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Published in:

01-09-2008

Clinical biomarkers for hypoxia targeting

Authors: Quynh-Thu Le, Don Courter

Published in: Cancer and Metastasis Reviews | Issue 3/2008

Abstract

Tumor hypoxia or a reduction of the tissue oxygen tension is a key microenvironmental factor for tumor progression and treatment resistance in solid tumors. Because hypoxic tumor cells have been demonstrated to be more resistant to ionizing radiation, hypoxia has been a focus of laboratory and clinical research in radiation therapy for many decades. It is believed that proper detection of hypoxic regions would guide treatment options and ultimately improve tumor response. To date, most clinical efforts in targeting tumor hypoxia have yielded equivocal results due to the lack of appropriate patient selection. However, with improved understanding of the molecular pathways regulated by hypoxia and the discovery of novel hypoxia markers, the prospect of targeting hypoxia has become more tangible. This chapter will focus on the development of clinical biomarkers for hypoxia targeting.

Brown, J. M., & Giaccia, A. J. (1998). The unique physiology of solid tumors: Opportunities (and problems) for cancer therapy. Cancer Research, 58, 1408–1416.PubMed

Thomlinson, R. H., & Gray, L. H. (1955). The histological structure of some human lung cancers and the possible implications for radiotherapy. British Journal of Cancer, 9, 539–549.PubMed

Kennedy, K. A., Teicher, B. A., Rockwell, S., et al. (1980). The hypoxic tumor cell: A target for selective cancer chemotherapy. Biochemical Pharmacology, 29, 1–8.PubMed

Graeber, T. G., Peterson, J. F., Tsai, M., et al. (1994). Hypoxia induces the accumulation of p53 protein, but the activation of a G1-phase checkpoint by low oxygen conditions is independent of p53 status. Molecular and Cellular Biology, 14, 6264–6277.PubMed

Le, Q. T., Denko, N. C., & Giaccia, A. J. (2004). Hypoxic gene expression and metastasis. Cancer and Metastasis Reviews, 23, 293–310.PubMed

Fazekas, J. T., Pajak, T. F., Wasserman, T., et al. (1987). Failure of misonidazole-sensitized radiotherapy to impact upon outcome among stage III–IV squamous cancers of the head and neck. International Journal of Radiation Oncology, Biology, Physics, 13, 1155–1160.PubMed

Lee, D. J., Moini, M., Giuliano, J., et al. (1996). Hypoxic sensitizer and cytotoxin for head and neck cancer. Annals of the Academy of Medicine, Singapore, 25, 397–404.PubMed

Overgaard, J., Hansen, H. S., Anderson, A. P., et al. (1989). Misonidazole combined with split course radiotherapy in the treatment of invasive carcinoma of larynx and pharynx: Report from the DAHANCA study. International Journal of Radiation Oncology, Biology, Physics, 16, 1065–1068.PubMed

Van den Bogaert, W., van der Schueren, E., Horiot, J. C., et al. (1995). The EORTC randomized trial on three fractions per day and misonidazole (trial no. 22811) in advanced head and neck cancer: Long-term results and side effects. Radiotherapy and Oncology, 35, 91–99.PubMed

10.

Lee, D. J., Pajak, T. F., Stetz, J., et al. (1989). A phase I/II study of the hypoxic cell sensitizer misonidazole as an adjunct to high fractional dose radiotherapy in patients with unresectable squamous cell carcinoma of the head and neck: A RTOG randomized study (#79-04). International Journal of Radiation Oncology, Biology, Physics, 16, 465–470.PubMed

11.

Hill, R. P. (2005). Targeted treatment: insights from studies of osteopontin and hypoxia. Lancet Oncology, 6, 733–734.PubMed

12.

Tatum, J. L., Kelloff, G. J., Gillies, R. J., et al. (2006). Hypoxia: Importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. International Journal of Radiation Biology, 82, 699–757.PubMed

13.

