Real-time imaging of hypoxia-inducible factor-1 activity in tumor xenografts

Journal of Radiation Research

Volumn 46, Issue 1, 2005, Pages 93-102

  Liu, Junye ^a,b   Qu, Runjiang ^a,b   Ogura, Masakazu ^a   Shibata, Toru ^a   Harada, Hiroshi ^a   Hiraoka, Masahiro ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Destabilized Enhanced GFP (d2EGFP); Hypoxia; Hypoxia inducible factor 1 (HIF 1); Hypoxia response element (HRE); Pimonidazole

Indexed keywords

CELL CULTURE; GENE EXPRESSION; PROTEINS; TUMORS;

DESTABILIZED ENHANCED GFP (D2EGFP); ENHANCED GFP; HYPOXIA; HYPOXIA RESPONSE ELEMENTS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR-1; HYPOXIA-RESPONSE ELEMENT; PIMONIDAZOLE; REALTIME IMAGING; TUMOUR XENOGRAFTS;

FLUORESCENCE;

GREEN FLUORESCENT PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; DNA BINDING PROTEIN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR; TUMOR MARKER;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIAGNOSTIC VALUE; FLUORESCENCE; HUMAN; HUMAN CELL; HYPOXIA; IMAGING SYSTEM; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN DEGRADATION; REOXYGENATION; TUMOR XENOGRAFT; CELL HYPOXIA; COMPUTER SYSTEM; EVALUATION; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; MELANOMA; METABOLISM; METHODOLOGY; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALIA;

CELL HYPOXIA; CELL LINE, TUMOR; COMPUTER SYSTEMS; DNA-BINDING PROTEINS; FLOW CYTOMETRY; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MELANOMA; MICROSCOPY, FLUORESCENCE; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; TRANSPLANTATION, HETEROLOGOUS; TUMOR MARKERS, BIOLOGICAL;

EID: 18044364816     PISSN: 04493060     EISSN: None     Source Type: Journal    
DOI: 10.1269/jrr.46.93     Document Type: Article

References (41)

