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Journal of Cancer Research and Clinical Oncology

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Open Access 01-01-2014 | Review

Breast cancer adaptive resistance: HER2 and cancer stem cell repopulation in a heterogeneous tumor society

Authors: Nadire Duru, Demet Candas, Guochun Jiang, Jian Jian Li

Published in: Journal of Cancer Research and Clinical Oncology | Issue 1/2014

Abstract

Purpose

The lethal effects of cancer are associated with the enhanced tumor aggressiveness in recurrent and metastatic lesions that show resistant phenotype to anti-cancer therapy, a major barrier to improving overall survival of cancer patients. The presence of heterogeneous populations of cancer cells within a specific tumor including the tumor-initiating cells or so-called cancer stem cells (CSCs) has linked the acquired resistance (AR, or adaptive resistance). Herein, we discuss the CSC-mediated tumor repopulation in AR of breast cancer in this review.

Methods

We emphasize a dynamic feature of gene induction in tumor cells that undergo long-term treatment, and describe a specific HER2-NF-κB-HER2 pro-survival pathway that can be initiated in breast CSCs upon radiation therapy.

Results

Elucidation of HER2-induced pro-survival networks, specifically the force driving tumor repopulation due to radioresistant CSCs during anticancer therapies, will have a significant impact on the generation of new diagnostic and therapeutic targets to control of recurrent and metastatic breast tumors.

Ahmed KM, Cao N, Li JJ (2006) HER-2 and NF-kappaB as the targets for therapy-resistant breast cancer. Anticancer Res 26:4235–4243PubMedCentralPubMed

Ahmed KM, Li JJ (2007) ATM-NF-kappaB connection as a target for tumor radiosensitization. Curr Cancer Drug Targets 7:335–342PubMed

Ahmed KM, Li JJ (2008) NF-kappa B-mediated adaptive resistance to ionizing radiation. Free Radic Biol Med 44:1–13PubMedCentralPubMed

Ahmed KM, Nantajit D, Fan M, Murley JS, Grdina DJ, Li JJ (2009) Coactivation of ATM/ERK/NF-kappaB in the low-dose radiation-induced radioadaptive response in human skin keratinocytes. Free Radic Biol Med 46:1543–1550PubMed

Al-Hajj M (2007) Cancer stem cells and oncology therapeutics. Curr Opin Oncol 19:61–64PubMed

Al-Hajj M, Becker MW, Wicha M, Weissman I, Clarke MF (2004) Therapeutic implications of cancer stem cells. Curr Opin Genet Dev 14:43–47PubMed

Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988PubMed

Almasan A (2000) Cellular commitment to radiation-induced apoptosis. Radiat Res 153:347–350PubMed

Arteaga CL, Sliwkowski MX, Osborne CK, Perez EA, Puglisi F, Gianni L (2012) Treatment of HER2-positive breast cancer: current status and future perspectives. Nat Rev Clin Oncol 9:16–32

Asada S, Choi Y, Yamada M, Wang SC, Hung MC, Qin J, Uesugi M (2002) External control of Her2 expression and cancer cell growth by targeting a Ras-linked coactivator. Proc Natl Acad Sci USA 99:12747–12752PubMed

Baldwin AS (1996) The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 14:649–683PubMed

Baldwin AS (2001) Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 107:241–246PubMedCentralPubMed

Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006a) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMed

Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD, Rich JN (2006b) Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res 66:7843–7848PubMed

Barkett M, Gilmore TD (1999) Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 18:6910–6924PubMed

Baumann M, Krause M, Hill R (2008) Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8:545–554PubMed

Bebien M, Salinas S, Becamel C, Richard V, Linares L, Hipskind RA (2003) Immediate-early gene induction by the stresses anisomycin and arsenite in human osteosarcoma cells involves MAPK cascade signaling to Elk-1, CREB and SRF. Oncogene 22:1836–1847PubMed

Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3:730–737PubMed

Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K (2012) Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells. Oncogene 31:149–160PubMedCentralPubMed

