Is the hypoxia-inducible factor pathway important in gastric cancer?

European Journal of Cancer

Volumn 41, Issue 18, 2005, Pages 2792-2805

  Griffiths, E A ^a,b   Pritchard, S A ^a   Welch, I M ^a   Price, P M ^b   West, C M ^b  

^a WYTHENSHAWE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Gastric adenocarcinoma; HIF 1 ; Tumour hypoxia

Indexed keywords

1 BENZYL 3 (5 HYDROXYMETHYL 2 FURYL)INDAZOLE; ANTINEOPLASTIC AGENT; BCG VACCINE; BLEOMYCIN; CARBONATE DEHYDRATASE; CISPLATIN; DOXORUBICIN; ERYTHROPOIETIN RECEPTOR; ETOPOSIDE; FLUOROURACIL; GENE PRODUCT; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; NONSTEROID ANTIINFLAMMATORY AGENT; PROCARBAZINE; PROTEIN SUBUNIT; REACTIVE OXYGEN METABOLITE; REGULATOR PROTEIN; TAMOXIFEN; VASCULOTROPIN; VINCRISTINE;

ADVANCED CANCER; ASTROCYTOMA; BLADDER CANCER; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER GROWTH; CANCER INVASION; CANCER PREVENTION; CANCER RADIOTHERAPY; CANCER RISK; CANCER SURGERY; CARCINOGENESIS; CLINICAL TRIAL; COLORECTAL CANCER; CORRELATION ANALYSIS; DENSITY; DISEASE ASSOCIATION; DISEASE COURSE; DRUG SAFETY; DRUG TARGETING; ENDOMETRIUM CANCER; ESOPHAGUS CANCER; GASTRITIS; GASTROINTESTINAL STROMAL TUMOR; GENE EXPRESSION; GENE TARGETING; HEAD AND NECK CANCER; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HYPOXEMIA; IMMUNOHISTOCHEMISTRY; ISCHEMIA; LYMPH NODE METASTASIS; MICROVASCULATURE; MOUTH CANCER; NASOPHARYNX CANCER; NONHUMAN; OLIGODENDROGLIOMA; ONCOLOGY; OROPHARYNX CANCER; OVARY CANCER; OXYGENATION; PATIENT SELECTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN STABILITY; PROTEIN TARGETING; REVIEW; STOMACH CANCER; TRANSURETHRAL RESECTION; URINARY TRACT CANCER; UTERINE CERVIX CARCINOMA;

EID: 28244472139     PISSN: 09598049     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejca.2005.09.008     Document Type: Article

References (126)

1. P. Pisani, D.M. Parkin, and F. Bray Estimates of the worldwide mortality from 25 cancers in 1990 Int J Cancer 83 1 1999 18 29
2. M.R. Keighley Gastrointestinal cancers in Europe Aliment Pharmacol Ther 18 Suppl. 3 2003 7 30
3. E.W. Gillison, J. Powell, and C.C. McConkey Surgical workload and outcome after resection for carcinoma of the oesophagus and cardia Br J Surg 89 3 2002 344 348
4. J.S. Macdonald, S.R. Smalley, and J. Benedetti Chemoradiotherapy after surgery compared with surgery alone for adenocarcinoma of the stomach or gastroesophageal junction N Engl J Med 345 10 2001 725 730
5. R.H. Thomlinson, and L.H. Gray The histological structure of some human lung cancers and the possible implications for radiotherapy Br J Cancer 9 4 1955 539 549
6. M.A. Konerding, W. Malkusch, and B. Klapthor Evidence for characteristic vascular patterns in solid tumours: quantitative studies using corrosion casts Br J Cancer 80 5-6 1999 724 732
7. L.H. Gray, A.D. Conger, and M. Ebert The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy Br J Radiol 26 312 1953 638 648
8. P. Vaupel Tumor microenvironmental physiology and its implications for radiation oncology Semin Radiat Oncol 14 3 2004 198 206
9. R.K. Jain Barriers to drug delivery in solid tumors Sci Am 271 1 1994 58 65
10. J.S. Bedford, and J.B. Mitchell The effect of hypoxia on the growth and radiation response of mammalian cells in culture Br J Radiol 47 562 1974 687 696
