Antioxidant and Anticancer Potentials and Metabolic Profiling of Benjakul, A Thai Herbal Preparation

Main Article Content

Kunyarat Duenngai
Bundit Promraksa
Sutthiwan Janthamala
Malinee Thanee
Papitchaya Sirithawat
Supaporn Wisungre
Sumalin Deechan
Nawarat Meechai
Phakamas Paratang
Anchalee Techasen

Abstract

Benjakul (BJK), a Thai folk remedy has been used in traditional medicine for the treatment of
various illnesses. This study aimed to assess the antioxidant, and anticancer properties, and
metabolic profile of Benjakul. The antioxidant activity of the ethanol extract of BJK and its
component medicinal plants (Piper retrofractum Vahl., Piper sarmentosum Roxb., Piper
interuptum Opiz., Plumbago indica L., and Zingiber officinale Rosc.) was assessed using the
Ferric Reducing Antioxidant Power (FRAP) assay, and 2,2-diphenyl-1-picrylhydrazyl (DPPH)
free radical scavenging assay. The anticancer activity was assessed through cytotoxic effect
against cholangiocarcinoma (CCA) (bile duct cancer) cell lines (KKU-213B and KKU-100) using
the 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay. The metabolic
fingerprint and potential bioactive compounds in the ethanol extract of BJK and component
medicinal plants was investigated using Nuclear Magnetic Resonance (NMR) spectroscopy. The
FRAP and DPPH assays revealed that the ethanol extracts of BJK and its component medicinal
plants possessed antioxidant activity with Zingiber officinale exhibiting the highest activity. The
FRAP value and EC50 for DPPH radical scavenging activity for Zingiber officinale were 94.860 ±
0.156 µg AAE/mg extract and 86.63 g/mL, respectively. The metabolic profiling identified
vanillic acid and curcumin as the main bioactive metabolites in BJK and its component medicinal
plants. The partial least squares (PLS) loading plot revealed that the methoxy group is associated
with the inhibition of CCA cells, and phenolic hydroxyl protons as the potential pharmacophore
of the bioactive molecules. Therefore, BJK could be considered as a potentially effective treatment
for bile duct cancer.

Downloads

Download data is not yet available.

Article Details

How to Cite
Duenngai, K., Promraksa, B., Janthamala, S., Thanee, M., Sirithawat, P., Wisungre, S., Deechan, S., Meechai, N., Paratang, P., & Techasen, A. (2024). Antioxidant and Anticancer Potentials and Metabolic Profiling of Benjakul, A Thai Herbal Preparation. Tropical Journal of Natural Product Research (TJNPR), 8(4), 6877-6883. https://doi.org/10.26538/tjnpr/v8i4.18
Section
Articles

How to Cite

Duenngai, K., Promraksa, B., Janthamala, S., Thanee, M., Sirithawat, P., Wisungre, S., Deechan, S., Meechai, N., Paratang, P., & Techasen, A. (2024). Antioxidant and Anticancer Potentials and Metabolic Profiling of Benjakul, A Thai Herbal Preparation. Tropical Journal of Natural Product Research (TJNPR), 8(4), 6877-6883. https://doi.org/10.26538/tjnpr/v8i4.18

References

Yanda L, Tatsimo SJN, Tamokou JDD, Matsuete-Takongmo G, Meffo-Dongmo SC, Meli Lannang A, Sewald N. Antibacterial and antioxidant activities of isolated compounds from Prosopis africana leaves. Int J Anal Chem. 2022; 2022:4205823.

Wetchakul P, Goon JA, Adekoya AE, Olatunji OJ, Ruangchuay S, Jaisamut P, Issuriya A, Kunworarath N, Limsuwan S, Chusri S. Traditional tonifying polyherbal infusion, Jatu-Phala-Tiga, exerts antioxidant activities and extends lifespan of Caenorhabditis elegans. BMC Complement Alternat Med. 2019; 19:1–11.

