HER-2/neu overexpression increases the viable hypoxic cell population within solid tumors without causing changes in tumor vascularization

Molecular Cancer Research

Volumn 2, Issue 11, 2004, Pages 606-619

  Dragowska, Wieslawa H ^a   Warburton, Corinna ^a   Yapp, Donald T T ^a,b   Minchinton, Andrew I ^a,b   Hu, Yanping ^c   Waterhouse, Dawn N ^a   Gelmon, Karen ^a   Skov, Kirsten ^a,b   Woo, Janet ^a   Masin, Dana ^a   Huxham, Lynsey A ^a   Kyle, Alastair H ^a   Bally, Marcel B ^a,b  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c Genta Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 NITRO 1H IMIDAZOL 1 YL) N (2,2,3,3,3 PENTAFLUOROPROPYL)ACETAMIDE; ANTIBODY; HOE 33342; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEAR FACTOR KAPPA BETA P65 PROTEIN; PROTEIN; TRYPAN BLUE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER MODEL; CELL FRACTIONATION; CELL POPULATION; CELL SUSPENSION; CELL VIABILITY; CLONOGENIC ASSAY; CONTROLLED STUDY; DNA CONTENT; FEMALE; FLOW CYTOMETRY; GENE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; HYPOXIC CELL; LCC6 HER 2 GENE; LCC6 VECTOR GENE; MICROENVIRONMENT; MOUSE; NONHUMAN; ONCOGENE C ERB; ONCOGENE C ERB B2; ONCOGENE NEU; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SCID MOUSE; SOLID TUMOR; STAINING; TISSUE SECTION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL MARKERS; BREAST NEOPLASMS; CARCINOMA; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL RESPIRATION; CELL SURVIVAL; CLONE CELLS; DRUG RESISTANCE, NEOPLASM; ETANIDAZOLE; FEMALE; GRAFT SURVIVAL; HUMANS; HYDROCARBONS, FLUORINATED; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; NF-KAPPA B; RECEPTOR, ERBB-2; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 9344229790     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Normanno N, Bianco C, De Luca A, Maiello MR, Salomon DS. Target-based agents against ErbB receptors and their ligands: a novel approach to cancer treatment. Endocr Relat Cancer 2003;10:1-21.
2. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177-82.
3. Yu D, Jing T, Liu B, et al. Overexpression of ErbB2 blocks Taxol-induced apoptosis by upregulation of p21Cip1, which inhibits p34Cdc2 kinase. Mol Cell 1998;2:581-91.
4. Knuefermann C, Lu Y, Liu B, et al. HER2/PI-3K/Akt activation leads to a multidrug resistance in human breast adenocarcinoma cells. Oncogene 2003;22:3205-12.
5. Liang K, Lu Y, Jin W, Ang KK, Milas L, Fan Z. Sensitization of breast cancer cells to radiation by trastuzumab. Mol Cancer Ther 2003;2:1113-20.
6. Liu Y, el-Ashry D, Chen D, Ding IY, Kern FG. MCF-7 breast cancer cells overexpressing transfected c-erbB-2 have an in vitro growth advantage in estrogen-depleted conditions and reduced estrogen-dependence and tamoxifen-sensitivity in vivo. Breast Cancer Res Treat 1995;34:97-117.
7. Carlomagno C, Perrone F, Gallo C, et al. c-erbB2 Overexpression decreases the benefit of adjuvant tamoxifen in early-stage breast cancer without axillary lymph node metastases. J Clin Oncol 1996;14:2702-8.
8. Zhou BP, Hu MC, Miller SA, et al. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-κB pathway. J Biol Chem 2000;275:8027-31.
9. Pianetti S, Arsura M, Romieu-Mourez R, Coffey RJ, Sonenshein GE. Her-2/neu overexpression induces NF-κB via a P13-kinase/Akt pathway involving calpain-mediated degradation of 1κB-α that can be inhibited by the tumor suppressor PTEN. Oncogene 2001;20:1287-99.
10. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 2001;21:3995-4004.
11. Janes PW, Daly RJ, deFazio A, Sutherland RL. Activation of the Ras signalling pathway in human breast cancer cells overexpressing erbB-2. Oncogene 1994;9:3601-8.
12. Karni R, Jove R, Levitzki A. Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors. Oncogene 1999;18:4654-62.
13. 1 cell cycle regulators in breast tumour cells. Oncogene 2000;19:1647-56.
14. Petit AM, Rak J, Hung MC, et al. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor ryrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo: angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 1997;151:1523-30.
15. Yen L, Benlimame N, Nie ZR, et al. Differential regulation of tumor angiogenesis by distinct ErbB homo- and heterodimers. Mol Biol Cell 2002;13:4029-44.
16. Nagy P, Jenei A, Damjanovich S, Jovin TM, Szolosi J. Complexity of signal transduction mediated by ErbB2: clues to the potential of receptor-targeted cancer therapy. Pathol Oncol Res 1999;5:255-71.
17. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF III, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci U S A 2003;100:8933-8.
18. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997;16:1647-55.
