M, Belasque J, do Amaral AM, Taboga SR, Ferreira H (2010) Subcellular localization of proteins labeled with GFP in Xanthomonas citri ssp. citri: targeting the division septum. FEMS Microbiol Lett 310:76–83. https://doi.org/10.1111/j.1574-6968.2010.02047.x NCCLS (2003) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard—6th edn. NCCLS document M7-A6. NCCLS, Wayne, PA. ISBN 1-56238-486-4 Rautio J, Kumpulainen H, Heimbach T, Oliyai R, Oh D, Jarvinen T, Savolainen J (2008) Prodrugs: design and clinical applications. Nat Rev Drug Discov 7:255–270. https://doi.org/10.1038/nrd2468 Rosso R, Vieira TO, Leal PC, Nunes RJ, Yunes RA, Creczynski-Pasa TB (2006) Relationship between the lipophilicity of gallic acid n-alquil esters' derivatives and both myeloperoxidase activity and HOCl scavenging. Bioorg Med Chem 14:6409–6413 Sardi JCO et al (2017) Antibacterial activity of diacetylcurcumin against Staphylococcus aureus results in decreased biofilm and cellular adhesion. J Med Microbiol 66:816–824. https://doi.org/10.1099/jmm.0.000494 Schaad NW et al (2006) Emended classification of xanthomonad pathogens on citrus. Syst Appl Microbiol 29:690–695 Silva IC et al (2013) Antibacterial activity of alkyl gallates against Xanthomonas citri subsp. citri. J Bacteriol 195:85–94. https://doi.org/10.1128/JB.01442-12 Silva IC, Polaquini CR, Regasini LO, Ferreira H, Pavan FR (2017) Evaluation of cytotoxic, apoptotic, mutagenic, and chemopreventive activities of semi-synthetic esters of gallic acid food and chemical toxicology: an international journal published for the British industrial. Biol Res Assoc 105:300–307. https://doi.org/10.1016/j.fct.2017.04.033 Strahl H, Hamoen LW (2010) Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 107:12281–12286. https://doi.org/10.1073/pnas.1005485107 Vlachogianni IC, Fragopoulou E, Kostakis IK, Antonopoulou S (2015) In vitro assessment of antioxidant activity of tyrosol, resveratrol and their acetylated derivatives. Food Chem 177:165–173. https://doi.org/10.1016/j.foodchem.2014.12.092 Zhang H, Lu X, Zhang Y, Ma X, Wang S, Ni Y, Chen J (2016) Bioaccumulation of organochlorine pesticides and polychlorinated biphenyls by loaches living in rice paddy fields of. Northeast China Environ Pollut 216:893–901. https://doi.org/10.1016/j.envpol.2016.06.064