Tyrosine kinase inhibitor emodin suppresses growth of HER-2/neu- overexpressing breast cancer cells in athymic mice and sensitizes these cells to the inhibitory effect of paclitaxel

Clinical Cancer Research

Volumn 5, Issue 2, 1999, Pages 343-353

  Zhang, Lisha ^a   Lau, Yiu Keung ^a   Xia, Weiya ^a   Hortobagyi, Gabriel N ^a   Hung, Mien Chie ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EMODIN; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; DRUG SCREENING; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NUDE MOUSE; ONCOGENE NEU; PRIORITY JOURNAL;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL DIVISION; DISEASE MODELS, ANIMAL; DRUG SYNERGISM; EMODIN; ENZYME INHIBITORS; HUMANS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; PACLITAXEL; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RECEPTOR, ERBB-2; TUMOR CELLS, CULTURED; TYROSINE;

EID: 0033049036     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Parker, S. L., Tong, T., Bolden, S., and Wingo, P. A. Cancer statistics, 1997. CA Cancer J. Clin., 47: 5-27, 1997.
2. Slamon, D. J., Clark, G. M., Wong, S. G., Levin, W. J., Ullrich, A., and McGuire, W. L. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science (Washington DC), 235: 177-182, 1987.
3. Slamon, D. J., Godolphin, W., Jones, L. A., Holt, J. A., Wong, S. G., Keith, D. E., Levin, W. J., Stuart, S. G., Udove, J., Ullrich, A., and Press, M. F. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science (Washington DC), 244: 707-712, 1989.
4. Zhang, X., Silva, E., Gershenson, D., and Hung, M. C. Amplification and rearrangement of c-erbB proto-oncogenes in cancer of human female genital tract. Oncogene, 4: 985-989, 1989.
5. Weiner, D. B., Nordberg, J., Robinson, R., Nowell, P. C., Gazdar, A., Greene, M. I., Williams, W. V., Cohen, J. A., and Kern, J. A. Expression of the neu gene-encoded protein (P185neu) in human non-small cell carcinomas of the lung. Cancer Res., 50: 421-425, 1990.
6. Yokota, J., Yamamoto, T., Miyajima, N., Toyoshima, K., Nomura, N., Sakamoto, H., Yoshida, T., Terada, M., and Sugimura, T. Genetic alterations of the c-erbB-2 oncogene occur frequently in tubular adenocarcinoma of the stomach and are often accompanied by amplification of the v-erbA homologue. Oncogene, 2: 283-287, 1988.
7. Zhau, H. E., Zhang, X., von Eschenbach, A. C., Scorsone, K., Babaian, R. J., Ro, J. Y., and Hung, M. C. Amplification and expression of the c-erbB-2/neu proto-oncogene in human bladder cancer. Mol. Carcinog., 3: 254-257, 1990.
8. Hou, L., Shi, D., Tu, S. M., Zhang, H. Z., Hung, M. C., and Ling, D. Oral cancer progression and c-erbB-2/neu proto-oncogene expression. Cancer Lett., 65: 215-220, 1992.
9. Xia, W., Lau, Y-K., Zhang, H-Z., Liu, A-R., Kiyokawa, N., Clayman, G. L., Katz, R. L., and Hung, M-C. Strong correlation between c-erbB-2 overexpression and overall survival of patients with oral squamous cell carcinoma. Clin. Cancer Res., 3: 3-9, 1997.
10. Lacroix, H., Iglehart, J. D., Skinner, M. A., and Kraus, M. H. Overexpression of erbB-2 or EGF receptor proteins present in early stage mammary carcinoma is detected simultaneously in matched primary tumors and regional metastases. Oncogene, 4: 145-151, 1989.
11. Tarakhovsky, A. M., Resnikov, M., Zaichuk, T., Tugusheva, M. V., Butenko, Z. A., and Prassolov, V. S. Polymorphic changes of cell phenotype caused by elevated expression of an exogenous NEU proto-oncogene. Oncogene, 5: 405-410, 1990.
12. Yu, D. H., and Hung, M. C. Expression of activated rat neu oncogene is sufficient to induce experimental metastasis in 3T3 cells. Oncogene, 6: 1991-1996, 1991.
