Next Article in Journal
Properties of Biomimetic Artificial Spider Silk Fibers Tuned by PostSpin Bath Incubation
Previous Article in Journal
In Vivo Biosynthesis of Inorganic Nanomaterials Using Eukaryotes—A Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Molecules
Volume 25
Issue 14
10.3390/molecules25143249
molecules-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Ferulago nodosa Subsp. geniculata (Guss.) Troia & Raimondo from Sicily (Italy): Isolation of Essential Oil and Evaluation of Its Bioactivity

by
Natale Badalamenti
1,
Vincenzo Ilardi
2,
Sergio Rosselli
3,4,
Maurizio Bruno
1,4,
Filippo Maggi
5,
Mariarosaria Leporini
6,
Tiziana Falco
6,
Monica R. Loizzo
6,* and
Rosa Tundis
6
1
Department of Biological, Chemical and Pharmaceutical Sciences and Technologies (STEBICEF), University of Palermo, Viale delle Scienze, ed. 17, I-90128 Palermo, Italy
2
Department of Earth and Marine Sciences (DISTeM), University of Palermo, Via Archirafi 26, I-90128 Palermo, Italy
3
Department of Agricultural, Food and Forest Sciences (SAAF), University of Palermo, Viale delle Scienze, ed. 4, I-90128 Palermo, Italy
4
Centro Interdipartimentale di Ricerca “Riutilizzo Bio-Based Degli Scarti da Matrici Agroalimentari” (RIVIVE), University of Palermo, I-90128 Palermo, Italy
5
School of Pharmacy, University of Camerino, Via Sant’Agostino 1, I-62032 Camerino, Italy
6
Department of Pharmacy, Health Science and Nutrition, University of Calabria, I-87036 Arcavacata Rende (CS), Italy
*
Author to whom correspondence should be addressed.
Molecules 2020, 25(14), 3249; https://doi.org/10.3390/molecules25143249
Submission received: 23 June 2020 / Revised: 8 July 2020 / Accepted: 14 July 2020 / Published: 16 July 2020
(This article belongs to the Section Flavours and Fragrances)
Browse Figure
Versions Notes

Abstract

:
Ferulago nodosa (L.) Boiss. (Apiaceae) is a species occurring in the Balkan-Tyrrhenian area. The object of the present study is Sicilian F. nodosa subsp. geniculata (Guss.) Troia & Raimondo, classified as an endemic F. nodosa subspecies. Aerial parts of this plant species were subjected to hydrodistillation to obtain an essential oil. A total of 93 compounds were identified with 2,3,6-trimethyl benzaldehyde (19.0%), spathulenol (9.0%), (E)-caryophyllene (5.4%), and caryophyllene oxide (5.4%) as the main components. The biological activities of F. nodosa essential oil were also investigated. This oil showed an interesting antioxidant potential in a 2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) test (IC50 of 14.05 μg/mL). Additionally, hypoglycemic and antilipidemic effects were evaluated. Lipase enzyme was inhibited with an IC50 value of 41.99 μg/mL. Obtained data demonstrated that F. nodosa could be considered a promising source of bioactive compounds useful for the treatment and management of obesity.

Graphical Abstract

1. Introduction

The genus Ferulago W.D.J. Koch (Apiaceae) includes about 50 species distributed in the Mediterranean area, from Portugal to Iran and from Russia to Northwestern Africa [1,2].
The center of origin and diversification of the genus was identified to be in Turkey, which houses 34 species, many of which are exclusive [1,2]. Tomkovich and Pimenov [2] divide the genus Ferulago into two subgenera (Ferulago and Galbanifera) and nine sections.
In Sicily, the genus Ferulago is represented by Ferulago nodosa (L.) Boiss. and Ferulago campestris (Besser) Grecescu, both belonging to the subgenus Galbanifera [2]. In particular, F. nodosa, the object of this contribution, highlights a Balkan-Tyrrhenian distribution, being present in Greece, Albania, and probably also in the Yugoslav Republic of North Macedonia, with a western population exists in Sicily.
Based on morphological characteristics and in consideration of the current geographical and genetic isolation of the Sicilian population, Peruzzi et al. [3] proposed to assign the Sicilian population of Ferulago nodosa to the rank of subspecies, with the combination Ferulago nodosa subsp. geniculata (Guss.) Troia & Raimondo.
The genus Ferulago is recognized in traditional medicine as a remedy for gastrointestinal tract panics, ulcer. Moreover it was known as sedative, a treatment for hemorrhoids, skin infection and spleen disease, as well as a natural preservative in different foods, such as meat and cheese [4].
Oxidative stress is defined as an imbalance between the production of Radical Oxygen Species (ROS) and the antioxidant defensive mechanisms in our bodies, that results in the development of pathological conditions such as pre-diabetes [5,6]. It was reported that 5–10% of people per year with pre-diabetes would progress to diabetes and its associated complications, such as obesity [6]. Therapeutic implications of the pre-diabetes condition include the inhibition of α-amylase and α-glucosidase enzyme suppressing postprandial hyperglycemia and reduced dietary carbohydrate digestion and absorption [7]. In addition, inhibition of pancreatic lipase, with a reduction of fat absorption, is a therapeutic strategy to reduce the risk of obesity [8]. Thus, natural inhibitors of these enzymes and antioxidant agents from dietary plants may be proposed as an effective therapy for management of post-prandial hyperglycemia and obesity diseases.
Essential oils have been used since ancient times due to their biological properties. Many essential oils, in fact, are characterized by antioxidant properties [9]. For this reason, it will be used as a substitute for butylated hydroxyanisole and butylated hydroxytoluene (BHT), which are harmful to human health [9]. For this reason, essential oils from edible plants, alone or inserted in active packaging and edible coatings, may represent a valid instrument to prolong shelf life. Several research papers evidenced that Ferulago extracts and essential oils are characterized by antioxidant activity and are used as medicinal plants or food preservatives [10,11,12].
Moreover, several essential oils have been proven to possess hypoglycemic and hypolipidemic properties [13,14,15,16]. However, no previous study investigated the inhibition of carbohydrate-hydrolyzing enzymes and the hypolipidemic activity of Ferulago subspecies.
For this purpose, this study aimed to investigate the phytochemical composition of Sicilian F. nodosa subsp. geniculata essential oil obtained by the hydrodistillation of aerial parts, as well as its biological properties, including antioxidant, hypoglycemic, and hypolipidemic potentials.

