Cytotoxic Activities of Methanol Extract and Compounds of Porodaedalea pini Against Colorectal Cancer

Abstract

Porodaedalea pini is a medicinally important mushroom with antioxidant, cytotoxic, immunostimulating, antitumor, antiviral and immunomodulating activities. Therefore, in this study, P. pini methanol extract and isolated compounds from the methanol extract were tested for cytotoxic activities against DLD-1 (colorectal cancer) and CCD-18Co (human colon fibroblast cell line) by using Alamar Blue assay. Cytotoxic activity on DLD-1 was decreased in the order of P. pini methanol extract> 4-(3,4-dihydroxyphenyl)but-3-en-2-one (3)> pinoresinol (2)> ergosta-7,24(28)-dien-3β-ol (1). P. pini methanol extract was determined to have the best cytotoxic activity with the lowest IC50 value on DLD-1 (IC50: 25.33±0.29 µg/mL) and the highest IC50 value on CCD-18Co (434.30±1.45 µg/mL). Within the scope of the findings, it is thought that P. pini mushroom can be used as a new and natural agent in the treatment of colorectal cancer.

Keywords

• Porodaedalea pini
• Colorectal cancer
• Cytotoxic activity
• Extract
• Isolation

References

1. Arnold, M., Sierra, M.S., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2017). Global Patterns and Trends in Colorectal Cancer Incidence and Mortality. Gut, 66, 683-691. http://dx.doi.org/10.1136/gutjnl-2015-310912
2. Ayer, W.A., Muir, D.J., & Chakravarty, P. (1996). Phenolic and Other Metabolites of Phellinus pini, A Fungus Pathogenic to Pine. Phytochemistry, 42, 1321 1324. http://doi.org/10.1016/0031-9422(96)00125-2
3. Dekker, E., Tanis, P.J., Vleugels, J.L.A., Kasi, P.M., & Wallace, M.B. (2019). Colorectal Cancer. Lancet, 394, 1467-1480. https://doi.org/10.1016/S0140-6736(19)32319-0
4. Deveci, E., Tel-Çayan, G., Duru, M.E., & Öztürk, M. (2019a). Chemical Constituents of Porodaedalea pini Mushroom with Cytotoxic, Antioxidant and Anticholinesterase Activities. J. Food Meas. Charact., 13, 2686-2695. https://doi.org/10.1007/s11694-019-00189-2
5. Deveci, E., Çayan, F., Tel‐Çayan, G., & Duru, M.E. (2019b). Structural Characterization and Determination of Biological Activities for Different Polysaccharides Extracted from Tree Mushroom Species. J. Food Biochem., 43(9), e12965. https://doi.org/10.1111/jfbc.12965
6. Dimitrijevic, M., Jovanovic, V.S., Cvetkovic, J., Mitic, M., Petrovic, G., Dordevic, A., & Mitic, V. (2017). Phenolics, Antioxidant Potentials, and Antimicrobial Activities of Six Wild Boletaceae Mushrooms. Anal. Lett., 50, 1691 1709. https://doi.org/10.1080/00032719.2016.1242133
7. Ganeshpurkar, A., Rai, G., & Jain, A.P. (2010). Medicinal Mushrooms: Towards A New Horizon. Pharmacogn. Rev., 4(8), 127-135. https://doi.org/10.4103/0973-7847.70904
8. He, J.B., Tao, J., Miao, X.S., Feng, Y.P., Bu, W., Dong, Z.J., Li, Z.H., Feng, T., & Liu, J.K. (2015). Two New Illudin Type Sesquiterpenoids from Cultures of Phellinus tuberculosus and Laetiporus sulphureus. J. Asian Nat. Prod. Res., 17, 1054-1058. https://doi.org/10.1080/10286020.2015.1040774

