Chemical radiosensitizers for use in radiotherapy.

Radiosensitizers are intended to enhance tumour cell killing while having much less effect on normal tissues. Some drugs target different physiological characteristics of the tumour, particularly hypoxia associated with radioresistance. Oxygen is the definitive hypoxic cell radiosensitizer, the large differential radiosensitivity of oxic vs hypoxic cells being an attractive factor. The combination of nicotinamide to reduce acute hypoxia with normobaric carbogen breathing is showing clinical promise. 'Electron-affinic' chemicals that react with DNA free radicals have the potential for universal activity to combat hypoxia-associated radioresistance; a nitroimidazole, nimorazole, is clinically effective at tolerable doses. Hypoxia-specific cytotoxins, such as tirapazamine, are valuable adjuncts to radiotherapy. Nitric oxide is a potent hypoxic cell radiosensitizer; variations in endogenous levels might have prognostic significance, and routes to deliver nitric oxide specifically to tumours are being developed. In principle, many drugs can be delivered selectively to hypoxic tumours using either reductase enzymes or radiation-produced free radicals to activate drug release from electron-affinic prodrugs. A redox-active agent based on a gadolinium chelate is being evaluated clinically. Pyrimidines substituted with bromine or iodine are incorporated into DNA and enhance free radical damage; fluoropyrimidines act by different mechanisms. A wide variety of drugs that influence the nature or repair of DNA damage are being evaluated in conjunction with radiation; it is often difficult to define the mechanisms underlying chemoradiation regimens. Drugs being evaluated include topoisomerase inhibitors (e.g. camptothecin, topotecan), and the hypoxia-activated anthraquinone AQ4N; alkylating agents include temozolomide. Drugs involved in DNA repair pathways being investigated include the potent poly(ADP ribose)polymerase inhibitor, AG14,361. Proteins involved in cell signalling, such as the Ras family, are attractive targets linked to radioresistance, as are epidermal growth factor receptors and linked kinases (drugs including vandetanib [ZD6,474], cetuximab and gefitinib), and cyclooxygenase-2 (celecoxib). The suppression of radioprotective thiols seems to offer more potential with alkylating agents than with radiotherapy, although it remains a strategy worthy of exploration.

[1]  Chryso Kanthou,et al.  Disrupting tumour blood vessels , 2005, Nature Reviews Cancer.

[2]  Y. Shibamoto,et al.  In vitro and in vivo evaluation of novel antitumor prodrugs of 5-fluoro-2'-deoxyuridine activated by hypoxic irradiation. , 2004, International journal of radiation oncology, biology, physics.

[3]  A. Lott,et al.  Copper as a hypoxic cell sensitizer of mammalian cells. , 1978, The British journal of cancer. Supplement.

[4]  J. Hendry Sensitization of hypoxic normal tissue. , 1978, The British journal of cancer. Supplement.

[5]  P. Neta,et al.  Intramolecular electron transfer and dehalogenation of anion radicals. 2. Halonitroaromatic compounds , 1981 .

[6]  D. Mahvi,et al.  Phase I study of continuous-infusion L-S,R-buthionine sulfoximine with intravenous melphalan. , 1997, Journal of the National Cancer Institute.

[7]  B. Telfer,et al.  ZD6474, a Potent Inhibitor of Vascular Endothelial Growth Factor Signaling, Combined With Radiotherapy , 2004, Clinical Cancer Research.

[8]  D. Wink,et al.  Redox generation of nitric oxide to radiosensitize hypoxic cells. , 1998, International journal of radiation oncology, biology, physics.

[9]  B. Palcic,et al.  Survival measurements at low doses: oxygen enhancement ratio. , 1982, British Journal of Cancer.

[10]  J. Overgaard,et al.  Modification of Hypoxia-Induced Radioresistance in Tumors by the Use of Oxygen and Sensitizers. , 1996, Seminars in radiation oncology.

[11]  I. Stratford,et al.  Enhancement of chemotherapy and radiotherapy of murine tumours by AQ4N, a bioreductively activated anti-tumour agent , 2000, British Journal of Cancer.

[12]  R. Jain,et al.  NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. , 2005, The Journal of clinical investigation.

[13]  J. Sessler,et al.  Gadolinium(III) texaphyrin: a tumor selective radiation sensitizer that is detectable by MRI. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  V. Grégoire,et al.  Insulin increases the sensitivity of tumors to irradiation: involvement of an increase in tumor oxygenation mediated by a nitric oxide-dependent decrease of the tumor cells oxygen consumption. , 2002, Cancer research.

[15]  T. McMillan,et al.  Oxygen effect for DNA double-strand break induction determined by pulsed-field gel electrophoresis. , 1992, International journal of radiation biology.

[16]  A. Rosenberg,et al.  Radiation sensitization with redox modulators: a promising approach. , 2006, International journal of radiation oncology, biology, physics.

[17]  S. Rockwell,et al.  Effects of motexafin gadolinium on DNA damage and X-ray-induced DNA damage repair, as assessed by the Comet assay. , 2005, International journal of radiation oncology, biology, physics.

[18]  J. Brown,et al.  Therapeutic targets in radiotherapy. , 2001, International journal of radiation oncology, biology, physics.

[19]  D. Hornig DISTRIBUTION OF ASCORBIC ACID, METABOLITES AND ANALOGUES IN MAN AND ANIMALS , 1975, Annals of the New York Academy of Sciences.

