Schinus terebinthifolius Leaf extract causes midgut damage, interfering with survival and development of Aedes aegypti larvae

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Procópio, Thamara Figueiredo ^a   Fernandes, Kenner Morais ^b   Pontual, Emmanuel Viana ^a,c   Ximenes, Rafael Matos ^d   De Oliveira, Aline Rafaella Cardoso ^a   Souza, Carolina De Santana ^a   De Albuquerque Melo, Ana Maria Mendonça ^a   Navarro, Daniela Maria Do Amaral Ferraz ^e   Paiva, Patrí Maria Guedes ^a   Martins, Gustavo Ferreira ^b   Napoleão, Thiago Henrique ^a  

^a DEPARTAMENTO DE MICOLOGIA   (Brazil)

^b FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^c UNIVERSIDADE FEDERAL RURAL DE PERNAMBUCO   (Brazil)

^d FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^e DEPARTAMENTO DE QUÍMICA FUNDAMENTAL   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CINNAMIC ACID DERIVATIVE; DNA FRAGMENT; FLAVONOID; HETEROSID; LECTIN; PLANT EXTRACT; PLANT MEDICINAL PRODUCT; PROANTHOCYANIDIN DERIVATIVE; SCHINUS TEREBINTHIFOLIUS EXTRACT; STEROID; TANNIN DERIVATIVE; UNCLASSIFIED DRUG; CINNAMIC ACID;

ADULT; AEDES AEGYPTI; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTEMIA SALINA; ARTHROPOD LARVA; ARTICLE; CELL DAMAGE; CELL PROLIFERATION; CELL VACUOLE; CONTROLLED STUDY; DRUG IDENTIFICATION; LARVAL DEVELOPMENT; LC50; MICROVILLUS; MIDGUT; NONHUMAN; PHYTOCHEMISTRY; PLANT LEAF; SCHINUS TEREBINTHIFOLIUS; SURVIVAL; TREE; AEDES; ANACARDIACEAE; ANIMAL; CHEMISTRY; DNA FRAGMENTATION; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; INTESTINE; ISOLATION AND PURIFICATION; LARVA; METABOLISM; PATHOLOGY; SOLID PHASE EXTRACTION; TRANSMISSION ELECTRON MICROSCOPY;

AEDES AEGYPTI; ARTEMIA SALINA; SCHINUS TEREBINTHIFOLIUS;

AEDES; ANACARDIACEAE; ANIMALS; CINNAMATES; DNA FRAGMENTATION; FLAVONOIDS; INTESTINES; LARVA; LECTINS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; PLANT EXTRACTS; PLANT LEAVES; SOLID PHASE EXTRACTION;

EID: 84929376784     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126612     Document Type: Article

References (63)

