Strategies to assess hypoxic/HIF-1-active cancer cells for the development of innovative radiation therapy

Cancers

Volumn 3, Issue 3, 2011, Pages 3610-3631

  Yeom, Chan Joo ^a   Zeng, Lihua ^a,b   Zhu, Yuxi ^a,b   Hiraoka, Masahiro ^b   Harada, Hiroshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Hypoxia inducible factor 1 (HIF 1); Molecular imaging; Radiation therapy; Radioresistance; Tumor hypoxia

Indexed keywords

2 NITROIMIDAZOLE DERIVATIVE; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; OXYGEN; PIMONIDAZOLE; THIOSEMICARBAZONE DERIVATIVE; VASCULOTROPIN;

BOLD SIGNAL; CANCER CELL; CANCER GROWTH; CANCER INVASION; CANCER RADIOTHERAPY; CANCER RESISTANCE; CARCINOGENESIS; CELL HYPOXIA; DNA DAMAGE; ELECTRON SPIN RESONANCE; EPITHELIAL MESENCHYMAL TRANSITION; EXPERIMENTAL THERAPY; FLUORINE NUCLEAR MAGNETIC RESONANCE; HUMAN; IMMUNOHISTOCHEMISTRY; METASTASIS; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POLAROGRAPHY; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; RADIATION DOSE; RADIOSENSITIVITY; REPORTER GENE; REVIEW; SCINTISCANNING; TREATMENT FAILURE; TUMOR XENOGRAFT;

EID: 80053211032     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers3033610     Document Type: Review

References (127)

1. Deschner, E.E.; Gray, L.H. Influence of oxygen tension on x-ray-induced chromosomal damage in Ehrlich ascites tumor cells irradiated in vitro and in vivo. Radiat. Res. 1959, 11, 115-146.
2. Gray, L.H.; Conger, A.D.; Ebert, M.; Hornsey, S.; Scott, O.C. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol. 1953, 26, 638-648.
3. Thomlinson, R.H.; Gray, L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer 1955, 9, 539-549.
4. Vaupel, P.; Kallinowski, F. Okunieff, P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res. 1989, 49, 6449-6465.
5. Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell 2011, 144, 646-674.
6. Jain, R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9, 685-693.
7. Brown, J.M.; Wilson, W.R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 2004, 4, 437-447.
8. Harada, H.; Hiraoka, M. Hypoxia-inducible factor 1 in tumor radioresistance. Curr. Signal Transduct. Ther. 2010, 5, 188-196.
9. Harada, H.; Itasaka, S.; Zhu, Y.; Zeng, L.; Xie, X.; Morinibu, A.; Shinomiya, K.; Hiraoka, M. Treatment regimen determines whether an HIF-1 inhibitor enhances or inhibits the effect of radiation therapy. Br. J. Cancer 2009, 100, 747-757.
10. Moeller, B.J.; Cao, Y.; Li, C.Y.; Dewhirst, M.W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: Role of reoxygenation, free radicals, and stress granules. Cancer Cell 2004, 5, 429-441.
11. Moeller, B.J.; Dewhirst, M.W. Raising the bar: How HIF-1 helps determine tumor radiosensitivity. Cell Cycle 2004, 3, 1107-1110.
12. Moeller, B.J.; Dreher, M.R.; Rabbani, Z.N.; Schroeder, T.; Cao, Y.; Li, C.Y.; Dewhirst, M.W. Pleiotropic effects of HIF-1 blockade on tumor radiosensitivity. Cancer Cell 2005, 8, 99-110.
13. Moeller, B.J.; Richardson, R.A.; Dewhirst, M.W. Hypoxia and radiotherapy: Opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007, 26, 241-248.
14. Zeng, L.; Ou, G.; Itasaka, S.; Harada, H.; Xie, X.; Shibuya, K.; Kizaka-Kondoh, S.; Morinibu, A.; Shinomiya, K.; Hiraoka, M. TS-1 enhances the effect of radiotherapy by suppressing radiation-induced hypoxia-inducible factor-1 activation and inducing endothelial cell apoptosis. Cancer Sci. 2008, 99, 2327-2335.
