Hypoxia/HIF1 induces lapatinib resistance in ERBB2-positive breast cancer cells via regulation of DUSP2

Oncotarget

Volumn 6, Issue 4, 2015, Pages 1967-1980

  Karakashev, Sergey V ^a   Reginato, Mauricio J ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Breast cancer; DUSP2; ERBB2 HER2; HIF 1; Hypoxia; Lapatinib

Indexed keywords

DUAL SPECIFICITY PHOSPHATASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HYPOXIA INDUCIBLE FACTOR 1; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; TRAMETINIB; DUSP2 PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN KINASE INHIBITOR; PYRIDONE DERIVATIVE; PYRIMIDINONE DERIVATIVE; QUINAZOLINE DERIVATIVE;

APOPTOSIS; ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; CANCER CELL; CANCER INHIBITION; CANCER PROGNOSIS; CANCER RESISTANCE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HYPOXIA; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; BREAST TUMOR; CELL HYPOXIA; CELL LINE; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOBLOTTING; KAPLAN MEIER METHOD; METABOLISM; PATHOLOGY; PROGNOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR CELL LINE;

APOPTOSIS; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; DUAL SPECIFICITY PHOSPHATASE 2; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOBLOTTING; KAPLAN-MEIER ESTIMATE; PROGNOSIS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDONES; PYRIMIDINONES; QUINAZOLINES; RECEPTOR, ERBB-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84923062592     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2806     Document Type: Article

