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

Evidence-based Complementary and Alternative Medicine

Volumn 2013, Issue , 2013, Pages

  Kang, Xiao Hong ^a   Xu, Zhen Ye ^a   Gong, Ya Bin ^a   Wang, Li Fang ^a   Wang, Zhong Qi ^a,b   Xu, Ling ^a   Cao, Fei ^b   Liao, Ming Juan ^a  

^a SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b Pingdingshan First People's Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BUFALIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; PHOSPHATIDYLINOSITOL 3 KINASE; SCATTER FACTOR; SCATTER FACTOR RECEPTOR;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG STRUCTURE; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; WESTERN BLOTTING;

EID: 84875413419     PISSN: 1741427X     EISSN: 17414288     Source Type: Journal    
DOI: 10.1155/2013/243859     Document Type: Article

References (51)

1. Pao W., Girard N., New driver mutations in non-small-cell lung cancer. The Lancet Oncology 2011 12 2 175 180 2-s2.0-79251490374 10.1016/S1470-2045(10) 70087-5
2. Weinstein I. B., Cancer: addiction to oncogenes-the Achilles heal of cancer. Science 2002 297 5578 63 64 2-s2.0-0037025173 10.1126/science.1073096 (Pubitemid 34743088)
3. Laskin J. J., Sandler A. B., Epidermal growth factor receptor: a promising target in solid tumours. Cancer Treatment Reviews 2004 30 1 1 17 2-s2.0-1242329830 10.1016/j.ctrv.2003.10.002 (Pubitemid 38240085)
4. Suda K., Tomizawa K., Mitsudomi T., Biological and clinical significance of KRAS mutations in lung cancer: an oncogenic driver that contrasts with EGFR mutation. Cancer and Metastasis Reviews 2010 29 1 49 60 2-s2.0-77349091545 10.1007/s10555-010-9209-4
5. Pao W., Chmielecki J., Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer. Nature Reviews Cancer 2010 10 11 760 774 2-s2.0-77958478674 10.1038/nrc2947
6. Jackman D., Pao W., Riely G. J., Engelman J. A., Kris M. G., Jänne P. A., Lynch T., Johnson B. E., Miller V. A., Clinical definition of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. Journal of Clinical Oncology 2010 28 2 357 360 2-s2.0-74949110711 10.1200/JCO.2009.24.7049
7. Kobayashi S., Boggon T. J., Dayaram T., Jänne P. A., Kocher O., Meyerson M., Johnson B. E., Eck M. J., Tenen D. G., Halmos B., EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. The New England Journal of Medicine 2005 352 8 786 792 2-s2.0-13844317894 10.1056/NEJMoa044238 (Pubitemid 40271173)
8. Engelman J. A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Joon O. P., Lindeman N., Gale C. M., Zhao X., Christensen J., Kosaka T., Holmes A. J., Rogers A. M., Cappuzzo F., Mok T., Lee C., Johnson B. E., Cantley L. C., Jänne P. A., MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007 316 5827 1039 1043 2-s2.0-34249075147 10.1126/science.1141478 (Pubitemid 46799492)
9. Yano S., Wang W., Li Q., Matsumoto K., Sakurama H., Nakamura T., Ogino H., Kakiuchi S., Hanibuchi M., Nishioka Y., Uehara H., Mitsudomi T., Yatabe Y., Nakamura T., Sone S., Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Research 2008 68 22 9479 9487 2-s2.0-56449089812 10.1158/0008-5472.CAN- 08-1643
10. Sequist L. V., Waltman B. A., Dias-Santagata D., Digumarthy S., Turke A. B., Fidias P., Bergethon K., Shaw A. T., Gettinger S., Cosper A. K., Akhavanfard S., Heist R. S., Temel J., Christensen J. G., Wain J. C., Lynch T. J., Vernovsky K., Mark E. J., Lanuti M., Iafrate A. J., Mino-Kenudson M., Engelman J. A., Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Science Translational Medicine 2011 3 75 2-s2.0-79953118839 10.1126/scitranslmed.3002003 75ra26
11. Yano S., Wang W., Li Q., Matsumoto K., Sakurama H., Nakamura T., Ogino H., Kakiuchi S., Hanibuchi M., Nishioka Y., Uehara H., Mitsudomi T., Yatabe Y., Nakamura T., Sone S., Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations. Cancer Research 2008 68 22 9479 9487 2-s2.0-56449089812 10.1158/0008-5472.CAN- 08-1643
