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Article

Phytochemical Composition and In Vitro Antioxidant, Anti-Inflammatory, Anticancer, and Enzyme-Inhibitory Activities of Artemisia nilagirica (C.B. Clarke) Pamp

by
Jawaher J. Albaqami
1,†,
Tancia P. Benny
2,†,
Hamida Hamdi
1,3,
Ammar B. Altemimi
4,5,
Aswathi Moothakoottil Kuttithodi
2,
Joice Tom Job
2,*,
Anju Sasidharan
2 and
Arunaksharan Narayanankutty
2,*
1
Department of Biology, College of Science, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia
2
Division of Cell and Molecular Biology, PG and Research Department of Zoology, St. Joseph’s College (Autonomous), Devagiri, Calicut 673 008, Kerala, India
3
Zoology Department, Faculty of Science, Cairo University, Giza 12613, Egypt
4
Department of Food Science, College of Agriculture, University of Basrah, Basrah 61004, Iraq
5
College of Medicine, University of Warith Al-Anbiyaa, Karbala 56001, Iraq
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Molecules 2022, 27(20), 7119; https://doi.org/10.3390/molecules27207119
Submission received: 27 September 2022 / Revised: 14 October 2022 / Accepted: 18 October 2022 / Published: 21 October 2022
(This article belongs to the Special Issue Natural Bioactive Compounds and Human Health)

Abstract

:
Plants have been employed in therapeutic applications against various infectious and chronic diseases from ancient times. Various traditional medicines and folk systems have utilized numerous plants and plant products, which act as sources of drug candidates for modern medicine. Artemisia is a genus of the Asteraceae family with more than 500 species; however, many of these species are less explored for their biological efficacy, and several others are lacking scientific explanations for their uses. Artemisia nilagirica is a plant that is widely found in the Western Ghats, Kerala, India and is a prominent member of the genus. In the current study, the phytochemical composition and the antioxidant, enzyme-inhibitory, anti-inflammatory, and anticancer activities were examined. The results indicated that the ethanol extract of A. nilagirica indicated in vitro DPPH scavenging (23.12 ± 1.28 µg/mL), ABTS scavenging (27.44 ± 1.88 µg/mL), H2O2 scavenging (12.92 ± 1.05 µg/mL), and FRAP (5.42 ± 0.19 µg/mL). The anti-inflammatory effect was also noticed in the Raw 264.7 macrophages, where pretreatment with the extract reduced the LPS-stimulated production of cytokines (p < 0.05). A. nilagirica was also efficient in inhibiting the activities of α-amylase (38.42 ± 2.71 µg/mL), α-glucosidase (55.31 ± 2.16 µg/mL), aldose reductase (17.42 ± 0.87 µg/mL), and sorbitol dehydrogenase (29.57 ± 1.46 µg/mL). It also induced significant inhibition of proliferation in breast (MCF7 IC50 = 41.79 ± 1.07, MDAMB231 IC50 = 55.37 ± 2.11µg/mL) and colon (49.57 ± 1.46 µg/mL) cancer cells. The results of the phytochemical screening indicated a higher level of polyphenols and flavonoids in the extract and the LCMS analysis revealed the presence of various bioactive constituents including artemisinin.

1. Introduction

Medicinal plants are important sources of various biologically and pharmacologically active compounds [1,2]. Several traditional medicinal plants have been shown to have strong pharmacological properties, such as radical neutralizing, inflammation-preventing, antiproliferative, hypolipidemic, hepatoprotective, neuroprotective, antithrombotic, and immunomodulatory activities [3,4]. Among the various plant families, Asteraceae is one of the most widely utilized ones, and it is also equipped with numerous biological and pharmacological activities. Among the various genera, the Artemesia genus is well-known [5,6,7].
The Artemisia genus and the member species are well-studied for their various biological activities [8,9,10,11,12,13]. Artemisia annua L. has demonstrated significant medicinal benefits because of the presence of artemisinin [14]. Artemisia mongolica is another important member of the genus, which is rich in lactone derivatives of Sesquiterpene and a wide range of pharmacological activities [15]. The different species of the genus were found to have strong antibacterial and antifungal properties against pathogenic organisms in humans, livestock, and plants [16,17,18,19,20]. Antiproliferative and apoptotic effects are attributed to the bioactive compounds and extracts of various species of Artemisia [21,22,23,24].
Artemisia nilagirica is distributed throughout the Western Ghats, India; it has been traditionally applied by various tribal healers in the area for the treatment of infectious diseases and toxicity prevention. The plant has been shown to have significant biological and pharmacological activities based on various in vitro and in vivo studies. The initial studies by Ahameethunisa and Hopper [25] identified the antibacterial potential of the methanol extract of A. nilagirica against 15 bacterial strains. Further, the extract was found to be effective against Mycobacterium smegmatis and M. bovis [26]. The extract was also found to be effective against the malarial parasite Plasmodium falciparum [27].
The anticancer activities of the methanol and ethyl acetate extracts were also elucidated against the human monocytic leukemia cell (THP-1) [28]. Later, studies by Sahu, Meena, Shukla, Chaturvedi, Kumar, Datta, and Arya [24] also supported these results in colorectal cancer cell models. Studies by Raju et al. [29] indicated that the anticancer activity was mediated through the inhibition of TGF-beta signaling. The plant extract was also found to inhibit inflammatory insults in human red blood cell models [30]. The fruit of A. nilagirica was found to have significant antiradical activity via scavenging DPPH and nitric oxide radicals [31]. The essential oil extracted from A. nilagirica was a rich source of monoterpenoid compounds such as thujone, and by virtue of these compounds, the essential oil inhibited the growth of various fungal pathogens [32]. The essential oil was also effective against the phytopathogenic fungal groups of table grapes [33]. Additionally, the essential oil was also effective against various bacterial populations and capable of repelling mosquitoes [34].
Although several studies have reported the preliminary pharmacological activity of the plant, there is no clear-cut information on its quantitative chemical profile and nutritional value. Additionally, the anti-inflammatory properties are yet to be discovered in cell line models, and its mechanism of action is also not specified. Therefore, the present study aimed to analyze the chemical composition of the ethanol extract of Artemisia nilagirica leaves in terms of the bioactive compounds and proximate composition, as well as their antioxidant potential. Further, this study for the first time attempted to analyze the enzyme-inhibitory and anti-inflammatory activities of the extract in Raw 264.7 cells stimulated by lipopolysaccharides.

2. Results and Discussion

2.1. Determination of Proximate Composition of A. nilagirica

The Artemisia species, which includes 200–400 identified plants, are extensively spread in tropical and temperate areas [6]. The importance of the artemisia species in traditional medicine is well established [5]. The plant’s antiviral, antifungal, antibiotic, insecticidal, hepatoprotective, and neuroprotective qualities make it useful in both Chinese and Ayurvedic medical systems [35]. The current study examined a specific member Artemisia nilagirica, its phytochemical makeup, and its pharmacological effects.
The physicochemical parameters of the A. nilagirica leaf powder are shown in Table 1. The predominant compounds were carbohydrate, protein, fat, and ash contents. The moisture content was estimated to be 87.4 ± 2.12%.

