Antioxidant properties and cytotoxic effects of Alternanthera sissoo and Alternanthera bettzickiana extracts against cancer cells

Authors

  • Worachot SAENGHA Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Thipphiya KARIRAT Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Benjaporn BURANRAT Mahasarakham University, Faculty of Medicine, Mahasarakham 44000 (TH)
  • Teeraporn KATISART Mahasarakham University, Faculty of Science, Department of Biology, Mahasarakham 44150 (TH)
  • Nyuk Ling MA University Malaysia Terengganu, Faculty of Science and Marine Environment, 21030, Kuala Nerus, Terengganu (MY)
  • Vijitra LUANG-IN Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)

DOI:

https://doi.org/10.15835/nbha50312776

Keywords:

A549, Brazilian spinach, flavonoid, HepG2 , joyweed, MCF-7 , phenolic acid

Abstract

This work aimed to evaluate the antioxidant capacities and cytotoxic attributes of Alternanthera sissoo (AS) and Alternanthera bettzickiana Green (AB) which are commonly grown in Thailand, yet not extensively-studied. Dried leaves were extracted by maceration using ethanol for 48 h and ethanolic extract solution was used. Cytotoxic, anti-proliferative, anti-migratory capacities and apoptosis-related gene expressions of AS and AB extracts on MCF-7, HepG2, and HeLa cell lines were investigated using 3-(4,5-dimethylthiazolyl-2)-2, 5-diphenyltetra zolium bromide (MTT) assay, anti-colony formation and wound healing test, respectively. The antioxidant activities by DPPH assay and FRAP assay of AS (130.62±1.61 µg TE/g extract and 24.76 ± 0.54 mg Fe(II)/g extract, respectively) were significantly higher than those of AB (104.34±3.68 µg TE/g extract and 23.13± 0.90 mg Fe(II)/g extract, respectively). Likewise, total phenolic content and the total flavonoid content of AS (7.43±0.39 mg GAE/g and 184.22±3.20 mg RE/g extract, respectively) were significantly higher than AB (6.10±0.29 mg GAE/g extract and 168.07±7.90 mg RE/g extract, respectively). HPLC analysis showed the predominance of myricetin, rutin and ferulic acid. For MCF-7, HepG2 and HeLa, the lowest IC50 values of 48.53 µg/mL, 69.94 µg/mL and 43.98 µg/mL, respectively were found in AS extract at 72 h exposure using MTT assay. Apoptotic bodies, gene expression and protein expressions related to apoptosis were more pronounced in AS treatment. Both AS and AB can be served as local foods with chemopreventive effects against breast, liver and cervical cancers. This work provided a foundation for future pharmacological research on Alternanthera plant extracts.

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References

Abotsi WKM, Ainooson GK, Woode E (2011). Anti-inflammatory and antioxidant effects of an ethanolic extract of the aerial parts of Hilleria latifolia (Lam.) H. Walt. (Phytolaccaceae). African Journal of Traditional, Complementary and Alternative Medicines 9:138-152. https://doi.org/10.4314/ajtcam.v9i1.19

Akhtar MF, Sharif A, Saleem M, Saleem A, Akhtar B, Raza M, ... Peerzada, S. (2017). Genotoxic and cytotoxic potential of Alternanthera bettzickiana, an important ethno-medicinal plant. Molecular and Cellular Biology (Noisy-le-grand) 63:109-114. https://doi.org/10.14715/cmb/2017.63.8.23

Balasuriya BMGK, Dharmaratne HRW. Cytotoxicity and antioxidant activity studies of green leafy vegetables consumed in Sri Lanka. Journal of the National Science Foundation of Sri Lanka 35:255-258. https://doi.org/10.4038/jnsfsr.v35i4.1315

Buitrago D, Buitrago-Villanueva I, Barbosa-Cornelio R, Coy-Barrera E (2019). Comparative examination of antioxidant capacity and fingerprinting of unfractionated extracts from different plant parts of quinoa (Chenopodium quinoa) grown under greenhouse conditions. Antioxidants 8:238. https://doi.org/10.3390/antiox8080238

Chakraborty C, Sharma AR, Sharma G, Sarkar BK, Lee SS (2018). The novel strategies for next-generation cancer treatment: miRNA combined with chemotherapeutic agents for the treatment of cancer. Oncotarget 9:10164-10174. https://doi.org/10.18632/oncotarget.24309

Chumroenphat T, Somboonwatthanakul I, Saensouk S, Siriamornpun S (2021). Changes in curcuminoids and chemical components of turmeric (Curcuma longa L.) under freeze-drying and low-temperature drying methods. Food Chemistry 339:128121. https://doi.org/10.1016/j.foodchem.2020.128121