19. Chen X, Yeung TK, Wang Z. Enhanced drug resistance in cells coexpressing ErbB2 with EGF receptor or ErbB3. Biochem Biophys Res Commun 2000;277:757-63.
20. Brown JM. The hypoxic cell: a target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res 1999;59:5863-70.
21. Williams KJ, Cowen RL, Stratford IJ. Hypoxia and oxidative stress. Tumour hypoxia - therapeutic considerations. Breast Cancer Res 2001;3:328-31.
22. Kurebayashi J, Otsuki T, Moriya T, Sonoo H. Hypoxia reduces hormone responsiveness of human breast cancer cells. Jpn J Cancer Res 2001;92:1093-101.
23. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 2003;29:297-307.
24. Bacus SS, Altomare DA, Lyass L, et al. AKT2 is frequently upregulated in HER-2/neu-positive breast cancers and may contribute to tumor aggressiveness by enhancing cell survival. Oncogene 2002;21:3532-40.
25. Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 2001;93:266-76.
26. Hill RP, De Jaeger K, Jang A, Cairns R. pH, hypoxia and metastasis [discussion 165-8]. Novartis Found Symp 2001;240:154-65.
27. Vaupel P, Kelleher DK, Hockel M. Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 2001;28:29-35.
28. Durand RE. The influence of microenvironmental factors during cancer therapy. In Vivo 1994;8:691-702.
29. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W. IκB kinases phosphorylate NF-κB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 1999;274:30353-6.
30. Warburton C, Dragowska W, Waterhouse D, et al. A Herceptin sensitive model for aggressive breast cancer. Proc AACR 2002;43:88.
31. Evans SM, Joiner B, Jenkins WT, Laughlin KM, Lord EM, Koch CJ. Identification of hypoxia in cells and tissues of epigastric 9L rat glioma using EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl) acetamide]. Br J Cancer 1995;72:875-82.
32. Pegram M, Slamon D. Biological rationale for HER2/neu (c-erbB2) as a target for monoclonal antibody therapy. Semin Oncol 2000;27:13-9.
33. Hortobagyi GN. Overview of treatment results with trastuzumab (Herceptin) in metastatic breast cancer. Semin Oncol 2001;28:43-7.
34. Baselga J. Clinical trials of Herceptin (trastuzumab). Eur J Cancer 2001;37 Suppl 1:18-24.
35. Vogel CL, Cobleigh MA, Tripathy D, 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.
36. Leonessa F, Green D, Licht T, et al. MDA435/LCC6 and MDA435/LCC6MDR1: ascites models of human breast cancer. Br J Cancer 1996;73:154-61.
37. Nieves-Neira W, Pommier Y. Apoptotic response to camptothecin and 7-hydroxystaurosporine (UCN-01) in the 8 human breast cancer cell lines of the NCI Anticancer Drug Screen: multifactorial relationships with topoisomerase I, protein kinase C, Bcl-2, p53, MDM-2 and caspase pathways. Int J Cancer 1999;82:396-404.
38. Sellappan S, Grijalva R, Zhou X, et al. Lineage infidelity of MDA-MB-435 cells: expression of melanocyte proteins in a breast cancer cell line. Cancer Res 2004;64:3479-85.
39. Waterhouse DN, Dragowska WH, Gelmon KA, Mayer LD, Bally MB. Pharmacodynamic behavior of liposomal antisense oligonucleotides targeting Her-2/neu and vascular endothelial growth factor in an ascitic MDA435/LCC6 human breast cancer model. Cancer Biol Ther 2004;3:197-204.
40. Romieu-Mourez R, Landesman-Bollag E, Seldin DC, Sonenshein GE. Protein kinase CK2 promotes aberrant activation of nuclear factor-κB, transformed phenotype, and survival of breast cancer cells. Cancer Res 2002;62:6770-8.
41. Wen Y, Hu MC, Makino K, et al. HER-2/neu promotes androgen-independent survival and growth of prostate cancer cells through the Akt pathway. Cancer Res 2000;60:6841-5.
42. Le NT, Richardson DR. The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim Biophys Acta 2002;1603:31-46.
43. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000;88:1474-80.
44. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000;35:71-103.
45. Warburton C, Dragowska WH, Gelmon K, et al. Treatment of HER-2/neu overexpressing breast cancer xenograft models with trastuzumab (Herceptin) and gefitinib (ZD1839): drug combination effects on tumor growth, HER-2/neu and epidermal growth factor receptor expression, and viable hypoxic cell fraction. Clin Cancer Res 2004;10:2512-24.
46. Bartosova M, Parkkila S, Pohlodek K, et al. Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J Pathol 2002;197:314-21.
47. Blackwell KL, Dewhirst MW, Liotcheva V, et al. HER-2 gene amplification correlates with higher levels of angiogenesis and lower levels of hypoxia in primary breast tumors. Clin Cancer Res 2004;10:4083-8.
48. Lu H, Forbes RA, Verma A. Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 2002;277:23111-5.
49. Metzen E, Zhou J, Jelkmann W, Fandrey J, Brune B. Nitric oxide impairs normoxic degradation of HIF-1α by inhibition of prolyl hydroxylases. Mol Biol Cell 2003;14:3470-81.
