Doxorubicin induces cell death in breast cancer cells regardless of Survivin and XIAP expression levels

European Journal of Cell Biology

Volumn 92, Issue 8-9, 2013, Pages 247-256

  Nestal de Moraes, Gabriela ^a   Vasconcelos, Flavia C ^a   Delbue, Deborah ^a   Mognol, Giuliana P ^a   Sternberg, Cinthya ^a   Viola, João P B ^a   Maia, Raquel C ^a  

^a INSTITUTO NACIONAL DE CÂNCER   (Brazil)

Author keywords

Breast cancer; Chemoresistance; Doxorubicin; Survivin; XIAP

Indexed keywords

BIOLOGICAL MARKER; DOXORUBICIN; MESSENGER RNA; PACLITAXEL; PROTEIN; SURVIVIN; TAMOXIFEN; TRASTUZUMAB;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CELL DEATH; CELL VIABILITY; DNA FRAGMENTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BREAST CANCER; CHEMORESISTANCE; DOXORUBICIN; SURVIVIN; XIAP;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BREAST NEOPLASMS; CELL DEATH; CELL SURVIVAL; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MCF-7 CELLS; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53; X-LINKED INHIBITOR OF APOPTOSIS PROTEIN;

EID: 84888438927     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2013.08.001     Document Type: Article

References (52)

