Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017 (2017), Article ID 2413197, 9 pages
https://doi.org/10.1155/2017/2413197
Research Article

In Vitro Anticancer Effect of Gedunin on Human Teratocarcinomal (NTERA-2) Cancer Stem-Like Cells

Institute of Biochemistry, Molecular Biology and Biotechnology, University of Colombo, 90 Cumaratunga Munidasa Mawatha, 03 Colombo, Sri Lanka

Correspondence should be addressed to Sameera Ranganath Samarakoon

Received 5 April 2017; Accepted 9 May 2017; Published 7 June 2017

Academic Editor: Dong-Wook Han

Copyright © 2017 Luxmiga Tharmarajah et al. 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.

Linked References

  1. C. Delude, “Tumorigenesis: testing ground for cancer stem cells,” Nature, vol. 480, no. 7377, pp. S43–S45, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Schwitalla, A. A. Fingerle, P. Cammareri et al., “Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties,” Cell, vol. 152, no. 1-2, pp. 25–38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Zhao, A. Chen, C. H. Jamieson et al., “Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia,” Nature, vol. 458, no. 7239, pp. 776–779, 2009. View at Publisher · View at Google Scholar
  4. X. Lan, Y.-Z. Wu, Y. Wang et al., “CD133 silencing inhibits stemness properties and enhances chemoradiosensitivity in CD133-positive liver cancer stem cells,” International Journal of Molecular Medicine, vol. 31, no. 2, pp. 315–324, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Zheng, Y. Li, J. D. Yang et al., “NDRG2 inhibits hepatocellular carcinoma adhesion, migration and invasion by regulating CD24 expression,” BMC Cancer, vol. 11, article 251, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. G. M. Cragg, D. J. Newman, and K. M. Snader, “Natural products in drug discovery and development,” Journal of Natural Products, vol. 60, no. 1, pp. 52–60, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. S. S. Karhadkar, G. S. Bova, N. Abdallah et al., “Hedgehog signalling in prostate regeneration, neoplasia and metastasis,” Nature, vol. 431, no. 7009, pp. 707–712, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. B. E. Batsaikhan, K. Yoshikawa, N. Kurita et al., “Cyclopamine decreased the expression of sonic hedgehog and its downstream genes in colon cancer stem cells,” Anticancer Research, vol. 34, no. 11, pp. 6339–6344, 2014. View at Google Scholar · View at Scopus
  9. S. S. Chung and J. V. Vadgama, “Curcumin and epigallocatechin gallate inhibit the cancer stem cell phenotype via down-regulation of STAT3-NFκB signaling,” Anticancer Research, vol. 35, no. 1, pp. 39–46, 2015. View at Google Scholar · View at Scopus
  10. Q. Shen and S. Christakos, “The vitamin D receptor, Runx2, and the notch signaling pathway cooperate in the transcriptional regulation of osteopontin,” Journal of Biological Chemistry, vol. 280, no. 49, pp. 40589–40598, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Kakarala, D. E. Brenner, H. Korkaya et al., “Targeting breast stem cells with the cancer preventive compounds curcumin and piperine,” Breast Cancer Research and Treatment, vol. 122, no. 3, pp. 777–785, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. C. A. Patwardhan, A. Fauq, L. B. Peterson, C. Miller, B. S. Blagg, and A. Chadli, “Gedunin inactivates the co-chaperone p23 protein causing cancer cell death by apoptosis,” Journal of Biological Chemistry, vol. 288, no. 10, pp. 7313–7325, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. S. J. Uddin, L. Nahar, J. A. Shilpi et al., “Gedunin, a limonoid from Xylocarpus granatum, inhibits the growth of CaCo-2 colon cancer cell line in vitro,” Phytotherapy Research, vol. 21, no. 8, pp. 757–761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. S. G. Kamath, N. Chen, Y. Xiong et al., “Gedunin, a novel natural substance, inhibits ovarian cancer cell proliferation,” International Journal of Gynecological Cancer, vol. 19, no. 9, pp. 1564–1569, 2009. View at Publisher · View at Google Scholar
  15. S. Santagata, Y. M. Xu, E. M. Wijeratne et al., “Using the heatshock response to discover anticancer compounds that target protein homeostasis,” ACS Chemical Biology, vol. 7, no. 2, pp. 340–349, 2012. View at Google Scholar
  16. K. Mayan, S. R. Samarakoon, K. H. Tennekoon, A. Siriwardana, and J. R. Valverde, “Evaluation of selected natural compounds for cancer stem cells targeted anti-cancer activity: a molecular docking study,” European Journal of Medicinal Plants, vol. 15, no. 4, pp. 1–21, 2016. View at Google Scholar
