In vivo profiling of hypoxic gene expression in gliomas using the hypoxia marker EF5 and laser-capture microdissection

Cancer Research

Volumn 71, Issue 3, 2011, Pages 779-789

  Marotta, Diane ^a   Karar, Jayashree ^a   Jenkins, W Timothy ^a   Kumanova, Monika ^a   Jenkins, Kevin W ^a   Tobias, John W ^a   Baldwin, Donald ^a   Hatzigeorgiou, Artemis ^b   Alexiou, Panagiotis ^b   Evans, Sydney M ^a   Alarcon, Rodolfo ^c   Maity, Amit ^a   Koch, Cameron ^a   Koumenis, Constantinos ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^c Kinetic Concepts 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; CXCL9 CHEMOKINE; DEOXYRIBONUCLEOPROTEIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLUCOSE TRANSPORTER 1; HEAT SHOCK PROTEIN 27; MESSENGER RNA; PROTEIN CD3D; RAD51 PROTEIN; RNA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION PROFILING; GLIOMA; HYPOXIA; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; LASER CAPTURE MICRODISSECTION; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; RNA ISOLATION; SOLID TUMOR;

ANIMALS; CELL HYPOXIA; ETANIDAZOLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HSP27 HEAT-SHOCK PROTEINS; HYDROCARBONS, FLUORINATED; MALE; MICRODISSECTION; RAD51 RECOMBINASE; RATS; RATS, INBRED F344; RNA, MESSENGER; RNA, NEOPLASM;

EID: 79551542410     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3061     Document Type: Article

References (50)