9. Hong, Y.J., Jang, A.R., & Yang, K.S. (2013). Inhibition of Melanin Production and Tyrosinase Expression of Ergosterol Derivatives from Phellinus pini. Nat. Prod. Sci., 19(3), 258-262.
10. Huang, W.Y., Cai, Y.Z. & Zhang, Y. (2010). Natural Phenolic Compounds from Medicinal Herbs and Dietary Plants: Potential Use for Cancer Prevention. Nutr. Cancer, 62(1), 1-20. https://doi.org/10.1080/01635580903191585
11. Ivanova, T.S., Krupodorova, T.A., Barshteyn, V.Y., Artamonova, A.B., & Shlyakhovenko, V.A. (2014). Anticancer Substances of Mushroom Origin. Exp. Oncol., 36(2), 58-66.
12. Jang, H.J., & Yang, K.S. (2011). Inhibition of Nitric Oxide Production in RAW 264.7 Macrophages by Diterpenoids from Phellinus pini. Arch. Pharm. Res., 34, 913-917. https://doi.org/10.1007/s12272-011-0608-z
13. Jeon, T.I., Jung, C.H., Cho, J.Y., Park, D.K., & Moon, J.H. (2013). Identification of an Anticancer Compound Against HT-29 Cells from Phellinus linteus Grown on Germinated Brown Rice. Asian Pac. J. Trop. Biomed., 3(10), 785-789. https://doi.org/10.1016/S2221-1691(13)60156-2
14. Kang, J.H., Jang, J.E., Mishra, S.K., Lee, H.J., Nho, C.W., Shin, D., Jin, M., Kim, M.K., Choi, C., & Oh, S.H. (2015). Ergosterol Peroxide from Chaga Mushroom (Inonotus obliquus) Exhibits Anti-Cancer Activity by Down-Regulation of the β-Catenin Pathway in Colorectal Cancer. J. Ethnopharmacol., 173, 303 312. https://doi.org/10.1016/j.jep.2015.07.030
15. Karakurt, S., & Adali, O. (2016). Tannic Acid Inhibits Proliferation, Migration, Invasion of Prostate Cancer and Modulates Drug Metabolizing and Antioxidant Enzymes. Anti-Cancer Agents Med Chem., 16(6), 781 789. https://doi.org/10.2174/1871520616666151111115809
16. Kelly, J.J., Alberts, S.R., Sacco, F., & Lanier, A.P. (2012). Colorectal Cancer in Alaska Native People, 2005-2009. Gastrointes. Cancer Res., 5, 149-154.
17. Kim, K.A., Chang, H.Y., Choi, S.W., Yoon, J.W., & Lee, C. (2006). Cytotoxic Effects of Extracts from Tremella fuciformis Strain FB001 on the Human Colon Adenocarcinoma Cell Line DLD-1. Food Sci. Biotechnol., 15(6), 889-895.
18. Lim, J.H., Lee, Y.M., Park, S.R., Kim, D.H., & Lim, B.O. (2014). Anticancer Activity of Hispidin via Reactive Oxygen Species-Mediated Apoptosis in Colon Cancer Cells. Anticancer Res., 34, 4087-4094.
19. Mishra, S.K., Kang, K.H., Song, K.H., Park, M.S., Kim, D.K., Park, Y.J., Chop, C., Kim, H.M., Kim, M.K., & Oh, S.H. (2013). Inonotus obliquus Suppresses Proliferation of Colorectal Cancer Cells and Tumor Growth in Mice Models by Downregulation of β-Catenin/NF-kB Signaling Pathways. Eur. J. Inflamm., 11, 615 629. https://doi.org/10.1177/1721727X1301100306
20. Oba, S., Shimizu, N., Nagata, C., Shimizu, H., Kametani, M., Takeyama, N., Ohnuma, T., & Matsushita, S. (2006). The Relationship Between the Consumption of Meat, Fat, and Coffee and the Risk of Colon Cancer: A Prospective Study in Japan. Cancer Lett., 244, 260-267. https://doi.org/10.1016/j.canlet.2005.12.037
21. Patel, S., & Goyal, A. (2012). Recent Developments in Mushrooms as Anti-Cancer Therapeutics: A Review. 3 Biotech., 2, 1-15. https://doi.org/10.1007/s13205-011-0036-2
22. Pei, J.J., Wang, Z.B., Ma, H.L., & Yan, J.K. (2015). Structural Features and Antitumor Activity of A Novel Polysaccharide from Alkaline Extract of Phellinus linteus Mycelia. Carbohyd. Polym., 115, 472-477. https://doi.org/10.1016/j.carbpol.2014.09.017