11. R.E. Durand, and N.E. LePard Modulation of tumor hypoxia by conventional chemotherapeutic agents Int J Radiat Oncol Biol Phys 29 3 1994 481 486
12. K. Sakata, T.T. Kwok, and B.J. Murphy Hypoxia-induced drug resistance: comparison to P-glycoprotein-associated drug resistance Br J Cancer 64 5 1991 809 814
13. B.A. Teicher Hypoxia and drug resistance Cancer Metastasis Rev 13 2 1994 139 168
14. C. Grau, and J. Overgaard Effect of etoposide, carmustine, vincristine, 5-fluorouracil, or methotrexate on radiobiologically oxic and hypoxic cells in a C3H mouse mammary carcinoma in situ Cancer Chemother Pharmacol 30 4 1992 277 280
15. M. Hockel, K. Schlenger, and B. Aral Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix Cancer Res 56 19 1996 4509 4515
16. D.M. Brizel, S.P. Scully, and J.M. Harrelson Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma Cancer Res 56 5 1996 941 943
17. M. Hockel, and P. Vaupel Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects J Natl Cancer Inst 93 4 2001 266 276
18. 2 homeostasis by hypoxia-inducible factor 1 Annu Rev Cell Dev Biol 15 1999 551 578
19. J.F. O'Rourke, G.U. Dachs, and J.M. Gleadle Hypoxia response elements Oncol Res 9 6-7 1997 327 332
20. C.W. Pugh, J.F. O'Rourke, and M. Nagao Activation of hypoxia-inducible factor-1; definition of regulatory domains within the alpha subunit J Biol Chem 272 17 1997 11205 11214
21. P.H. Maxwell, M.S. Wiesener, and G.W. Chang The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis Nature 399 6733 1999 271 275
22. H. Zhong, A.M. De Marzo, and E. Laughner Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases Cancer Res 59 22 1999 5830 5835
23. G.L. Semenza HIF-1 and tumor progression: pathophysiology and therapeutics Trends Mol Med 8 Suppl. 4 2002 S62 S67
24. N.J. Beasley, R. Leek, and M. Alam 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 Res 62 9 2002 2493 2497
25. M. Volm, and R. Koomagi Hypoxia-inducible factor (HIF-1) and its relationship to apoptosis and proliferation in lung cancer Anticancer Res 20 3A 2000 1527 15233
26. T. Fillies, R. Werkmeister, and P.J. van Diest HIF1-alpha overexpression indicates a good prognosis in early stage squamous cell carcinomas of the oral floor BMC Cancer 5 1 2005 84
27. A.E. Greijer, and E. van der Wall The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis J Clin Pathol 57 10 2004 1009 1014
28. D.M. Aebersold, P. Burri, and K.T. Beer Expression of hypoxia-inducible factor-1alpha: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer Cancer Res 61 7 2001 2911 2916
29. M. Sohda, H. Ishikawa, and N. Masuda Pretreatment evaluation of combined HIF-1alpha, p53 and p21 expression is a useful and sensitive indicator of response to radiation and chemotherapy in esophageal cancer Int J Cancer 110 6 2004 838 844
30. P.H. Maxwell, C.W. Pugh, and P.J. Ratcliffe Activation of the HIF pathway in cancer Curr Opin Genet Dev 11 3 2001 293 299
31. J.W. Park, Y.S. Chun, and M.S. Kim Hypoxia-inducible factor 1-related diseases and prospective therapeutic tools J Pharmacol Sci 94 3 2004 221 232
32. N.J. Beasley, C.C. Wykoff, and P.H. Watson 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 Res 61 13 2001 5262 5267
33. E.A. Newsholme, and M. Board Application of metabolic-control logic to fuel utilization and its significance in tumor cells Adv Enzyme Regul 31 1991 225 246
