Anticancer activity of Celtis tournefortii Lam. against human liver cancer cells

Kavitha Krishna Nadiger; Valli Gunam; Rajagopal Kalyanaraman; Meenashree Balakrishnan; Kasturi Revathi; Sathya T. Narasimma Barathy

doi:10.7324/JAPS.2024.151332

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Abstract

Celtis tournefortii Lam. (Celtis aetnensis) is a species of plant with extraordinary bioactivities that has received little research and documentation. Its potential to treat human liver cancer has not yet been studied. Therefore, the bark extract was tested in vitro against human hepatocellular carcinoma (HepG2) cells in the current investigation. The extract was found to increase the Reactive Oxygen Species (ROS) levels in tumor cells, causing cytotoxicity. In addition, the lactate dehydrogenase level was found to be elevated, indicating cellular damage. The likelihood that C. tournefortii Lam. will target the AKT protein is suggested by a considerable drop in the expression of the AKT gene. This is the first report on the effectiveness of C. tournefortii Lam. against liver cancer reported thus far. Our results suggest the presence of promising therapeutic compounds in the bark of C. tournefortii Lam.

Keyword: Celtis tournefortii Lam. (Celtis aetnensis) hepatocellular carcinoma anticancer activity cytotoxicity oxidative stress necrosis

Citation:

Nadiger KK, Gunam V, Kalyanaraman R, Balakrishnan M, Revathi K, Barathy STN. Anticancer activity of Celtis tournefortii Lam. against human liver cancer cells. J Appl Pharm Sci. 2024. Online First. http://doi.org/10.7324/JAPS.2024.151332

