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Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31165–31174 | Cite as

Evaluation of (–)-borneol derivatives against the Zika vector, Aedes aegypti and a non-target species, Artemia sp.

  • Rafaela K. V. Nunes
  • Ulisses N. Martins
  • Thaysnara B. Brito
  • Angelita Nepel
  • Emmanoel V. Costa
  • Andersson Barison
  • Roseli L. C. Santos
  • Sócrates C. H. Cavalcanti
Research Article

Abstract

Zika, dengue, and chikungunya are vector-borne diseases of pronounced concern transmitted by the mosquito Aedes aegypti Linn. (Diptera: Culicidae). The most important method to avoid outbreaks is to control mosquito spreading by the employment of insecticides and larvicides. Failure to control mosquito dispersal is mostly accounted to Ae. aegypti resistance to currently available larvicides and insecticides, encouraging the development of novel pesticides. In addition, the excessive use of larvicides poses serious threats to human health and the environment. Evaluation of natural products as larvicides in an attempt to overcome this situation is often found in the literature because products originated from nature are considered less toxic to non-target species and more eco-friendly. (–)-Borneol is a bicyclic monoterpene present in essential oils with moderate larvicidal activity. On account of these facts, it was of our interest to synthesize (–)-borneol ester derivatives aiming to study its structure-activity relationships against Ae. aegypti larvae. With the goal to estimate toxicity to a non-target species, evaluation of the lethal concentration 50% (LC50) on Artemia sp. (Artemiidae) and calculation of selectivity towards Ae. aegypti were carried out. The most potent derivative, (–)-Bornyl chloroacetate, exhibited the highest suitability index, demonstrating lower environmental toxicity than other borneol ester derivatives. A parabolic relationship between (–)-borneol esters larvicidal activity and partition coefficient (Log P) was achieved and a correlation equation obtained, validating the importance of lipophilicity to the larvicidal activity of these compounds.

Keywords

Dengue Larvicidal activity Microcephaly Terpenes QSAR Borneol esters 

Notes

Acknowledgements

The authors would like to acknowledge the Brazilian National Scientific and Development Council (CNPq) for supporting grant number 47601/2013-2. We also extend our gratefulness to Norberto Peporine Lopes and Jose Carlos Tomaz for mass spectra analyses.

Supplementary material

11356_2018_2809_MOESM1_ESM.docx (46 kb)
ESM 1 (DOCX 46 kb)

