Acute Hypoxia Enhances Spontaneous Lymph Node Metastasis in an Orthotopic Murine Model of Human Cervical Carcinoma

Cancer Research

Volumn 64, Issue 6, 2004, Pages 2054-2061

  Cairns, Rob A ^a,b   Hill, Richard P ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 NITRO 1H IMIDAZOL 1 YL) N (2,2,3,3,3 PENTAFLUOROPROPYL)ACETAMIDE; CD31 ANTIGEN; CELL PROTEIN; PROTEIN DSRED2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE MARKER; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GROWTH RATE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LUNG METASTASIS; LYMPH NODE METASTASIS; OPTICAL INSTRUMENTATION; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; UTERINE CERVIX CARCINOMA;

ANIMALS; ANOXIA; DISEASE MODELS, ANIMAL; ETANIDAZOLE; FEMALE; HUMANS; HYDROCARBONS, FLUORINATED; INDICATORS AND REAGENTS; LUMINESCENT PROTEINS; LUNG NEOPLASMS; LYMPH NODES; LYMPHATIC METASTASIS; MICE; MICE, SCID; MICROCIRCULATION; MICROSCOPY, FLUORESCENCE; OXYGEN; UTERINE CERVICAL NEOPLASMS;

EID: 1542405875     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-3196     Document Type: Article

References (60)

