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Biotransformation of 4-nerolidylcatechol by Heraclides brasiliensis (Lepidoptera: Papilionidae) reduces the toxicity of Piper umbellata (Piperaceae)

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Abstract

Heraclides brasiliensis (Lepidoptera: Papilionidae) larvae feed preferably on Piperaceae, foraging successfully on leaf tissues even though species of this contain high levels of secondary metabolites such as amides and lignans, associated with diverse biological activities including insecticidal properties. Studies examining the metabolism of chemical constituents in Piperaceae by insects are rare. In this study, we characterized the metabolites of 4-nerolidylcatechol (4-NC), the major constituent of Piper umbellata (Piperaceae), and E-2,3-dihydro-3-(3,4-dihydroxyphenyl)farnesoic acid, compounds from fecal material of H. brasiliensis larvae fed a diet containing only P. umbellata leaves. The biotransformed product was also detected in larval and pupal tissues. Moreover, we observed deactivation of the toxicity of P. umbellata leaves against brine shrimp after their metabolism in H. brasiliensis larvae from a LC50 of 523.3 to 3,460.7 μg/mL. This deactivation is closely associated with the biotransformation of 4-NC to E-2,3-dihydro-3-(3,4-dihydroxyphenyl)farnesoic acid, which showed LC50 of 8.0 and >1,000 μg/mL, respectively.

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References

  • Baldoqui DC, Bolzani VS, Furlan M, Kato MJ, Marques MOM (2009) Flavones, lignans and terpenes from Piper umbellata (Piperaceae). Quim Nova 32:1107–1109

    Article  CAS  Google Scholar 

  • Barahona MV, Sánchez-Fortún S (1999) Toxicity of carbamates to the brine shrimp Artemia salina and the effect of atropine, BW284c51, iso-OMPA and 2-PAM on carbaryl toxicity. Environ Pollut 104:469–476

    Article  CAS  Google Scholar 

  • Batista R, Brandão GC, Braga FC, Oliveira AB (2009) Cytotoxicity of Wedelia paludosa D.C. extracts and constituents. Braz J Pharmacogn 19:36–40

    CAS  Google Scholar 

  • Bernard CB, Krishnamurty HG, Chauret D, Durst T, Philogène BJR, Sanchez-Vindas P, Hasbun C, Poveda L, San Román L, Arnason JT (1995) Insecticidal defense of Piperaceae from the Neotropics. J Chem Ecol 21:801–814

    Article  CAS  Google Scholar 

  • Carballo JL, Hernández-inda ZL, Pérez P, García-Grávalos MD (2002) A comparison between two brine shrimp assays to detect in vitro cytotoxicity in marine natural products. BMC Biotechnol 2:17–23

    Article  PubMed  Google Scholar 

  • Edwards PJ, Wratten SD (1980) Ecologia das interações entre insetos e plantas. EPU/EDUSP, São Paulo

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Harwig J, Scott P (1971) Brine shrimp (Artemia salina L.) larvae as a screening system for fungal toxins. Appl Microbiol 21:1011–1016

    PubMed  CAS  Google Scholar 

  • Isobe T, Ohsaki A, Nagata K (2002) Antibacterial constituents against Helicobacter pylori of Brazilian medicinal plant, pariparoba. Yakugaku Zasshi 122:291–294

    Article  PubMed  CAS  Google Scholar 

  • Ivie GW, Bull DL, Beier RC, Pryor NW, Oertli RH (1983) Metabolic detoxification: mechanism of insect resistance to plant psoralens. Science 221:374–376

    Article  PubMed  CAS  Google Scholar 

  • Jaki B, Orjala J, Bürji HR, Sticher O (1999) Biological screening of cyanobacteria for antimicrobial and molluscicidal activity, brine shrimp lethality, and cytotoxicity. Pharm Biol 37:138–143

    Article  Google Scholar 

  • Kijjoa A, Giesbrecht AM, Akisue MK, Gottlieb OR, Gottlieb HE (1980) 4-nerolydilcatechol from Pothomorphe umbellata. Planta Med 39:85–87

    Article  CAS  Google Scholar 

  • Konno K, Hirayama C, Shinbo H (1997) Glycine in digestive juice: a strategy of herbivorous insects against chemical defense of host plants. J Insect Physiol 43:217–224

    Article  PubMed  CAS  Google Scholar 

  • Mclauglin JL, Chang CJ, Smith DL (1991) Bench top bioassay for the discovery of bioactive natural products: an update. In: Rahman AU(ed) Studies in natural products chemistry. Elsevier, Amsterdam, pp 383–409

  • Mello MO, Silva-Filho MC (2002) Plant-insect interactions: An evolutionary arms race between two distinct defense mechanisms. Braz J Plant Physiol 14:71–81

    Article  CAS  Google Scholar 

  • Meyer BN, Ferrigni NR, Putnam LB, Jacobsen LB, Nichols DE, McLaughlin JL (1982) Brine shrimp: a convenient general bioassay for active plant constituents. J Med Plant Res 45:31–34

    Article  CAS  Google Scholar 

  • Michael AS, Thompson CG, Abramovitz M (1956) Artemia salina as a test organism for a bioassay. Science 123:464–469

    Article  PubMed  CAS  Google Scholar 

  • Nitao JK, Berhow M, Duval SM, Weisleder D, Waughn SF, Zangerl A, Bernenbaum MR (2003) Characterization of furanocoumarin metabolites in parsnip webworm, Depressaria pastinacella. J Chem Ecol 29:671–682