23. Perdue, D.G., Haverkamp, D., Perkins, C., Daley, C.M., & Provost, E. (2014). Geographic Variation in Colorectal Cancer Incidence and Mortality, Age of Onset, and Stage at Diagnosis Among American Indian and Alaska Native People, 1990-2009. Am. J. Public Health, 104, 404-414. https://doi.org/10.2105/AJPH.2013.301654
24. Reis, F.S., Barreira, J.C.M., Calhelha, R.C., van Griensven, L.J.I.D., Ciric, A., Glamoclija, J., Soković, M., & Ferreira, I.C.F.R. (2014). Chemical Characterization of the Medicinal Mushroom Phellinus linteus (Berkeley & Curtis) Teng and Contribution of Different Fractions to Its Bioactivity. LWT-Food Sci. Technol., 58, 478-485. https://doi.org/10.1016/j.lwt.2014.04.013
25. Seephonkai, P., Samchai, S., Thongsom, A., Sunaart, S., Kiemsanmuang, B., & Chakuton, B. (2011). DPPH Radical Scavenging Activity and Total Phenolics of Phellinus Mushroom Extracts Collected from Northeast of Thailand. Chinese J. Nat. Med., 9(6), 0441-0445. https://doi.org/10.3724/SP.J.1009.2011.00441
26. Seidel, D.V., Azcarate-Peril, M.A., Chapkin, R.S., & Turner, N.D. (2017). Shaping Functional Gut Microbiota Using Dietary Bioactives to Reduce Colon Cancer Risk. Sem. Cancer Biol., 46, 191-204. https://doi.org/10.1016/j.semcancer.2017.06.009
27. Song, A.R., Sun, X.L., Kong, C., Zhao, C., Qin, D., Huang, F., & Yang, S. (2014). Discovery of A New Sesquiterpenoid from Phellinus ignarius with Antiviral Activity Against Influenza Virus. Arch. Virol., 159, 753-760. https://doi.org/10.1007/s00705-013-1857-6
28. Surya, R., Héliès-Toussaint, C., Martin, O.C., Gauthier, T., Guéraud, F., Taché, S., Naud, N., Jouanin, I., Chantelauze, C., Durand, D., Joly, C., Pujos-Guillot, E., Pierre, F.H., & Huc, L. (2016). Red Meat and Colorectal Cancer: Nrf2-Dependent Antioxidant Response Contributes to the Resistance of Preneoplastic Colon Cells to Fecal Water of Hemoglobinand Beef Fed Rats. Carcinogenesis, 37, 635 645. https://doi.org/10.1093/carcin/bgw035
29. Takachi, R., Tsubono, Y., Baba, K., Inoue, M., Sasazuki, S., Iwasaki, M., & Tsugane, S. (2011). Red Meat Intake May Increase the Risk of Colon Cancer in Japanese, A Population with Relatively Low Red Meat Consumption. Asia Pac. J. Clin. Nutr., 20, 603-612.
30. Tao, J., Li, Y., Li, S., & Li, H.B. (2018). Plant Foods for the Prevention and Management of Colon Cancer. J. Funct. Foods, 42, 95-110. https://doi.org/10.1016/j.jff.2017.12.064
31. Turati, F., Rossi, M., Pelucchi, C., Levi, F., & La Vecchia, C. (2015). Fruit and Vegetables and Cancer Risk: A Review of Southern European Studies. Br. J. Nutr., 113, 102-110. https://doi.org/10.1017/S0007114515000148
32. Wang, J., Hu, F., Luo, Y., Luo, H., Huang, N., Cheng, F., Deng, Z., Deng, W., & Zou, K. (2014). Estrogenic and Anti-Estrogenic Activities of Hispolon from Phellinus lonicerinus (Bond.) Bond. et sing. Fitoterapia, 95, 93 101. https://doi.org/10.1016/j.fitote.2014.03.007
33. Wangun, H.V.K., & Hertweck, C. (2007). Squarrosidine and Pinillidine: 3,3'-Fused Bis (Styrylpyrones) from Pholiota squarrosa and Phellinus pini. Eur. J. Org. Chem., 2007, 3292-3295. https://doi.org/10.1002/ejoc.200700090
34. Wu, X., Lin, S., Zhu, C., Yue, Z., Yu, Y., Zhao, F., Liu, B., Dai, J., & Shi, J. (2010). Homo- and Heptanor-Sterols and Tremulane Sesquiterpenes from Cultures of Phellinus igniarius. J. Nat. Prod., 73(7), 1294-1300. https://doi.org/10.1021/np100216k
35. Zhang, H., Shao, Q., Wang, W., Zhang, J., Zhang, Z., Liu, Y., & Yang, Y. (2017). Characterization of Compounds with Tumor–Cell Proliferation Inhibition Activity from Mushroom (Phellinus baumii) Mycelia Produced by Solid-State Fermentation. Molecules, 22(5), 698. https://doi.org/10.3390/molecules22050698