15. Kizaka-Kondoh, S.; Inoue, M.; Harada, H.; Hiraoka, M. Tumor hypoxia: A target for selective cancer therapy. Cancer Sci. 2003, 94, 1021-1028.
16. Comerford, K.M.; Wallace, T.J.; Karhausen, J.; Louis, N.A.; Montalto, M.C.; Colgan, S.P. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 2002, 62, 3387-3394.
17. Elkind, M.M.; Sutton-Gilbert, H.; Moses, W.B.; Alescio, T.; Swain, R.W. Radiation Response of Mammalian Cells Grown in Culture. V. Temperature Dependence of the Repair of X-Ray Damage in Surviving Cells (Aerobic and Hypoxic). Radiat. Res. 1965, 25, 359-376.
18. Suit, H.D. Application of radiobiologic principles to radiation therapy. Cancer 1968, 22, 809-815.
19. Trott, K.R. Experimental results and clinical implications of the four R's in fractionated radiotherapy. Radiat. Environ. Biophys. 1982, 20, 159-170.
20. Rajendran, J.G.; Hendrickson, K.R.; Spence, A.M.; Muzi, M.; Krohn, K.A.; Mankoff, D.A. Hypoxia imaging-directed radiation treatment planning. Eur. J. Nucl. Med. Mol. Imaging 2006, 33S, 44-53.
21. Yeo, E.J.; Chun, Y.S.; Cho, Y.S.; Kim, J.; Lee, J.C.; Kim, M.S.; Park, J.W. YC-1: A potential anticancer drug targeting hypoxia-inducible factor 1. J. Natl. Cancer Inst. 2003, 95, 516-525.
22. Harada, H.; Kizaka-Kondoh, S.; Hiraoka, M. Optical imaging of tumor hypoxia and evaluation of efficacy of a hypoxia-targeting drug in living animals. Mol. Imaging 2005, 4, 182-193.
23. Harada, H.; Xie, X.; Itasaka, S.; Zeng, L.; Zhu, Y.; Morinibu, A.; Shinomiya, K.; Hiraoka, M. Diameter of tumor blood vessels is a good parameter to estimate HIF-1-active regions in solid tumors. Biochem. Biophys. Res. Commun. 2008, 373, 533-538.
24. Harada, H.; Itasaka, S.; Kizaka-Kondoh, S.; Shibuya, K.; Morinibu, A.; Shinomiya, K.; Hiraoka, M. The Akt/mTOR pathway assures the synthesis of HIF-1alpha protein in a glucoseand reoxygenation-dependent manner in irradiated tumors. J. Biol. Chem. 2009, 284, 5332-5342.
25. Murata, R.; Shibamoto, Y.; Sasai, K.; Oya, N.; Shibata, T.; Takagi, T.; Abe, M. Reoxygenation after single irradiation in rodent tumors of different types and sizes. Int. J. Radiat. Oncol. Biol. Phys. 1996, 34, 859-865.
26. Kim, J.G.; Zhao, D.; Song, Y.; Constantinescu, A.; Mason, R.P.; Liu, H. Interplay of tumor vascular oxygenation and tumor pO2 observed using near-infrared spectroscopy, an oxygen needle electrode, and 19F MR pO2 mapping. J. Biomed. Opt. 2003, 8, 53-62.
27. Cardenas-Navia, L.I.; Yu, D.; Braun, R.D.; Brizel, D.M.; Secomb, T.W.; Dewhirst, M.W. Tumor-dependent kinetics of partial pressure of oxygen fluctuations during air and oxygen breathing. Cancer Res. 2004, 64, 6010-6017.
28. Mueller-Klieser, W.; Schlenger, K.H.; Walenta, S.; Gross, M.; Karbach, U.; Hoeckel, M.; Vaupel, P. Pathophysiological approaches to identifying tumor hypoxia in patients. Radiother. Oncol. 1991, 20S, 21-28.
29. Rumsey, W.L.; Vanderkooi, J.M.; Wilson, D.F. Imaging of phosphorescence: A novel method for measuring oxygen distribution in perfused tissue. Science 1988, 241, 1649-1651.