Ci Y, Zhang Y, Liu Y, Lu S, Cao J, Li, H., … Han M (2018). Myricetin suppresses breast cancer metastasis through down-regulating the activity of matrix metalloproteinase (MMP)-2/9. Phytotherapy Research 32:1373-1381. https://doi.org/10.1002/ptr.6071

de Alencar Filho JMT, Sampaio PA, de Carvalho LS, Guimarães AL, Araujo e Amariz I, Pereira ECV, … da Cruz Araújo EC (2020). Flavonoid enriched extract of Alternanthera brasiliana with photoprotective effect: Formulation development and evaluation of quality. Industrial Crops and Products 149:112371. https://doi.org/10.1016/j.indcrop.2020.112371

Frusciante L, Barone A, Maria D, Manuela M (2015). Antioxidant bioactive compounds in tomato fruits at different ripening stages and their effects on normal and cancer cells. Journal of Functional Foods. 18:83-94. https://doi.org/10.1016/j.jff.2015.06.060

Gothai S, Muniandy K, Mohd Esa N, Subbiah SK, Arulselvan P (2018). Anticancer potential of Alternanthera sessilis extract on HT-29 human colon cancer cells. Asian Pacific Journal of Tropical Biomedicine 8:394-402. https://doi.org/10.4103/2221-1691.239427

Greenwell M, Rahman PK (2015). Medicinal plants: Their use in anticancer treatment. International Journal of Pharmaceutical Sciences and Research 6:4103-4112. https://doi.org/10.13040/IJPSR.0975-8232.6(10).4103-12

Gregoriou G, Neophytou CM, Vasincu A, Gregoriou Y, Hadjipakkou H, Pinakoulaki E, … Constantinou AI (2021). Anti-cancer activity and phenolic content of extracts derived from Cypriot carob (Ceratonia siliqua L.) pods using different solvents. Molecules 26:5017. https://doi.org/10.3390/molecules26165017

Hossain AI, Faisal M, Rahman S, Jahan R, Rahmatullah M (2014). A preliminary evaluation of antihyperglycemic and analgesic activity of Alternanthera sessilis aerial parts. BMC Complementary and Alternative Medicine 14:169. https://doi.org/10.1186/1472-6882-14-169

Khazendar M, Chalak J, El-Huneidi W, Vinod A, Abdel-Rahman WM, Abu-Gharbieh E (2019). Antiproliferative and proapoptotic activities of ferulic acid in breast and liver cancer cell lines. Tropical Journal of Pharmaceutical Research 18:2571-2576.

Kubola J, Siriamornpun S (2011). Phytochemicals and antioxidant activity of different fruit fractions (peel, pulp, aril and seed) of Thai gac (Momordica cochinchinensis Spreng). Food Chemistry 127:1138-1145. https://doi.org/10.1016/j.foodchem.2011.01.115.

Kumar S, Singh P, Mishra G, Srivasta S, Jha KK, Khosa RL (2011). Phytopharmacological review of Alternanthera brasiliana (Amaranthaceae). Asian Journal of Plant Science and Research 1:41-7.

Luang-In V, Saengha W, Karirat T, Buranrat B, Matra K, Deeseenthum S, … Katisart T (2021). Effect of cold plasma and elicitors on bioactive contents, antioxidant activity and cytotoxicity of Thai rat-tailed radish microgreens. Journal of the Science of Food and Agriculture 101:1685-1698. https://doi.org/10.1002/jsfa.10985

Manan M, Saleem U, Akash MSH, Qasim M, Hayat M, Raza Z, ... Ahman B (2020). Antiarthritic potential of comprehensively standardized extract of Alternanthera bettzickiana: In vitro and in vivo studies. ACS Omega 2020; 5: 19478-19496. https://doi.org/10.1021/acsomega.0c01670

Mohd Hazli UH, Abdul-Aziz A, Mat-Junit S, Chee CF, Kong KW (2019). Solid-liquid extraction of bioactive compounds with antioxidant potential from Alternanthera sesillis (red) and identification of the polyphenols using UHPLC-QqQ-MS/MS. Food Research International 115:241-250. https://doi.org/10.1016/j.foodres.2018.08.094

Muniandy K, Gothai S, Tan WS, Kumar SS, Mohd Esa N, Chandramohan G, … Arulselvan P (2018). In vitro wound healing potential of stem extract of Alternanthera sessilis. Evidence-Based Complementary and Alternative Medicine 2018:3142073. https://doi.org/10.1155/2018/3142073

Okaiyeto K, Oguntibeju OO (2021). African herbal medicines: Adverse effects and cytotoxic potentials with different therapeutic applications. International Journal of Environmental Research and Public Health 18:5988. https://doi.org/10.3390/ijerph18115988

Othman A, Ismail A, Hassan FA, Yusof BNM, Khatib A (2016). Comparative evaluation of nutritional compositions, antioxidant capacities, and phenolic compounds of red and green sessile joyweed (Alternanthera sessilis). Journal of Functional Foods 21:263-271. https://doi.org/10.1016/j.jff.2015.12.014

Pamila A, Karpagam S, Jayaraman P (2018). Morphological and anatomical features of Alternanthera bettzickiana (Regel) G. Nicholson. International Journal of Botany and Research 8:5-18.