Gatenby, R. A., Kessler, H. B., Rosenblum, J. S., et al. (1988). Oxygen distribution in squamous cell carcinoma metastases and its relationship to outcome of radiation therapy. International Journal of Radiation Oncology, Biology, Physics, 14, 831–838.PubMed

14.

Wendling, P., Manz, R., Thews, G., et al. (1984). Heterogeneous oxygenation of rectal carcinomas in humans: A critical parameter for preoperative irradiation? Advances in Experimental Medicine and Biology, 180, 293–300.PubMed

15.

Vaupel, P. (2004). Tumor microenvironmental physiology and its implications for radiation oncology. Seminars in Radiation Oncology, 14, 198–206.PubMed

16.

Brizel, D. M., Dodge, R. K., Clough, R. W., et al. (1999). Oxygenation of head and neck cancer: Changes during radiotherapy and impact on treatment outcome. Radiotherapy and Oncology, 53, 113–117.PubMed

17.

Nordsmark, M., & Overgaard, J. (2000). A confirmatory prognostic study on oxygenation status and loco-regional control in advanced head and neck squamous cell carcinoma treated by radiation therapy. Radiotherapy and Oncology, 57, 39–43.PubMed

18.

Rudat, V., Stadler, P., Becker, A., et al. (2001). Predictive value of the tumor oxygenation by means of pO2 histography in patients with advanced head and neck cancer. Strahlentherapie und Onkologie, 177, 462–468.PubMed

19.

Le, Q. T., Chen, E., Salim, A., et al. (2006). An evaluation of tumor oxygenation and gene expression in patients with early stage non-small cell lung cancers. Clinical Cancer Research, 12, 1507–1514.PubMed

20.

Hockel, M., Schlenger, K., Aral, B., et al. (1996). Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Research, 56, 4509–4515.PubMed

21.

Hockel, M., Schlenger, K., Hockel, S., et al. (1999). Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Research, 59, 4525–4528.PubMed

22.

Fyles, A., Milosevic, M., Hedley, D., et al. (2002). Tumor hypoxia has independent predictor impact only in patients with node-negative cervix cancer. Journal Clinical Oncology, 20, 680–687.

23.

Movsas, B., Chapman, J. D., Hanlon, A. L., et al. (2002). Hypoxic prostate/muscle pO2 ratio predicts for biochemical failure in patients with prostate cancer: Preliminary findings. Urology, 60, 634–639.PubMed

24.

Brizel, D. M., Prosnitz, R. G., Hunter, S., et al. (2004). Necessity for adjuvant neck dissection in setting of concurrent chemoradiation for advanced head-and-neck cancer. International Journal of Radiation Oncology, Biology, Physics, 58, 1418–1423.PubMed

25.

Nordsmark, M., Bentzen, S. M., Rudat, V., et al. (2005). Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiotherapy and Oncology, 77, 18–24.PubMed

26.

Brizel, D. M., Scully, S. P., Harrelson, J. M., et al. (1996). Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Research, 56, 941–943.PubMed

27.

Nordsmark, M., Alsner, J., Keller, J., et al. (2001). Hypoxia in human soft tissue sarcomas: adverse impact on survival and no association with p53 mutations. British Journal of Cancer, 84, 1070–1075.PubMed

28.

Stone, H. B., Brown, J. M., Phillips, T. L., et al. (1993). Oxygen in human tumors: Correlations between methods of measurement and response to therapy. Radiation Research, 136, 422–434.PubMed

29.

Howe, F. A., Robinson, S. P., McIntyre, D. J., et al. (2001). Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR in Biomedicine, 14, 497–506.PubMed

30.

Hoskin, P. J., Carnell, D. M., Taylor, N. J., et al. (2007). Hypoxia in prostate cancer: Correlation of BOLD-MRI with pimonidazole immunohistochemistry-initial observations. International Journal of Radiation Oncology, Biology, Physics, 68, 1065–1071.PubMed

31.

Chapman, J. D. (1979). Hypoxic sensitizers—Implications for radiation therapy. New England Journal of Medicine, 301, 1429–1432.PubMed

32.