34. G. Acs, P. Acs, and S.M. Beckwith Erythropoietin and erythropoietin receptor expression in human cancer Cancer Res 61 9 2001 3561 3565
35. H. Maeda, and T. Akaike Nitric oxide and oxygen radicals in infection, inflammation, and cancer Biochemistry (Mosc) 63 7 1998 854 865
36. J. Folkman What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82 1 1990 4 6
37. M.I. Koukourakis, A. Giatromanolaki, and E. Sivridis Hypoxia-activated tumor pathways of angiogenesis and pH regulation independent of anemia in head-and-neck cancer Int J Radiat Oncol Biol Phys 59 1 2004 67 71
38. K.L. Talks, H. Turley, and K.C. Gatter The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages Am J Pathol 157 2 2000 411 421
39. M. Ito, S. Tanaka, and S. Kim The specific expression of hypoxia inducible factor-1alpha in human gastric mucosa induced by nonsteroidal anti-inflammatory drugs Aliment Pharmacol Ther 18 Suppl. 1 2003 90 98
40. I.L. Szabo, H. Kawanaka, and M.K. Jones Activation of hypoxia inducible factor-1alpha in gastric mucosa in response to ethanol injury: a trigger for angiogenesis? Life Sci 69 25-26 2001 3035 3044
41. H. Brenner, V. Arndt, and C. Stegmaier Is Helicobacter pylori infection a necessary condition for noncardia gastric cancer? Am J Epidemiol 159 3 2004 252 258
42. M. Naumann, and J.E. Crabtree Helicobacter pylori-induced epithelial cell signalling in gastric carcinogenesis Trends Microbiol 12 1 2004 29 36
43. B. Obst, S. Wagner, and K.F. Sewing Helicobacter pylori causes DNA damage in gastric epithelial cells Carcinogenesis 21 6 2000 1111 1115
44. J.H. Park, T.Y. Kim, and H.S. Jong Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1alpha in gastric cancer cells Clin Cancer Res 9 1 2003 433 440
45. E.E. Mannick, L.E. Bravo, and G. Zarama Inducible nitric oxide synthase, nitrotyrosine, and apoptosis in Helicobacter pylori gastritis: effect of antibiotics and antioxidants Cancer Res 56 14 1996 3238 3243
46. B. Pignatelli, B. Bancel, and J. Esteve Inducible nitric oxide synthase, anti-oxidant enzymes and Helicobacter pylori infection in gastritis and gastric precancerous lesions in humans Eur J Cancer Prev 7 6 1998 439 447
47. E. Metzen, J. Zhou, and W. Jelkmann Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases Mol Biol Cell 14 8 2003 3470 3481
48. K. Akre, A.M. Ekstrom, and L.B. Signorello Aspirin and risk for gastric cancer: a population-based case-control study in Sweden Br J Cancer 84 7 2001 965 968
49. W.H. Wang, J.Q. Huang, and G.F. Zheng Non-steroidal anti-inflammatory drug use and the risk of gastric cancer: a systematic review and meta-analysis J Natl Cancer Inst 95 23 2003 1784 1791
50. H. Shi, J.M. Xu, and N.Z. Hu Prognostic significance of expression of cyclooxygenase-2 and vascular endothelial growth factor in human gastric carcinoma World J Gastroenterol 9 7 2003 1421 1426
51. X.H. Liu, A. Kirschenbaum, and M. Lu Prostaglandin E2 induces hypoxia-inducible factor-1alpha stabilization and nuclear localization in a human prostate cancer cell line J Biol Chem 277 51 2002 50081 50086
52. Y.Q. Wang, J.M. Luk, and K. Ikeda Regulatory role of vHL/HIF-1alpha in hypoxia-induced VEGF production in hepatic stellate cells Biochem Biophys Res Commun 317 2 2004 358 362
53. M.K. Jones, I.L. Szabo, and H. Kawanaka von Hippel Lindau tumor suppressor and HIF-1alpha: new targets of NSAIDs inhibition of hypoxia-induced angiogenesis FASEB J 16 2 2002 264 266