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Reference

1. Duke JA, Ayensu ES. Medicinal plants of China. 1-5th ed. Algonac, MI: Reference Publications; 1985.
2. Y?ld?r?m I, Ugur Y, Kutlu T. Investigation of antioxidant activity and phytochemical compositions of Celtis tournefortii. Free Radic Antioxid. 2017 Mar 1;7(2):160-5. https://doi.org/10.5530/fra.2017.2.24
3. Benamar K, Koraichi SI, Fikri-Benbrahim K. Ethnobotany, phytochemistry and pharmacological activities of Celtis australis: a review. J Herbmed Pharmacol. 2023 Jan;12(1):54-72. https://doi.org/10.34172/jhp.2023.05
4. Nao A. Acute toxicity, phytochemistry and anti-diarrheal effects of Celtis integrifolia Lam. aqueous leaf extract in Wistar Albino rats. Br J Pharm Res. 2016;14(5):1-7. https://doi.org/10.9734/BJPR/2016/31222
5. Gecibesler IH. Antioxidant activity and phenolic profile of Turkish Celtis tournefortii. Chem Nat Compd. 2019 Jul 1;55(4):738-43. https://doi.org/10.1007/s10600-019-02796-3
6. Adedapo AA, Jimoh FO, Afolayan AJ, Masika PJ. Antioxidant properties of the methanol extracts of the leaves and stems of Celtis africana. Rec Nat Prod. 2009 Jan 1;3(1):23-31. https://doi.org/10.1186/1472-6882-8-53
7. Kim DK, Lim JP, Kim JW, Park HW, Eun JS. Antitumour and anti-inflammatory constituents from Celtis sinensis. Arch Pharm Res. 2005 Jan;28(1):39-43. https://doi.org/10.1007/BF02975133
8. Acquaviva R, Sorrenti V, Santangelo R, Cardile V, Tomasello B, Malfa G, et al. Effects of an extract of Celtis aetnensis (Tornab.) Strobl twigs on human colon cancer cell cultures. Oncol Rep. 2016 Oct 1;36(4):2298-304. https://doi.org/10.3892/or.2016.5035
9. Baran A, Keskin C, Kandemir S?. Rapid biosynthesis of silver nanoparticles by Celtis tournefortii Lam. leaf extract; investigation of antimicrobial and anticancer activities. Kahramanmara? Sütçü ?mam Üniv Tar?m Do?a Derg. 2022 Dec 30;25(1):72-84. https://doi.org/10.18016/ksutarimdoga.vi.1036488
10. Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol. 2010;594:57-72. https://doi.org/10.1007/978-1-60761-411-1_4
11. Watanabe W, Sudo K, Asawa S, Konno K, Yokota T, Shigeta S. Use of lactate dehydrogenase to evaluate the anti-viral activity against influenza A virus. J Virol Methods. 1995;51(2-3):185-91. https://doi.org/10.1016/0166-0934(94)00103-N
12. Nagiah S, Phulukdaree A, Chuturgoon A. Inverse association between microRNA-124a and ABCC4 in HepG2 cells treated with antiretroviral drugs. Xenobiotica. 2016;46(9):825-30. https://doi.org/10.3109/00498254.2015.1118649
13. Yurdakök B, Baydan E. Cytotoxic effects of Eryngium kotschyi and Eryngium maritimum on Hep2, HepG2, Vero and U138 MG cell lines. Pharm Biol. 2013;51(12):1579-85. https://doi.org/10.3109/13880209.2013.803208
14. Tamboli AM, Wadkar KA. Comparative cytotoxic activity of Convolvulus pluricaulis against human hepatoma cell line (HepG2) and normal cell line (L929) via apoptosis pathways by flow cytometry analysis. Bull Natl Res Cent. 2022;46:145. https://doi.org/10.1186/s42269-022-00835-8
15. Sibiya T, Ghazi T, Mohan J, Nagiah S, Chuturgoon AA. Spirulina platensis mitigates the inhibition of selected miRNAs that promote inflammation in HAART-treated HepG2 cells. Plants. 2023;12(1):119. https://doi.org/10.3390/plants12010119
16. Singh N, Zaidi D, Shyam H, Sharma R, Balapure AK. Polyphenols sensitization potentiates susceptibility of MCF-7 and MDA MB-231 cells to centchroman. PLoS One. 2012;7(6):e37736. https://doi.org/10.1371/journal.pone.0037736
17. Sun Y, Liu WZ, Liu T, Feng X, Yang N, Zhou HF. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J Recept Signal Transduct Res. 2015;35(6):600-4. https://doi.org/10.3109/10799893.2015.1030412
18. Tan BL, Norhaizan ME, Chan LC. Manilkara zapota (L) P. Royen leaf water extract induces apoptosis in human hepatocellular carcinoma (HepG2) cells via ERK1/2/Akt1/JNK1 signaling pathways. Evid Based Complement Alternat Med. 2018;2018:7826576. https://doi.org/10.1155/2018/7826576
19. Lim E, Kim G, Kim B, Kim E, Kim SY, Kim Y. Ethanol extract from Cnidium monnieri (L.) Cusson induces cell cycle arrest and apoptosis via regulation of the p53 independent pathway in HepG2 and Hep3B hepatocellular carcinoma cells. Mol Med Rep. 2018;17(2):2572-80. https://doi.org/10.3892/mmr.2017.8183
20. Butt SS, Khan K, Badshah Y, Rafiq M, Shabbir M. Evaluation of pro-apoptotic potential of taxifolin against liver cancer. PeerJ. 2021 May 25;9:e11276. https://doi.org/10.7717/peerj.11276
21. Huang KF, Zhang GD, Huang YQ, Diao Y. Wogonin induces apoptosis and down-regulates survivin in human breast cancer MCF-7 cells by modulating PI3K-AKT pathway. Int Immunopharmacol. 2012;12(2):334-41. https://doi.org/10.1016/j.intimp.2011.12.004

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Nadiger K K [PubMed] [Google Scholar ]

Gunam V [PubMed] [Google Scholar ]

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1. Duke JA, Ayensu ES. Medicinal plants of China. 1-5th ed. Algonac, MI: Reference Publications; 1985.

2. Y?ld?r?m I, Ugur Y, Kutlu T. Investigation of antioxidant activity and phytochemical compositions of Celtis tournefortii. Free Radic Antioxid. 2017 Mar 1;7(2):160-5. https://doi.org/10.5530/fra.2017.2.24

3. Benamar K, Koraichi SI, Fikri-Benbrahim K. Ethnobotany, phytochemistry and pharmacological activities of Celtis australis: a review. J Herbmed Pharmacol. 2023 Jan;12(1):54-72. https://doi.org/10.34172/jhp.2023.05

4. Nao A. Acute toxicity, phytochemistry and anti-diarrheal effects of Celtis integrifolia Lam. aqueous leaf extract in Wistar Albino rats. Br J Pharm Res. 2016;14(5):1-7. https://doi.org/10.9734/BJPR/2016/31222

5. Gecibesler IH. Antioxidant activity and phenolic profile of Turkish Celtis tournefortii. Chem Nat Compd. 2019 Jul 1;55(4):738-43. https://doi.org/10.1007/s10600-019-02796-3

6. Adedapo AA, Jimoh FO, Afolayan AJ, Masika PJ. Antioxidant properties of the methanol extracts of the leaves and stems of Celtis africana. Rec Nat Prod. 2009 Jan 1;3(1):23-31. https://doi.org/10.1186/1472-6882-8-53

