Localized Irradiation of Cell Membrane by Auger Electrons Is Cytotoxic Through Oxidative Stress-Mediated Nontargeted Effects

Antioxidants and Redox Signaling

Volumn 25, Issue 8, 2016, Pages 467-484

  Paillas, Salomé ^a,b,c,d   Ladjohounlou, Riad ^a,b,c   Lozza, Catherine ^a,b,c   Pichard, Alexandre ^a,b,c   Boudousq, Vincent ^a,b,c   Jarlier, Marta ^c   Sevestre, Samuel ^a,b,c   Le Blay, Marion ^a,b,c   Deshayes, Emmanuel ^a,b,c   Sosabowski, Jane ^d   Chardès, Thierry ^a,b,c   Navarro Teulon, Isabelle ^a,b,c   Mairs, Robert J ^e   Pouget, Jean Pierre ^a,b,c  

^a INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^b UNIV MONTPELLIER   (France)

^c CENTRE VAL D AURELLE   (France)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CARCINOEMBRYONIC ANTIGEN MONOCLONAL ANTIBODY; CELL SURFACE RECEPTOR; DEOXYURIDINE; DEOXYURIDINE DERIVATIVE; FILIPIN; FOCAL ADHESION KINASE 2; METHYL BETA CYCLODEXTRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCLONAL ANTIBODY I 125; PAXILLIN; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEIN; PROTEIN C JUN; PROTEIN KINASE B; PROTEIN P53; SCAVENGER; SPHINGOMYELIN PHOSPHODIESTERASE; ANTIBODY CONJUGATE; RADIOACTIVE IODINE; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUGER ELECTRON SPECTROSCOPY; CANCER CELL; CANCER SURVIVAL; CELL DISRUPTION; CELL MEMBRANE; CELL SURFACE; COLON CANCER; CYTOTOXICITY; DNA DAMAGE; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; IRRADIATION; LIPID RAFT; LOW ENERGY RADIATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR VOLUME; BIOLOGICAL MODEL; CELL SURVIVAL; DRUG EFFECTS; ELECTRON; GENE INACTIVATION; GENETICS; HCT 116 CELL LINE; MEMBRANE MICRODOMAIN; METABOLISM; RADIATION RESPONSE; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

CELL LINE, TUMOR; CELL MEMBRANE; CELL SURVIVAL; DNA DAMAGE; ELECTRONS; GENE KNOCKOUT TECHNIQUES; GENES, P53; HCT116 CELLS; HUMANS; IMMUNOCONJUGATES; IODINE RADIOISOTOPES; MAP KINASE SIGNALING SYSTEM; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PHOSPHOPROTEINS; REACTIVE OXYGEN SPECIES;

EID: 84984924920     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2015.6309     Document Type: Article

References (68)