12. Turke A. B., Zejnullahu K., Wu Y. L., Song Y., Dias-Santagata D., Lifshits E., Toschi L., Rogers A., Mok T., Sequist L., Lindeman N. I., Murphy C., Akhavanfard S., Yeap B. Y., Xiao Y., Capelletti M., Iafrate A. J., Lee C., Christensen J. G., Engelman J. A., Jänne P. A., Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010 17 1 77 88 2-s2.0-73649102105 10.1016/j.ccr.2009.11.022
13. Yamada T., Matsumoto K., Wang W., Li Q., Nishioka Y., Sekido Y., Sone S., Yano S., Hepatocyte growth factor reduces susceptibility to an irreversible epidermal growth factor receptor inhibitor in EGFR-T790M mutant lung cancer. Clinical Cancer Research 2010 16 1 174 183 2-s2.0-74949142595 10.1158/1078-0432.CCR-09-1204
14. Nakagawa T., Takeuchi S., Yamada T., Nanjo S., Ishikawa D., Sano T., Kita K., Nakamura T., Matsumoto K., Suda K., Mitsudomi T., Sekido Y., Uenaka T., Yano S., Combined therapy with mutant-selective EGFR inhibitor and met kinase inhibitor for overcoming erlotinib resistance in EGFR-mutant lung cancer. Molecular Cancer Therapeutics 2012 11 10 2149 2157 10.1158/1535-7163.MCT-12-0195
15. Lu C. X., Nan K. J., Lei Y., Agents from amphibians with anticancer properties. Anti-Cancer Drugs 2008 19 10 931 939 2-s2.0-54249139787 10.1097/CAD.0b013e3283139100
16. Cui X., Inagaki Y., Xu H., Wang D., Qi F., Kokudo N., Fang D., Tang W., Anti-hepatitis B virus activities of cinobufacini and its active components bufalin and cinobufagin in HepG2.2.15 Cells. Biological and Pharmaceutical Bulletin 2010 33 10 1728 1732 2-s2.0-77958001851
17. Qi F., Li A., Inagaki Y., Kokudo N., Tamura S., Nakata M., Tang W., Antitumor activity of extracts and compounds from the skin of the toad Bufo bufo gargarizans Cantor. International Immunopharmacology 2011 11 3 342 349 2-s2.0-79952101058 10.1016/j.intimp.2010.12.007
18. Qi F., Inagaki Y., Gao B., Cui X., Xu H., Kokudo N., Li A., Tang W., Bufalin and cinobufagin induce apoptosis of human hepatocellular carcinoma cells via Fas- and mitochondria-mediated pathways. Cancer Science 2011 102 5 951 958 2-s2.0-79954672344 10.1111/j.1349-7006.2011.01900.x
19. +-ATPase α 3 mediates sensitivity of hepatocellular carcinoma cells to bufalin. Oncology Reports 2011 25 3 825 830 2-s2.0-79551607782 10.3892/or.2010.1120
20. Xie C.-M., Chan W. Y., Yu S., Zhao J., Cheng C. H. K., Bufalin induces autophagy-mediated cell death in human colon cancer cells through reactive oxygen species generation and JNK activation. Free Radical Biology and Medicine 2011 51 7 1365 1375 10.1016/j.freeradbiomed.2011.06.016
21. Amano Y., Cho Y., Matsunawa M., Komiyama K., Makishima M., 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 2009 114 3-5 144 151 2-s2.0-63049110881 10.1016/j.jsbmb.2009.01.022
22. Li D., Qu X., Hou K., Zhang Y., Dong Q., Teng Y., Zhang J., Liu Y., PI3K/Akt is involved in bufalin-induced apoptosis in gastric cancer cells. Anti-Cancer Drugs 2009 20 1 59 64 2-s2.0-57349119864 10.1097/CAD. 0b013e3283160fd6
23. Yu C. H., Kan S. F., Pu H. F., Jea Chien E., Wang P. S., Apoptotic signaling in bufalin- and cinobufagin-treated androgen-dependent and -independent human prostate cancer cells. Cancer Science 2008 99 12 2467 2476 2-s2.0-57349105671 10.1111/j.1349-7006.2008.00966.x
24. Hsiao Y.-P., Yu C.-S., Yu C.-C., Yang J.-S., Chiang J.-H., Lu C.-C., Huang H.-Y., Tang N.-Y., Yang J.-H., Huang A.-C., Chung J.-G., 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 2012 2012 9 591241 10.1155/2012/591241
25. Jiang Y., Zhang Y., Luan J., Duan H., Zhang F., Yagasaki K., Zhang G., Effects of bufalin on the proliferation of human lung cancer cells and its molecular mechanisms of action. Cytotechnology 2010 62 6 573 583 2-s2.0-78651518059 10.1007/s10616-010-9310-0
26. Zhu Z., Sun H., Ma G., Wang Z., Li E., Liu Y., Liu Y., Bufalin induces lung cancer cell apotosis via the inhibition of PI3K/Akt pathway. International Journal of Molecular Sciences 2012 13 2 2025 2035 10.3390/ijms13022025
