The remarkable yin and yang of tumour hypoxia

References

• Ahn GO, Brown JM. 2008. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: Role of bone marrow-derived myelomonocytic cells. Cancer Cell 13:193–205.
   PubMed Web of Science ®Google Scholar
• Alper T, Howard-Flanders P. 1956. Role of oxygen in modifying the radiosensitivity of E. coli B. Nature 178:978–979.
   PubMed Web of Science ®Google Scholar
• Anderson RF, Shinde SS, Hay MP, Gamage SA, Denny WA. 2003. Activation of 3-amino-1,2,4-benzotriazine 1,4-dioxide antitumor agents to oxidizing species following their one-electron reduction. Journal of American Chemical Society 125:748–756.
   PubMed Web of Science ®Google Scholar
• Asahara T, Murohara T, Sullivan A, Silver M, Van Der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275:964–967.
   PubMed Web of Science ®Google Scholar
• Brizel DM, Dodge RK, Clough RW, Dewhirst MW. 1999. Oxygenation of head and neck cancer: Changes during radiotherapy and impact on treatment outcome. Radiotherapy and Oncology 53:113–117.
   PubMed Web of Science ®Google Scholar
• Brown JM. 1975. Selective radiosensitization of the hypoxic cells of mouse tumors with the nitroimidazoles metronidazole and Ro 7-0582. Radiation Research 64:633–647.
   PubMed Web of Science ®Google Scholar
• Brown JM. 1977. Cytotoxic effects of the hypoxic cell radiosensitizer Ro 7–0582 to tumor cells in vivo. Radiation Research 72:469–486.
   PubMedGoogle Scholar
• Brown JM. 1979. Evidence for acutely hypoxic cells in mouse tumours, and a possible mechanism of reoxygenation. British Journal of Radiology 52:650–656.
   PubMed Web of Science ®Google Scholar
• Brown JM. 2000. Exploiting the hypoxic cancer cell: Mechanisms and therapeutic strategies. Molecular Medicine Today 6:157–162.
   PubMedGoogle Scholar
• Brown JM. 2007. Tumor hypoxia in cancer therapy. Methods in Enzymology 435:298–321.
   Google Scholar
• Brown JM, Yu NY, Brown DM, Lee WW. 1981. SR-2508: A 2-nitroimidazole amide which should be superior to misonidazole as a radiosensitizer for clinical use. International Journal of Radiation Oncology, Biology, and Physics 7:695–703.
   PubMed Web of Science ®Google Scholar
• Budach W, Taghian A, Freeman J, Gioioso D, Suit HD. 1993. Impact of stromal sensitivity on radiation response of tumors. Journal of National Cancer Institute 85:988–993.
   PubMedGoogle Scholar
• Bussink J, Kaanders JH, Van Der Kogel AJ. 2003. Tumor hypoxia at the micro-regional level: Clinical relevance and predictive value of exdogenous and endogenous hypoxic cell markers. Radiotherapy and Oncology 67:3–15.
   PubMed Web of Science ®Google Scholar
• Chaplin DJ, Olive PL, Durand RE. 1987. Intermittent blood flow in a murine tumor: Radiobiological effects. Cancer Research 47:597–601.
   PubMed Web of Science ®Google Scholar
• Churchill-Davidson I, Foster CA, Thomlinson RH. 1958. High-pressure oxygen and radiotherapy. Medical World Journal 88:125–128.
   PubMedGoogle Scholar
• Coffelt SB, Hughes R, Lewis CE. 2009. Tumor-associated macrophages: Effectors of angiogenesis and tumor progression. Biochimestry Biophysics Acta 1796:11–18.
   PubMed Web of Science ®Google Scholar
• Denekamp J, Joiner MC. 1982. The potential benefit from a perfect radiosensitizer and its dependence on reoxygenation. British Journal of Radiology 55:657–663.
   PubMedGoogle Scholar
• Dische S, Saunders MI. 1978. Clinical experience with misonidazole. British Journal of Cancer 37:311–313.
   Google Scholar
• Evans JW, Chernikova SB, Kachnic LA, Banath JP, Sordet O, Delahoussaye YM, Treszezamsky A, Chon BH, Feng Z, Gu Y, Wilson WR, Pommier Y, Olive PL, Powell SN, Brown JM. 2008. Homologous recombination is the principal pathway for the repair of DNA damage induced by tirapazamine in mammalian cells. Cancer Research 68:257–265.
   PubMedGoogle Scholar
• Garcia-Barros M, Paris F, Cordon-Cardo C, Lyden D, Rafii S, Haimovitz-Friedman A, Fuks Z, Kolesnick R. 2003. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300:1155–1159.
