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Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 243859, 9 pages
http://dx.doi.org/10.1155/2013/243859
Research Article

Bufalin Reverses HGF-Induced Resistance to EGFR-TKIs in EGFR Mutant Lung Cancer Cells via Blockage of Met/PI3k/Akt Pathway and Induction of Apoptosis

1Department of Clinical Oncology, Long Hua Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200032, China
2Department of Clinical Oncology, Ping Ding Shan First People’s Hospital, Henan 467000, China
3Department of Infection, Ping Ding Shan First People’s Hospital, Henan 467000, China

Received 12 December 2012; Accepted 4 February 2013

Academic Editor: Vincenzo de Feo

Copyright © 2013 Xiao-Hong Kang 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. W. Pao and N. Girard, “New driver mutations in non-small-cell lung cancer,” The Lancet Oncology, vol. 12, no. 2, pp. 175–180, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. I. B. Weinstein, “Cancer: addiction to oncogenes—the Achilles heal of cancer,” Science, vol. 297, no. 5578, pp. 63–64, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. J. J. Laskin and A. B. Sandler, “Epidermal growth factor receptor: a promising target in solid tumours,” Cancer Treatment Reviews, vol. 30, no. 1, pp. 1–17, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Suda, K. Tomizawa, and T. Mitsudomi, “Biological and clinical significance of KRAS mutations in lung cancer: an oncogenic driver that contrasts with EGFR mutation,” Cancer and Metastasis Reviews, vol. 29, no. 1, pp. 49–60, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. W. Pao and J. Chmielecki, “Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer,” Nature Reviews Cancer, vol. 10, no. 11, pp. 760–774, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Jackman, W. Pao, G. J. Riely et al., “Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer,” Journal of Clinical Oncology, vol. 28, no. 2, pp. 357–360, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Kobayashi, T. J. Boggon, T. Dayaram et al., “EGFR mutation and resistance of non-small-cell lung cancer to gefitinib,” The New England Journal of Medicine, vol. 352, no. 8, pp. 786–792, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. J. A. Engelman, K. Zejnullahu, T. Mitsudomi et al., “MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling,” Science, vol. 316, no. 5827, pp. 1039–1043, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Yano, W. Wang, Q. Li et al., “Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations,” Cancer Research, vol. 68, no. 22, pp. 9479–9487, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. L. V. Sequist, B. A. Waltman, D. Dias-Santagata et al., “Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors,” Science Translational Medicine, vol. 3, no. 75, Article ID 75ra26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Yano, W. Wang, Q. Li et al., “Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations,” Cancer Research, vol. 68, no. 22, pp. 9479–9487, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. A. B. Turke, K. Zejnullahu, Y. L. Wu et al., “Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC,” Cancer Cell, vol. 17, no. 1, pp. 77–88, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Yamada, K. Matsumoto, W. Wang et al., “Hepatocyte growth factor reduces susceptibility to an irreversible epidermal growth factor receptor inhibitor in EGFR-T790M mutant lung cancer,” Clinical Cancer Research, vol. 16, no. 1, pp. 174–183, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Nakagawa, S. Takeuchi, T. Yamada et al., “Combined therapy with mutant-selective EGFR inhibitor and met kinase inhibitor for overcoming erlotinib resistance in EGFR-mutant lung cancer,” Molecular Cancer Therapeutics, vol. 11, no. 10, pp. 2149–2157, 2012. View at Publisher · View at Google Scholar
  15. C. X. Lu, K. J. Nan, and Y. Lei, “Agents from amphibians with anticancer properties,” Anti-Cancer Drugs, vol. 19, no. 10, pp. 931–939, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. X. Cui, Y. Inagaki, H. Xu et al., “Anti-hepatitis B virus activities of cinobufacini and its active components bufalin and cinobufagin in HepG2.2.15 Cells,” Biological and Pharmaceutical Bulletin, vol. 33, no. 10, pp. 1728–1732, 2010. View at Google Scholar · View at Scopus
