Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Taxol Produced from Endophytic Fungi Induces Apoptosis in Human Breast, Cervical and Ovarian Cancer Cells

  • Wang, Xin (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University) ;
  • Wang, Chao (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University) ;
  • Sun, Yu-Ting (Heilongjiang College Construction) ;
  • Sun, Chuan-Zhen (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University) ;
  • Zhang, Yue (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University) ;
  • Wang, Xiao-Hua (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University) ;
  • Zhao, Kai (Key Laboratory of Microbiology, School of Life Science, Heilongjiang University)
  • Published : 2015.02.04
Download PDF
⟨ Previous Next ⟩

Abstract

Currently, taxol is mainly extracted from the bark of yews; however, this method can not meet its increasing demand on the market because yews grow very slowly and are a rare and endangered species belonging to first-level conservation plants. Recently, increasing efforts have been made to develop alternative means of taxol production; microbe fermentation would be a very promising method to increase the production scale of taxol. To determine the activities of the taxol extracted from endophytic fungus N. sylviforme HDFS4-26 in inhibiting the growth and causing the apoptosis of cancer cells, on comparison with the taxol extracted from the bark of yew, we used cellular morphology, cell counting kit (CCK-8) assay, staining (HO33258/PI and Giemsa), DNA agarose gel electrophoresis and flow cytometry (FCM) analyses to determine the apoptosis status of breast cancer MCF-7 cells, cervical cancer HeLa cells and ovarian cancer HO8910 cells. Our results showed that the fungal taxol inhibited the growth of MCF-7, HeLa and HO8910 cells in a dose-and time-dependent manner. IC50 values of fungal taxol for HeLa, MCF-7 and HO8910 cells were $0.1-1.0{\mu}g/ml$, $0.001-0.01{\mu}g/ml$ and $0.01-0.1{\mu}g/ml$, respectively. The fungal taxol induced these tumor cells to undergo apoptosis with typical apoptotic characteristics, including morphological changes for chromatin condensation, chromatin crescent formation, nucleus fragmentation, apoptotic body formation and G2/M cell cycle arrest. The fungal taxol at the $0.01-1.0{\mu}g/ml$ had significant effects of inducing apoptosis between 24-48 h, which was the same as that of taxol extracted from yews. This study offers important information and a new resource for the production of an important anticancer drug by endofungus fermentation.