1. Anthony LB, et al. Indium-111-pentetreotide prolongs survival in gastroenteropancreatic malignancies. Semin Nucl Med 32: 123-132, 2002.
2. Azzam EI, de Toledo SM, and Little JB. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 22: 7050-7057, 2003.
3. Azzam EI, et al. Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from alpha-particle-irradiated normal human fibroblast cultures. Cancer Res 62: 5436-5442, 2002.
4. Belyakov OV, et al. Delayed lethality, apoptosis and micronucleus formation in human fibroblasts irradiated with X-rays or alpha-particles. Int J Radiat Biol 75: 985-993, 1999.
5. Bishayee A, Rao DV, and Howell RW. Evidence for pronounced bystander effects caused by nonuniform distributions of radioactivity using a novel three-dimensional tissue culture model. Radiat Res 152: 88-97, 1999.
6. Boyd M, et al. Radiation-induced biologic bystander effect elicited in vitro by targeted radiopharmaceuticals labeled with alpha-, beta-, and auger electron-emitting radionuclides. J Nucl Med 47: 1007-1015, 2006.
7. Bradley EW, Chan PC, and Adelstein SJ. The radiotoxicity of iodine-125 in mammalian cells. I. Effects on the survival curve of radioiodine incorporated into DNA. Radiat Res 64: 555-563, 1975.
8. Chalfant CE, et al. Long chain ceramides activate protein phosphatase-1 and protein phosphatase-2A. Activation is stereospecific and regulated by phosphatidic acid. J Biol Chem 274: 20313-20317, 1999.
9. Chen P, et al. Antitumor effects and normal tissue toxicity of 111In-labeled epidermal growth factor administered to athymic mice bearing epidermal growth factor receptorpositive human breast cancer xenografts. J Nucl Med 44: 1469-1478, 2003.
10. Chouin N, et al. Evidence of extranuclear cell sensitivity to alpha-particle radiation using a microdosimetric model. II. Application of the microdosimetric model to experimental results. Radiat Res 171: 664-673, 2009.
11. Church LD, et al. TNFR1-induced sphingomyelinase activation modulates TCR signaling by impairing storeoperated Ca2+ influx. J Leukoc Biol 78: 266-278, 2005.
12. Commerford SL, et al. Radiotoxicity of intranuclear 125I atoms not bound to DNA. Int J Radiat Biol Relat Stud Phys Chem Med 37: 547-554, 1980.
13. Cordes N, et al. Human pancreatic tumor cells are sensitized to ionizing radiation by knockdown of caveolin-1. Oncogene 26: 6851-6862, 2007.
14. Costantini DL, et al. 111In-labeled trastuzumab (herceptin) modified with nuclear localization sequences (NLS): an Auger electron-emitting radiotherapeutic agent for HER2/ neu-amplified breast cancer. J Nucl Med 48: 1357-1368, 2007.
15. Costantini DL, et al. Antitumor effects and normal-tissue toxicity of 111In-nuclear localization sequence-trastuzumab in athymic mice bearing HER-positive human breast cancer xenografts. J Nucl Med 51: 1084-1091, 2010.
16. Delpassand ES, et al. Safety and efficacy of radionuclide therapy with high-activity In-111 pentetreotide in patients with progressive neuroendocrine tumors. Cancer Biother Radiopharm 23: 292-300, 2008.
17. DeSombre ER, et al. Therapy of estrogen receptor-positive micrometastases in the peritoneal cavity with Auger electron-emitting estrogens - Theoretical and practical considerations. Acta Oncol 39: 659-666, 2000.
18. Galanis E, et al. Phase I trial of sequential administration of raltitrexed (Tomudex) and 5-iodo-2'-deoxyuridine (IdUrd). Ann Oncol 12: 701-707, 2001.
19. Hamada N. Evidence and significance of non-targeted effects of ionizing radiation. Curr Mol Pharmacol 4: 78, 2011.
20. Havaki S, et al. The role of oxidative DNA damage in radiation induced bystander effect. Cancer Lett 356: 43-51, 2015.
21. Hehlgans S, Eke I, and Cordes N. Targeting FAK radiosensitizes 3-dimensional grown human HNSCC cells through reduced Akt1 and MEK1/2 signaling. Int J Radiat Oncol Biol Phys 83: e669-e676, 2012.