References

  1. Abe FR, Coleone AC, Machado AA, Machado-Neto JG (2014) Ecotoxicity and environmental risk assessment of larvicides used in the control of Aedes aegypti to Daphnia magna (Crustacea, Cladocera). J Toxicol Environ Health A 77:37–45.  https://doi.org/10.1080/15287394.2014.865581 CrossRefGoogle Scholar
  2. Acerson MJ, Bingham BS, Allred CA, Andrus MB (2015) Design and synthesis of terpene based englerin A mimics using chromium oxide mediated remote CH2 oxidation. Tetrahedron Lett 56:3277–3280.  https://doi.org/10.1016/j.tetlet.2015.02.071 CrossRefGoogle Scholar
  3. Alencar-Filho EB, Silva JWC, Cavalcanti SCH (2016) Quantitative structure-toxicity relationships and molecular highlights about Aedes aegypti larvicidal activity of monoterpenes and related compounds. Med Chem Res 25:2171–2178.  https://doi.org/10.1007/s00044-016-1650-7 CrossRefGoogle Scholar
  4. Alves PB, Freire-Filho PS, Moraes VRS et al (2007) Chemical composition of essential oil from seven Ocimum basilicum L. accessions, brine shrimp lethality bioassay and inhibitory activities against GAPDH and APRT. J Essent Oil Res 19:89–92.  https://doi.org/10.1080/10412905.2007.9699236 CrossRefGoogle Scholar
  5. Araújo H, Carvalho D, Ioshino R, Costa-da-Silva A, Capurro M (2015) Aedes aegypti Control Strategies in Brazil: Incorporation of New Technologies to Overcome the Persistence of Dengue Epidemics. Insects 6(2):576-594CrossRefGoogle Scholar
  6. Barbosa JDF, Silva VB, Alves PB, Gumina G, Santos RLC, Sousa DP, Cavalcanti SCH (2012) Structure-activity relationships of eugenol derivatives against Aedes aegypti (Diptera: Culicidae) larvae. Pest Manag Sci 68:1478–1483.  https://doi.org/10.1002/ps.3331 CrossRefGoogle Scholar
  7. Benelli G, Mehlhorn H (2016) Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitol Res 115:1747–1754.  https://doi.org/10.1007/s00436-016-4971-z CrossRefGoogle Scholar
  8. Benelli G, Romano D (2017) Mosquito vectors of Zika virus. Entomol Gen 36:309–318.  https://doi.org/10.1127/entomologia/2017/0496 CrossRefGoogle Scholar
  9. Benelli G, Pavela R, Canale A, Cianfaglione K, Ciaschetti G, Conti F, Nicoletti M, Senthil-Nathan S, Mehlhorn H, Maggi F (2017) Acute larvicidal toxicity of five essential oils (Pinus nigra, Hyssopus officinalis, Satureja montana, Aloysia citrodora and Pelargonium graveolens) against the filariasis vector Culex quinquefasciatus: synergistic and antagonistic effects. Parasitol Int 66:166–171.  https://doi.org/10.1016/j.parint.2017.01.012 CrossRefGoogle Scholar
  10. Benelli G, Maggi F, Pavela R, Murugan K, Govindarajan M, Vaseeharan B, Petrelli R, Cappellacci L, Kumar S, Hofer A, Youssefi MR, Alarfaj AA, Hwang J-S, Higuchi A (2018) Mosquito control with green nanopesticides: towards the One Health approach? A review of non-target effects. Environ Sci Pollut Res 25(11):10184-10206CrossRefGoogle Scholar
  11. Burke DM, Mayer RT (1983) Differential effects of phenobarbitone and 3-methylcholanthrene induction on the hepatic microsomal metabolism and cytochrome P-450-binding of phenoxazone and a homologous series of its n-alkyl ethers (alkoxyresorufins). Chem Biol Interact 45:243–258.  https://doi.org/10.1016/0009-2797(83)90072-8 CrossRefGoogle Scholar
  12. Capeding MR, Tran NH, Hadinegoro SRS, Ismail HIHJM, Chotpitayasunondh T, Chua MN, Luong CQ, Rusmil K, Wirawan DN, Nallusamy R, Pitisuttithum P, Thisyakorn U, Yoon IK, van der Vliet D, Langevin E, Laot T, Hutagalung Y, Frago C, Boaz M, Wartel TA, Tornieporth NG, Saville M, Bouckenooghe A (2014) Clinical efficacy and safety of a novel tetravalent dengue vaccine in healthy children in Asia: a phase 3, randomised, observer-masked, placebo-controlled trial. Lancet 384:1358–1365.  https://doi.org/10.1016/S0140-6736(14)61060-6 CrossRefGoogle Scholar
  13. Catelan TBS, Arruda EJ, Oliveira LCS et al (2015) Evaluation of toxicity of phenolic compounds using Aedes aegypti (Diptera: Culicidae) and Artemia salina. Adv Infect Dis 05:48–56.  https://doi.org/10.4236/aid.2015.51005 CrossRefGoogle Scholar