2.2. Quantitative and Qualitative Estimation of Phytochemicals in A. nilagirica

The qualitative phytochemical screening identified the presence of compounds such as alkaloids, flavonoids, glycosides, sterols, and triterpenes (Table 2). The LCMS analysis of the A. nilagirica ethanol extract indicated the presence of various phytocompounds, including artemisinin, quercetin, apigenin, Β-caryophyllene, luteolin, and simple phenolic acids (Figure 1 and Table 3). Previous reports have also confirmed that numerous kinds of bioactive substances are found in A. vulgaris, A. annua, and other species, including flavonoids, sesquiterpenoids, essential oils, tannins, phenols, and saponins [15,36]. The total polyphenol content of A. nilagirica was estimated to be 89.51 ± 2.5 mg gallic acid equivalent/g of extract. The total flavonoid content was 14.35 ± 0.9 mg quercetin equivalent/g of extract (Table 4). Further, the HPLC quantification indicated higher levels of quercetin (240.39 ± 4.87 µg/g extract), luteolin (146.87 ± 5.29 µg/g extract), and apigenin (103.41 ± 3.35 µg/g extract) in the A. nilagirica extract (Table 5). These compounds are known to possess strong anti-inflammatory, antiproliferative and antidiabetic activities [37,38,39,40].

2.3. In Vitro Antioxidant Activities of A. nilagirica Extract

The Artemisia genus members frequently display antioxidant activity [41]; our study also confirmed the antioxidant activity of A. nilagirica for the first time in terms of the radical generation inhibition and reducing potentials. The IC50 value of the A. nilagirica extract in the anti-DPPH radical assay was estimated to be 23.12 ± 1.28 µg/mL. Likewise, Table 6 shows the other antioxidant activities in terms of the ABTS radical scavenging activity, hydrogen peroxide scavenging potential, and ferric-reducing antioxidant power; the respective IC50 values were found to be 27.44 ± 1.88, 12.92 ± 1.05, and 5.42 ± 0.19 µg/mL. On the contrary, the level of inhibition of nitric oxide radical generation (IC50) was determined to be 367.09 ± 12.05 µg/mL for the extract. However, in comparison with the standard antioxidant ascorbic acid (Table 6), the activity was much lower in the A. nilagirica extract; further purification of the extract may yield more active antioxidant compounds. The antioxidant properties are attributed to the bioactive compounds identified in the plant via LC-MS. Oxidative stress is the central independent factor that drives many chronic diseases, including cancers [42,43]; hence, the antioxidant properties of the plant may be useful in the management of diseases associated with oxidative stress.

2.4. Enzyme-Inhibitory Activities of A. nilagirica Ethanol Extract

The enzyme-inhibitory properties of the extract were analyzed against four enzymes involved in type 2 diabetes mellitus, including α-amylase, α-glucosidase, aldose reductase, and sorbitol dehydrogenase (Table 7). The IC50 values for these enzymes were 38.42 ± 2.71, 55.31 ± 2.16, 17.42 ± 0.87, and 29.57 ± 1.46 µg/mL, respectively. Furthermore, α-amylase and α-glucosidase are enzymes involved in carbohydrate metabolism and are common targets of antidiabetic drugs [44]. Similarly, the polyol pathway enzymes, including aldose reductase and sorbitol dehydrogenase, are involved in diabetic complications [45,46]. Hence, the inhibition of these enzymes could result in strong antidiabetic activity for the A. nilagirica extract.

2.5. Antiproliferative Activity of the A. nilagirica

Additionally, the results showed the anticancer properties of A. nilagirica in human breast and colon cancer cells. The anticancer activity was analyzed in three cancer cell lines, including MCF-7, MDA-MB-231, and HCT-15. We observed dose-dependent cytotoxicity in these three cell lines (Figure 2). The IC50 values against the three cells were estimated to be 41.79 ± 1.07, 55.37 ± 2.11, and 49.57 ± 1.46 µg/mL, respectively. In comparison, the standard cyclophosphamide was more toxic to these cells, with respective IC50 values of 3.12 ± 0.13, 5.74 ± 0.20, and 6.04 ± 0.21 µg/mL. Previous studies have also shown different species of Artemisia in various cancer cells [47,48,49,50]. In addition, the green synthesized nanoparticles from different Artemisia species are also reported to exert antiproliferative effects on cancer cells mediated through apoptotic cell death [23,51,52]. A study by Sahu, Meena, Shukla, Chaturvedi, Kumar, Datta, and Arya [24] indicated that ethyl acetate and hexane fractions of A. nilagirica induced cell death in colon, lung, and breast cancer cells. In addition, the bioactive compounds, including quercetin, apigenin, and eugenol, have also been shown to have significant antiproliferative effects by modulating different signaling pathways [53,54].

2.6. Anti-Inflammatory Activity of A. nilagirica

The Artemisia nilagirica extract was shown to inhibit the production of nitric oxide radicals in vitro. Further, the pretreatment of the extract also inhibited cytokine production and inflammatory insults in lipopolysaccharide-stimulated macrophages. The LPS is a microbial component that is known to stimulate inflammatory insults [55,56]. The Artemisia nilagirica leaf ethanol extract (AN) was found to inhibit the lipopolysaccharide-induced activation of macrophages and the subsequent cytokine release. The level of IL-1β was found to be significantly increased after LPS stimulation in macrophages; however, the pretreatment with AN at different doses significantly brought down the IL-1β levels in the macrophages (Table 8). Likewise, the levels of IL-6 and TNF-α also showed a similar increase during LPS exposure, which were successfully brought down by the treatment with different concentrations of A. nilagirica. The level of nitric oxide was determined biochemically and was also significantly elevated in LPS control cells. Pretreatment with 2.5, 5.0, and 7.5 µg/mL of AN successfully brought down the levels to 40.7 ± 1.6 (p < 0.05), 32.2 ± 2.4 (p < 0.05), and 25.7 ± 2.1 (p < 0.01). In addition, it is noted that the high dose of the extract resulted in stronger anti-inflammatory molecules compared to quercetin, which is a well-known anti-inflammatory molecule [57,58]. The LPS is known to stimulate cytokine production in macrophages by upregulating the NF-κB translocation to the nuclear compartment [59,60]. It is, therefore, possible that the A. nilagirica extract may also influence the LPS-induced activation of intracellular NF-KB signaling.
Thus, the study concludes that the Artemisia nilagirica ethanol extract exhibits antioxidant and anti-inflammatory properties in vitro and cultured cells. Further, the extract is also capable of inhibiting the proliferation of various cancer cells. The inhibition of enzymes associated with type 2 diabetes mellitus is also indicative of its anti-diabetic properties. The biological properties of the plant are expected to be due to the bioactive compounds identified in the A. nilagirica extract.