7. Kim DK, Lim JP, Kim JW, Park HW, Eun JS. Antitumour and anti-inflammatory constituents from Celtis sinensis. Arch Pharm Res. 2005 Jan;28(1):39-43. https://doi.org/10.1007/BF02975133

8. Acquaviva R, Sorrenti V, Santangelo R, Cardile V, Tomasello B, Malfa G, et al. Effects of an extract of Celtis aetnensis (Tornab.) Strobl twigs on human colon cancer cell cultures. Oncol Rep. 2016 Oct 1;36(4):2298-304. https://doi.org/10.3892/or.2016.5035

9. Baran A, Keskin C, Kandemir S?. Rapid biosynthesis of silver nanoparticles by Celtis tournefortii Lam. leaf extract; investigation of antimicrobial and anticancer activities. Kahramanmara? Sütçü ?mam Üniv Tar?m Do?a Derg. 2022 Dec 30;25(1):72-84. https://doi.org/10.18016/ksutarimdoga.vi.1036488

10. Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol. 2010;594:57-72. https://doi.org/10.1007/978-1-60761-411-1_4

11. Watanabe W, Sudo K, Asawa S, Konno K, Yokota T, Shigeta S. Use of lactate dehydrogenase to evaluate the anti-viral activity against influenza A virus. J Virol Methods. 1995;51(2-3):185-91. https://doi.org/10.1016/0166-0934(94)00103-N

12. Nagiah S, Phulukdaree A, Chuturgoon A. Inverse association between microRNA-124a and ABCC4 in HepG2 cells treated with antiretroviral drugs. Xenobiotica. 2016;46(9):825-30. https://doi.org/10.3109/00498254.2015.1118649

13. Yurdakök B, Baydan E. Cytotoxic effects of Eryngium kotschyi and Eryngium maritimum on Hep2, HepG2, Vero and U138 MG cell lines. Pharm Biol. 2013;51(12):1579-85. https://doi.org/10.3109/13880209.2013.803208

14. Tamboli AM, Wadkar KA. Comparative cytotoxic activity of Convolvulus pluricaulis against human hepatoma cell line (HepG2) and normal cell line (L929) via apoptosis pathways by flow cytometry analysis. Bull Natl Res Cent. 2022;46:145. https://doi.org/10.1186/s42269-022-00835-8

15. Sibiya T, Ghazi T, Mohan J, Nagiah S, Chuturgoon AA. Spirulina platensis mitigates the inhibition of selected miRNAs that promote inflammation in HAART-treated HepG2 cells. Plants. 2023;12(1):119. https://doi.org/10.3390/plants12010119

16. Singh N, Zaidi D, Shyam H, Sharma R, Balapure AK. Polyphenols sensitization potentiates susceptibility of MCF-7 and MDA MB-231 cells to centchroman. PLoS One. 2012;7(6):e37736. https://doi.org/10.1371/journal.pone.0037736

17. Sun Y, Liu WZ, Liu T, Feng X, Yang N, Zhou HF. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J Recept Signal Transduct Res. 2015;35(6):600-4. https://doi.org/10.3109/10799893.2015.1030412

18. Tan BL, Norhaizan ME, Chan LC. Manilkara zapota (L) P. Royen leaf water extract induces apoptosis in human hepatocellular carcinoma (HepG2) cells via ERK1/2/Akt1/JNK1 signaling pathways. Evid Based Complement Alternat Med. 2018;2018:7826576. https://doi.org/10.1155/2018/7826576

19. Lim E, Kim G, Kim B, Kim E, Kim SY, Kim Y. Ethanol extract from Cnidium monnieri (L.) Cusson induces cell cycle arrest and apoptosis via regulation of the p53 independent pathway in HepG2 and Hep3B hepatocellular carcinoma cells. Mol Med Rep. 2018;17(2):2572-80. https://doi.org/10.3892/mmr.2017.8183

20. Butt SS, Khan K, Badshah Y, Rafiq M, Shabbir M. Evaluation of pro-apoptotic potential of taxifolin against liver cancer. PeerJ. 2021 May 25;9:e11276. https://doi.org/10.7717/peerj.11276

21. Huang KF, Zhang GD, Huang YQ, Diao Y. Wogonin induces apoptosis and down-regulates survivin in human breast cancer MCF-7 cells by modulating PI3K-AKT pathway. Int Immunopharmacol. 2012;12(2):334-41. https://doi.org/10.1016/j.intimp.2011.12.004