[20]  W. Dobrowsky,et al.  AK-2123 (Sanazol) as a radiation sensitizer in the treatment of stage III cervical cancer: results of an IAEA multicentre randomised trial. , 2007, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[21]  D. Abraham,et al.  Allosteric modifiers of hemoglobin: 2-[4-[[(3,5-disubstituted anilino)carbonyl]methyl]phenoxy]-2-methylpropionic acid derivatives that lower the oxygen affinity of hemoglobin in red cell suspensions, in whole blood, and in vivo in rats. , 1992, Biochemistry.

[22]  B. James,et al.  Further studies on toxic and radiosensitizing properties of ruthenium complexes of 4-nitroimidazoles. , 1987, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[23]  P. Wardman Evaluation of the “radical sink” hypothesis from a chemical-kinetic viewpoint , 1998 .

[24]  R. Mikkelsen,et al.  Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms , 2003, Oncogene.

[25]  J. Denekamp,et al.  Nicotinamide as a repair inhibitor in vivo: studies using single and fractionated X-ray doses in mouse skin and kidneys. , 1996, Radiation research.

[26]  G. Rosner,et al.  Effects of diethylamine/nitric oxide on blood perfusion and oxygenation in the R3230Ac mammary carcinoma. , 1997, British Journal of Cancer.

[27]  G. Hanks,et al.  Single-photon emission computed tomography and positron-emission tomography assays for tissue oxygenation. , 2001, Seminars in radiation oncology.

[28]  S. Dische,et al.  Clinical results of hypoxic cell radiosensitisation from hyperbaric oxygen to accelerated radiotherapy, carbogen and nicotinamide. , 1996, The British journal of cancer. Supplement.

[29]  W. Cramp Radiosensitization by Copper Ions, and Consequent Reversal of the Oxygen Effect , 1965, Nature.

[30]  J. Downward Targeting RAS signalling pathways in cancer therapy , 2003, Nature Reviews Cancer.

[31]  J. Fowler,et al.  Eighth annual Juan del Regato lecture. Chemical modifiers of radiosensitivity--theory and reality: a review. , 1985, International journal of radiation oncology, biology, physics.

[32]  M. Mehta,et al.  Motexafin gadolinium in the treatment of brain metastases , 2007, Expert opinion on pharmacotherapy.

[33]  B. Bridges Sensitization of Escherichia coli to Gamma-Radiation by N-Ethylmaleimide , 1960, Nature.

[34]  J. Sessler,et al.  One-electron reduction and oxidation studies of the radiation sensitizer gadolinium(III) texaphyrin (PCI-0120) and other water soluble metallotexaphyrins , 1999 .

[35]  M. Watts,et al.  Radiosensitization by misonidazole, pimonidazole and azomycin and intracellular uptake in human tumour cell lines. , 1990, International journal of radiation biology.

[36]  G. Thomas Raising Hemoglobin: An Opportunity for Increasing Survival? , 2002, Oncology.

[37]  B. Ertl-Wagner,et al.  Feasibility of Photofrin II as a Radiosensitizing Agent in Solid Tumors – Preliminary Results , 2006, Oncology Research and Treatment.

[38]  P. Harari,et al.  Radiation and new molecular agents, part II: targeting HDAC, HSP90, IGF-1R, PI3K, and Ras. , 2006, Seminars in radiation oncology.

[39]  D. Chaplin,et al.  Spatial characterization of glutathione depletion in the KHT sarcoma using flow cytometry. , 1991, International journal of radiation biology.

[40]  C. Coleman,et al.  Sensitizers and protectors of radiation and chemotherapy. , 2001, Current problems in cancer.

[41]  W. Denny,et al.  Reduction of nitroarylmethyl quaternary ammonium prodrugs of mechlorethamine by radiation. , 1998, Radiation research.

[42]  R. Willson,et al.  Metronidazole (Flagyl): characterization as a cytotoxic drug specific for hypoxic tumour cells. , 1976, British Journal of Cancer.

[43]  G. Berthon Handbook of metal-ligand interactions in biological fluids, bioinorganic chemistry , 1995 .

[44]  R. A. Crabtree,et al.  Enhanced radiation-induced cell killing by carboplatin in cells of repair-proficient and repair-deficient cell lines. , 1995, Radiation research.

[45]  P. D. de Wilde,et al.  The prognostic value of endogenous hypoxia-related markers for head and neck squamous cell carcinomas treated with ARCON. , 2006, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[46]  Vicky Goh,et al.  Effect of nitric-oxide synthesis on tumour blood volume and vascular activity: a phase I study. , 2007, The Lancet. Oncology.

[47]  W. Wilson,et al.  Pathways of Reductive Fragmentation of Heterocyclic Nitroarylmethyl Quaternary Ammonium Prodrugs of Mechlorethamine , 2002, Radiation research.

[48]  N. Farrell,et al.  Platinum complexes with one radiosensitizing ligand [PtCl2(NH3) (sensitizer)]: radiosensitization and toxicity studies in vitro. , 1987, Radiation research.

[49]  E. Cadenas,et al.  Nitric Oxide, Cell Signaling, and Gene Expression , 2005 .

[50]  D. Abraham,et al.  RSR13, an allosteric effector of haemoglobin, and carbogen radiosensitize FSAII and SCCVII tumours in C3H mice , 1999, British Journal of Cancer.

[51]  C. Sartor,et al.  Mechanisms of Disease: radiosensitization by epidermal growth factor receptor inhibitors , 2004, Nature Clinical Practice Oncology.

[52]  Christopher U. Jones,et al.  Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. , 2006, The New England journal of medicine.