3. Materials and Methods

3.1. Artemisia Nilagirica (C.B.Clarke) Pamp. Collection and Extraction Using 100% Ethanol

The Artemisia nilagirica plant samples were collected from the Wayanad District, Kerala (11.7917° N, 76.1716° E). The mature leaves were carefully cleaned of all kinds of dust via washing. These leaves were dried under shade for 2 weeks and powdered using a mixer grinder; the powder was extracted with 100% ethanol using the Soxhlet method. Briefly, 100 g of the powder was extracted with ethanol at 80 °C for 8 h and the extract was collected, filtered, and concentrated before storage.

3.2. Phytochemical Analysis of Artemesia nilagirica

The leaf powder of A. nilagirica was analyzed for the proximate composition according to the methods used by Shukla et al. [61]. The qualitative phytochemical screening was carried out for the detection of alkaloids, flavonoids, glycosides, sterols, and triterpenes by referring to standard protocols [62,63]. The LC-MS analysis (Shimadzu LC- 8045, Kyoto, Japan) was used for phytochemical screening [64]; briefly, the C18 column measuring 4.6  ×  150 mm and 5 μm in size was used for the study, with methanol (A) and water with 0.1% formic acid (B) as the mobile phase (gradient elution mode). The gradient was set as 95% solution A (0–5 min), 70% solution A (5 to 10 min), 65% solution A (10 to 20 min), 50% solution A (20 to 30 min), and 90% of solution B (until 50 min), with a flow rate of 1.0 mL/min.
The quantitative profiling was estimated in terms of the total polyphenols [65] and total flavonoids [66], and the concentrations of ferulic acid, luteolin, caffeic acid, quercetin, and apigenin were determined using an HPLC analysis according to the same LC-MS conditions mentioned above.

3.3. Analysis of the Antioxidant Activity of A. nilagirica Ethanol Extract

The antioxidant activities were determined as the scavenging potentials of different radicals, including diphenyl picryl hydrazyl (DPPH), ABTS [67], and hydrogen peroxide [68]; the reducing potential on ferric ions was also estimated using the procedures described in [69]. The nitric oxide radical removal rate was used as an indicator of the inflammatory process inhibition model [70]. The DPPH was dissolved in methanol (0.1 mM) and varying concentrations of the extract were mixed with it. The solution was incubated for 20 min in the dark at 30 °C and the change in absorbance was used to estimate the percentage inhibition. Likewise, the ABTS radical generated was mixed with different doses of the A. nilagirica extract and the % inhibition was calculated spectrophotometrically. The nitric oxide scavenging was determined using sodium nitroprusside (8 mM) as the radical source; the Griess reagent was used to estimate the nitrite remaining in the treated samples using spectrophotometry at 596 nm.
Ascorbic acid was used as a positive control and standard for the antioxidant assays. The percentage inhibition was determined using the formula
P e r c e n t a g e   i n h i b i t i o n = A b s o r b a n c e   o f   C o n t r o l A b s o r b a n c e   o f   S a m p l e A b s o r b a n c e   o f   C o n t r o l × 100

3.4. Efficacy of A. nilagirica Ethanol Extract on Activities of Enzymes

The enzyme-inhibitory properties were analyzed against the selected enzymes involved in diabetes and secondary diabetic complications. The inhibitory effect on α-amylase [71], α-glucosidase [72], aldose reductase [73], and sorbitol dehydrogenase [46] was assessed according to the standard methods.

3.5. Effect of A. nilagirica Ethanol Extract on Cancer Cell Proliferation

The human breast cancer cell lines MCF7 and MDA-MB-231 and a colon cancer cell line (HCT-15) were collected from NCCS, Pune, India. These cells were maintained in complete MEM, Leibovitz’s L-15, and RPMI-1640 media. The cells were selected as they are widely used in the anticancer screening of phytochemicals.
The inhibitory potential of the extract on human cancer cell proliferation (MCF7, MDA-MB-231, and HCT-15) was assessed using the MTT assay [74]. The IC50 value was determined using probit analysis.

3.6. Effect of A. nilagirica Extract on Lipopolysaccharide-Induced Cytokine Production in Macrophages

The murine Raw 264.7 cells were allowed to attach (1 × 107 cells/mL) in a 24-well plate in complete growth media. The RPMI-1640 media was used to dilute the different concentrations of A. nilagirica (AN) (2.5, 5.0, and 7.5 µg/mL). Next, the cells were exposed to 1 µg/mL lipopolysaccharide for another 24 h. The protein expression of cytokines such as interleukin-1β and interleukin-6 and the tumor necrosis factor-α release were determined using PeproTech ELISA kits (Rocky Hill, CT, USA), as per the commercially prescribed methods. The nitric oxide release was quantified using the Griess reaction method [64]. Quercetin was used as a standard anti-inflammatory compound in the study.

3.7. Presentation of the Data, Software Used, and Statistical Analysis

The accuracy of the results obtained was ensured by conducting three independent assignments, with each having four replicates. Microsoft Excel 2010 was used for data consolidation and verification. The processed data are presented as means ± standard deviations; the IC50 values were estimated using probit analysis (GraphPad Prism 7.0, San Diego, CA, USA).

4. Conclusions

Artemisia nilagirica is an ethnomedicinal plant in India. In our study, the ethanol extract of A. nilagirica leaves showed significant antiradical and reducing potentials, which are indicative of its antioxidant potential. The IC50 values were lower but comparable with those of the standard ascorbic acid. The extract also inhibited enzymes associated with diabetes mellitus, including alpha-amylase and α-glucosidase. Additionally, the extract treatment significantly reduced the proliferative potential of breast and colon cancer cells. In Raw 264.7 macrophages, the pretreatment with the extract inhibited the LPS-stimulated production of cytokines and proved itself to be anti-inflammatory. Most importantly, the higher dose of the extract caused significantly higher activity than the standard quercetin used. Hence, we conclude that the ethanol extract of A. nilagirica leaves has antioxidant, anti-inflammatory, and anticancer properties; further studies on animal models and with bioassay-guided purification are necessary to identify the bioactive components.

Author Contributions

A.N.: Study design, methodology, analysis, manuscript editing. J.J.A. and H.H.: Study design, methodology, experimentation, analysis, funding acquisition, manuscript preparation, manuscript editing. A.M.K., A.S., T.P.B. and J.T.J.: Experimentation, analysis; manuscript draft preparation. A.B.A.: Analysis, manuscript preparation, manuscript editing. All authors have read and agreed to the published version of the manuscript.

Funding

This study received no funding support.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article.

Acknowledgments

ARN and JTJ acknowledge the DBT star scheme for the infrastructural developments in the college. ARN and JTJ is thankful to St. Joseph’s College (Autonomous), Devagiri for the research promotion (seed grant) scheme RPSG-2022-23.