Brach MA, Hass R, Sherman ML, Gunji H, Weichselbaum R, Kufe D (1991) Ionizing radiation induces expression and binding activity of the nuclear factor kappa B. J Clin Invest 88:691–695PubMedCentralPubMed

Britten CD (2004) Targeting ErbB receptor signaling: a pan-ErbB approach to cancer. Mol Cancer Ther 3:1335–1342PubMed

Cao N, Li S, Wang Z, Ahmed KM, Degnan ME, Fan M, Dynlacht JR, Li JJ (2009) NF-kappaB-mediated HER2 overexpression in radiation-adaptive resistance. Radiat Res 171:9–21PubMedCentralPubMed

Ch’ang HJ, Maj JG, Paris F, Xing HR, Zhang J, Truman JP, Cardon-Cardo C, Haimovitz-Friedman A, Kolesnick R, Fuks Z (2005) ATM regulates target switching to escalating doses of radiation in the intestines. Nat Med 11:484–490PubMed

Chu EC, Tarnawski AS (2004) PTEN regulatory functions in tumor suppression and cell biology. Med Sci Monit 10:RA235–RA241PubMed

Citri A, Yarden Y (2006) EGF–ERBB signalling: towards the systems level. Nat Rev Mol Cell Biol 7:505–516PubMed

Clementz AG, Rogowski A, Pandya K, Miele L, Osipo C (2011) NOTCH-1 and NOTCH-4 are novel gene targets of PEA3 in breast cancer: novel therapeutic implications. Breast Cancer Res 13:R63PubMedCentralPubMed

Curry HA, Clemens RA, Shah S, Bradbury CM, Botero A, Goswami P, Gius D (1999) Heat shock inhibits radiation-induced activation of NF-kappaB via inhibition of I-kappaB kinase. J Biol Chem 274:23061–23067PubMed

Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205–219PubMed

Dewey WC, Ling CC, Meyn RE (1995) Radiation-induced apoptosis: relevance to radiotherapy. Int J Radiat Oncol Biol Phys 33:781–796PubMed

Diehn M, Cho RW, Clarke MF (2009) Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol 19:78–86PubMedCentralPubMed

Dolcet X, Llobet D, Pallares J, Matias-Guiu X (2005) NF-kB in development and progression of human cancer. Virchows Arch 446:475–482PubMed

Duru N, Fan M, Candas D, Menaa C, Liu HC, Nantajit D, Wen Y, Xiao K, Eldridge A, Chromy BA et al (2012) HER2-associated radioresistance of breast cancer stem cells isolated from HER2-negative breast cancer cells. Clin Cancer Res 18:6634–6647PubMedCentralPubMed

Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S et al (2008) Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 3:e2428PubMedCentralPubMed

Eccles SA (2001) The role of c-erbB-2/HER2/neu in breast cancer progression and metastasis. J Mammary Gland Biol Neoplasia 6:393–406PubMed

Fassl A, Tagscherer KE, Richter J, Berriel Diaz M, Alcantara Llaguno SR, Campos B, Kopitz J, Herold-Mende C, Herzig S, Schmidt MH et al (2012) Notch1 signaling promotes survival of glioblastoma cells via EGFR-mediated induction of anti-apoptotic Mcl-1. Oncogene 31:4698–4708PubMed

Feinendegen LE (1999) The role of adaptive responses following exposure to ionizing radiation. Hum Exp Toxicol 18:426–432PubMed

Feinendegen LE (2002) Reactive oxygen species in cell responses to toxic agents. Hum Exp Toxicol 21:85–90PubMed

Feng C, Neumeister V, Ma W, Xu J, Lu L, Bordeaux J, Maihle NJ, Rimm DL, Huang Y (2012) Lin28 regulates HER2 and promotes malignancy through multiple mechanisms. Cell Cycle 11:2486–2494PubMed

Fornace AJ, Amundson SA, Bittner M, Myers TG, Meltzer P, Weinsten JN, Trent J (1999) The complexity of radiation stress responses: analysis by informatics and functional genomics approaches. Gene Expr 7:387–400PubMed