30. Vinogradov, S.A.; Grosul, P.; Rozhkov, V.; Dunphy, I.; Shuman, L.; Dugan, B.W.; Evans, S.; Wilson, D.F. Oxygen distributions in tissue measured by phosphorescence quenching. Adv. Exp. Med. Biol. 2003, 510, 181-185.
31. Hall, E.J., Ed. Radiobiology for the Radiologist, 4th ed.; J.B. Lippincott Company: Philadelphia, PA, USA, 1994.
32. Brown, J.M. Evidence for acutely hypoxic cells in mouse tumours, and a possible mechanism of reoxygenation. Br. J. Radiol. 1979, 52, 650-656.
33. Dewhirst, M.W. Relationships between cycling hypoxia, HIF-1, angiogenesis and oxidative stress. Radiat. Res. 2009, 172, 653-665.
34. Dewhirst, M.W.; Cao, Y.; Moeller, B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat. Rev. Cancer 2008, 8, 425-437.
35. Vaupel, P.; Hockel, M.; Mayer, A. Detection and characterization of tumor hypoxia using pO2 histography. Antioxid. Redox Signal 2007, 9, 1221-1235.
36. 2 tension measurements. Cancer Res. 1991, 51, 3316-3322.
37. Bindra, R.S.; Crosby, M.E.; Glazer, P.M. Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev. 2007, 26, 249-260.
38. Semenza, G.L. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010, 29, 625-634.
39. Teicher, B.A. Hypoxia and drug resistance. Cancer Metastasis Rev. 1994, 13, 139-168.
40. Durand, R.E. The influence of microenvironmental factors during cancer therapy. In Vivo 1994, 8, 691-702.
41. Hicks, K.O.; Pruijn, F.B.; Secomb, T.W.; Hay, M.P.; Hsu, R.; Brown, J.M.; Denny, W.A.; Dewhirst, M.W.; Wilson, W.R. Use of three-dimensional tissue cultures to model extravascular transport and predict in vivo activity of hypoxia-targeted anticancer drugs. J. Natl. Cancer Inst. 2006, 98, 1118-1128.
42. Tannock, I.F. Conventional cancer therapy: Promise broken or promise delayed? Lancet 1998, 351(Suppl. 2),SII9-SII16.
43. Tannock, I.F. The relation between cell proliferation and the vascular system in a transplanted mouse mammary tumour. Br. J. Cancer 1968, 22, 258-273.
44. Batchelder, R.M.; Wilson, W.R.; Hay, M.P.; Denny, W.A. Oxygen dependence of the cytotoxicity of the enediyne anti-tumour antibiotic esperamicin A1. Br. J. Cancer Suppl. 1996, 27, S52-S56.
45. Teicher, B.A.; Lazo, J.S.; Sartorelli, A.C. Classification of antineoplastic agents by their selective toxicities toward oxygenated and hypoxic tumor cells. Cancer Res. 1981, 41, 73-81.
46. Wartenberg, M.; Ling, F.C.; Muschen, M.; Klein, F.; Acker, H.; Gassmann, M.; Petrat, K.; Putz, V.; Hescheler, J.; Sauer, H. Regulation of the multidrug resistance transporter P-glycoprotein in multicellular tumor spheroids by hypoxia-inducible factor (HIF-1) and reactive oxygen species. FASEB J. 2003, 17, 503-505.
47. Chan, N.; Koritzinsky, M.; Zhao, H.; Bindra, R.; Glazer, P.M.; Powell, S.; Belmaaza, A.; Wouters, B.; Bristow, R.G. Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res. 2008, 68, 605-614.
48. Brizel, D.M.; Scully, S.P.; Harrelson, J.M.; Layfield, L.J.; Bean, J.M.; Prosnitz, L.R.; Dewhirst, M.W. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res. 1996, 56, 941-943.
49. Chan, D.A.; Giaccia, A.J. Hypoxia, gene expression, and metastasis. Cancer Metastasis Rev. 2007, 26, 333-339.
50. Erler, J.T.; Bennewith, K.L.; Nicolau, M.; Dornhofer, N.; Kong, C.; Le, Q.T.; Chi, J.T.; Jeffrey, S.S.; Giaccia, A.J. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006, 440, 1222-1226.