2. Results and Discussion

2.1. Essential Oil

The chemical composition of the essential oil obtained from the aerial parts of F. nodosa subsp. geniculata is reported in Table 1. A total of 93 compounds, accounting for 73.9% of the total composition, were identified. From a semi-quantitative perspective, they were represented by aromatics (21.0%, shared by 5 constituents), followed by oxygenated sesquiterpenes (17.5%, 11 constituents), sesquiterpene hydrocarbons (12.4%, 21 constituents), monoterpene hydrocarbons (8.8%, 17 constituents), and oxygenated monoterpenes (8.4%, 24 constituents).
The major components were the aromatic, 2,3,6-trimethyl benzaldehyde (19.0%), and the sesquiterpenoids, spathulenol (9.0%), (E)-caryophyllene (5.4%), and caryophyllene oxide (5.4%).
Among monoterpenoids, bornyl acetate (4.6%) and α-pinene (2.9%) were the most representative compounds. The presence of aromatic aldehydes, such as 2,3,6-trimethyl benzaldehyde, is considered a hallmark of several Ferulago species [18,19,20,21,22,23]. It is worth mentioning that these compounds are formed during distillation from the cleavage and molecular rearrangement of ferulol-type monoterpenoids [19].
The essential oil obtained from the aerial parts of F. nodosa growing in Sicily has previously been studied by Ruberto et al. [18], who found a different chemical profile, with 2,3,4-trimethylbenzaldehyde (42.2%) and α-pinene (22.4%) as the main constituents. These authors did not detect the 2,3,6-trimethylbenzaldehyde which instead was the major component of our sample. Demetzos et al. [24] studied the essential oil composition of flowering aerial parts from F. nodosa growing in Greece and identified α-pinene (31.1%) as the major component. Notably, they did not detect any aromatic aldehydes. Similar results were published by Evergetis et al. [25], who studied the essential oil profile of F. nodosa growing in Greece, showing α-pinene (30.8%) and β-phellandrene (10.2%) as the main constituents. Thus, the notable chemical polymorphism observed may be the result of significant variability in genetics (e.g., occurrence of different subspecies) together with the influence of geographic factors and the type of processing and extraction of the plant material (e.g., hydrodistillation vs. steam distillation).

2.2. Antioxidant Activity of Essential Oil

The antioxidant potential of F. nodosa subsp. geniculata essential oil was screened using different assays (Table 2). ABTS+ radical cation resulted more sensitive to the action of F. nodosa essential oil with an IC50 value of 14.0 μg/mL, while an IC50 value of 26.3 μg/mL was observed in a 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay. The results can be justified because ABTS+ and DPPH. radicals have different stereochemistry, and after a reaction with essential oil these two radicals give diverse responses. Percentages of 39.4% and 32.7% after 30 and 60 min of incubation, respectively, were recorded in a β-carotene bleaching test when the essential oil was tested at maximum concentration. In a FRAP assay, an IC50 value of 16.9 μg/mL was observed.
Several research articles that have Ferulago ssp. as the object of investigation confirmed the antioxidant potential of these plants. Previously, Cecchini et al. [26] compared the DPPH radical scavenging activity of F. campestris fruit and root essential oils, and found IC50 mean values of 0.23 and 0.24 μg/mL of oil, respectively. In disagreement with our data, both oils were able to protect lipids from peroxidation in a similar manner to the positive control BHT (IC50 mean values of 0.010 and 0.011 μg/mL for fruit and root essential oils, respectively). A great variability was observed in the DPPH radical scavenging activity of F. angulate essential oils derived from different organs. Among them, unripe seed oil showed the highest radical scavenging potential with an IC50 value of 162 μg/mL, followed by leaf (IC50 value of 210 μg/mL). These organs are characterized by a higher phenol and flavonoid content, compared with other parts [10]. Lower DPPH radical scavenging was found for Iranian F. angulata aerial part essential oil (IC50 value of 488 μg/mL) [27]. A similar situation was observed for F. trifida essential oils with IC50 values in the range 95–120 μg/mL [28].
Our data are in line, also, with those reported by Karakaya et al. [29], who investigated the antioxidant potential of F. pauciradiata extracts and essential oils derived from roots and aerial parts. The highest DPPH activity was observed in root essential oil and ethyl acetate fraction, with IC50 values of 4.59 and 6.56 μg/mL, respectively. Shahbazi and Shavisi [30] compared the DPPH radical scavenging activity of sub-fractions of methanol extract and the essential oil obtained from F. bernardii aerial parts, and found IC50 values of 5.66, 6.88 and 14.81 mg/mL, respectively.
The aqueous and methanol extracts obtained from flowers, stems, and leaves of F. angulata were investigated by Faride et al. [31], who found IC50 values ranged from 214 to 1606 µg/mL against the DPPH radical. Values in the range from 264 to 393 μmol of Trolox equivalent per gram of dry weight were found for F. angulata ethanol flower extract and leaf methanol extract, respectively [32].
The antioxidant potential of this species was confirmed in vivo. In fact, treatment with F. angulata extract at doses from 200 to 800 mg/kg/day resulted in an increase in catalase, glutathione peroxidase, and super oxide dismutase activities in diabetic Wistar rats [33].
Mileski et al. [34] reported the antioxidant activity of methanol, ethanol, and aqueous extracts obtained from aerial parts and inflorescences of F. macedonica. The DPPH results demonstrated that extract derived from the inflorescences (in the range of 490–1170 μg/mL) were more active than the extract obtained from the aerial parts (630–1810 μg/mL). This evidence was confirmed, also, in an ABTS test. The antioxidant potential of the crude extract and four fractions of F. carduchorum aerial parts, at two vegetative stages, were analyzed by Golfakhrabadi et al. [35]. The highest DPPH radical scavenging activity was found for flower crude extract, with an IC50 of 0.49 mg/mL, followed by fruit crude extract (IC50 of 0.62 mg/mL) and flower methanol fraction (IC50 of 0.68 mg/mL).
Among the identified compounds, spathulenol, the main abundant volatile component of the F. nodosa essential oil, was able to inhibit both DPPH and ABTS radicals, with IC50 values of 85.60 and 639.25 μg/mL, respectively [36]. Additionally, this tricyclic sesquiterpenoid exhibited protection against lipoperoxidation in rat brains, with an IC50 value of 26.13 μg/mL and, consequently, decreased the generation of malondialdehyde [36]. Coté et al. [37] demonstrated the DPPH radical scavenging potential of α-pinene and caryophyllene oxide, with IC50 values of 3.4 and 183 μg/mL, respectively, while IC50 > 200 μg/mL was found for both β-caryophyllene and bornyl acetate.

