Smad7 foci are present in micronuclei induced by heavy particle radiation

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 756, Issue 1-2, 2013, Pages 108-114

  Wang, Minli ^a   Saha, Janapriya ^a   Cucinotta, Francis A ^b  

^a UNIVERSITIES SPACE RESEARCH ASSOCIATION   (United States)

^b NASA JOHNSON SPACE CENTER   (United States)

Author keywords

DNA repair; High LET radiation; Micronuclei; Smad7; TGF Smad pathway

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BORON; HISTONE H2AX; IRON; SMAD2 PROTEIN; SMAD7 PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; FIBROBLAST; HUMAN; HUMAN CELL; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MALE; MICRONUCLEUS; PARTICLE RADIATION; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN LOCALIZATION;

ATAXIA TELANGIECTASIA MUTATED; ATM; BNL; BROOKHAVEN NATIONAL LABORATORY; DDR; DNA DAMAGE RESPONSE; DNA REPAIR; DOUBLE STRAND BREAK; DSB; HIGH CHARGE AND ENERGY; HIGH LET RADIATION; HZE; IONIZING RADIATION; IR; IR-INDUCED FOCI; IRIF; LET; LINEAR ENERGY TRANSFER; MICRONUCLEI; MN; NASA SPACE RADIATION LABORATORY; NSRL; PHOSPHO-SMAD2; PSMAD2; REACTIVE OXYGEN SPECIES; ROS; SMAD7; TGFΒ; TGFΒ/SMAD PATHWAY; TRANSFORMING GROWTH FACTOR BETA;

ACTIVATING TRANSCRIPTION FACTOR 2; ADULT; CELL CYCLE PROTEINS; CELL NUCLEUS; CELLS, CULTURED; CESIUM RADIOISOTOPES; DNA-BINDING PROTEINS; ESOPHAGUS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA RAYS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LINEAR ENERGY TRANSFER; MALE; MICRONUCLEUS TESTS; PHOSPHORYLATION; PROSTATIC NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES; SKIN; SMAD2 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEINS;

EID: 84884209773     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2013.04.011     Document Type: Article

References (45)

1. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
2. Goodhead D.T., Thacker J., Cox R. Effects of radiations of different qualities on cells: molecular mechanisms of damage and repair. Int. J. Radiat. Biol. 1993, 63:543-556.
3. Cucinotta F.A., Nikjoo H., Goodhead D.T. Model of the radial distribution of energy imparted in nanometer volumes from HZE particle. Radiat. Res. 2000, 153:459-468.
4. Prise K.M., Pinto M., Newman H.C., Michael B.D. A review of studies of ionizing radiation-induced double-strand break clustering. Radiat. Res. 2001, 156:572-576.
5. Feinendegen L.E. Reactive oxygen species in cell responses to toxic agents. Hum. Exp. Toxicol. 2002, 21:85-90.
6. Wang M., Saha J., Hada M., Anderson J., Pluth J., O'Neill P., Cucinotta F.A. Novel Smad proteins localize to IR-induced double-strand breaks: interplay between TGFβ and ATM pathways. Nuclear Acid Res. 2013, 41:933-942.
7. Fernandez-Capetillo O., Celeste A., Nussenzweig A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2003, 2:426-427.
8. Rappold I., Iwabuchi K., Date T., Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 2001, 153:613-620.
9. Bhoumik A., Takahashi S., Breitweiser W., Shiloh Y., Jones N., Ronai Z. ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol. Cell 2005, 18:577-587.
10. Whalen M.K., Gurai S.K., Zahed-Kargaran H., Pluth J.M. Specific ATM-mediated phosphorylation dependent on radiation quality. Radiat. Res. 2008, 150:353-364.
11. Cucinotta F.A., Pluth J.M., Anderson J.A., Harper J.V., O'Neill P. Biochemical Kinetics model of DSB repair and induction of γ-H2AX foci by non-homologous end joining. Radiat. Res. 2008, 169:214-222.
12. Kinner A., Wu W., Staudt C., Iliakis G. γ-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008, 36:5678-5694.
13. Kirshner J., Jobling M.F., Pajares M.J., Ravani S.A., Glick A.B., Lavin M.J., Koslov S., Shiloh Y., Barcellos-Hoff M.H. Inhibition of transforming growth factor-beta1 signaling attenuates ataxia telangiectasia mutated activity in response to genotoxic stress. Cancer Res. 2006, 66:10861-10869.
14. Derynck R., Akhurst R.J., Balmain A. TGFβ signaling in tumor suppression and cancer progression. Nat. Genet. 2001, 29:117-129.
15. Levy L., Hill C.S. Smad4 dependency defines two classes of transforming growth factor beta target genes and distinguishes TGFβ-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol. Cell Biol. 2005, 25:8108-8125.
16. Hayashi H., Abdollah S., Qiu Y., Cai J., Xu Y.Y., Grinnell B.W., Richardson M.A., Topper J.N., Gimbrone M.A.J.J.L. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997, 9:1165-1173.
17. Simonsson M., Heldin C.H., Ericsson J., Gronroos E. The balance between acetylation and deacetylation controls Smad7 stability. J. Biol. Chem. 2005, 280:21797-21803.
18. Kume S., Haneda M., Kanasaki K., Sugimoto T., Araki S., Isshiki K., Isono M., Uzu T., Guarente L., Kashiwagi A., Koya D. SIRT1 inhibits transforming growth factor β-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J. Biol. Chem. 2007, 282:151-158.
19. Zhang S., Ekman M., Thakur N., Bu S., Davoodpour P., Grimsby S., Tagami S., Heldin C.H., Landström M. TGFbeta1-induced activation of ATM and p53 mediates apoptosis in a Smad7-dependent manner. Cell Cycle 2006, 5:2787-2795.
20. Hoot K.E., Lighthall J., Han G., Lu S.H., Li A., Ju W., Kulesz-Martin M., Bottinger E., Wang X.J. Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J. Clin. Invest. 2008, 118:2722-2732.
21. Hamamoto T., Beppu H., Okada H., Kawabata M., Kitamura T., Miyazono K., Kat M. Compound disruption of Smad2 accelerates malignant progression of intestinal tumors in Apc Knockout Mice. Cancer Res. 2002, 62:5955-5961.
22. Afrakhte M., Moren A., Jossan S., Itoh S., Sampath K., Westermark B., Heldin C.H., Heldin N.E., ten Dijke P. Induction of inhibitory Smad6 and Smad7 mRNA by TGF-β family members. Biochem. Biophys. Res. Commun. 1998, 249:505-511.
23. Bitzer M., von Gersdorff G., Liang D., Dominguez-Rosales A., Beg A.A., Rojkind M., Böttinger E.P. A mechanism of suppression of TGF-beta/SMAD signaling by NF-kappa B/RelA. Genes Dev. 2000, 14:187-197.