[53]  R. Bristow,et al.  Radiation and new molecular agents part I: targeting ATM-ATR checkpoints, DNA repair, and the proteasome. , 2006, Seminars in radiation oncology.

[54]  C. Sonntag Free-Radical-Induced DNA Damage and Its Repair: A Chemical Perspective , 2006 .

[55]  V. Grégoire,et al.  Nitric oxide-mediated increase in tumor blood flow and oxygenation of tumors implanted in muscles stimulated by electric pulses. , 2003, International journal of radiation oncology, biology, physics.

[56]  G. Steel,et al.  Terminology in the description of drug-radiation interactions. , 1979, International journal of radiation oncology, biology, physics.

[57]  P. Howard-Flanders Effect of Nitric Oxide on the Radiosensitivity of Bacteria , 1957, Nature.

[58]  M. Horsman,et al.  Vascular‐targeting therapies for treatment of malignant disease , 2004, Cancer.

[59]  S. Dische,et al.  The uptake of the radiosensitizing compound Ro 03-8799 (Pimonidazole) in human tumors. , 1989, International journal of radiation oncology, biology, physics.

[60]  J. Wahr,et al.  Allosteric Modification of Oxygen Delivery by Hemoglobin , 2001, Anesthesia and analgesia.

[61]  J. Fowler,et al.  Radiosensitisation in normal tissues with oxygen, carbogen or nicotinamide: therapeutic gain comparisons for fractionated x-ray schedules. , 1996, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[62]  James B. Mitchell,et al.  Hypoxic mammalian cell radiosensitization by nitric oxide. , 1993, Cancer research.

[63]  D. Hedley,et al.  Microregional heterogeneity of non-protein thiols in cervical carcinomas assessed by combined use of HPLC and fluorescence image analysis. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

[64]  C. Koch,et al.  Radiosensitization of hypoxic tumor cells by dodecafluoropentane: a gas-phase perfluorochemical emulsion. , 2002, Cancer research.

[65]  Min Zhang,et al.  Novel radiation-enhancing agents in malignant gliomas. , 2006, Seminars in radiation oncology.

[66]  G. Adams,et al.  Electron-affinic sensitization. I. A structural basis for chemical radiosensitizers in bacteria. , 1969, International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine.

[67]  Timothy W Secomb,et al.  Use of three-dimensional tissue cultures to model extravascular transport and predict in vivo activity of hypoxia-targeted anticancer drugs. , 2006, Journal of the National Cancer Institute.

[68]  T. Kinsella,et al.  New radiosensitizing regimens, drugs, prodrugs, and candidates. , 2004, Clinical advances in hematology & oncology : H&O.

[69]  A. Minchinton,et al.  Measurement of delivery and metabolism of tirapazamine to tumour tissue using the multilayered cell culture model , 1999, Cancer Chemotherapy and Pharmacology.

[70]  C. Koch A thin-film culturing technique allowing rapid gas-liquid equilibration (6 sec) with no toxicity to mammalian cells. , 1984, Radiation research.

[71]  S. Rockwell,et al.  Pentoxifylline improves the oxygenation and radiation response of BA1112 rat rhabdomyosarcomas and EMT6 mouse mammary carcinomas , 2000, International journal of cancer.

[72]  G. Jori,et al.  On the double role of Photofrin as a photo- and a radio-sensitising agent: a possible new combination therapy for tumours , 2002, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[73]  E. Douple,et al.  Carboplatin as a potentiator of radiation therapy. , 1985, Cancer treatment reviews.

[74]  Hala Gali-Muhtasib,et al.  Radiation Oncology Radiosensitization by 2-benzoyl-3-phenyl-6,7-dichloroquinoxaline 1,4-dioxide under Oxia and Hypoxia in Human Colon Cancer Cells , 2022 .

[75]  S. Rockwell,et al.  Preliminary studies of the effects of gadolinium texaphyrin on the growth and radiosensitivity of EMT6 cells in vitro. , 2002, International journal of radiation oncology, biology, physics.

[76]  Raleigh,et al.  Measuring Tumor Hypoxia. , 1996, Seminars in radiation oncology.

[77]  E. Malaise,et al.  SR-2508 plus buthionine sulfoximine or SR-2508 alone: effects on the radiation response and the glutathione content of a human tumor xenograft. , 1987, Radiation research.

[78]  J. Fowler,et al.  Radiosensitization of Chinese hamster cells by oxygen and misonidazole at low X-ray doses. , 1986, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[79]  M. Stratford,et al.  Synthesis and biological properties of bioreductively targeted nitrothienyl prodrugs of combretastatin A-4 , 2006, Molecular Cancer Therapeutics.

[80]  Simon C Watkins,et al.  Nitric Oxide and Ionizing Radiation Synergistically Promote Apoptosis and Growth Inhibition of Cancer by Activating p53 , 2004, Cancer Research.

[81]  P. Harari,et al.  Radiation combined with EGFR signal inhibitors: head and neck cancer focus. , 2006, Seminars in radiation oncology.

[82]  G. Steel,et al.  Basic Clinical Radiobiology , 1997 .

[83]  W. Zapol,et al.  Inhaled nitric oxide does not reduce systemic vascular resistance in mice. , 2006, American journal of physiology. Heart and circulatory physiology.

[84]  J. Brown,et al.  Re-evaluating gadolinium(III) texaphyrin as a radiosensitizing agent. , 2000, Cancer research.

