Anticancer effects of Rhinacanthus nasutus and Acanthus ebracteatus extracts against human cervical 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)
  • Panida LOUTCHANWOOT Mahasarakham University, Faculty of Science, Department of Biology, Mahasarakham 44150 (TH)
  • Abdulhadi Ali ALBASER Sebha University, Department of Microbiology, Sebha (LY)
  • 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/nbha51113035

Keywords:

Acanthus ebracteatus, apoptosis, cytotoxic activity, HeLa cells, Rhinacanthus nasutus

Abstract

Cervical cancer is second only to breast cancer in terms of incidence; however, it is the most lethal form of cancer among Thai women due to the asymptomatic nature of its early stages. This work aimed to examine cytotoxic and antiproliferative capacities of Rhinacanthus nasutus (RN) and Acanthus ebracteatus (AE) extracts against human cervical cancer cells (HeLa). Plant leaves were used for ethyl acetate extraction. The antioxidant assays, HPLC analysis, a cytotoxic MTT assay, a clonogenic assay and real-time PCR were conducted. Both RN and AE displayed similar DPPH scavenging activity (3.97 and 4.05 mg TE/g DW) and ferric reducing antioxidant power (4.79 and 4.35 mg Fe2+/g DW). However, AE was richer in total phenolic content than RN (13.30 and 10.84 mg GAE/g DW, respectively). Rutin, catechin, chlorogenic acid, and cinnamic acid were found in AE, whilst only cinnamic acid with much higher content was found in RN. Higher cytotoxicity of 91.73% against HeLa cells was found in RN (IC50 value of 62.06 µg/mL). RN showed higher antiproliferative effect (IC50 of 25.24 µg/mL) than AE (34.35 µg/mL). Genes (Bcl-2, Bax, MMP-2, MMP-9, caspase-3, p21, and cyclin D1) and proteins (cytochrome c, caspase-3 and p21) linked to apoptosis and migration were substantially more affected by RN. To conclude, both RN and AE hold promise as anticancer herbal plants against human cervical cancer; however, RN was more cytotoxic and antiproliferative in HeLa cells. RN offers a better alternative herbal medicine or complementary remedy to the standard drug for human cervical cancer treatment.

References

Alper M, Gunes M (2020). Evaluation of cytotoxic, apoptotic effects and phenolic compounds of sea cucumber Holothuria tubulosa (Gmelin, 1791) extracts. Turkish Journal of Veterinary and Animal Sciences 44(3):21. https://doi.org/10.3906/vet-1909-80

Banjerdpongchai R, Wudtiwai B, Sringarm K (2014). Cytotoxic and apoptotic-inducing effects of purple rice extracts and chemotherapeutic drugs on human cancer cell lines. Asian Pacific Journal of Cancer Prevention 14:6541-6548. https://doi.org/10.7314/APJCP.2013.14.11.6541

Bouvard V, Wentzensen N, Mackie A, Berkhof J, Brotherton J, Giorgi-Rossi P, … Lauby-Secretan B (2021). The IARC perspective on cervical cancer screening. The New England Journal of Medicine 385(20):1908-1918. https://doi.org/10.1056/NEJMsr2030640

Brimson JM, Brimson SJ, Brimson CA, Rakkhitawatthana V, Tencomnao T (2012). Rhinacanthus nasutus extracts prevent glutamate and amyloid-β neurotoxicity in HT-22 mouse hippocampal cells: possible active compounds include lupeol, stigmasterol and β-sitosterol. International Journal of Molecular Sciences 13(4):5074-5097. https://doi.org/10.3390/ijms13045074

Chinembiri TN, du Plessis LH, Gerber M, Hamman JH, du Plessis J (2014). Review of natural compounds for potential skin cancer treatment. Molecules 19:11679-11721. https://doi.org/10.3390/molecules190811679

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

Gotoh A, Sakaeda T, Kimura T, Shirakawa T, Wada Y, Wada A, … Okumura K. (2004). Antiproliferative activity of Rhinacanthus nasutus (L.) Kurz extracts and the active moiety, Rhinacanthin C. Biological and Pharmaceutical Bulletin 27(7):1070-1074. https://doi.org/10.1248/bpb.27.1070

Hara-Terawaki A, Takagaki A, Kobayashi H, Nanjo F (2017). Inhibitory activity of catechin metabolites produced by intestinal microbiota on proliferation of HeLa cells. Biological and Pharmaceutical Bulletin 40(8):1331-1335. https://doi.org/10.1248/bpb.b17-00127

Khamwut A, Jevapatarakul D, Reamtong O, T-Thienprasert NP (2019). In vitro evaluation of anti-epidermoid cancer activity of Acanthus ebracteatus protein hydrolysate and their effects on apoptosis and cellular proteins. Oncology Letters 18(3):3128-3136. https://doi.org/10.3892/ ol.2019.10647

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

Mahasiripanth T, Hokputsa S, Niruthisard S, Bhattarakosol P, Patumraj S (2012). Effects of Acanthus ebracteatus Vahl on tumor angiogenesis and on tumor growth in nude mice implanted with cervical cancer. Cancer Management and Research 4:269-279. https://doi.org/10.2147/CMAR.S33596

