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Piper anisum as a promising new source of bioactive metabolites

  • Danilo Batista
  • Patrícia Campos
  • Valdenizia R. Silva
  • Luciano de S. Santos
  • Daniel P. Bezerra
  • Milena B. P. Soares
  • Pio Colepicolo
  • Leonardo Zambotti-Villela
  • Ernani Pinto
  • Floricea M. Araújo
  • Dirceu Martins
  • Luzimar G. Fernandez
  • Wilco Ligterink
  • Gisele A. B. Canuto
  • Martins Dias de Cerqueira
  • Paulo R. RibeiroEmail author
Original Paper
  • 39 Downloads

Abstract

Piper species are commonly used by indigenous communities to treat several gastrointestinal diseases. In China, they are also used as an active ingredient in formulae to treat cancer. The objective of the study was to perform a large-scale metabolite profiling analysis to identify bioactive compounds in Piper anisum. Antioxidant capacity was assessed by the DPPH assay and total phenolics were assessed by Folin–Ciocalteu’s method. Antimicrobial activity was assessed against several Gram-positive and Gram-negative bacteria, whereas cytotoxicity was assessed against tumor cell lines MCF-7, HCT116, HepG2 and HL-60, and non-tumor cell line MRC-5. The multiplatform metabolite profiling approach encompassed NMR, GC–MS and LC–MS analyses. P. anisum root extract showed the greatest antioxidant capacity and total phenolic content, followed by the stem and leaf extracts. P. anisum extracts showed a highly selective antimicrobial profile, being specifically active against C. albicans (MIC of 500 μg mL−1). Additionally, the root extract (50 μg mL−1) showed the highest cell inhibition percentages against tumor cell lines MCF-7 (59.5%), HCT116 (49.2%), and HepG2 (61.0%). Forty-eight metabolites were annotated by GC–MS and 27 by LC–MS. These included alkaloids, carbohydrates, fatty acids, hydrocarbons, organic acids, phenolic compounds, and terpenes. Taken together, these results showed that P. anisum root extract is a promising source of bioactive compounds.

Keywords

Antioxidant capacity Antimicrobial compounds Antitumor activity Bioactive metabolites Ethnopharmacology Metabolomics 

Notes

Acknowledgements

Funding was provided by Federal University of Bahia (Project no: 11301), FAPESB, CNPq and CAPES.

Author contributions

PRR designed and supervised all experiments. The extraction, antioxidant activity assay, total phenolic quantification, and antimicrobial activity were performed by DB and PRR. Plant collection and voucher production were performed by PRR, PC, DB, WL and LGF. Cytotoxicity assays were performed by VRS, LSS, DPB, and MBPS. Nuclear magnetic resonance (NMR) analysis was performed by PRR, DB, and MDC. GC–MS and LC–MS analysis were performed by PRR, DB, GABC, PC, LZV, and EP. Data processing and metabolite identification were performed by PRR, and GABC. Statistical analysis was performed by PRR and DB. PRR and DB wrote the manuscript, whereas WL, LGF, DPB, and GABC provided suggestions to the manuscript draft.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11696_2019_1004_MOESM1_ESM.docx (365 kb)
Supplementary material 1 (DOCX 365 KB)

