Chronic sub-lethal oxidative stress by spermine oxidase overactivity induces continuous DNA repair and hypersensitivity to radiation exposure

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1773, Issue 6, 2007, Pages 774-783

  Bianchi, M ^a,b   Bellini, A ^a,b   Cervelli, M ^b   Degan, P ^c   Marcocci, L ^d   Martini, F ^e   Scatteia, M ^a,b   Mariottini, P ^b   Amendola, R ^a  

^a ENEA   (Italy)

^b ROMA TRE UNIVERSITY   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e NATIONAL INSTITUTE FOR INFECTIOUS DISEASES L SPALLANZANI   (Italy)

Author keywords

DNA damage; DNA repair; Oxidative stress; Radiation; Spermine oxidase

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; ORNITHINE DECARBOXYLASE; OXIDOREDUCTASE; SPERMIDINE DERIVATIVE; SPERMIDINE SPERMINE N 1 ACETYLTRANSFERASE; SPERMINE OXIDASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; HYPERSENSITIVITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RADIATION EXPOSURE;

AGING; ANIMALS; CELL DEATH; CELL LINE, TUMOR; CELL PROLIFERATION; DNA DAMAGE; DNA REPAIR; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HISTONES; MICE; OXIDATIVE STRESS; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; X-RAYS;

MURINAE;

EID: 34249748927     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.01.014     Document Type: Article

References (53)

