Cytotoxic and antiproliferative effects of Streblus asper from northeastern Thailand on A549 lung cancer cells

Authors

  • Thipphiya KARIRAT Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Thitiyakorn PHANITCHA Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Wanatsuda WIBOONCHAT Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Worachot SAENGHA Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Sirirat DEESEENTHUM Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Issaraporn SOMBOONWATTANAKUL Mahasarakham University, Faculty of Technology, Department of Biotechnology, Natural Antioxidant Innovation Research Unit, Mahasarakham 44150 (TH)
  • Chadaporn SENAKUN Mahasarakham University, Walai Rukhavej Botanical Research Institute, Mahasarakham 44150 (TH)
  • Eakapol WANGKAHART Mahasarakham University, Faculty of Technology, Laboratory of Fish Immunology and Nutrigenomics, Applied Animal and Aquatic Sciences Research Unit, Division of Fisheries, Maha Sarakham 44150 (TH)
  • Sirinya PHOLCHAMAT Mahasarakham University, Faculty of Technology, Department of Biotechnology, Maha Sarakham 44150 (TH)
  • Phitcharat SUNTHAMALA Mahasarakham University, Faculty of Technology, Department of Biotechnology, Maha Sarakham 44150 (TH)
  • 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/nbha51213112

Keywords:

A549, antiproliferation, apoptosis, cytotoxicity, Streblus asper

Abstract

Thailand's second-leading cause of death is lung cancer. Thai indigenous herbal plants are sought after as an alternative treatment against lung cancer. This work aimed to examine cytotoxic, antiproliferative and antimigratory capacities of different parts of Streblus asper (SA) from northeastern Thailand on A549 lung cancer cells. Plant leaves, twigs, bark and wood were used for ethanolic extraction by maceration. The highest cytotoxicity of 85.46% was found in twig extract (IC50 57.46 µg/mL) assessed by an MTT assay. The lowest IC50 (18.42 µg/mL) was also found in twig extract using a clonogenic assay indicating its most antiproliferative activity in a long-term therapy. In addition, all SA extracts displayed antimigratory activity against A549 cells in a dose-dependent fashion, especially twig extract. Apoptotic characteristics were noticeable in SA extract treated cells. The maximum DPPH-scavenging activity, FRAP value, total phenolic and flavonoid content were found in twig extract. GC-MS analysis revealed that twig extract contained four prominent components namely ethyl-α-D-glucopyranoside, hexadecanoic acid, ethyl ester, lupeol and γ-sitosterol. Real-time PCR results showed that genes (Bcl-2, Bax, p21, and cytochrome c) linked to apoptosis were significantly affected by all SA extracts. The various SA components' ethanolic extracts exhibited moderate-to-high cytotoxic action towards A549 cells. This work will significantly advance the utilization of the plant as an alternative source of medicine for rural Thais, and it paves the way for future research to determine the active compound(s) and anticipate new drug candidates.

References

Addai ZR, Abood MS, Hlail SH (2022). GC-MS profiling, antioxidants and antimicrobial activity of prickly pear (Opuntiaficus-indica) pulp extract. Pharmacognosy Journal 14(2):262-267. https://doi.org/10.5530/pj.2022.14.32

Ahmad S, Ullah F, Zeb A, Ayaz M, Ullah F, Sadiq A (2016). Evaluation of Rumex hastatus D. Don for cytotoxic potential against HeLa and NIH/3T3 cell lines: chemical characterization of chloroform fraction and identification of bioactive compounds. BMC Complementary and Alternative Medicine 16(1):308. https://doi.org/10.1186/s12906-016-1302-y

Ahmed FRS, Amin R, Hasan I, Asaduzzaman AKM, Kabir SR (2017). Antitumor properties of a methyl-β-d-galactopyranoside specific lectin from Kaempferia rotunda against Ehrlich ascites carcinoma cells. International Journal of Biological Macromolecules 102:952-959. https://doi.org/10.1016/j.ijbiomac.2017.04.109