Keywords

References

  1. Amos LA, Lowe J (1999). How Taxol stabilises microtubule structure. Chem Biol, 6, 65-9. https://doi.org/10.1016/S1074-5521(99)89002-4
  2. Chakravarthi BV, Sujay R, Kuriakose GC, et al (2013). Inhibition of cancer cell proliferation and apoptosis-inducing activity of fungal taxol and its precursor baccatin III purified from endophytic Fusarium solani. Cancer Cell Int, 13, 105. https://doi.org/10.1186/1475-2867-13-105
  3. Chandar N, Billig B, McMaster J, et al (1992). Inactivation of p53 gene in human and murine osteosarcoma cells. Br J Cancer, 65, 208-14. https://doi.org/10.1038/bjc.1992.43
  4. Davies AM, Weinberg U, Palti Y (2013). Tumor treating fields: a new frontier in cancer therapy. Ann NY Acad Sci, 1291, 86-95. https://doi.org/10.1111/nyas.12112
  5. Dodson M, Darley-Usmar V, Zhang J (2013). Cellular metabolic and autophagic pathways: traffic control by redox signaling. Free Radic Biol Med, 63, 207-21. https://doi.org/10.1016/j.freeradbiomed.2013.05.014
  6. Fauzee NJ (2011). Taxanes: promising anti-cancer drugs. Asian Pac J Cancer Prev, 12, 837-51.
  7. Gangadevi V, Muthumary J (2008). A simple and rapid method for the determination of taxol produced by fungal endophytes from medicinal plants using high performance thin layer chromatography. Se Pu, 26, 50-5.
  8. Ge JP, Ping WX, Ma X, et al (2004). Identification of taxolproducing strain HU1353. J Microbiol, 24, 19-21.
  9. Henley D, Isbill M, Fernando R, et al (2007). Paclitaxel induced apoptosis in breast cancer cells requires cell cycle transit but not Cdc2 activity. Cancer Chemother Pharmacol, 59, 235-49.
  10. Jones WB, Schneider J, Shapiro F, et al (1996). Treatment of resistant gestational choriocarcinoma with taxol: a report of two cases. Gynecol Oncol, 61, 126-30. https://doi.org/10.1006/gyno.1996.0110
  11. Kumaran RS, Muthumary J, Hur BK (2009). Isolation and identification of an anticancer drug, taxol from Phyllosticta tabernaemontanae, a leaf spot fungus of an angiosperm, Wrightia tinctoria. J Microbiol, 47, 40-9. https://doi.org/10.1007/s12275-008-0127-x
  12. Li JY, Strobel G, Sidhu R, et al (1996). Endophytic taxolproducing fungi from bald cypress, Taxodium distichum. Microbiology, 142, 2223-6. https://doi.org/10.1099/13500872-142-8-2223
  13. Mullan PB, Quinn JE, Gilmore PM, et al (2001). BRCA1 and GADD45 mediated G2/M cell cycle arrest in response to antimicrotubule agents. Oncogene, 20, 6123-31. https://doi.org/10.1038/sj.onc.1204712
  14. Park SJ, Wu CH, Gordon JD, et al (2004). Taxol induces caspase-10-dependent apoptosis. J Biol Chem, 279, 51057-67. https://doi.org/10.1074/jbc.M406543200
  15. Raj KG, Sambantham S, Manikanadan R, et al (2014). Fungal taxol extracted from Cladosporium oxysporum induces apoptosis in T47D human breast cancer cell line. Asian Pac J Cancer Prev, 15, 6627-32. https://doi.org/10.7314/APJCP.2014.15.16.6627
  16. Ruden M, Puri N (2013). Novel anticancer therapeutics targeting telomerase. Cancer Treat Rev, 39, 444-56. https://doi.org/10.1016/j.ctrv.2012.06.007
  17. Samadi N, Gaetano C, Goping IS, et al (2009). Autotaxin protects MCF-7 breast cancer and MDA-MB-435 melanoma cells against Taxol-induced apoptosis. Oncogene, 28, 1028-39. https://doi.org/10.1038/onc.2008.442
  18. Schiff PB, Fant J, Horwitz SB (1979). Promotion of microtubule assembly in vitro by taxol. Nature, 277, 665-7. https://doi.org/10.1038/277665a0
  19. Signore M, Ricci-Vitiani L, De Maria R (2013). Targeting apoptosis pathways in cancer stem cells. Cancer Lett, 332, 374-82. https://doi.org/10.1016/j.canlet.2011.01.013
  20. Srinivasan V, Ciddi V, Bringi V, et al (1996). Metabolic inhibitors, elicitors, and precursors as tools for probing yield limitation in taxane production by Taxus chinensis cell cultures. Biotechnol Prog, 12, 457-65. https://doi.org/10.1021/bp9600344
  21. Stierle A, Strobel G, Stierle D (1993). Taxol and taxane production by Taxomyces andreanae, an endophytic fungus of Pacific yew. Science, 260, 214-6. https://doi.org/10.1126/science.8097061
  22. Sun JQ, Zhou DP, Ping WX (2003). A new species of the genus Pleurocytospora. Mycosystema, 22, 12-3.
  23. Tan M, Yu D (2007). Molecular mechanisms of erbB2-mediated breast cancer chemoresistance. Adv Exp Med Biol, 608, 119-29. https://doi.org/10.1007/978-0-387-74039-3_9
  24. Wani MC, Taylor HL, Wall ME, et al (1971). Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc, 93, 2325-7. https://doi.org/10.1021/ja00738a045
  25. Woo HL, Swenerton KD, Hoskins PJ (1996). Taxol is active in platinum-resistant endometrial adenocarcinoma. Am J Clin Oncol, 19, 290-1. https://doi.org/10.1097/00000421-199606000-00016
  26. Yoo YD, Park JK, Choi JY, et al (1998). CDK4 down-regulation induced by paclitaxel is associated with G1 arrest in gastric cancer cells. Clin Cancer Res, 4, 3063-8.
  27. Zaiyou J, Li M, Guifang X, et al (2013). Isolation of an endophytic fungus producing baccatin III from Taxus wallichiana var. mairei. J Ind Microbiol Biotechnol, 40, 1297-302. https://doi.org/10.1007/s10295-013-1320-4
  28. Zhao K, Zhao Li-Fei, Jin Yuan-Yuan, et al (2008a).Isolation of a taxol-producing endophytic fungus and inhibiting effect of the fungus metabolites on HeLa cell. Microbiology, 27, 735-44.
  29. Zhao K, Ping W, Zhang L, et al (2008b). Screening and breeding of high taxol producing fungi by genome shuffling. Sci China C Life Sci, 51, 222-31. https://doi.org/10.1007/s11427-008-0037-5
  30. Zhao K, Ping W, Li Q, et al (2009). Aspergillus niger var. taxi, a new species variant of taxol-producing fungus isolated from Taxus cuspidata in China. J App Microbiol, 107, 1202-7. https://doi.org/10.1111/j.1365-2672.2009.04305.x
  31. Zhou HB, Zhu JR (2003). Paclitaxel induces apoptosis in human gastric carcinoma cells. World J Gastroenterol, 9, 442-5. https://doi.org/10.3748/wjg.v9.i3.442
  32. Zhou DP, Sun JQ, Yu HY, et al (2001). Nodulisporium, a genus new to China. Mycosystema, 20, 277-8.

Cited by

  1. Evaluation of Effects of Metformin in Primary Ovarian Cancer Cells vol.16, pp.16, 2015, https://doi.org/10.7314/APJCP.2015.16.16.6973
  2. An endophytic Basidiomycete, Grammothele lineata, isolated from Corchorus olitorius, produces paclitaxel that shows cytotoxicity vol.12, pp.6, 2017, https://doi.org/10.1371/journal.pone.0178612
  3. Developments in taxol production through endophytic fungal biotechnology: a review pp.2211-1069, 2019, https://doi.org/10.1007/s13596-018-0352-8
  4. Yield enhancement strategies of rare pharmaceutical metabolites from endophytes vol.40, pp.5, 2018, https://doi.org/10.1007/s10529-018-2531-6