51. Rofstad, E.K. Microenvironment-induced cancer metastasis. Int. J. Radiat. Biol. 2000, 76, 589-605.
52. . Folkman, J. Tumor angiogenesis: Therapeutic implications. N. Engl. J. Med. 1971, 285, 1182-1186.
53. Semenza, G.L. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin. Cancer Biol.2009, 19, 12-16.
54. Sullivan, R.; Graham, C.H. Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev. 2007, 26, 319-331.
55. Forsythe, J.A.; Jiang, B.H.; Iyer, N.V.; Agani, F.; Leung, S.W.; Koos, R.D.; Semenza, G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 1996, 16, 4604-4613.
56. Liao, D.; Johnson, R.S. Hypoxia: A key regulator of angiogenesis in cancer. Cancer Metastasis Rev. 2007, 26, 281-290.
57. 2 tension. Proc. Natl. Acad. Sci. USA 1995, 92, 5510-5514.
58. Berra, E.; Roux, D.; Richard, D.E.; Pouyssegur, J. Hypoxia-inducible factor-1 alpha (HIF-1 alpha) escapes O(2)-driven proteasomal degradation irrespective of its subcellular localization: Nucleus or cytoplasm. EMBO Rep. 2001, 2, 615-620.
59. Hirota, K.; Semenza, G.L. Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases. Biochem. Biophys. Res. Commun. 2005, 338, 610-616.
60. Jaakkola, P.; Mole, D.R.; Tian, Y.M.; Wilson, M.I.; Gielbert, J.; Gaskell, S.J.; Kriegsheim, A.; Hebestreit, H.F.; Mukherji, M.; Schofield, C.J.; Maxwell, P.H.; Pugh, C.W.; Ratcliffe, P.J. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292, 468-472.
61. 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.; Ratcliffe, P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399, 271-275.
62. Semenza, G.L. HIF-1, O(2), and the 3 PHDs: How animal cells signal hypoxia to the nucleus. Cell 2001, 107, 1-3.
63. Kim, J.W.; Gao, P.; Dang, C.V. Effects of hypoxia on tumor metabolism. Cancer Metastasis Rev. 2007, 26, 291-298.
64. Mahon, P.C.; Hirota, K.; Semenza, G.L. FIH-1: A novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes. Dev. 2001, 15, 2675-2686.
65. Moeller, B.J.; Dewhirst, M.W. HIF-1 and tumour radiosensitivity. Br. J. Cancer 2006, 95, 1-5.
66. Zhang, X.; Kon, T.; Wang, H.; Li, F.; Huang, Q.; Rabbani, Z.N.; Kirkpatrick, J.P.; Vujaskovic, Z.; Dewhirst, M.W.; Li, C.Y. Enhancement of hypoxia-induced tumor cell death in vitro and radiation therapy in vivo by use of small interfering RNA targeted to hypoxia-inducible factor-1alpha. Cancer Res. 2004, 64, 8139-8142.
67. Aebersold, D.M.; Burri, P.; Beer, K.T.; Laissue, J.; Djonov, V.; Greiner, R.H.; Semenza, G.L. Expression of hypoxia-inducible factor-1alpha: A novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res. 2001, 61, 2911-2916.
68. Ishikawa, H.; Sakurai, H.; Hasegawa, M.; Mitsuhashi, N.; Takahashi, M.; Masuda, N.; Nakajima, M.; Kitamoto, Y.; Saitoh, J.; Nakano, T. Expression of hypoxic-inducible factor 1alpha predicts metastasis-free survival after radiation therapy alone in stage IIIB cervical squamous cell carcinoma. Int. J. Radiat. Oncol. Biol. Phys. 2004, 60, 513-521.
69. Semenza, G.L. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem. J. 2007, 405, 1-9.
70. Semenza, G.L. Mitochondrial autophagy: Life and breath of the cell. Autophagy 2008, 4, 534-536.
71. Semenza, G.L. Tumor metabolism: Cancer cells give and take lactate. J. Clin. Invest. 2008, 118, 3835-3837.
72. Wood, S.M.; Wiesener, M.S.; Yeates, K.M.; Okada, N.; Pugh, C.W.; Maxwell, P.H.; Ratcliffe, P.J. Selection and analysis of a mutant cell line defective in the hypoxia-inducible factor-1 alpha-subunit (HIF-1alpha). Characterization of hif-1alpha-dependent and -independent hypoxia-inducible gene expression. J. Biol. Chem. 1998, 273, 8360-8368.