27. Green L. M., Reade J. L., Ware C. F., Rapid colormetric assay for cell viability: application to the quantitation of cytotoxic and growth inhibitory lymphokines. Journal of Immunological Methods 1984 70 2 257 268 2-s2.0-0021287698 10.1016/0022-1759(84)90190-X (Pubitemid 14111307)
28. Okabe T., Okamoto I., Tamura K., Terashima M., Yoshida T., Satoh T., Takada M., Fukuoka M., Nakagawa K., Differential constitutive activation of the epidermal growth factor receptor in non-small cell lung cancer cells bearing EGFR gene mutation and amplification. Cancer Research 2007 67 5 2046 2053 2-s2.0-33947224133 10.1158/0008-5472.CAN-06-3339 (Pubitemid 46424222)
29. Wang W., Li Q., Yamada T., Matsumoto K., Matsumoto I., Nishioka Y., Sone S., Crosstalk to stromal fibroblasts induces resistance of lung cancer to epidermal growth factor receptor tyrosine kinase inhibitors. Clinical Cancer Research 2009 15 21 6630 6638 10.1158/1078-0432.CCR-09-1001
30. Donev I. S., Wang W., Yamada T., Li Q., Takeuchi S., Matsumoto K., Yamori T., Nishioka Y., Sone S., Yano S., Transient PI3K inhibition induces apoptosis and overcomes HGF-mediated resistance to EGFR-TKIs in EGFR mutant lung cancer. Clinical Cancer Research 2011 17 8 2260 2269 2-s2.0-79954620289 10.1158/1078-0432.CCR-10-1993
31. Wang W., Li Q., Takeuchi S., Yamada T., Koizumi H., Nakamura T., Matsumoto K., Mukaida N., Nishioka Y., Sone S., Nakagawa T., Uenaka T., Yano S., 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 2012 18 6 1663 1671 10.1158/1078-0432.CCR-11- 1171
32. Gusenbauer S., Vlaicu P., Ullrich A., HGF induces novel EGFR functions involve in resistance formation to tyrosine kinase inhibitors. Oncogene 2012 10.1038/onc.2012.396
33. Kwak E. L., Sordella R., Bell D. W., Godin-Heymann N., Okimoto R. A., Brannigan B. W., Harris P. L., Fidias P., Lynch T. J., Rabindran S. K., McGinnis J. P., Wissner A., Sharma S. V., Isselbacher K. J., Settleman J., Haber D. A., 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 2005 102 21 7665 7670 10.1073/pnas.0502860102 (Pubitemid 40741028)
34. Mitsudomi T., Morita S., Yatabe Y., Negoro S., Okamoto I., Tsurutani J., Seto T., Satouchi M., Tada H., Hirashima T., Asami K., Katakami N., Takada M., Yoshioka H., Shibata K., Kudoh S., Shimizu E., Saito H., Toyooka S., Nakagawa K., Fukuoka M., 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 2010 11 2 121 128 2-s2.0-75249087060 10.1016/S1470-2045(09)70364-X
35. Maemondo M., Inoue A., Kobayashi K., Sugawara S., Oizumi S., Isobe H., Gemma A., Harada M., Yoshizawa H., Kinoshita I., Fujita Y., Okinaga S., Hirano H., Yoshimori K., Harada T., Ogura T., Ando M., Miyazawa H., Tanaka T., Saijo Y., Hagiwara K., Morita S., Nukiwa T., Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. The New England Journal of Medicine 2010 362 25 2380 2388 2-s2.0-77953930730 10.1056/NEJMoa0909530
36. Zhou C., Wu Y. L., Chen G., Feng J., Liu X. Q., Wang C., Zhang S., Wang J., Zhou S., Ren S., Lu S., Zhang L., Hu C., Hu C., Luo Y., Chen L., Ye M., Huang J., Zhi X., Zhang Y., Xiu Q., Ma J., Zhang L., You C., 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 2011 12 8 735 742 2-s2.0-79960889662 10.1016/S1470-2045(11)70184-X
37. Rosell R., Carcereny E., Gervais R., Vergnenegre A., Massuti B., Felip E., Palmero R., Garcia-Gomez R., Pallares C., Sanchez J. M., Porta R., Cobo M., Garrido P., Longo F., Moran T., Insa A., De Marinis F., Corre R., Bover I., Illiano A., Dansin E., de Castro J., Milella M., Reguart N., Altavilla G., Jimenez U., Provencio M., Moreno M. A., Terrasa J., Muñoz-Langa J., Valdivia J., Isla D., Domine M., Molinier O., Mazieres J., Baize N., Garcia-Campelo R., Robinet G., Rodriguez-Abreu D., Lopez-Vivanco G., Gebbia V., Ferrera-Delgado L., Bombaron P., Bernabe R., Bearz A., Artal A., Cortesi E., Rolfo C., Sanchez-Ronco M., Drozdowskyj A., Queralt C., de Aguirre I., Ramirez J. L., Sanchez J. J., Molina M. A., Taron M., Paz-Ares L., 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 2012 13 3 239 246 10.1016/S1470-2045(11)70393-X