Alkhatib MH, Alkhayyal NS (2016). The apoptotic effect of gemcitabine-loaded-microemulsion (isopropyl myristate/tween 80/span 20/water/ethanol) on A549 non-small cell lung cancer cells. Cytologia 81(4):423-429. https://doi.org/10.1508/CYTOLOGIA.81.423

Bakrim S, Benkhaira N, Bourais I, Benali T, Lee LH, El Omari N, ... Bouyahya A (2022). Health benefits and pharmacological properties of Stigmasterol. Antioxidants (Basel, Switzerland) 11(10):1912. https://doi.org/10.3390/antiox11101912

Bastos IVGA, Oliveira TB, Rodrigues MD, Militão GCG, Silva TGD, Turatti ICC, … Melo SJ (2017). Use of GC/MS to identify chemical constituents and cytotoxic activity of the leaves of Phoradendron mucronatum and Phoradendron microphyllum (Viscaceae). Anais da Academia Brasileira de Ciencias 89(2):991-1001. https://doi.org/10.1590/0001-3765201720160586

Chen WL, Ren Y, Ren J, Erxleben C, Johnson ME, Gentile S, … Burdette JE (2017). (+)-Strebloside-induced cytotoxicity in ovarian cancer cells is mediated through cardiac glycoside signaling networks. Journal of Natural Products 80(3):659-669. https://doi.org/10.1021/acs.jnatprod.6b01150

Chudzik M, Korzonek-Szlacheta I, Król W (2015). Triterpenes as potentially cytotoxic compounds. Molecules (Basel, Switzerland) 20(1):1610-1625. https://doi.org/10.3390/molecules20011610

Cioccoloni G, Soteriou C, Websdale A, Wallis L, Zulyniak MA, Thorne JL (2022). Phytosterols and phytostanols and the hallmarks of cancer in model organisms: A systematic review and meta-analysis. Critical Reviews in Food Science and Nutrition 62(5):1145-1165. https://doi.org/10.1080/10408398.2020.1835820

Ettinger DS, Akerley W, Bepler G, Blum MG, Chang A, Cheney RT, ... Yang SC (2010). Non–small cell lung cancer. Journal of the National Comprehensive Cancer Network 8(7):740-801. https://doi.org/10.6004/ jnccn.2012.0130

Hasan A, Artika I, Kuswandi TG (2014). Analysis of active components of Trigona spp. propolis from Pandeglang Indonesia. Global Journal of Biology, Agriculture and Health Science 3:215-219.

Hecht I, Natan S, Zaritsky A, Levine H, Tsarfaty I, Ben-Jacob E (2015). The motility-proliferation-metabolism interplay during metastatic invasion. Scientific Reports 4(5):13538. https://doi.org/10.1038/srep13538

Ibrahim NM, Mat I, Lim V, Ahmad R (2013). Antioxidant activity and phenolic content of Streblus asper leaves from various drying methods. Antioxidants (Basel, Switzerland) 2(3):156-166. https://doi.org/10.3390/antiox 2030156

Kadir MF, Bin Sayeed MS, Setu NI, Mostafa A, Mia MM (2014). Ethnopharmacological survey of medicinal plants used by traditional health practitioners in Thanchi, Bandarban Hill Tracts, Bangladesh. Journal of Ethnopharmacology 155(1):495-508. http://dx.doi.org/10.1016/j.jep.2014.05.043

Khan G N, Kumar N, Ballal R A, Datta D, Belle VS (2021). Unveiling antioxidant and anti-cancer potentials of characterized Annona reticulata leaf extract in 1,2-dimethylhydrazine-induced colorectal cancer in Wistar rats. Journal of Ayurveda and Integrative Medicine 12(4):579-589. https://doi.org/10.1016/ j.jaim.2021.05.010

Kumar M, Prakash S, Kumari N, Pundir A, Punia S, Saurabh V, ... Mekhemar M (2021). Beneficial role of antioxidant secondary metabolites from medicinal plants in maintaining oral health. Antioxidants 10(7):1061. https://doi.org/10.3390/antiox10071061

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(4):1685-1698. https://doi.org/10.1002/jsfa.10985