2.3. Hypoglycemic and Hypolipidemic Potential of Essential Oil

F. nodosa essential oil α-amylase, α-glucosidase, and lipase inhibitory activities were concentration-dependent, and results are summarized in Table 3. The essential oil exhibited promising lipase enzyme inhibitory activity, with an IC50 value of 42.0 μg/mL. This value was 0.8 times higher than that found for the positive control, orlistat. A lower enzyme inhibitory activity was found against α-amylase and α-glucosidase, with IC50 values of 196.4 and 365.9 μg/mL, respectively.
The α-glucosidase and α-amylase inhibitory activities of F. bracteata root extracts were investigated by Karakaya et al. [38]. Dichloromethane and ethyl acetate extracts exhibited the lowest IC50 values of 0.95 μg/mL, followed by methanol extract (IC50 of 4.19 μg/mL), whereas the aqueous extract was inactive. The effects of F. angulata hydroalcoholic extract were evaluated by Musavi-Ezmareh et al. [39] in diabetic male rats. After supplementation of 200 mg/kg body weight of extract for four weeks, a reduction of blood sugar and an improvement of blood lipid profiles were observed. A similar situation was observed with supplementation of Ferulago angulata hydroalcoholic extract in Wistar rats, where a reduction of total cholesterol, low-density lipoproteins, and triglycerides, and an inhibition of lipid peroxidation were observed [39,40]. More recently, Parsamehr et al. [41] confirmed that intraperitoneal injection of F. angulata hydroalcoholic extract for three weeks in diabetic rats could be effective in the treatment of diabetes and at the same time alleviate liver damage.
Several terpenes identified in F. nodosa essential oil are able to exert hypoglycemic and hypolipidemic activity. The intraperitoneal administration of α-pinene in diabetic mice at different doses (0.05, 0.10, 0.25 and 0.50 mL/kg) resulted in a reduction of fasting blood glucose levels [42]. Previously, Bae et al. [43] demonstrated that intraperitoneal administration of α-pinene (5, 25, or 50 mg/kg) reduced body weight and the serum levels of α-amylase and lipase. Additionally, the combination of β-caryophyllene (500 μmol) and L-arginine (500 μmol) stabilized glucose tolerance and reduced pancreatic cell damage in diabetic rats [44].
Zhou et al. [45] suggested, also, that β-caryophyllene could be used as a therapeutic target for the treatment of diabetic patients, since this terpene acts at the level of arginine-specific mono-ADP-ribosyltransferase 1. Moreover, β-caryophyllene oral administration at a dose of 200 mg/kg induced a reduction of glucose, increase of plasma insulin levels, and improvement of altered activities of carbohydrate metabolic enzymes [46].

3. Materials and Methods

3.1. Chemicals and Reagents

Solvents of analytical grade were purchased from Honeywell (Seelze, Germany). Reagents, α-amylase, lipase from porcine pancreas, and α-glucosidase from Saccharomyces cerevisiae were purchased from Sigma-Aldrich S.p.a. (Milan, Italy). Acarbose from Actinoplanes sp. was obtained from Serva (Heidelberg, Germany).

3.2. Plant Materials

Aerial parts of F. nodosa subsp. geniculata were harvested in April 2019, immediately before flowering, from different plants growing on a flat-lying litho-soil near Noto Antica, Syracuse, (Sicily, Italy) (36°57′27.37” N; 15°02′18.76” E) of 378 m above sea level. This plant has a distribution limited to the southeastern sector of Sicily, in particular the complex of the Iblei Mountains. It is a circular-limestone plateau of circular shape, dating back to the Miocene, in which the presence of numerous streams dug deep incisions (canyons), locally known as “cave iblee”. The bioclimate of the area is thermo-Mediterranean dry, which favors both aspects of thermo-xerophilous pine forest (Pinus halepensis and Coridothymus capitatus) and all aspects of mesophilic shrub (Myrtus communis, Arbutus unedo, and Pistacia lentiscus). Samples were identified by Prof. Vincenzo Ilardi, University of Palermo, Italy. A voucher specimen (PAL 109707) has been deposited in the Herbarium Mediterraneum Panormitanum of the “Orto Botanico”, University of Palermo, Italy.

3.3. Isolation of the Essential Oil

Fresh leaves and stems (200 g) of F. nodosa subsp. geniculata were reduced to small pieces and subjected to hydrodistillation according to the standard procedure previously described [47]. The obtained oil (0.22% w/w) was stored in dark vials at −20 °C before analyses.

3.4. GC-FID Analysis of the Essential Oil

An Agilent 4890D gas chromatograph (GC) coupled with an ionization flame detector (FID) (Santa Clara, CA, USA) was used to analyze the essential oil. The separation stationary phase was represented by an HP-5 capillary column (5% phenylmethylpolysiloxane, 25 m, 0.32 mm i.d.; 0.17 μm f.t.) (Agilent, Folsom, CA, USA). The mobile phase was helium (99.999%) flowing at 1.0 mL/min. The oven temperature programmer was as follows: 60 °C isothermal for 5 min, then ramp (4 °C/min) to 220 °C, and ramp (11 °C/min) to 280 °C. The essential oil was diluted 1:100 in hexane and the volume injected was 1 μL in split mode (1:34). The injector and detector temperatures were set to 280 °C. A commercial mix of n-alkanes (C8–C30) purchased from Supelco (Bellefonte, CA, USA) was used to determine the peak linear retention index (RI). Quantitative values, expressed as percentages, were obtained following the procedure of Cecchini et al. [26].