[85]  J. Brown,et al.  Aerobic radiosensitization by SR 4233 in vitro and in vivo. , 1990, International journal of radiation oncology, biology, physics.

[86]  P. Wardman Electron transfer and oxidative stress as key factors in the design of drugs selectively active in hypoxia. , 2001, Current medicinal chemistry.

[87]  C J Gomer,et al.  Properties and applications of photodynamic therapy. , 1989, Radiation research.

[88]  R. Muschel,et al.  The Ras radiation resistance pathway. , 2001, Cancer research.

[89]  V. Shafirovich,et al.  Nitroxyl and its anion in aqueous solutions: Spin states, protic equilibria, and reactivities toward oxygen and nitric oxide , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[90]  S. Evans,et al.  Cysteine concentrations in rodent tumors: Unexpectedly high values may cause therapy resistance , 1996, International journal of cancer.

[91]  P. Hoskin,et al.  Accelerated radiotherapy, carbogen and nicotinamide (ARCON) in locally advanced head and neck cancer: a feasibility study. , 1997, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[92]  S. Chakraborty,et al.  Preparation and preliminary biological evaluation of a 177Lu labeled sanazole derivative for possible use in targeting tumor hypoxia. , 2004, Bioorganic & medicinal chemistry.

[93]  P. Wood The redox potential of the system oxygen—superoxide , 1974 .

[94]  J. Fowler,et al.  Radiosensitizers of hypoxic cells in solid tumors. , 1976, Cancer treatment reviews.

[95]  J. Overgaard,et al.  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. , 2005, The Lancet. Oncology.

[96]  E. Hall,et al.  Radiobiology for the radiologist , 1973 .

[97]  P. Hoskin,et al.  Acute and late morbidity in the treatment of advanced bladder carcinoma with accelerated radiotherapy, carbogen, and nicotinamide , 2005, Cancer.

[98]  G. Adams Chemical radiosensitization of hypoxic cells. , 1973, British Medical Bulletin.

[99]  J. Horiot,et al.  ARCON: accelerated radiotherapy with carbogen and nicotinamide in head and neck squamous cell carcinomas. The experience of the Co-operative group of radiotherapy of the european organization for research and treatment of cancer (EORTC). , 2000, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[100]  W. Denny,et al.  Recent developments in the design of bioreductive drugs. , 1996, The British journal of cancer. Supplement.

[101]  S. Rockwell,et al.  Effects of texaphyrins on the oxygenation of EMT6 mouse mammary tumors. , 2004, International journal of radiation oncology, biology, physics.

[102]  L. Wirth,et al.  Cetuximab and radiotherapy for head and neck cancer. , 2006, The New England journal of medicine.

[103]  Sulfoglycolipids as candidate antiangiogenic radiosensitizers , 2007, Anti-cancer drugs.

[104]  H. Nagasawa,et al.  Design of hypoxia-targeting drugs as new cancer chemotherapeutics. , 2006, Biological & pharmaceutical bulletin.

[105]  L. Brady,et al.  Radiation sensitizers, their use in the clinical management of cancer , 1980 .

[106]  P. O'Neill Pulse radiolytic study of the interaction of thiols and ascorbate with OH adducts of dGMP and dG: implications for DNA repair processes. , 1983, Radiation research.

[107]  M. Burkitt A critical overview of the chemistry of copper-dependent low density lipoprotein oxidation: roles of lipid hydroperoxides, alpha-tocopherol, thiols, and ceruloplasmin. , 2001, Archives of biochemistry and biophysics.

[108]  S. Shih,et al.  Ku86 modulates DNA topoisomerase I-mediated radiosensitization, but not cytotoxicity, in mammalian cells. , 2005, Cancer research.

[109]  Jane Worthington,et al.  p21(WAF1)-mediated transcriptional targeting of inducible nitric oxide synthase gene therapy sensitizes tumours to fractionated radiotherapy , 2007, Gene Therapy.

[110]  C. Streffer,et al.  A comparison of the physiological effects of RSU1069 and RB6145 in the SCCVII murine tumour. , 1996, Acta oncologica.

[111]  K. Skov Modification of radiation response by metal complexes: a review with emphasis of nonplatinum studies. , 1987, Radiation research.

[112]  B. Wouters,et al.  Cells at intermediate oxygen levels can be more important than the "hypoxic fraction" in determining tumor response to fractionated radiotherapy. , 1997, Radiation research.

[113]  L. Ignarro Nitric oxide : biology and pathobiology , 2000 .

[114]  Clemens von Sonntag,et al.  Free-Radical-Induced DNA Damage and Its Repair , 2006 .

[115]  B. Marples,et al.  The effect of oxygen on low-dose hypersensitivity and increased radioresistance in Chinese hamster V79-379A cells. , 1994, Radiation research.

[116]  J. C. Bremner,et al.  Assessing the bioreductive effectiveness of the nitroimidazole RSU1069 and its prodrug RB6145: with particular reference toin vivo methods of evaluation , 1993, Cancer and Metastasis Reviews.

[117]  J. Bussink,et al.  ARCON: a novel biology-based approach in radiotherapy. , 2002, The Lancet. Oncology.

[118]  F. Stewart,et al.  Skin sensitization by misonidazole: a demonstration of uniform mild hypoxia. , 1982, British Journal of Cancer.

[119]  E. Clarke,et al.  Structure-activity relationships in the development of hypoxic cell radiosensitizers. I. Sensitization efficiency. , 1979, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[120]  P. Wardman Chapter 4 – SENSITIZATION AND PROTECTION OF OXIDATIVE DAMAGE CAUSED BY HIGH ENERGY RADIATION , 1993 .