References

  1. Afolabi OB, Oloyede OI, Agunbiade SO (2018) Inhibitory potentials of phenolic-rich extracts from Bridelia ferruginea on two key carbohydrate-metabolizing enzymes and Fe2 + -induced pancreatic oxidative stress. J Integr Med 16:192–198PubMedCrossRefGoogle Scholar
  2. Ansar Ahmed S, Gogal RM Jr, Walsh JE (1994) A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3H]thymidine incorporation assay. J Immunol Methods 170:211–224CrossRefGoogle Scholar
  3. Bauer R, Pröbstle A, Lotter H, Wagner-Redecker W, Matthiesen U (1996) Cyclooxygenase inhibitory constituents from Houttuynia cordata. Phytomedicine 2:305–308PubMedCrossRefGoogle Scholar
  4. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA 68:394–424PubMedGoogle Scholar
  5. Brú J, Guzman JD (2016) Folk medicine, phytochemistry and pharmacological application of piper marginatum. Braz J Pharmacogn 26:767–779CrossRefGoogle Scholar
  6. Chen YC, Chen JJ, Chang YL, Teng CM, Lin WY, Wu CC, Chen IS (2004) A new aristolactam alkaloid and anti-platelet aggregation constituents from Piper taiwanense. Planta Med 70:174–177PubMedCrossRefGoogle Scholar
  7. Chen Y, Chen Y, Shi Y, Ma C, Wang X, Li Y, Miao Y, Chen J, Li X (2016) Antitumor activity of Annona squamosa seed oil. J Ethnopharmacol 193:362–367PubMedCrossRefGoogle Scholar
  8. Christ JA, Sarnaglia-Junior VB, Barreto LM, Guimarães EF, Garbin ML, Carrijo TT (2016) The genus Piper (Piperaceae) in the Mata das Flores state park, Espírito Santo, Brazil. Rodriguesia 67:1031–1046CrossRefGoogle Scholar
  9. Cox MC, Dan TD, Swain SM (2006) Emerging drugs to replace current leaders in first-line therapy for breast cancer. Expert Opin Emerg Drugs 11:489–501PubMedCrossRefGoogle Scholar
  10. Cüce M, Bekircan T, Laghari AH, Sökmen M, Sökmen A, Önay Uçar E, Kılıç AO (2017) Antioxidant phenolic constituents, antimicrobial and cytotoxic properties of Stachys annua L. From both natural resources and micropropagated plantlets. Indian J Tradit Knowl 16:407–416Google Scholar
  11. Cunha Lima ST, Rodrigues ED, Alves C, Merrigan TL, Melo T, Guedes MLS, Nascimento AF, Toralles MB (2012) The use of medicinal plants by an indigenous Pataxó community in NE Brazil. Revista Brasileira de Plantas Medicinais 14:84–91CrossRefGoogle Scholar
  12. D’Sousa Costa C, Ribeiro P, Loureiro M, Simoes R, de Castro R, Fernandez L (2015) Phytochemical screening, antioxidant and antibacterial activities of extracts prepared from different tissues of  Schinus terebinthifolius  Raddi that occurs in the coast of Bahia, Brazil. Pharmacogn Mag 11:607–614CrossRefGoogle Scholar
  13. da Silva JK, da Trindade R, Alves NS, Figueiredo PL, Maia JGS, Setzer WN (2017) Essential oils from Neotropical Piper Species and their biological activities. Int J Mol Sci 18:2571PubMedCentralCrossRefPubMedGoogle Scholar
  14. Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dasyam N, Munkacsi AB, Fadzilah NH, Senanayake DS, O’Toole RF, Keyzers RA (2014) Identification and bioactivity of 3-epi-xestoaminol C isolated from the New Zealand brown alga Xiphophora chondrophylla. J Nat Prod 77:1519–1523PubMedCrossRefGoogle Scholar
  16. de Ávila JM, Dalcol II, Pereira AO, Santos EW, Ferraz A, Santos MZ, Mostardeiro MA, Morel AF (2018) Antimicrobial evaluation of erythrinan alkaloids from Erythrina cristagalli L. Med Chem [Shariqah (United Arab Emirates)] 14:784–790CrossRefGoogle Scholar
  17. De Lima EJSP, Alves RG, D’Elia GMA, Da Anunciação TA, Silva VR, Santos LDS, Soares MBP, Cardozo NMD, Costa EV, Da Silva FMA, Koolen HHF, Bezerra DP (2018) Antitumor effect of the essential oil from the leaves of Croton matourensis Aubl. (Euphorbiaceae). Molecules 23:1–12Google Scholar
  18. De Oliveira Chaves MC, De Oliveira AH, De Oliveira Santos BV (2006) Aristolactams from Piper marginatum Jacq (Piperaceae). Biochem Syst Ecol 34:75–77CrossRefGoogle Scholar