3.5. GC-MS Analysis of the Essential Oil

An Agilent 6890N GC equipped with a 5973N single quadrupole mass spectrometer (MS) (Santa Clara, CA, USA) was employed. The stationary phase was an HP-5MS capillary column (30 m, 0.25 mm i.d., 0.1 μm f.t.) (Agilent, Folsom, CA, USA). The operative conditions and the mobile phase were the same as those reported above. The injector and transfer line temperatures were 280 and 250 °C, respectively. The same dilution as that reported above was injected into the GC-MS system in split mode (1:50). Mass spectra were acquired in electron impact (EI) mode in the range of 29–400 m/z. The identification was carried out by a combination of MS matching and RI overlapping against the Adams 2007 [17], NIST 17 (NIST 17, 2017) [48], and FFNSC2 (FFNSC2) [49] libraries. The comparison with available authentic standards (Sigma-Aldrich, Milan, Italy) was also used.

3.6. Antioxidant Activity

The in vitro antioxidant potential of F. nodosa subsp. geniculata essential oil samples was screened by ABTS, DPPH, β-carotene bleaching test, and FRAP assay. Both DPPH and ABTS tests were applied to examine the radical scavenging activity of the essential oil, using the procedure previously described by Loizzo et al. [50]. In both cases, ascorbic acid was used as a positive control.
In the β-carotene bleaching test a mixture of linoleic acid, β-carotene, and Tween 20 was prepared and the resulting emulsion was mixed with the essential oil at different concentrations (2.5–100 μg/mL) [50,51]. The absorbance was read after 30 min of incubation at 470 nm. Propyl gallate was used as a positive control. The essential oil at a concentration of 2.5 mg/mL was tested, also, to evaluate the ability of samples to protect iron from a redox reaction [52]. BHT was used as a control.

3.7. Hypoglycemic and Hypolipidemic Potential

In the α-amylase inhibitory test, a mixture of α-amylase, starch, and essential oil was prepared as previously reported [52]. In the α-glucosidase inhibitory test, a mixture of maltose, α-glucosidase, ο-dianisidine, peroxidase/glucose oxidase, and samples was prepared. In both cases, essential oil was tested at different concentrations, ranging from 25 to 1000 μg/mL, and absorbance was measured at 540 and 500 nm, respectively [50].
The pancreatic lipase inhibitory test was performed as previously reported [53]. A mixture of p- nitrophenyl caprylate and porcine pancreatic lipase enzyme was prepared and added to 96-well-plate-contained essential oil at different concentrations (2.5–40 μg/mL). After that, the absorbance was measured (405 nm).

4. Conclusions

The goal of this study was to chemically characterize and biologically investigate the essential oil obtained from F. nodosa subsp. geniculata aerial parts collected in Sicily (Italy).
The major components of essential oil were 2,3,6-trimethyl benzaldehyde, spathulenol, (E)-caryophyllene, and caryophyllene oxide. Among monoterpenoids, bornyl acetate and α-pinene were the most representative compounds. F. nodosa subsp. geniculata essential oil showed, also, an interesting antioxidant potential, with particular reference to ABTS testing. Additionally, hypoglycemic and antilipidemic effects were evaluated with interesting activity against lipase. Obtained data demonstrated that F. nodosa subsp. geniculata essential oil could be considered a promising phytocomplex useful for formulation of nutraceutical products to prevent diseases associated with oxidative stress, such as type 2 diabetes and obesity.

Author Contributions

Conceptualization, M.B. and V.I., S.R.; methodology, M.R.L., R.T., and S.R.; validation, M.B., R.T., M.R.L., and S.R.; formal analysis, N.B., F.M., T.F., and M.L.; investigation, F.M., M.L., N.B., S.R., R.T., T.F., and M.B.; resources, M.R.L. and M.B.; writing—original draft preparation, M.R.L., N.B., and F.M.; writing—review and editing, M.B., M.R.L., R.T., and S.R.; funding acquisition, M.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by a grant from MIUR-ITALY PRIN 2017 (Project N. 2017A95NCJ). The APC was funded by MDPI.

Conflicts of Interest

The authors declare that they have no conflict of interest.