22. Hofer KG and Hughes WL. Radiotoxicity of intranuclear tritium, 125 iodine and 131 iodine. Radiat Res 47: 94-101, 1971.
23. Humm JL, Howell RW, and Rao DV. Dosimetry of Augerelectron-emitting radionuclides: Report no. 3 of AAPM Nuclear Medicine Task Group No. 6. Med Phys 21: 1901-1915, 1994.
24. ICRP, A.o.t. (Ed). The 2007 Recommendations of the International Commission on Radiological Protection. Oxford: Elsevier, Vol. 37, 2007.
25. Kassis AI. Radiotargeting agents for cancer therapy. Expert Opin Drug Deliv 2: 981-991, 2005.
26. Kassis AI, et al. Lethality of Auger electrons from the decay of bromine-77 in the DNA of mammalian cells. Radiat Res 90: 362-373, 1982.
27. Kassis AI, et al. Radiotoxicity of an 125I-labeled DNA intercalator in mammalian cells. Radiat Res 118: 283-294, 1989.
28. Kassis AI, et al. Radiotoxicity of 125I in mammalian cells. Radiat Res 111: 305-318, 1987.
29. Kassis AI, Sastry KS, and Adelstein SJ. Kinetics of uptake, retention, and radiotoxicity of 125IUdR in mammalian cells: Implications of localized energy deposition by Auger processes. Radiat Res 109: 78-89, 1987.
30. Kohler G, Howe SC, and Milstein C. Fusion between immunoglobulin-secreting and nonsecreting myeloma cell lines. Eur J Immunol 6: 292-295, 1976.
31. Krenning EP, et al. The role of radioactive somatostatin and its analogues in the control of tumor growth. Recent Results Cancer Res 153: 1-13, 2000.
32. Lajoie P, et al. Caveolin-1 regulation of dynamindependent, raft-mediated endocytosis of cholera toxin-B sub-unit occurs independently of caveolae. J Cell Mol Med 13: 3218-3225, 2009.
33. Lehnert BE, Goodwin EH, and Deshpande A. Extracellular factor(s) following exposure to alpha particles can cause sister chromatid exchanges in normal human cells. Cancer Res 57: 2164-2171, 1997.
34. Lev S, et al. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376: 737-745, 1995.
35. Li L, et al. A Phase II study of anti-epidermal growth factor receptor radioimmunotherapy in the treatment of glioblastoma multiforme. J Neurosurg 113: 192-198, 2010.
36. Li PL and Gulbins E. Lipid rafts and redox signaling. Antioxid Redox Signal 9: 1411-1415, 2007.
37. Limouris GS, et al. Selective hepatic arterial infusion of In-111-DTPA-Phe1-octreotide in neuroendocrine liver metastases. Eur J Nucl Med Mol Imaging 35: 1827-1837, 2008.
38. Lyng FM, et al. The involvement of calcium and MAP kinase signaling pathways in the production of radiationinduced bystander effects. Radiat Res 165: 400-409, 2006.
39. Lyng FM, Seymour CB, and Mothersill C. Initiation of apoptosis in cells exposed to medium from the progeny of irradiated cells: A possible mechanism for bystanderinduced genomic instability? Radiat Res 157: 365-370, 2002.
40. Macapinlac HA, et al. Pilot clinical trial of 5-[125I]iodo-2′-deoxyuridine in the treatment of colorectal cancer metastatic to the liver. J Nucl Med 37: 25S-29S, 1996.
41. Mariani G, et al. Tumor targeting in vivo and metabolic fate of 5-[iodine-125]iodo-2′-deoxyuridine following intratumoral injection in patients with colorectal cancer. J Nucl Med 34: 1175-1183, 1993.
42. Mothersill C and Seymour CB. Cell-cell contact during gamma irradiation is not required to induce a bystander effect in normal human keratinocytes: Evidence for release during irradiation of a signal controlling survival into the medium. Radiat Res 149: 256-262, 1998.
43. Nagasawa H, et al. Involvement of membrane signaling in the bystander effect in irradiated cells. Cancer Res 62: 2531-2534, 2002.
44. Narayanan PK, Goodwin EH, and Lehnert BE. Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res 57: 3963-3971, 1997.
45. Oskouian B and Saba JD. Cancer treatment strategies targeting sphingolipid metabolism. Adv Exp Med Biol 688: 185-205, 2010.