1. Dang, C.V. and Semenza, G. L. (1999) Oncogenic alterations of metabolism. Trends Biochem. Sci. 24: 68-72.
2. Vaupel, P., Kallinowski, F. and Okunieff, P. (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49: 6449-6465
3. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 16: 4604-4613.
4. Semenza, G. L., Roth, P. H., Fang, H. M. and Wang, G. L. (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269: 23757-23763.
5. Zhong, H., De Marzo, A. M., Laughner, E., Lim, M., Hilton, D. A., Zagzag, D., Buechler, P., Isaacs, W. B., Semenza, G. L. and Simons, J. W. (1999) Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 59: 5830-5835.
6. Kizaka-Kondoh, S., Inoue, M., Harada, H. and Hiraoka, M. (2003) Tumor hypoxia: A target for selective cancer therapy. Cancer Sci. 94, 1021-1028.
7. Brown, J. M. (1999) The hypoxic cell: a target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res. 59: 5863-5870.
8. Moeller, B. J., Cao, Y., Li, C. Y. and Dewhirst, M. W. (2004) Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell. 5: 429-441.
9. Birner, P., Gatterbauer, B., Oberhuber, G., Schindl, M., Rossler, K., Prodinger, A., Budka, H. and Hainfellner, J. A. (2001) Expression of hypoxia-inducible factor-1 alpha in oligodendrogliomas: its impact on prognosis and on neoangiogenesis. Cancer. 92: 165-171.
10. Schindl, M., Schoppmann, S. F., Samonigg, H., Hausmaninger, H., Kwasny, W., Gnant, M., Jakesz, R., Kubista, E., Birner, P. and Oberhuber, G.; Austrian Breast and Colorectal Cancer Study Group. (2002) Overexpression of hypoxia-inducible factor 1alpha is associated with an unfavorable prognosis in lymph node-positive breast cancer. Clin. Cancer Res. 8: 1831-1837.
11. Bos, R., van der Groep, P., Greijer, A. E., Shvarts, A., Meijer, S., Pinedo, H. M., Semenza, G. L., van Diest, P. J. and van der Wall, E. (2003) Levels of hypoxia-inducible factor-1alpha independently predict prognosis in patients with lymph node negative breast carcinoma. Cancer. 97: 1573-1581.
12. Birner, P., Schindl, M., Obermair, A., Plank, C., Breitenecker, G. and Oberhuber, G. (2000) Overexpression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res. 60: 4693-4696.
13. Aebersold, D. M., Burri, P., Beer, K. T., Laissue, J., Djonov, V., Greiner, R. H. and Semenza, G. L. (2001) Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 61: 2911-2916.
14. Birner, P., Schindl, M., Obermair, A., Breitenecker, G. and Oberhuber, G. (2001) Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: its impact on prognosis and on response to chemotherapy. Clin. Cancer Res. 7: 1661-1668.
15. Wang, G. L., Jiang, B. H., Rue, E. A. and Semenza, G. L. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U S A. 92: 5510-5514.
16. Kallio, P. J., Pongratz, I., Gradin, K., McGuire, J. and Poellinger, L. (1997) Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc. Natl. Acad. Sci. U S A. 94: 5667-5672.
17. Jaakkola, P., Mole, D. R., Tian, Y. M., Wilson, M. I., Gielbert, J., Gaskell, S. J., Kriegsheim, A. v., Hebestreit, H. F., Mukherji, M., Schofield, C. J., Maxwell, P. H., Pugh, C. W. and Ratcliffe, P. J. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 292: 468-472.
18. Semenza, G. L. (2001) HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell. 107: 1-3.
19. Wang, G. L. and Semenza, G. L. (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc. Natl. Acad. Sci. U S A. 90: 4304-4308.
20. Norris, M. L. and Millhorn, D. E. (1995) Hypoxia-induced protein binding to O2-responsive sequences on the tyrosine hydroxylase gene. J. Biol. Chem. 270: 23774-23779.
21. Shibata, T., Akiyama, N., Noda, M., Sasai, K. and Hiraoka, M. (1998) Enhancement of gene expression under hypoxic conditions using fragments of the human vascular endothelial growth factor and the erythropoietin genes. Int. J. Radiat. Oncol. Biol. Phys. 42: 913-916.
22. Shibata, T., Giaccia, A. J. and Brown, J. M. (2000) Development of a hypoxia-responsive vector for tumor-specific gene therapy. Gene Ther. 7: 493-498.
23. Aboagye, E. O., Lewis, A. D., Johnson, A., Workman, P., Tracy, M. and Huxham, I. M. (1995) The novel fluorinated 2-nitroimidazole hypoxia probe SR-4554: reductive metabolism and semiquantitative localisation in human ovarian cancer multicellular spheroids as measured by electron energy loss spectroscopic analysis. Br. J. Cancer. 72: 312-318.
24. Seddon, B. M., Payne, G. S., Simmons, L., Ruddle, R., Grimshaw, R., Tan, S., Turner, A., Raynaud, F., Halbert, G., Leach, M. O., Judson, I. and Workman, P. (2003) A phase I study of SR-4554 via intravenous administration for noninvasive investigation of tumor hypoxia by magnetic resonance spectroscopy in patients with malignancy. Clin. Cancer Res. 9: 5101-5112.
25. Koch, C. J and Evans, S. M. (2003) Non-invasive PET and SPECT imaging of tissue hypoxia using isotopically labeled 2-nitroimidazoles. Adv. Exp. Med. Biol. 510: 285-292.
26. Durand, R. E. and Raleigh, J. A. (1998) Identification of non-proliferating but viable hypoxic tumor cells in vivo. Cancer Res. 58: 3547-3550.
27. Nordsmark, M., Loncaster, J., Aquino-Parsons, C., Chou, S. C., Ladekarl, M., Havsteen, H., Lindegaard, J. C., Davidson, S. E., Varia, M., West, C., Hunter, R., Overgaard, J. and Raleigh, J. A. (2003) Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas. Radiother. Oncol. 67: 35-44.
28. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer. 3: 721-32.
29. Laughner, E., Taghavi, P., Chiles, K., Mahon, P. C. and Semenza, G. L. (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21: 3995-4004.
30. Zhong, H., Chiles, K., Feldser, D., Laughner, E., Hanrahan, C., Georgescu, M. M., Simons, J. W. and Semenza, G. L. (2000) Modulation of hypoxia-inducible factor 1 alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 60: 1541-1545.
31. Fukuda, R., Hirota, K., Fan, F., Jung, Y. D., Ellis, L. M. and Semenza, G. L. (2002) Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 277: 38205-38211.
32. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R. and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature. 399: 271-275.
33. Li, X., Zhao, X., Fang, Y., Jiang, X., Duong, T., Fan, C., Huang, C. C. and Kain, S. R. (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J. Biol. Chem. 273: 34970-34975.
34. Oya, N., Zolzer, F., Werner, F. and Streffer, C. (2003) Effects of serum starvation on radiosensitivity, proliferation and apoptosis in four human tumor cell lines with different p53 status. Strahlenther Onkol. 179: 99-106.
35. Harada, H., Hiraoka, M. and Kizaka-Kondoh, S. (2002) Anti-tumor effect of TAT-oxygen-dependent degradation-caspase-3 fusion protein specifically stabilized and activated in hypoxic tumor cells. Cancer Res. 62: 2013-2018.
36. Heim, R., Prasher, D. C. and Tsien RY. (1994) Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. U S A. 91:12501-12504.
37. Serganova, I., Doubrovin, M., Vider, J., Ponomarev, V., Soghomonyan, S., Beresten, T., Ageyeva, L., Serganov, A., Cai, S., Balatoni, J., Blasberg, R. and Gelovani, J. (2004) Molecular imaging of temporal dynamics and spatial heterogeneity of hypoxia-inducible factor-1 signal transduction activity in tumors in living mice. Cancer Res. 64: 6101-6108.
38. Krieg, M., Haas, R., Brauch, H., Acker, T., Flamme, I. and Plate, K. H. (2000) Up-regulation of hypoxia-inducible factors HIF-1 alpha and HIF-2alpha under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function. Oncogene. 19: 5435-5443.
39. Ema, M., Taya, S., Yokotani, N., Sogawa, K., Matsuda, Y. and Fujii-Kuriyama, Y. (1997) A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. U S A. 94: 4273-4278.
40. Yeo, E. J., Chun, Y. S., Cho, Y. S., Kim, J., Lee, J. C., Kim, M. S. and Park, J. W. (2003) YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1. J. Natl. Cancer Inst. 95: 516-525.
41. Inoue, M., Mukai, M., Hamanaka, Y., Tatsuta, M., Hiraoka, M. and Kizaka-Kondoh, S. (2004) Targeting hypoxic cancer cells with a protein prodrug is effective in experimental malignant ascites. Int. J. Oncol. 25: 713-720.