[121]  E. Clarke,et al.  Structure-activity relationships in the development of hypoxic cell radiosensitizers. II. Cytotoxicity and therapeutic ratio. , 1979, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[122]  J. Overgaard Clinical evaluation of nitroimidazoles as modifiers of hypoxia in solid tumors. , 1994, Oncology research.

[123]  E. Clarke,et al.  Redox properties and rate constants in free-radical mediated damage. , 1987, The British journal of cancer. Supplement.

[124]  Deepak Khuntia,et al.  Motexafin gadolinium: a clinical review of a novel radioenhancer for brain tumors , 2004, Expert review of anticancer therapy.

[125]  M. Naylor,et al.  Recent advances in bioreductive drug targeting. , 2001, Mini reviews in medicinal chemistry.

[126]  Y. Kataoka,et al.  Radioprotectants: Current Status and New Directions , 2002, Oncology.

[127]  I. Tannock,et al.  Drug penetration in solid tumours , 2006, Nature Reviews Cancer.

[128]  J. Collier,et al.  A therapeutic benefit from combining normobaric carbogen or oxygen with nicotinamide in fractionated X-ray treatments. , 1991, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[129]  E. Bernhard,et al.  How does radiation kill cells? , 1999, Current opinion in chemical biology.

[130]  Johan Bussink,et al.  Clinical studies of hypoxia modification in radiotherapy. , 2004, Seminars in radiation oncology.

[131]  T. Chang Evolution of Artificial Cells Using Nanobiotechnology of Hemoglobin Based RBC Blood Substitute as an Example , 2006, Artificial cells, blood substitutes, and immobilization biotechnology.

[132]  D. Hedley,et al.  Differential effects of buthionine sulphoximine in hypoxic and non-hypoxic regions of human cervical carcinoma xenografts. , 2001, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[133]  R. Willson,et al.  Metronidazole ("Flagyl"). A radiosensitizer of hypoxic cells. , 1974, The British journal of radiology.

[134]  G. Tozer,et al.  Nitric oxide in tumor biology and cancer therapy. Part 2: Therapeutic implications. , 1997, Clinical oncology (Royal College of Radiologists (Great Britain)).

[135]  C. Szabó,et al.  The Therapeutic Potential of Poly(ADP-Ribose) Polymerase Inhibitors , 2002, Pharmacological Reviews.

[136]  K. Ang,et al.  Inhibition of DNA repair as a mechanism of enhanced radioresponse of head and neck carcinoma cells by a selective cyclooxygenase-2 inhibitor, celecoxib. , 2005, International Journal of Radiation Oncology, Biology, Physics.

[137]  C. Coleman,et al.  Final report of the phase I trial of the hypoxic cell radiosensitizer SR 2508 (etanidazole) Radiation Therapy Oncology Group 83-03. , 1990, International journal of radiation oncology, biology, physics.

[138]  Louis B Harrison,et al.  Impact of tumor hypoxia and anemia on radiation therapy outcomes. , 2002, The oncologist.

[139]  D. Hirst,et al.  A cytochrome P450 2B6 meditated gene therapy strategy to enhance the effects of radiation or cyclophosphamide when combined with the bioreductive drug AQ4N , 2005, The journal of gene medicine.

[140]  P. Vaupel,et al.  Erythropoietin: effects on life expectancy in patients with cancer-related anaemia , 2006 .

[141]  H. Bailey L-S,R-buthionine sulfoximine: historical development and clinical issues. , 1998, Chemico-biological interactions.

[142]  S. Nishimoto,et al.  Hypoxia-selective activation of 5-fluorodeoxyuridine prodrug possessing indolequinone structure: radiolytic reduction and cytotoxicity characteristics. , 2005, Bioorganic & medicinal chemistry letters.

[143]  Y. Shibamoto,et al.  Radiosensitizing effect of misonidazole in combination with an inhibitor of glutathione synthesis in murine tumors. , 1986, International journal of radiation oncology, biology, physics.

[144]  C. Mcginn,et al.  Recent advances in the use of radiosensitizing nucleosides. , 2001, Seminars in radiation oncology.

[145]  Olive Pl,et al.  Lack of a correlation between radiosensitivity and DNA double-strand break induction or rejoining in six human tumor cell lines , 1994 .

[146]  I. Tannock,et al.  Treatment of cancer with radiation and drugs. , 1996, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[147]  G. Adams,et al.  Synthesis and evaluation of alpha-[[(2-haloethyl)amino]methyl]-2- nitro-1H-imidazole-1-ethanols as prodrugs of alpha-[(1-aziridinyl)methyl]-2- nitro-1H-imidazole-1-ethanol (RSU-1069) and its analogues which are radiosensitizers and bioreductively activated cytotoxins. , 1990, Journal of medicinal chemistry.

[148]  D. Boothman,et al.  Cellular and Molecular Responses to Topoisomerase I Poisons: Exploiting Synergy for Improved Radiotherapy , 2000, Annals of the New York Academy of Sciences.

[149]  G. Buettner,et al.  Catalytic metals, ascorbate and free radicals: combinations to avoid. , 1996, Radiation research.

[150]  G. Adams,et al.  Studies of the mechanisms of radiosensitization of bacterial and mammalian cells by Diamide. , 1975, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[151]  G. Adams,et al.  Time-resolved oxygen effects in irradiated bacteria and mammalian cells: a rapid-mix study. , 1975, Radiation research.