1. Aird K.M., Ding X., Baras A., Wei J., Morse M.A., Clay T., Lyerly H.K., Devi G.R. Trastuzumab signaling in ErbB2-overexpressing inflammatory breast cancer correlates with X-linked inhibitor of apoptosis protein expression. Mol. Cancer Ther. 2008, 7:38-47.
2. Ambrosini G., Adida C., Altieri D.C. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat. Med. 1997, 3:917-921.
3. Borresen-Dale A.L. TP53 and breast cancer. Hum. Mutat. 2003, 21:292-300.
4. Burnell M., Levine M.N., Chapman J.A., Bramwell V., Gelmon K., Walley B., Vandenberg T., ChalChal H., Albain K.S., Perez E.A., Rugo H., Pritchard K., O'Brien P., Shepherd L.E. Cyclophosphamide, epirubicin, and fluorouracil versus dose-dense epirubicin and cyclophosphamide followed by paclitaxel versus doxorubicin and cyclophosphamide followed by Paclitaxel in node-positive or high-risk node-negative breast cancer. J. Clin. Oncol. 2010, 28:77-82.
5. Chen Y.Q., Zhao C.L., Li W. Effect of hypoxia-inducible factor-1alpha on transcription of survivin in non-small cell lung cancer. J. Exp. Clin. Cancer Res. 2009, 28:29.
6. Coley H.M. Mechanisms and strategies to overcome chemotherapy resistance in metastatic breast cancer. Cancer Treat. Rev. 2008, 34:378-390.
7. Curtis C., Shah S.P., Chin S.F., Turashvili G., Rueda O.M., Dunning M.J., Speed D., Lynch A.G., Samarajiwa S., Yuan Y., Gräf S., Ha G., Haffari G., Bashashati A., Russell R., McKinney S., Metabric Group, Langerød A., Green A., Provenzano E., Wishart G., Pinder S., Watson P., Markowetz F., Murphy L., Ellis I., Purushotham A., Børresen-Dale A.L., Brenton J.D., Tavaré S., Caldas C., Aparicio S. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352.
8. Dean E., Jodrell D., Connolly K., Danson S., Jolivet J., Durkin J., Morris S., Jowle D., Ward T., Cummings J., Dickinson G., Aarons L., Lacasse E., Robson L., Dive C., Ranson M. Phase I trial of AEG35156 administered as a 7-day and 3-day continuous intravenous infusion in patients with advanced refractory cancer. J. Clin. Oncol. 2009, 27:1660-1666.
9. Dhillon K.K., Swisher E.M., Taniguchi T. Secondary mutations of BRCA1/2 and drug resistance. Cancer Sci. 2011, 102:663-669.
10. Di X., Shiu R.P., Newsham I.F., Gewirtz D.A. Apoptosis, autophagy, accelerated senescence and reactive oxygen in the response of human breast tumor cells to adriamycin. Biochem. Pharmacol. 2009, 77:1139-1150.
11. Dohi T., Okada K., Xia F., Wilford C.E., Samuel T., Welsh K., Marusawa H., Zou H., Armstrong R., Matsuzawa S., Salvesen G.S., Reed J.C., Altieri D.C. An IAP-IAP complex inhibits apoptosis. J. Biol. Chem. 2004, 279:34087-34090.
12. Eckelman B.P., Salvesen G.S., Scott F.L. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 2006, 7:988-994.
13. Fisher B., Brown A.M., Dimitrov N.V., Poisson R., Redmond C., Margolese R.G., Bowman D., Wolmark N., Wickerham D.L., Kardinal C.G., et al. Two months of doxorubicin-cyclophosphamide with and without interval reinduction therapy compared with 6 months of cyclophosphamide, methotrexate, and fluorouracil in positive-node breast cancer patients with tamoxifen-nonresponsive tumors: results from the National Surgical Adjuvant Breast and Bowel Project B-15. J. Clin. Oncol 1990, 8:1483-1490.
14. Flygare J.A., Beresini M., Budha N., Chan H., Chan I.T., Cheeti S., Cohen F., Deshayes K., Doerner K., Eckhardt S.G., Elliott L.O., Feng B., Franklin M.C., Reisner S.F., Gazzard L., Halladay J., Hymowitz S.G., La H., LoRusso P., Maurer B., Murray L., Plise E., Quan C., Stephan J.P., Young S.G., Tom J., Tsui V., Um J., Varfolomeev E., Vucic D., Wagner A.J., Wallweber H.J., Wang L., Ware J., Wen Z., Wong H., Wong J.M., Wong M., Wong S., Yu R., Zobel K., Fairbrother W.J. Discovery of a potent small-molecule antagonist of inhibitor of apoptosis (IAP) proteins and clinical candidate for the treatment of cancer (GDC-0152). J. Med. Chem. 2012, 55:4101-4113.
15. Foster F.M., Owens T.W., Tanianis-Hughes J., Clarke R.B., Brennan K., Bundred N.J., Streuli C.H. Targeting inhibitor of apoptosis proteins in combination with ErbB antagonists in breast cancer. Breast Cancer Res. 2009, 11:R41.
16. Galban S., Duckett C.S. XIAP as a ubiquitin ligase in cellular signaling. Cell Death Differ. 2010, 17:54-60.