24. Quan T., He T., Voorhees J.J., Fisher G.J. Ultraviolet irradiation induces Smad7 via induction of transcription factor AP-1 in human skin fibroblasts. J. Biol. Chem. 2005, 280:8079-8085.
25. He W., Cao T., Smith D.A., Myers T.E., Wang X.J. Smads mediate signaling of the TGFbeta superfamily in normal keratinocytes but are lost during skin chemical carcinogenesis. Oncogene 2001, 20:471-483.
26. Kleeff J., Ishiwata T., Maruyama H., Friess H., Truong P., Buchler M.W., Falb D., Korc M. The TGF-β signaling inhibitor Smad7 enhances tumorigenicity in pancreatic cancer. Oncogene 1999, 18:5363-5372.
27. Liu X., Lee J., Cooley M., Bhogte E., Hartley S., Glick A. Smad7 but not Smad6 cooperates with oncogenic ras to cause malignant conversion in a mouse model for squamous cell carcinoma. Cancer Res. 2003, 63:7760-7768.
28. Bonassi S., Znaor A., Ceppi M., Lando C., Chang W.P., et al. An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis 2007, 28:625-631.
29. Vukovic B., Beheshti B., Park P., Lim G., Bayani J., Zielenska M., Squire J.A. Correlating breakage-fusion-bridge events with the overall chromosomal instability and in vitro karyotype evolution in prostate cancer. Cytogenet. Genome Res. 2007, 116:1-11.
30. Fenech M., Kirsch-Volders M., Natarajan A.T., Surralles J., Crott J.W., Parry J., Norppa H., Eastmond D.A., Tucker J.D., Thomas P. Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 2011, 26:125-132.
31. Medvedeva N.G., Panyutin I.V., Panyutin I.G., Neumann R.D. Phosphorylation of histone H2AX in radiation-induced micronuclei. Radiat. Res. 2007, 168:493-498.
32. Yoshikawa T., Kashino G., Ono K., Watanabe M. Phosphorylated H2AX foci in tumor cells have no correlation with their radiation sensitivities. J. Radiat. Res. 2009, 50:151-160.
33. Wang M., Hada M., Saha J., Sridharan D.M., Pluth J., Cucinotta F.A. Protons sensitize epithelial to mesenchymal transition. PLoS ONE 2012, 7(7):e41249.
34. Fenech M. The in vitro micronucleus technique. Mutat. Res. 2000, 455:81-95.
35. Terradas M., Martín M., Tusell L.A., Genescà A. DNA lesions sequestered in micronuclei induce a local defective-damage response. DNA Repair (Amst.) 2009, 8:1225-1234.
36. Cucinotta F.A., Katz R., Wilson J.W., Townsend L.W., Shinn J.L. Biological effectiveness of high-energy protons: target fragmentation. Radiat. Res. 1991, 127:130-137.
37. Pandita T.K., Richardson C. Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res. 2009, 37:1363-1377.
38. Emori T., Kitamura K., Okazaki K. Nuclear Smad7 overexpressed in mesenchymal cells acts as a transcriptional corepressor by interacting with HDAC-1 and E2F to regulate cell cycle. Biol. Open 2012, 1:247-260.
39. Gronroos E., Hellman U., Heldin C.H., Ericsson J. Control of Smad7 stability by competition between acetylation and ubiquitination. Mol. Cell 2002, 10:483-493.
40. Innocente S.A., Abrahamson J.L., Cogswell J.P., Lee J.M. p53 regulates a G2 checkpoint through cyclin B1. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:2147-2152.
41. Scott S.L., Earle J.D., Gumerlock P.H. Functional p53 increases prostate cancer cell survival after exposure to fractionated doses of ionizing radiation. Cancer Res. 2003, 63:7190-7196.
42. Lallemand F., Mazars A., Prunier C., Bertrand F., Kornprost M., Gallea S., Roman-Roman S., Cherqui G., Atfi A. Smad7 inhibits the survival nuclear factor kappaB and potentiates apoptosis in epithelial cells. Oncogene 2001, 20:879-884.
43. Hong S., Lee C., Kim S.J. Smad7 sensitizes tumor necrosis factor induced apoptosis through the inhibition of antiapoptotic gene expression by suppressing activation of the nuclear factor-kappaB pathway. Cancer Res. 2007, 67:9577-9583.
44. Edlund S., Lee S.Y., Grimsby S., Zhang S., Aspenström P., Heldin C.H., Landström M. Interaction between Smad7 and beta-catenin: importance for transforming growth factor beta-induced apoptosis. Mol. Cell Biol. 2005, 25:1475-1488.
45. Landström M., Heldin N.E., Bu S., Hermansson A., Itoh S., ten Dijke P., Heldin C.H. Smad7 mediates apoptosis induced by transforming growth factor beta in prostatic carcinoma cells. Curr. Biol. 2000, 10:535-538.