[152]  J. Feldmeier,et al.  Hyperbaric oxygen for delayed radiation injuries. , 2004, Undersea & hyperbaric medicine : journal of the Undersea and Hyperbaric Medical Society, Inc.

[153]  D. Hirst,et al.  Use of the radiation‐inducible WAF1 promoter to drive iNOS gene therapy as a novel anti‐cancer treatment , 2004, The journal of gene medicine.

[154]  W. Wilson,et al.  Radiolytic and cellular reduction of a novel hypoxia-activated cobalt(III) prodrug of a chloromethylbenzindoline DNA minor groove alkylator. , 2006, Biochemical pharmacology.

[155]  J. Sessler,et al.  Redox cycling by motexafin gadolinium enhances cellular response to ionizing radiation by forming reactive oxygen species. , 2001, International journal of radiation oncology, biology, physics.

[156]  D. Shrieve,et al.  Glutathione depletion in tissues after administration of buthionine sulphoximine. , 1984, International journal of radiation oncology, biology, physics.

[157]  K. Peters,et al.  Tirapazamine: a hypoxia-activated topoisomerase II poison. , 2002, Cancer research.

[158]  Yuji Seo,et al.  Differential Radiosensitization in DNA Mismatch Repair-Proficient and -Deficient Human Colon Cancer Xenografts with 5-Iodo-2-pyrimidinone-2′-deoxyribose , 2004, Clinical Cancer Research.

[159]  G. Storme,et al.  The radiosensitizing effect of immunoadjuvant OM-174 requires cooperation between immune and tumor cells through interferon-gamma and inducible nitric oxide synthase. , 2006, International journal of radiation oncology, biology, physics.

[160]  K. Haustermans,et al.  Hypoxia in head and neck cancer: How much, how important? , 2005, Head & neck.

[161]  Darren Magda,et al.  Motexafin gadolinium: a novel redox active drug for cancer therapy. , 2006, Seminars in cancer biology.

[162]  W. Leopold,et al.  A new class of analogues of the bifunctional radiosensitizer alpha-(1-aziridinylmethyl)-2-nitro-1H-imidazole-1-ethanol (RSU 1069): the cycloalkylaziridines. , 1991, Journal of medicinal chemistry.

[163]  D. Hirst What is the importance of anaemia in radiotherapy? The value of animal studies. , 1991, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[164]  R. McClelland,et al.  DNA-targeted 2-nitroimidazoles: in vitro and in vivo studies. , 1994, British Journal of Cancer.

[165]  T. Ward,et al.  Hypoxia in head and neck cancer. , 2006, The British journal of radiology.

[166]  H. Thaler,et al.  Effects of Motexafin gadolinium on tumor metabolism and radiation sensitivity. , 2001, International journal of radiation oncology, biology, physics.

[167]  Jane Worthington,et al.  Evaluation of a synthetic CArG promoter for nitric oxide synthase gene therapy of cancer , 2005, Gene Therapy.

[168]  N. Andratschke,et al.  Current status of angiogenesis inhibitors combined with radiation therapy. , 2006, Cancer treatment reviews.

[169]  R. G. Webb,et al.  Radiosensitization of mammalian cells by p-nitroacetophenone. I. Characterization in asynchronous and synchronous populations. , 1971, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[170]  C. Coleman,et al.  Clinical radiosensitization: why it does and does not work. , 1999, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[171]  S. Marangoz,et al.  Induction of cachexia in mice. , 1999, British journal of cancer.

[172]  P. Dendy,et al.  Hypoxia in biology and medicine: the legacy of L H Gray. , 2006, The British journal of radiology.

[173]  G. Scott,et al.  Atmospheric Oxidation and Antioxidants , 1965 .

[174]  W. Denny,et al.  Optimization of the Auxiliary Ligand Shell of Cobalt(III)(8-hydroxyquinoline) Complexes as Model Hypoxia-Selective Radiation-Activated Prodrugs , 2004, Radiation research.

[175]  E. Douple,et al.  Production of DNA double-strand breaks by interactions between carboplatin and radiation: a potential mechanism for radiopotentiation. , 1995, Radiation research.

[176]  L. H. Gray,et al.  Effect of Nitric Oxide on the Radio-sensitivity of Tumour Cells , 1958, Nature.

[177]  T. Kinsella,et al.  Targeting DNA mismatch repair for radiosensitization. , 2001, Seminars in Radiation Oncology.

[178]  Keith A Cengel,et al.  Molecular targets for altering radiosensitivity: lessons from Ras as a pre-clinical and clinical model. , 2005, Critical reviews in oncology/hematology.

[179]  C. Coleman,et al.  Radiation and chemotherapy sensitizers and protectors. , 1990, Critical reviews in oncology/hematology.

[180]  K. Blackwell,et al.  Hypoxia and anemia: factors in decreased sensitivity to radiation therapy and chemotherapy? , 2004, The oncologist.

[181]  Gerald Batist,et al.  Structure-Based Identification of Novel Human γ-Glutamylcysteine Synthetase Inhibitors , 2007, Molecular Pharmacology.

[182]  P. O'Neill,et al.  Redox Dependence of the Rate of Interaction of Hydroxyl Radical Adducts of DNA Nucleobases with Oxidants: Consequences for DNA Strand Breakage , 1998 .

[183]  J. Soranson,et al.  Enhancement of misonidazole radiosensitization by buthionine sulphoximine. , 1984, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[184]  Robert Almassy,et al.  Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. , 2004, Journal of the National Cancer Institute.