17. Gewirtz D.A. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 1999, 57:727-741.
18. Gewirtz D.A., Sundaram S., Magnet K.J. Influence of topoisomerase II inhibitors and ionizing radiation on growth arrest and cell death pathways in the breast tumor cell. Cell Biochem. Biophys. 2000, 33:19-31.
19. Gonzalez-Lopez M., Welsh K., Finlay D., Ardecky R.J., Ganji S.R., Su Y., Yuan H., Teriete P., Mace P.D., Riedl S.J., Vuori K., Reed J.C., Cosford N.D. Design, synthesis and evaluation of monovalent Smac mimetics that bind to the BIR2 domain of the anti-apoptotic protein XIAP. Bioorg. Med. Chem. Lett. 2011, 21:4332-4336.
20. Guha M., Altieri D.C. Survivin as a global target of intrinsic tumor suppression networks. Cell Cycle 2009, 8:2708-2710.
21. Henderson I.C., Berry D.A., Demetri G.D., Cirrincione C.T., Goldstein L.J., Martino S., Ingle J.N., Cooper M.R., Hayes D.F., Tkaczuk K.H., Fleming G., Holland J.F., Duggan D.B., Carpenter J.T., Frei E., Schilsky R.L., Wood W.C., Muss H.B., Norton L. Improved outcomes from adding sequential paclitaxel but not from escalating doxorubicin dose in an adjuvant chemotherapy regimen for patients with node-positive primary breast cancer. J. Clin. Oncol. 2003, 21:976-983.
22. Hinnis A.R., Luckett J.C., Walker R.A. Survivin is an independent predictor of short-term survival in poor prognostic breast cancer patients. Br. J. Cancer 2007, 96:639-645.
23. Jaffer S., Orta L., Sunkara S., Sabo E., Burstein D.E. Immunohistochemical detection of antiapoptotic protein X-linked inhibitor of apoptosis in mammary carcinoma. Hum. Pathol. 2007, 38:864-870.
24. Knappskog S., Lonning P.E. P53 and its molecular basis to chemoresistance in breast cancer. Expert Opin. Ther. Targets 2012, 16(Suppl 1):S23-S30.
25. Konecny G.E., Pauletti G., Untch M., Wang H.J., Mobus V., Kuhn W., Thomssen C., Harbeck N., Wang L., Apple S., Jänicke F., Slamon D.J. Association between HER2, TOP2A, and response to anthracycline-based preoperative chemotherapy in high-risk primary breast cancer. Breast Cancer Res. Treat. 2010, 120:481-489.
26. Lavasani M.A., Moinfar F. Molecular classification of breast carcinomas with particular emphasis on "basal-like" carcinoma: a critical review. J. Biophotonics 2012, 5:345-366.
27. Li F., Ambrosini G., Chu E.Y., Plescia J., Tognin S., Marchisio P.C., Altieri D.C. Control of apoptosis and mitotic spindle checkpoint by survivin. Nature 1998, 396:580-584.
28. Li Q.X., Zhao J., Liu J.Y., Jia L.T., Huang H.Y., Xu Y.M., Zhang Y., Zhang R., Wang C.J., Yao L.B., Chen S.Y., Yang A.G. Survivin stable knockdown by siRNA inhibits tumor cell growth and angiogenesis in breast and cervical cancers. Cancer Biol. Ther. 2006, 5:860-866.
29. Lothstein L., Israel M., Sweatman T.W. Anthracycline drug targeting: cytoplasmic versus nuclear-a fork in the road. Drug Resist. Updat. 2001, 4:169-177.
30. Mirza A., McGuirk M., Hockenberry T.N., Wu Q., Ashar H., Black S., Wen S.F., Wang L., Kirschmeier P., Bishop W.R., Nielsen L.L., Pickett C.B., Liu S. Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 2002, 21:2613-2622.
31. Moriai R., Tsuji N., Moriai M., Kobayashi D., Watanabe N. Survivin plays as a resistant factor against tamoxifen-induced apoptosis in human breast cancer cells. Breast Cancer Res. Treat. 2009, 117:261-271.
32. Nassar A., Lawson D., Cotsonis G., Cohen C. Survivin and caspase-3 expression in breast cancer: correlation with prognostic parameters, proliferation, angiogenesis, and outcome. Appl. Immunohistochem. Mol. Morphol. 2008, 16:113-120.
33. Nestal de Moraes G., Carvalho E., Maia R.C., Sternberg C. Immunodetection of caspase-3 by Western blot using glutaraldehyde. Anal. Biochem. 2011, 415:203-205.
34. Papanikolaou V., Iliopoulos D., Dimou I., Dubos S., Kappas C., Kitsiou-Tzeli S., Tsezou A. Survivin regulation by HER2 through NF-kappaB and c-myc in irradiated breast cancer cells. J. Cell. Mol. Med. 2011, 15:1542-1550.
35. Peng X.H., Karna P., Cao Z., Jiang B.H., Zhou M., Yang L. Cross-talk between epidermal growth factor receptor and hypoxia-inducible factor-1alpha signal pathways increases resistance to apoptosis by up-regulating survivin gene expression. J. Biol. Chem. 2006, 281:25903-25914.