1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, et al. The global distribution and burden of dengue. Nature. 2013; 496: 504-507. doi: 10.1038/nature12060 PMID: 23563266
2. World Health Organization (2014) Dengue and severe dengue. Fact sheet No 117.
3. Maciel-de-Freitas R, Avendanho FC, Santos R, Sylvestre G, Araújo SC, Lima JBP, et al. Undesirable consequences of insecticide resistance following Aedes aegypti control activities due to a dengue outbreak. PLoS ONE. 2014; 9: e92424. doi: 10.1371/journal.pone.0092424 PMID: 24676277
4. Aiub CAF, Coelho ECA, Sodré E, Pinto LFR, Felzenszwalb I. Genotoxic evaluation of the organophosphorous pesticide temephos. Genet Mol Res. 2002; 1: 159-166. PMID: 14963843
5. Melo-Santos MAV, Varjal-Melo JJM, Araújo AP, Gomes TCS, Paiva MHS, Regis LN, et al. Resistance to the organophosphate temephos: mechanisms, evolution and reversion in an Aedes aegypti laboratory strain from Brazil. Acta Trop. 2010; 113: 180-189. doi: 10.1016/j.actatropica.2009.10.015 PMID: 19879849
6. Ocampo C, Salazar-Terreros M, Mina N, Mcallister J, Brogdon W. Insecticide resistance status of Aedes aegypti in 10 localities of Colombia. Acta Trop. 2011; 118: 37-44. doi: 10.1016/j.actatropica.2011.01.007 PMID: 21300017
7. Polson KA, Brogdon WG, Rawlins SC, Chadee DD. Characterization of insecticide resistance in Trinidadian strains of Aedes aegypti mosquitoes. Acta Trop. 2011; 117: 31-38. doi: 10.1016/j.actatropica.2010.09.005 PMID: 20858454
8. Vontas J, Kioulos E, Pavlidi N, Morou E, della Torre A, Ranson H. Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti. Pest Biochem Physiol. 2012; 104: 126-131.
9. Pontual EV, Napoleão TH, Assis CRD, Bezerra RS, Xavier HS, Navarro DMAF, et al. Effect of Moringa oleifera flower extract on larval trypsin and acethylcholinesterase activities in Aedes aegypti. Arch Insect Biochem Physiol. 2012; 79: 135-152. doi: 10.1002/arch.21012 PMID: 22392801
10. Murray T, Miles C, Daniels C. Natural insecticides. Washington State University, Oregon State University, University of Idaho. PNW649; 2013.
11. Amer A, Mehlhorn H. Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res. 2006; 99: 466-472. PMID: 16642386
12. Costa MS, Pinheiro DO, Serrão JE, Pereira MJB. Morphological changes in the midgut of Aedes aegypti L. (Diptera: Culicidae) larvae following exposure to an Annona coriacea (Magnoliales: Annonaceae) extract. Neotrop Entomol. 2012; 41: 311-314. doi: 10.1007/s13744-012-0050-z PMID: 23950067
13. Deletre E, Martin T, Campagne P, Bourguet D, Cadin A, Menut C, et al. Repellent, irritant and toxic effects of 20 plant extracts on adults of the malaria vector Anopheles gambiae mosquito. PLoS ONE. 2013; 8: e82103. doi: 10.1371/journal.pone.0082103 PMID: 24376515
14. Kamiabi F, Jaal Z, Keng CL. Bioefficacy of crude extract of Cyperus aromaticus (Family: Cyperaceae) cultured cells, against Aedes aegypti and Aedes albopictus mosquitoes. Asian Pac J Trop Biomedic. 2013; 3: 767-775. doi: 10.1016/S2221-1691(13)60153-7 PMID: 24075340
15. Navarro DMAF, Oliveira PES, Potting RJP, Brito AC, Fital SJF, Sant'Ana AEG. The potential attractant or repellent effects of different water types on oviposition in Aedes aegypti L. (Dipt., Culicidae). J Appl Entomol. 2003; 127: 46-50.
16. Pontual EV, Santos NDL, Moura MC, Coelho LCBB, Navarro DMAF, Napoleão TH, et al. Trypsin inhibitor from Moringa oleifera flowers interferes with survival and development of Aedes aegypti larvae and kills bacteria inhabitant of larvae midgut. Parasitol Res. 2014; 113: 727-733. doi: 10.1007/s00436-013-3702-y PMID: 24271154
17. Paiva PMG, Pontual EV, Napoleão TH, Coelho LCBB. Lectins and trypsin inhibitors from plants: Biochemical characteristics and adverse effects on insect larvae. New York: Nova Science Publishers, Inc.; 2013.
18. Brusca GJ, Brusca RC. Invertebrates. Sunderland: Sinauer Associates; 2003.
19. Ray K, Mercedes M, Chan D, Choi CY, Nishiura JT. Growth and differentiation of the larval mosquito midgut. J Insect Sci. 2007; 9: 1-13.
20. Fernandes KM, Neves CA, Serrão JE, Martins GF. Aedes aegypti midgut remodeling during metamorphosis. Parasitol Int. 2014; 63: 506-512. doi: 10.1016/j.parint.2014.01.004 PMID: 24472855
21. Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas do Brasil. Nova Odessa: Plantarum; 2008;
22. Balbachas A. As plantas curam. São Paulo: Missionária; 1959.
23. Lindenmaier DS. Etnobotânica em comunidades indígenas Guaranis no Rio Grande do Sul. Santa Cruz do Sul: Universidade de Santa Cruz do Sul; 2008.
24. Jain MK, Yu BZ, Rogers JM, Smith AE, Boger ETA, Ostrander RL, et al. Specific competitive inhibitor of secreted phospholipase A2 from berries of Schinus terebinthifolius. Phytochemistry. 1995; 39: 537-547. PMID: 7576451
25. Matsuo AL, Figueiredo CR, Arruda DC, Pereira FV, Scutti JAB, Massaoka MH, et al. α-Pinene isolated from Schinus terebinthifolius Raddi (Anacardiaceae) induces apoptosis and confers antimetastatic protection in a melanoma model. Biochem Biophys Res Commun. 2011; 411: 449-454. doi: 10.1016/j.bbrc.2011.06.176 PMID: 21756878
26. Pawlowski Â, Kaltchuk-Santos E, Zini CA, Caramão EB, Soares GLG. Essential oils of Schinus terebinthifolius and S. molle (Anacardiaceae): Mitodepressive and aneugenic inducers in onion and lettuce root meristems. South Afric J Bot. 2012; 80: 96-103.
27. Cavalher-Machado SC, Rosas EC, Brito FA, Heringe AP, Oliveira RR, Kaplan MAC, et al. The anti-allergic activity of the acetate fraction of Schinus terebinthifolius leaves in IgE induced mice paw edema and pleurisy. Int Immunopharmacol. 2008; 8: 1552-1560. doi: 10.1016/j.intimp.2008.06.012 PMID: 18672096
28. Gomes FS, Procópio TF, Napoleão TH, Coelho LCBB, Paiva PMG. Antimicrobial lectin from Schinus terebinthifolius leaf. J Appl Microbiol. 2013; 114: 672-679. doi: 10.1111/jam.12086 PMID: 23190078
29. Coelho AAM, de Paula JE, Espíndola LS. Atividade larvicida de extratos vegetais sobre Aedes aegypti (L.) (Diptera: Culicidae), em condições de laboratório. BioAssay. 2009; 4: 3.
30. Silva AG, Almeida DL, Ronchi SN, Bento AC, Scherer R, Ramos AC, et al. The essential oil of Brazilian pepper, Schinus terebinthifolia Raddi in larval control of Stegomyia aegypti (Linnaeus, 1762). Parasit Vectors. 2010; 3: 79. doi: 10.1186/1756-3305-3-79 PMID: 20799936
31. Roberts EH, Cartwright RA, Wood DJ. The flavonols of tea. J Sci Food Agric. 1956; 7: 637-646.
32. Wagner H, Bladt S. Plant drug analysis. New York: Springer; 1996.
33. Harborne JB. Phytochemical Methods: a guide to modern techniques of plant analysis. London: Chapman & Hall; 1998.
34. Napoleão TH, Pontual EV, Lima TA, Santos NDL, Sá RA, Coelho LCBB, et al. Effect of Myracrodruon urundeuva leaf lectin on survival and digestive enzymes of Aedes aegypti larvae. Parasitol Res. 2012; 110: 609-616. doi: 10.1007/s00436-011-2529-7 PMID: 21735148
35. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193: 265-275. PMID: 14907713
36. Navarro DMAF, Silva PCB, Silva MR, Napoleão TH, Paiva PMG. Larvicidal activity of plant and algae extracts, essential oils and isolated chemical constituents against Aedes aegypti. Nat Prod J. 2013; 3: 268-291.
37. World Health Organization. Instructions for determining the susceptibility or resistance of mosquito larvae to insecticides. WHO/VBC/81.807. p 1-6; 1981.
38. Fernandes KM, Araújo VA, Serrão JE, Martins GF, Campos LAO, Neves CA. Quantitative Analyses of the digestive and regenerative cells of the midgut of Melipona quadrifasciata anthidioides (Hymenoptera; Apidae). Sociobiology. 2010; 56: 489-505.
39. Preuss U, Landsberg G, Scheidtmann KH. Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res. 2003; 31: 878-885. PMID: 12560483
40. Meyer BN, Ferrigini NR, Putman JE, Jacobson LB, Nichols DE, McLaughlin JL. Brine shrimp: a convenient general bioassay for active plant constituents. Planta Med. 1982; 45: 31-34. PMID: 17396775
41. Al-Mehmadi RM, Al-Khalaf AA. Larvicidal and histological effects of Melia azedarach extract on Culex quinquefasciatus Say larvae (Diptera: Culicidae). J King Saud Univ. 2010; 22: 77-85.
42. Pratti DLA, Ramos AC, Scherer R, Cruz ZMA, Ary G. Mechanistic basis for morphological damage induced by essential oil from Brazilian pepper tree, Schinus terebinthifolia,onlarvaeofStegomyia aegypti, the dengue vector. Parasit Vectors. 2015; 8: 136. doi: 10.1186/s13071-015-0746-0 PMID: 25886180