73. Fukuda, R.; Zhang, H.; Kim, J.W.; Shimoda, L.; Dang, C.V.; Semenza, G.L. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 2007, 129, 111-122.
74. Zhang, H.; Bosch-Marce, M.; Shimoda, L.A.; Tan, Y.S.; Baek, J.H.; Wesley, J.B.; Gonzalez, F.J.; Semenza, G.L. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 2008, 283, 10892-10903.
75. Pennacchietti, S.; Michieli, P.; Galluzzo, M.; Mazzone, M.; Giordano, S.; Comoglio, P.M. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003, 3, 347-361.
76. Prasad, P.V.; Edelman, R.R.; Epstein, F.H. Noninvasive evaluation of intrarenal oxygenation with BOLD MRI. Circulation 1996, 94, 3271-3275.
77. Prasad, P.; Li, L.P.; Halter, S.; Cabray, J.; Ye, M.; Batlle, D. Evaluation of renal hypoxia in diabetic mice by BOLD MRI. Invest. Radiol. 2010, 45, 819-822.
78. Padhani, A. Science to practice: What does MR oxygenation imaging tell us about human breast cancer hypoxia? Radiology 2010, 254, 1-3.
79. Prasad, P.V. Evaluation of intra-renal oxygenation by BOLD MRI. Nephron Clin. Pract. 2006, 103, c58-c65.
80. Egeland, T.A.; Gaustad, J.V.; Vestvik, I.K.; Benjaminsen, I.C.; Mathiesen, B.; Rofstad, E.K. Assessment of fraction of radiobiologically hypoxic cells in human melanoma xenografts by dynamic contrast-enhanced MRI. Magn. Reson. Med. 2006, 55, 874-882.
81. Cooper, R.A.; Carrington, B.M.; Loncaster, J.A.; Todd, S.M.; Davidson, S.E.; Logue, J.P.; Luthra, A.D.; Jones, A.P.; Stratford, I.; Hunter, R.D.; West, C.M.L. Tumour oxygenation levels correlate with dynamic contrast-enhanced magnetic resonance imaging parameters in carcinoma of the cervix. Radiother. Oncol. 2000, 57, 53-59.
82. Wang, Z.; Su, M.Y.; Nalcioglu, O. Applications of dynamic contrast enhanced MRI in oncology: Measurement of tumor oxygen tension. Technol. Cancer Res. Treat. 2002, 1, 29-38.
83. Gulliksrud, K.; Ovrebo, K.M.; Mathiesen, B.; Rofstad, E.K. Differentiation between hypoxic and non-hypoxic experimental tumors by dynamic contrast-enhanced magnetic resonance imaging. Radiother. Oncol. 2011, 98, 360-364.
84. van Lin, E.N.; Futterer, J.J.; Heijmink, S.W.; van der Vight, L.P.; Hoffmann, A.L.; van Kollenburg, P.; Huisman, H.J.; Scheenen, T.W.; Witjes, J.A.; Leer, J.W.; et al. IMRT boost dose planning on dominant intraprostatic lesions: gold marker-based three-dimensional fusion of CT with dynamic contrast-enhanced and 1H-spectroscopic MRI. Int J Radiat Oncol Biol Phys. 2006, 65,291-303.
85. Magat, J.; Jordan, B.F.; Cron, G.O.; Gallez, B. Noninvasive mapping of spontaneous fluctuations in tumor oxygenation using 19F MRI. Med. Phys. 2010, 37, 5434-5441.
86. Yu, J.X.; Kodibagkar, V.D.; Cui, W.; Mason, R.P. 19F: A versatile reporter for non-invasive physiology and pharmacology using magnetic resonance. Curr. Med. Chem. 2005, 12, 819-848.
87. Matsumoto, S.; Yasui, H.; Mitchell, J.B.; Krishna, M.C. Imaging cycling tumor hypoxia. Cancer Res. 2010, 70, 10019-10023.