46. Paillas S, et al. Apoptosis and p53 are not involved in the anti-tumor efficacy of 125I-labeled monoclonal antibodies targeting the cell membrane. Nucl Med Biol 40: 471-480, 2013.
47. Patel HH, Murray F, and Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48: 359-391, 2008.
48. Piron B, et al. DNA damage-centered signaling pathways are effectively activated during low dose-rate Auger radioimmunotherapy. Nucl Med Biol 41 Suppl: e75-e83, 2014.
49. Pomplun E, Booz J, and Charlton DE. A Monte Carlo simulation of Auger cascades. Radiat Res 111: 533-552, 1987.
50. Pouget JP, et al. Cell membrane is a more sensitive target than cytoplasm to dense ionization produced by auger electrons. Radiat Res 170: 192-200, 2008.
51. Prise KM and O'Sullivan JM. Radiation-induced bystander signalling in cancer therapy. Nat Rev Cancer 9: 351-360, 2009.
52. Quang TS and Brady LW. Radioimmunotherapy as a novel treatment regimen: 125I-labeled monoclonal antibody 425 in the treatment of high-grade brain gliomas. Int J Radiat Oncol Biol Phys 58: 972-975, 2004.
53. Santoro L, et al. Noninternalizing monoclonal antibodies are suitable candidates for 125I radioimmunotherapy of small-volume peritoneal carcinomatosis. J Nucl Med 50: 2033-2041, 2009.
54. Sastry KS and Rao DV. Dosimetry of low energy electrons. In: Physics of Nuclear Medicine: Recent Advances, edited by Rao DV, Chandra R, and Graham MC. New York: American Institute of Physics, 1984, pp. 169-208.
55. Sawant SG, et al. The bystander effect in radiation oncogenesis: I. Transformation in C3H 10T1/2 cells in vitro can be initiated in the unirradiated neighbors of irradiated cells. Radiat Res 155: 397-401, 2001.
56. Scheel-Toellner D, et al. Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104: 2557-2564, 2004.
57. Singer SJ, and Nicolson GL. The fluid mosaic model of the structure of cell membranes. Science 175: 720-731, 1972.
58. Sisson JC, et al. Treatment of neuroblastoma with. 125I metaiodobenzylguanidine. J Nucl Biol Med 35: 255-259, 1991.
59. Smith EL and Schuchman EH. The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J 22: 3419-3431, 2008.
60. Todd DG, et al. Ionizing radiation stimulates existing signal transduction pathways involving the activation of epidermal growth factor receptor and ERBB-3, and changes of intracellular calcium in A431 human squamous carcinoma cells. J Recept Signal Transduct Res 19: 885-908, 1999.
61. Valerie K, et al. Radiation-induced cell signaling: insideout and outside-in. Mol Cancer Ther 6: 789-801, 2007.
62. Vallis KA, et al. Phase I trial to evaluate the tumor and normal tissue uptake, radiation dosimetry and safety of (111)In-DTPA-human epidermal growth factor in patients with metastatic EGFR-positive breast cancer. Am J Nucl Med Mol Imaging 4: 181-192, 2014.
63. Walicka MA, Adelstein SJ, and Kassis AI. Indirect mechanisms contribute to biological effects produced by decay of DNA-incorporated iodine-125 in mammalian cells in vitro: clonogenic survival. Radiat Res 149: 142-146, 1998.
64. Walicka MA, Adelstein SJ, and Kassis AI. Indirect mechanisms contribute to biological effects produced by decay of DNA-incorporated iodine-125 in mammalian cells in vitro: double-strand breaks. Radiat Res 149: 134-141, 1998.
65. Welt S, et al. Phase I/II study of iodine 125-labeled monoclonal antibody A33 in patients with advanced colon cancer. J Clin Oncol 14: 1787-1797, 1996.
66. Xue LY, et al. Bystander effect produced by radiolabeled tumor cells in vivo. Proc Natl Acad Sci U S A 99: 13765-13770, 2002.
67. Zhang AY, et al. Acid sphingomyelinase and its redox amplification in formation of lipid raft redox signaling platforms in endothelial cells. Antioxid Redox Signal 9: 817-828, 2007.
68. Zhang Y, et al. Ceramide-enriched membrane domains - Structure and function. Biochim Biophys Acta 1788: 178-183, 2009.