13. Yusa, K., Sugimoto, Y., Yamori, T., Yamamoto, T., Toyoshima, K., and Tsuruo, T. Low metastatic potential of clone from murine colon adenocarcinoma 26 increased by transfection of activated c-erbB-2 gene. J. Natl. Cancer Inst., 82: 1633-1636, 1990.
14. Yu, D., Wang, S. S., Dulski, K. M., Tsai, C. M., Nicolson, G. L., and Hung, M. C. c-erbB-2/neu overexpression enhances metastatic potential of human lung cancer cells by induction of metastasis-associated properties. Cancer Res., 54: 3260-3266, 1994.
15. Benz, C. C., Scott, G. K., Sarup, J. C., Johnson, R. M., Tripathy, D., Coronado, E., Shepard, H. M., and Osborne, C. K. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res. Treat., 24: 85-95, 1993.
16. Yu, D., Liu, B., Tan, M., Li, J., Wang, S. S., and Hung, M. C. Overexpression of c-erbB-2/neu in breast cancer cells confers increased resistance to Taxol via mdr-1-independent mechanisms. Oncogene, 13: 1359-1365, 1996.
17. Holmes, F. A., Walters, R. S., Theriault, R. L., Forman, A. D., Newton, L. K., Raber, M. N., Buzdar, A. U., Frye, D. K., and Hortobagyi, G. N. Phase II trial of taxol, an active drug in the treatment of metastatic breast cancer. J. Natl. Cancer Inst., 83: 1797-1805, 1991.
18. Rowinsky, E. K., and Donehower, R. C. Paclitaxel (taxol). N. Engl. J. Med., 332: 1004-1014, 1995.
19. Holmes, F. A., Kudelka, A. P., Kavanagh, J. J., Huber, M. H., Ajani, J. A., and Valero, V. Taxane Anticancer Agents. Basic Science and Current Status., Vol. 583, pp. 31-57. Washington, DC: American Chemical Society, 1995.
20. Chevallier, B., Fumoleau, P., Kerbrat, P., Dieras, V., Roche. H., Krakowski, I., Azli, N., Bayssas, M., Lentz, M. A., and Van Glabbeke, M. Docetaxel is a major cytotoxic drug for the treatment of advanced breast cancer: a phase II trial of the Clinical Screening Cooperative Group of the European Organization for Research and Treatment of Cancer. J. Clin. Oncol., 13: 314-322, 1995.
21. Jayasuriya, H., Koonchanok, N. M., Geahlen, R. L., McLaughlin, J. L., and Chang, C. J. Emodin, a protein tyrosine kinase inhibitor from Polygonum cuspidatum. J. Nat. Prod., 55: 696-698, 1992.
22. Zhang, L., Chang, C. J., Bacus, S. S., and Hung, M. C. Suppressed transformation and induced differentiation of HER-2/neu-overexpressing breast cancer cells by emodin. Cancer Res., 55: 3890-3896, 1995.
23. Zhang, L., and Hung, M. C. Sensitization of HER-2/neu-overexpressing non-small cell lung cancer cells to chemotherapeutic drugs by tyrosine kinase inhibitor emodin. Oncogene, 12: 571-576, 1996.
24. Miller, S. J., Suen, T. C., Sexton, T. B., and Hung, M. C. HER-2/ neu overexpression counteracts the growth effects of c-myc in breast cancer cells. Int. J. Oncol., 4: 599-608, 1994.
25. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65: 55-63, 1983.
26. Rubinstein, L. V., Shoemaker, R. H., Paull, K. D., Simon, R. M., Tosini, S., Skehan, P., Scudiero, D. A., Monks, A., and Boyd, M. R. Comparison of in vitro anticancer-drug-screening data generated with a tetrazolium assay versus a protein assay against a diverse panel of human tumor cell lines. J. Natl. Cancer Inst., 82: 1113-1118, 1990.
27. Webb, J. L. Enzyme and Metabolic Inhibitors, Vol. 1, pp. 507-510. New York: Academic Press, 1963.
28. Hata, Y., Sandler, A., Loehrer, P. J., Sledge, G. W., Jr., and Weber, G. Synergism of taxol and gallium nitrate in human breast carcinoma cells: schedule dependency. Oncol. Res., 6: 19-24, 1994.
29. Chang, J. Y., Xia, W., Shao, R., Sorgi, F., Hortobagyi, G. N., Huang, L., and Hung, M. C. The tumor suppression activity of E1A in HER-2/neu-overexpressing breast cancer. Oncogene, 14: 561-568, 1997.