Conflicts of Interest

The authors declare no conflict of interest.

Sample Availability

Samples of the compounds are available from the corresponding author.

References

  1. Behera, N.K.; Mahalakshmi, G.S. A cloud based knowledge discovery framework, for medicinal plants from PubMed literature. Inform. Med. Unlocked 2019, 16, 100105. [Google Scholar] [CrossRef]
  2. Karpavičienė, B. Traditional Uses of Medicinal Plants in South-Western Part of Lithuania. Plants 2022, 11, 2093. [Google Scholar] [CrossRef] [PubMed]
  3. Noor, F.; Tahir ul Qamar, M.; Ashfaq, U.A.; Albutti, A.; Alwashmi, A.S.S.; Aljasir, M.A. Network Pharmacology Approach for Medicinal Plants: Review and Assessment. Pharmaceuticals 2022, 15, 572. [Google Scholar] [CrossRef] [PubMed]
  4. Adeleke, B.S.; Babalola, O.O. Pharmacological Potential of Fungal Endophytes Associated with Medicinal Plants: A Review. J. Fungi 2021, 7, 147. [Google Scholar] [CrossRef] [PubMed]
  5. Septembre-Malaterre, A.; Lalarizo Rakoto, M.; Marodon, C.; Bedoui, Y.; Nakab, J.; Simon, E.; Hoarau, L.; Savriama, S.; Strasberg, D.; Guiraud, P.; et al. Artemisia annua, a Traditional Plant Brought to Light. Int. J. Mol. Sci. 2020, 21, 4986. [Google Scholar] [CrossRef] [PubMed]
  6. Bora, K.S.; Sharma, A. The genus Artemisia: A comprehensive review. Pharm Biol. 2011, 49, 101–109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Bisht, D.; Kumar, D.; Kumar, D.; Dua, K.; Chellappan, D.K. Phytochemistry and pharmacological activity of the genus artemisia. Arch. Pharmacal Res. 2021, 44, 439–474. [Google Scholar] [CrossRef]
  8. Salaroli, R.; Andreani, G.; Bernardini, C.; Zannoni, A.; La Mantia, D.; Protti, M.; Forni, M.; Mercolini, L.; Isani, G. Anticancer activity of an Artemisia annua L. hydroalcoholic extract on canine osteosarcoma cell lines. Res. Vet. Sci. 2022, 152, 476–484. [Google Scholar] [CrossRef]
  9. Baies, M.H.; Gherman, C.; Boros, Z.; Olah, D.; Vlase, A.M.; Cozma-Petrut, A.; Gyorke, A.; Miere, D.; Vlase, L.; Crisan, G.; et al. The Effects of Allium sativum L., Artemisia absinthium L., Cucurbita pepo L., Coriandrum sativum L., Satureja hortensis L. and Calendula officinalis L. on the Embryogenesis of Ascaris suum Eggs during an In Vitro Experimental Study. Pathogens 2022, 11, 1065. [Google Scholar] [CrossRef]
  10. Suroowan, S.; Llorent-Martinez, E.J.; Zengin, G.; Dall’Acqua, S.; Sut, S.; Buskaran, K.; Fakurazi, S.; Mahomoodally, M.F. Phytochemical Characterization, Anti-Oxidant, Anti-Enzymatic and Cytotoxic Effects of Artemisia verlotiorum Lamotte Extracts: A New Source of Bioactive Agents. Molecules 2022, 27, 5886. [Google Scholar] [CrossRef]
  11. Chen, X.Y.; Liu, T.; Hu, Y.Z.; Qiao, T.T.; Wu, X.J.; Sun, P.H.; Qian, C.W.; Ren, Z.; Zheng, J.X.; Wang, Y.F. Sesquiterpene lactones from Artemisia vulgaris L. as potential NO inhibitors in LPS-induced RAW264.7 macrophage cells. Front. Chem. 2022, 10, 948714. [Google Scholar] [CrossRef]
  12. Chen, J.; Chen, F.; Peng, S.; Ou, Y.; He, B.; Li, Y.; Lin, Q. Effects of Artemisia argyi Powder on Egg Quality, Antioxidant Capacity, and Intestinal Development of Roman Laying Hens. Front. Physiol. 2022, 13, 902568. [Google Scholar] [CrossRef]
  13. Su, S.H.; Sundhar, N.; Kuo, W.W.; Lai, S.C.; Kuo, C.H.; Ho, T.J.; Lin, P.Y.; Lin, S.Z.; Shih, C.Y.; Lin, Y.J.; et al. Artemisia argyi extract induces apoptosis in human gemcitabine-resistant lung cancer cells via the PI3K/MAPK signaling pathway. J. Ethnopharmacol. 2022, 299, 115658. [Google Scholar] [CrossRef]
  14. Agrawal, P.K.; Agrawal, C.; Blunden, G. Artemisia Extracts and Artemisinin-Based Antimalarials for COVID-19 Management: Could These Be Effective Antivirals for COVID-19 Treatment? Molecules 2022, 27, 3828. [Google Scholar] [CrossRef]
  15. Zhu, Z.; Turak, A.; Aisa, H.A. Sesquiterpene lactones from Artemisia mongolica. Phytochemistry 2022, 199, 113158. [Google Scholar] [CrossRef]
  16. Zhang, J.J.; Qu, L.B.; Bi, Y.F.; Pan, C.X.; Yang, R.; Zeng, H.J. Antibacterial activity and mechanism of chloroform fraction from aqueous extract of mugwort leaves (Artemisia argyi L.) against Staphylococcus aureus. Lett. Appl. Microbiol. 2022, 74, 893–900. [Google Scholar] [CrossRef]
  17. Wang, Y.; Li, J.; Chen, Q.; Zhou, J.; Xu, J.; Zhao, T.; Huang, B.; Miao, Y.; Liu, D. The role of antifungal activity of ethyl acetate extract from Artemisia argyi on Verticillium dahliae. J. Appl. Microbiol. 2022, 132, 1343–1356. [Google Scholar] [CrossRef]
  18. Tao, A.; Feng, X.; Sheng, Y.; Song, Z. Optimization of the Artemisia Polysaccharide Fermentation Process by Aspergillus niger. Front. Nutr. 2022, 9, 842766. [Google Scholar] [CrossRef]
  19. Suvaithenamudhan, S.; Ananth, S.; Mariappan, V.; Dhayabaran, V.V.; Parthasarathy, S.; Ganesh, P.S.; Shankar, E.M. In Silico Evaluation of Bioactive Compounds of Artemisia pallens Targeting the Efflux Protein of Multidrug-Resistant Acinetobacter baumannii (LAC-4 Strain). Molecules 2022, 27, 5188. [Google Scholar] [CrossRef]
  20. Son, S.R.; Ju, I.G.; Kim, J.; Park, K.T.; Oh, M.S.; Jang, D.S. Chemical Constituents from the Aerial Parts of Artemisia iwayomogi and Their Anti-Neuroinflammatory Activities. Plants 2022, 11, 1954. [Google Scholar] [CrossRef]
  21. Kolesar, J.M.; Seeberger, P.H. Editorial: Anticancer Potential of Artemisia annua. Front. Oncol. 2022, 12, 853406. [Google Scholar] [CrossRef]
  22. Jung, E.J.; Paramanantham, A.; Kim, H.J.; Shin, S.C.; Kim, G.S.; Jung, J.M.; Hong, S.C.; Chung, K.H.; Kim, C.W.; Lee, W.S. Identification of Growth Factors, Cytokines and Mediators Regulated by Artemisia annua L. Polyphenols (pKAL) in HCT116 Colorectal Cancer Cells: TGF-beta1 and NGF-beta Attenuate pKAL-Induced Anticancer Effects via NF-kappaB p65 Upregulation. Int. J. Mol. Sci. 2022, 23, 1598. [Google Scholar] [CrossRef]
  23. Bordoni, V.; Sanna, L.; Lyu, W.; Avitabile, E.; Zoroddu, S.; Medici, S.; Kelvin, D.J.; Bagella, L. Silver Nanoparticles Derived by Artemisia arborescens Reveal Anticancer and Apoptosis-Inducing Effects. Int. J. Mol. Sci. 2021, 22, 8621. [Google Scholar] [CrossRef]