  14. Cauchemez S, Besnard M, Bompard P, Dub T, Guillemette-Artur P, Eyrolle-Guignot D, Salje H, van Kerkhove MD, Abadie V, Garel C, Fontanet A, Mallet HP (2016) Association between Zika virus and microcephaly in French Polynesia, 2013-15: a retrospective study. Lancet 387:2125–2132.  https://doi.org/10.1016/S0140-6736(16)00651-6 CrossRefGoogle Scholar
  15. Corte RL, Melo VAD, Dolabella SS, Marteis LS (2018) Variation in temephos resistance in field populations of Aedes aegypti (Diptera: Culicidae) in the State of Sergipe, Northeast Brazil. Rev Soc Bras Med Trop 51:In press.  https://doi.org/10.1590/0037-8682-0449-2017 CrossRefGoogle Scholar
  16. Cristani M, D’Arrigo M, Mandalari G et al (2007) Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J Agric Food Chem 55:6300–6308.  https://doi.org/10.1021/jf070094x CrossRefGoogle Scholar
  17. Deo PG, Hasan SB, Majumder SK (1988) Toxicity and suitability of some insecticides for household use. Int Pest Control 30:118–121Google Scholar
  18. Finney DJ (1971) Probit analysis, third edn. University Press, CambridgeGoogle Scholar
  19. Gamal ZA (2012) Effectiveness of Gambusia holbrooki fish in domestic water containers and controlling Aedes aegypti larvae (Linnaeus, 1762) in southwest Saudi Arabia (Jeddah). J Egypt Soc Parasitol 240:1–10.  https://doi.org/10.12816/0006289 CrossRefGoogle Scholar
  20. Gartenstein S, Quinnell RG, Larkum AWD (2006) Toxicity effects of diflubenzuron, cypermethrin and diazinon on the development of Artemia salina and Heliocidaris Tuberculata. Australas J Ecotoxicol 12:83–90Google Scholar
  21. Gilliom J, Barbash, JE, Martin JD, et al (2017) Pesticides in the nation’s streams and ground water, 1992–2001, U.S. Department of the Interior. U.S. geological survey. Circular 1291Google Scholar
  22. Govindarajan M, Benelli G (2016) Eco-friendly larvicides from Indian plants: effectiveness of lavandulyl acetate and bicyclogermacrene on malaria, dengue and Japanese encephalitis mosquito vectors. Ecotoxicol Environ Saf 133:395–402.  https://doi.org/10.1016/j.ecoenv.2016.07.035 CrossRefGoogle Scholar
  23. Govindarajan M, Rajeswary M, Senthilmurugan S, Vijayan P, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2018a) Curzerene, trans-β-elemenone, and γ-elemene as effective larvicides against Anopheles subpictus, Aedes albopictus, and Culex tritaeniorhynchus: toxicity on non-target aquatic predators. Environ Sci Pollut Res Int 25:10272–10282.  https://doi.org/10.1007/s11356-017-8822-y CrossRefGoogle Scholar
  24. Govindarajan M, Vaseeharan B, Alharbi NS, Kadaikunnan S, Khaled JM, al-anbr MN, Alyahya SA, Maggi F, Benelli G (2018b) High efficacy of Z-γ-bisabolene from the essential oil of Galinsoga parviflora (Asteraceae) as larvicide and oviposition deterrent against six mosquito vectors. Environ Sci Pollut Res 25:10555–10566.  https://doi.org/10.1007/s11356-018-1203-3 CrossRefGoogle Scholar
  25. Grover S, Boyé O, Getahun Z, Brossi A, Hamel E (1992) Chloroacetates of 2- and 3-demethylthiocolchicine: specific covalent interactions with tubulin with preferential labeling of the β-subunit. Biochem Biophys Res Commun 187:1350–1358.  https://doi.org/10.1016/0006-291X(92)90451-P CrossRefGoogle Scholar
  26. Hansch C, Verma RP (2009) Larvicidal activities of some organotin compounds on mosquito larvae: a QSAR study. Eur J Med Chem 44:260–273.  https://doi.org/10.1016/j.ejmech.2008.02.040 CrossRefGoogle Scholar
  27. He K, Shi G, Zeng L, Ye Q, McLaughlin J (1997) Konishiol, a new sesquiterpene, and bioactive components from Cunninghamia konishii. Planta Med 63:158–160.  https://doi.org/10.1055/s-2006-957635 CrossRefGoogle Scholar
  28. Kiviranta J, Abdel-Hameed A, Sivonen K, Niemelä SI, Carlberg G (1993) Toxicity of cyanobacteria to mosquito larvae—screening of active compounds. Environ Toxicol Water Qual 8:63–71.  https://doi.org/10.1002/tox.2530080107 CrossRefGoogle Scholar