References

  1. Bernardi, L. Tentamen revisionis generis Ferulago. Boissiera 1979, 30, 1–182. [Google Scholar]
  2. Tomkovich, L.P.; Pimenov, M.G. Botanico-geographical analysis of the genus Ferulago W.D.J. Koch. Feddes Reper. 1989, 100, 119–129. [Google Scholar]
  3. Peruzzi, L.; Domina, G.; Bartolucci, F.; Galasso, G.; Peccenini, S.; Raimondo, F.M.; Albano, A.; Alessandrini, A.; Banfi, E.; Barberis, G.; et al. An inventory of the names of vascular plants endemic to Italy, their loci classici and types. Phytotaxa 2015, 196, 1–217. [Google Scholar] [CrossRef] [Green Version]
  4. Mumivand, A.H.; Aghemiri, A.; Morshedloo, M.R.; Nikoumanesh, K. Ferulago angulata and Tetrataenium lasiopetalum: Essential oils composition and antibacterial activity of the oils and extracts. Biocatal. Agric. Biotechnol. 2019, 22, 101407. [Google Scholar] [CrossRef]
  5. Asmat, U.; Abad, K.; Ismail, K. Diabetes mellitus and oxidative stress-A concise review. Saudi Pharm. J. 2016, 24, 547–553. [Google Scholar] [CrossRef] [Green Version]
  6. Tabák, A.G.; Herder, C.; Rathmann, W.; Brunner, E.J.; Kivimäki, M. Prediabetes: A high-risk state for diabetes development. Lancet 2012, 379, 2279–2290. [Google Scholar] [CrossRef] [Green Version]
  7. Tundis, R.; Loizzo, M.R.; Menichini, F. Natural products as alpha-amylase and alpha-glucosidase inhibitors and their hypoglycaemic potential in the treatment of diabetes: An update. Mini Rev. Med. Chem. 2010, 10, 315–331. [Google Scholar] [CrossRef]
  8. Rajan, L.; Palaniswamy, D.; Mohankumar, S.K. Targeting obesity with plant-derived pancreatic lipase inhibitors: A comprehensive review. Pharmacol. Res. 2020, 155, 104681–104808. [Google Scholar] [CrossRef]
  9. Amorati, R.; Foti, M.C.; Valgimigli, L. Antioxidant activity of essential oils. J. Agric. Food. Chem. 2013, 61, 10835–10847. [Google Scholar] [CrossRef] [PubMed]
  10. Hazrati, S.; Ebadi, M.-T.; Mollaei, S.; Khurizadeh, S. Evaluation of volatile and phenolic compounds, and antioxidant activity of different parts of Ferulago angulata (Schlecht.) Boiss. Ind. Crops Prod. 2019, 140, 111589. [Google Scholar]
  11. Pirbalouti, A.G.; Craker, L.; Alavi-Samani, S.M. Phytochemistry and antioxidant activity of essential oils of condiment and spice plants from South Western, Iran. J. Eng. Appl. Sci. 2018, 13, 204–207. [Google Scholar] [CrossRef]
  12. Celik, A.; Arslan, I.; Herken, E.N.; Ermis, A. Constituents, oxidant-antioxidant profile, and antimicrobial capacity of the essential oil obtained from Ferulago sandrasica Peşmen and Quézel. Int. J. Food Prop. 2013, 16, 1655–1662. [Google Scholar] [CrossRef]
  13. Hichri, F.; Omri, A.; Hossan, A.S.M.; Ben Jannet, H. Alpha-glucosidase and amylase inhibitory effects of Eruca vesicaria subsp. longirostris essential oils: Synthesis of new 1,2,4-triazole-thiol derivatives and 1,3,4-thiadiazole with potential inhibitory activity. Pharm Biol. 2019, 57, 564–570. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Oboh, G.; Olasehinde, T.; Ademosun, A. Inhibition of enzymes linked to type-2 diabetes and hypertension by essential oils from peels of orange and lemon. Int. J. Food Prop. 2017, 20, S586–S594. [Google Scholar] [CrossRef] [Green Version]
  15. Hadrich, F.; Cher, S.; Gargouri, Y.T.; Adel, S. Antioxidant and lipase inhibitory activities and essential oil composition of pomegranate peel extracts. J. Oleo Sci. 2014, 63, 515–525. [Google Scholar] [CrossRef] [Green Version]
  16. Noor, Z.I.; Ahmed, D.; Rehman, H.M.; Qamar, M.T.; Froeyen, M.; Ahmad, S.; Mirza, M.U. In vitro antidiabetic, anti-obesity and antioxidant analysis of Ocimum basilicum aerial biomass and in silico molecular docking simulations with alpha-amylase and lipase enzymes. Biology 2019, 8, 92. [Google Scholar] [CrossRef] [Green Version]
  17. Adams, R. Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, 4th ed.; Allured Publishing Corp.: Carol Stream, IL, USA, 2007. [Google Scholar]
  18. Ruberto, G.; Biondi, D.; Renda, A. The composition of the volatile oil of Ferulago nodosa obtained by steam distillation and supercritical carbon dioxide extraction. Phytochem. Anal. 1999, 10, 241–246. [Google Scholar] [CrossRef]
  19. Maggio, A.; Faraone, N.; Rosselli, S.; Raimondo, F.M.; Spadaro, V.; Bruno, M. Monoterpene derivatives from the flowers of Ferulago campestris, (Apiaceae). Nat. Prod. Res. 2013, 27, 1827–1831. [Google Scholar] [CrossRef]
  20. Riela, S.; Bruno, M.; Rosselli, S.; Saladino, M.L.; Caponetti, E.; Formisano, C.; Senatore, F. A study on the essential oil of Ferulago campestris: How much does extraction method influence the oil composition? J. Sep. Sci. 2011, 34, 483–492. [Google Scholar] [CrossRef] [Green Version]
  21. Ruberto, G.; Cannizzo, S.; Amico, V.; Bizzini, M.; Plattelli, M. Chemical constituents of Ferulago nodosa. J. Nat. Prod. 1994, 57, 1731–1733. [Google Scholar] [CrossRef]
  22. Özkan, A.M.G.; Demirci, B.; Demirci, F.; Başer, K.H.C. Composition and antimicrobial activity of essential oil of Ferulago longistylis Boiss. fruits. J. Ess. Oil Res. 2008, 20, 569–573. [Google Scholar] [CrossRef]
  23. Maggi, F.; Tirillini, B.; Papa, F.; Sagratini, G.; Vittori, S.; Cresci, A.; Coman, M.M.; Cecchini, C. Chemical composition and antimicrobial activity of the essential oil of Ferulago campestris (Besser) Grecescu growing in central Italy. Flavour Frag. J. 2009, 24, 309–315. [Google Scholar] [CrossRef]
  24. Demetzos, C.; Perdetzoglou, D.; Gazouli, M.; Tan, K.; Economakis, C. Chemical analysis and antimicrobial studies on three species of Ferulago from Greece. Planta Med. 2000, 66, 560–563. [Google Scholar] [CrossRef]
  25. Evergetis, E.; Michaelakis, A.; Haroutounian, S.A. Essential oils of umbelliferae family taxa as potent agents for mosquito control. In Integrated Pest Management and Pest Control; Larramendy, M.L., Soloneski, L., Eds.; InTech—Open Access Publisher: Rijeka, Croatia, 2012; pp. 613–637. [Google Scholar] [CrossRef] [Green Version]