   PubMed Web of Science ®Google Scholar
• Gerber HP, Mcmurtrey A, Kowalski J, Lyden D, Yan M, Keyt BA, Dixit V, Ferrara N. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. Journal of Biological Chemistry 273:30336–30343.
   PubMed Web of Science ®Google Scholar
• Gray LH, Conger AD, Ebert M, Hornsey S, Scott OC. 1953. Concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. British Journal of Radiology 26:638–648.
   PubMed Web of Science ®Google Scholar
• Hall EJ, Roizin-Towle L. 1975. Hypoxic sensitizers: Radiobiological studies at the cellular level. Radiology 117:453–457.
   PubMed Web of Science ®Google Scholar
• Hay MP, Hicks KO, Pruijn FB, Pchalek K, Siim BG, Wilson WR, Denny WA. 2007. Pharmacokinetic/pharmacodynamic model-guided identification of hypoxia-selective 1,2,4-benzotriazine 1,4-dioxides with antitumor activity: The role of extravascular transport. Journal of Medicinal Chemistry 50:6392–6404.
   PubMed Web of Science ®Google Scholar
• Hill RP. 1986. Sensitizers and radiation dose fractionation: Results and interpretations. International Journal of Radiation Oncology, Biology, and Physics 12:1049–1054.
   PubMed Web of Science ®Google Scholar
• Hill RP. 1992. Experimental radiotherapy. In: Tannock IF, Hill RP, editors. The basic science of oncology. 2nd ed. Toronto: McGraw-Hill, Inc.
   Google Scholar
• Jameson MB, Rischin D, Pegram M, Gutheil J, Patterson AV, Denny WA, Wilson WR. 2010. A phase I trial of PR-104, a nitrogen mustard prodrug activated by both hypoxia and aldo-keto reductase 1C3, in patients with solid tumors. Cancer Chemotherapy Pharmacology 65:791–801.
   PubMed Web of Science ®Google Scholar
• Janssen HL, Haustermans KM, Balm AJ, Begg AC. 2005. Hypoxia in head and neck cancer: How much, how important? Head and Neck 27:622–638.
   PubMed Web of Science ®Google Scholar
• Kallman RF. 1972. The phenomenon of reoxygenation and its implications for fractionated radiotherapy. Radiology 105:135–142.
   PubMed Web of Science ®Google Scholar
• Kaplan HS. 1974. On the relative importance of hypoxic cells for the radiotherapy of human tumours. European Journal of Cancer 10:275–280.
   Google Scholar
• Kioi M, Vogel H, Schultz G, Hoffman RM, Harsh GR, Brown JM. 2010. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. Journal of Clinical Investigation 120:694–705.
   PubMed Web of Science ®Google Scholar
• Koch CJ. 1993. Unusual oxygen concentration dependence of toxicity of SR-4233, a hypoxic cell toxin. Cancer Research 53:3992–3997.
   PubMed Web of Science ®Google Scholar
• Lanzen J, Braun RD, Klitzman B, Brizel D, Secomb TW, Dewhirst MW. 2006. Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor. Cancer Research 66:2219–2223.
   PubMedGoogle Scholar
• Lee D-J, Pajak TF, Marcial VA, Fu KK, Rotman M, Cooper JS, Ortiz HG, Beitler JJ, Abrams RA, Curran WJ, Coleman CN, Wasserman TH. 1995. Results of an RTOG phase III trial (RTOG 85-27) comparing radiotherapy plus etanidazole with radiotherapy alone for locally advanced head and neck carcinomas. International Journal of Radiation Oncology, Biology, and Physics 32:567–576.
   PubMed Web of Science ®Google Scholar
• Moeller BJ, Cao Y, Li CY, Dewhirst MW. 2004. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: Role of reoxygenation, free radicals, and stress granules. Cancer Cell 5:429–441.
   PubMed Web of Science ®Google Scholar
• Mohindra JK, Rauth AM. 1976. Increased cell killing by metronidazole and nitrofurazone of hypoxic compared to aerobic mammalian cells. Cancer Research 36:930–936.
   PubMed Web of Science ®Google Scholar
• Movsas B, Chapman JD, Hanlon AL, Horwitz EM, Greenberg RE, Stobbe C, Hanks GE, Pollack A. 2002. Hypoxic prostate/muscle pO2 ratio predicts for biochemical failure in patients with prostate cancer: Preliminary findings. Urology 60:634–639.
   PubMed Web of Science ®Google Scholar
• Nordsmark M, Bentzen SM, Overgaard J. 1994. Measurement of human tumour oxygenation status by a polarographic needle electrode. Acta Oncology 33:383–389.
   PubMed Web of Science ®Google Scholar
• Nordsmark M, Overgaard M, Overgaard J. 1996. Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck. Radiotherapy and Oncology 41:31–40.