54. S.T. Palayoor, P.J. Tofilon, and C.N. Coleman Ibuprofen-mediated reduction of hypoxia-inducible factors HIF-1alpha and HIF-2alpha in prostate cancer cells Clin Cancer Res 9 8 2003 3150 3157
55. S.P. Huang, M.S. Wu, and C.T. Shun Cyclooxygenase-2 increases hypoxia-inducible factor-1 and vascular endothelial growth factor to promote angiogenesis in gastric carcinoma J Biomed Sci 12 1 2005 229 241
56. R. Takahashi, S. Tanaka, and T. Hiyama Hypoxia-inducible factor-1alpha expression and angiogenesis in gastrointestinal stromal tumor of the stomach Oncol Rep 10 4 2003 797 802
57. W.T. Chen, C.J. Huang, and M.T. Wu Hypoxia-inducible factor-1alpha is associated with risk of aggressive behavior and tumor angiogenesis in gastrointestinal stromal tumor Jpn J Clin Oncol 35 4 2005 207 213
58. L. Yang, L.G. Kuang, and H.C. Zheng PTEN encoding product: a marker for tumorigenesis and progression of gastric carcinoma World J Gastroenterol 9 1 2003 35 39
59. H.S. Lee, H.K. Lee, and H.S. Kim Tumour suppressor gene expression correlates with gastric cancer prognosis J Pathol 200 1 2003 39 46
60. J.I. Bardos, and M. Ashcroft Hypoxia-inducible factor-1 and oncogenic signalling Bioessays 26 3 2004 262 269
61. M. Leppilampi, J. Saarnio, and T.J. Karttunen Carbonic anhydrase isozymes IX and XII in gastric tumors World J Gastroenterol 9 7 2003 1398 1403
62. S. Pastorekova, S. Parkkila, and A.K. Parkkila Carbonic anhydrase IX, MN/CA IX: analysis of stomach complementary DNA sequence and expression in human and rat alimentary tracts Gastroenterology 112 2 1997 398 408
63. M.O. Gut, S. Parkkila, and Z. Vernerova Gastric hyperplasia in mice with targeted disruption of the carbonic anhydrase gene Car9 Gastroenterology 123 6 2002 1889 1903
64. J. Chen, C. Rocken, and J. Hoffmann Expression of carbonic anhydrase 9 at the invasion front of gastric cancers Gut 54 7 2005 920 927
65. Y. Noguchi, D. Marat, and A. Saito Expression of facilitative glucose transporters in gastric tumors Hepatogastroenterology 46 28 1999 2683 2689
66. W.S. Kim, Y.Y. Kim, and S.J. Jang Glucose transporter 1 (GLUT1) expression is associated with intestinal type of gastric carcinoma J Korean Med Sci 15 4 2000 420 424
67. T. Yamamoto, Y. Seino, and H. Fukumoto Over-expression of facilitative glucose transporter genes in human cancer Biochem Biophys Res Commun 170 1 1990 223 230
68. T. Kawamura, T. Kusakabe, and T. Sugino Expression of glucose transporter-1 in human gastric carcinoma: association with tumor aggressiveness, metastasis, and patient survival Cancer 92 3 2001 634 641
69. D. Ribatti, A. Marzullo, and B. Nico Erythropoietin as an angiogenic factor in gastric carcinoma Histopathology 42 3 2003 246 250
70. C.W. Feng, L.D. Wang, and L.H. Jiao Expression of p53, inducible nitric oxide synthase and vascular endothelial growth factor in gastric precancerous and cancerous lesions: correlation with clinical features BMC Cancer 2 1 2002 8
71. A. Rajnakova, S. Moochhala, and P.M. Goh Expression of nitric oxide synthase, cyclooxygenase, and p53 in different stages of human gastric cancer Cancer Lett 172 2 2001 177 185
72. Z.J. Song, P. Gong, and Y.E. Wu Relationship between the expression of iNOS, VEGF, tumor angiogenesis and gastric cancer World J Gastroenterol 8 4 2002 591 595
