Endogenous hypoxia markers in locally advanced cancers of the uterine cervix: Reality or wishful thinking?

Strahlentherapie und Onkologie

Volumn 182, Issue 9, 2006, Pages 501-510

  Mayer, Arnulf ^a   Höckel, Michael ^b   Vaupel, Peter ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Carbonic anhydrase IX; Glucose transporter 1; Hypoxia marker; Hypoxia inducible factor 1 ; Oxygenation status; Tumor hypoxia

Indexed keywords

BIOCHEMICAL MARKER; CARBONATE DEHYDRATASE IX; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ADVANCED CANCER; CANCER CELL; GENE TARGETING; HUMAN; HYPOXIA; PROTEIN EXPRESSION; REVIEW; TISSUE OXYGENATION; UTERINE CERVIX CANCER;

BIOLOGICAL MARKERS; BIOPSY; CARBONIC ANHYDRASES; CELL HYPOXIA; CERVIX UTERI; DIAGNOSIS, DIFFERENTIAL; FEMALE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; OXYGEN; PROGNOSIS; UTERINE CERVICAL NEOPLASMS;

EID: 33748199697     PISSN: 01797158     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00066-006-1525-9     Document Type: Review

References (115)

1. Aebersold DM, Burri P, Beer KT, et al. Expression of hypoxia-inducible factor-1α: a novel predictive and prognostic parameter in the radiotherapy of oropharyngeal cancer. Cancer Res 2001;61:2911-6.
2. Airley R, Loncaster J, Davidson S, et al. Glucose transporter Glut-1 expression correlates with tumor hypoxia and predicts metastasis-free survival in advanced carcinoma of the cervix. Clin Cancer Res 2001;7:928-34.
3. Airley RE, Loncaster J, Raleigh JA, et al. GLUT-1 and CA IX as intrinsic markers of hypoxia in carcinoma of the cervix: relationship to pimonidazole binding. Int J Cancer 2003;104:85-91.
4. Bachtiary B, Schindl M, Potter R, et al. Overexpression of hypoxia-inducible factor 1α indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clin Cancer Res 2003;9:2234-40.
5. Barnes K, Ingram JC, Porras OH, et al. Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK). J Cell Sci 2002;115:2433-42.
6. Boado RJ, Pardridge WM. Glucose deprivation and hypoxia increase the expression of the GLUT1 glucose transporter via a specific mRNA cis-acting regulatory element. J Neurochem 2002;80:552-4.
7. Brizel DM, Sibley GS, Prosnitz LR, et al. Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 1997;38:285-9.
8. Brugarolas J, Kaelin WG Jr. Dysregulation of HIF and VEGF is a unifying feature of the familial hamartoma syndromes. Cancer Cell 2004;6:7-10.
9. Burri P, Djonov V, Aebersold DM, et al. Significant correlation of hypoxia-inducible factor-1α with treatment outcome in cervical cancer treated with radical radiotherapy. Int J Radiat Oncol Biol Phys 2003;56:494-501.
10. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 2001;61:8903-8.
11. Catrina SB, Okamoto K, Pereira T, et al. Hyperglycemia regulates hypoxia-inducible factor-1α protein stability and function. Diabetes 2004;53:3226-32.
12. Chrastina A. High cell density-mediated pericellular hypoxia is a crucial factor inducing expression of the intrinsic hypoxia marker CA IX in vitro in HeLa cells. Neoplasma 2003;50:251-6.
13. Comerford KM, Wallace TJ, Karhausen J, et al. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res 2002;62:3387-94.
14. Coquelle A, Toledo F, Stern S, et al. A new role for hypoxia in tumor progression: induction of fragile site triggering genomic rearrangements and formation of complex DMs and HSRs. Mol Cell 1998;2:259-65.
15. Dunst J. Management of anemia in patients undergoing curative radiotherapy. Erythropoietin, transfusions, or better nothing? Strahlenther Onkol 2004;180:671-81.
16. Evans SM, Judy KD, Dunphy I, et al. Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res 2004;64:1886-92.