88. Yasui, H.; Matsumoto, S.; Devasahayam, N.; Munasinghe, J.P.; Choudhuri, R.; Saito, K.; Subramanian, S.; Mitchell, J.B.; Krishna, M.C. Low-field magnetic resonance imaging to visualize chronic and cycling hypoxia in tumor-bearing mice. Cancer Res. 2010, 70, 6427-6436.
89. Kang, J.H.; Chung, J.K. Molecular-genetic imaging based on reporter gene expression. J. Nucl. Med. 2008, 49S, 164S-179S.
90. Varghese, A.J.; Gulyas, S.; Mohindra, J.K. Hypoxia-dependent reduction of 1-(2-nitro-1- imidazolyl)-3-methoxy-2-propanol by Chinese hamster ovary cells and KHT tumor cells in vitro and in vivo. Cancer Res. 1976, 36, 3761-3765.
91. Chapman, J.D. Hypoxic sensitizers-Implications for radiation therapy. N. Engl. J. Med. 1979, 301, 1429-1432.
92. Chapman, J.D. The detection and measurement of hypoxic cells in solid tumors. Cancer 1984, 54, 2441-2449.
93. Blasberg, R.; Horowitz, M.; Strong, J.; Molnar, P.; Patlak, C.; Owens, E.; Fenstermacher, J. Regional measurements of [14C]misonidazole distribution and blood flow in subcutaneous RT-9 experimental tumors. Cancer Res. 1985, 45, 1692-1701.
94. Rasey, J.S.; Grunbaum, Z.; Magee, S.; Nelson, N.J.; Olive, P.L.; Durand, R.E.; Krohn, K.A. Characterization of radiolabeled fluoromisonidazole as a probe for hypoxic cells. Radiat. Res. 1987, 111, 292-304.
95. Koh, W.J.; Rasey, J.S.; Evans, M.L.; Grierson, J.R.; Lewellen, T.K.; Graham, M.M.; Krohn, K.A.; Griffin, T.W. Imaging of hypoxia in human tumors with [F-18]fluoromisonidazole. Int. J. Radiat. Oncol. Biol. Phys. 1992, 22, 199-212.
96. Rajendran, J.G.; Krohn, K.A. Imaging hypoxia and angiogenesis in tumors. Radiol. Clin. North Am. 2005, 43, 169-187.
97. Bruehlmeier, M.; Roelcke, U.; Schubiger, P.A.; Ametamey, S.M. Assessment of hypoxia and perfusion in human brain tumors using PET with 18F-fluoromisonidazole and 15O-H2O. J. Nucl. Med. 2004, 45, 1851-1859.
98. Cherk, M.H.; Foo, S.S.; Poon, A.M.; Knight, S.R.; Murone, C.; Papenfuss, A.T.; Sachinidis, J.I.; Saunder, T.H.; O'Keefe, G.J.; Scott, A.M. Lack of correlation of hypoxic cell fraction and angiogenesis with glucose metabolic rate in non-small cell lung cancer assessed by 18F-Fluoromisonidazole and 18F-FDG PET. J. Nucl. Med. 2006, 47, 1921-1926.
99. Rajendran, J.G.; Schwartz, D.L.; O'Sullivan, J.; Peterson, L.M.; Ng, P.; Scharnhorst, J.; Grierson, J.R.; Krohn, K.A. Tumor hypoxia imaging with [F-18] fluoromisonidazole positron emission tomography in head and neck cancer. Clin. Cancer Res. 2006, 12, 5435-5441.
100. Bentzen, L.; Keiding, S.; Nordsmark, M.; Falborg, L.; Hansen, S.B.; Keller, J.; Nielsen, O.S.; Overgaard, J. Tumour oxygenation assessed by 18F-fluoromisonidazole PET and polarographic needle electrodes in human soft tissue tumours. Radiother. Oncol. 2003, 67, 339-344.
101. Rasey, J.S.; Hofstrand, P.D.; Chin, L.K.; Tewson, T.J. Characterization of [18F]fluoroetanidazole, a new radiopharmaceutical for detecting tumor hypoxia. J. Nucl. Med. 1999, 40, 1072-1079.
102. Gronroos, T.; Bentzen, L.; Marjamaki, P.; Murata, R.; Horsman, M.R.; Keiding, S.; Eskola, O.; Haaparanta, M.; Minn, H.; Solin, O. Comparison of the biodistribution of two hypoxia markers [18F]FETNIM and [18F]FMISO in an experimental mammary carcinoma. Eur. J. Nucl. Med. Mol. Imaging 2004, 31, 513-520.