73. Z.Y. Song, S.Q. Wen, and J.P. Peng Significance of vascular endothelial growth factor expression and its correlation with inducible nitric oxide synthase in gastric cancer World J Gastroenterol 10 9 2004 1250 1255
74. C.J. van der Woude, J.H. Kleibeuker, and A.T. Tiebosch Diffuse and intestinal type gastric carcinomas differ in their expression of apoptosis related proteins J Clin Pathol 56 9 2003 699 702
75. D.H. Liu, X.Y. Zhang, and D.M. Fan Expression of vascular endothelial growth factor and its role in oncogenesis of human gastric carcinoma World J Gastroenterol 7 4 2001 500 505
76. K. Maeda, Y.S. Chung, and Y. Ogawa Prognostic value of vascular endothelial growth factor expression in gastric carcinoma Cancer 77 5 1996 858 863
77. K. Maeda, S.M. Kang, and N. Onoda Vascular endothelial growth factor expression in preoperative biopsy specimens correlates with disease recurrence in patients with early gastric carcinoma Cancer 86 4 1999 566 571
78. C. Fondevila, J.P. Metges, and J. Fuster p53 and VEGF expression are independent predictors of tumour recurrence and survival following curative resection of gastric cancer Br J Cancer 90 1 2004 206 215
79. J.R. Du, Y. Jiang, and Y.M. Zhang Vascular endothelial growth factor and microvascular density in esophageal and gastric carcinomas World J Gastroenterol 9 7 2003 1604 1606
80. M.I. Koukourakis, A. Giatromanolaki, and E. Sivridis Cancer vascularization: implications in radiotherapy? Int J Radiat Oncol Biol Phys 48 2 2000 545 553
81. G.L. Semenza Targeting HIF-1 for cancer therapy Nat Rev Cancer 3 10 2003 721 732
82. A. Unruh, A. Ressel, and H.G. Mohamed The hypoxia-inducible factor-1alpha is a negative factor for tumor therapy Oncogene 22 21 2003 3213 3220
83. E.J. Yeo, Y.S. Chun, and Y.S. Cho YC-1: a potential anticancer drug targeting hypoxia-inducible factor 1 J Natl Cancer Inst 95 7 2003 516 525
84. O. Stoeltzing, M.F. McCarty, and J.S. Wey Role of hypoxia-inducible factor 1alpha in gastric cancer cell growth, angiogenesis, and vessel maturation J Natl Cancer Inst 96 12 2004 946 956
85. S. Wen, C.P. Felley, and H. Bouzourene Inflammatory gene profiles in gastric mucosa during Helicobacter pylori infection in humans J Immunol 172 4 2004 2595 2606
86. Y. Hippo, H. Taniguchi, and S. Tsutsumi Global gene expression analysis of gastric cancer by oligonucleotide microarrays Cancer Res 62 1 2002 233 240
87. M.M. Weiss, E.J. Kuipers, and C. Postma Genome wide array comparative genomic hybridisation analysis of premalignant lesions of the stomach Mol Pathol 56 5 2003 293 298
88. J.P. Higgins, R. Shinghal, and H. Gill Gene expression patterns in renal cell carcinoma assessed by complementary DNA microarray Am J Pathol 162 3 2003 925 932
89. C. Gulmann, D. Butler, and E. Kay Biopsy of a biopsy: validation of immunoprofiling in gastric cancer biopsy tissue microarrays Histopathology 42 1 2003 70 76
90. R.L. Cowen, K.J. Williams, and E.C. Chinje Hypoxia targeted gene therapy to increase the efficacy of tirapazamine as an adjuvant to radiotherapy: reversing tumor radioresistance and effecting cure Cancer Res 64 4 2004 1396 1402
91. A. Rapisarda, B. Uranchimeg, and D.A. Scudiero Identification of small molecule inhibitors of hypoxia-inducible factor 1 transcriptional activation pathway Cancer Res 62 15 2002 4316 4324