50. Schindl M, Schoppmann SF, Samonigg H, et al. Overexpression of hypoxia-inducible factor 1α is associated with an unfavorable prognosis in lymph node-positive breast cancer. Clin Cancer Res 2002;8:1831-7.
51. Bos R, van der Groep P, Greijer AE, et al. Levels of hypoxia-inducible factor-1α independently predict prognosis in patients with lymph node negative breast carcinoma. Cancer 2003;97:1573-81.
52. Lantzsch T, Hefler L, Krause U, et al. The correlation between immunohistochemically-detected markers of angiogenesis and serum vascular endothelial growth factor in patients with breast cancer. Anticancer Res 2002;22:1925-8.
53. Adams J, Carder PJ, Downey S, et al. Vascular endothelial growth factor (VEGF) in breast cancer: comparison of plasma, serum, and tissue VEGF and microvessel density and effects of tamoxifen. Cancer Res 2000;60:2898-905.
54. Callagy G, Dimitriadis E, Harmey J, Bouchier-Hayes D, Leader M, Kay E. Immunohistochemical measurement of tumor vascular endothelial growth factor in breast cancer. A more reliable predictor of tumor stage than microvessel density or serum vascular endothelial growth factor. Appl Immunohistochem Mol Morphol 2000;8:104-9.
55. West CM, Cooper RA, Loncaster JA, Wilks DP, Bromley M. Tumor vascularity: a histological measure of angiogenesis and hypoxia. Cancer Res 2001;61:2907-10.
56. Hlatky L, Hahnfeldt P, Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J Natl Cancer Inst 2002;94:883-93.
57. Delmas C, End D, Rochaix P, Favre G, Toulas C, Cohen-Jonathan E. The farnesyltransferase inhibitor R115777 reduces hypoxia and matrix metalloproteinase 2 expression in human glioma xenograft. Clin Cancer Res 2003;9:6062-8.
58. Dragowska WH, Warburton C, Minchinton A, et al. Gefitinib ("Iressa," ZD1839) reduces tumor hypoxia and blood vessel density in HER-2/neu overexpressing MCF-7 human breast cancer xenografts. Cytometry 2004;59A:1.
59. Sovak MA, Bellas RE, Kim DW, et al. Aberrant nuclear factor-κB/Rel expression and the pathogenesis of breast cancer. J Clin Invest 1997;100:2952-60.
60. Sartor CI. Molecular targets as therapeutic strategies in the management of breast cancer. Semin Radiat Oncol 2002;12:341-51.
61. Karin M, Cao Y, Greten FR, Li ZW. NF-κB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002;2:301-10.
62. Garg AK, Hortobagyi GN, Aggarwal BB, Sahin AA, Buchholz TA. Nuclear factor-κB as a predictor of treatment response in breast cancer. Curr Opin Oncol 2003;15:405-11.
63. Pajonk F, Pajonk K, McBride WH. Inhibition of NF-κB, clonogenicity, and radiosensitivity of human cancer cells. J Natl Cancer Inst 1999;91:1956-60.
64. Evans SM, Koch CJ, Laughlin KM, Jenkins WT, Van Winkle T, Wilson DF. Tamoxifen induces hypoxia in MCF-7 xenografts. Cancer Res 1997;57:5155-61.
65. Yu JL, Rak JW, Coomber BL, Hicklin DJ, Kerbel RS. Effect of p53 status on tumor response to antiangiogenic therapy. Science 2002;295:1526-8.
66. 13C magnetic resonance spectroscopy, Eppendorf electrode, and redox scanning. Cancer Res 2003;63:8813-20.
67. Izumi Y, Xu L, di Tomaso E, Fukumura D, Jain RK. Tumour biology: Herceptin acts as an anti-angiogenic cocktail. Nature 2002;416:279-80.
68. Besch GJ, Wolberg WH, Gilchrist KW, Voelkel JG, Gould MN. A comparison of methods for the production of monodispersed cell suspensions from human primary breast carcinomas. Breast Cancer Res Treat 1983;3:15-22.
69. Novelli M, Savoia P, Cambieri I, et al. Collagenase digestion and mechanical disaggregation as a method to extract and immunophenotype tumour lymphocytes in cutaneous T-cell lymphomas. Clin Exp Dermatol 2000;25:423-31.
70. Dragowska WH, Lopes de Menezes DE, Sartor J, Mayer LD. Quantitative fluorescence cytometric analysis of Bcl-2 levels in tumor cells exhibiting a wide range of inherent Bcl-2 protein expression: correlation with Western blot analysis. Cytometry 2000;40:346-52.
71. Koch CJ, Evans SM, Lord EM. Oxygen dependence of cellular uptake of EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl)acetamide]: analysis of drug adducts by fluorescent antibodies vs bound radioactivity. Br J Cancer 1995;72:869-74.
72. Hansen S, Grabau DA, Sorensen FB, Bak M, Vach W, Rose C. The prognostic value of angiogenesis by Chalkley counting in a confirmatory study design on 836 breast cancer patients. Clin Cancer Res 2000;6:139-46.