  17. S. A. Azouaou, F. Emhemmed, N. Idris-Khodja et al., “Selective ROS-dependent p53-associated anticancer effects of the hypoxoside derivative rooperol on human teratocarcinomal cancer stem-like cells,” Investigational New Drugs, vol. 33, no. 1, pp. 64–74, 2015. View at Google Scholar
  18. S. R. Samarakoon, S. B. Kotigala, I. Gammana-Liyanage et al., “Cytotoxic and apoptotic effect of the decoction of the aerial parts of Flueggea leucopyrus on human endometrial carcinoma (AN3CA) cells,” Tropical Journal of Pharmaceutical Research, vol. 13, no. 6, pp. 873–880, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. S. R. Samarakoon, I. Thabrew, B. P. Galhena, and K. H. Tennekoon, “Modulation of apoptosis in human hepatocellular carcinoma (HepG2 cells) by a standardized herbal decoction of Nigella sativa seeds, Hemidesmus indicus roots and Smilax glabra rhizomes with antihepatocarcinogenic effects,” BMC Complement and Alternate Medicine, vol. 12, p. 25, 2012. View at Google Scholar
  20. M. K. Ediriweera, K. H. Tennekoon, S. R. Samarakoon, I. Thabrew, and E. D. de Silva, “Induction of apoptosis in MCF-7 breast cancer cells by sri lankan endemic mango (Mangifera zeylanica) fruit peel through oxidative stress and analysis of its phytochemical constituents,” Journal of Food Biochemistry, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. T. O. Famuyiwa, A. Boe, J. K. Diaka, J. Jebelli, and N. Esiobu, “Enhancement of genistein-induced apoptosis in LNCaP prostate cancer cells,” Journal of Cancer Prevention and Current Research, vol. 4, Article ID 000111, 2016. View at Google Scholar
  22. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. G. T. Yiang, H. F. Tsai, J. R. Chen, P. L. Chou, T. K. Wu et al., “RC-6 ribonuclease induces caspase activation, cellular senescence and neuron-like morphology in NT2 embryonal carcinoma cells,” Oncology Reports, vol. 31, no. 4, pp. 1738–1744, 2014. View at Google Scholar
  24. X. Jiang, H. Jiang, Z. Shen, and X. Wang, “Activation of mitochondrial protease OMA1 by bax and bak promotes cytochrome c release during apoptosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 41, pp. 14782–14787, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Li and J. Yuan, “Caspases in apoptosis and beyond,” Oncogene, vol. 27, no. 48, pp. 6194–6206, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Rana, H. Piplani, V. Vaish, B. Nehru, and S. N. Sanyal, “Downregulation of PI3-K/Akt/PTEN pathway and activation of mitochondrial intrinsic apoptosis by Diclofenac and Curcumin in colon cancer,” Molecular and Cellular Biochemistry, vol. 402, no. 1-2, pp. 225–241, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Lopez and S. W. G. Tait, “Mitochondrial apoptosis: killing cancer using the enemy within,” British Journal of Cancer, vol. 112, pp. 957–962, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Elmore, “Apoptosis: a review of programmed cell death,” Toxicologic Pathology, vol. 35, no. 4, pp. 495–516, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Haupt, M. Berger, Z. Goldberg, and Y. Haupt, “Apoptosis—the p53 network,” Journal of Cell Science, vol. 116, no. 20, pp. 4077–4085, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Damasio Dde, S. Nolte, L. P. Polak et al., “The lectin BJcuL induces apoptosis through TRAIL expression, caspase cascade activation and mitochondrial membrane permeability in a human colon adenocarcinoma cell line,” Toxicon, vol. 90, pp. 299–307, 2014. View at Publisher · View at Google Scholar
  31. J. R. Dynlacht, Z. V. Roberts, M. Earles, J. Henthorn, and J. D. Seno, “Different patterns of DNA fragmentation and degradation of nuclear matrix proteins during apoptosis induced by radiation, hyperthermia or etoposide,” Radiation Research, vol. 154, no. 5, pp. 515–530, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. S. D. Mundle, X. Z. Gao, S. Khan, S. A. Gregory, H. D. Preisler, and A. Raza, “Two in situ labeling techniques reveal different patterns of DNA fragmentation during spontaneous apoptosis in vivo and induced apoptosis in vitro,” Anticancer Research, vol. 15, no. 5, pp. 1895–1904, 1995. View at Google Scholar · View at Scopus
  33. D. Ziech, R. Franco, A. G. Georgakilas et al., “The role of reactive oxygen species and oxidative stress in environmental carcinogenesis and biomarker development,” Chemico-Biological Interactions, vol. 188, no. 2, pp. 334–339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. T. C. Hsieh, D. Halicka, X. Lu et al., “Effects of resveratrol on the G0-G1 transition and cell cycle progression of mitogenically stimulated human lymphocytes,” Biochemical and Biophysical Research Communications, vol. 297, no. 5, pp. 1311–1317, 2002. View at Google Scholar