  24. Sahu, N.; Meena, S.; Shukla, V.; Chaturvedi, P.; Kumar, B.; Datta, D.; Arya, K.R. Extraction, fractionation and re-fractionation of Artemisia nilagirica for anticancer activity and HPLC-ESI-QTOF-MS/MS determination. J. Ethnopharmacol. 2018, 213, 72–80. [Google Scholar] [CrossRef]
  25. Ahameethunisa, A.R.; Hopper, W. Antibacterial activity of Artemisia nilagirica leaf extracts against clinical and phytopathogenic bacteria. BMC Complement. Altern. Med. 2010, 10, 6. [Google Scholar] [CrossRef] [Green Version]
  26. Naik, S.K.; Mohanty, S.; Padhi, A.; Pati, R.; Sonawane, A. Evaluation of antibacterial and cytotoxic activity of Artemisia nilagirica and Murraya koenigii leaf extracts against mycobacteria and macrophages. BMC Complement. Altern. Med. 2014, 14, 87. [Google Scholar] [CrossRef]
  27. Panda, S.; Rout, J.R.; Pati, P.; Ranjit, M.; Sahoo, S.L. Antimalarial activity of Artemisia nilagirica against Plasmodium falciparum. J. Parasit. Dis. 2018, 42, 22–27. [Google Scholar] [CrossRef]
  28. Gul, M.Z.; Chandrasekaran, S.; Manjulatha, K.; Bhat, M.Y.; Maurya, R.; Qureshi, I.A.; Ghazi, I.A. Bioassay-Guided Fractionation and In Vitro Antiproliferative Effects of Fractions of Artemisia nilagirica on THP-1 cell line. Nutr. Cancer 2016, 68, 1210–1224. [Google Scholar] [CrossRef]
  29. Raju, S.R.; Balakrishnan, S.; Kollimada, S.; Chandrashekara, K.N.; Jampani, A. Anti-tumor effects of Artemisia nilagirica extract on MDA-MB-231 breast cancer cells: Deciphering the biochemical and biomechanical properties via TGF-beta upregulation. Heliyon 2020, 6, e05088. [Google Scholar] [CrossRef]
  30. Parameswari, P.; Devika, R.; Vijayaraghavan, P. In vitro anti-inflammatory and antimicrobial potential of leaf extract from Artemisia nilagirica (Clarke) Pamp. Saudi J. Biol. Sci. 2019, 26, 460–463. [Google Scholar] [CrossRef]
  31. Suseela, V.; Gopalakrishnan, V.K.; Varghese, S. In vitro Antioxidant Studies of Fruits of Artemisia nilagirica (Clarke) Pamp. Indian J. Pharm. Sci. 2010, 72, 644–649. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Sati, S.C.; Sati, N.; Ahluwalia, V.; Walia, S.; Sati, O.P. Chemical composition and antifungal activity of Artemisia nilagirica essential oil growing in northern hilly areas of India. Nat. Prod. Res. 2013, 27, 45–48. [Google Scholar] [CrossRef] [PubMed]
  33. Sonker, N.; Pandey, A.K.; Singh, P. Efficiency of Artemisia nilagirica (Clarke) Pamp. essential oil as a mycotoxicant against postharvest mycobiota of table grapes. J. Sci. Food Agric. 2015, 95, 1932–1939. [Google Scholar] [CrossRef] [PubMed]
  34. Stappen, I.; Wanner, J.; Tabanca, N.; Wedge, D.E.; Ali, A.; Khan, I.A.; Kaul, V.K.; Lal, B.; Jaitak, V.; Gochev, V.; et al. Chemical composition and biological effects of Artemisia maritima and Artemisia nilagirica essential oils from wild plants of western Himalaya. Planta Med. 2014, 80, 1079–1087. [Google Scholar] [CrossRef] [Green Version]
  35. Ekiert, H.; Świątkowska, J.; Klin, P.; Rzepiela, A.; Szopa, A. Artemisia annua—Importance in Traditional Medicine and Current State of Knowledge on the Chemistry, Biological Activity and Possible Applications. Planta Med. 2021, 87, 584–599. [Google Scholar] [CrossRef]
  36. Matvieieva, N.; Drobot, K.; Duplij, V.; Ratushniak, Y.; Shakhovsky, A.; Kyrpa-Nesmiian, T.; Mickevičius, S.; Brindza, J. Flavonoid content and antioxidant activity of Artemisia vulgaris L. “hairy” roots. Prep. Biochem. Biotechnol. 2019, 49, 82–87. [Google Scholar] [CrossRef]
  37. Tavsan, Z.; Kayali, H.A. Flavonoids showed anticancer effects on the ovarian cancer cells: Involvement of reactive oxygen species, apoptosis, cell cycle and invasion. Biomed. Pharmacother. 2019, 116, 109004. [Google Scholar] [CrossRef]
  38. Al-Ishaq, R.K.; Abotaleb, M.; Kubatka, P.; Kajo, K.; Büsselberg, D. Flavonoids and Their Anti-Diabetic Effects: Cellular Mechanisms and Effects to Improve Blood Sugar Levels. Biomolecules 2019, 9, 430. [Google Scholar] [CrossRef] [Green Version]
  39. Tian, C.; Liu, X.; Chang, Y.; Wang, R.; Lv, T.; Cui, C.; Liu, M. Investigation of the anti-inflammatory and antioxidant activities of luteolin, kaempferol, apigenin and quercetin. S. Afr. J. Bot. 2021, 137, 257–264. [Google Scholar] [CrossRef]
  40. Crascì, L.; Cardile, V.; Longhitano, G.; Nanfitò, F.; Panico, A. Anti-degenerative effect of Apigenin, Luteolin and Quercetin on human keratinocyte and chondrocyte cultures: SAR evaluation. Drug Res. 2018, 68, 132–138. [Google Scholar] [CrossRef]
  41. Skowyra, M.; Gallego, M.G.; Segovia, F.; Almajano, M.P. Antioxidant Properties of Artemisia annua Extracts in Model Food Emulsions. Antioxidants 2014, 3, 116–128. [Google Scholar] [CrossRef] [Green Version]
  42. Perillo, B.; Di Donato, M.; Pezone, A.; Di Zazzo, E.; Giovannelli, P.; Galasso, G.; Castoria, G.; Migliaccio, A. ROS in cancer therapy: The bright side of the moon. Exp. Mol. Med. 2020, 52, 192–203. [Google Scholar] [CrossRef]
  43. Hayes, J.D.; Dinkova-Kostova, A.T.; Tew, K.D. Oxidative Stress in Cancer. Cancer Cell 2020, 38, 167–197. [Google Scholar] [CrossRef]
  44. Alqahtani, A.S.; Hidayathulla, S.; Rehman, M.T.; ElGamal, A.A.; Al-Massarani, S.; Razmovski-Naumovski, V.; Alqahtani, M.S.; El Dib, R.A.; AlAjmi, M.F. Alpha-Amylase and Alpha-Glucosidase Enzyme Inhibition and Antioxidant Potential of 3-Oxolupenal and Katononic Acid Isolated from Nuxia oppositifolia. Biomolecules 2020, 10, 61. [Google Scholar] [CrossRef] [Green Version]
  45. Jannapureddy, S.; Sharma, M.; Yepuri, G.; Schmidt, A.M.; Ramasamy, R. Aldose Reductase: An Emerging Target for Development of Interventions for Diabetic Cardiovascular Complications. Front. Endocrinol. 2021, 12, 636267. [Google Scholar] [CrossRef]
  46. Kazeem, M.I.; Adeyemi, A.A.; Adenowo, A.F.; Akinsanya, M.A. Carica papaya Linn. fruit extract inhibited the activities of aldose reductase and sorbitol dehydrogenase: Possible mechanism for amelioration of diabetic complications. Future J. Pharm. Sci. 2020, 6, 96. [Google Scholar] [CrossRef]
  47. Ali, A.N.M.; Saeed, N.; Omear, H.A. The Anticancer Properties of Artemisia aucheri Boiss Extract on HT29 Colon Cancer Cells. J. Gastrointest. Cancer 2021, 52, 113–119. [Google Scholar] [CrossRef]