17. Feldser D, Agani F, Iyer NV, et al. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res 1999;59:3915-8.
18. Fu XS, Choi E, Bubley GJ, et al. Identification of hypoxia-inducible factor-1α (HIF-1α) polymorphism as a mutation in prostate cancer that prevents normoxia-induced degradation. Prostate 2005;63:215-21.
19. Fukuda R, Hirota K, Fan F, et al. 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 2002;277:38205-11.
20. Fyles AW, Milosevic M, Wong R, et al. Oxygenation predicts radiation response and survival in patients with cervix cancer. Radiother Oncol 1998;48:149-56.
21. 18F]-2-fluoro-27prime;-deoxyglucose). An appraisal of radiotherapeutically relevant hypoxia. Strahlenther Onkol 2004;180:616-22.
22. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001;15:807-26.
23. Graeber TG, Osmanian C, Jacks T, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996;379:88-91.
24. Gray LH, Conger AD, Ebert M, et al. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br J Radiol 1953;26:638-48.
25. Hänsgen G, Holzapfel D, Bache M, et al. Hif-1-alpha-expression and its relationship to tumour oxygenation, hemoglobin level and its impact as a prognostic marker in patients with advanced cervical carcinoma. Strahlenther Onkol 2005;181 (Sondernr 1):77.
26. Haugland HK, Vukovic V, Pintilie M, et al. Expression of hypoxia-inducible factor-1α in cervical carcinomas: correlation with tumor oxygenation. Int J Radiat Oncol Biol Phys 2002;53:854-61.
27. Hedley D, Pintilie M, Woo J, et al. Carbonic anhydrase IX expression, hypoxia, and prognosis in patients with uterine cervical carcinomas. Clin Cancer Res 2003;9:5666-74.
28. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 1997;3:177-82.
29. Höckel M, Schlenger K, Aral B, et al. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 1996;56:4509-15.
30. Höckel M, Schlenger K, Höckel S, et al. Hypoxic cervical cancers with low apoptotic index are highly aggressive. Cancer Res 1999;59:4525-8.
31. 2 tension measurements. Cancer Res 1991;51:6098-102.
32. Höckel M, Vorndran B, Schlenger K, et al. Tumor oxygenation: a new predictive parameter in locally advanced cancer of the uterine cervix. Gynecol Oncol 1993;51:141-9.
33. Hoogsteen IJ, Marres HA, Wijffels KI, et al. Co-localization of carbonic anhydrase 9 expression and cell proliferation in human head and neck squamous cell carcinoma. Clin Cancer Res 2005;11:97-106.
34. Hoskin PJ, Sibtain A, Daley FM, et al. GLUT1 and CA IX as intrinsic markers of hypoxia in bladder cancer: relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer 2003;89:1290-7.
35. Hutchison GJ, Valentine HR, Loncaster JA, et al. Hypoxia-inducible factor 1α 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 2004;10:8405-12.
36. Hwang DY, Ismail-Beigi F. Stimulation of GLUT-1 glucose transporter expression in response to hyperosmolarity. Am J Physiol Cell Physiol 2001;281:C1365-72.
37. 2 sensing. Science 2001;292:464-8.
38. 2-regulated prolyl hydroxylation. Science 2001;292:468-72.
39. Jankovic B, Aquino-Parsons C, Raleigh JA, et al. Comparison between pimonidazole binding, oxygen electrode measurements, and expression of endogenous hypoxia markers in cancer of the uterine cervix. Cytometry B Clin Cytom 2006;70:45-55.
40. Janssen HL, Haustermans KM, Sprong D, et al. HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. Int J Radiat Oncol Biol Phys 2002;54:1537-49.
41. Jewell UR, Kvietikova I, Scheid A, et al. Induction of HIF-1α in response to hypoxia is instantaneous. FASEB J 2001;15:1312-4.
42. 2 tension. Am J Physiol 1996;271:C1172-80.
43. Kaanders JHAM, Wijffels KIEM, Marres HAM, et al. Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Res 2002;62:7066-74.