Forrester HB, Albright N, Ling CC, Dewey WC (2000) Computerized video time-lapse analysis of apoptosis of REC: myc cells X-irradiated in different phases of the cell cycle. Radiat Res 154:625–639PubMed

Frosina G (2009) DNA repair in normal and cancer stem cells, with special reference to the central nervous system. Curr Med Chem 16:854–866PubMed

Gangopadhyay S, Nandy A, Hor P, Mukhopadhyay A (2013) Breast cancer stem cells: a novel therapeutic target. Clin Breast Cancer 13:7–15PubMed

Gilmore TD (2003) The Re1/NF-kappa B/I kappa B signal transduction pathway and cancer. Cancer Treat Res 115:241–265PubMed

Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S et al (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1:555–567PubMedCentralPubMed

Granville DJ, Carthy CM, Jiang H, Levy JG, McManus BM, Matroule JY, Piette J, Hunt DW (2000) Nuclear factor-kappaB activation by the photochemotherapeutic agent verteporfin. Blood 95:256–262PubMed

Gu Q, Wang D, Wang X, Peng R, Liu J, Jiang T, Wang Z, Wang S, Deng H (2004) Basic fibroblast growth factor inhibits radiation-induced apoptosis of HUVECs. I. The PI3K/AKT pathway and induction of phosphorylation of BAD. Radiat Res 161(6):692–702PubMed

Guo G, Wang T, Gao Q, Tamae D, Wong P, Chen T, Chen WC, Shively JE, Wong JY, Li JJ (2004) Expression of ErbB2 enhances radiation-induced NF-kappaB activation. Oncogene 23:535–545PubMed

Guo G, Yan-Sanders Y, Lyn-Cook BD, Wang T, Tamae D, Ogi J, Khaletskiy A, Li Z, Weydert C, Longmate JA et al (2003) Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol Cell Biol 23:2362–2378PubMedCentralPubMed

Haffty BG, Brown F, Carter D, Flynn S (1996) Evaluation of HER-2 neu oncoprotein expression as a prognostic indicator of local recurrence in conservatively treated breast cancer: a case-control study. Int J Radiat Oncol Biol Phys 35:751–757PubMed

Hambardzumyan D, Squatrito M, Holland EC (2006) Radiation resistance and stem-like cells in brain tumors. Cancer Cell 10(6):454–456PubMed

Hambardzumyan D, Becher OJ, Rosenblum MK, Pandolfi PP, Manova-Todorova K, Holland EC (2008) PI3 K pathway regulates survival of cancer stem cells residing in the perivascular niche following radiation in medulloblastoma in vivo. Genes Dev 22:436–448PubMed

Hartwell LH, Kastan MB (1994) Cell cycle control and cancer. Science 266:1821–1828PubMed

Harvie RM, Davey MW, Davey RA (1997) Increased MRP expression is associated with resistance to radiation, anthracyclines and etoposide in cells treated with fractionated gamma-radiation. Int J Cancer 73:164–167PubMed

Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1:313–323PubMed

Hicks DG, Yoder BJ, Pettay J, Swain E, Tarr S, Hartke M, Skacel M, Crowe JP, Budd GT, Tubbs RR (2005) The incidence of topoisomerase II-alpha genomic alterations in adenocarcinoma of the breast and their relationship to human epidermal growth factor receptor-2 gene amplification: a fluorescence in situ hybridization study. Hum Pathol 36:348–356PubMed

Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, Hynes NE (2003) The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA 100:8933–8938PubMed

Hong Y, Cervantes RB, Tichy E, Tischfield JA, Stambrook PJ (2007) Protecting genomic integrity in somatic cells and embryonic stem cells. Mutat Res 614:48–55PubMed

Hurt EM, Kawasaki BT, Klarmann GJ, Thomas SB, Farrar WL (2008) CD44+ CD24(−) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis. Br J Cancer 98:756–765PubMedCentralPubMed

Johannessen TC, Bjerkvig R, Tysnes BB (2008) DNA repair and cancer stem-like cells—potential partners in glioma drug resistance? Cancer Treat Rev 34:558–567PubMed