  19. Deborde C, Fontaine JX, Jacob D, Botana A, Nicaise V, Richard-Forget F, Lecomte S, Decourtil C, Hamade K, Mesnard F, Moing A, Molinié R (2019) Optimizing 1D 1H-NMR profiling of plant samples for high throughput analysis: extract preparation, standardization, automation and spectra processing. Metabolomics 15:28PubMedPubMedCentralCrossRefGoogle Scholar
  20. Desai SJ, Prabhu BR, Mulchandani NB (1988) Aristolactams and 4,5-dioxoaporphines from Piper longum. Phytochemistry 27:1511–1515CrossRefGoogle Scholar
  21. Desai SJ, Chaturvedi R, Mulchandani NB (1990) Piperolactam D, a new aristolactam from indian piper species. J Nat Prod 53:496–497CrossRefGoogle Scholar
  22. Diekema DJ, Messer SA, Brueggemann AB, Coffman SL, Doern GV, Herwaldt LA, Pfaller MA (2002) Epidemiology of candidemia: 3-year results from the emerging infections and the epidemiology of Iowa organisms study. J Clin Microbiol 40:1298–1302PubMedPubMedCentralCrossRefGoogle Scholar
  23. Đurđević S, Šavikin K, Živković J, Böhm V, Stanojković T, Damjanović A, Petrović S (2018) Antioxidant and cytotoxic activity of fatty oil isolated by supercritical fluid extraction from microwave pretreated seeds of wild growing Punica granatum L. J Supercrit Fluids 133:225–232CrossRefGoogle Scholar
  24. Edmond MB, Wallace SE, McClish DK, Pfaller MA, Jones RN, Wenzel RP (1999) Nosocomial bloodstream infections in United States hospitals: a 3-year analysis. Clin Infect Dis 29:239–244PubMedCrossRefGoogle Scholar
  25. Ee GCL, Lim SK, Lim CM, Dzulkefly K (2008) Alkaloids and carboxylic acids from Piper nigrum. Asian J Chem 20:5931–5940Google Scholar
  26. Erik Olsen C, Dutt Tyagi O, Boll PM, Hussaini FA, Parmar VS, Sharma NK, Taneja P, Jain SC (1993) An aristolactam from Piper acutisleginum and revision of the structures of piperolactam B and D. Phytochemistry 33:518–520CrossRefGoogle Scholar
  27. Fajriah S, Megawati Hudiyono S, Kosela S, Hanafi M (2017) Chemical constituents and potential cytotoxic activity of n- hexane fraction from Myristica fatua Houtt leaves C3—AIP Conference Proceedings. 1862Google Scholar
  28. Gertsch J (2011) Botanical drugs, synergy, and network pharmacology: forth and back to intelligent mixtures. Planta Med 77:1086–1098PubMedCrossRefGoogle Scholar
  29. Goleniowski M, Bonfill M, Cusido R, Palazón J (2013) Phenolic acids. In: Ramawat K, Mérillon JM (eds) Natural products. Springer, Berlin, Heidelberg.  https://doi.org/10.1007/978-3-642-22144-6_64 CrossRefGoogle Scholar
  30. Gu F, Wu G, Fang Y, Zhu H (2018) Nontargeted metabolomics for phenolic and polyhydroxy compounds profile of pepper (Piper nigrum L.) products based on LC-MS/MS analysis. Molecules 23:1985PubMedCentralCrossRefPubMedGoogle Scholar
  31. Hu S, Yin J, Nie S, Wang J, Phillips GO, Xie M, Cui SW (2016) In vitro evaluation of the antioxidant activities of carbohydrates. Bioact Carbohydr Diet Fibre 7:19–27CrossRefGoogle Scholar
  32. Ibrahim TA, El Dib RA, Al-Youssef HM, Amina M (2019) Chemical composition and antimicrobial and cytotoxic activities of Antidesm abunius L. Pak J Pharm Sci 32:153–163PubMedGoogle Scholar
  33. Islam MT, Ali ES, Uddin SJ, Shaw S, Islam MA, Ahmed MI, Chandra Shill M, Karmakar UK, Yarla NS, Khan IN, Billah MM, Pieczynska MD, Zengin G, Malainer C, Nicoletti F, Gulei D, Berindan-Neagoe I, Apostolov A, Banach M, Yeung AWK, El-Demerdash A, Xiao J, Dey P, Yele S, Jóźwik A, Strzałkowska N, Marchewka J, Rengasamy KRR, Horbańczuk J, Kamal MA, Mubarak MS, Mishra SK, Shilpi JA, Atanasov AG (2018) Phytol: a review of biomedical activities. Food Chem Toxicol 121:82–94PubMedCrossRefGoogle Scholar
  34. Jong T-T, Jean M-Y (1993) Alkaloids from Houttuynia cordata. Jnl Chin Chem Soc 40:301–303CrossRefGoogle Scholar
  35. Karak S, Das S, Biswas M, Choudhury A, Dutta M, Chaudhury K, De B (2019) Phytochemical composition, β-glucuronidase inhibition, and antioxidant properties of two fractions of Piper betle leaf aqueous extract. J Food Biochem 00:e13048.  https://doi.org/10.1111/jfbc.13048 CrossRefGoogle Scholar
