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.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.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
References
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 160:31–38
Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nat Protoc 2:875–877
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 5:741–744
Benmehdi H, Hasnaoui O, Benali O, Salhi F (2012) Phytochemical investigation of leaves and fruits extracts of Chamaerops humilis L. J Mater Environ Sci 3:320–337
Bnouham M, Mekhfi H, Legssyer A, Ziyyat A (2002) Medicinal plants used in the treatment of diabetes in Morocco. Int J Diabetes Metab 10:33–50
Broadhurst RB, Jones WT (1978) Analysis of condensed tannins using acidified vanillin. J Sci Food Agric 29:788–794
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 17:862–868
Ellman GL, Courtney KD, Andres V, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Francis PT, Palmer AM, Snape M, Wilcock GK (1999) The cholinergic hypothesis of Alzheimer’s disease: a review of progress. J Neurol Neurosurg Psychiatry 66:137–147
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 176:66–81
Harborne JB, Williams CA, Greenham J (1974) Distribution of charged favones and caffeylshikimic acid in Palmae. Phytochemistry 13:1557–1559
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 4:910–918
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
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 34:82–87
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 133:671–677
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 194:1048–1055
Khan MTH (2007) Heterocyclic compounds against the enzyme tyrosinase essential for melanin production: biochemical features of inhibition. Top Heterocycl Chem 9:119–138
Krishnaih D, Sarbatly R, Bono A (2007) Phytochemical antioxidants for health and medicine—a move towards nature. Biotechnol Mol Biol Rev 1:97–104
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 8:11768–11781
Massoud F, Gauthier S (2010) Update on the pharmacological treatment of Alzheimer’s disease. Curr Neuropharmacol 8:69–80
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 69:197–201
Merlo ME, Aleman MM, Cabello J, Penasm J (1993) On the Mediterranean fan palm (Chamaerops humilis). Principes 37:151–158
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 43:583–600
Miguel M, Bouchmaaa N, Aazza S, Gaamoussi F, Lyoussi B (2014) Antioxidant, anti-inflammatory and anti-acetylcholinesterase activities of Moroccan plants. Fresenius Environ Bull 23:1–14
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–C539
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 7:76
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 48:3396–3402
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 26:1231–1237
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 149:62–70
Robards K, Prenzler PD, Tucker G, Swatsitang P, Glover W (1999) Phenolic compounds and their role in oxidative processes in fruits. Food Chem 66:401–436
Seo SY, Sharma VK, Sharma N (2003) Mushroom tyrosinase: recent propects. J Agric Food Chem 51:2837–2853
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–S329
Soler-Rivas C, Espín JC, Wichers HJ (2000) An easy and fast test to compare total free radical scavenger capacity of foodstuffs. Phytochem Anal 11:330–338
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 6:569–577
Suluvoy JK, Grace VMB (2017) Phytochemical profile and free radical nitric oxide (NO) scavenging activity of Averrhoa bilimbi L. fruit extract. 3 Biotech 7:85
Tabet N (2006) Acetylcholinesterase inhibitors for Alzheimer’s disease: anti-inflammatories in acetylcholine clothing. Age Ageing 35:336–338
Uc EY, Rizzo M (2008) Driving and neurodegenerative diseases. Curr Neurol Neurosci Rep 8:377–383
Woisky RG, Salantino A (1998) Analysis of propolis: some parameters and procedures for chemical quality control. J Apicult Res 37:99–105
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 70:1–6
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 15:5658–5670
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).
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
Authors declared no conflict of interest.
Rights and permissions
About this article
Cite this article
Gonçalves, S., Medronho, J., Moreira, E. et al. Bioactive properties of Chamaerops humilis L.: antioxidant and enzyme inhibiting activities of extracts from leaves, seeds, pulp and peel. 3 Biotech 8, 88 (2018). https://doi.org/10.1007/s13205-018-1110-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-018-1110-9