Raleigh, J. A., Calkins-Adams, D. P., Rinker, L. H., et al. (1998). Hypoxia and vascular endothelial growth factor expression in human squamous cell carcinomas using pimonidazole as a hypoxia marker. Cancer Research, 58, 3765–3768.PubMed

33.

Evans, S. M., Hahn, S., Pook, D. R., et al. (2000). Detection of hypoxia in human squamous cell carcinoma by EF5 binding. Cancer Research, 60, 2018–2024.PubMed

34.

Varghese, A. J., Gulyas, S., & Mohindra, J. K. (1976). 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 Research, 36, 3761–3765.PubMed

35.

Ljungkvist, A. S., Bussink, J., Kaanders, J. H., et al. (2007). Dynamics of tumor hypoxia measured with bioreductive hypoxic cell markers. Radiation Research, 167, 127–145.PubMed

36.

Evans, S. M., & Koch, C. J. (2003). Prognostic significance of tumor oxygenation in humans. Cancer Letters, 195, 1–16.PubMed

37.

Raleigh, J. A., Chou, S. C., Arteel, G. E., et al. (1999). Comparisons among pimonidazole binding, oxygen electrode measurements, and radiation response in C3H mouse tumors. Radiation Research, 151, 580–589.PubMed

38.

Koch, C. J., Hahn, S. M., Rockwell Jr., K., et al. (2001). Pharmacokinetics of EF5 [2-(2-nitro-1-H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl) acetamide] in human patients: Implications for hypoxia measurements in vivo by 2-nitroimidazoles. Cancer Chemotherapy and Pharmacology, 48, 177–187.PubMed

39.

Ljungkvist, A. S., Bussink, J., Rijken, P. F., et al. (2000). Changes in tumor hypoxia measured with a double hypoxic marker technique. International Journal of Radiation Oncology, Biology, Physics, 48, 1529–1538.PubMed

40.

van Laarhoven, H. W., Klomp, D. W., Kamm, Y. J., et al. (2003). In vivo monitoring of capecitabine metabolism in human liver by 19fluorine magnetic resonance spectroscopy at 1.5 and 3 Tesla field strength. Cancer Research, 63, 7609–7612.PubMed

41.

Kaanders, J. H., Wijffels, K. I., Marres, H. A., et al. (2002). Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Research, 62, 7066–7074.PubMed

42.

Evans, S. M., Fraker, D., Hahn, S. M., et al. (2006). EF5 binding and clinical outcome in human soft tissue sarcomas. International Journal of Radiation Oncology, Biology, Physics, 64, 922–927.PubMed

43.

Evans, S. M., Judy, K. D., Dunphy, I., et al. (2004). Hypoxia is important in the biology and aggression of human glial brain tumors. Clinical Cancer Research, 10, 8177–8184.PubMed

44.

Gagel, B., Reinartz, P., Dimartino, E., et al. (2004). pO(2) Polarography versus positron emission tomography ([(18)F] fluoromisonidazole, [(18)F]-2-fluoro-2'-deoxyglucose). An appraisal of radiotherapeutically relevant hypoxia. Strahlentherapie und Onkologie, 180, 616–622.PubMed

45.

Rajendran, J. G., Schwartz, D. L., O'Sullivan, J., et al. (2006). Tumor hypoxia imaging with [F-18] fluoromisonidazole positron emission tomography in head and neck cancer. Clinical Cancer Research, 12, 5435–5441.PubMed

46.

Lehtio, K., Eskola, O., Viljanen, T., et al. (2004). Imaging perfusion and hypoxia with PET to predict radiotherapy response in head-and-neck cancer. International Journal of Radiation Oncology, Biology, Physics, 59, 971–982.PubMed

47.

Thorwarth, D., Eschmann, S. M., Holzner, F., et al. (2006). Combined uptake of [18F]FDG and [18F]FMISO correlates with radiation therapy outcome in head-and-neck cancer patients. Radiotherapy and Oncology, 80, 151–156.PubMed

48.