  48. Mashati, P.; Esmaeili, S.; Dehghan-Nayeri, N.; Bashash, D.; Darvishi, M.; Gharehbaghian, A. Methanolic Extract from Aerial Parts of Artemisia annua L. Induces Cytotoxicity and Enhances Vincristine-Induced Anticancer Effect in Pre-B Acute Lymphoblastic Leukemia Cells. Int. J. Hematol. Oncol. Stem Cell Res. 2019, 13, 132–139. [Google Scholar] [CrossRef]
  49. Choi, E.J.; Kim, G.H. Antioxidant and anticancer activity of Artemisia princeps var. orientalis extract in HepG2 and Hep3B hepatocellular carcinoma cells. Chin. J. Cancer Res. Chung-Kuo Yen Cheng Yen Chiu 2013, 25, 536–543. [Google Scholar] [CrossRef]
  50. Choi, E.; Park, H.; Lee, J.; Kim, G. Anticancer, antiobesity, and anti-inflammatory activity of Artemisia species in vitro. J. Tradit. Chin. Med. Chung I Tsa Chih Ying Wen Pan 2013, 33, 92–97. [Google Scholar] [CrossRef]
  51. Ghanbar, F.; Mirzaie, A.; Ashrafi, F.; Noorbazargan, H.; Dalirsaber Jalali, M.; Salehi, S.; Sadat Shandiz, S.A. Antioxidant, antibacterial and anticancer properties of phyto-synthesised Artemisia quttensis Podlech extract mediated AgNPs. IET Nanobiotechnol. 2017, 11, 485–492. [Google Scholar] [CrossRef] [PubMed]
  52. Salehi, S.; Shandiz, S.A.; Ghanbar, F.; Darvish, M.R.; Ardestani, M.S.; Mirzaie, A.; Jafari, M. Phytosynthesis of silver nanoparticles using Artemisia marschalliana Sprengel aerial part extract and assessment of their antioxidant, anticancer, and antibacterial properties. Int. J. Nanomed. 2016, 11, 1835–1846. [Google Scholar] [CrossRef] [Green Version]
  53. Briguglio, G.; Costa, C.; Pollicino, M.; Giambò, F.; Catania, S.; Fenga, C. Polyphenols in cancer prevention: New insights (Review). Int. J. Funct. Nutr. 2020, 1, 9. [Google Scholar] [CrossRef]
  54. Kopustinskiene, D.M.; Jakstas, V.; Savickas, A.; Bernatoniene, J. Flavonoids as Anticancer Agents. Nutrients 2020, 12, 457. [Google Scholar] [CrossRef] [Green Version]
  55. Tong, W.; Chen, X.; Song, X.; Chen, Y.; Jia, R.; Zou, Y.; Li, L.; Yin, L.; He, C.; Liang, X.; et al. Resveratrol inhibits LPS-induced inflammation through suppressing the signaling cascades of TLR4-NF-κB/MAPKs/IRF3. Exp. Ther. Med. 2020, 19, 1824–1834. [Google Scholar] [CrossRef] [Green Version]
  56. Yücel, G.; Zhao, Z.; El-Battrawy, I.; Lan, H.; Lang, S.; Li, X.; Buljubasic, F.; Zimmermann, W.-H.; Cyganek, L.; Utikal, J.; et al. Lipopolysaccharides induced inflammatory responses and electrophysiological dysfunctions in human-induced pluripotent stem cell derived cardiomyocytes. Sci. Rep. 2017, 7, 2935. [Google Scholar] [CrossRef] [Green Version]
  57. Tang, J.; Diao, P.; Shu, X.; Li, L.; Xiong, L. Quercetin and Quercitrin Attenuates the Inflammatory Response and Oxidative Stress in LPS-Induced RAW264.7 Cells: In Vitro Assessment and a Theoretical Model. Biomed. Res. Int. 2019, 2019, 7039802. [Google Scholar] [CrossRef] [Green Version]
  58. Kim, Y.J.; Park, W. Anti-Inflammatory Effect of Quercetin on RAW 264.7 Mouse Macrophages Induced with Polyinosinic-Polycytidylic Acid. Molecules 2016, 21, 450. [Google Scholar] [CrossRef] [Green Version]
  59. Lee, A.J.; Cho, K.-J.; Kim, J.-H. MyD88–BLT2-dependent cascade contributes to LPS-induced interleukin-6 production in mouse macrophage. Exp. Mol. Med. 2015, 47, e156. [Google Scholar] [CrossRef] [Green Version]
  60. Sakai, J.; Cammarota, E.; Wright, J.A.; Cicuta, P.; Gottschalk, R.A.; Li, N.; Fraser, I.D.C.; Bryant, C.E. Lipopolysaccharide-induced NF-κB nuclear translocation is primarily dependent on MyD88, but TNFα expression requires TRIF and MyD88. Sci. Rep. 2017, 7, 1428. [Google Scholar] [CrossRef]
  61. Shukla, A.; Vats, S.; Shukla, R.K. Phytochemical Screening, Proximate Analysis and Antioxidant Activity of Dracaena reflexa Lam. Leaves. Indian J. Pharm. Sci. 2015, 77, 640–644. [Google Scholar] [CrossRef] [Green Version]
  62. Agidew, M.G. Phytochemical analysis of some selected traditional medicinal plants in Ethiopia. Bull. Natl. Res. Cent. 2022, 46, 87. [Google Scholar] [CrossRef]
  63. Owolabi, O.O.; James, D.B.; Sani, I.; Andongma, B.T.; Fasanya, O.O.; Kure, B. Phytochemical analysis, antioxidant and anti-inflammatory potential of FERETIA APODANTHERA root bark extracts. BMC Complement. Altern. Med. 2018, 18, 12. [Google Scholar] [CrossRef] [Green Version]
  64. House, N.C.; Puthenparampil, D.; Malayil, D.; Narayanankutty, A. Variation in the polyphenol composition, antioxidant, and anticancer activity among different Amaranthus species. S. Afr. J. Bot. 2020, 135, 408–412. [Google Scholar] [CrossRef]
  65. Ortiz-Cruz, R.A.; Ramírez-Wong, B.; Ledesma-Osuna, A.I.; Torres-Chávez, P.I.; Sánchez-Machado, D.I.; Montaño-Leyva, B.; López-Cervantes, J.; Gutiérrez-Dorado, R. Effect of Extrusion Processing Conditions on the Phenolic Compound Content and Antioxidant Capacity of Sorghum (Sorghum bicolor (L.) Moench) Bran. Plant Foods Hum. Nutr. 2020, 75, 252–257. [Google Scholar] [CrossRef]
  66. Wang, B.; Liu, L.; Huang, Q.; Luo, Y. Quantitative Assessment of Phenolic Acids, Flavonoids and Antioxidant Activities of Sixteen Jujube Cultivars from China. Plant Foods Hum. Nutr. 2020, 75, 154–160. [Google Scholar] [CrossRef]
  67. Liu, D.; Guo, Y.; Wu, P.; Wang, Y.; Kwaku Golly, M.; Ma, H. The necessity of walnut proteolysis based on evaluation after in vitro simulated digestion: ACE inhibition and DPPH radical-scavenging activities. Food Chem. 2020, 311, 125960. [Google Scholar] [CrossRef]
  68. Bi, X.; Zhang, J.; Chen, C.; Zhang, D.; Li, P.; Ma, F. Anthocyanin contributes more to hydrogen peroxide scavenging than other phenolics in apple peel. Food Chem. 2014, 152, 205–209. [Google Scholar] [CrossRef]
  69. Dutta, S.; Ray, S. Comparative assessment of total phenolic content and in vitro antioxidant activities of bark and leaf methanolic extracts of Manilkara hexandra (Roxb.) Dubard. J. King Saud Univ. Sci. 2020, 32, 643–647. [Google Scholar] [CrossRef]
  70. Tonisi, S.; Okaiyeto, K.; Mabinya, L.V.; Okoh, A.I. Evaluation of bioactive compounds, free radical scavenging and anticancer activities of bulb extracts of Boophone disticha from Eastern Cape Province, South Africa. Saudi J. Biol. Sci. 2020, 27, 3559–3569. [Google Scholar] [CrossRef]