Lyantagaye SL (2013). Methyl-α-D-glucopyranoside from Tulbaghia violacea extract induces apoptosis in vitro in cancer cells. Bangladesh Journal of Pharmacology 8(2):93-101. https://doi.org/10.3329/bjp.v8i2.13717

Miao D, Zhang T, Xu J, Ma C, Liu W, Kikuchi T, … Zhang J (2018). Three new cardiac glycosides obtained from the roots of Streblus asper Lour. and their cytotoxic and melanogenesis-inhibitory activities. RSC Advances 8(35):19570-19579. https://doi.org/10.1039/c8ra00733k

Mofeed J, Deyab M, Sabry AEN, Ward F (2021). In vitro anticancer activity of five marine seaweeds extract from Egypt against human breast and colon cancer cell lines. Research Square. https://doi.org/10.21203/rs.3.rs-462221/v1

Nabil M, Seeni A, Ismail WI, Rahim Ab, Dzulkarnain SMH (2019). Induction of apoptotic mechanism by Streblus asper root extract on cervical cancer using in vitro and in vivo models. Biomedical and Pharmacology Journal 12(4):1661-1673. https://dx.doi.org/10.13005/bpj/1796

Neto SF, Prada AL, Achod LDR, Torquato HFV, Lima CS, Paredes-Gamero EJ, … Amado JRR (2021). α-amyrin-loaded nanocapsules produce selective cytotoxic activity in leukemic cells. Biomedicine and Pharmacotherapy 139:111656. https://doi.org/10.1016/j.biopha.2021.111656

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(11):5988. https://doi.org/10.3390/ijerph18115988

Osman Mohammed RM, Huang Y, Guan X, Huang X, Deng S, Yang R, … Li J (2022). Cytotoxic cardiac glycosides from the root of Streblus asper. Phytochemistry 200:113239. https://doi.org/10.1016/j.phytochem.2022.113239

Priaulx J, de Koning HJ, de Kok IMCM, Széles G, McKee M (2018). Identifying the barriers to effective breast, cervical and colorectal cancer screening in thirty-one European countries using the Barriers to Effective Screening Tool (BEST). Health Policy (Amsterdam, Netherlands) 122(11):1190-1197. https://doi.org/10.1016/ j.healthpol.2018.08.004

Rajendran N, Ananthathamula R, Arun KP, Brindha P (2014). Anticancer and antioxidant activity of ethanolic extract of Markhamia lutea (Benth) K. schum stem bark. Asian Journal of Chemistry 26(12):3741-3744. https://doi.org/10.14233/ajchem.2014.17066

Rastogi S, Kulshreshtha DK, Rawat AK (2006). Streblus asper Lour. (Shakhotaka): A review of its chemical, pharmacological and ethnomedicinal properties. Evidence-based Complementary and Alternative Medicine 3(2):217-222. https://doi.org/10.1093/ecam/nel018

Rawat P, Kumar A, Singh TD, Pal M (2018). Chemical composition and cytotoxic activity of methanol extract and its fractions of Streblus asper leaves on human cancer cell lines. Pharmacognosy Magazine 14(54):141-144. https://doi.org/10.4103/pm.pm_391_17

Ren Y, Tan Q, Heath K, Wu S, Wilson JR, Ren J, … Kinghorn AD (2020). Cytotoxic and non-cytotoxic cardiac glycosides isolated from the combined flowers, leaves, and twigs of Streblus asper. Bioorganic and Medicinal Chemistry 28(4):115301. https://doi.org/10.1016/j.bmc.2019.115301

Reungwetwattana T, Oranratnachai S, Puataweepong P, Tangsujaritvijit V, Cherntanomwong P (2020). Lung cancer in Thailand. Lung Cancer Worldwide 15(11):1714-1721. https://doi.org/10.1016/j.jtho.2020.04.024