Petrus A, Kalpana K, Devi AB (2014). Foliar biophenolic antioxidant metabolites of Alternanthera bettzickiana. Oriental Journal of Chemistry 30:1197-1203. http://dx.doi.org/10.13005/ojc/300334

Qian L, Su W, Wang Y, Dang M, Zhang W, Wang C (2019). Synthesis and characterization of gold nanoparticles from aqueous leaf extract of Alternanthera sessilis and its anticancer activity on cervical cancer cells (HeLa). Artificial Cells, Nanomedicine, and Biotechnology 47:1173-1180. https://doi.org/10.1080/21691401.2018.1549064

Raina H, Soni G, Jauhari N, Sharma N, Bharadvaja N (2014). Phytochemical importance of medicinal plants as potential sources of anticancer agents. Turkish Journal of Botany 38:1027-1035. https://doi.org/10.3906/bot-1405-93

Sajedi N, Homayoun M, Mohammadi F, Soleimani M (2020). Myricetin Exerts its Apoptotic Effects on MCF-7 Breast Cancer Cells through Evoking the BRCA1-GADD45 Pathway. Asian Pacific Journal of Cancer Prevention 21:3461-3468. https://doi.org/10.31557/APJCP.2020.21.12.3461

Satari A, Ghasemi S, Habtemariam S, Asgharian S, Lorigooini Z (2021). Rutin: A flavonoid as an effective sensitizer for anticancer therapy; Insights into multifaceted mechanisms and applicability for combination therapy. Evidence-Based Complementary and Alternative Medicine 2021: 9913179. https://doi.org/10.1155/2021/9913179

Suphanthip P, Waranya C, Orawan M, Pradit P, Kanokwan J (2013). Alternanthera sessilis and Alternanthera bettzickiana improved superoxide dismutase and catalase activities in the livers of ovariectomized mice. Journal of Applied Biopharmaceutics and Pharmacokinetics 1: 64-71. https://doi.org/10.14205/2309-4435.2013.01.02.2

Tiveron AP, Melo PS, Bergamaschi KB, Vieira TM, Regitano-d’Arce MA, Alencar SM (2012). Antioxidant activity of Brazilian vegetables and its relation with phenolic composition. International Journal of Molecular Sciences 13: 8943-8957. https://doi.org/10.3390/ijms13078943

Tukun AB, Shaheen N, Banu CP, Mohiduzzaman M, Islam S, Begum M (2014). Antioxidant capacity and total phenolic contents in hydrophilic extracts of selected Bangladeshi medicinal plants. Asian Pac J Trop Med 7S1:S568-S573. https://doi.org/10.1016/S1995-7645(14)60291-1

Tyagi G, Kapoor N, Chandra G, Gambhir L (2021). Cure lies in nature: medicinal plants and endophytic fungi in curbing cancer. 3 Biotech 11:263. https://doi.org/10.1007/s13205-021-02803-x

Vidhya T, Suji T, Dhatchayani R, Priya C, Bhaskara Rao K (2015). Evaluation of in vitro antioxidant, antimicrobial activities and GC-MS analysis of Alternanthera bettizicikiana Linn. leaf extracts. International Journal of Pharmacognosy and Phytochemical Research 2015: 1072.

Webb AH, Gao BT, Goldsmith ZK, Irvine AS, Saleh N, Lee RP, … Morales-Tirado, VM (2017). Inhibition of MMP-2 and MMP-9 decreases cellular migration, and angiogenesis in in vitro models of retinoblastoma. BMC Cancer 17:434. https://doi.org/10.1186/s12885-017-3418-y

Published

2022-09-06

How to Cite

SAENGHA, W., KARIRAT, T., BURANRAT, B., KATISART, T., MA, N. L., & LUANG-IN, V. (2022). Antioxidant properties and cytotoxic effects of Alternanthera sissoo and Alternanthera bettzickiana extracts against cancer cells. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50(3), 12776. https://doi.org/10.15835/nbha50312776

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Research Articles
CITATION
DOI: 10.15835/nbha50312776

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