Advertisement

3 Biotech

, 8:88 | Cite as

Bioactive properties of Chamaerops humilis L.: antioxidant and enzyme inhibiting activities of extracts from leaves, seeds, pulp and peel

  • Sandra Gonçalves
  • Joana Medronho
  • Elsa Moreira
  • Clara Grosso
  • Paula B. Andrade
  • Patrícia Valentão
  • Anabela Romano
Original Article
  • 69 Downloads

Abstract

In this work we evaluated methanolic extracts from different parts (leaves, seeds, fruit peel and pulp) of Chamaerops humilis L. for antioxidant activity and the ability to inhibit enzymes linked with neurodegenerative diseases: acetylcholinesterase (AChE), butyrylcholinesterase (BChE) and tyrosinase (TYR). The total content of phenolics, flavonoids and condensed tannins was also determined. The antioxidant and inhibitory activities of the extracts varied significantly according to the tissue. Seed extracts showed the greatest ability to scavenge DPPH (IC50 = 81.28 µg mL−1) and ABTS (1440.42 µmolTE \( {{\text{g}}^{-1}}_{\text{extract}} \)) and to reduce iron (1142.46 µmolAAE \( {{\text{g}}^{-1}}_{\text{extract}} \)). Seed and peel extracts strongly inhibited AChE (IC50 = 660.16 and 653.68 µg mL−1, respectively) and BChE (IC50 = 304.86 and 701.54 µg mL−1, respectively). The strongest inhibition of TYR was achieved by the seed and pulp extracts (268.97 and 279.99 µg mL−1, respectively). The highest levels of phenolics and condensed tannins were found in the seed extract (1564.88 µmolGAE \( {{\text{g}}^{-1}}_{\text{extract}} \) and 170.00 µmolcE \( {{\text{g}}^{-1}}_{\text{extract}} \), respectively) whereas the leaf extract was the richest in flavonoids (139.88 µmolQE \( {{\text{g}}^{-1}}_{\text{extract}} \)). HPLC-DAD analysis indicated the presence of flavonoids and phenolic acids (hydroxycinnamic acids) in the leaf and pulp extracts. A high correlation was found between the total condensed tannins content and the antioxidant and enzyme inhibition activities, suggesting these compounds are responsible for the biological activity of the extracts. Overall, our results indicate that C. humilis extracts may provide a new and alternative source of agents for medical and industrial applications.

Keywords

Acetylcholinesterase Butyrylcholinesterase Dwarf palm Tannins Tyrosinase 

Abbreviations

AAE

Ascorbic acid equivalents

ABTS

2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid)

AChE

Acetylcholinesterase

AD

Alzheimer’s disease

ATCI

Acetylthiocholine iodide

BChE

Butyrylcholinesterase

BTCI

Butyrylthiocholine chloride

CE

Catechin equivalents

DPPH

2,2-diphenyl-1-picrylhydrazyl

l-DOPA

3,4-dihydroxy-l-phenylalanine

DTNB

5,5′-dithiobis(2-nitrobenzoic acid)

F–C reagent

Folin–Ciocalteu reagent

FRAP

Ferric reducing antioxidant power

GAE

Gallic acid equivalents

HPLC-DAD

High-performance liquid chromatography-diode array detection

PD

Parkinson’s disease

QE

Quercetin equivalents

TCA

Trichloroacetic acid

TE

Trolox equivalents

Trolox

6-Hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid

TYR

Tyrosinase

Notes

Acknowledgements

We would like to acknowledge financial support from the EU (FEDER funds through COMPETE) and from National Funds (FCT/MEC, Fundação para a Ciência e Tecnologia/Ministério da Educação e Ciência) through project UID/QUI/50006/2013, co-financed by the EU (FEDER under the Partnership Agreement PT2020). S. Gonçalves acknowledges a Grant from FCT (SFRH/BPD/84112/2012) and C. Grosso thanks FCT for the FCT Investigator award (IF/01332/2014).

Authors’ contribution

The work presented here was accomplished with the collaboration of all authors. The research topic and framework were defined by S. Gonçalves and A. Romano. E. Moreira and C. Grosso preformed the HPLC analysis under the supervision of P.B. Andrade and P. Valentão. S. Gonçalves and J. Medronho prepared the plant material and conducted the biological activity assays. S. Gonçalves analyzed the data and wrote the paper. All authors revised and approved the manuscript.

Compliance with ethical standards

Conflict of interest

Authors declared no conflict of interest.