103. Piert, M.; Machulla, H.J.; Picchio, M.; Reischl, G.; Ziegler, S.; Kumar, P.; Wester, H.J.; Beck, R.; McEwan, A.J.; Wiebe, L.I.; Schwaiger, M. Hypoxia-specific tumor imaging with 18Ffluoroazomycin arabinoside. J. Nucl. Med. 2005, 46, 106-113.
104. Koch, C.J.; Evans, S.M. Non-invasive PET and SPECT imaging of tissue hypoxia using isotopically labeled 2-nitroimidazoles. Adv. Exp. Med. Biol. 2003, 510, 285-292.
105. Komar, G.; Seppanen, M.; Eskola, O.; Lindholm, P.; Gronroos, T.J.; Forsback, S.; Sipila, H.; Evans, S.M.; Solin, O.; Minn, H. 18F-EF5: A new PET tracer for imaging hypoxia in head and neck cancer. J. Nucl. Med. 2008, 49, 1944-1951.
106. Fujibayashi, Y.; Taniuchi, H.; Yonekura, Y.; Ohtani, H.; Konishi, J.; Yokoyama, A. Copper-62-ATSM: A new hypoxia imaging agent with high membrane permeability and low redox potential. J. Nucl. Med. 1997, 38, 1155-1160.
107. Lewis, J.S.; McCarthy, D.W.; McCarthy, T.J.; Fujibayashi, Y.; Welch, M.J. Evaluation of 64Cu-ATSM in vitro and in vivo in a hypoxic tumor model. J. Nucl. Med. 1999, 40, 177-183.
108. Lewis, J.S.; Sharp, T.L.; Laforest, R.; Fujibayashi, Y.; Welch, M.J. Tumor uptake of copper-diacetyl-bis(N(4)-methylthiosemicarbazone): Effect of changes in tissue oxygenation. J. Nucl. Med. 2001, 42, 655-661.
109. Yuan, H.; Schroeder, T.; Bowsher, J.E.; Hedlund, L.W.; Wong, T.; Dewhirst, M.W. Intertumoral differences in hypoxia selectivity of the PET imaging agent 64Cu(II)-diacetyl-bis(N4-methylthiosemicarbazone). J. Nucl. Med. 2006, 47, 989-998.
110. Takahashi, N.; Fujibayashi, Y.; Yonekura, Y.; Welch, M.J.; Waki, A.; Tsuchida, T.; Sadato, N.; Sugimoto, K.; Itoh, H. Evaluation of 62Cu labeled diacetyl-bis(N4-methylthiosemicarbazone) as a hypoxic tissue tracer in patients with lung cancer. Ann. Nucl. Med. 2000, 14, 323-328.
111. Dehdashti, F.; Grigsby, P.W.; Mintun, M.A.; Lewis, J.S.; Siegel, B.A.; Welch, M.J. Assessing tumor hypoxia in cervical cancer by positron emission tomography with 60Cu-ATSM: Relationship to therapeutic response-a preliminary report. Int. J. Radiat. Oncol. Biol. Phys. 2003, 55, 1233-1238.
112. Dehdashti, F.; Mintun, M.A.; Lewis, J.S.; Bradley, J.; Govindan, R.; Laforest, R.; Welch, M.J.; Siegel, B.A. In vivo assessment of tumor hypoxia in lung cancer with 60Cu-ATSM. Eur. J. Nucl. Med. Mol. Imaging 2003, 30, 844-850.
113. Lord, E.M.; Harwell, L.; Koch, C.J. Detection of hypoxic cells by monoclonal antibody recognizing 2-nitroimidazole adducts. Cancer Res. 1993, 53, 5721-5726.
114. Raleigh, J.A.; Calkins-Adams, D.P.; Rinker, L.H.; Ballenger, C.A.; Weissler, M.C.; Fowler, W.C., Jr.; Novotny, D.B.; Varia, M.A. Hypoxia and vascular endothelial growth factor expression in human squamous cell carcinomas using pimonidazole as a hypoxia marker. Cancer Res. 1998, 58, 3765-3768.