44. Kabuubi P, Loncaster JA, Davidson SE, et al. No relationship between thymidine phosphorylase (TP, PD-ECGF) expression and hypoxia in carcinoma of the cervix. Br J Cancer 2006;94:115-20.
45. 2-histography. Int J Radiat Oncol Biol Phys 1990;19:953-61.
46. Kaluz S, Kaluzova M, Chrastina A, et al. Lowered oxygen tension induces expression of the hypoxia marker MN/carbonic anhydrase IX in the absence of hypoxia-inducible factor 1α stabilization: a role for phosphatidylinositol 3′-kinase. Cancer Res 2002;62:4469-77.
47. Kavanagh MC, Tsang V, Chow S, et al. A comparison in individual murine tumors of techniques for measuring oxygen levels. Int J Radiat Oncol Biol Phys 1999;44:1137-46.
48. Kim WY, Kaelin WG. Role of VHL gene mutation in human cancer. J Clin Oncol 2004;22:4991-5004.
49. Kinoshita M, Johnson DL, Shatney CH, et al. Cancer cells surviving hypoxia obtain hypoxia resistance and maintain anti-apoptotic potential under reoxygenation. Int J Cancer 2001;91:322-6.
50. Koivunen P, Hirsila M, Gunzler V, et al. Catalytic properties of the asparaginyl hydroxylase (FIH) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases. J Biol Chem 2004;279:9899-904.
51. Kondo A, Safaei R, Mishima M, et al. Hypoxia-induced enrichment and mutagenesis of cells that have lost DNA mismatch repair. Cancer Res 2001;61:7603-7.
52. Krishnamachary B, Berg-Dixon S, Kelly B, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 2003;63:1138-43.
53. Kwon SJ, Lee YJ. Effect of low glutamine/glucose on hypoxia-induced elevation of hypoxia-inducible factor-1α in human pancreatic cancer MiaPa-Ca-2 and human prostatic cancer DU-145 cells. Clin Cancer Res 2005;11:4694-700.
54. Lal A, Peters H, St Croix B, et al. Transcriptional response to hypoxia in human tumors. J Natl Cancer Inst 2001;93:1337-43.
55. Lando D, Peet DJ, Gorman JJ, et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 2002;16:1466-71.
56. Lando D, Peet DJ, Whelan DA, et al. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 2002;295:858-61.
57. Loncaster JA, Harris AL, Davidson SE, et al. 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 Res 2001;61:6394-9.
58. Lyng H, Sundfor K, Rofstad EK. Oxygen tension in human tumours measured with polarographic needle electrodes and its relationship to vascular density, necrosis and hypoxia. Radiother Oncol 1997;44:163-9.
59. Mandriota SJ, Turner KJ, Davies DR, et al. HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell 2002;1:459-68.
60. Maxwell PH, Wiesener MS, Chang GW, et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999;399:271-5.
61. Mayer A, Höckel M, Vaupel P. Carbonic anhydrase IX expression and tumor oxygenation status do not correlate at the microregional level in locally advanced cancers of the uterine cervix. Clin Cancer Res 2005;11:7220-5.
62. Mayer A, Höckel M, Wree A, et al. Microregional expression of glucose transporter-1 and oxygenation status: lack of correlation in locally advanced cervical cancers. Clin Cancer Res 2005;11:2768-73.
63. Mayer A, Wree A, Höckel M, et al. Lack of correlation between expression of HIF-1α protein and oxygenation status in identical tissue areas of squamous cell carcinomas of the uterine cervix. Cancer Res 2004;64:5876-81.
64. Mekhail K, Gunaratnam L, Bonicalzi ME, et al. HIF activation by pH-dependent nucleolar sequestration of VHL. Nat Cell Biol 2004;6:642-7.
65. Möller LC, Dumitrescu AM, Refetoff S. Cytosolic action of thyroid hormone leads to induction of HIF-1α and glycolytic genes. Mol Endocrinol 2005;90:936-43.
66. Nordsmark M, Alsner J, Keller J, et al. Hypoxia in human soft tissue sarcomas: adverse impact on survival and no association with p53 mutations. Br J Cancer 2001;84:1070-5.