   PubMed Web of Science ®Google Scholar
• Overgaard J. 2007. Hypoxic radiosensitization: Adored and ignored. Journal of Clinical Oncology 25:4066–4074.
   PubMed Web of Science ®Google Scholar
• Patterson AV, Ferry DM, Edmunds SJ, Gu Y, Singleton RS, Patel K, Pullen SM, Hicks KO, Syddall SP, Atwell GJ, Yang S, Denny WA, Wilson WR. 2007. Mechanism of action and preclinical antitumor activity of the novel hypoxia-activated DNA cross-linking agent PR-104. Clinical Cancer Research 13:3922–3932.
   PubMed Web of Science ®Google Scholar
• Peters LJ, Rischin D, Hicks RJ, Hughes PG, Sizeland AM. 1999. Extraordinary tumor control in phase I trial of concurrent tirapazamine cisplatin and radiotherapy for far advanced head and neck cancer. International Journal of Radiation Oncology, Biology, and Physics 45:148–149 (Abstr #148).
   Google Scholar
• Peters LJ, Rischin D, Fisher R, Corry J, Hicks R. 2007. Identification and therapeutic targeting of hypoxia in H&N cancer. Abstract PS1042. International Congress of Radiation Research, San Francisco, July 2007.
   Google Scholar
• Rischin D, Peters L, Fisher R, Macann A, Denham J, Poulsen M, Jackson M, Kenny L, Penniment M, Corry J, Lamb D, McClure B. 2005. Tirapazamine, cisplatin, and radiation versus fluorouracil, cisplatin, and radiation in patients with locally advanced head and neck cancer: A randomized phase II trial of the Trans-Tasman Radiation Oncology Group (TROG 98.02). Journal of Clinical Oncology 23:79–87.
   PubMed Web of Science ®Google Scholar
• Rischin D, Peters L, O'Sullivan B, Giralt J, Yuen K, Trotti A, Bernier J, Bourhis J, Henke M, Fisher R, Group T-Tro. 2008. Phase III study of tirapazamine, cisplatin and radiation versus cisplatin and radiation for advanced squamous cell carcinoma of the head and neck. Journal of Clinical Oncology 26: Abstract 2008 ASCO Annual Meeting Proceedings.
   Google Scholar
• Sheldon PW, Foster JL, Fowler JF. 1974. Radiosensitization of C3H mouse mammary tumours by a 2-nitroimidazole drug. British Journal of Cancer 30:560–565.
   PubMedGoogle Scholar
• Stone HB, Withers HR. 1975. Enhancement of the radioresponse of a murine tumour by a nitroimidazole. British Journal of Radiology 48:411–412.
   PubMedGoogle Scholar
• Suit HD, Sedlacek R, Silver G, Hsieh C-C, Epp ER, Ngo FQH, Roberts WK, Verhey L. 1988. Therapeutic gain factors for fractionated radiation treatment of spontaneous murine tumours using fast neutrons, photons plus O2(1) or 3 ATA, or photons plus misonidazole. Radiation Research 116:482–502.
   PubMedGoogle Scholar
• Sutherland RM, Franko AJ. 1980. On the nature of the radiobiologically hypoxic fraction in tumors. International Journal of Radiation Oncology, Biology, and Physics 6:117–120.
   PubMed Web of Science ®Google Scholar
• Thomlinson RH, Gray LH. 1955. The histological structure of some human lung cancers and the possible implications for radiotherapy. British Journal of Cancer 9:539–549.
   PubMed Web of Science ®Google Scholar
• Trotter MJ, Chaplin DJ, Olive PL. 1989. Use of a carbocyanine dye as a marker of functional vasculature in murine tumours. British Journal of Cancer 59:706–709.
   PubMedGoogle Scholar
• Wouters BG, Brown JM. 1997. Cells at intermediate oxygen levels can be more important than the ‘hypoxic fraction’ in determining tumor response to fractionated radiotherapy. Radiation Research 147:541–550.
   PubMed Web of Science ®Google Scholar
• Yamaura H, Matsuzawa T. 1979. Tumor regrowth after irradiation: An experimental approach. International Journal of Radiation Biology and Related Studies in Physics, Chemistry, and Medicine 35:201–219.
   PubMed Web of Science ®Google Scholar
• Yang L, Debusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC. 2004. Expansion of myeloid immune suppressor Gr+CD11b + cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6:409–421.
   PubMed Web of Science ®Google Scholar
• Zagorevskii D, Song M, Breneman C, Yuan Y, Fuchs T, Gates KS, Greenlief CM. 2003. A mass spectrometry study of tirapazamine and its metabolites. Insights into the mechanism of metabolic transformations and the characterization of reaction intermediates. Journal of American Society Mass Spectrometry 14:881–892.
   Google Scholar