115. Maseide, K.; Kandel, R.A.; Bell, R.S.; Catton, C.N.; O'Sullivan, B.; Wunder, J.S.; Pintilie, M.; Hedley, D.; Hill, R.P. Carbonic anhydrase IX as a marker for poor prognosis in soft tissue sarcoma. Clin. Cancer Res. 2004, 10, 4464-4471.
116. Koukourakis, M.I.; Giatromanolaki, A.; Danielidis, V.; Sivridis, E. Hypoxia inducible factor (HIf1alpha and HIF2alpha) and carbonic anhydrase 9 (CA9) expression and response of head-neck cancer to hypofractionated and accelerated radiotherapy. Int. J. Radiat. Biol. 2008, 84, 47-52.
117. Schrijvers, M.L.; van der Laan, B.F.; de Bock, G.H.; Pattje, W.J.; Mastik, M.F.; Menkema, L.; Langendijk, J.A.; Kluin, P.M.; Schuuring, E.; van der Wal, J.E. Overexpression of intrinsic hypoxia markers HIF1alpha and CA-IX predict for local recurrence in stage T1-T2 glottic laryngeal carcinoma treated with radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 2008, 72, 161-169.
118. Binley, K.; Iqball, S.; Kingsman, A.; Kingsman, S.; Naylor, S. An adenoviral vector regulated by hypoxia for the treatment of ischaemic disease and cancer. Gene Ther. 1999, 6, 1721-1727.
119. Boast, K.; Binley, K.; Iqball, S.; Price, T.; Spearman, H.; Kingsman, S.; Kingsman, A.; Naylor, S. Characterization of physiologically regulated vectors for the treatment of ischemic disease. Hum. Gene Ther. 1999, 10, 2197-2208.
120. Dachs, G.U.; Patterson, A.V.; Firth, J.D.; Ratcliffe, P.J.; Townsend, K.M.; Stratford, I.J.; Harris, A.L. Targeting gene expression to hypoxic tumor cells. Nat. Med. 1997, 3, 515-520.
121. Harada, H.; Kizaka-Kondoh, S.; Itasaka, S.; Shibuya, K.; Morinibu, A.; Shinomiya, K.; Hiraoka, M. The combination of hypoxia-response enhancers and an oxygen-dependent proteolytic motif enables real-time imaging of absolute HIF-1 activity in tumor xenografts. Biochem. Biophys. Res. Commun. 2007, 360, 791-796.
122. Rinsch, C.; Regulier, E.; Deglon, N.; Dalle, B.; Beuzard, Y.; Aebischer, P. A gene therapy approach to regulated delivery of erythropoietin as a function of oxygen tension. Hum. Gene Ther. 1997, 8, 1881-1889.
123. Shibata, T.; Akiyama, N.; Noda, M.; Sasai, K.; Hiraoka, M. 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. 1998, 42, 913-916.
124. Shibata, T.; Giaccia, A.J.; Brown, J.M. Development of a hypoxia-responsive vector for tumorspecific gene therapy. Gene Ther. 2000, 7, 493-498.
125. Liu, J.; Qu, R.; Ogura, M.; Shibata, T.; Harada, H.; Hiraoka, M. Real-time imaging of hypoxiainducible factor-1 activity in tumor xenografts. J. Radiat. Res. (Tokyo). 2005, 46, 93-102.
126. Yeom, C.J.; Chung, J.K.; Kang, J.H.; Jeon, Y.H.; Kim, K.I.; Jin, Y.N.; Lee, Y.M.; Jeong, J.M.; Lee, D.S. Visualization of hypoxia-inducible factor-1 transcriptional activation in C6 glioma using luciferase and sodium iodide symporter genes. J. Nucl. Med. 2008, 49, 1489-1497.
127. He, F.; Deng, X.; Wen, B.; Liu, Y.; Sun, X.; Xing, L.; Minami, A.; Huang, Y.; Chen, Q.; Zanzonico, P.B.; et al. Noninvasive molecular imaging of hypoxia in human xenografts: Comparing hypoxia-induced gene expression with endogenous and exogenous hypoxia markers. Cancer Res. 2008, 68, 8597-8606.