References

  1. Abdel-Hameed E-SS, Nagaty MA, Salman MS, Bazaidm SA (2014) Phytochemicals, nutritionals and antioxidant properties of two prickly pear cactus cultivars (Opuntia ficus indica Mill.) growing in Taif, KSA. Food Chem 160:31–38CrossRefGoogle Scholar
  2. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877CrossRefGoogle Scholar
  3. Benahmed-Bouhafsoun A, Djied S, Mouzaz F, Kaid-Harche M (2013) Phytochemical composition and in vitro antioxidant activity of Chamaerops humilis L. extracts. Int J Pharm Pharm Sci 5:741–744Google Scholar
  4. Benmehdi H, Hasnaoui O, Benali O, Salhi F (2012) Phytochemical investigation of leaves and fruits extracts of Chamaerops humilis L. J Mater Environ Sci 3:320–337Google Scholar
  5. Bnouham M, Mekhfi H, Legssyer A, Ziyyat A (2002) Medicinal plants used in the treatment of diabetes in Morocco. Int J Diabetes Metab 10:33–50Google Scholar
  6. Broadhurst RB, Jones WT (1978) Analysis of condensed tannins using acidified vanillin. J Sci Food Agric 29:788–794CrossRefGoogle Scholar
  7. Dufaÿ M, Anstett M-C (2004) Cheating is not always punished: killer female plants and pollination by deceit in the dwarf palm Chamaerops humilis. J Evol Biol 17:862–868CrossRefGoogle Scholar
  8. Ellman GL, Courtney KD, Andres V, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  9. Francis PT, Palmer AM, Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer’s disease: a review of progress. J Neurol Neurosurg Psychiatry 66:137–147CrossRefGoogle Scholar
  10. Giovino A, Scibetta S, Saia S, Guarino C (2014) Genetic and morphologic diversity of European fan palm (Chamaerops humilis L.) populations from different environments from Sicily. Bot J Linn Soc 176:66–81CrossRefGoogle Scholar
  11. Harborne JB, Williams CA, Greenham J (1974) Distribution of charged favones and caffeylshikimic acid in Palmae. Phytochemistry 13:1557–1559CrossRefGoogle Scholar
  12. Hasnaoui O, Benali O, Bouazza M, Benmehdi H (2013) Ethnobotanical approaches and phytochemical analysis of Chamaerops humilis L. (Arecaceae) in the area of Tlemcen (western Algeria). Res J Pharm Biol Chem Sci 4:910–918Google Scholar
  13. Haynes J, Mc-Laughlin J (2000) Edible palms and their uses. Fact sheet MDCE-00-50-1. Homestead, Fla. http://www.plantapalm.com/vpe/ethnobotany/EdiblePalms.PDF. Accessed 23 Feb 2016
  14. Hirai Y, Sanada S, Ida Y, Shoji J (1986) Studies on the constituents of Palmae plants. III. The constituents of Chamaerops humilis L. and Trachycarpus wagnerianus Becc. Chem Pharm Bull 34:82–87CrossRefGoogle Scholar
  15. Kang J, Thakali KM, Xiem C, Kondo M, Tong Y, Ou B, Jensen G, Medina MB, Schauss AG, Wu X (2012) Bioactivities of açaí (Euterpe precatoria Mart.) fruit pulp, superior antioxidant and anti-inflammatory properties to Euterpe oleracea Mart. Food Chem 133:671–677CrossRefGoogle Scholar
  16. 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 194:1048–1055CrossRefGoogle Scholar
  17. Khan MTH (2007) Heterocyclic compounds against the enzyme tyrosinase essential for melanin production: biochemical features of inhibition. Top Heterocycl Chem 9:119–138Google Scholar
  18. Krishnaih D, Sarbatly R, Bono A (2007) Phytochemical antioxidants for health and medicine—a move towards nature. Biotechnol Mol Biol Rev 1:97–104Google Scholar
  19. Left DB, Zertoubi M, Khoudali S, Benaissa M, Irhzo A, Azzi M (2013) Effect of methanol extract of Chamaerops humilis L. leaves (MECHLL) on the protection performance of oxide film formed on reinforcement steel surface in concrete simulated pore solution. Int J Electrochem Sci 8:11768–11781Google Scholar
  20. Massoud F, Gauthier S (2010) Update on the pharmacological treatment of Alzheimer’s disease. Curr Neuropharmacol 8:69–80CrossRefGoogle Scholar
  21. Masuda T, Yamashita D, Takeda Y, Yonemori S (2005) Screening for tyrosinase inhibitors among extracts of seashore plants and identification of potent inhibitors from Garcinia subelliptica. Biosci Biotechnol Biochem 69:197–201CrossRefGoogle Scholar