30. Hung, M. C., Schechter, A. L., Chevray, P. Y., Stern, D. F., and Weinberg, R. A. Molecular cloning of the neu gene: absence of gross structural alteration in oncogenic alleles. Proc. Natl. Acad. Sci. USA, 83: 261-264, 1986.
31. Hung, M. C., Yan, D. H., and Zhao, X. Y. Amplification of the proto-neu oncogene facilitates oncogenic activation by a single point mutation. Proc. Natl. Acad. Sci. USA, 86: 2545-2548, 1989.
32. Bargmann, C. I., Hung, M. C., and Weinberg, R. A. Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of p185. Cell, 45: 649-657, 1986.
33. Kokai, Y., Myers, J. N., Wada, T., Brown, V. I., LeVea, C. M., Davis, J. G., Dobashi, K., and Greene, M. I. Synergistic interaction of p185c-neu and the EGF receptor leads to transformation of rodent fibroblasts. Cell, 58: 287-292, 1989.
34. Di Fiore, P. P., Pierce, J. H., Kraus, M. H., Segatto, O., King, C. R., and Aaronson, S. A. erbB-2 is a potent oncogene when overexpressed in NIH/3T3 cells. Science (Washington DC), 237: 178-182, 1987.
35. Chazin, V. R., Kaleko, M., Miller, A. D., and Slamon, D. J. Transformation mediated by the human HER-2 gene independent of the epidermal growth factor receptor. Oncogene, 7: 1859-1866, 1992.
36. Samanta, A., LeVea, C. M., Dougall, W. C., Qian, X., and Greene, M. I. Ligand and p185c-neu density govern receptor interactions and tyrosine kinase activation. Proc. Natl. Acad. Sci. USA, 91: 1711-1715, 1994.
37. Drebin, J. A., Link, V. C., Stern, D. F., Weinberg, R. A., and Greene, M. I. Down-modulation of an oncogene protein product and reversion of the transformed phenotype by monoclonal antibodies. Cell, 41: 697-706, 1985.
38. Drebin, J. A., Link, V. C., Weinberg, R. A., and Greene, M. I. Inhibition of tumor growth by a monoclonal antibody reactive with an oncogene-encoded tumor antigen. Proc. Natl. Acad. Sci. USA, 83: 9129-9133, 1986.
39. Drebin, J. A., Link, V. C., and Greene, M. I. Monoclonal antibodies reactive with distinct domains of the neu oncogene-encoded p185 molecule exert synergistic anti-tumor effects in vivo. Oncogene, 2: 273-277, 1988.
40. Drebin, J. A., Link, V. C., and Greene, M. I. Monoclonal antibodies specific for the neu oncogene product directly mediate anti-tumor effects in vivo. Oncogene, 2: 387-394, 1988.
41. Shepard, H. M., Lewis, G. D., Sarup, J. C., Fendly, B. M., Maneval, D., Mordenti, J., Figari, I., Kotts, C. E., Palladino, M. A., Jr., Ullrich, A., et al. Monoclonal antibody therapy of human cancer: taking the HER2 protooncogene to the clinic. J. Clin. Immunol., 11: 117-127, 1991.
42. Hudziak, R. M., Schlessinger, J., and Ullrich, A. Increased expression of the putative growth factor receptor p185HER2 causes transformation and tumorigenesis of NIH 3T3 cells. Proc. Natl. Acad. Sci. USA, 84: 7159-7163, 1987.
43. Hung, M. C., Matin, A., Zhang, Y., Xing, X., Sorgi, F., Huang, L., and Yu, D. HER-2/neu-targeting gene therapy - a review. Gene (Amst.), 159: 65-71, 1995.
44. Yu, D., Matin, A., Xia, W., Sorgi, F., Huang, L., and Hung, M. C. Liposome-mediated in vivo E1A gene transfer suppressed dissemination of ovarian cancer cells that overexpress HER-2/neu. Oncogene, 11: 1383-1388, 1995.
45. Zhang, Y., Yu, D., Xia, W., and Hung, M. C. HER-2/neu-targeting cancer therapy via adenovirus-mediated E1A delivery in an animal model. Oncogene, 10: 1947-1954, 1995.