Eschmann, S. M., Paulsen, F., Reimold, M., et al. (2005). Prognostic impact of hypoxia imaging with 18F-misonidazole PET in non-small cell lung cancer and head and neck cancer before radiotherapy. Journal of Nuclear Medicine, 46, 253–260.PubMed

49.

Rischin, D., Hicks, R. J., Fisher, R., et al. (2006). Prognostic significance of [18F]-misonidazole positron emission tomography-detected tumor hypoxia in patients with advanced head and neck cancer randomly assigned to chemoradiation with or without tirapazamine: a substudy of Trans-Tasman Radiation Oncology Group Study 98.02. Journal Clinical Oncology, 24, 2098–2104.

50.

Hicks, R. J., Rischin, D., Fisher, R., et al. (2005). Utility of FMISO PET in advanced head and neck cancer treated with chemoradiation incorporating a hypoxia-targeting chemotherapy agent. European Journal of Nuclear Medicine and Molecular Imaging, 32, 1384–1391.PubMed

51.

Thorwarth, D., Eschmann, S. M., Paulsen, F., et al. (2007). Hypoxia dose painting by numbers: a planning study. International Journal of Radiation Oncology, Biology, Physics, 68, 291–300.PubMed

52.

Souvatzoglou, M., Grosu, A. L., Roper, B., et al. (2007). Tumour hypoxia imaging with [¹⁸F]FAZA PET in head and neck cancer patients: A pilot study. European Journal of Nuclear Medicine and Molecular Imaging, 34(10), 1566–1575.PubMed

53.

Fujibayashi, Y., Taniuchi, H., Yonekura, Y., et al. (1997). Copper-62-ATSM: a new hypoxia imaging agent with high membrane permeability and low redox potential. Journal of Nuclear Medicine, 38, 1155–1160.PubMed

54.

Chao, K. S., Bosch, W. R., Mutic, S., et al. (2001). A novel approach to overcome hypoxic tumor resistance: Cu-ATSM-guided intensity-modulated radiation therapy. International Journal of Radiation Oncology, Biology, Physics, 49, 1171–1182.PubMed

55.

Grigsby, P. W., Malyapa, R. S., Higashikubo, R., et al. (2007). Comparison of molecular markers of hypoxia and imaging with (60)Cu-ATSM in cancer of the uterine cervix. Molecular Imaging and Biology, 9, 278–283.PubMed

56.

Dehdashti, F., Mintun, M. A., Lewis, J. S., et al. (2003). In vivo assessment of tumor hypoxia in lung cancer with ⁶⁰Cu-ATSM.. European Journal of Nuclear Medicine and Molecular Imaging, 30, 844–850.PubMed

57.

Lee, N. Y., Mechalakos, J. G., Nehmeh, S., et al. (2008). Fluorine-18-labeled fluoromisonidazole positron emission and computed tomography-guided intensity-modulated radiotherapy for head and neck cancer: A feasibility study.. International Journal of Radiation Oncology, Biology, Physics, 70(1), 2–13.PubMed

58.

Grosu, A. L., Souvatzoglou, M., Roper, B., et al. (2007). Hypoxia imaging with FAZA-PET and theoretical considerations with regard to dose painting for individualization of radiotherapy in patients with head and neck cancer. International Journal of Radiation Oncology, Biology, Physics, 69, 541–551.PubMed

59.

Le, Q. T., Shi, G., Cao, H., et al. (2005). Galectin-1: A link between tumor hypoxia and tumor immune privilege. Journal Clinical Oncology, 23, 8932–8941.

60.

Le, Q. T., Kong, C., Lavori, P. W., et al. (2007). Expression and prognostic significance of a panel of tissue hypoxia markers in head-and-neck squamous cell carcinomas. International Journal of Radiation Oncology, Biology, Physics, 69, 167–175.PubMed

61.

Erler, J. T., Bennewith, K. L., Nicolau, M., et al. (2006). Lysyl oxidase is essential for hypoxia-induced metastasis. Nature, 440, 1222–1226.PubMed

62.