  17. F. Qi, A. Li, Y. Inagaki et al., “Antitumor activity of extracts and compounds from the skin of the toad Bufo bufo gargarizans Cantor,” International Immunopharmacology, vol. 11, no. 3, pp. 342–349, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Qi, Y. Inagaki, B. Gao et al., “Bufalin and cinobufagin induce apoptosis of human hepatocellular carcinoma cells via Fas- and mitochondria-mediated pathways,” Cancer Science, vol. 102, no. 5, pp. 951–958, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. H. Li, P. Wang, Y. Gao et al., “Na+/K+-ATPase α3 mediates sensitivity of hepatocellular carcinoma cells to bufalin,” Oncology Reports, vol. 25, no. 3, pp. 825–830, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. C.-M. Xie, W. Y. Chan, S. Yu, J. Zhao, and C. H. K. Cheng, “Bufalin induces autophagy-mediated cell death in human colon cancer cells through reactive oxygen species generation and JNK activation,” Free Radical Biology and Medicine, vol. 51, no. 7, pp. 1365–1375, 2011. View at Publisher · View at Google Scholar
  21. Y. Amano, Y. Cho, M. Matsunawa, K. Komiyama, and M. Makishima, “Increased nuclear expression and transactivation of vitamin D receptor by the cardiotonic steroid bufalin in human myeloid leukemia cells,” Journal of Steroid Biochemistry and Molecular Biology, vol. 114, no. 3-5, pp. 144–151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Li, X. Qu, K. Hou et al., “PI3K/Akt is involved in bufalin-induced apoptosis in gastric cancer cells,” Anti-Cancer Drugs, vol. 20, no. 1, pp. 59–64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. H. Yu, S. F. Kan, H. F. Pu, E. Jea Chien, and P. S. Wang, “Apoptotic signaling in bufalin- and cinobufagin-treated androgen-dependent and -independent human prostate cancer cells,” Cancer Science, vol. 99, no. 12, pp. 2467–2476, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. Y.-P. Hsiao, C.-S. Yu, C.-C. Yu et al., “Triggering apoptotic death of human malignant melanoma A375.S2 cells by bufalin: involvement of caspase cascade-dependent and independent mitochondrial signaling pathways,” Evidence-Based Complementary and Alternative Medicine, vol. 2012, Article ID 591241, 9 pages, 2012. View at Publisher · View at Google Scholar
  25. Y. Jiang, Y. Zhang, J. Luan et al., “Effects of bufalin on the proliferation of human lung cancer cells and its molecular mechanisms of action,” Cytotechnology, vol. 62, no. 6, pp. 573–583, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. Z. Zhu, H. Sun, G. Ma et al., “Bufalin induces lung cancer cell apotosis via the inhibition of PI3K/Akt pathway,” International Journal of Molecular Sciences, vol. 13, no. 2, pp. 2025–2035, 2012. View at Publisher · View at Google Scholar
  27. L. M. Green, J. L. Reade, and C. F. Ware, “Rapid colormetric assay for cell viability: application to the quantitation of cytotoxic and growth inhibitory lymphokines,” Journal of Immunological Methods, vol. 70, no. 2, pp. 257–268, 1984. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Okabe, I. Okamoto, K. Tamura et al., “Differential constitutive activation of the epidermal growth factor receptor in non-small cell lung cancer cells bearing EGFR gene mutation and amplification,” Cancer Research, vol. 67, no. 5, pp. 2046–2053, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. W. Wang, Q. Li, T. Yamada et al., “Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors,” Clinical Cancer Research, vol. 15, no. 21, pp. 6630–6638, 2009. View at Publisher · View at Google Scholar
  30. I. S. Donev, W. Wang, T. Yamada et al., “Transient PI3K inhibition induces apoptosis and overcomes HGF-mediated resistance to EGFR-TKIs in EGFR mutant lung cancer,” Clinical Cancer Research, vol. 17, no. 8, pp. 2260–2269, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. W. Wang, Q. Li, S. Takeuchi et al., “Met kinase inhibitor E7050 reverses three different mechanisms of hepatocyte growth factor-induced tyrosine kinase inhibitor resistance in EGFR mutant lung cancer,” Clinical Cancer Research, vol. 18, no. 6, pp. 1663–1671, 2012. View at Publisher · View at Google Scholar
  32. S. Gusenbauer, P. Vlaicu, and A. Ullrich, “HGF induces novel EGFR functions involve in resistance formation to tyrosine kinase inhibitors,” Oncogene, 2012. View at Publisher · View at Google Scholar
  33. E. L. Kwak, R. Sordella, D. W. Bell et al., “Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 21, pp. 7665–7670, 2005. View at Publisher · View at Google Scholar