[185]  G. Adams,et al.  Electron affinic sensitization. II. Para-nitroacetophenone: a radiosensitizer for anoxic bacterial and mammalian cells. , 1971, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[186]  J. Harris,et al.  Mammalian cell studies with diamide. , 1979, Pharmacology & therapeutics.

[187]  P. Wardman The reduction potential of benzyl viologen: an important reference compound for oxidant/radical redox couples. , 1991, Free radical research communications.

[188]  M. Renschler The emerging role of reactive oxygen species in cancer therapy. , 2004, European journal of cancer.

[189]  D. Gandara,et al.  Enhancement of radiotherapy with DNA topoisomerase I-targeted drugs. , 2004, Critical reviews in oncology/hematology.

[190]  J. Vermorken,et al.  Combined modality therapy of gemcitabine and radiation. , 2005, The oncologist.

[191]  T. Lawrence,et al.  New and Emerging Radiosensitizers and Radioprotectors , 2006, Cancer investigation.

[192]  M. Stratford,et al.  Radiosensitizer-DNA interactions in relation to intracellular uptake. , 1989, International journal of radiation oncology, biology, physics.

[193]  P. Cullis,et al.  Uptake and cytotoxicity of novel nitroimidazole-polyamine conjugates in Ehrlich ascites tumour cells. , 1992, Biochemical pharmacology.

[194]  B. Bridges SENSITIZATION OF ORGANISMS TO RADIATION BY SULFHYDRYL-BINDING AGENTS. , 1969 .

[195]  K. Hicks,et al.  Measurement of extravascular drug diffusion in multicellular layers. , 1999, British journal of cancer.

[196]  M. Stratford,et al.  Competitive dose-modification between ascorbate and misonidazole in human and hamster cells: effects of glutathione depletion. , 1988, International journal of radiation biology.

[197]  E. Clarke,et al.  Oxygen inhibition of nitroreductase: electron transfer from nitro radical-anions to oxygen. , 1976, Biochemical and biophysical research communications.

[198]  C. Koch,et al.  Oxygen dependence of cellular uptake of EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl)a cet amide] : analysis of drug adducts by fluorescent antibodies vs bound radioactivity. , 1995, British Journal of Cancer.

[199]  Y. Vodovotz,et al.  Adenoviral Gene Transfer of the Human Inducible Nitric Oxide Synthase Gene Enhances the Radiation Response of Human Colorectal Cancer Associated with Alterations in Tumor Vascularity , 2004, Cancer Research.

[200]  G. Calais,et al.  In situ tumour radiosensitization induced by clofibrate administration: single dose and fractionated studies. , 1991, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[201]  C. Sonntag,et al.  The chemical basis of radiation biology , 1987 .

[202]  J. Kaanders,et al.  Administration of nicotinamide during a five- to seven-week course of radiotherapy: pharmacokinetics, tolerance, and compliance. , 1997, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[203]  M. Molls,et al.  The role of pentoxifylline as a modifier of radiation therapy. , 2005, Cancer treatment reviews.

[204]  M. Ritter,et al.  Platinum-based concurrent chemoradiotherapy for tumors of the head and neck and the esophagus. , 2006, Seminars in radiation oncology.

[205]  M. Stuschke,et al.  Chemoradiation paradigm for the treatment of lung cancer , 2006, Nature Clinical Practice Oncology.

[206]  J. Debus,et al.  Improving chemoradiotherapy in rectal cancer. , 2001, The oncologist.

[207]  I. Stratford,et al.  Quinone bioreductive prodrugs as delivery agents. , 2004, Current drug delivery.

[208]  R. Middleton,et al.  Enhancement of misonidazole radiosensitization by an inhibitor of glutathione biosynthesis. , 1983, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[209]  P. Wardman,et al.  The one-electron reduction potential of 3-amino-1,2,4-benzotriazine 1,4-dioxide (tirapazamine): a hypoxia-selective bioreductive drug. , 1996, Free radical research.

[210]  B. Telfer,et al.  Tirapazamine Administered as a Neoadjuvant to Radiotherapy Reduces Metastatic Dissemination , 2005, Clinical Cancer Research.

[211]  A. Rauth,et al.  Molecular mechanisms for the hypoxia-dependent activation of 3-amino-1,2,4-benzotriazine-1,4-dioxide (SR 4233). , 1988, Biochemical pharmacology.

[212]  C. Willett,et al.  Chemotherapeutic and biologic agents as radiosensitizers in rectal cancer. , 2003, Seminars in radiation oncology.

[213]  Jesse D. Roberts,et al.  Inhaled Nitric Oxide A Selective Pulmonary Vasodilator Current Uses and Therapeutic Potential , 2004 .

[214]  M. Stratford,et al.  Targeting radiosensitizers to DNA by minor groove binding: nitroarenes based on netropsin and distamycin , 1993 .

[215]  K. Rothkamm,et al.  Radiosensitization by Nitric Oxide at Low Radiation Doses , 2007, Radiation research.

[216]  J. Weiss,et al.  Radioprotection by Antioxidants a , 2000, Annals of the New York Academy of Sciences.

[217]  Chryssostomos Chatgilialoglu,et al.  Sulfur-Centered Reactive Intermediates in Chemistry and Biology , 1990, NATO ASI Series.

[218]  J. Brown,et al.  Exploiting tumour hypoxia in cancer treatment , 2004, Nature Reviews Cancer.