  36. Karthikeyan SC, Velmurugan S, Donio MBS, Michaelbabu M, Citarasu T (2014) Studies on the antimicrobial potential and structural characterization of fatty acids extracted from Sydney rock oyster Saccostrea glomerata. Ann Clin Microbiol Antimicrob 13:332PubMedPubMedCentralCrossRefGoogle Scholar
  37. Kchaou W, Abbès F, Mansour RB, Blecker C, Attia H, Besbes S (2016) Phenolic profile, antibacterial and cytotoxic properties of second grade date extract from Tunisian cultivars (Phoenix dactylifera L.). Food Chem 194:1048–1055PubMedCrossRefGoogle Scholar
  38. Kim SK, Ryu SY, No J, Choi SU, Kim YS (2001) Cytotoxic alkaloids from Houttuynia cordata. Arch Pharmacal Res 24:518–521CrossRefGoogle Scholar
  39. Kitahara T, Koyama N, Matsuda J, Aoyama Y, Hirakata Y, Kamihira S, Kohno S, Nakashima M, Sasaki H (2004) Antimicrobial activity of saturated fatty acids and fatty amines against methicillin-resistant Staphylococcus aureus. Biol Pharm Bull 27:1321–1326PubMedCrossRefGoogle Scholar
  40. Kumar V, Poonam AKP, Parmar VS (2003) Naturally occurring aristolactams, aristolochic acids and dioxoaporphines and their biological activities. Nat Product Rep 20:565–583CrossRefGoogle Scholar
  41. Lang G, Mayhudin NA, Mitova MI, Sun L, Van Der Sar S, Blunt JW, Cole ALJ, Ellis G, Laatsch H, Munro MHG (2008) Evolving trends in the dereplication of natural product extracts: new methodology for rapid, small-scale investigation of natural product extracts. J Nat Prod 71:1595–1599PubMedCrossRefGoogle Scholar
  42. Levrier C, Sadowski MC, Nelson CC, Davis RA (2015) Cytotoxic C20 diterpenoid alkaloids from the Australian Endemic Rainforest Plant Anopterus macleayanus. J Nat Prod 78:2908–2916PubMedCrossRefGoogle Scholar
  43. Lim SM, Loh SP (2016) In vitro antioxidant capacities and antidiabetic properties of phenolic extracts from selected citrus peels. Int Food Res J 23:211–219Google Scholar
  44. Limmongkon A, Nopprang P, Chaikeandee P, Somboon T, Wongshaya P, Pilaisangsuree V (2018) LC-MS/MS profiles and interrelationships between the anti-inflammatory activity, total phenolic content and antioxidant potential of Kalasin 2 cultivar peanut sprout crude extract. Food Chem 239:569–578PubMedCrossRefGoogle Scholar
  45. Luís Â, Domingues F, Duarte AP (2016) Biological properties of plant-derived alkylresorcinols: mini-review. Mini-Rev Med Chem 16:851–854PubMedCrossRefGoogle Scholar
  46. Mandel S, Youdim MBH (2004) Catechin polyphenols: neurodegeneration and neuroprotection in neurodegenerative diseases. Free Radical Biol Med 37:304–317CrossRefGoogle Scholar
  47. McGaw LJ, Jäger AK, Van Staden J (2002) Antibacterial effects of fatty acids and related compounds from plants. S Afr J Bot 68:417–423CrossRefGoogle Scholar
  48. Merah S, Dahmane D, Krimat S, Metidji H, Nouasri A, Lamari L, Dob T (2018) Chemical analysis of phenolic compounds and determination of anti-oxidant, antimicrobial and cytotoxic activities of organic extracts of Pinus coulteri. Bangladesh J Pharmacol 13:120–129CrossRefGoogle Scholar
  49. Mgbeahuruike EE, Yrjönen T, Vuorela H, Holm Y (2017) Bioactive compounds from medicinal plants: focus on Piper species. S Afr J Bot 112:54–69CrossRefGoogle Scholar
  50. Milliken W, Albert B (1997) The use of medicinal plants by the Yanomami Indians of Brazil, Part II. Econ Bot 51:264–278CrossRefGoogle Scholar
  51. Milroy MJ (2018) “Cancer statistics: global and national” Qual Cancer Care: survivorship before, during and after treatment. Springer, NY, pp 29–35CrossRefGoogle Scholar
  52. Monteiro D (2013) Piperaceae em um fragmento de floresta atlântica da Serra da Mantiqueira, Minas Gerais, Brasil. Rodriguésia 64:379–398CrossRefGoogle Scholar