Louis XL, Thandapilly SJ, Kalt W, Vinqvist-Tymchuk M, Aloud BM, Raj P, Yu L, Le H, Netticadan T. Blueberry polyphenols prevent cardiomyocyte death by preventing calpain activation and oxidative stress. Food Funct. 2014; 5(8):1785–1794.

Itharat A, Singchangchai P, Ratanasuwan P. Wisdom of Southern Thai traditional doctors. Prince of Songkla University, Songkla. 1998. 126 p.

Rachawat P, Pinsornsak P, Kanokkangsadal P, Itharat A. Clinical efficacy and safety of Benjakul remedy extract for treating primary osteoarthritis of knee compared with diclofenac: double blind, randomized controlled trial. Evid-Based Complement Alternat Med. 2017; 2017:9593580.

Pawa KK. In vitro cytotoxic activity of Benjakul herbal preparation and its active compounds against human lung, cervical and liver cancer cells. J Med Assoc Thai. 2012; 95(1):S127–134.

Makchuchit S, Rattarom R, Itharat A. The anti-allergic and anti-inflammatory effects of Benjakul extract (a Thai traditional medicine), its constituent plants and its some pure constituents using in vitro experiments. Biomed Pharmacother.

; 89:1018–1026.

Burodom A and Itharat A. Inflammatory suppressive effect of Benjakul, a Thai traditional medicine on intestinal epithelial cell line. J Med Plant Res. 2013; 7(44):3286–3291.

Thummawan C, Itharat A, Asasutjarit R. Anti-inflammatory activities of nanoemulsion containing Benjakul Remedy extract. Thammasat Med J. 2019; 19(2):359–370.

Kuropakornpong P, Itharat A, Panthong S, Sireeratawong S, Ooraikul B. In vitro and in vivo anti-inflammatory activities of Benjakul: a potential medicinal product from Thai traditional medicine. Evid-Based Complement Alternat Med. 2020; 2020:9760948.

Sakpakdeejaroen I and Itharat A. Cytotoxic compounds against breast adenocarcinoma cells (MCF-7) from Pikutbenjakul. J Health Res. 2009; 23(2):71–76.

Rattarom R, Hansakul P, Sakpakdeejaroen I, Itharat A. Induction of apoptosis in human lung cancer NCI-H226 cells by ethanolic extract of Benjakul preparation and its isolated compound. Planta Med. 2013; 79(13):PN89.

Itharat A, Rattarom R, Hansakul P, Sakpakdeejaroen I, Ooraikul B, Davies NM. The effects of Benjakul extract and its isolated compounds on cell cycle arrest and apoptosis in human non-small cell lung cancer cell line NCI-H226. Res Pharm Sci. 2021; 16(2):129.

Pfeffer CM and Singh ATK. Apoptosis: a target for anticancer therapy. Int J Mol Sci. 2018; 19(2):448.

Golshan A, Amini E, Emami SA, Asili J, Jalali Z, Sabouri-Rad S, Sanjar-Mousavi N, Tayarani-Najaran Z. Cytotoxic evaluation of different fractions of Salvia chorassanica Bunge on MCF-7 and DU 145 cell lines. Res Pharm Sci. 2016; 11(1):73.

Homayoun M, Targhi RG, Soleimani M. Anti-proliferative and anti-apoptotic effects of grape seed extract on chemo-resistant OVCAR-3 ovarian cancer cells. Res Pharm Sci. 2020; 15(4):390.

Ahmadi F, Mojarrab M, Ghazi-Khansari M, Hosseinzadeh L. A semipolar fraction of petroleum ether extract of Artemisia aucheri induces apoptosis and enhances the apoptotic response to doxorubicin in human neuroblastoma SKNMC cell line. Res Pharm Sci. 2015; 10(4):335.

Ahmad A, Banerjee S, Wang Z, Kong D, Sarkar FH. Plumbagin‐induced apoptosis of human breast cancer cells is mediated by inactivation of NF‐κB and Bcl‐2. J Cell Biochem. 2008; 105(6):1461–1471.