  35. H. W. Findley, L. Gu, A. M. Yeager, and M. Zhou, “Expression and regulation of Bcl-2, Bcl-xl, and Bax correlate with p53 status and sensitivity to apoptosis in childhood acute lymphoblastic leukemia,” Blood, vol. 89, no. 8, pp. 2986–2993, 1997. View at Google Scholar · View at Scopus
  36. A. Mirza, M. McGuirk, T. N. Hockenberry et al., “Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway,” Oncogene, vol. 21, no. 17, pp. 2613–2622, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. R. J. Youle and A. Strasser, “The BCL-2 protein family: opposing activities that mediate cell death,” Nature Reviews Molecular Cell Biology, vol. 9, no. 1, pp. 47–59, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. D. P. Liu, H. Song, and Y. Xu, “A common gain of function of p53 cancer mutants in inducing genetic instability,” Oncogene, vol. 29, no. 7, pp. 949–956, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. L. E. Giono and J. J. Manfredi, “The p53 tumor suppressor participates in multiple cell cycle checkpoints,” Journal of Cellular Physiology, vol. 209, no. 1, pp. 13–20, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. D. W. Davis, D. A. Weidner, A. Holian, and D. J. McConkey, “Nitric oxide-dependent activation of p53 suppresses bleomycin-induced apoptosis in the lung,” Journal of Experimental Medicine, vol. 192, no. 6, pp. 857–869, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Ritossa, “Discovery of the heat shock response,” Experientia, vol. 18, no. 2, pp. 97-98, 1966. View at Google Scholar
  42. D. Lanneau, M. Brunet, E. Frisan, E. Solary, M. Fontenay, and C. Garrido, “Heat shock proteins: essential proteins for apoptosis regulation,” Journal of Cellular and Molecular Medicine, vol. 12, no. 3, pp. 743–761, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Whitesell and S. L. Lindquist, “HSP90 and the chaperoning of cancer,” Nature Reviews Cancer, vol. 5, no. 10, pp. 761–772, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. C. M. Palermo, C. A. Westlake, and T. A. Gasiewicz, “Epigallocatechin gallate inhibits aryl hydrocarbon receptor gene transcription through an indirect mechanism involving binding to a 90 kDa heat shock protein,” Biochemistry, vol. 44, no. 13, pp. 5041–5052, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. G. E. L. Brandt, T. E. Schmidt, and B. S. J. Blagg, “Gedunin, a novel Hsp90 inhibitor: semisynthesis of derivatives and preliminary structureactivity relationships,” Journal of Medicinal Chemistry, vol. 51, no. 20, pp. 6495–6502, 2008. View at Google Scholar
  46. Y. Okawa, T. Hideshima, P. Steed et al., “SNX-2112, a selective Hsp90 inhibitor, potently inhibits tumor cell growth, angiogenesis, and osteoclastogenesis in multiple myeloma and other hematologic tumors by abrogating signaling via Akt and ERK,” Blood, vol. 113, no. 4, pp. 846–855, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Whitesell, E. G. Mimnaugh, B. De Costa, C. E. Myers, and L. M. Neckers, “Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 18, pp. 8324–8328, 1994. View at Publisher · View at Google Scholar · View at Scopus
  48. G. Chen, P. Cao, and D. V. Goeddel, “TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90,” Molecular Cell, vol. 9, no. 2, pp. 401–410, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. W. B. Pratt and D. O. Toft, “Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery,” Experimental Biology and Medicine, vol. 228, no. 2, pp. 111–133, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Shang and T. B. Tomasi, “The heat shock protein 90-CDC37 chaperone complex is required for signaling by types I and II interferons,” The Journal of Biological Chemistry, vol. 281, no. 4, pp. 1876–1884, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Citri, B. S. Kochupurakkal, and Y. Yarden, “The Achilles heel of ErbB-2/HER2: Regulation by the Hsp90 chaperone machine and potential for pharmacological intervention,” Cell Cycle, vol. 3, no. 1, pp. 51–60, 2004. View at Google Scholar · View at Scopus
  52. J. Davenport, J. R. Manjarrez, L. Peterson, B. Krumm, B. S. J. Blagg, and R. L. Matts, “Gambogic acid, a natural product inhibitor of Hsp90,” Journal of Natural Products, vol. 74, no. 5, pp. 1085–1092, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Li, T. Zhang, Y. Jiang, H.-F. Lee, S. J. Schwartz, and D. Sun, “(-)-Epigallocatechin-3-gallate inhibits Hsp90 function by impairing Hsp90 association with cochaperones in pancreatic cancer cell line mia paca-2,” Molecular Pharmaceutics, vol. 6, no. 4, pp. 1152–1159, 2009. View at Publisher · View at Google Scholar · View at Scopus