  34. T. Mitsudomi, S. Morita, Y. Yatabe et al., “Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial,” The Lancet Oncology, vol. 11, no. 2, pp. 121–128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Maemondo, A. Inoue, K. Kobayashi et al., “Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR,” The New England Journal of Medicine, vol. 362, no. 25, pp. 2380–2388, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Zhou, Y. L. Wu, G. Chen et al., “Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study,” The Lancet Oncology, vol. 12, no. 8, pp. 735–742, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Rosell, E. Carcereny, R. Gervais et al., “Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial,” The Lancet Oncology, vol. 13, no. 3, pp. 239–246, 2012. View at Publisher · View at Google Scholar
  38. S. Yano, T. Yamada, S. Takeuchi et al., “Hepatocyte growth factor expression in EGFR mutant lung cancer with intrinsic and acquired resistance to tyrosine kinase inhibitors in a japanese cohort,” Journal of Thoracic Oncology, vol. 6, no. 12, pp. 2011–2017, 2011. View at Publisher · View at Google Scholar
  39. J. M. Siegfried, L. A. Weissfeld, P. Singh-Kaw, R. J. Weyant, J. R. Testa, and R. J. Landreneau, “Association of immunoreactive hepatocyte growth factor with poor survival in resectable non-small cell lung cancer,” Cancer Research, vol. 57, no. 3, pp. 433–439, 1997. View at Google Scholar · View at Scopus
  40. K. Kasahara, T. Arao, K. Sakai et al., “Impact of serum hepatocyte growth factor on treatment response to epidermal growth factor receptor tyrosine kinase inhibitors in patients with non-small cell lung adenocarcinoma,” Clinical Cancer Research, vol. 16, no. 18, pp. 4616–4624, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Shojaei, J. H. Lee, B. H. Simmons et al., “HGF/c-Met acts as an alternative angiogenic pathway in sunitinib-resistant tumors,” Cancer Research, vol. 70, no. 24, pp. 10090–10100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Yamada, S. Takeuchi, J. Nakade et al., “Paracrine receptor activation by microenvironment triggers bypass survival signals and ALK inhibitor resistance in EML4-ALK lung cancer cells,” Clinical Cancer Research, vol. 18, no. 13, pp. 3592–3602, 2012. View at Publisher · View at Google Scholar
  43. T. R. Wilson, J. Fridlyand, Y. Yan et al., “Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors,” Nature, vol. 487, no. 7408, pp. 505–509, 2012. View at Publisher · View at Google Scholar
  44. R. Straussman, T. Morikawa, K. Shee et al., “Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion,” Nature, vol. 487, no. 7408, pp. 500–504, 2012. View at Publisher · View at Google Scholar
  45. C.-T. Chen, H. Kim, D. Liska, S. Gao, J. G. Christensen, and M. R. Weiser, “MET activation mediates resistance to lapatinib inhibition of HER2-amplified gastric cancer cells,” Molecular Cancer Therapeutics, vol. 11, no. 3, pp. 660–669, 2012. View at Publisher · View at Google Scholar
  46. D. Hanahan and R. A. Weinberg, “Hallmarks of cancer: the next generation,” Cell, vol. 144, no. 5, pp. 646–674, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. Sakuma, Y. Yanmazaki, Y. Nakamura et al., “NF-kB signaling is activated and confers resistance to apoptosis in three-dimensionally cultured EGFR-mutant lung adenocarcinoma cells,” Biochemical and Biophysical Research Communications, vol. 423, no. 4, pp. 667–671, 2012. View at Publisher · View at Google Scholar
  48. B. Shu, W. Duan, J. Yao, J. Huang, Z. Jiang, and L. Zhang, “Caspase 3 is involved in the apoptosis induced by triptolide in HK-2 cells,” Toxicology in Vitro, vol. 23, no. 4, pp. 598–602, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. S. H. Kaufmann, S. Desnoyers, Y. Ottaviano, N. E. Davidson, and G. G. Poirier, “Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis,” Cancer Research, vol. 53, no. 17, pp. 3976–3985, 1993. View at Google Scholar · View at Scopus
  50. G. Kroemer, L. Galluzzi, and C. Brenner, “Mitochondrial membrane permeabilization in cell death,” Physiological Reviews, vol. 87, no. 1, pp. 99–163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. E. Lai, T. Teodoro, and A. Volchuk, “Endoplasmic reticulum stress: signaling the unfolded protein response,” Physiology, vol. 22, no. 3, pp. 193–201, 2007. View at Publisher · View at Google Scholar · View at Scopus