  53. Mrkonjić ZO, Nađpal JD, Beara IN, Sabo VSA, Četojević-Simin DD, Mimica-Dukić NM, Lesjak MM (2017) Phenolic profiling and bioactivities of fresh fruits and jam of Sorbus species. J Serb Chem Soc 82:651–664CrossRefGoogle Scholar
  54. Ndhlala AR, Moyo M, Van Staden J (2010) Natural antioxidants: fascinating or mythical biomolecules? Molecules (Basel, Switzerland) 15:6905–6930CrossRefGoogle Scholar
  55. Parmar VS, Jain SC, Gupta S, Talwar S, Rajwanshi VK, Kumar R, Azim A, Malhotra S, Kumar N, Jain R, Sharma NK, Tyagi OD, Lawrie SJ, Errington W, Howarth OW, Olsen CE, Wengel SKSa (1998) Polyphenols and alkaloids from Piper species. Phytochemistry 49:1069–1078CrossRefGoogle Scholar
  56. Pereira EPL, Ribeiro PR, Loureiro MB, de Castro RD, Fernandez LG (2014) Effect of water restriction on total phenolics and antioxidant properties of Amburana cearensis (Fr. Allem) A.C. Smith cotyledons during seed imbibition. Acta Physiol Plant 36:1293–1297Google Scholar
  57. Perigo CV, Torres RB, Bernacci LC, Guimarães EF, Haber LL, Facanali R, Vieira MAR, Quecini V, Marques MOM (2016) The chemical composition and antibacterial activity of eleven Piper species from distinct rainforest areas in Southeastern Brazil. Ind Crops Prod 94:528–539CrossRefGoogle Scholar
  58. Pfaller MA, Diekema DJ (2004) Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol 42:4419–4431PubMedPubMedCentralCrossRefGoogle Scholar
  59. Raja Mazlan RNA, Rukayadi Y, Maulidiani M, Ismail IS (2018) Solvent extraction and identification of active anticarcinogenic metabolites in piper cubeba L. through 1H-NMR-based metabolomics approach. Molecules (Basel, Switzerland) 23:1–19PubMedCentralCrossRefPubMedGoogle Scholar
  60. Ribeiro PR, Willems LAJ, Mudde E, Fernandez LG, de Castro RD, Ligterink W, Hilhorst HWM (2015a) Metabolite profiling of the oilseed crop Ricinus communis during early seed imbibition reveals a specific metabolic signature in response to temperature. Ind Crops Prod 67:305–309CrossRefGoogle Scholar
  61. Ribeiro PR, Willems LAJ, Mutimawurugo MC, Fernandez LG, de Castro RD, Ligterink W, Hilhorst HWM (2015b) Metabolite profiling of Ricinus communis germination at different temperatures provides new insights into thermo-mediated requirements for successful seedling establishment. Plant Sci 239:180–191PubMedCrossRefGoogle Scholar
  62. Ribeiro PR, Zanotti RF, Deflers C, Fernandez LG, de Castro RD, Ligterink W, Hilhorst HWM (2015c) Effect of temperature on biomass allocation in seedlings of two contrasting genotypes of the oilseed crop Ricinus communis. J Plant Physiol 185:31–39PubMedCrossRefGoogle Scholar
  63. Ribeiro RV, Bieski IGC, Balogun SO, Martins DTDO (2017) Ethnobotanical study of medicinal plants used by Ribeirinhos in the North Araguaia microregion, Mato Grosso, Brazil. J Ethnopharmacol 205:69–102PubMedCrossRefGoogle Scholar
  64. Ricardo LM, De Paula-Souza J, Andrade A, Brandão MGL (2017) Plants from the Brazilian traditional medicine: species from the books of the Polish physician Piotr Czerniewicz (Pedro Luiz Napoleão Chernoviz, 1812–1881). Braz J Pharm 27:388–400CrossRefGoogle Scholar
  65. Richard D, Kefi K, Barbe U, Bausero P, Visioli F (2008) Polyunsaturated fatty acids as antioxidants. Pharmacol Res 57:451–455PubMedCrossRefGoogle Scholar
  66. Rivera E, Gomez H (2010) Chemotherapy resistance in metastatic breast cancer: the evolving role of ixabepilone. Breast Cancer Res 12(Suppl 2):S2–S2PubMedPubMedCentralCrossRefGoogle Scholar
  67. Rodrigues E, Carlini EA (2005) Ritual use of plants with possible action on the central nervous system by the Krahô Indians, Brazil. Phytother Res 19:129–135PubMedCrossRefGoogle Scholar
  68. Rodrigues E, Mendes FR, Negri G (2006) Plants indicated by Brazilian Indians for disturbances of the central nervous system: a bibliographical survey. Cent Nerv Syst Agents Med Chem 6:211–244CrossRefGoogle Scholar