  26. Cecchini, C.; Coman, M.M.; Cresci, A.; Tirillini, B.; Cristalli, G.; Papa, F.; Sagratini, G.; Vittori, S.; Maggi, F. Essential oil from fruits and roots of Ferulago campestris (Besser) Grecescu (Apiaceae): Composition and antioxidant and anti-Candida activity. Flavour Frag. J. 2010, 25, 493–502. [Google Scholar] [CrossRef]
  27. Ghasemi Pirbalouti, A.; Izadi, A.; Malek Poor, F.; Hamedi, B. Chemical composition, antioxidant and antibacterial activities of essential oils from Ferulago angulata. Pharm. Biol. 2016, 54, 2515–2520. [Google Scholar] [CrossRef] [Green Version]
  28. Tavakoli, S.; Yassa, N.; Delnavazi, M.R.; Akhbari, M.; Hadjiakhoondi, A.; Hajimehdipoor, H.; Khalighi-Sigaroodi, F.; Hajiaghaee, R. Chemical composition and biological activities of the essential oils from different parts of Ferulago trifida Boiss. J. Essent. Oil Res. 2017, 29, 407–419. [Google Scholar] [CrossRef]
  29. Karakaya, S.; Koca, M.; Simsek, D.; Bostanlik, D.F.; Ozbek, H.; Kiliç, C.S.; Güvenalp, G.; Demirci, B.; Altanlar, N. Antioxidant, antimicrobial and anticholinesterase activities of Ferulago pauciradiata Boiss. & Heldr. growing in Turkey. JBAPN 2018, 8, 364–375. [Google Scholar]
  30. Shahbazi, Y.; Shavisi, N. Chemical composition, antioxidant and antimicrobial activities of the essential oil and methanolic extract of Ferulago bernardii Tomk. & M. Pimen of Iran. Arch. Phytopathol. Pflanzenschutz 2015, 48, 699–710. [Google Scholar] [CrossRef]
  31. Farideh, A.; Zeinab, S.; Zareei, A.; Mohammadi, A. Phenolic contents, antibacterial and antioxidant activities of flower, leaf and stem extracts of Ferulago angulata (schlecht) Boiss. Int. J. Pharm. Pharm. Sci. 2014, 6, 123–125. [Google Scholar]
  32. Golezar, E.; Mdiuni, H.; Nazari, A. Different antioxidant activity measurements of the aerial parts of Ferulago angulata, traditional food additives in Iran. Indian J. Pharm. Sci. 2017, 79, 900–906. [Google Scholar] [CrossRef]
  33. Rezagholizadeh, L. The effect of hydroalcoholic extract of Ferulago angulata on liver function parameters and antioxidant status in alloxan-induced diabetic rats. J. Med. Plants Res. 2017, 20, 1–9. [Google Scholar] [CrossRef] [Green Version]
  34. Mileski, K.; Džamić, A.; Ćirić, A.; Ristić, M.S.; Grujić, S.; Matevski, V.; Marin, P. Composition, antimicrobial and antioxidant properties of endemic species Ferulago macedonica Micevski & E. Mayer. Rec. Nat. Prod. 2015, 9, 208–223. [Google Scholar]
  35. Golfakhrabadi, F.; Shams Ardekani, M.R.; Saeidnia, S.; Yousefbeyk, F.; Jamalifar, H.; Ramezani, N.; Akbarzadeh, T.; Khanavi, M. Phytochemical analysis, antimicrobial, antioxidant activities and total phenols of Ferulago carduchorum in two vegetative stages (flower and fruit). Pak. J. Pharm. Sci. 2016, 29, 623–628. [Google Scholar] [PubMed]
  36. Do Nascimento, K.F.; Moreira, F.M.F.; Alencar Santos, J.; Leite Kassuya, C.A.; Croda, J.H.R.; Cardoso, C.A.L.; do Carmo Vieira, M.; Ruiz, A.L.T.G.; Foglio, M.A.; de Carvalho, J.E.; et al. Antioxidant, anti-inflammatory, antiproliferative and antimycobacterial activities of the essential oil of Psidium guineense Sw. and spathulenol. J. Ethnopharmacol. 2018, 210, 351–358. [Google Scholar] [CrossRef]
  37. Coté, H.; Boucher, M.A.; Pichette, A.; Legault, J. Anti-Inflammatory, antioxidant, antibiotic, and cytotoxic activities of Tanacetum vulgare L. essential oil and its constituents. Medicines 2017, 4, 34. [Google Scholar] [CrossRef]
  38. Karakaya, S.; Gözcü, S.; Güvenalp, Z.; Özbek, H.; Yuca, H.; Dursunoğlu, B.; Kazaz, C.; Kılıç, C.S. The α-amylase and α-glucosidase inhibitory activities of the dichloromethane extracts and constituents of Ferulago bracteata roots. Pharm. Biol. 2018, 56, 18–24. [Google Scholar] [CrossRef] [Green Version]
  39. Musavi-Ezmareh, S.F.; Mazani, M.; Heidarian, E.; Reza, A.M.; Rafieian-Kopaei, M.; Ebrahimi, M.; Shahinfard, N.; Ghezel-Sofli, E. Effect of hydroalcoholic extract of Chevil (Ferulago angulata) on glucose and lipid in diabetic male rats. Iranian J. Clin. Endocrinol. Metab. 2015, 17, 230–237. [Google Scholar]
  40. Rafieian-kopaei, M.; Shahinfard, N.; Rouhi-Boroujeni, H.; Gharipour, M.; Darvishzadeh-Boroujeni, P. Effects of Ferulago angulata extract on serum lipids and lipid peroxidation. Evid. Based Compl. Altern. Med. 2014, 2014, 1–4. [Google Scholar] [CrossRef] [Green Version]
  41. Parsamehr, R.; Bohlouli, S. The effect of Ferulago angulata (Schelchet) Boiss on blood glucose levels and suppression of diabetes in rats. Acta Vet. Brno 2019, 88, 349–354. [Google Scholar] [CrossRef]
  42. Özbek, H.; Yilmaz, B.S. Anti-inflammatory and hypoglycemic activities of alpha-pinene. Acta Pharm. Sci. 2017, 55, 7–14. [Google Scholar] [CrossRef] [Green Version]
  43. Bae, G.S.; Park, K.C.; Choi, S.B.; Jo, I.J.; Choi, M.O.; Hong, S.H.; Song, K.; Song, H.J.; Park, S.J. Protective effects of alpha-pinene in mice with cerulein-induced acute pancreatitis. Life Sci. 2012, 91, 866–871. [Google Scholar] [CrossRef] [PubMed]
  44. Kumawat, V.S.; Kaur, G. Insulinotropic and antidiabetic effects of β-caryophyllene with l -arginine in type 2 diabetic rats. J. Food Biochem. 2020, 44, e13156. [Google Scholar] [CrossRef] [PubMed]
  45. Zhou, L.; Zhan, M.L.; Tang, Y.; Xiao, M.; Li, Q.S.; Yang, L.; Li, X.; Chen, W.W.; Wang, Y.L. Effects of β-caryophyllene on arginine ADP-ribosyltransferase 1-mediated regulation of glycolysis in colorectal cancer under high-glucose conditions. Int. J. Oncol. 2018, 53, 1613–1624. [Google Scholar] [CrossRef] [Green Version]
  46. Basha, R.H.; Sankaranarayanan, C. β-Caryophyllene, a natural sesquiterpene, modulates carbohydrate metabolism in streptozotocin-induced diabetic rats. Acta Histochem. 2014, 116, 1469–1479. [Google Scholar] [CrossRef]
  47. Ben Jemia, M.; Rouis, Z.; Maggio, A.; Venditti, A.; Bruno, M.; Senatore, F. Chemical composition and free radical scavenging activity of the essential oil of Achillea ligustica All. wild growing in Lipari (Aeolian Islands, Sicily). Nat. Prod. Commun. 2013, 8, 1629–1632. [Google Scholar]