38. Yano S., Yamada T., Takeuchi S., Tachibana K., Minami Y., Yatabe Y., Mitsudomi T., Tanaka H., Kimura T., Kudoh S., Nokihara H., Ohe Y., Yokota J., Uramoto H., Yasumoto K., Kiura K., Higashiyama M., Oda M., Saito H., Yoshida J., Kondoh K., Noguchi M., 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 2011 6 12 2011 2017 10.1097/JTO.0b013e31823ab0dd
39. Siegfried J. M., Weissfeld L. A., Singh-Kaw P., Weyant R. J., Testa J. R., Landreneau R. J., Association of immunoreactive hepatocyte growth factor with poor survival in resectable non-small cell lung cancer. Cancer Research 1997 57 3 433 439 2-s2.0-0031057905 (Pubitemid 27081660)
40. Kasahara K., Arao T., Sakai K., Matsumoto K., Sakai A., Kimura H., Sone T., Horiike A., Nishio M., Ohira T., Ikeda N., Yamanaka T., Saijo N., Nishio K., 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 2010 16 18 4616 4624 2-s2.0-77956654766 10.1158/1078-0432.CCR-10-0383
41. Shojaei F., Lee J. H., Simmons B. H., Wong A., Esparza C. O., Plumlee P. A., Feng J., Stewart A. E., Hu-Lowe D. D., Christensen J. G., HGF/c-Met acts as an alternative angiogenic pathway in sunitinib-resistant tumors. Cancer Research 2010 70 24 10090 10100 2-s2.0-78650339354 10.1158/0008-5472.CAN-10-0489
42. Yamada T., Takeuchi S., Nakade J., Kita K., Nakagawa T., Nanjo S., Nakamura T., Matsumoto K., Soda M., Mano H., Uenaka T., Yano S., Paracrine receptor activation by microenvironment triggers bypass survival signals and ALK inhibitor resistance in EML4-ALK lung cancer cells. Clinical Cancer Research 2012 18 13 3592 3602 10.1158/1078-0432.CCR-11-2972
43. Wilson T. R., Fridlyand J., Yan Y., Penuel E., Burton L., Chan E., Peng J., Lin E., Wang Y., Sosman J., Ribas A., Li J., Moffat J., Sutherlin D. P., Koeppen H., Merchant M., Neve R., Settleman J., Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012 487 7408 505 509 10.1038/nature11249
44. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z. R., Du J., Davis A., Mongare M. M., Gould J., Frederick D. T., Cooper Z. A., Chapman P. B., Solit D. B., Ribas A., Lo R. S., Flaherty K. T., Ogino S., Wargo J. A., Golub T. R., Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012 487 7408 500 504 10.1038/nature11183
45. Chen C.-T., Kim H., Liska D., Gao S., Christensen J. G., Weiser M. R., MET activation mediates resistance to lapatinib inhibition of HER2-amplified gastric cancer cells. Molecular Cancer Therapeutics 2012 11 3 660 669 10.1158/1535-7163.MCT-11-0754
46. Hanahan D., Weinberg R. A., Hallmarks of cancer: the next generation. Cell 2011 144 5 646 674 2-s2.0-79952284127 10.1016/j.cell.2011.02.013
47. Sakuma Y., Yanmazaki Y., Nakamura Y., Yoshihara M., Matsukuma S., Koizume S., Miyaqi Y., NF-kB signaling is activated and confers resistance to apoptosis in three-dimensionally cultured EGFR-mutant lung adenocarcinoma cells. Biochemical and Biophysical Research Communications 2012 423 4 667 671 10.1016/j.bbrc.2012.06.009
48. Shu B., Duan W., Yao J., Huang J., Jiang Z., Zhang L., Caspase 3 is involved in the apoptosis induced by triptolide in HK-2 cells. Toxicology in Vitro 2009 23 4 598 602 2-s2.0-67349149121 10.1016/j.tiv.2009.01.021
49. Kaufmann S. H., Desnoyers S., Ottaviano Y., Davidson N. E., Poirier G. G., Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Research 1993 53 17 3976 3985 2-s2.0-0027255417 (Pubitemid 23267698)
50. Kroemer G., Galluzzi L., Brenner C., Mitochondrial membrane permeabilization in cell death. Physiological Reviews 2007 87 1 99 163 2-s2.0-33845977959 10.1152/physrev.00013.2006 (Pubitemid 46209992)
51. Lai E., Teodoro T., Volchuk A., Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology 2007 22 3 193 201 2-s2.0-34447527676 10.1152/physiol.00050.2006