  69. Saleem M, Nazir M, Hussain H, Tousif MI, Elsebai MF, Riaz N, Akhtar N (2018) Natural phenolics as inhibitors of the human neutrophil elastase (HNE) release: an overview of natural anti-inflammatory discoveries during recent years. AntiInflamm Antiallerg Agents Med Chem 17:70–94CrossRefGoogle Scholar
  70. Santana AI, Vila R, Cañigueral S, Gupta MP (2016) Chemical composition and biological activity of essential oils from different species of Piper from panama. Planta Med 82:986–991PubMedCrossRefGoogle Scholar
  71. Santos MRA, Lima MR, Oliveira CLLG (2014) Medicinal plants used in rondônia, Western amazon, Brazil. Revista Brasileira de Plantas Medicinais 16:707–720CrossRefGoogle Scholar
  72. Santos PM, Batista DLJ, Ribeiro LAF, Boffo EF, de Cerqueira MD, Martins D, de Castro RD, de Souza-Neta LC, Pinto E, Zambotti-Villela L, Colepicolo P, Fernandez LG, Canuto GAB, Ribeiro PR (2018) Identification of antioxidant and antimicrobial compounds from the oilseed crop Ricinus communis using a multiplatform metabolite profiling approach. Ind Crops Prod 124:834–844CrossRefGoogle Scholar
  73. Setzer WN, Park G, Agius BR, Stokes SL, Walker TM, Haber WA (2008) Chemical compositions and biological activities of leaf essential oils of twelve species of Piper from Monteverde, Costa Rica. Nat Product Commun 3:1367–1374Google Scholar
  74. Shang Y, Du Q, Liu S, Staadler M, Wang S, Wang D (2018) Antitumor activity of isosteroidal alkaloids from the plants in the genus veratrum and fritillaria. Curr Protein Pept Sci 19:302–310PubMedCrossRefGoogle Scholar
  75. Stoessl A, Unwin CH (1970) The antifungal factors in barley. V. Antifungal activity of the hordatines. Can J Bot 48:465–470CrossRefGoogle Scholar
  76. Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Targeting multidrug resistance in cancer. Nat Rev Drug Discovery 5:219–234PubMedCrossRefGoogle Scholar
  77. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015a) Global cancer statistics. CA 65:87–108PubMedGoogle Scholar
  78. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015b) Global cancer statistics, 2012. CA 65:87–108PubMedGoogle Scholar
  79. Valente C, Pedro M, Duarte A, Nascimento Maria SJMSJ, Abreu PM, Ferreira MJU (2004) Bioactive diterpenoids, a new jatrophane and two ent-abietanes, and other constituents from Euphorbia pubescens. J Nat Prod 67:902–904PubMedCrossRefGoogle Scholar
  80. Vazquez JA (1999) Options for the management of mucosal candidiasis in patients with AIDS and HIV infection. Pharmacotherapy 19:76–87PubMedCrossRefGoogle Scholar
  81. Wang YH, Morris-Natschke SL, Yang J, Niu HM, Long CL, Lee KH (2014) Anticancer principles from medicinal piper (Hu Jiao) plants. J Tradit complement Med 4:8–16PubMedPubMedCentralCrossRefGoogle Scholar
  82. Watanabe T, Yamamoto Y, Miura M, Konno H, Yano S, Nonomura Y (2019) Systematic analysis of selective bactericidal activity of fatty acids against staphylococcus aureus with minimum inhibitory concentration and minimum bactericidal concentration. J Oleo Sci 68:291–296PubMedCrossRefGoogle Scholar
  83. Xia J, Wishart DS (2011) Web-based inference of biological patterns, functions and pathways from metabolomic data using MetaboAnalyst. Nat Protoc 6:743PubMedCrossRefGoogle Scholar
  84. Xiang CP, Han JX, Li XC, Li YH, Zhang Y, Chen L, Qu Y, Hao CY, Li HZ, Yang CR, Zhao SJ, Xu M (2017) Chemical composition and acetylcholinesterase inhibitory activity of essential oils from Piper species. J Agric Food Chem 65:3702–3710PubMedCrossRefGoogle Scholar
  85. Yoon BK, Jackman JA, Valle-González ER, Cho NJ (2018) Antibacterial free fatty acids and monoglycerides: biological activities, experimental testing, and therapeutic applications. Int J Mol Sci 19:1114PubMedCentralCrossRefPubMedGoogle Scholar
  86. Zhou SY, Fan F, Sun JZ, Guo Z, Sun WT, Chen L, Tang QQ, Qiu G, Yang SP, Yu J, Cai YS (2018) Cytotoxic alkaloids from the fruits and seeds of Alangium salviifolium (L.f.) Wangerin. Phytochem Lett 26:195–198CrossRefGoogle Scholar