References (44)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013; 63:11-30.
2. Hortobagyi GN, et al. The Global Breast Cancer Burden: Variations in Epidemiology and Survival. Clin Breast Cancer. 2005; 6:391-401.
3. Jemal A, Siegel R, Xu J, Ward E. Cancer Statistics, 2013. CA Cancer J Clin. 2010; 60:277-300.
4. Bonneterre J, Peyrat JP, Re F, Humaine â, Me O, Lambret CO, Ce L. Review ERBB2 Oncogene in Human Breast Cancer and its Clinical Significance. Eur J Cancer. 1998; 34:791-808.
5. Landgraf R. HER2 therapy. HER2 (ERBB2): functional diversity from structurally conserved building blocks. Breast Cancer Res. 2007; 9:202.
6. Geyer CE, et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med. 2006; 355:2733-43.
7. Ryan Q, Ibrahim A, Cohen MH, Johnson J, Ko C, Sridhara R, Justice R, Pazdur R. FDA drug approval summary: lapatinib in combination with capecitabine for previously treated metastatic breast cancer that overexpresses HER-2. Oncologist. 2008; 13:1114-9.
8. Wang Y-C, et al. Different mechanisms for resistance to trastuzumab versus lapatinib in HER2-positive breast cancers-role of estrogen receptor and HER2 reactivation. Breast Cancer Res. 2011; 13:R121.
9. Fink MY, Chipuk JE. Survival of HER2-Positive Breast Cancer Cells: Receptor Signaling to Apoptotic Control Centers. Genes Cancer. 2013; 4:187-95.
10. Ryan HE, Poloni M, Mcnulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS. Hypoxia-inducible Factor-1a Is a Positive Factor in Solid Tumor Growth. Cancer Res. 2000; 60:4010-4015.
11. Tyers M, Rottapel R. VHL: a very hip ligase. Proc Natl Acad SciUSA. 1999; 96:12230-2.
12. Schwab LP, Peacock DL, Majumdar D, Ingels JF, Jensen LC, Smith KD, Cushing RC, Seagroves TN. Hypoxia-inducible factor 1a promotes primary tumor growth and tumor-initiating cell activity in breast cancer. Breast Cancer Res. 2012; 14:R6.
13. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene. 2010; 29:625-34.
14. Kim J, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 2006; 3:177-85.
15. Forsythe JOA, Jiang B, Iyer NV, Agani F, Leung SW. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996; 16:4604-13.
16. Flamant L, Notte A, Ninane N, Raes M, Michiels C. Anti-apoptotic role of HIF-1 and AP-1 in paclitaxel exposed breast cancer cells under hypoxia. Mol Cancer. 2010; 9:191.
17. Selvendiran K, Bratasz A, Kuppusamy ML, Tazi MF, Rivera BK, Kuppusamy P. Hypoxia induces chemoresistance in ovarian cancer cells by activation of signal transducer and activator of transcription 3. Int J Cancer. 2009; 125:2198-204.
18. Liang S, Galluzzo P, Sobol A, Skucha S, Rambo B, Bocchetta M. Multimodality Approaches to Treat Hypoxic Non-Small Cell Lung Cancer (NSCLC) Microenvironment. Genes Cancer. 2012; 3:141-51.
19. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science. 1989; 244:707-12.
20. Whelan KA, Caldwell SA, Shahriari KS, Jackson SR, Franchetti LD, Johannes GJ, Reginato MJ. Hypoxia Suppression of Bim and Bmf Blocks Anoikis and Luminal Clearing during Mammary Morphogenesis. Mol Biol Cell. 2010; 21:3829-37.
21. Whelan KA, Schwab LP, Karakashev SV, Franchetti L, Johannes GJ, Seagroves TN, Reginato MJ. The oncogene HER2/neu (ERBB2) requires the hypoxia-inducible factor HIF-1 for mammary tumor growth and anoikis resistance. J Biol Chem. 2013; 288:15865-77.
22. Sullivan R, Paré GC, Frederiksen LJ, Semenza GL, Graham CH. Hypoxia-induced resistance to anticancer drugs is associated with decreased senescence and requires hypoxia-inducible factor-1 activity. Mol Cancer Ther. 2008; 7:1961-73.
23. Haenssen KK, Caldwell SA, Shahriari KS, Jackson SR, Whelan KA, Klein-Szanto AJ, Reginato MJ. ErbB2 requires integrin alpha5 for anoikis resistance via Src regulation of receptor activity in human mammary epithelial cells. J Cell Sci. 2010; 123:1373-82.
24. Catzavelos C, et al. Decreased levels of the cell-cycle inhibitor p27Kip1 protein: Prognostic implications in primary breast cancer. Nat Med. 1997; 3:227-30.
25. Tan P, Cady B, Wanner M, Worland P, Cukor B, Magi-galluzzi C, Lavin P, Draetta G, Pagano M, Loda M. The Cell Cycle Inhibitor p27 Is an Independent Prognostic Marker in Small (T 1a, b) Invasive Breast Carcinomas. Advances in Brief Invasive Breast Carcinomas. 1997:1259-63.
26. Faber AC, et al. BIM expression in treatment-naive cancers predicts responsiveness to kinase inhibitors. Cancer Discov. 2011; 1:352-65.
27. Hanna SC, et al. HIF1 α and HIF2 α independently activate SRC to promote melanoma metastases. J Clin Invest. 2013; 123:2078-93.
28. De Luca A, D'Alessio A, Gallo M, Maiello MR, Bode AM, Normanno N. Src and CXCR4 are involved in the invasiveness of breast cancer cells with acquired resistance to lapatinib. Cell Cycle. 2014; 13:148-56.
29. Kim KB, et al. Phase II study of the MEK1/MEK2 inhibitor Trametinib in patients with metastatic BRAF-mutant cutaneous melanoma previously treated with or without a BRAF inhibitor. J Clin Oncol. 2013; 31:482-9.
30. Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, Xavier RJ. An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res. 2009; 37:4587-602.
31. Ward Y, Gupta S, Jensen P, Wartmann M, Davis RJ, Kelly K. Control of MAP kinase activation by the mitogen-induced threonine/tyrosine phosphatase PAC1. Nature. 1994; 367:651-4.
32. Lin S, Chien C, Lee J, Yeh Y, Hsu K, Lai Y, Lin S, Tsai S. Suppression of dual-specificity phosphatase-2 by hypoxia increases chemoresistance and malignancy in human cancer cells. J Clin Invest. 2011; 121:1905-16.
33. Generali D, et al. Hypoxia-inducible factor-1alpha expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res. 2006; 12:4562-8.
34. Györffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22, 277 genes on breast cancer prognosis using microarray data of 1, 809 patients. Breast Cancer Res Treat. 2010; 123:725-31.
35. Rana P, Sridhar SS. Efficacy and tolerability of lapatinib in the management of breast cancer. Breast Cancer (Auckl). 2012; 6:67-77.
36. Rexer BN, Arteaga CL. Intrinsic and Acquired Resistance to HER2-Targeted Therapies in HER2 Gene-Amplified Breast Cancer: Mechanisms and Clinical Implications. Crit Rev Oncog. 2012; 17:1-16.
37. Walsh N, Kennedy S, Larkin A, Corkery B, O'Driscoll L, Clynes M, Crown J, O'Donovan N. EGFR and HER2 inhibition in pancreatic cancer. Invest New Drugs. 2013; 31:558-66.
38. Walters DM, Lindberg JM, Adair SJ, Newhook TE, Cowan CR, Stokes JB, Borgman CA, Stelow EB, Lowrey BT, Chopivsky ME. Inhibition of the Growth of Patient-Derived Pancreatic Cancer Xenografts with the MEK Inhibitor Trametinib Is Augmented by Combined Treatment with the Epidermal Growth Factor Receptor/HER2. Neoplasia. 2013; 15:143-55.
39. Noto A, De Vitis C, Roscilli G, Fattore L, Marra E, Luberto L, Andrilli AD, Giovagnoli MR, Normanno N, Ruco L, Mancini R, Ciliberto G. Combination therapy with anti-ErbB3 monoclonal antibodies and EGFR TKIs potently inhibits Non-small Cell Lung Cancer. Oncotarget. 2013; 4:1253-1265.
40. Dupouy S, Doan VK, Wu Z, Mourra N, Liu J. Activation of EGFR, HER2 and HER3 by neurotensin/neurotensin receptor 1 renders breast tumors aggressive yet highly responsive to lapatinib and metformin in mice. Oncotarget. 2013; 5:8235-8251.
41. Takagi S, Banno H, Hayashi A, Tamura T. HER2 and HER3 cooperatively regulate cancer cell growth and determine sensitivity to the novel investigational EGFR/HER2 kinase inhibitor TAK-285. Oncoscience. 2014; 1:196-204.
42. Muranen T, Selfors LM, Worster DT, Iwanicki MP, Song L, Morales FC, Gao S, Mills GB, Brugge JS. Inhibition of PI3K/mTOR leads to adaptive resistance in matrix-attached cancer cells. Cancer Cell. 2012; 21:227-39.
43. Caldwell SA, Jackson SR, Shahriari KS, Lynch TP, Sethi G, Walker S, Vosseller K, Reginato MJ. Nutrient sensor O-GlcNAc transferase regulates breast cancer tumorigenesis through targeting of the oncogenic transcription factor FoxM1. Oncogene. 2010; 29:2831-42.
44. Tandon P, Gallo CA, Khatri S, Barger JF, Yepiskoposyan H, Plas DR. Requirement for ribosomal protein S6 kinase 1 to mediate glycolysis and apoptosis resistance induced by Pten deficiency. Proc Natl Acad SciUSA. 2011; 108:2361-5.