Jung M, Dritschilo A (2001) NF-kappa B signaling pathway as a target for human tumor radiosensitization. Semin Radiat Oncol 11:346–351PubMed

Jung M, Zhang Y, Dritschilo A (1997) Expression of a dominant negative I kappa B-alpha modulates hypersensitivity of ataxia telangiectasia fibroblasts to streptonigrin-induced apoptosis. Radiat Oncol Investig 5:265–268PubMed

Jung M, Zhang Y, Lee S, Dritschilo A (1995) Correction of radiation sensitivity in ataxia telangiectasia cells by a truncated I kappa B-alpha. Science 268:1619–1621PubMed

Karin M (2006) NF-kappaB and cancer: mechanisms and targets. Mol Carcinog 45:355–361PubMed

Kataoka Y, Murley JS, Khodarev NN, Weichselbaum RR, Grdina DJ (2002) Activation of the nuclear transcription factor kappaB (NFkappaB) and differential gene expression in U87 glioma cells after exposure to the cytoprotector amifostine. Int J Radiat Oncol Biol Phys 53:180–189PubMed

Kelsey KT, Memisoglu A, Frenkel D, Liber HL (1991) Human lymphocytes exposed to low doses of X-rays are less susceptible to radiation-induced mutagenesis. Mutat Res 263:197–201PubMed

Kim JJ, Tannock IF (2005) Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5:516–525PubMed

Klokov D, Criswell T, Leskov KS, Araki S, Mayo L, Boothman DA (2004) IR-inducible clusterin gene expression: a protein with potential roles in ionizing radiation-induced adaptive responses, genomic instability, and bystander effects. Mutat Res 568:97–9110PubMed

Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, Los M (2008) Cancer stem cell markers in common cancers—therapeutic implications. Trends Mol Med 14:450–460PubMed

Korkaya H, Kim GI, Davis A, Malik F, Henry NL, Ithimakin S, Quraishi AA, Tawakkol N, D’Angelo R, Paulson AK et al (2012) Activation of an IL6 inflammatory loop mediates trastuzumab resistance in HER2+ breast cancer by expanding the cancer stem cell population. Mol Cell 570–584

Korkaya H, Liu S, Wicha MS (2011) Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J Clin Invest 121:3804–3809PubMedCentralPubMed

Korkaya H, Paulson A, Iovino F, Wicha MS (2008) HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 27:6120–6130PubMedCentralPubMed

Korkaya H, Wicha MS (2009) HER-2, notch, and breast cancer stem cells: targeting an axis of evil. Clin Cancer Res 15:1845–1847PubMed

Kucharczak J, Simmons MJ, Fan Y, Gelinas C (2003) To be, or not to be: NF-kappaB is the answer–role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 22:8961–8982PubMed

Kurokawa H, Arteaga CL (2001) Inhibition of erbB receptor (HER) tyrosine kinases as a strategy to abrogate antiestrogen resistance in human breast cancer. Clin Cancer Res 7:4442

Lacroix M (2006) Significance, detection and markers of disseminated breast cancer cells. Endocr Relat Cancer 13:1033–1067PubMed

Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F (2012) Radiation-induced reprogramming of breast cancer cells. Stem Cells 30:833–844PubMedCentralPubMed

Lavon I, Fuchs D, Zrihan D, Efroni G, Zelikovitch B, Fellig Y, Siegal T (2007) Novel mechanism whereby nuclear factor kappaB mediates DNA damage repair through regulation of O(6)-methylguanine-DNA-methyltransferase. Cancer Res 67:8952–8959PubMed

Lenardo MJ, Baltimore D (1989) NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell 58:227–229PubMed

Li L, Neaves WB (2006) Normal stem cells and cancer stem cells: the niche matters. Cancer Res 66:4553–4557PubMed

Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2:725–734PubMed

Li Z, Xia L, Lee ML, Khaletskiy A, Wang J, Wong JYC, Li JJ (2001) Effector genes altered in MCF-7 human breast cancer cells after exposure to fractionated ionizing radiation. Radiat Res 155:543–553PubMed