  29. Lau KW, Chen CD, Lee HL, Norma-Rashid Y, Sofian-Azirun M (2015) Evaluation of insect growth regulators against field-collected Aedes aegypti and Aedes albopictus (Diptera: Culicidae) from Malaysia. J Med Entomol 52:199–206.  https://doi.org/10.1093/jme/tju019 CrossRefGoogle Scholar
  30. Lee SJ, Kim JH, Lee SC (2018) Effects of oil-film layer and surfactant on the siphonal respiration and survivorship in the fourth instar larvae of Aedes togoi mosquito in laboratory conditions. Sci Rep 8:5694.  https://doi.org/10.1038/s41598-018-23980-5 CrossRefGoogle Scholar
  31. Lewis DFV, Lake BG, Dickins M (2004) Quantitative structure-activity relationships within a homologous series of 7-alkoxyresorufins exhibiting activity towards CYP1A and CYP2B enzymes: molecular modelling studies on key members of the resorufin series with CYP2C5-derived models of human CYP1A1, CYP1A2, CYP2B6 and CYP3A4. Xenobiotica 34:501–513.  https://doi.org/10.1080/00498250410001691316 CrossRefGoogle Scholar
  32. López MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crop Prod 31:284–288.  https://doi.org/10.1016/j.indcrop.2009.11.005 CrossRefGoogle Scholar
  33. Lu Y, Xu XL, Meng C, Zhou JQ, Sheng JJ, Wu CK, Xu SW (2013) The toxicity assay of Artemia salina as a biological model for the preliminary toxic evaluation of chemical pollutants. Adv Mater Res 726–731:230–233.  https://doi.org/10.4028/www.scientific.net/AMR.726-731.230 CrossRefGoogle Scholar
  34. Lucia A, Zerba E, Masuh H (2013) Knockdown and larvicidal activity of six monoterpenes against Aedes aegypti (Diptera: Culicidae) and their structure-activity relationships. Parasitol Res 112:4267–4272.  https://doi.org/10.1007/s00436-013-3618-6 CrossRefGoogle Scholar
  35. Marcelino PRF, Silva VL, Philippini RR et al (2017) Biosurfactants produced by Scheffersomyces stipitis cultured in sugarcane bagasse hydrolysate as new green larvicides for the control of Aedes aegypti, a vector of neglected tropical diseases. PLoS One 12:e0187125.  https://doi.org/10.1371/journal.pone.0187125 CrossRefGoogle Scholar
  36. Minguez L, Pedelucq J, Farcy E, Ballandonne C, Budzinski H, Halm-Lemeille MP (2016) Toxicities of 48 pharmaceuticals and their freshwater and marine environmental assessment in northwestern France. Environ Sci Pollut Res 23:4992–5001.  https://doi.org/10.1007/s11356-014-3662-5 CrossRefGoogle Scholar
  37. Miron D, Battisti F, Silva FK, Lana AD, Pippi B, Casanova B, Gnoatto S, Fuentefria A, Mayorga P, Schapoval EES (2014) Antifungal activity and mechanism of action of monoterpenes against dermatophytes and yeasts. Rev Bras Farmacogn 24:660–667.  https://doi.org/10.1016/j.bjp.2014.10.014 CrossRefGoogle Scholar
  38. Monnerat RG, Dumas V, Ramos F et al (2012) Evaluation of different larvicides for the control of Aedes aegypti (Linnaeus) (Diptera: Culicidae) under simulated field conditions. BioAssay 7:1–4CrossRefGoogle Scholar
  39. Murugan K, Murugan P, Noortheen A (2007) Larvicidal and repellent potential of Albizzia amara Boivin and Ocimum basilicum Linn against dengue vector, Aedes aegypti (Insecta: Diptera: Culicidae). Bioresour Technol 98:198–201.  https://doi.org/10.1016/j.biortech.2005.12.009 CrossRefGoogle Scholar
  40. Nanyonga SK, Opoku Y, Lewu FB et al (2013) Chemical composition, antioxidant activity and cytotoxicity of the essential oils of the leaves and stem of Tarchonanthus camphoratus. Afr J Pharm Pharmacol 7:360–367.  https://doi.org/10.5897/AJPP12.600 CrossRefGoogle Scholar
  41. Nascimento AM, Maia TD, Soares TE et al (2017) Repellency and larvicidal activity of essential oils from Xylopia laevigata, Xylopia frutescens, Lippia pedunculosa, and their individual compounds against Aedes aegypti Linnaeus. Neotrop Entomol 46:223–230.  https://doi.org/10.1007/s13744-016-0457-z CrossRefGoogle Scholar