  71. Mechchate, H.; Es-safi, I.; Louba, A.; Alqahtani, A.S.; Nasr, F.A.; Noman, O.M.; Farooq, M.; Alharbi, M.S.; Alqahtani, A.; Bari, A.; et al. In Vitro Alpha-Amylase and Alpha-Glucosidase Inhibitory Activity and In Vivo Antidiabetic Activity of Withania frutescens L. Foliar Extract. Molecules 2021, 26, 293. [Google Scholar] [CrossRef]
  72. 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]
  73. Kim, T.H.; Kim, J.K.; Kang, Y.-H.; Lee, J.-Y.; Kang, I.J.; Lim, S.S. Aldose Reductase Inhibitory Activity of Compounds from Zea mays L. Biomed. Res. Int. 2013, 2013, 727143. [Google Scholar] [CrossRef] [Green Version]
  74. Al-Yousef, H.M.; Fantoukh, O.I.; El-Sayed, M.A.; Amina, M.; Adel, R.; Hassan, W.H.B.; Abdelaziz, S. Metabolic profiling and biological activities of the aerial parts of Micromeria imbricata Forssk. growing in Saudi Arabia. Saudi J. Biol. Sci. 2021, 28, 5609–5616. [Google Scholar] [CrossRef]
Figure 1. The LC-MS total ion chromatogram of the A. nilagirica extract.
Figure 1. The LC-MS total ion chromatogram of the A. nilagirica extract.
Molecules 27 07119 g001
Figure 2. The anticancer potentials of the leaf extract of A. nilagirica (a) and cyclophosphamide (b).
Figure 2. The anticancer potentials of the leaf extract of A. nilagirica (a) and cyclophosphamide (b).
Molecules 27 07119 g002
Table 1. Physicochemical parameters of A. nilagirica leaf powder.
Table 1. Physicochemical parameters of A. nilagirica leaf powder.
Physicochemical ParametersResult
Moisture content (%)87.4 ± 2.12
Carbohydrate (%)55.80 ± 4.1
Protein (%)3.90 ± 0.16
Crude fat (%)2.12 ± 0.18
Ash content (%)0.74 ± 0.04
Table 2. Phytochemical constituents in the ethanol extract of A. nilagirica.
Table 2. Phytochemical constituents in the ethanol extract of A. nilagirica.
TestReaction
Alkaloids
Marqui’s test++
Wagner’s test++
Mayer’s test+++
Hager’s test+
Froehde’s test++
Dragendorff test++
Glycosides
Legal’s test+
Keller-Kiliani test+
Flavonoids
Alkaline reagent test++
Lead acetate test++
Shinoda’s test+++
Tannins
Ferric Chloride test++
Gelatin test++
Phytosterols
Salkowski’s test++
Liebermann-Burchard test+++
Saponins
Froth test+
Foam test+
Carbohydrates
Fehling test++
Molish test++
Benedict’s test++
Phenols
Folin-Ciocalteu test+++
Resin
Acetone-water test+
Fixed oils and fats
Stain test-
Triterpenes
Liebermann-Burchardt’s test+++
Note: +++ high level, ++ moderate level, and + low-level presence of the compound.
Table 3. LCMS profiling of A. nilagirica with the retention time (RT), molecular mass, and chemical formula.
Table 3. LCMS profiling of A. nilagirica with the retention time (RT), molecular mass, and chemical formula.
Sl. No.RT (mins)Compound NameFormulaMass
12.53Ferulic acidC10H10O4194.00
26.38EugenolC10H12O2164.08
38.18Β-caryophylleneC21H20O11448.40
49.06LuteolinC15H10O6286.00
510.71caffeic acidC9H8O4180.16
611.29QuercetinC15H10O7302.00
712.14MyricetinC15H10O8318.00
812.89ApigeninC15H10O5270.05
914.03Luteolin 5-0-beta-d-glucopyranosideC21H20O11448.13
1015.52KaempferolC15H10O6286.23
1121.56Carnosic acidC20H28O4332.19
1225.09ArtemisininC20H20O8388.11
1329.362alpha, 3 beta-Dihydroxyolean-12en-28-oic acidC30H48O4472.35
1430.45Menthyl acetateC12H22O2198.16
1533.61Oleanolic acidC30H48O3456.36
1644.12BasilimosideC36H60O6588.47
Table 4. The total polyphenol and flavonoid contents of A. nilagirica ethanol extract.
Table 4. The total polyphenol and flavonoid contents of A. nilagirica ethanol extract.
Assaymg Equivalent/g
Total phenolic content 89.51 ± 2.5
Total flavonoid content14.35 ± 0.9
Table 5. The quantification of selected compounds in the extract via HPLC.
Table 5. The quantification of selected compounds in the extract via HPLC.
RT (mins)Compound NameQuantity (µg/g Extract)
2.50Ferulic acid18.51 ± 1.82
9.05Luteolin146.87 ± 5.29
10.70caffeic acid88.62 ± 1.30
11.30Quercetin240.39 ± 4.87
12.87Apigenin103.41 ± 3.35
Table 6. In vitro antioxidant activities of A. nilagirica extract (AN) expressed as IC50 values (µg/mL).
Table 6. In vitro antioxidant activities of A. nilagirica extract (AN) expressed as IC50 values (µg/mL).
Antioxidant ActivityIC50 Value (µg/mL)
ANAscorbic Acid
DPPH scavenging 23.12 ± 1.289.64 ± 0.89
ABTS scavenging27.44 ± 1.8835.19 ± 1.47
H2O2 scavenging12.92 ± 1.0519.08 ± 1.65
FRAP value (EC50)5.42 ± 0.193.22 ± 0.15
Nitric oxide scavenging367.09 ± 12.0568.10 ± 2.11
Table 7. In vitro enzyme-inhibitory properties of A. nilagirica expressed as IC50 values (µg/mL).
Table 7. In vitro enzyme-inhibitory properties of A. nilagirica expressed as IC50 values (µg/mL).
EnzymeIC50 Value (µg/mL)
α-Amylase 38.42 ± 2.71
α-Glucosidase55.31 ± 2.16
Aldose reductase17.42 ± 0.87
Sorbitol dehydrogenase29.57 ± 1.46
Table 8. Effect of the Artemisia nilagirica leaf ethanol extract (AN) against lipopolysaccharide-induced macrophage (Raw 264.7) activation, cytokine release (in pg/mg protein), and nitric oxide production (µM/mg protein).
Table 8. Effect of the Artemisia nilagirica leaf ethanol extract (AN) against lipopolysaccharide-induced macrophage (Raw 264.7) activation, cytokine release (in pg/mg protein), and nitric oxide production (µM/mg protein).
NatureTumor Necrosis Factor αInterleukin 6Interleukin 1βNO
Untreated97.6 ± 2.876.4 ± 3.167.8 ± 2.87.4 ± 0.57
Negative Control (LPS alone)420.8 ± 10.6795.2 ± 11.7628.9 ± 14.252.1 ± 2.0
Quercetin (4.5 µg/mL)279.1 ± 11.3 **414.2 ± 10.7 ***334.8 ± 11.7 **30.7 ± 1.2 *
Artemisia nilagirica extract2.5 µg/mL314.1 ± 14.5 *698.0 ± 17.3 **477.6 ± 11.8 **40.7 ± 1.6 *
5.0 µg/mL265.7 ± 10.7 **524.3 ± 15.6 **389.5 ± 14.6 **32.2 ± 2.4 *
7.5 µg/mL190.9 ± 14.8 ***388.2 ± 15.8 ***298.7 ± 15.2 ***25.7 ± 2.1 **
Artemisia nilagirica leaf ethanol extract (AN), lipopolysaccharide (LPS), nitric oxide (NO). The significance is indicated as * (p < 0.05), ** (p < 0.01), *** (p < 0.001).
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Albaqami, J.J.; Benny, T.P.; Hamdi, H.; Altemimi, A.B.; Kuttithodi, A.M.; Job, J.T.; Sasidharan, A.; Narayanankutty, A. Phytochemical Composition and In Vitro Antioxidant, Anti-Inflammatory, Anticancer, and Enzyme-Inhibitory Activities of Artemisia nilagirica (C.B. Clarke) Pamp. Molecules 2022, 27, 7119. https://doi.org/10.3390/molecules27207119