Li Z, Wang H, Eyler CE, Hjelmeland AB, Rich JN (2009) Turning cancer stem cells inside out: an exploration of glioma stem cell signaling pathways. J Biol Chem 284:16705–16709PubMed

Liang K, Jin W, Knuefermann C, Schmidt M, Mills GB, Ang KK, Milas L, Fan Z (2003a) Targeting the phosphatidylinositol 3-kinase/Akt pathway for enhancing breast cancer cells to radiotherapy. Mol Cancer Ther 2:353–360PubMed

Liang K, Lu Y, Jin W, Ang KK, Milas L, Fan Z (2003b) Sensitization of breast cancer cells to radiation by trastuzumab. Mol Cancer Ther 2:1113–1120PubMed

Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS (2006) Analysis of gene expression and chemoresistance of CD133 + cancer stem cells in glioblastoma. Mol Cancer 5:67PubMedCentralPubMed

Liu S, Wicha MS (2010) Targeting breast cancer stem cells. J Clin Oncol 28:4006–4012PubMed

Locke JE, Bradbury CM, Wei SJ, Shah S, Rene LM, Clemens RA, Roti Roti J, Horikoshi N, Gius D (2002) Indomethacin lowers the threshold thermal exposure for hyperthermic radiosensitization and heat-shock inhibition of ionizing radiation-induced activation of NF-kappaB. Int J Radiat Biol 78:493–502PubMed

Luo J-L, Kamata H, Karin M (2005) IKK/NF-kappaB signaling: balancing life and death–a new approach to cancer therapy. J Clin Invest 115:2625–2632PubMedCentralPubMed

Maity A, Kao GD, Muschel RJ, McKenna WG (1997) Potential molecular targets for manipulating the radiation response. Int J Radiat Oncol Biol Phys 37:639–653PubMed

Malik F, Korkaya H, Clouthier SG, Wicha MS (2012) Lin28 and HER2: two stem cell regulators conspire to drive aggressive breast cancer. Cell Cycle 11:2780–2781PubMed

Margison GP, Povey AC, Kaina B, Santibanez Koref MF (2003) Variability and regulation of O6-alkylguanine-DNA alkyltransferase. Carcinogenesis 24:625–635PubMed

Mass RD, Press MF, Anderson S, Cobleigh MA, Vogel CL, Dybdal N, Leiberman G, Slamon DJ (2005) Evaluation of clinical outcomes according to HER2 detection by fluorescence in situ hybridization in women with metastatic breast cancer treated with trastuzumab. Clin Breast Cancer 6:240–246PubMed

McBride WH, Pajonk F, Chiang C-S, Sun J-R (2002) NF-kappa B, cytokines, proteasomes, and low-dose radiation exposure. Mil Med 167:66–67PubMed

McDermott SP, Wicha MS (2010) Targeting breast cancer stem cells. Mol Oncol 4:404–419PubMedCentralPubMed

Morgan WF (2003) Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene 22:7094–7099PubMed

Morgan WF, Murnane JP (1995) A role for genomic instability in cellular radioresistance? Cancer Metastasis Rev 14:49–58PubMed

O’Brien KM, Cole SR, Tse CK, Perou CM, Carey LA, Foulkes WD, Dressler LG, Geradts J, Millikan RC (2010) Intrinsic breast tumor subtypes, race, and long-term survival in the Carolina Breast Cancer Study. Clin Cancer Res 16:6100–6110PubMedCentralPubMed

Odoux C, Fohrer H, Hoppo T, Guzik L, Stolz DB, Lewis DW, Gollin SM, Gamblin TC, Geller DA, Lagasse E (2008) A stochastic model for cancer stem cell origin in metastatic colon cancer. Cancer Res 68:6932–6941PubMedCentralPubMed

Olayioye MA (2001) Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members. Breast Cancer Res 3:385–389PubMedCentralPubMed

Olivieri G, Bodycote J, Wolff S (1984) Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science 223:594–597PubMed