  42. Pavela R (2009) Larvicidal property of essential oils against Culex quinquefasciatus Say (Diptera: Culicidae). Ind Crop Prod 30:311–315.  https://doi.org/10.1016/j.indcrop.2009.06.005 CrossRefGoogle Scholar
  43. Pavela R (2015a) Essential oils for the development of eco-friendly mosquito larvicides: a review. Ind Crop Prod 76:174–187.  https://doi.org/10.1016/j.indcrop.2015.06.050 CrossRefGoogle Scholar
  44. Pavela R (2015b) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus say larvae. Parasitol Res 114:3835–3853.  https://doi.org/10.1007/s00436-015-4614-9 CrossRefGoogle Scholar
  45. Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007.  https://doi.org/10.1016/j.tplants.2016.10.005 CrossRefGoogle Scholar
  46. Perumalsamy H, Kim N-J, Ahn Y-J (2009) Larvicidal activity of compounds isolated from Asarum heterotropoides against Culex pipiens pallens, Aedes aegypti, and Ochlerotatus togoi (Diptera: Culicidae). J Med Entomol 46:1420–1423CrossRefGoogle Scholar
  47. Picollo MI, Toloza AC, Mougabure Cueto G, Zygadlo J, Zerba E (2008) Anticholinesterase and pediculicidal activities of monoterpenoids. Fitoterapia 79:271–278.  https://doi.org/10.1016/j.fitote.2008.01.005 CrossRefGoogle Scholar
  48. Pirsaheb M, Hossini H, Asadi F, Janjani H (2017) A systematic review on organochlorine and organophosphorus pesticides content in water resources. Toxin Rev 36:210–221.  https://doi.org/10.1080/15569543.2016.1269810 CrossRefGoogle Scholar
  49. Poupardin R, Srisukontarat W, Yunta C, Ranson H (2014) Identification of carboxylesterase genes implicated in temephos resistance in the dengue vector Aedes aegypti. PLoS Negl Trop Dis 8:1–11.  https://doi.org/10.1371/journal.pntd.0002743 CrossRefGoogle Scholar
  50. Radwan MA, El-Zemity SR, Mohamed SA, Sherby SM (2008) Larvicidal activity of some essential oils, monoterpenoids and their corresponding N-methyl carbamate derivatives against Culex pipiens (Diptera: Culicidae). Int J Trop Insect Sci 28:61–68.  https://doi.org/10.1017/S1742758408962366 CrossRefGoogle Scholar
  51. Rajeswary M, Govindarajan M, Alharbi NS, Kadaikunnan S, Khaled JM, Benelli G (2018) Zingiber cernuum (Zingiberaceae) essential oil as effective larvicide and oviposition deterrent on six mosquito vectors, with little non-target toxicity on four aquatic mosquito predators. Environ Sci Pollut Res 25:10307–10316.  https://doi.org/10.1007/s11356-017-9093-3 CrossRefGoogle Scholar
  52. Rajkumar S, Jebanesan A (2010) Chemical composition and larvicidal activity of leaf essential oil from Clausena dentata (Willd) M. Roam. (Rutaceae) against the chikungunya vector, Aedes aegypti Linn. (Diptera: Culicidae). J Asia Pac Entomol 13:107–109.  https://doi.org/10.1016/j.aspen.2010.02.001 CrossRefGoogle Scholar
  53. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR (2016) Zika virus and birth defects—reviewing the evidence for causality. N Engl J Med 374:1981–1987.  https://doi.org/10.1056/NEJMsr1604338 CrossRefGoogle Scholar
  54. Saavedra-Rodriguez K, Strode C, Flores AE, Garcia-Luna S, Reyes-Solis G, Ranson H, Hemingway J, Black WC IV (2014) Differential transcription profiles in Aedes aegypti detoxification genes following temephos selection. Insect Mol Biol 23:199–215.  https://doi.org/10.1111/imb.12073 CrossRefGoogle Scholar
  55. Santos SRL, Silva VB, Melo MA, Barbosa JDF, Santos RLC, de Sousa DP, Cavalcanti SCH (2010) Toxic effects on and structure-toxicity relationships of phenylpropanoids, terpenes, and related compounds in Aedes aegypti larvae. Vector-Borne Zoonotic Dis 10:1049–1054.  https://doi.org/10.1089/vbz.2009.0158 CrossRefGoogle Scholar
  56. Santos SRL, Melo MA, Cardoso AV, Santos RLC, de Sousa DP, Cavalcanti SCH (2011) Structure-activity relationships of larvicidal monoterpenes and derivatives against Aedes aegypti Linn. Chemosphere 84:150–153.  https://doi.org/10.1016/j.chemosphere.2011.02.018 CrossRefGoogle Scholar