67. Nordsmark M, Bentzen SM, Rudat V, et al. Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother Oncol 2005;77:18-24.
68. Nordsmark M, Loncaster J, Aquino-Parsons C, et al. Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas. Radiother Oncol 2003;67:35-44.
69. Nordsmark M, Loncaster J, Chou SC, et al. Invasive oxygen measurements and pimonidazole labeling in human cervix carcinoma. Int J Radiat Oncol Biol Phys 2001;49:581-6.
70. Nordsmark M, Overgaard J. Tumor hypoxia is independent of hemoglobin and prognostic for loco-regional tumor control after primary radiotherapy in advanced head and neck cancer. Acta Oncol 2004;43:396-403.
71. Olive PL, Aquino-Parsons C, MacPhail SH, et al. Carbonic anhydrase 9 as an endogenous marker for hypoxic cells in cervical cancer. Cancer Res 2001;61:8924-9.
72. Osthus RC, Shim H, Kim S, et al. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 2000;275:21797-800.
73. Page EL, Robitaille GA, Pouyssegur J, et al. Induction of hypoxia-inducible factor-1α by transcriptional and translational mechanisms. J Biol Chem 2002;277:48403-9.
74. Pastorek J, Pastorekova S, Callebaut I, et al. Cloning and characterization of MN, a human tumor-associated protein with a domain homologous to carbonic anhydrase and a putative helix-loop-helix DNA binding segment. Oncogene 1994;9:2877-88.
75. Pennacchietti S, Michieli P, Galluzzo M, et al. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-61.
76. Potter CP, Harris AL. Diagnostic, prognostic and therapeutic implications of carbonic anhydrases in cancer. Br J Cancer 2003;89:2-7.
77. Rafajova M, Zatovicova M, Kettmann R, et al. Induction by hypoxia combined with low glucose or low bicarbonate and high posttranslational stability upon reoxygenation contribute to carbonic anhydrase IX expression in cancer cells. Int J Oncol 2004;24:995-1004.
78. Ravi R, Mookerjee B, Bhujwalla ZM, et al. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev 2000;14:34-44.
79. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment. Cancer Res 1996;56:5754-7.
80. Rice GC, Hoy C, Schimke RT. Transient hypoxia enhances the frequency of dihydrofolate reductase gene amplification in Chinese hamster ovary cells. Proc Natl Acad Sci U S A 1986;83:5978-82.
81. Richard DE, Berra E, Gothie E, et al. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1α (HIF-1α) and enhance the transcriptional activity of HIF-1. J Biol Chem 1999;274:32631-7.
82. Rofstad EK, Rasmussen H, Galappathi K, et al. Hypoxia promotes lymph node metastasis in human melanoma xenografts by up-regulating the urokinase-type plasminogen activator receptor. Cancer Res 2002;62:1847-53.
83. Saarnio J, Parkkila S, Parkkila AK, et al. Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation. Am J Pathol 1998;153:279-85.
84. Sang N, Stiehl DP, Bohensky J, et al. MAPK signaling up-regulates the activity of hypoxia-inducible factors by its effects on p300. J Biol Chem 2003; 278:14013-9.
85. Saramaki OR, Savinainen KJ, Nupponen NN, et al. Amplification of hypoxia-inducible factor 1α gene in prostate cancer. Cancer Genet Cytogenet 2001;128:31-4.
86. Schmaltz C, Hardenbergh PH, Wells A, et al. Regulation of proliferation-survival decisions during tumor cell hypoxia. Mol Cell Biol 1998;18:2845-54.
87. Schreiber A, Krause M, Zips D, et al. Effect of the hypoxic cell sensitizer isometronidazole on local control of two human squamous cell carcinomas after fractionated irradiation. Strahlenther Onkol 2004;180:375-82.
88. Schroeder T, Yuan H, Viglianti BL, et al. Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res 2005;65:5163-71.
89. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
90. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 2004;19:176-82.