Pahl HL (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853–6866PubMed

Pardal R, Clarke MF, Morrison SJ (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3:895–902PubMed

Patrawala L, Calhoun T, Schneider-Broussard R, Li H, Bhatia B, Tang S, Reilly JG, Chandra D, Zhou J, Claypool K et al (2006) Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25:1696–1708PubMed

Phillips TM, McBride WH, Pajonk F (2006) The response of CD24(−/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98:1777–1785PubMed

Pianetti S, Arsura M, Romieu-Mourez R, Coffey RJ, Sonenshein GE (2001) Her-2/neu overexpression induces NF-kappaB via a PI3-kinase/Akt pathway involving calpain-mediated degradation of IkappaB-alpha that can be inhibited by the tumor suppressor PTEN. Oncogene 20:1287–1299PubMed

Pietras RJ, Poen JC, Gallardo D, Wongvipat PN, Lee HJ, Slamon DJ (1999) Monoclonal antibody to HER-2/neuoreceptor modulates repair of radiation-induced DNA damage and enhances radiosensitivity of human breast cancer cells overexpressing this oncogene. Cancer Res 59:1347–1355PubMed

Press MF, Slamon DJ, Flom KJ, Park J, Zhou JY, Bernstein L (2002) Evaluation of HER-2/neu gene amplification and overexpression: comparison of frequently used assay methods in a molecularly characterized cohort of breast cancer specimens. J Clin Oncol 20:3095–3105PubMed

Prieur-Carrillo G, Chu K, Lindqvist J, Dewey WC (2003) Computerized video time-lapse (CVTL) analysis of the fate of giant cells produced by X-irradiating EJ30 human bladder carcinoma cells. Radiat Res 159:705–712PubMed

Puc J, Keniry M, Li HS, Pandita TK, Choudhury AD, Memeo L, Mansukhani M, Murty VV, Gaciong Z, Meek SE et al (2005) Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 7:193–204PubMed

Ren Z, Schaefer TS (2002) ErbB-2 activates Stat3 alpha in a Src- and JAK2-dependent manner. J Biol Chem 277:38486–38493PubMed

Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111PubMed

Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111–115PubMed

Rich JN (2007) Cancer stem cells in radiation resistance. Cancer Res 67(19):8980–8984PubMed

Robson T, Price ME, Moore ML, Joiner MC, McKelvey-Martin VJ, McKeown SR, Hirst DG (2000) Increased repair and cell survival in cells treated with DIR1 antisense oligonucleotides: implications for induced radioresistance. Int J Radiat Biol 76:617–623PubMed

Romashkova JA, Makarov SS (1999) NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86–90PubMed

Schmidt-Ullrich RK, Dent P, Grant S, Mikkelsen RB, Valerie K (2000) Signal transduction and cellular radiation responses. Radiat Res 153:245–257PubMed

Schmidt-Ullrich RK, Mikkelsen RB, Dent P, Todd DG, Valerie K, Kavanagh BD, Contessa JN, Rorrer WK, Chen PB (1997) Radiation-induced proliferation of the human A431 squamous carcinoma cells is dependent on EGFR tyrosine phosphorylation. Oncogene 15:1191–1197PubMed

Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R, Badve S, and Nakshatri H (2006). CD44+/CD24− breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8:R59

Singh SK, Clarke ID, Hide T, Dirks PB (2004) Cancer stem cells in nervous system tumors. Oncogene 23:7267–7273PubMed

Skov KA (1999) Perspectives on the adaptive response from studies on the response to low radiation doses (or to cisplatin) in mammalian cells. Hum Exp Toxicol 18:447–451PubMed

Skvortsova (2008) Intracellular signaling pathways regulating radioresistance of human prostate carcinoma cells. Proteomics 8:4521–4533PubMed

Skvortsova I, Skvortsov S, Stasyk T, Raju U, Popper BA, Schiestl B, von Guggenberg E, Neher A, Bonn GK, Huber LA, Lukas P (2008) Intracellular signaling pathways regulating radioresistance of human prostate carcinoma cells. Proteomics 8(21):4521–4533PubMed

Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL (1987) Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235:177–182PubMed

Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M et al (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344:783–792PubMed

Soomro S, Shousha S, Taylor P, Shepard HM, Feldmann M (1991) c-erbB-2 expression in different histological types of invasive breast carcinoma. J Clin Pathol 44:211–214PubMed

Spitz DR, Azzam EI, Li JJ, Gius D (2004) Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev 23:311–322PubMed

Stecca C, Gerber GB (1998) Adaptive response to DNA-damaging agents: a review of potential mechanisms. Biochem Pharmacol 55:941–951PubMed

Stockler M, Wilcken NR, Ghersi D, Simes RJ (2000) Systematic reviews of chemotherapy and endocrine therapy in metastatic breast cancer. Cancer Treat Rev 26:151–168PubMed

Suzuki K, Kodama S, Watanabe M (1998) Suppressive effect of low-dose preirradiation on genetic instability induced by X rays in normal human embryonic cells. Radiat Res 150:656–662PubMed

Suzuki K, Kodama S, Watanabe M (2001) Extremely low-dose ionizing radiation causes activation of mitogen-activated protein kinase pathway and enhances proliferation of normal human diploid cells. Cancer Res 61:5396–5401PubMed

Tang G, Minemoto Y, Dibling B, Purcell NH, Li Z, Karin M, Lin A (2001) Inhibition of JNK activation through NF-kappaB target genes. Nature 414:313–317PubMed

Uno M, Otsuki T, Kurebayashi J, Sakaguchi H, Isozaki Y, Ueki A, Yata K, Fujii T, Hiratsuka J, Akisada T et al (2001) Anti-HER2-antibody enhances irradiation-induced growth inhibition in head and neck carcinoma. Int J Cancer 94:474–479PubMed

Valabrega G, Montemurro F, Aglietta M (2007) Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Ann Oncol 18:977–984PubMed

Waldman T, Zhang Y, Dillehay L, Yu J, Kinzler K, Vogelstein B, Williams J (1997) Cell-cycle arrest versus cell death in cancer therapy. Nat Med 3:1034–1036PubMed

Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, Sullenger BA (2010) Notch promotes radioresistance of glioma stem cells. Stem Cells 28:17–28PubMedCentralPubMed

Warren CM, Landgraf R (2006) Signaling through ERBB receptors: multiple layers of diversity and control. Cell Signal 18:923–933PubMed

Weichselbaum RR, Hallahan D, Fuks Z, Kufe D (1994) Radiation induction of immediate early genes: effectors of the radiation-stress response. Int J Radiat Oncol Biol Phys 30:229–234PubMed

Wolff S (1989) Are radiation-induced effects hormetic? Science 245:575PubMed

Wolff S (1998) The adaptive response in radiobiology: evolving insights and implications. Environ Health Perspect 106(Suppl 1):277–283PubMedCentralPubMed

Yang HY, Zhou BP, Hung MC, Lee MH (2000) Oncogenic signals of HER-2/neu in regulating the stability of the cyclin-dependent kinase inhibitor p27. J Biol Chem 275:24735–24739PubMed

Zardawi SJ, Zardawi I, McNeil CM, Millar EK, McLeod D, Morey AL, Crea P, Murphy NC, Pinese M, Lopez-Knowles E et al (2010) High Notch1 protein expression is an early event in breast cancer development and is associated with the HER-2 molecular subtype. Histopathology 56:286–296PubMed

Title: Breast cancer adaptive resistance: HER2 and cancer stem cell repopulation in a heterogeneous tumor society
Authors: Nadire Duru
Demet Candas
Guochun Jiang
Jian Jian Li
Publication date: 01-01-2014
Publisher: Springer Berlin Heidelberg
Published in: Journal of Cancer Research and Clinical Oncology / Issue 1/2014
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI: https://doi.org/10.1007/s00432-013-1494-1

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Breast cancer adaptive resistance: HER2 and cancer stem cell repopulation in a heterogeneous tumor society

Abstract

Purpose

Methods

Results

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Abstract

Purpose

Methods

Results

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