36. Ryan B.M., Konecny G.E., Kahlert S., Wang H.J., Untch M., Meng G., Pegram M.D., Podratz K.C., Crown J., Slamon D.J., Duffy M.J. Survivin expression in breast cancer predicts clinical outcome and is associated with HER2, VEGF, urokinase plasminogen activator and PAI-1. Ann. Oncol. 2006, 17:597-604.
37. Sanchez C.G., Ma C.X., Crowder R.J., Guintoli T., Phommaly C., Gao F., Lin L., Ellis M.J. Preclinical modeling of combined phosphatidylinositol-3-kinase inhibition with endocrine therapy for estrogen receptor-positive breast cancer. Breast Cancer Res. 2011, 13:R21.
38. Sanchez-Rovira P., Anton A., Barnadas A., Velasco A., Lomas M., Rodríguez-Pinilla M., Ramírez J.L., Ramírez C., Ríos M.J., Castellá E., García-Andrade C., San Antonio B., Carrasco E., Palacios J.L. Classical markers like ER and ki-67, but also survivin and pERK, could be involved in the pathological response to gemcitabine, adriamycin and paclitaxel (GAT) in locally advanced breast cancer patients: results from the GEICAM/2002-01 phase II study. Clin. Transl. Oncol. 2012, 14:430-436.
39. Seeger J.M., Brinkmann K., Yazdanpanah B., Haubert D., Pongratz C., Coutelle O., Krönke M., Kashkar H. Elevated XIAP expression alone does not confer chemoresistance. Br. J. Cancer 2010, 102:1717-1723.
40. Simi L., Pratesi N., Vignoli M., Sestini R., Cianchi F., Valanzano R., Nobili S., Mini E., Pazzagli M., Orlando C. High-resolution melting analysis for rapid detection of KRAS, BRAF, and PIK3CA gene mutations in colorectal cancer. Am. J. Clin. Pathol. 2008, 130:247-253.
41. Srivastava R.K., Srivastava A.R., Korsmeyer S.J., Nesterova M., Cho-Chung Y.S., Longo D.L. Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 1998, 18:3509-3517.
42. Tamm I., Wang Y., Sausville E., Scudiero D.A., Vigna N., Oltersdorf T., Reed J.C. IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res. 1998, 58:5315-5320.
43. Tanaka T., Yamaguchi J., Shoji K., Nangaku M. Anthracycline inhibits recruitment of hypoxia-inducible transcription factors and suppresses tumor cell migration and cardiac angiogenic response in the host. J. Biol. Chem. 2012, 287:34866-34882.
44. Vayssade M., Haddada H., Faridoni-Laurens L., Tourpin S., Valent A., Bénard J., Ahomadegbe J.C. P73 functionally replaces p53 in Adriamycin-treated, p53-deficient breast cancer cells. Int. J. Cancer 2005, 116:860-869.
45. Wang S., Huang X., Lee C.K., Liu B. Elevated expression of erbB3 confers paclitaxel resistance in erbB2-overexpressing breast cancer cells via upregulation of Survivin. Oncogene 2010, 29:4225-4236.
46. Wind N.S., Holen I. Multidrug resistance in breast cancer: from in vitro models to clinical studies. Int. J. Breast Cancer 2011, 2011:967419.
47. Wong S.W., Tiong K.H., Kong W.Y., Yue Y.C., Chua C.H., Lim J.Y., Lee C.Y., Quah S.I., Fow C., Chung C., So I., Tan B.S., Choo H.L., Rosli R., Cheong S.K., Leong C.O. Rapamycin synergizes cisplatin sensitivity in basal-like breast cancer cells through up-regulation of p73. Breast Cancer Res. Treat. 2011, 128:301-313.
48. Yamanaka K., Nakata M., Kaneko N., Fushiki H., Kita A., Nakahara T., Koutoku H., Sasamata M. YM155, a selective survivin suppressant, inhibits tumor spread and prolongs survival in a spontaneous metastatic model of human triple negative breast cancer. Int. J. Oncol. 2011, 39:569-575.
49. Yeh P.Y., Chuang S.E., Yeh K.H., Song Y.C., Chang L.L., Cheng A.L. Phosphorylation of p53 on Thr55 by ERK2 is necessary for doxorubicin-induced p53 activation and cell death. Oncogene 2004, 23:3580-3588.
50. Zhang M., Yang J., Li F. Transcriptional and post-transcriptional controls of survivin in cancer cells: novel approaches for cancer treatment. J. Exp. Clin. Cancer Res. 2006, 25:391-402.
51. Zhang Y., Zhu J., Tang Y., Li F., Zhou H., Peng B., Zhou C., Fu R. X-linked inhibitor of apoptosis positive nuclear labeling: a new independent prognostic biomarker of breast invasive ductal carcinoma. Diagn. Pathol. 2011, 6:49.
52. Zhu H., Zhang G., Wang Y., Xu N., He S., Zhang W., Chen M., Liu M., Quan L., Bai J., Xu N. Inhibition of ErbB2 by Herceptin reduces survivin expression via the ErbB2-beta-catenin/TCF4-survivin pathway in ErbB2-overexpressed breast cancer cells. Cancer Sci. 2010, 101:1156-1162.