    Article  PubMed  CAS  Google Scholar 

  • Nunes BS, Carvalho FD, Guilhermino LM, Van Stappen G (2006) Use of the genus Artemia in ecotoxicity testing. Environ Pollut 144:453–462

    Article  PubMed  CAS  Google Scholar 

  • Núnez V, Castro V, Murillo R, Ponce-Soto LA, Merfort I, Lomonte B (2005) Inhibitory effects of Piper umbellatum and Piper peltatum extracts towards myotoxic phospholipases A2 from Bothrops snake venoms: isolation of 4-nerolidylcatechol as active principle. Phytochemistry 66:017–025

    Article  Google Scholar 

  • Perazzo FF, Souza GHB, Lopes W, Cardoso LGV, Carvalho JCT, Nanayakkara NP, Bastos JK (2005) Antiinflammatory and analgesic properties of water–ethanolic extract from Pothomorphe umbellata (Piperaceae) aerial parts. J Ethnopharm 3:215–220

    Article  Google Scholar 

  • Pinto ACS (2002) Estudo fitoquímico e biológico de Pothomorphe peltata (L.) Miquel (Piperaceae). Masters Dissertation, Federal University of Amazonas (UFAM), Manaus, Amazonas State, Brazil

  • Pinto ACS, Pessoa C, Lotufo LVC, Moraes MOM, Moraes ME, Cavalcanti BC, Nunomura SN, Pohlit AM (2006) In vitro cytotoxicity of Pothomorphe peltata (L.) Miquel (Piperaceae) isolated 4-nerolidylcatechol and its semi-synthetic diacetyl derivative. Rev Bras Pl Med 8:205–211

    Google Scholar 

  • Ramos CS, Kato MJ (2009) Hydrolysis of methyl benzoate from Piper arboreum by Naupactus bipes beetle. J Braz Chem Soc 20:560–563

    Article  CAS  Google Scholar 

  • Ramos CS, Vanin SA, Kato MJ (2008) Metabolism of (−)-grandisin from Piper solmsianum in Coleoptera and Lepidoptera species. Phytochemistry 69:2157–2161

    Article  PubMed  CAS  Google Scholar 

  • Ramos CS, Vanin SA, Kato MJ (2009) Sequestration of prenylated benzoic acid and chromenes by Naupactus bipes (Coleoptera: Curculionidae) feeding on Piper gaudichaudianum (Piperaceae). Chemoecology 19:73–80

    Article  CAS  Google Scholar 

  • Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864

    Article  PubMed  CAS  Google Scholar 

  • Ropke CD, Meirelles RR, Da Silva VV, Sawada TCH, Barros SBM (2003) Pothomorphe umbellata extract prevents β-tocopherol depletion after UV-irradiation. Photochem Photobiol 78:436–439

    Article  PubMed  CAS  Google Scholar 

  • Scott JG (1999) Cytochromes P450 and insecticide resistance. Insect Biochem Mol Biol 29:757–777

    Article  PubMed  CAS  Google Scholar 

  • Sleet RB, Brendel K (1983) Improved methods for harvesting and counting synchronous populations of Artemia nauplii for use in developmental toxicology. Ecotoxicol Environ Saf 7:435–446

    Article  PubMed  CAS  Google Scholar 

  • Solís PN, Wright CW, Anderson MM, Gupta MP, Phillipson JD (1993) A microwell cytotoxicity assay using Artemia salina. Plant Med 59:250–252

    Article  Google Scholar 

  • Vanhaecke P, Persoone G, Claus C, Sorgeloos P (1981) Proposal for a short-term toxicity test with Artemia nauplii. Ecotoxicol Environ Saf 5:382–387

    Article  PubMed  CAS  Google Scholar 

  • Vanin SA, Ramos CS, Guimarães EF, Kato MJ (2008) Insect feeding preferences on Piperaceae species observed in São Paulo city, Brazil. Rev Bras Entomol 52:72–77

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from FAPESB and CNPq. MJK and CSR are grateful to CNPq and FAPESB for research fellowships. We also thank Dr. Elsie F. Guimarães and Dr. Sérgio Antônio Vanin for the identification of the plant and insect species, respectively.

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Authors and Affiliations

  1. Departamento de Química, Universidade Federal Rural de Pernambuco, Recife, PE, CP 52.171-030, Brazil

    Clécio S. Ramos

  2. Departamento de Estudos Básicos e Instrumentais, Universidade Estadual do Sudoeste da Bahia, Itapetinga, BA, CP 45700-000, Brazil

    Luciano de J. Souza & Ronan Batista

  3. Instituto de Química, Universidade de São Paulo, São Paulo, SP, CP 26077, 05513-970, Brazil

    Massuo J. Kato

Authors
  1. Clécio S. Ramos
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  2. Luciano de J. Souza
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  3. Massuo J. Kato
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  4. Ronan Batista
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Correspondence to Clécio S. Ramos or Ronan Batista.

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Ramos, C.S., Souza, L.d., Kato, M.J. et al. Biotransformation of 4-nerolidylcatechol by Heraclides brasiliensis (Lepidoptera: Papilionidae) reduces the toxicity of Piper umbellata (Piperaceae). Chemoecology 22, 39–45 (2012). https://doi.org/10.1007/s00049-011-0096-0

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