  48. NIST 17. Mass Spectral Library (NIST/EPA/NIH); National Institute of Standards and Technology: Gaithersburg, MD, USA, 2017. [Google Scholar]
  49. FFNSC 2. Flavors and Fragrances of Natural and Synthetic Compounds: Mass Spectral Database; Wiley: Kyoto, Japan, 2012. [Google Scholar]
  50. Loizzo, M.R.; Leporini, M.; Sicari, V.; Falco, T.; Pellicanò, M.T.; Tundis, R. Investigating the in vitro hypoglycemic and antioxidant properties of Citrus × clementina Hort Juice. Eur. Food Res. Technol. 2018, 244, 523–534. [Google Scholar] [CrossRef]
  51. Sicari, V.; Loizzo, M.R.; Branca, V.; Pellicanò, T.M. Bioactive and Antioxidant Activity from Citrus bergamia Risso (Bergamot) Juice Collected in Different Areas of Reggio Calabria Province, Italy. Int. J. Food Prop. 2016, 19, 1962–1971. [Google Scholar] [CrossRef] [Green Version]
  52. Leporini, M.; Loizzo, M.R.; Sicari, V.; Pellicanò, T.M.; Reitano, A.; Dugay, A.; Deguin, B.; Tundis, R. Citrus × clementina Hort. juice enriched with its by-products (peels and leaves): Chemical composition, in vitro bioactivity, and impact of processing. Antioxidants 2020, 9, 298. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Leporini, M.; Tundis, R.; Sicari, V.; Pellicanò, T.M.; Dugay, A.; Deguin, B.; Loizzo, M.R. Impact of extraction processes on phytochemicals content and biological activity of Citrus × clementina Hort. Ex Tan leaves: New opportunity for under-utilized food by-products. Food Res. Int. 2020, 127, 108742. [Google Scholar] [CrossRef]
Sample Availability: Samples of the essentail oil is not available.
Table
Table 1. Chemical composition of the essential oil of the aerial parts (leaves and stems) of F. nodosa subsp. geniculata from Sicily.
Table 1. Chemical composition of the essential oil of the aerial parts (leaves and stems) of F. nodosa subsp. geniculata from Sicily.
CompoundRi aRi ba.p. (%) c
Santolina triene9049060.8 ± 0.07
Tricyclene914921t
α-Thujene918924t
α-Pinene9239322.9 ± 0.30
Camphene9369460.3 ± 0.02
Sabinene9629690.5 ± 0.04
β-Pinene9659740.2 ± 0.02
Dehydro-1,8-cineole9849880.1 ± 0.01
Myrcene9859880.8 ± 0.07
δ-2-Carene99510010.2 ± 0.02
m-Mentha-1(7),8-diene10001000t
(3Z)-Hexenyl acetate10071004t
1,2,4-Trimethyl benzene101610210.2 ± 0.02
p-Cymene101910200.9 ± 0.08
Limonene + β-Phellandrene10221024 + 10251.8 ± 0.11
(Z)-β-Ocimene103410320.1 ± 0.01
β-Isophorone103610440.1 ± 0.01
Benzene acetaldehyde10401036t
(E)-β-Ocimene104310440.3 ± 0.02
γ-Terpinene10531054t
Terpinolene10821086t
p-Cymenene10841089t
6-Camphenone108910950.1 ± 0.01
α-Pinene oxide109010990.3 ± 0.02
Isophorone111511180.2 ± 0.01
α-Campholenal11211122t
cis-Limonene oxide11281132t
trans-Pinocarveol11311135t
trans-p-Menth-2-en-1-ol113411360.1 ± 0.01
Camphor11361141t
trans-Verbenol113911400.1 ± 0.01
1,4-Dimethyl-δ-3-tetrahydroacetophenone11451152t
Borneol115711650.5 ± 0.04
(E)-Isocitral116811770.1 ± 0.01
Terpinen-4-ol11711174t
2,4-Dimethyl-benzaldehyde117611780.6 ± 0.05
Cryptone117911830.4 ± 0.03
p-Cymen-8-ol118111790.2 ± 0.02
cis-Piperitol118911950.1 ± 0.01
trans-Piperitol120312070.1 ± 0.01
4-methylene-Isophorone12091216t
β-Cyclocitral12141217t
Cumin aldehyde123312380.1 ± 0.01
cis-Chrysanthenyl acetate125612611.0 ± 0.12
Bornyl acetate127912874.6 ± 0.51
trans-Sabinyl acetate128712890.2 ± 0.01
trans-Pinocarvyl acetate129312980.2 ± 0.02
Carvacrol130212980.2 ± 0.01
2,3,4-Trimethyl benzaldehyde130613151.0 ± 0.11
Myrtenyl acetate131913240.1 ± 0.01
δ-Elemene132913350.3 ± 0.02
2,3,6-Trimethyl benzaldehyde1346135219.0 ± 1.89
α-Copaene136413740.1 ± 0.01
β-Bourbonene137213870.8 ± 0.07
β-Cubebene138013870.1 ± 0.01
β-Elemene138213890.7 ± 0.06
α-Cedrene139614100.2 ± 0.01
(E)-Caryophyllene140514175.4 ± 0.58
β-Copaene141514300.2 ± 0.02
Aromadendrene142314390.2 ± 0.02
α-Humulene143714520.5 ± 0.06
cis-Cadina-1(6),4-diene145014610.1 ± 0.01
α-Acoradiene145114640.1 ± 0.01
γ-Muurolene146314780.1 ± 0.01
Germacrene D146514841.3 ± 0.14
γ-Gurjunene146914750.1 ± 0.01
α-Curcumene147214790.5 ± 0.04
(E)-β-ionone147414870.2 ± 0.01
Bicyclogermacrene147915000.9 ± 0.10
α-Muurolene148615000.1 ± 0.01
Cuparene148715040.1 ± 0.01
β-Bisabolene149715050.3 ± 0.03
α-Cuprenene149915050.3 ± 0.04
(E)-Nerolidol155515610.2 ± 0.02
Spathulenol156215779.0 ± 0.97
Caryophyllene oxide156515825.4 ± 0.51
Viridiflorol157415920.5 ± 0.04
Cubeban-11-ol157715950.3 ± 0.02
Rosifoliol158416000.6 ± 0.05
Humulene epoxide II159016080.5 ± 0.04
trans-Isolongifolanone160516250.2 ± 0.01
epi-α-Muurolol162616400.5 ± 0.06
α-Cadinol163916520.3 ± 0.02
Neophytadiene183418380.2 ± 0.01
Phytone183918430.2 ± 0.02
Benzyl salicylate185218640.1 ± 0.01
Hexadecanoic acid196119590.2 ± 0.01
Phytol209921031.6 ± 0.18
Tricosane230123000.1 ± 0.01
Pentacosane250025000.1 ± 0.01
Heptacosane270027000.2 ± 0.02
Nonacosane290029002.5 ± 0.26
Class of Compounds ±0.07
Oxygenated Monoterpene 8.4
Monoterpene Hydrocarbons 8.8
Sesquiterpene Hydrocarbons 12.4
Oxygenated Sesquiterpene 17.5
Aromatic 21.0
Others 5.8
Total 73.9
Ri a: retention index on a HP-5MS column; Ri b: retention index from Adams [17]; c: relative peak area ± standard deviation (S.D.) (n = 3); t: traces.
Table
Table 2. The antioxidant potential of F. nodosa subsp. geniculata.
Table 2. The antioxidant potential of F. nodosa subsp. geniculata.
DPPH Test
IC50 (µg/mL)		ABTS Test
IC50 (µg/mL)		β-Carotene Bleaching Test
(IC50, µg/mL or % Inhibition)		FRAP
μM Fe (II)/g
t 30 min at 60 min a
Essential oil26.3 ± 4.314.0 ± 1.139.4%32.7%16.9 ± 1.3
Positive control
Ascorbic acid5.1 ± 0.821.7 ± 0.3
Propyl gallate 0.09 ± 0.080.09 ± 0.06
BHT 63.4 ± 4.6
Data are expressed as means ± S.D. (n = 3). a: at maximum concentration tested of 100 μg/mL.
Table
Table 3. Hypoglycemic and hypolipidemic potential (IC50, µg/mL) of F. nodosa subsp. geniculata.
Table 3. Hypoglycemic and hypolipidemic potential (IC50, µg/mL) of F. nodosa subsp. geniculata.
α-Amylaseα-GlucosidaseLipase
Essential oil196.4 ± 4.3365.9 ± 5.142.0 ± 2.1
Positive control
Acarbose50.6 ± 0.9 35.8 ± 1.3
Orlistat 37.4 ± 1.1
Data are expressed as means ± S.D. (n = 3).