  57. Santos VSV, Caixeta ES, Campos EO Jr, Pereira BB (2017) Ecotoxicological effects of larvicide used in the control of Aedes aegypti on nontarget organisms: redefining the use of pyriproxyfen. J Toxicol Environ Health A 80:155–160.  https://doi.org/10.1080/15287394.2016.1266721 CrossRefGoogle Scholar
  58. Scotti L, Scotti MT, Silva VB, Santos S, Cavalcanti S, Junior F (2014) Chemometric studies on potential larvicidal compounds against Aedes aegypti. Med Chem 10:201–210.  https://doi.org/10.2174/15734064113099990005 CrossRefGoogle Scholar
  59. Shrivastava SR, Shrivastava PS, Ramasamy J (2017) Potential risk of Zika virus outbreak in the European region: public health alert. Ann Trop Med Public Health 10:764–765.  https://doi.org/10.4103/1755-6783.213140 CrossRefGoogle Scholar
  60. Silva JJ, Mendes J (2007) Susceptibility of Aedes aegypti (L) to the insect growth regulators diflubenzuron and methoprene in Uberlandia, State of Minas Gerais. Rev Soc Bras Med Trop 40:612–616.  https://doi.org/10.1590/S0037-86822007000600002 CrossRefGoogle Scholar
  61. Silva WJ, Dória GAA, Maia RT, Nunes RS, Carvalho GA, Blank AF, Alves PB, Marçal RM, Cavalcanti SCH (2008) Effects of essential oils on Aedes aegypti larvae: alternatives to environmentally safe insecticides. Bioresour Technol 99:3251–3255.  https://doi.org/10.1016/j.biortech.2007.05.064 CrossRefGoogle Scholar
  62. Silva VB, Travassos DL, Nepel A, Barison A, Costa EV, Scotti L, Scotti MT, Mendonça-Junior FJB, la Corte Dos Santos R, de Holanda Cavalcanti SC (2017) Synthesis and chemometrics of thymol and carvacrol derivatives as larvicides against Aedes aegypti. J Arthropod-Borne Dis 11:315–330Google Scholar
  63. Songa EA, Okonkwo JO (2016) Recent approaches to improving selectivity and sensitivity of enzyme-based biosensors for organophosphorus pesticides: a review. Talanta 155:289–304.  https://doi.org/10.1016/j.talanta.2016.04.046 CrossRefGoogle Scholar
  64. Stevenson PC, Isman MB, Belmain SR (2017) Pesticidal plants in Africa: a global vision of new biological control products from local uses. Ind Crop Prod 110:2–9.  https://doi.org/10.1016/j.indcrop.2017.08.034 CrossRefGoogle Scholar
  65. Vanhaecke P (1981) Report on an intercalibration exercise on a short-term standard toxicity test with Artemia nauplii (ARC-test). INSERM 106:359–376Google Scholar
  66. Vehovszky Á, Farkas A, Ács A, Stoliar O, Székács A, Mörtl M, Győri J (2015) Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system. Aquat Toxicol 167:172–179.  https://doi.org/10.1016/j.aquatox.2015.08.009 CrossRefGoogle Scholar
  67. Volpe PLO (1997) Flow microcalorimetric measurements of the antibacterial activity of the homologous series m-alkoxyphenols and p-hydroxybenzoates on Escherichia coli. J Braz Chem Soc 8:1–6.  https://doi.org/10.1590/S0103-50531997000400005 CrossRefGoogle Scholar
  68. Weerasinghe AJ, Wickramasinghe A, Carr G et al (2015) Gardinerin, a biologically active acetogenin from the Sri Lankan Goniothalamus gardineri Hook. F. and Thomson. Int J Pharm Pharm Sci 7:459–461Google Scholar
  69. Yourno J, Mastropaolo W (1981) Nonspecific esterases of the formed elements: zymograms produced by pH 9.5 polyacrylamide gel electrophoresis. Blood 58:939–946Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rafaela K. V. Nunes
    • 1
  • Ulisses N. Martins
    • 1
  • Thaysnara B. Brito
    • 1
  • Angelita Nepel
    • 2
  • Emmanoel V. Costa
    • 3
  • Andersson Barison
    • 2
  • Roseli L. C. Santos
    • 4
  • Sócrates C. H. Cavalcanti
    • 1
  1. 1.Medicinal Chemistry Laboratory, Pharmacy DepartmentFederal University of SergipeSão CristóvãoBrazil
  2. 2.Nuclear Magnetic Resonance Laboratory, Chemistry DepartmentFederal University of ParanáCuritibaBrazil
  3. 3.Chemistry Department, Institute of Applied SciencesFederal University of AmazonasManausBrazil
  4. 4.Parasitology Laboratory, Morphology DepartmentFederal University of SergipeSão CristóvãoBrazil

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