Giatromanolaki, A., Koukourakis, M. I., Gatter, K. C., et al. (2007). BNIP3 expression in endometrial cancer relates to active hypoxia inducible factor 1a pathway and prognosis.. Journal of Clinical Pathology, 61(2), 217–220.PubMed

63.

Koukourakis, M. I., Giatromanolaki, A., Sivridis, E., et al. (2006). Lactate dehydrogenase 5 expression in operable colorectal cancer: Strong association with survival and activated vascular endothelial growth factor pathway—A report of the Tumour Angiogenesis Research Group. Journal Clinical Oncology, 24, 4301–4308.

64.

Giatromanolaki, A., Sivridis, E., Gatter, K. C., et al. (2006). Lactate dehydrogenase 5 (LDH-5) expression in endometrial cancer relates to the activated VEGF/VEGFR2(KDR) pathway and prognosis. Gynecologic Oncology, 103, 912–918.PubMed

65.

Giatromanolaki, A., Koukourakis, M. I., Sowter, H. M., et al. (2004). BNIP3 expression is linked with hypoxia-regulated protein expression and with poor prognosis in non-small cell lung cancer. Clinical Cancer Research, 10, 5566–5571.PubMed

66.

de Witte, J. H., Sweep, C. G., Klijn, J. G., et al. (1999). Prognostic impact of urokinase-type plasminogen activator (uPA) and its inhibitor (PAI-1) in cytosols and pellet extracts derived from 892 breast cancer patients. British Journal of Cancer, 79, 1190–1198.PubMed

67.

Linderholm, B. K., Lindh, B., Beckman, L., et al. (2003). Prognostic correlation of basic fibroblast growth factor and vascular endothelial growth factor in 1307 primary breast cancers. Clinical Breast Cancer, 4, 340–347.PubMedCrossRef

68.

De Paola, F., Granato, A. M., Scarpi, E., et al. (2002). Vascular endothelial growth factor and prognosis in patients with node-negative breast cancer. International Journal of Cancer, 98, 228–233.

69.

Kyzas, P. A., Cunha, I. W., & Ioannidis, J. P. (2005). Prognostic significance of vascular endothelial growth factor immunohistochemical expression in head and neck squamous cell carcinoma: a meta-analysis. Clinical Cancer Research, 11, 1434–1440.PubMed

70.

Stroka, D. M., Burkhardt, T., Desbaillets, I., et al. (2001). HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB Journal, 15, 2445–2453.PubMed

71.

Zundel, W., Schindler, C., Haas-Kogan, D., et al. (2000). Loss of PTEN facilitates HIF-1-mediated gene expression. Genes & Development, 14, 391–396.

72.

Zelzer, E., Levy, Y., Kahana, C., et al. (1998). Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO Journal, 17, 5085–5094.PubMed

73.

Zhong, H., Chiles, K., Feldser, D., et al. (2000). Modulation of hypoxia-inducible factor 1alpha 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 Research, 60, 1541–1545.PubMed

74.

Janssen, H. L., Haustermans, K. M., Sprong, D., et al. (2002). HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. International Journal of Radiation Oncology, Biology, Physics, 54, 1537–1549.PubMed

75.

Mayer, A., Hockel, M., & Vaupel, P. (2005). Carbonic anhydrase IX expression and tumor oxygenation status do not correlate at the microregional level in locally advanced cancers of the uterine cervix. Clinical Cancer Research, 11, 7220–7225.PubMed

76.

Mayer, A., Hockel, M., Wree, A., et al. (2005). Microregional expression of glucose transporter-1 and oxygenation status: Lack of correlation in locally advanced cervical cancers. Clinical Cancer Research, 11, 2768–2773.PubMed

77.

Mayer, A., Wree, A., Hockel, M., et al. (2004). Lack of correlation between expression of HIF-1alpha protein and oxygenation status in identical tissue areas of squamous cell carcinomas of the uterine cervix. Cancer Research, 64, 5876–5881.PubMed

78.