  22. Merlo ME, Aleman MM, Cabello J, Penasm J (1993) On the Mediterranean fan palm (Chamaerops humilis). Principes 37:151–158Google Scholar
  23. Metzler-Baddeley C (2007) A review of cognitive impairments in dementia with Lewy bodies relative to Alzheimer’s disease and Parkinson’s disease with dementia. Cortex 43:583–600CrossRefGoogle Scholar
  24. Miguel M, Bouchmaaa N, Aazza S, Gaamoussi F, Lyoussi B (2014) Antioxidant, anti-inflammatory and anti-acetylcholinesterase activities of Moroccan plants. Fresenius Environ Bull 23:1–14Google Scholar
  25. Nehdi IA, Mokbli S, Sbihi H, Tan CP, Al-Resayesm SI (2014) Chamaerops humilis L. var. argentea André date palm seed oil: a potential dietetic plant product. J Food Sci 79:C534–C539CrossRefGoogle Scholar
  26. Nile SH, Nile AS, Keum Y-S (2017) Total phenolics, antioxidant, antitumor, and enzyme inhibitory activity of Indian medicinal and aromatic plants extracted with different extraction methods. 3 Biotech 7:76CrossRefGoogle Scholar
  27. Pulido R, Bravo L, Saura-Calixto F (2000) Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J Agric Food Chem 48:3396–3402CrossRefGoogle Scholar
  28. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237CrossRefGoogle Scholar
  29. Rezaire A, Robinson J-C, Bereaum D, Verbaere A, Sommerer N, Khan MK, Durand P, Prost E, Fils-Lycaon B (2014) Amazonian palm Oenocarpus bataua (‘‘patawa’’): chemical and biological antioxidant activity—phytochemical composition. Food Chem 149:62–70CrossRefGoogle Scholar
  30. Robards K, Prenzler PD, Tucker G, Swatsitang P, Glover W (1999) Phenolic compounds and their role in oxidative processes in fruits. Food Chem 66:401–436CrossRefGoogle Scholar
  31. Seo SY, Sharma VK, Sharma N (2003) Mushroom tyrosinase: recent propects. J Agric Food Chem 51:2837–2853CrossRefGoogle Scholar
  32. Serrano J, Puupponen-Pimi R, Dauer A, Aura A-M, Saura-Calixto F (2009) Tannins: current knowledge of food sources, intake, bioavailability and biological effects. Mol Nutr Food Res 53:S310–S329CrossRefGoogle Scholar
  33. Soler-Rivas C, Espín JC, Wichers HJ (2000) An easy and fast test to compare total free radical scavenger capacity of foodstuffs. Phytochem Anal 11:330–338CrossRefGoogle Scholar
  34. Sousa AD, Brito ESD (2015) Optimization of condensed tannin aqueous extraction from cashew tree pruning residue using response surface methodology and its drying. Waste Biomass Valoriz 6:569–577CrossRefGoogle Scholar
  35. Suluvoy JK, Grace VMB (2017) Phytochemical profile and free radical nitric oxide (NO) scavenging activity of Averrhoa bilimbi L. fruit extract. 3 Biotech 7:85CrossRefGoogle Scholar
  36. Tabet N (2006) Acetylcholinesterase inhibitors for Alzheimer’s disease: anti-inflammatories in acetylcholine clothing. Age Ageing 35:336–338CrossRefGoogle Scholar
  37. Uc EY, Rizzo M (2008) Driving and neurodegenerative diseases. Curr Neurol Neurosci Rep 8:377–383CrossRefGoogle Scholar
  38. Woisky RG, Salantino A (1998) Analysis of propolis: some parameters and procedures for chemical quality control. J Apicult Res 37:99–105CrossRefGoogle Scholar
  39. Zengin G, Uysal S, Ceylan R, Aktumsek A (2015) Phenolic constituent, antioxidative and tyrosinase inhibitory activity of Ornithogalum narbonense L. from Turkey: a phytochemical study. Ind Crop Prod 70:1–6CrossRefGoogle Scholar
  40. Zhang S-J, Lin Y-M, Zhou HC, Wei S-D, Lin G-H, Ye G-F (2010) Antioxidant tannins from stem bark and fine root of Casuarina equisetifolia. Molecules 15:5658–5670CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Faculty of Sciences and Technology, MeditBioUniversity of AlgarveFaroPortugal
  2. 2.REQUIMTE/LAQV, Laboratório de Farmacognosia, Departamento de Química, Faculdade de FarmáciaUniversidade do PortoPortoPortugal

Personalised recommendations