Share and Cite

MDPI and ACS Style

Badalamenti, N.; Ilardi, V.; Rosselli, S.; Bruno, M.; Maggi, F.; Leporini, M.; Falco, T.; Loizzo, M.R.; Tundis, R. Ferulago nodosa Subsp. geniculata (Guss.) Troia & Raimondo from Sicily (Italy): Isolation of Essential Oil and Evaluation of Its Bioactivity. Molecules 2020, 25, 3249. https://doi.org/10.3390/molecules25143249

AMA Style

Badalamenti N, Ilardi V, Rosselli S, Bruno M, Maggi F, Leporini M, Falco T, Loizzo MR, Tundis R. Ferulago nodosa Subsp. geniculata (Guss.) Troia & Raimondo from Sicily (Italy): Isolation of Essential Oil and Evaluation of Its Bioactivity. Molecules. 2020; 25(14):3249. https://doi.org/10.3390/molecules25143249

Chicago/Turabian Style

Badalamenti, Natale, Vincenzo Ilardi, Sergio Rosselli, Maurizio Bruno, Filippo Maggi, Mariarosaria Leporini, Tiziana Falco, Monica R. Loizzo, and Rosa Tundis. 2020. "Ferulago nodosa Subsp. geniculata (Guss.) Troia & Raimondo from Sicily (Italy): Isolation of Essential Oil and Evaluation of Its Bioactivity" Molecules 25, no. 14: 3249. https://doi.org/10.3390/molecules25143249

Article Metrics

Back to TopTop