46. Xing, X., Matin, A., Yu, D., Xia, W., Sorgi, F., Huang, L., and Hung, M. C. Mutant SV40 large T antigen as a therapeutic agent for HER-2/neu-overexpressing ovarian cancer. Cancer Gene Ther., 3: 168-174, 1996.
47. Katsumata, M., Okudaira, T., Samanta, A., Clark, D. P., Drebin, J. A., Jolicoeur, P., and Greene, M. I. Prevention of breast tumour development in vivo by downregulation of the p185neu receptor [see comments]. Nat. Med., 1: 644-648, 1995.
48. Zhang, L., Lau, Y-K., Xi, L., Hong, R-L., Kim, D. S. H. L., Chen, C-F., Hortobagyi, G. N., Chang, C-J., and Hung, M-C. Tyrosine kinase inhibitors, emodin and its derivative repress HER-2/neu-induced cellular transformation and metastasis-associated properties. Oncogene, 16: 2855-2863, 1998.
49. Allred, D. C., Clark, G. M., Tandon, A. K., Molina, R., Tormey, D. C., Osborne, C. K., Gilchrist, K. W., Mansour, E. G., Abeloff, M., Eudey, L., and McGuire, W. L. HER-2/neu in node-negative breast cancer: prognostic significance of overexpression influenced by the presence of in situ carcinoma. J. Clin. Oncol., 10: 599-605, 1992.
50. Harris, J. R., Lippman, M. E., Veronesi, U., and Willett, W. Breast cancer (1). N. Engl. J. Med., 327: 319-328, 1992.
51. Harris, J. R., Lippman, M. E., Veronesi, U., and Willett, W. Breast cancer (2). N. Engl. J. Med., 327: 390-398, 1992.
52. Harris, J. R., Lippman, M. E., Veronesi, U., and Willett, W. Breast cancer (3). N. Engl. J. Med., 327: 473-480, 1992.
53. Gusterson, B. A., Gelber, R. D., Goldhirsch, A., Price, K. N., Save-Soderborgh, J., Anbazhagan, R., Styles, J., Rudenstam, C. M., Golouh, R., Reed, R., Martinez-Tello, F., Tiltman, A., Torhorst, J., Grigolato, P., Bettelheim, R., Neville, A. M., Bürki, K., Castiglione, M., Collins, J., Lindther, J., and Senn, H-J. Prognostic importance of c-erbB-2 expression in breast cancer. International (Ludwig) Breast Cancer Study Group. J. Clin. Oncol., 10: 1049-1056, 1992.
54. Felip, E., Del Campo, J. M., Rubio, D., Vidal, M. T., Colomer, R., and Bermejo, B. Overexpression of c-erbB-2 in epithelial ovarian cancer. Prognostic value and relationship with response to chemotherapy. Cancer (Phila.), 75: 2147-2152, 1995.
55. Colomer, R., Montera, S., Lluch, A., Ojeda, B., Barnadas, A., and Martin, M. Circulating HER-2/neu predicts resistance to Taxo1/Adriamycin in metastatic breast carcinoma: preliminary results of a multicentric prospective study. Proc. Annu. Meet. Am. Soc. Clin. Oncol., 16: A492, 1997.
56. Klijn, J. G., Berns, E. M., and Foekens, J. A. Cancer Surveys, Vol. 18, pp. 165-198. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1993.
57. Berns, E. M., Foekens, J. A., van Staveren, I. L., van Putten, W. L., de Koning, H. Y., Portengen, H., and Klijn, J. G. Oncogene amplification and prognosis in breast cancer: relationship with systemic treatment. Gene (Amst), 159: 11-18, 1995.
58. Baselga, J., Seidman, A. D., Rosen, P. P., and Norton, L. HER2 overexpression and paclitaxel sensitivity in breast cancer: therapeutic implications. Oncology, 11: 43-48, 1997.
59. Gianni, L., Capri, G., Messelani, A., Valagussa, P., Greco, M., Bertuzzi, A., Brasselli, G., Tarenzi, E., Moliterni, A., Pilotti, S., and Bonadonna, G. HER-2/neu amplification and response to doxorubicin/ paclitaxel in women with metastatic breast cancer. Proc. Annu. Meet. Am. Soc. Clin. Oncol., 16: A491, 1997.