Copyright information

© Institute of Chemistry, Slovak Academy of Sciences 2019

Authors and Affiliations

  • Danilo Batista
    • 1
  • Patrícia Campos
    • 2
  • Valdenizia R. Silva
    • 3
  • Luciano de S. Santos
    • 3
  • Daniel P. Bezerra
    • 3
  • Milena B. P. Soares
    • 3
  • Pio Colepicolo
    • 4
  • Leonardo Zambotti-Villela
    • 4
  • Ernani Pinto
    • 5
  • Floricea M. Araújo
    • 1
  • Dirceu Martins
    • 1
  • Luzimar G. Fernandez
    • 2
  • Wilco Ligterink
    • 6
  • Gisele A. B. Canuto
    • 1
  • Martins Dias de Cerqueira
    • 1
  • Paulo R. Ribeiro
    • 1
    • 2
    Email author
  1. 1.Metabolomics Research Group, Departamento de Química Orgânica, Instituto de QuímicaUniversidade Federal da BahiaSalvadorBrazil
  2. 2.Laboratório de Bioquímica, Biotecnologia e Bioprodutos, Departamento de Bioquímica e BiofísicaUniversidade Federal da BahiaSalvadorBrazil
  3. 3.Instituto Gonçalo MonizFundação Oswaldo CruzSalvadorBrazil
  4. 4.Departamento de Bioquímica, Instituto de QuímicaUniversidade de São PauloSão PauloBrazil
  5. 5.Faculdade de Ciências FarmacêuticasUniversidade de São PauloSão PauloBrazil
  6. 6.Wageningen Seed Lab, Laboratory of Plant PhysiologyWageningen University (WU)WageningenThe Netherlands

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