[219]  P. van Houtte,et al.  Cysteine but not glutathione modulates the radiosensitivity of human melanoma cells by affecting both survival and DNA damage. , 2003, Pigment cell research.

[220]  George D Wilson,et al.  Biologic basis for combining drugs with radiation. , 2006, Seminars in radiation oncology.

[221]  J. Brown,et al.  Pre- and post-irradiation adiosensitization by SR 4233 , 1989 .

[222]  C. Coleman,et al.  Lisofylline as a modifier of radiation therapy. , 1996, Oncology research.

[223]  Benjamin Georgi,et al.  Low-dose hyperradiosensitivity of human glioblastoma cell lines in vitro does not translate into improved outcome of ultrafractionated radiotherapy in vivo , 2005, International journal of radiation biology.

[224]  J. Denekamp Limited role of vasculature-mediated injury in tumor response to radiotherapy. , 1993, Journal of the National Cancer Institute.

[225]  M. Stevenson,et al.  Anemia, tumor hypoxemia, and the cancer patient. , 2005, International journal of radiation oncology, biology, physics.

[226]  M. Lemmon,et al.  Potentiation by the hypoxic cytotoxin SR 4233 of cell killing produced by fractionated irradiation of mouse tumors. , 1990, Cancer research.

[227]  R. Handrick,et al.  Membrane targeted anticancer drugs: potent inducers of apoptosis and putative radiosensitisers. , 2003, Current medicinal chemistry. Anti-cancer agents.

[228]  M. Horsman Nicotinamide and the hypoxia problem. , 1991, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[229]  V. Grégoire,et al.  Potentiation of radiation‐induced regrowth delay by isosorbide dinitrate in FSaII murine tumors , 2003, International journal of cancer.

[230]  M. Stratford,et al.  Cellular uptake of misonidazole and analogues with acidic or basic functions. , 1985, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[231]  P. Wardman The kinetics of the reaction of 'anomalous' 4-nitroimidazole radiosensitizers with thiols. , 1982, International journal of radiation biology and related studies in physics, chemistry, and medicine.

[232]  J. Sarkaria,et al.  ATM as a target for novel radiosensitizers. , 2001, Seminars in radiation oncology.

[233]  G. Adams Hypoxia‐mediated druGS FOR RADIATION AND CHEMOTHERAPY , 1981 .

[234]  E. Rowinsky UFT and oral calcium folinate as first-line chemotherapy for metastatic gastric cancer. , 1999 .

[235]  Elke S. Bergmann-Leitner,et al.  Editorial [Hot Topic: Anti-Cancer Drugs Executive Editor: Elke Bergmann-Leitner] , 2005 .

[236]  P Lambin,et al.  Low-dose hypersensitivity: current status and possible mechanisms. , 2001, International journal of radiation oncology, biology, physics.

[237]  E. Wong,et al.  The role of topotecan in the treatment of brain metastases. , 2004, The oncologist.

[238]  P. Hoskin,et al.  Carbogen and nicotinamide in the treatment of bladder cancer with radical radiotherapy. , 1997, British Journal of Cancer.

[239]  Joe Y. Chang,et al.  A Phase I Clinical Trial of Thoracic Radiotherapy and Concurrent Celecoxib for Patients with Unfavorable Performance Status Inoperable/Unresectable Non–Small Cell Lung Cancer , 2005, Clinical Cancer Research.

[240]  Y. Nishimura,et al.  Phase III Trial of Radiosensitizer PR-350 Combined With Intraoperative Radiotherapy for the Treatment of Locally Advanced Pancreatic Cancer , 2004, Pancreas.

[241]  Joseph K Salama,et al.  The concurrent chemoradiation paradigm—general principles , 2007, Nature Clinical Practice Oncology.

[242]  A. Fornace,et al.  Enhancement of X ray induced DNA damage by pre-treatment with halogenated pyrimidine analogs. , 1987, International journal of radiation oncology, biology, physics.

[243]  G. Tozer,et al.  Nitric oxide in tumour biology and cancer therapy. Part 1: Physiological aspects. , 1997, Clinical oncology (Royal College of Radiologists (Great Britain)).

[244]  A. Meister,et al.  Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). , 1979, The Journal of biological chemistry.

[245]  J. Hendry,et al.  Tumor radiosensitizers--current status of development of various approaches: report of an International Atomic Energy Agency meeting. , 2006, International journal of radiation oncology, biology, physics.

[246]  J. Kaanders,et al.  Oxygen-modifying treatment with ARCON reduces the prognostic significance of hemoglobin in squamous cell carcinoma of the head and neck. , 2006, International journal of radiation oncology, biology, physics.

[247]  A. Saha,et al.  Influence of copper (II) ions and its derivatives on radiosensitivity of Escherichia coli , 2007 .

[248]  C. Koch,et al.  Radiation Response of Cells during Altered Protein Thiol Redox , 2003, Radiation research.

[249]  E. Shaw,et al.  Whole-brain radiotherapy with or without efaproxiral for the treatment of brain metastases: Determinants of response and its prognostic value for subsequent survival. , 2006, International journal of radiation oncology, biology, physics.

[250]  A. Rauth,et al.  An experimental and analytical study of oxygen depletion in stirred cell suspensions. , 1980, Radiation research.

[251]  H. Elsaleh,et al.  Radiation modifiers: treatment overview and future investigations. , 2006, Hematology/oncology clinics of North America.

[252]  Y. Shibamoto,et al.  Reevaluation of the radiosensitizing effects of sanazole and nimorazole in vitro and in vivo. , 2005, Journal of radiation research.