Saengha W, Karirat T, Buranrat B, Matra K, Deeseenthum S, Katisart T, … Luang-In V (2021). Cold plasma treatment on mustard green seeds and its effect on growth, isothiocyanates, antioxidant activity and anticancer activity of microgreens. International Journal of Agriculture and Biology 25(3):667-676. https://doi.org/10.17957/IJAB/15.1715

Seeni A, Zulkepli NA, Wahab RA (2012). Apoptosis inducer from Streblus asper extracts for cancer chemoprevention. In: Chen G, Lai P (Eds). Novel Apoptotic Regulators in Carcinogenesis. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4917-7_1

Sundarraj S, Thangam R, Sreevani V, Kaveri K, Gunasekaran P, Achiraman S, Kannan S (2012). γ-Sitosterol from Acacia nilotica L. induces G2/M cell cycle arrest and apoptosis through c-Myc suppression in MCF-7 and A549 cells. Journal of Ethnopharmacology 141(3):803-809. https://doi.org/10.1016/j.jep.2012.03.014

Vicus D, Sutradhar R, Lu Y, Elit L, Kupets R, Paszat L, ... Investigators of the Ontario Cancer Screening Research Network (2014). The association between cervical cancer screening and mortality from cervical cancer: a population based case-control study. Gynecologic Oncology 133(2):167-171. https://doi.org/10.1016/j.ygyno.2014.02.037

Wangkahart E, Jumpalueang S, Ardprachan S, Phudkliang J, Sunthamala P, Pholchamat S, ... Qi Z (2022). Molecular characterization and expression analysis of novel interleukin-1 family member (nIL-1Fm) gene in Nile Tilapia (Oreochromis niloticus). Journal of Marine Science and Engineering 10(9):1272. https://doi.org/10.3390/jmse10091272

Yoshida Y, Schmaltz CL, Jackson-Thompson J, Simoes EJ (2018). The impact of screening on cancer incidence and mortality in Missouri, USA, 2004-2013. Public Health 154:51-58. https://doi.org/10.1016/j.puhe.2017.10.015

Zhang BD, Zhu WF, Akihisa T, Kikuchi T, Ukiya M, Maya F, … Zhang J (2021). Cardiac glycosides from the roots of Streblus asper Lour. and their apoptosis-inducing activities in A549 cells. Phytochemistry 181:112544. https://doi.org/10.1016/j.phytochem.2020.112544

Zhang P, Chen PL, Li ZH, Zhang A, Zhang XR, Zhang YJ, … Mao C (2022). Association of smoking and polygenic risk with the incidence of lung cancer: a prospective cohort study. British Journal of Cancer 126(11):1637-1646. https://doi.org/10.1038/s41416-022-01736-3

Downloads

Published

2023-06-07

How to Cite

KARIRAT, T., PHANITCHA, T., WIBOONCHAT, W., SAENGHA, W., DEESEENTHUM, S., SOMBOONWATTANAKUL, I., SENAKUN, C., WANGKAHART, E., PHOLCHAMAT, S., SUNTHAMALA, P., & LUANG-IN, V. (2023). Cytotoxic and antiproliferative effects of Streblus asper from northeastern Thailand on A549 lung cancer cells. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 51(2), 13112. https://doi.org/10.15835/nbha51213112

Issue

Vol. 51 No. 2 (2023)

Section

Research Articles
CITATION
DOI: 10.15835/nbha51213112

License

Copyright (c) 2023 Thipphiya KARIRAT, Thitiyakorn PHANITCHA, Wanatsuda WIBOONCHAT, Worachot SAENGHA, Sirirat DEESEENTHUM, Issaraporn SOMBOONWATTANAKUL, Chadaporn SENAKUN, Eakapol WANGKAHART, Sirinya PHOLCHAMAT, Phitcharat SUNTHAMALA, Vijitra LUANG-IN

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

License:

© Articles by the authors; licensee UASVM and SHST, Cluj-Napoca, Romania. Papers published in the journal Notulae Botanicae Horti Agrobotanici Cluj-Napoca are open access distributed under the terms and conditions of the Creative Commons Attribution License (http://creativecommons.org/licenses).

Open Access Journal:

The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.

Most read articles by the same author(s)