1. Brizel DM, Dodge RK, Clough RW, Dewhirst MW. Oxygenation of head and neck cancer: changes during radiotherapy and impact on treatment outcome, Radiother Oncol 1999;53:113-7.
2. Brizel DM, Scully SP, Harrelson JM, Layfield LJ, Bean JM, Prosnitz LR, Dewhirst MW. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma, Cancer Res 1996;56:941-3.
3. Nordsmark M, Overgaard J A confirmatory prognostic study on oxygenation status and loco-regional control in advanced head and neck squamous cell carcinoma treated by radiation therapy, Radiother Oncol 2000;57:39-43.
4. Rofstad EK, Sundfor K, Lyng H, Trope CG. Hypoxia-induced treatment failure in advanced squamous cell carcinoma of the uterine cervix is primarily due to hypoxia-induced radiation resistance rather than hypoxia-induced metastasis, Br J Cancer 2000;83:354-9.
5. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P. Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix, Cancer Res 1996;56:4509-15.
6. Vaupel P, Schlenger K, Knoop C, Hockel M. Oxygenation of human tumors: evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements, Cancer Res 1991;51:3316-22.
7. Fyles A, Milosevic M, Hedley D, Pintilie M, Levin W, Manchul L, Hill RP. Tumor hypoxia has independent predictor impact only in patients with node-negative cervix cancer, J Clin Oncol 2002;20:680-7.
8. Dewhirst MW. Concepts of oxygen transport at the microcirculatory level, Semin Radiat Oncol 1998;8:143-50.
9. Gulledge CJ, Dewhirst MW. Tumor oxygenation: a matter of supply and demand, Anticancer Res 1996;16:741-9.
10. Dewhirst MW, Ong ET, Braun RD, Smith B, Klitzman B, Evans SM, Wilson D. Quantification of longitudinal tissue pO2 gradients in window chamber tumours: impact on tumour hypoxia, Br J Cancer 1999;79:1717-22.
11. Durand RE, Aquino-Parsons C. Clinical relevance of intermittent tumour blood flow, Acta Oncol 2001;40:929-36.
12. Kimura H, Braun RD, Ong ET, Hsu R, Secomb TW, Papahadjopoulos D, Hong K, Dewhirst MW. Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma, Cancer Res 1996;56: 5522-8.
13. Chaplin DJ, Hill SA. Temporal heterogeneity in microregional erythrocyte flux in experimental solid tumours, Br J Cancer 1995;71:1210-3.
14. Hill SA, Chaplin DJ. Detection of microregional fluctuations in erythrocyte flow using laser Doppler microprobes, Adv Exp Med Biol 1996;388:367-71.
15. Rofstad EK, Maseide K. Radiobiological and immunohistochemical assessment of hypoxia in human melanoma xenografts: acute and chronic hypoxia in individual tumours, Int J Radiat Biol 1999;75:1377-93.
16. Biurberg KG, Graff BA, Rofstad EK. Temporal heterogeneity in oxygen tension in human melanoma xenografts, Br J Cancer 2003;89:350-6.
17. Bennewith KL, Raleigh JA, Durand RE. Orally administered pimonidazole to label hypoxic tumor cells, Cancer Res 2002;62:6827-30.
18. Mollica F, Jain RK, Netti PA. A model for temporal heterogeneities of tumor blood flow, Microvasc Res 2003;65:56-60.
19. Pirson G, Fyles A, Milosevic M, Wylie J, Pintilie M, Hill RP. Tumor size and oxygenation are independent predictors of nodal diseases in patients with cervix cancer, Int J Radiat Oncol Biol Phys 2001;51:699-703.
20. Sundfor 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.
21. Kolstad P. Intercapillary distance, oxygen tension and local recurrence in cervix cancer, Scand J Clin Lab Investig Suppl 1968;106:145-57.
22. Tjalma W, Van Marck E, Weyler J, Dirix L, Van Daele A, Goovaerts G, Albertyn G, van Dam P. Quantification and prognostic relevance of angiogenic parameters in invasive cervical cancer, Br J Cancer 1998;78:170-4.
23. Cooper RA, Wilks DP, Logue JP, Davidson SE, Hunter RD, Roberts SA, West CM. High tumor angiogenesis is associated with poorer survival in carcinoma of the cervix treated with radiotherapy, Clin Cancer Res 1998;4:2795-800.
24. Revesz L, Siracka E, Siracky J, Delides G, Pavlaki K. Variation of vascular density within and between tumors of the uterine cervix and its predictive value for radiotherapy, Int J Radiat Oncol Biol Phys 1989;16:1161-3.
25. Awwad HK, el Naggar M, Mocktar N, Barsoum M. Intercapillary distance measurement as an indicator of hypoxia in carcinoma of the cervix uteri, Int J Radiat Oncol Biol Phys 1986;12:1329-33.
26. West CM, Cooper RA, Loncaster JA, Wilks DP, Bromley M. Tumor vascularity: a histological measure of angiogenesis and hypoxia, Cancer Res 2001;61:2907-10.
27. Schlenger K, Hockel M, Mitze M, Schaffer U, Weikel W, Knapstein PG, Lambert A. Tumor vascularity-a novel prognostic factor in advanced cervical carcinoma, Gynecol Oncol 1995;59:57-66.
28. Kaanders JH, Wijffels KI, Marres HA, Ljungkvist AS, Pop LA, van den Hoogen FJ, de Wilde PC, Bussink J, Raleigh JA, van der Kogel AJ. Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer, Cancer Res 2002;62:7066-74.
29. Rofstad EK. Microenvironment-induced cancer metastasis, Int J Radiat Biol 2000; 76:589-605.
30. Subarsky P, Hill RP. The hypoxic tumor microenvironment and metastatic progression, Clin Exp Metastasis 2003;20:237-50.