Haugland, H., Vukovic, V., Pintilie, M., et al. (2002). Expression of hypoxia-inducible factor-1alpha in cervical carcinomas: Correlation with tumor oxygenation. International Journal of Radiation Oncology, Biology, Physics, 53, 854–861.PubMed

79.

Chi, J. T., Wang, Z., Nuyten, D. S., et al. (2006). Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med, 3, e47.PubMed

80.

Winter, S. C., Buffa, F. M., Silva, P., et al. (2007). Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Research, 67, 3441–3449.PubMed

81.

Riedel, F., Gotte, K., Schwalb, J., et al. (2000). Serum levels of vascular endothelial growth factor in patients with head and neck cancer. European Archives of Oto-rhino-laryngology, 257, 332–336.PubMed

82.

Salven, P., Manpaa, H., Orpana, A., et al. (1997). Serum vascular endothelial growth factor is often elevated in disseminated cancer. Clinical Cancer Research, 3, 647–651.PubMed

83.

Imagawa, S., Yamaguchi, Y., Higuchi, M., et al. (2001). Levels of vascular endothelial growth factor are elevated in patients with obstructive sleep apnea–hypopnea syndrome. Blood, 98, 1255–1257.PubMed

84.

Dunst, J., Stadler, P., Becker, A., et al. (2001). Tumor hypoxia and systemic levels of vascular endothelial growth factor (VEGF) in head and neck cancers. Strahlentherapie und Onkologie, 177, 469–473.PubMed

85.

Le, Q. T., Sutphin, P. D., Raychaudhuri, S., et al. (2003). Identification of osteopontin as a prognostic plasma marker for head and neck squamous cell carcinomas. Clinical Cancer Research, 9, 59–67.PubMed

86.

Nordsmark, M., Eriksen, J. G., Gebski, V., et al. (2007). Differential risk assessments from five hypoxia specific assays: The basis for biologically adapted individualized radiotherapy in advanced head and neck cancer patients.. Radiotherapy and Oncology, 83(3), 389–397.PubMed

87.

Petrik, D., Lavori, P. W., Cao, H., et al. (2006). Plasma osteopontin is an independent prognostic marker for head and neck cancers. Journal Clinical Oncology, 24, 5291–5297.

88.

Overgaard, J., Eriksen, J. G., Nordsmark, M., et al. (2005). Plasma osteopontin, hypoxia, and response to the hypoxia sensitiser nimorazole in radiotherapy of head and neck cancer: Results from the DAHANCA 5 randomised double-blind placebo-controlled trial. Lancet Oncology, 6, 757–764.PubMed

89.

Aebersold, D. M., Burri, P., Beer, K. T., et al. (2001). Expression of hypoxia-inducible factor-1alpha: A novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Research, 61, 2911–2916.PubMed

90.

Koukourakis, M. I., Giatromanolaki, A., Sivridis, E., et al. (2002). Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer. International Journal of Radiation Oncology, Biology, Physics, 53, 1192–1202.PubMed

91.

Beasley, N. J., Leek, R., Alam, M., et al. (2002). Hypoxia-inducible factors HIF-1alpha and HIF-2alpha in head and neck cancer: Relationship to tumor biology and treatment outcome in surgically resected patients. Cancer Research, 62, 2493–2497.PubMed

92.

Hui, E. P., Chan, A. T., Pezzella, F., et al. (2002). Coexpression of hypoxia-inducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival. Clinical Cancer Research, 8, 2595–2604.PubMed

93.

Kyzas, P. A., Stefanou, D., Batistatou, A., et al. (2005). Hypoxia-induced tumor angiogenic pathway in head and neck cancer: An in vivo study. Cancer Letters, 225, 297–304.PubMed

94.

Winter, S. C., Shah, K. A., Han, C., et al. (2006). The relation between hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression with anemia and outcome in surgically treated head and neck cancer. Cancer, 107, 757–766.PubMed

95.