1. Ames B.N., Shigenaga M.K., and Hagen T.M. Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 7915-7922
2. Kamata H., Honda S., Maeda S., Chang L., Hirata H., and Karin M. Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 120 (2005) 649-661
3. Goldman M. Cancer risk of low-level exposure. Science 271 (1996) 1821-1822
4. Dennog C., Hartmann A., Frey G., and Speit G. Detection of DNA damage after hyperbaric oxygen (HBO) therapy. Mutagenesis 11 (1996) 605-609
5. Zastawny T.H., Czerwinska B., Drzewiecka B., and Olinski R. Radiation-induced oxidative DNA base damage and its repair in nuclear matrix-associated DNA and in bulk DNA in hepatic chromatin of rat upon whole-body gamma-irradiation. Free Radical Biol. Med. 22 (1997) 101-107
6. Beckman K.B., and Ames B.N. Oxidative decay of DNA. J. Biol. Chem. 272 (1997) 19633-19636
7. Zhou B.-B., and Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 408 (2000) 433-439
8. Wallace H.M., Fraser A.V., and Hughes A. A perspective of polyamine metabolism. Biochem. J. 376 (2003) 1-14
9. Schiller M., Blank N., Heyeder P., Herrmann M., Gaipl U.S., Kalden J.R., and Lorenz H.-M. Induction of apoptosis by spermine-metabolites in primary human blood cells and various tumor cell lines. Apoptosis 10 (2005) 1151-1162
10. Calcabrini A., Arancia G., Marra M., Crateri P., Befani O., Martone A., and Agostinelli E. Enzymatic oxidation products of spermine induce greater cytotoxic effects on human multidrug-resistant colon carcinoma cells [LoVo] than on their wild-type counterparts. Int. J. Cancer 99 (2002) 43-52
11. 2 in polyamine analogue-treated human breast cancer cell lines. J. Biol. Chem. 280 (2005) 39843-39851
12. Amendola R., Bellini A., Cervelli M., Degan P., Marcocci L., Martini F., and Mariottini P. Direct oxidative DNA damage, apoptosis and radio sensitivity by spermine oxidase activities in mouse neuroblastoma cells. Biochim. Biophysic. Acta Rev. Cancer 1755 (2005) 15-24
13. Nicoletti I., Migliorati G., Pagliacci M.C., Grignani F., and Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139 (1991) 271-279
14. Pfaffl M.W., Horgan G.H., and Demplfe L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30 (2002) e36
15. Chen Y., Vujcic S., Liang P., Diegelman P., Kramer D.L., and Porter C.W. Genomic identification and biochemical characterization of a second spermidine/spermine N1-acetyltransferase. Biochem. J. 373 (2003) 661-667
16. Hockenbery D.M., Oltval Z.N., Yin X.-M., Milliman C.L., and Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75 (1993) 241-251
17. Fiers W., Beyaert R., Declercq W., and Vandenabeele P. More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene 18 (1999) 7719-7730
18. Herceg Z., and Wang Z.-Q. Functions of poly[ADP-ribose] polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477 (2001) 97-110
19. Holgersson A., Jernberg A.R., Persson L.M., Edgren M.R., Lewensohn R., Nilsson A., Brahme A., and Meijer A.E. Low and high LET radiation-induced apoptosis in M059J and M059K cells. Int. J. Radiat. Biol. 79 (2003) 611-621
20. Ha H.C., Woster P.M., Yager J.D., and Casero Jr. R.A. The role of polyamine catabolism in polyamine analogue-induced programmed cell death. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 11557-11562
21. Grassilli E., Desiderio M.A., Bellesia E., Salomoni P., Benfatti F., and Franceschi C. Is polyamine decrease a common feature of apoptosis? Evidence from gamma rays- and heat shock-induced cell death. Biochem. Biophysi. Res. Commun. 216 (1995) 708-714
22. Lindsay G.S., and Wallace H.M. Changes in polyamine catabolism in HL-60 human promyelogenous leukaemic cells in response to etoposide-induced apoptosis. Biochem. J. 337 (1999) 83-87
23. Piacentini M., Davies P.J., and Fesus L. The molecular basis of apoptosis in diseases. In: Tomei L.D., and Cope F.O. (Eds). Apoptosis II (1994), Cold Spring Harbor Laboratory Press, New York 143-164
24. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
25. Cadet J., Douki T., Gasparutto D., and Ravanat J.L. Oxidative damage to DNA: formation, measurement and biochemical features. Mutat. Res. 531 (2003) 5-23
26. Dypbukt J.M., Ankarcrona M., Burkitt M., Sjoholm, Strom K., Orrenius S., and Nicotera P. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J. Biol. Chem. 269 (1994) 30553-30560
27. Dai H., Kramer D.L., Gopal Murti K., Porter C.W., and Cleveland J.L. The polyamine oxidase inhibitor MDL-72,527 selectively induces apoptosis of transformed hematopoietic cells through lysosomotropic effects. Cancer Res. 59 (1999) 4944-4954
28. Bianchi M., Polticelli F., Ascenzi P., Botta M., Federico R., Mariottini P., and Cona A. Inhibition of polyamine and spermine oxidases by polyamine analogues. FEBS J. 273 (2006) 1115-1123
29. Ramana C.V., Boldogh I., Izumi T., and Mitra S. Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 5061-5066
30. Allinson S.L., Dianova I.L., and Dianov G.L. DNA polymerase beta is the major dRP lyase involved in repair of oxidative base lesions in DNA by mammalian cell extracts. EMBO J. 23 (2001) 6919-6926
31. Meira L.B., Devaraj S., Kisby G.E., Burns D.K., Daniel R.L., Hammer R.E., Grundy S., Jialal I., and Friedberg E.C. Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress. Cancer Res. 61 (2001) 5552-5557
32. Wilson S.H., and Kundel T.A. Passing the baton in base excision repair. Nat. Struct. Biol. 7 (2000) 176-178
33. Vidal A.E., Boiteux S., Hickson I.D., and Radicella J.P. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J. 20 (2001) 6530-6539
34. Raffoul J.J., Cabelof D.C., Nakamura J., Meira L.B., Friedberg E.C., and Heydari A.R. Apurinic/apyrimidinic endonuclease (APE/REF-1) haploinsufficient mice display tissue-specific differences in DNA polymerase beta-dependent base excision repair. J. Biol. Chem. 279 (2004) 18425-18433
35. Hill J.W., Hazra T.K., Izumi T., and Mitra S. Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29 (2001) 430-438
36. Vidal A.E., Hickson I.D., Boiteux S.J., and Radicella P. Mechanism of stimulation of the DNA glycosylase activity of hOGG1 by the major human AP endonuclease: bypass of the AP lyase activity step. Nucleic Acids Res. 29 (2001) 1285-1292
37. Rogakou E.P., Nieves-Niera W., Boon C., Pommier, and Bonner W.M. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 275 (2000) 9390-9395
38. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
39. Banath J.P., MacPhail S.H., and Olive P.L. Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res. 64 (2004) 7144-7149
40. Wang H., Wang M., Wang H., Bocker W., and Iliakis G. Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J. Cell. Physiol. 202 (2005) 492-502
41. Huang X., Okafuji M., Traganos F., Luther E., Holden E., and Darzynkiewicz Z. Assessment of histone H2AX phosphorylation induced by DNA topoisomerase I and II inhibitors topotecan and mitoxantrone and by the DNA cross-linking agent cisplatin. Cytometry 58 (2004) 99-110
42. Furuta T., Takemura H., Liao Z.-Y., Aune G.J., Redon C., Sedelnikova O.A., Pilch D.R., Rogakou E.P., Celeste A., Chen H.T., Nussenzweig A., Aladjem M.I., Bonner W.M., and Pommier Y. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J. Biol. Chem. 278 (2003) 20303-20312
43. Wang J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3 (2002) 430-440
44. Sordet O., Khan Q.A., Plo I., Pourquier P., Urasaki Y., Yoshida A., Antony S., Kohlagen G., Solary E., Saparbaev M., Laval J., and Pommier Y. Apoptotic topoisomerase I-DNA complexes induced by staurosporine-mediated oxygen radicals. J. Biol. Chem. 279 (2004) 50499-50504
45. Rothkamm K., and Lobrich M. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5057-5062
46. MacPhail S.H., Banath J.P., Yu T.Y., Chu E.H., Lambur H., and Olive P.L. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int. J. Radiat. Biol. 79 (2003) 351-358
47. Fernandez-Capetillo O., Chen H.-T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero R.D., Motoyama N., Carpenter P.B., Bonner W.M., Chen J., and Nussenzweig A. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4 (2002) 993-997
48. Bartkova J., Horejsi Z., Koed K., Tort F., Zieger K., Guidberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
49. Gorgoulis V.G., Vassilliou L.-V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., DiTullio Jr. R.A., Kastrinakis N.G., Levy B., Kietsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
50. Marples B., and Joiner M.C. The elimination of low-dose hypersensitivity in Chinese hamster V79-379A cells by pretreatment with X rays or hydrogen peroxide. Radiat. Res. 141 (1995) 160-169
51. Marples B., Wouters B.G., Collis S.J., Chalmers A.J., and Joiner M.C. Low-dose hyper-radiosensitivity: a consequence of ineffective cell cycle arrest of radiation-damaged G2-phase cells. Radiat. Res. 161 (2004) 247-255
52. Cervelli M., Bellini A., Bianchi M., Marcocci L., Nocera S., Ponticelli F., Federico R., Amendola R., and Mariottini P. Mouse spermine oxidase gene splice variants. Nuclear subcellular localization of a novel active isoform. Eur. J. Biochem. 271 (2004) 1-11
53. Taneja N., Davis M., Choy J.S., Beckett M.A., Singh R., Kron S.J., and Weichselbaum R.R. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J. Biol. Chem. 279 (2004) 2273-2280