60. Thor, A. D., Budman, D. R., Berry, D. A., Muss, H. B., Kute, T., Barcos, M., Cirrincione, C., Edgerton, S., Weiss, R. B., Ferree, C., Allred, C., Wood, W., Frei, E., Henderson, I. C., and Liu, E. T. Selecting patients for higher dose adjuvant CAF: c-erbB-2, p53, dose and dose intensity in stage II node+ breast cancer (CALGB 8869 and 8541). Proc. Annu. Meet. Am. Soc. Clin. Oncol., 16: A452, 1997.
61. Tsai, C. M., Chang, K. T., Perng, R. P., Mitsudomi, T., Chen, M. H., Kadoyama, C., and Gazdar, A. F. Correlation of intrinsic chemoresistance of non-small-cell lung cancer cell lines with HER-2/neu gene expression but not with ras gene mutations. J. Natl. Cancer Inst., 85: 897-901, 1993.
62. Tsai, C. M., Yu, D., Chang, K. T., Wu, L. H., Perng, R. P., Ibrahim, N. K., and Hung, M. C. Enhanced chemoresistance by elevation of p185neu levels in HER-2/neu-transfected human lung cancer cells. J. Natl. Cancer Inst., 87: 682-684, 1995.
63. Tsai, C. M., Chang, K. T., Chen, J. Y., Chen, Y. M., Chen, M. H., and Perng, R. P. Cytotoxic effects of gemcitabine-containing regimens against human non-small cell lung cancer cell lines which express different levels of p185neu. Cancer Res., 56: 794-801, 1996.
64. mdr-1 renders breast cancer cells highly resistant to taxol. Oncogene, 16: 2087-2094, 1998.
65. Pegram, M. D., Finn, R. S., Arzoo, K., Beryt, M., Pietras, R. J., and Slamon, D. J. The effect of HER-2/neu overexpression on chemotherapeutic drug sensitivity in human breast and ovarian cancer cells. Oncogene, 15: 537-547, 1997.
66. Muss, H. B., Thor, A. D., Berry, D. A., Kute, T., Liu, E. T., Koerner, F., Cirrincione, C. T., Budman, D. R., Wood, W. C., Barcos, M., and Henderson, I. C. c-erbB-2 expression and response to adjuvant therapy in women with node-positive early breast cancer [published erratum appears in N. Engl. J. Med., 331: 211, 1994]. N. Engl. J. Med., 330: 1260-1266, 1994.
67. Hancock, M. C., Langton, B. C., Chan, T., Toy, P., Monahan, J. J., Mischak, R. P., and Shawver, L. K. A monoclonal antibody against the c-erbB-2 protein enhances the cytotoxicity of cis-diamminedichloro-platinum against human breast and ovarian tumor cell lines. Cancer Res., 51: 4575-4580, 1991.
68. Arteaga, C. L., Winnier, A. R., Poirier, M. C., Lopez-Larraza, D. M., Shawver, L. K., Hurd, S. D., and Stewart, S. J. p185c-erbB-2 signal enhances cisplatin-induced cytotoxicity in human breast carcinoma cells: association between an oncogenic receptor tyrosine kinase and drug-induced DNA repair. Cancer Res., 54: 3758-3765, 1994.
69. Pietras, R. J., Fendly, B. M., Chazin, V. R., Pegram, M. D., Howell, S. B., and Slamon, D. J. Antibody to HER-2/neu receptor blocks DNA repair after cisplatin in human breast and ovarian cancer cells. Oncogene, 9: 1829-1838, 1994.
70. Baselga, J., Tripathy, D., Mendelsohn, J., Baughman, S., Benz, C. C., Dantis, L., Sklarin, N. T., Seidman, A. D., Hudis, C. A., Moore, J., Rosen, P. P., Twaddell, T., Henderson, I. C., and Norton, L. Phase II study of weekly intravenous recombinant humanized anti-p185HER2 monoclonal antibody in patients with HER2/neu-overexpressing metastatic breast cancer. J. Clin. Oncol., 14: 737-744, 1996.
71. Yen, L., Nie, Z. R., You, X. L., Richard, S., Langton-Webster, B. C., and Alaoui-Jamali, M. A. Regulation of cellular response to cisplatin-induced DNA damage and DNA repair in cells overexpressing p185(erbB-2) is dependent on the ras signaling pathway. Oncogene, 14: 1827-1835, 1997.