92. N.J. Mabjeesh, D.E. Post, and M.T. Willard Geldanamycin induces degradation of hypoxia-inducible factor 1alpha protein via the proteosome pathway in prostate cancer cells Cancer Res 62 9 2002 2478 2482
93. M. Nordsmark, J. Loncaster, and C. Aquino-Parsons Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas Radiother Oncol 67 1 2003 35 44
94. C. Parker, M. Milosevic, and A. Toi Polarographic electrode study of tumor oxygenation in clinically localized prostate cancer Int J Radiat Oncol Biol Phys 58 3 2004 750 757
95. S.M. Evans, K.D. Judy, and I. Dunphy Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding Cancer Res 64 5 2004 1886 1892
96. C.J. Koch, and S.M. Evans Non-invasive PET and SPECT imaging of tissue hypoxia using isotopically labeled 2-nitroimidazoles Adv Exp Med Biol 510 2003 285 292
97. A. Giatromanolaki, M.I. Koukourakis, and E. Sivridis Relation of hypoxia inducible factor 1alpha and 2alpha in operable non-small cell lung cancer to angiogenic/molecular profile of tumours and survival Br J Cancer 85 6 2001 881 890
98. H.M. Sowter, R.R. Raval, and J.W. Moore Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia Cancer Res 63 19 2003 6130 6134
99. K. Kondo, J. Klco, and E. Nakamura Inhibition of HIF is necessary for tumor suppression by the von Hippel-Lindau protein Cancer Cell 1 3 2002 237 246
100. K. Tanimoto, K. Yoshiga, and H. Eguchi Hypoxia-inducible factor-1alpha polymorphisms associated with enhanced transactivation capacity, implying clinical significance Carcinogenesis 24 11 2003 1779 1783
101. E. Gothie, D.E. Richard, and E. Berra Identification of alternative spliced variants of human hypoxia-inducible factor-1alpha J Biol Chem 275 10 2000 6922 6927
102. M.A. Maynard, H. Qi, and J. Chung Multiple splice variants of the human HIF-3alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex J Biol Chem 278 13 2003 11032 11040
103. P. Korkolopoulou, E. Patsouris, and A.E. Konstantinidou Hypoxia-inducible factor 1alpha/vascular endothelial growth factor axis in astrocytomas. Associations with microvessel morphometry, proliferation and prognosis Neuropathol Appl Neurobiol 30 3 2004 267 278
104. V.E. Theodoropoulos, A. Lazaris, and F. Sofras Hypoxia-inducible factor 1alpha expression correlates with angiogenesis and unfavorable prognosis in bladder cancer Eur Urol 46 2 2004 200 208
105. V.E. Theodoropoulos, A.C. Lazaris, and I. Kastriotis Evaluation of hypoxia-inducible factor 1alpha overexpression as a predictor of tumour recurrence and progression in superficial urothelial bladder carcinoma BJU Int 95 3 2005 425 431
106. M. Schindl, S.F. Schoppmann, and H. Samonigg Overexpression of hypoxia-inducible factor 1alpha is associated with an unfavorable prognosis in lymph node-positive breast cancer Clin Cancer Res 8 6 2002 1831 1837
107. G. Gruber, R.H. Greiner, and R. Hlushchuk Hypoxia-inducible factor 1alpha in high-risk breast cancer: an independent prognostic parameter? Breast Cancer Res 6 3 2004 R191 R198
108. R. Bos, P. van der Groep, and A.E. Greijer Levels of hypoxia-inducible factor-1alpha independently predict prognosis in patients with lymph node negative breast carcinoma Cancer 97 6 2003 1573 1581
109. J.P. Dales, S. Garcia, and S. Meunier-Carpentier Overexpression of hypoxia-inducible factor HIF-1alpha predicts early relapse in breast cancer: retrospective study in a series of 745 patients Int J Cancer 116 5 2005 734 739