43. Abedi ZH, Brown AWA. Peritrophic membrane as vehicle for DDT and DDE excretion in Aedes aegypti larvae. Ann Entomol Soc America. 1961; 54: 539-542.
44. Gusmão DS, Páscoa V, Mathias L, Vieira IJC, Braz-Filho R, Lemos FJA. Derris (Lonchocarpus) urucu (Leguminosae) extract modifies the peritrophic matrix structure of Aedes aegypti (Diptera:Culicidae). Mem Inst Oswaldo Cruz. 2002; 97: 371-375. PMID: 12051197
45. Levi T, Ben-Dov E, Shahi P, Borovsky D, Zaritsky A. Growth and development of Aedes aegypti larvae at limiting food concentrations. Acta Trop. 2014; 133: 42-44. doi: 10.1016/j.actatropica.2014.02.001 PMID: 24524949
46. Shao Q, Yang B, Xu Q, Li X, Lu Z, Wang C, et al. Hindgut innate immunity and regulation of fecal microbiota through melanization in insects. J Biol Chem. 2012; 287: 14270-14279. doi: 10.1074/jbc.M112.354548 PMID: 22375003
47. Ashida M, Ishizaki Y, Iwahana H. Activation of pro-phenoloxidase by bacterial cell wall or β-1,3-glucans in plasma of the silkworm, Bombyx mori. Biochem Biophys Res Commun. 1983; 113: 562-564. PMID: 6409105
48. Rowley AF; Brookman JL, Ratcliffe NA. Possible involvement of the prophenoloxidase system of the locust, Locusta migratoria, in antimicrobial activity. J Inv Pathol. 1990; 56: 31-38.
49. Silva CCA. Aspectos do sistema imunológico dos insetos. Biotecnol Ciên Desenv. 2002; 24: 68-72.
50. Arruda W, Oliveira GMC, Silva IG. Toxicidade do extrato etanólico de Magonia pubescens sobre larvas de Aedes aegypti. Rev Soc Bras Med Trop. 2003; 36: 17-25. PMID: 12715059
51. Costa MS, Cossolin JFS, Pereira MJB, Sant'Ana AEG, Lima MD, Zanuncio JC, et al. Larvicidal and cytotoxic potential of squamocin on the midgut of Aedes aegypti (Diptera: Culicidae). Toxins. 2014; 6: 1169-1176. doi: 10.3390/toxins6041169 PMID: 24674934
52. Perumalsamy H, Kim J-R, Oh SM, Jung JW, Ahn Y-J, Kwon HW. Novel histopathological and molecular effects of natural compound pellitorine on larval midgut epithelium and anal gills of Aedes aegypti. PLoS ONE. 2013; 8: e80226. doi: 10.1371/journal.pone.0080226 PMID: 24260359
53. Nishiura JT, Ho P, Ray K. Methoprene interferes with mosquito midgut remodeling during metamorphosis. J Med Entomol. 2003; 40: 498-507. PMID: 14680117
54. Brown MR, Raikhel AS, Lea AO. Ultrastructure of midgut endocrine cells in the adult mosquito, Aedes aegypti. Tissue Cell. 1985; 17: 709-721. PMID: 4060146
55. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005; 73: 1907-1916. PMID: 15784530
56. Ochieng CO, Midiwo JO, Owuor PO. Anti-plasmodial and larvicidal effects of surface exudates of Gardenia ternifolia aerial parts. Res J Pharmacol. 2010; 4: 45-50.
57. Mitchell MJ, Keogh DP, Crooks JR, Smith SL. Effects of plant flavonoids and other allelochemicals on insect cytochrome P-450 dependent steroid hydroxylase activity. Insect Biochem Mol Biol. 1993; 23: 65-71. PMID: 8485518
58. Zhang YE, Ma HJ, Feng DD, Lai XF, Chen ZM, Xu MY, et al. Induction of detoxification enzymes by quercetin in the silkworm. J Econ Entomol. 2012; 105: 1034-1042. PMID: 22812145
59. Cheng SS, Liu JY, Tsai KH, Chen WJ, Chang ST. Chemical composition and mosquito larvicidal activity of essential oils from leaves of different Cinnamomum osmophloeum provenances. J Agric Food Chem. 2004; 14: 4935-4400.
60. Shaalan EA, Canyon D, Younes MWF, Abdel-Wahab M, Mansour A-H. A review of botanical phytochemicals with mosquitocidal potential. Environ Int. 2005; 31: 1149-1166. PMID: 15964629
61. Coelho JS, Santos NDL, Napoleão TH, Gomes FS, Ferreira RS, Zingali RB, et al. Effect of Moringa oleifera lectin on development and mortality of Aedes aegypti larvae. Chemosphere. 2009; 77: 934-938. doi: 10.1016/j.chemosphere.2009.08.022 PMID: 19747711
62. Sá RA, Santos NDL, Silva CSB, Napoleão TH, Gomes FS, Cavada BS, et al. Larvicidal activity of lectins from Myracrodruon urundeuva on Aedes aegypti. Comp. Biochem. Physiol C. 2009; 149: 300-306. doi: 10.1016/j.cbpc.2008.08.004 PMID: 18761426
63. Agra-Neto AC, Napoleão TH, Pontual EV, Santos NDL, Luz LA, Oliveira CMF, et al. Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res. 2014; 113: 175-184. doi: 10.1007/s00436-013-3640-8 PMID: 24142287