Autophagy protects from trastuzumab-induced cytotoxicity in HER2 overexpressing breast tumor spheroids

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Rodríguez, Cristina E ^a   Reidel, Sara I ^b   De Kier Joffé, Elisa D Bal ^a   Jasnis, Maria A ^a   Fiszman, Gabriel L ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INSTITUTO NACIONAL DE TECNOLOGÍA INDUSTRIAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

TRASTUZUMAB; ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BREAST ADENOCARCINOMA; BREAST TUMOR; CANCER CELL; CANCER RESISTANCE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; GROWTH INHIBITION; HUMAN; HUMAN CELL; PHENOTYPE; PROTEIN LOCALIZATION; TUMOR SPHEROID; CELL CYCLE CHECKPOINT; DOSE RESPONSE; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; GENETICS; METABOLISM; MULTICELLULAR SPHEROID; TUMOR CELL CULTURE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; HUMANS; PHENOTYPE; RECEPTOR, ERBB-2; SPHEROIDS, CELLULAR; TRASTUZUMAB; TUMOR CELLS, CULTURED;

EID: 84945588907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137920     Document Type: Article

References (39)

1. Press MF, Bernstein L, Thomas PA, Meisner LF, Zhou JY, Ma Y, et al. HER-2/neu gene amplification characterized by fluorescence in situ hybridization: poor prognosis in node-negative breast carcinomas. J Clin Oncol. 1997; 15: 2894-904. PMID: 9256133
2. Ghosh R, Narasanna A, Wang SE, Liu S, Chakrabarty A, Balko JM, et al. Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers. Cancer Res. 2011; 71: 1871-82. doi: 10. 1158/0008-5472.CAN-10-1872 PMID: 21324925
3. Junttila TT, Akita RW, Parsons K, Fields C, Lewis Phillips GD, Friedman LS, et al. Ligand-independent HER2/HER3/PI3K complex is disrupted by trastuzumab and is effectively inhibited by the PI3K inhibitor GDC-0941. Cancer Cell. Elsevier Ltd; 2009; 15: 429-40. doi: 10.1016/j.ccr.2009.03.020 PMID: 19411071
4. Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer. J Clin Oncol. 2008; 26: 1789-96. doi: 10.1200/JCO.2007.14. 8957 PMID: 18347005
5. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol. 2002; 20: 719-26. PMID: 11821453
6. Vu T, Claret FX. Trastuzumab: updated mechanisms of action and resistance in breast cancer. Front Oncol. 2012; 2: 62. doi: 10.3389/fonc.2012.00062 PMID: 22720269
7. Fiszman GL, Jasnis MA. Molecular Mechanisms of Trastuzumab Resistance in HER2 Overexpressing Breast Cancer. Int J Breast Cancer. 2011; 2011: 352182. doi: 10.4061/2011/352182 PMID: 22295219
8. Correia AL, Bissell MJ. The tumor microenvironment is a dominant force in multidrug resistance. Drug Resist Updat. Elsevier Ltd; 2012; 15: 39-49. doi: 10.1016/j.drup.2012.01.006 PMID: 22335920
9. Muñoz L, Espinosa M, Quintanar-Jurado V, Hidalgo A, Melendez-Zajgla J, Maldonado V. Paradoxial changes in the expression of estrogen receptor alpha in breast cancer multicellular spheroids. Tissue Cell. 2010; 42: 334-7. doi: 10.1016/j.tice.2010.07.006 PMID: 20817241
10. Trédan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst. 2007; 99: 1441-54. doi: 10.1093/jnci/djm135 PMID: 17895480
11. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000; 290: 1717-21. PMID: 11099404
12. Negri T, Tarantino E. Chromosome band 17q21 in breast cancer: significant association between beclin 1 loss and HER2/NEU amplification. Genes Chromosomes Cancer. 2010; 909: 901-909. doi: 10.1002/gcc
13. Maes H, Rubio N, Garg AD, Agostinis P. Autophagy: shaping the tumor microenvironment and therapeutic response. Trends Mol Med. 2013; 19: 428-46. doi: 10.1016/j.molmed.2013.04.005 PMID: 23714574
14. Del Duca D, Werbowetski T, Del Maestro RF. Spheroid preparation from hanging drops: characterization of a model of brain tumor invasion. J Neurooncol. 2004; 67: 295-303. PMID: 15164985
15. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood. 1994; 84: 1415-20. PMID: 8068938
16. Martin HL, Smith L, Tomlinson DC. Multidrug-resistant breast cancer: current perspectives. Breast cancer (Dove Med Press. 2014; 6: 1-13. doi: 10.2147/BCTT.S37638 PMID: 24648765
17. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 1996; 56: 4509-15. PMID: 8813149
18. Berardi DE, Campodónico PB, Díaz Bessone MI, Urtreger AJ, Todaro LB. Autophagy: friend or foe in breast cancer development, progression, and treatment. Int J Breast Cancer. 2011; 2011: 595092. doi: 10.4061/2011/595092 PMID: 22295229
19. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007; 542-545. PMID: 17611390
20. Esteve JM, Knecht E. Mechanisms of autophagy and apoptosis: Recent developments in breast cancer cells. World J Biol Chem. 2011; 2: 232-8. doi: 10.4331/wjbc.v2.i10.232 PMID: 22031846
21. Pickl M, Ries CH. Comparison of 3D and 2D tumor models reveals enhanced HER2 activation in 3D associated with an increased response to trastuzumab. Oncogene. 2009; 28: 461-8. doi: 10.1038/onc. 2008.394 PMID: 18978815
22. Weigelt B, Lo AT, Park CC, Gray JW, Bissell MJ. HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is dependent strongly on the 3D microenvironment. Breast Cancer Res Treat. 2010; 122: 35-43. doi: 10.1007/s10549-009-0502-2 PMID: 19701706
23. Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer. 2006; 6: 583-92. doi: 10.1038/nrc1893 PMID: 16862189
24. Yakes F, Chinratanalab W, Ritter C. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt Is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res. 2002; 62: 4132-4141. PMID: 12124352
25. Nahta R, Esteva FJ. HER2 therapy: molecular mechanisms of trastuzumab resistance. Breast Cancer Res. 2006; 8: 215. doi: 10.1186/bcr1612 PMID: 17096862
26. Bailey TA, Luan H, Clubb RJ, Naramura M, Band V, Raja SM, et al. Mechanisms of Trastuzumab resistance in ErbB2-driven breast cancer and newer opportunities to overcome therapy resistance. J Carcinog. 2011; 10: 28. doi: 10.4103/1477-3163.90442 PMID: 22190870
27. Moulder S, Yakes F, Muthuswamy S. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res. 2001; 1839: 8887-8895.
28. Ginestier C, Adélaïde J, Gonçalvès a, Repellini L, Sircoulomb F, Letessier a, et al. ERBB2 phosphorylation and trastuzumab sensitivity of breast cancer cell lines. Oncogene. 2007; 26: 7163-9. doi: 10.1038/sj.onc.1210528 PMID: 17525746
29. Harris AL. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer. 2002; 2: 38-47. doi: 10. 1038/nrc704 PMID: 11902584
30. Kute T, Lack CM, Willingham M, Bishwokama B, Williams H, Barrett K, et al. Development of Herceptin resistance in breast cancer cells. Cytometry A. 2004; 57: 86-93. doi: 10.1002/cyto.a.10095 PMID: 14750129
31. Lee S, Yang W, Lan K, Sellappan S. Enhanced sensitization to taxol-induced apoptosis by herceptin pretreatment in ErbB2-overexpressing breast cancer cells. Cancer Res. 2002; 5703-5710. PMID: 12384528
32. Xia W, Gerard CM, Liu L, Baudson NM, Ory TL, Spector NL. Combining lapatinib (GW572016), a small molecule inhibitor of ErbB1 and ErbB2 tyrosine kinases, with therapeutic anti-ErbB2 antibodies enhances apoptosis of ErbB2-overexpressing breast cancer cells. Oncogene. 2005; 24: 6213-21. doi: 10.1038/sj.onc.1208774 PMID: 16091755
33. Liu Q, Shi X, Zhou X, Wang D, Wang L, Li C. Effect of autophagy inhibition on cell viability and cell cycle progression in MDA-MB-231 human breast cancer cells. Mol Med Rep. 2014; 10: 625-30. doi: 10. 3892/mmr.2014.2296 PMID: 24898397
34. Vazquez Martin A. Regulatory gene ATG6/BECN1 in ERBB2-positive breast carcinomas: Bypassing ERBB2-induced oncogenic senescence to regulate the efficacy of ERBB2-targeted therapies. Genes Chromosomes Cancer. 2011; 290: 284-290. doi: 10.1002/gcc
35. Feitelson MA, Arzumanyan A, Kulathinal RJ, Blain SW, Holcombe RF, Mahajna J, et al. Sustained proliferation in cancer: Mechanisms and novel therapeutic targets. Semin Cancer Biol. 2015; doi: 10.1016/j.semcancer.2015.02.006
36. Vazquez-Martin A, Oliveras-Ferraros C, Menendez J a. Autophagy facilitates the development of breast cancer resistance to the anti-HER2 monoclonal antibody trastuzumab. PLoS One. 2009; 4: e6251. doi: 10.1371/journal.pone.0006251 PMID: 19606230
37. Zhu X, Wu L, Qiao H, Han T, Chen S, Liu X, et al. Autophagy stimulates apoptosis in HER2-overexpressing breast cancers treated by lapatinib. J Cell Biochem. 2013; 114: 2643-53. doi: 10.1002/jcb.24611 PMID: 23794518
38. Han J, Hou W, Lu C, Goldstein L a, Stolz DB, Watkins SC, et al. Interaction between Her2 and Beclin-1 proteins underlies a new mechanism of reciprocal regulation. J Biol Chem. 2013; 288: 20315-25. doi: 10.1074/jbc.M113.461350 PMID: 23703612
39. Choi C, Jung Y, Oh S. Autophagy induction by Capsaicin in malignant human breast cells is modulated by p38 and extracellular signal-regulated mitogen-activated protein kinases and retards cell death by suppressing endoplasmic reticulum stress-mediated. Mol Pharmacol. 2010; 1: 114-125. doi: 10.1124/mol.110.063495