1. Vaupel P, Mayer A, Hockel M. Tumor hypoxia and malignant progression. Methods Enzymol 2004;381:335-54.
2. Tatum JL, Kelloff GJ, Gillies RJ, et al. Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. Int J Radiat Biol 2006;82:699-757.
3. Graeber TG, Osmanian C, Jacks T, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumors. Nature 1996;379:88-91.
4. Erler JT, Bennewith KL, Nicolau M, et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006;440:1222-6.
5. Subarsky P, Hill RP. The hypoxic tumour microenvironment and metastatic progression. Clin Exp Metastasis 2003;20:237-50.
6. Nelson DA, Tan T-T, Rabson AB, Anderson D, Degenhardt K, White E. Hypoxia and defective apoptosis drive genomic instability and tumorigenesis. Genes Dev 2004;18:2095-107.
7. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000;35:71-103.
8. Koch CJ. Importance of antibody concentration in the assessment of cellular hypoxia by flow cytometry: EF5 and pimonidazole. Radiat Res 2008;169:677-88.
9. Koch CJ. Measurement of absolute oxygen levels in cells and tissues using oxygen sensors and 2-nitroimidazole EF5. Methods Enzymol 2002;352:3-31.
10. Vordermark D, Brown JM. Endogenous markers of tumor hypoxia predictors of clinical radiation resistance?Strahlenther Onkol 2003;179:801-11.
11. van 't Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6.
12. Yu SL, Chen HY, Chang GC, et al. MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell 2008;13:48-57.
13. van't Veer LJ, Bernards R. Enabling personalized cancer medicine through analysis of gene-expression patterns. Nature 2008;452:564-70.
14. Denko NC, Fontana LA, Hudson KM, et al. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 2003;22:5907-14.
15. Weinmann M, Belka C, Guner D, et al. Array-based comparative gene expression analysis of tumor cells with increased apoptosis resistance after hypoxic selection. Oncogene 2005;24:5914-22. (Pubitemid 43080083)
16. Ord JJ, Streeter EH, Roberts IS, Cranston D, Harris AL. Comparison of hypoxia transcriptome in vitro with in vivo gene expression in human bladder cancer. Br J Cancer 2005;93:346-54.
17. Mayer A, Hockel M, Vaupel P. Endogenous hypoxia markers: case not proven!Adv Exp Med Biol 2008;614:127-36.
18. Vordermark D, Brown JM. Evaluation of hypoxia-inducible factor-1alpha (HIF-1alpha) as an intrinsic marker of tumor hypoxia in U87 MG human glioblastoma: in vitro and xenograft studies. Int J Radiat Oncol Biol Phys 2003;56:1184-93.
19. 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.
20. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990;9:811-8.
21. Evans SM, Jenkins WT, Joiner B, Lord EM, Koch CJ. 2-Nitroimidazole (EF5) binding predicts radiation resistance in individual 9L s.c. tumors. Cancer Res 1996;56:405-11.
22. Koch CJ, Shuman AL, Jenkins WT, et al. The radiation response of cells from 9L gliosarcoma tumours is correlated with [F18]-EF5 uptake. Int J Radiat Biol 2009;85:1137-47.
23. 14C-misonidazole to hypoxic cells: kinetic dependence on oxygen concentration and misonidazole concentration. Int J Radiat Oncol Biol Phys 1984;10:1327-31.
24. Koong AC, Denko NC, Hudson KM, et al. Candidate genes for the hypoxic tumor phenotype. Cancer Res 2000;60:883-7.
25. Evans SM, Judy KD, Dunphy I, et al. Hypoxia is important in the biology and aggression of human glial brain tumors. Clin Cancer Res 2004;10:8177-84.
26. Rensink WA, Hazen SP. Statistical issues in microarray data analysis. Methods Mol Biol 2006;323:359-66.
27. Gordan JD, Simon MC. Hypoxia-inducible factors: central regulators of the tumor phenotype. Curr Opin Genet Dev 2007;17:71-7.
28. Allen JW, Johnson RS, Bhatia SN. Hypoxic inhibition of 3-methylcholanthrene- induced CYP1A1 expression is independent of HIF-1alpha. Toxicol Lett 2005;155:151-9.
29. Bruick RK. Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci U S A 2000;97:9082-7.
30. Mazure NM, Pouyssegur J. Hypoxia-induced autophagy: cell death or cell survival?Curr Opin Cell Biol 2010;22:177-80.
31. Whitlock NA, Agarwal N, Ma JX, Crosson CE. Hsp27 upregulation by HIF-1 signaling offers protection against retinal ischemia in rats. Invest Ophthalmol Vis Sci 2005;46:1092-8. (Pubitemid 41321050)
32. Chiral M, Grongnet JF, Plumier JC, David JC. Effects of hypoxia on stress proteins in the piglet brain at birth. Pediatr Res 2004;56:775-82.
33. Hardison JL, Wrightsman RA, Carpenter PM, Lane TE, Manning JE. The chemokines CXCL9 and CXCL10 promote a protective immune response but do not contribute to cardiac inflammation following infection with Trypanosoma cruzi. Infect Immun 2006;74:125-34.
34. Ruehlmann JM, Xiang R, Niethammer AG, et al. MIG (CXCL9) chemokine gene therapy combines with antibody-cytokine fusion protein to suppress growth and dissemination of murine colon carcinoma. Cancer Res 2001;61:8498-503.
35. Bogunovic D, O'Neill DW, Belitskaya-Levy I, et al. Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A 2009;106:20429-34.
36. Bindra RS, Schaffer PJ, Meng A, et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 2004;24:8504-18.
37. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009;10:48.
38. Kato Y, Lambert CA, Colige AC, et al. Acidic extracellular pH induces matrix metalloproteinase-9 expression in mouse metastatic melanoma cells through the phospholipase D-mitogen-activated protein kinase signaling. J Biol Chem 2005;280:10938-44.
39. Chen H, Pan YX, Dudenhausen EE, Kilberg MS. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive basic region/leucine zipper transcription factors as well as localized histone acetylation. J Biol Chem 2004;279:50829-39.
40. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008;13:453-61.
41. Lewis CE, Hughes R. Inflammation and breast cancer. Microenvironmental factors regulating macrophage function in breast tumours: hypoxia and angiopoietin-2. Breast Cancer Res 2007;9:209.
42. Sharma S, Yang SC, Hillinger S, et al. SLC/CCL21-mediated antitumor responses require IFNgamma, MIG/CXCL9 and IP-10/CXCL10. Mol Cancer 2003;2:22.
43. Erreni M, Bianchi P, Laghi L, et al. Expression of chemokines and chemokine receptors in human colon cancer. Methods Enzymol 2009;460:105-21.
44. Doedens AL, Stockmann C, Rubinstein MP, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res 2010;70:7465-75.
45. Khodarev NN, Park JO, Yu J, et al. Dose-dependent and independent temporal patterns of gene responses to ionizing radiation in normal and tumor cells and tumor xenografts. Proc Natl Acad Sci U S A 2001;98:12665-70.
46. Camphausen K, Purow B, Sproull M, et al. Orthotopic growth of human glioma cells quantitatively and qualitatively influences radiation-induced changes in gene expression. Cancer Res 2005;65:10389-93.
47. Le QT, Chen E, Salim A, et al. An evaluation of tumor oxygenation and gene expression in patients with early stage non-small cell lung cancers. Clin Cancer Res 2006;12:1507-14.
48. Gee HE, Camps C, Buffa FM, et al. hsa-mir-210 is a marker of tumor hypoxia and a prognostic factor in head and neck cancer. Cancer 2010;116:2148-58.
49. Giannakakis A, Sandaltzopoulos R, Greshock J, et al. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol Ther 2008;7:255-64.
50. Evans SM, Jenkins KW, Chen HI, et al. The relationship among hypoxia, proliferation, and outcome in patients with de novo glioblastoma: a pilot study. Transl Oncol 2010;3:160-9.