110. P. Burri, V. Djonov, and D.M. Aebersold Significant correlation of hypoxia-inducible factor-1alpha with treatment outcome in cervical cancer treated with radical radiotherapy Int J Radiat Oncol Biol Phys 56 2 2003 494 501
111. P. Birner, M. Schindl, and A. Obermair Overexpression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer Cancer Res 60 17 2000 4693 4696
112. H.K. Haugland, V. Vukovic, and M. Pintilie Expression of hypoxia-inducible factor-1alpha in cervical carcinomas: correlation with tumor oxygenation Int J Radiat Oncol Biol Phys 53 4 2002 854 861
113. G.J. Hutchison, H.R. Valentine, and J.A. Loncaster 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 Clin Cancer Res 10 24 2004 8405 8412
114. A. Mayer, A. Wree, and M. Hockel 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 Res 64 16 2004 5876 5881
115. T. Kuwai, Y. Kitadai, and S. Tanaka Expression of hypoxia-inducible factor-1alpha is associated with tumor vascularization in human colorectal carcinoma Int J Cancer 105 2 2003 176 181
116. H. Yoshimura, D.K. Dhar, and H. Kohno Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression Clin Cancer Res 10 24 2004 8554 8560
117. E. Sivridis, A. Giatromanolaki, and K.C. Gatter Association of hypoxia-inducible factors 1alpha and 2alpha with activated angiogenic pathways and prognosis in patients with endometrial carcinoma Cancer 95 5 2002 1055 1063
118. M.I. Koukourakis, A. Giatromanolaki, and E. Sivridis Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer Int J Radiat Oncol Biol Phys 53 5 2002 1192 1202
119. S. Kimura, Y. Kitadai, and S. Tanaka Expression of hypoxia-inducible factor (HIF)-1alpha is associated with vascular endothelial growth factor expression and tumour angiogenesis in human oesophageal squamous cell carcinoma Eur J Cancer 40 12 2004 1904 1912
120. M.I. Koukourakis, A. Giatromanolaki, and J. Skarlatos Hypoxia inducible factor (HIF-1α and HIF-2α) expression in early esophageal cancer and response to photodynamic therapy and radiotherapy Cancer Res 61 5 2001 1830 1832
121. T. Kurokawa, M. Miyamoto, and K. Kato Overexpression of hypoxia-inducible-factor 1alpha(HIF-1alpha) in oesophageal squamous cell carcinoma correlates with lymph node metastasis and pathologic stage Br J Cancer 89 6 2003 1042 1047
122. P. Birner, B. Gatterbauer, and G. Oberhuber Expression of hypoxia-inducible factor-1alpha in oligodendrogliomas: its impact on prognosis and on neoangiogenesis Cancer 92 1 2001 165 171
123. P. Birner, M. Schindl, and A. Obermair Expression of hypoxia-inducible factor 1alpha in epithelial ovarian tumors: its impact on prognosis and on response to chemotherapy Clin Cancer Res 7 6 2001 1661 1668
124. E.P. Hui, A.T. Chan, and F. Pezzella Coexpression of hypoxia-inducible factors 1alpha and 2alpha, carbonic anhydrase IX, and vascular endothelial growth factor in nasopharyngeal carcinoma and relationship to survival Clin Cancer Res 8 8 2002 2595 2604
125. K. Nakanishi, S. Hiroi, and S. Tominaga Expression of hypoxia-inducible factor-1alpha protein predicts survival in patients with transitional cell carcinoma of the upper urinary tract Clin Cancer Res 11 7 2005 2583 2590
126. T. Ichikura, S. Tomimatsu, and E. Ohkura Prognostic significance of the expression of vascular endothelial growth factor (VEGF) and VEGF-C in gastric carcinoma J Surg Oncol 78 2 2001 132 137