Warin RF, Chen H, Soroka DN, Zhu Y, Sang S. Induction of lung cancer cell apoptosis through a p53 pathway by [6]-shogaol and its cysteine-conjugated metabolite M2. J Agric Food Chem. 2014; 62(6):1352–1362.

Gomathinayagam R, Sowmyalakshmi S, Mardhatillah F, Kumar R, Akbarsha MA, Damodaran C. Anticancer mechanism of plumbagin, a natural compound, on non-small cell lung cancer cells. Anticancer Res. 2008; 28(2A):785–792.

Chen CY, Liu TZ, Liu YW, Tseng WC, Liu RH, Lu FJ, Lin YS, Kuo SH, Chen CH. 6-shogaol (alkanone from ginger) induces apoptotic cell death of human hepatoma p53 mutant Mahlavu subline via an oxidative stress-mediated caspase-dependent mechanism. J Agric Food Chem. 2007; 55(3):948–954.

Rabbi F, Sharmin N, Khatun MCS, Hasan M, Muhit MA. Comparative Phytochemical and Biological Analyses of commercial Green Tea Products Marketed in Dhaka, Bangladesh. Trop J Nat Prod Res. 2023; 7(12):5470-5478.

Gougeon L, Da Costa G, Le Mao I, Ma W, Teissedre PL, Guyon F, Richard T. Wine analysis and authenticity using 1 H-NMR metabolomics data: Application to Chinese wines. Food Anal Methods. 2018; 11:3425–3434.

Ravaglia LM, Freitas D dos S, Ricci TG, Nazario CED, Alcantara GB. Sodium quantitation in soft drinks: A rapid methodology by qNMR. Magn Reson Chem. 2020; 58(2):186–190.

Herlyanti K, Fakhrudin N, Murwanti R, Wahyono A. Identification of Cubebin from Cubeb (Piper cubeba) as An Antiplatelet Agent. Trop J Nat Prod Res. 2023; 7(7):3392-3397.

Jaurila H, Koivukangas V, Koskela M, Gäddnäs F, Myllymaa S, Kullaa A, Salo T, Ala-Kokko TI. 1H NMR based metabolomics in human sepsis and healthy serum. Metabol. 2020; 10(2):70.

Petras M, Kalenska D, Samos M, Bolek T, Sarlinova M, Racay P, Halasova E, Strbak O, Stasko J, Musak L. NMR plasma metabolomics study of patients overcoming acute myocardial infarction: in the first 12 h after onset of chest pain with statistical discrimination towards metabolomic biomarkers. Physiol Res. 2020; 69(5):823.

Igbo EU, Igoli OJ, Onyiriuka OS, Ogukwe EC, Ayuk AA, Gray IA. Isolation and Characterization of Pyropheophorbide-a from Moringa oleifera Lam. Trop J Nat Prod Res. 2019; 3(10):314 - 318.

Tamvapee P, Samosorn S, Watanapokasin R. Identification of Active Fatty Acid Mixture Extracted from Rice Bran Oil Using NMR Spectroscopy. Trop J Nat Prod Res. 2023; 7(4):2756-2759.

Wang ZF, You YL, Li FF, Kong WR, Wang SQ. Research progress of NMR in natural product quantification. Molecules. 2021; 26(20):6308.

Lin Y, Li JJ, He L, Li QR, Long QD, Zhang X, Zeng Z. A new modified pterocarpan glycoside from Sophora flavescens. Nat Prod Res. 2023; 37(20):3374-3379.

Tajidin NE, Shaari K, Maulidiani M, Salleh NS, Ketaren BR, Mohamad M. Metabolite profiling of Andrographis paniculata (Burm. f.) Nees. young and mature leaves at different harvest ages using 1H NMR-based metabolomics approach. Sci Rep. 2019; 9(1):16766.

Promraksa B, Phetcharaburanin J, Namwat N, Techasen A, Boonsiri P, Loilome W. Evaluation of anticancer potential of Thai medicinal herb extracts against cholangiocarcinoma cell lines. PLoS One. 2019; 14(5):e0216721.

Benzie IFF and Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem. 1996; 239(1):70–76.