Koukourakis, M. I., Bentzen, S. M., Giatromanolaki, A., et al. (2006). Endogenous markers of two separate hypoxia response pathways (hypoxia inducible factor 2 alpha and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial. Journal Clinical Oncology, 24, 727–735.

96.

Bachtiary, B., Schindl, M., Potter, R., et al. (2003). Overexpression of hypoxia-inducible factor 1alpha indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clinical Cancer Research, 9, 2234–2240.PubMed

97.

Birner, P., Schindl, M., Obermair, A., et al. (2000). Overexpression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Research, 60, 4693–4696.PubMed

98.

Burri, P., Djonov, V., Aebersold, D. M., et al. (2003). Significant correlation of hypoxia-inducible factor-1alpha with treatment outcome in cervical cancer treated with radical radiotherapy. International Journal of Radiation Oncology, Biology, Physics, 56, 494–501.PubMed

99.

Hutchison, G. J., Valentine, H. R., Loncaster, J. A., et al. (2004). Hypoxia-inducible factor 1alpha expression as an intrinsic marker of hypoxia: correlation with tumor oxygen, pimonidazole measurements, and outcome in locally advanced carcinoma of the cervix. Clinical Cancer Research, 10, 8405–8412.PubMed

100.

Dales, J. P., Garcia, S., Meunier-Carpentier, S., et al. (2005). Overexpression of hypoxia-inducible factor HIF-1alpha predicts early relapse in breast cancer: retrospective study in a series of 745 patients. International Journal of Cancer, 116, 734–739.

101.

Kronblad, A., Jirstrom, K., Ryden, L., et al. (2006). Hypoxia inducible factor-1alpha is a prognostic marker in premenopausal patients with intermediate to highly differentiated breast cancer but not a predictive marker for tamoxifen response. International Journal of Cancer, 118, 2609–2616.

102.

Schindl, M., Schoppmann, S. F., Samonigg, H., et al. (2002). Overexpression of hypoxia-inducible factor 1alpha is associated with an unfavorable prognosis in lymph node-positive breast cancer. Clinical Cancer Research, 8, 1831–1837.PubMed

103.

Vleugel, M. M., Greijer, A. E., Shvarts, A., et al. (2005). Differential prognostic impact of hypoxia induced and diffuse HIF-1alpha expression in invasive breast cancer. Journal of Clinical Pathology, 58, 172–177.PubMed

104.

Trastour, C., Benizri, E., Ettore, F., et al. (2007). HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. International Journal of Cancer, 120, 1451–1458.

105.

Giatromanolaki, A., Koukourakis, M. I., Sivridis, E., et al. (2001). Relation of hypoxia inducible factor 1 alpha and 2 alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival. British Journal of Cancer, 85, 881–890.PubMed

106.

Swinson, D. E., Jones, J. L., Cox, G., et al. (2004). Hypoxia-inducible factor-1 alpha in non small cell lung cancer: relation to growth factor, protease and apoptosis pathways. International Journal of Cancer, 111, 43–50.

107.

Kim, S. J., Rabbani, Z. N., Dewhirst, M. W., et al. (2005). Expression of HIF-1alpha, CA IX, VEGF, and MMP-9 in surgically resected non-small cell lung cancer.. Lung Cancer, 49(3), 325–335.PubMed

108.

Beasley, N. J., Wykoff, C. C., Watson, P. H., et al. (2001). Carbonic anhydrase IX, an endogenous hypoxia marker, expression in head and neck squamous cell carcinoma and its relationship to hypoxia, necrosis, and microvessel density. Cancer Research, 61, 5262–5267.PubMed

109.

Koukourakis, M. I., Giatromanolaki, A., Sivridis, E., et al. (2001). Hypoxia-regulated carbonic anhydrase-9 (CA9) relates to poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clinical Cancer Research, 7, 3399–3403.PubMed

110.

Jonathan, R. A., Wijffels, K. I., Peeters, W., et al. (2006). The prognostic value of endogenous hypoxia-related markers for head and neck squamous cell carcinomas treated with ARCON. Radiotherapy and Oncology, 79, 288–297.PubMed

111.