31. Rofstad EK, Danielsen T. Hypoxia-induced metastasis of human melanoma cells: involvement of vascular endothelial growth factor-mediated angiogenesis, Br J Cancer 1999;80:1697-707.
32. 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.
33. Young SD, Hill RP. Effects of reoxygenation on cells from hypoxic regions of solid tumors: anticancer drug sensitivity and metastatic potential, J Natl Cancer Inst (Bethesda) 1990;82:371-80.
34. Stackpole CW, Groszek L, Kalbag SS. Benign-to-malignant B16 melanoma progression induced in two stages in vitro by exposure to hypoxia, J Natl Cancer Inst (Bethesda) 1994;86:361-7.
35. Rofstad EK, Rasmussen H, Galappathi K, Mathiesen B, Nilsen K, Graff BA. Hypoxia promotes lymph node metastasis in human melanoma xenografts by up-regulating the urokinase-type plasminogen activator receptor, Cancer Res 2002;62:1847-53.
36. De Jaeger K, Kavanagh, M-C and Hill RP. Relationship of hypoxia to metastatic ability in rodent tumors, Br J Cancer 2001;84:1280-5.
37. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors, Cancer Res 2001;61:8903-8.
38. Evans SM, Joiner B, Jenkins WT, Laughlin KM, Lord EM, Koch CJ. Identification of hypoxia in cells and tissues of epigastric 9L rat glioma using EF5 [2-(2-nitro-1H-imidazol-lyl)-N-(2,2,3,3,3-pentafluoropropyl)acetamide], Br J Cancer 1995;72: 875-82.
39. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. Hypoxia-inducible expression of tumor-associated carbonic anhydrases, Cancer Res 2000;60: 7075-83.
40. Fyles AW, Pintilie M, Kirkbride P, Levin W, Manchul LA, Rawlings GA. Prognostic factors in patients with cervix cancer treated by radiation therapy: results of a multiple regression analysis, Radiother Oncol 1995;35:107-17.
41. Lal A, Peters H, St. Croix B, Haroon ZA, Dewhirst MW, Strausberg RL, Kaanders JH, van der Kogel AJ, Riggins GJ. Transcriptional response to hypoxia in human tumors, J Natl Cancer Inst (Bethesda) 2001;93:1337-43.
42. Wong RK, Fyles A, Milosevic M, Pintilie M, Hill RP. 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.
43. Olive PL, Banath JP, Aquino-Parsons C. Measuring hypoxia in solid tumours-is there a gold standard? Acta Oncol 2001;40:917-23.
44. Jenkins WT, Evans SM, Koch CJ. Hypoxia and necrosis in rat 9L glioma and Morris 7777 hepatoma tumors: comparative measurements using EF5 binding and the Eppendorf needle electrode, Int J Radiat Oncol Biol Phys 2000;46:1005-17.
45. Nordsmark M, Loncaster J, Aquino-Parsons C, Chou SC, Ladekarl M, Havsteen H, Lindegaard JC, Davidson SE, Varia M, West C, Hunter R, Overgaard J, Raleigh JA. Measurements of hypoxia using pimonidazole and polarographic oxygen-sensitive electrodes in human cervix carcinomas, Radiother Oncol 2003;67:35-44.
46. Denko N, Wernke-Dollries K, Johnson AB, Hammond E, Chiang CM, Barton MC. Hypoxia actively represses transcription by inducing negative cofactor 2 (Dr1/DrAP1) and blocking preinitiation complex assembly, J Biol Chem 2003; 278:5744-9.
47. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N, Koromilas A, Wouters BG. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha, Mol Cell Biol 2002;22:7405-16.
48. McCord JM. Oxygen-derived free radicals in postischemic tissue injury, N Engl J Med 1985;312:159-63.
49. Kuroda S, Siesjo BK. Reperfusion damage following focal ischemia: pathophysiology and therapeutic windows, Clin Neurosci 1997;4:199-212.
50. Ambrosio G, Tritto I. Reperfusion injury: experimental evidence and clinical implications, Am Heart J 1999;138:S69-75.
51. Parkins CS, Hill SA, Stratford MR, Dennis MF, Chaplin DJ. Metabolic and clonogenic consequences of ischaemia reperfusion insult in solid tumours, Exp Physiol 1997;82:361-8.
52. Pohlman TH, Harlan JM. Adaptive responses of the endothelium to stress, J Surg Res 2000;89:85-119.
53. Kalyanaraman B, Joseph J, Kalivendi S, Wang S, Konorev E, Kotamraju S. Doxorubicin-induced apoptosis: implications in cardiotoxicity, Mol Cell Biochem 2002; 234-235:119-24.
54. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours, Nature (Lond) 1996;379:88-91.
55. Reynolds TY, Rockwell S, Glazer PM. Genetic instability induced by the tumor microenvironment, Cancer Res 1996;56:5754-7.
56. Shi Q, Abbruzzese JL, Huang S, Fidler IJ, Xiong Q, Xie K. Constitutive and inducible interleukin 8 expression by hypoxia and acidosis renders human pancreatic cancer cells more tumorigenic and metastatic, Clin Cancer Res 1999;5:3711-21.
57. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene, Cancer Cell 2003;3:347-61.
58. Staller P, Sulitkova J, Lisztwan J, Moch H, Oakeley EJ, Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL, Nature (Lond) 2003;425:307-11.
59. Padera TP, Kadambi A, di Tomaso E, Carreira CM, Brown EB, Boucher Y, Choi NC, Mathisen D, Wain J, Mark EJ, Munn LL, Jain RK. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002;296:1883-6.
60. Hashimoto I, Kodama J, Seki N, Hongo A, Yoshinouchi M, Okuda H, Kudo T. Vascular endothelial growth factor-C expression and its relationship to pelvic lymph node status in invasive cervical cancer. Br J Cancer 2001;85:93-7.