AMA Style

Albaqami JJ, Benny TP, Hamdi H, Altemimi AB, Kuttithodi AM, Job JT, Sasidharan A, Narayanankutty A. Phytochemical Composition and In Vitro Antioxidant, Anti-Inflammatory, Anticancer, and Enzyme-Inhibitory Activities of Artemisia nilagirica (C.B. Clarke) Pamp. Molecules. 2022; 27(20):7119. https://doi.org/10.3390/molecules27207119

Chicago/Turabian Style

Albaqami, Jawaher J., Tancia P. Benny, Hamida Hamdi, Ammar B. Altemimi, Aswathi Moothakoottil Kuttithodi, Joice Tom Job, Anju Sasidharan, and Arunaksharan Narayanankutty. 2022. "Phytochemical Composition and In Vitro Antioxidant, Anti-Inflammatory, Anticancer, and Enzyme-Inhibitory Activities of Artemisia nilagirica (C.B. Clarke) Pamp" Molecules 27, no. 20: 7119. https://doi.org/10.3390/molecules27207119

APA Style

Albaqami, J. J., Benny, T. P., Hamdi, H., Altemimi, A. B., Kuttithodi, A. M., Job, J. T., Sasidharan, A., & Narayanankutty, A. (2022). Phytochemical Composition and In Vitro Antioxidant, Anti-Inflammatory, Anticancer, and Enzyme-Inhibitory Activities of Artemisia nilagirica (C.B. Clarke) Pamp. Molecules, 27(20), 7119. https://doi.org/10.3390/molecules27207119

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