Cloarec O, Dumas ME, Craig A, Barton RH, Trygg J, Hudson J, Blancher C, Gauguier D, Lindon JC, Holmes E. Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets. Anal Chem. 2005; 77(5):1282–1289.

Wishart DS, Guo A, Oler E, Wang F, Anjum A, Peters H, Dizon R, Sayeeda Z, Tian S, Lee BL. HMDB 5.0: the human metabolome database for 2022. Nucl Acids Res. 2022; 50(D1):D622–631.

Lefort G, Liaubet L, Canlet C, Tardivel P, Père MC, Quesnel H, Paris A, Iannuccelli N, Vialaneix N, Servien R. ASICS: an R package for a whole analysis workflow of 1D 1H NMR spectra. Bioinformatics. 2019; 35(21):4356–4363.

Vu TN, Valkenborg D, Smets K, Verwaest KA, Dommisse R, Lemiere F, Verschoren A, Goethals B, Laukens K. An integrated workflow for robust alignment and simplified quantitative analysis of NMR spectrometry data. BMC Bioinformatics. 2011; 12(1):1–14.

Dieterle F, Ross A, Schlotterbeck G, Senn H. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal Chem. 2006; 78(13):4281–4290.

Ma L, Zhang M, Zhao R, Wang D, Ma Y, Ai L. Plant natural products: promising resources for cancer chemoprevention. Molecules. 2021; 26(4):933.

Bekkouch O, Dalli M, Harnafi M, Touiss I, Mokhtari I, Assri S El, Harnafi H, Choukri M, Ko SJ, Kim B. Ginger (Zingiber officinale Roscoe), lemon (Citrus limon L.) juices as preventive agents from chronic liver damage induced by CCl4: A Biochemical and Histological Study. Antioxidants. 2022; 11(2):390.

Khalaf NA, Shakya AK, Al-Othman A, El-Agbar Z, Farah H. Antioxidant activity of some common plants. Turk J Biol. 2008; 32(1):51–55.

Ghasemzadeh A, Jaafar HZE, Rahmat A. Antioxidant activities, total phenolics and flavonoids content in two varieties of Malaysia young ginger (Zingiber officinale Roscoe). Molecules. 2010; 15(6):4324–4333.

Marin JJG, Lozano E, Herraez E, Asensio M, Di Giacomo S, Romero MR, Briz O, Serrano MA, Efferth T, Macias RIR. Chemoresistance and chemosensitization in cholangiocarcinoma. Biochim Biophys Acta Mol Basis Dis. 2018; 1864(4 Pt B):1444-1453.

Wu HJ and Chu PY. Role of cancer stem cells in cholangiocarcinoma and therapeutic implications. Int J Mol Sci. 2019; 20(17):4154.

Bogdan M, Floare CG, Pîrnau A. 1H NMR investigation of self-association of vanillin in aqueous solution. In: J Physics: Conf Ser. IOP Publishing; 2009. 012002 p.

Gong J, Zhou S, Yang S. Vanillic acid suppresses HIF-1α expression via inhibition of mTOR/p70S6K/4E-BP1 and Raf/MEK/ERK pathways in human colon cancer HCT116 cells. Int J Mol Sci. 2019; 20(3):465.

Velli SK and Thiruvengadam D. Vanillic acid inhibits lung carcinogenesis by modulates glycoprotein abnormalities, membrane-bound enzymes, and inflammatory markers. Int J Pharm Pharm Sci. 2020; 12(3):83-88.

Ramadoss DP and Sivalingam N. Vanillin extracted from Proso and Barnyard millets induce apoptotic cell death in HT-29 human colon cancer cell line. Nutr Cancer. 2020; 72(8):1422–1437.

Alamri ES, El Rabey HA, Alzahrani OR, Almutairi FM, Attia ES, Bayomy HM, Albalwi RA, Rezk SM. Enhancement of the Protective Activity of Vanillic Acid against Tetrachloro-Carbon (CCl4) Hepatotoxicity in Male Rats by the Synthesis of Silver Nanoparticles (AgNPs). Molecules. 2022; 27(23):8308.