Nourazarian SM, Nourazarian A, Majidinia M, Roshaniasl E. (2015). Effect of root extracts of medicinal herb glycyrrhiza glabra on HSP90 gene expression and apoptosis in the HT-29 colon cancer cell line. Asian Pacific Journal of Cancer Prevention 16:8563-8566. https://doi.org/10.7314/APJCP.2015.16.18.8563

Olatunji OJ, Olatunde OO, Jayeoye TJ, Singh S, Nalinbenjapun S, Sripetthong S, … Ovatlarnporn C (2022). New insights on Acanthus ebracteatus Vahl: UPLC-ESI-QTOF-MS profile, antioxidant, antimicrobial and anticancer activities. Molecules (Basel, Switzerland) 27(6):1981. https://doi.org/10.3390/molecules27061981

Pandey P, Khan F, Farhan M, Jafri A (2021). Elucidation of rutin's role in inducing caspase-dependent apoptosis via HPV-E6 and E7 down-regulation in cervical cancer HeLa cells. Bioscience Reports 41(6):BSR20210670. https://doi.org/10.1042/BSR20210670

Phuseerit O, Wrigley C, Siriamornpun S (2021). Bioactives and antioxidant activities of marigold flower juices and the effect of different storage times. Science Technology and Engineering Journal 7(2):58-73.

Prasansuklab A, Tencomnao T (2018). Acanthus ebracteatus leaf extract provides neuronal cell protection against oxidative stress injury induced by glutamate. BMC Complementary and Alternative Medicine 18(1):278. https://doi.org/10.1186/s12906-018-2340-4

Ryu JY, Kang HR, Cho SK (2019). Changes over the fermentation period in phenolic compounds and antioxidant and anticancer activities of blueberries fermented by Lactobacillus plantarum. Journal of Food Science 84:2347-2356. https://doi.org/10.1111/1750-3841.14731

Sali VK, Mansingh DP, Vasanthi HR (2016). Relative apoptotic potential and specific G1 arrest of stigmasterol and cinnamic acid isolated from the brown algae Padina gymnospora in HeLa and A549 cells. Medicinal Chemistry Communication 7:1429-1435.

Siripong P, Hahnvajanawong C, Yahuafai J, Piyaviriyakul S, Kanokmedhakul K, Kongkathip N, … Oku N (2009). Induction of apoptosis by rhinacanthone isolated from Rhinacanthus nasutus roots in human cervical carcinoma cells. Biological and Pharmaceutical Bulletin 32(7):1251-1260. https://doi.org/10.1248/bpb.32.1251

Siripong P, Yahuafai J, Shimizu K, Ichikawa K, Yonezawa S, Asai T, … Oku N (2006). Induction of apoptosis in tumor cells by three naphthoquinone esters isolated from Thai medicinal plant: Rhinacanthus nasutus KURZ. Biological and Pharmaceutical Bulletin 29(10):2070-2076. https://doi.org/10.1248/bpb.29.2070

Siriwatanametanon N, Fiebich BL, Efferth T, Prieto JM, Heinrich M (2010). Traditionally used Thai medicinal plants: In vitro anti-inflammatory, anticancer and antioxidant activities. Journal of Ethnopharmacology 130(2):196-207. https://doi.org/10.1016/j.jep.2010.04.036

Song P, Sun C, Li J, Long T, Yan Y, Qin H, … Olatunji OJ (2021). Tiliacora triandra extract and its major constituent attenuates diabetic kidney and testicular impairment by modulating redox imbalance and pro-inflammatory responses in rats. Journal of the Science of Food and Agriculture 101:1598-1608. https://doi.org/10.1002/jsfa.10779

Suksawat T, Panichayupakaranant P (2022). Variation of rhinacanthin content in Rhinacanthus nasutus and its health products. Journal of Pharmaceutical and Biomedical Analysis 224:115177. https://doi.org/10.1016/j.jpba.2022.115177

Thephinlap C, Pangjit K, Suttajit M, Srichairatanakool S (2013). Anti-oxidant properties and anti-hemolytic activity of Psidium guajava, Pandanous odorus and Rhinacanthus nasutus. Journal of Medicinal Plants Research 7:2001-9. https://doi.org/10.5897/JMPR12.800

Wang H, Zhu Y, Hao C, Fan J, Liu Y, Wang Y (2019). Establishment of a drug-resistant human cervical cancer cell line and research on its drug-resistance. Journal of Cancer Research and Therapeutics 15:1221-1225. https://doi.org/10.4103/0973-1482.204900

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Published

2023-02-14

How to Cite

SAENGHA, W., KARIRAT, T., BURANRAT, B., KATISART, T., LOUTCHANWOOT, P., ALBASER, A. A., & LUANG-IN, V. (2023). Anticancer effects of Rhinacanthus nasutus and Acanthus ebracteatus extracts against human cervical cancer cells. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(1), 13035. https://doi.org/10.15835/nbha51113035

Issue

Vol. 51 No. 1 (2023)

Section

Research Articles
CITATION
DOI: 10.15835/nbha51113035

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Copyright (c) 2023 Worachot SAENGHA, Thipphiya KARIRAT, Benjaporn BURANRAT, Teeraporn KATISART, Panida LOUTCHANWOOT, Abdulhadi Ali ALBASER, Vijitra LUANG-IN

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