De Schutter, H., Landuyt, W., Verbeken, E., et al. (2005). The prognostic value of the hypoxia markers CA IX and GLUT 1 and the cytokines VEGF and IL 6 in head and neck squamous cell carcinoma treated by radiotherapy +/− chemotherapy. BMC Cancer, 5, 42.PubMed

112.

Hedley, D., Pintilie, M., Woo, J., et al. (2003). Carbonic anhydrase IX expression, hypoxia, and prognosis in patients with uterine cervical carcinomas. Clinical Cancer Research, 9, 5666–5674.PubMed

113.

Loncaster, J. A., Harris, A. L., Davidson, S. E., et al. (2001). Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Research, 61, 6394–6399.PubMed

114.

Span, P. N., Bussink, J., Manders, P., et al. (2003). Carbonic anhydrase-9 expression levels and prognosis in human breast cancer: Association with treatment outcome. British Journal of Cancer, 89, 271–276.PubMed

115.

Brennan, D. J., Jirstrom, K., Kronblad, A., et al. (2006). CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clinical Cancer Research, 12, 6421–6431.PubMed

116.

Hussain, S. A., Ganesan, R., Reynolds, G., et al. (2007). Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. British Journal of Cancer, 96, 104–109.PubMed

117.

Giatromanolaki, A., Koukourakis, M. I., Sivridis, E., et al. (2001). Expression of hypoxia-inducible carbonic anhydrase-9 relates to angiogenic pathways and independently to poor outcome in non-small cell lung cancer. Cancer Research, 61, 7992–7998.PubMed

118.

Kon-no, H., Ishii, G., Nagai, K., et al. (2006). Carbonic anhydrase IX expression is associated with tumor progression and a poor prognosis of lung adenocarcinoma. Lung Cancer, 54, 409–418.PubMed

119.

Swinson, D. E., Jones, J. L., Richardson, D., et al. (2003). Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer. Journal Clinical Oncology, 21, 473–482.

120.

Oliver, R. J., Woodwards, R. T., Sloan, P., et al. (2004). Prognostic value of facilitative glucose transporter Glut-1 in oral squamous cell carcinomas treated by surgical resection; results of EORTC Translational Research Fund studies. European Journal of Cancer, 40, 503–507.PubMed

121.

Kunkel, M., Reichert, T. E., Benz, P., et al. (2003). Overexpression of Glut-1 and increased glucose metabolism in tumors are associated with a poor prognosis in patients with oral squamous cell carcinoma. Cancer, 97, 1015–1024.PubMed

122.

Mineta, H., Miura, K., Takebayashi, S., et al. (2002). Prognostic value of glucose transporter 1 expression in patients with hypopharyngeal carcinoma. Anticancer Research, 22, 3489–3494.PubMed

123.

Airley, R., Loncaster, J., Davidson, S., et al. (2001). Glucose transporter glut-1 expression correlates with tumor hypoxia and predicts metastasis-free survival in advanced carcinoma of the cervix. Clinical Cancer Research, 7, 928–934.PubMed

124.

Stackhouse, B. L., Williams, H., Berry, P., et al. (2005). Measurement of glut-1 expression using tissue microarrays to determine a race specific prognostic marker for breast cancer. Breast Cancer Research and Treatment, 93, 247–253.PubMed

125.

Minami, K., Saito, Y., Imamura, H., et al. (2002). Prognostic significance of p53, Ki-67, VEGF and Glut-1 in resected stage I adenocarcinoma of the lung. Lung Cancer, 38, 51–57.PubMed

126.

Nguyen, X. C., Lee, W. W., Chung, J. H., et al. (2007). FDG uptake, glucose transporter type 1, and Ki-67 expressions in non-small-cell lung cancer: correlations and prognostic values. European Journal of Radiology, 62, 214–219.PubMed

Title: Clinical biomarkers for hypoxia targeting
Authors: Quynh-Thu Le
Don Courter
Publication date: 01-09-2008
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 3/2008
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-008-9144-9

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