91. Shweiki D, Neeman M, Itin A, et al. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci USA 1995;92:768-72.
92. Stein I, Neeman M, Shweiki D, et al. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol Cell Biol 1995;15:5363-8.
93. Sundfør K, Lyng H, Rofstad EK. Tumour hypoxia and vascular density as predictors of metastasis in squamous cell carcinoma of the uterine cervix. Br J Cancer 1998;78:822-7.
94. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449-65.
95. Vaupel P, Mayer A, Höckel M. Tumor hypoxia and malignant progression. Methods Enzymol 2004;381:335-54.
96. Vaupel P, Mayer A, Höckel M. Impact of hemoglobin levels on tumor oxygenation: the higher, the better? Strahlenther Onkol 2006;182:63-71.
97. 2 tension measurements. Cancer Res 1991;51:3316-22.
98. Vleugel MM, Bos R, Buerger H, et al. No amplifications of hypoxia-inducible factor-1α gene in invasive breast cancer: a tissue microarray study. Cell Oncol 2004;26:347-51.
99. Vordermark D, Brown JM. Endogenous markers of tumor hypoxia predictors of clinical radiation resistance? Strahlenther Onkol 2003;179:801-11.
100. Vordermark D, Kaffer A, Riedl S, et al. Characterization of carbonic anhydrase IX (CA IX) as an endogenous marker of chronic hypoxia in live human tumor cells. Int J Radiat Oncol Biol Phys 2005;61:1197-207.
101. Vordermark D, Katzer A, Baier K, et al. Cell type-specific association of hypoxia-inducible factor-1α (HIF-1α) protein accumulation and radiobiologic tumor hypoxia. Int J Radiat Oncol Biol Phys 2004;58:1242-50.
102. Vukovic V, Haugland HK, Nicklee T, et al. Hypoxia-inducible factor-1α is an intrinsic marker for hypoxia in cervical cancer xenografts. Cancer Res 2001;61:7394-8.
103. Walenta S, Mueller-Klieser WF. Lactate: mirror and motor of tumor malignancy. Semin Radiat Oncol 2004;14:267-74.
104. Walenta S, Wetterling M, Lehrke M, et al. High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers. Cancer Res 2000;60:916-21.
105. 2 tension. Proc Natl Acad Sci USA 1995;92:5510-4.
106. Weitmann HD, Gustorff B, Vaupel P, et al. Oxygenation status of cervical carcinomas before and during spinal anesthesia for application of brachytherapy. Strahlenther Onkol 2003;179:633-40.
107. Weitmann HD, Knocke TH, Czembirek C, et al. Prognostische Faktoren für die primäre Radiotherapie des Zervixkarzinoms. Strahlenther Onkol 2005; 181 (Sondernr 1):17.
108. Wertheimer E, Sasson S, Cerasi E, et al. The ubiquitous glucose transporter GLUT-1 belongs to the glucose-regulated protein family of stress-inducible proteins. Proc Natl Acad Sci USA 1991;88:2525-9.
109. West CM, Cooper RA, Loncaster JA, et al. Tumor vascularity: a histological measure of angiogenesis and hypoxia. Cancer Res 2001;61:2907-10.
110. Wong RK, Fyles A, Milosevic M, et al. Heterogeneity of polarographic oxygen tension measurements in cervix cancer: an evaluation of within and between tumor variability, probe position, and track depth. Int J Radiat Oncol Biol Phys 1997;39:405-12.
111. Wykoff CC, Beasley NJ, Watson PH, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000;60:7075-83.
112. Young SD, Marshall RS, Hill RP. Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc Natl Acad Sci USA 1988;85:9533-7.
113. Yuan J, Narayanan L, Rockwell S, et al. Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Res 2000;60:4372-6.
114. Zhong H, De Marzo AM, Laughner E, et al. Overexpression of hypoxia-inducible factor 1α in common human cancers and their metastases. Cancer Res 1999;59:5830-5.
115. Zips D, Adam M, Flentje M, et al. Impact of hypoxia and the metabolic microenvironment on radiotherapy of solid tumors. Introduction of a multi-institutional research project. Strahlenther Onkol 2004;180:609-15.