The radioprotector Bowman-Birk proteinase inhibitor stimulates DNA repair via epidermal growth factor receptor phosphorylation and nuclear transport

Radiotherapy and Oncology

Volumn 86, Issue 3, 2008, Pages 375-382

  Dittmann, Klaus ^a   Mayer, Claus ^a   Kehlbach, Rainer ^b   Rodemann, H Peter ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Department of Radiology ^*  (Germany)

Author keywords

BBI; DNA repair; EGFR; MDC1; TP53

Indexed keywords

BOWMAN BIRK INHIBITOR; DOUBLE STRANDED DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEINASE INHIBITOR;

ARTICLE; CONTROLLED STUDY; DNA REPAIR; DRUG MECHANISM; HUMAN; HUMAN CELL; IN VITRO STUDY; IRRADIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ACTIVE TRANSPORT, CELL NUCLEUS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL NUCLEUS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; GENE EXPRESSION; HUMANS; MICROSCOPY, CONFOCAL; NUCLEAR PROTEINS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SERINE PROTEINASE INHIBITORS; TRANS-ACTIVATORS; TRYPSIN INHIBITOR, BOWMAN-BIRK SOYBEAN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 40249091300     PISSN: 01678140     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.radonc.2008.01.007     Document Type: Article

References (47)

1. Billings P.C., Newberne P.M., and Kennedy A.R. Protease inhibitor suppression of colon and anal gland carcinogenesis induced by dimethylhydrazine. Carcinogenesis 11 (1990) 1083-1086
2. Kennedy A.R., Billings P.C., Maki P.A., and Newberne P. Effects of various preparations of dietary protease inhibitors on oral carcinogenesis in hamsters induced by DMBA. Nutr Cancer 19 (1993) 191-200
3. Kennedy A.R., Szuhaj B.F., Newberne P.M., and Billings P.C. Preparation and production of a cancer chemopreventive agent, Bowman-Birk inhibitor concentrate. Nutr Cancer 19 (1993) 281-302
4. Armstrong W.B., Kennedy A.R., Wan X.S., et al. Single-dose administration of Bowman-Birk inhibitor concentrate in patients with oral leukoplakia. Cancer Epidemiol Biomarkers Prev 9 (2000) 43-47
5. Armstrong W.B., Kennedy A.R., Wan X.S., et al. Clinical modulation of oral leukoplakia and protease activity by Bowman-Birk inhibitor concentrate in a phase IIa chemoprevention trial. Clin Cancer Res 6 (2000) 4684-4691
6. Morocutti A., Earle K.A., Sethi M., et al. Premature senescence of skin fibroblasts from insulin-dependent diabetic patients with kidney disease. Kidney Int 50 (1996) 250-256
7. Herskind C., Bentzen S.M., Overgaard J., et al. Differentiation state of skin fibroblast cultures versus risk of subcutaneous fibrosis after radiotherapy. Radiother Oncol 47 (1998) 263-269
8. Rodemann H.P., and Blaese M.A. Responses of normal cells to ionizing radiation. Semin Radiat Oncol 17 (2007) 81-88
9. Dittmann K., Loffler H., Bamberg M., and Rodemann H.P. Bowman-Birk proteinase inhibitor (BBI) modulates radiosensitivity and radiation-induced differentiation of human fibroblasts in culture. Radiother Oncol 34 (1995) 137-143
10. Dittmann K.H., Gueven N., Mayer C., et al. The presence of wild-type TP53 is necessary for the radioprotective effect of the Bowman-Birk proteinase inhibitor in normal fibroblasts. Radiat Res 150 (1998) 648-655
11. Dittmann K.H., Mayer C., and Rodemann H.P. Radioprotection of normal tissue to improve radiotherapy: the effect of the Bowman-Birk protease inhibitor. Curr Med Chem Anticancer Agents 3 (2003) 360-363
12. Petitjean A., Mathe E., Kato S., et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 28 (2007) 622-629
13. Dittmann K., Toulany M., Classen J., et al. Selective Radioprotection of Normal Tissues by Bowman-Birk Proteinase Inhibitor (BBI) in Mice. Strahlenther Onkol 181 (2005) 191-196
14. Dittmann K.H., Gueven N., and Mayer CRodemann H.P. The radioprotective effect of BBI is associated with the activation of DNA repair-relevant genes. Int J Radiat Biol 74 (1998) 225-230
15. Dittmann K., Virsik-Kopp P., Mayer C., Rave-Frank M., and Rodemann H.P. Bowman-Birk protease inhibitor activates DNA-dependent protein kinase and reduces formation of radiation-induced dicentric chromosomes. Int J Radiat Biol 79 (2003) 801-808
16. Kennedy A.R. Chemopreventive agents: protease inhibitors. Pharmacol Ther 78 (1998) 167-209
17. Yavelow J., Caggana M., and Beck K.A. Proteases occurring in the cell membrane: a possible cell receptor for the Bowman-Birk type of protease inhibitors. Cancer Res 47 (1987) 1598-1601
18. Dittmann K.H., Gueven N., Mayer C., and Rodemann H.P. Characterization of the amino acids essential for the photo- and radioprotective effects of a Bowman-Birk protease inhibitor-derived nonapeptide. Protein Eng 14 (2001) 157-160
19. Dittmann K.H., Mayer C., and Rodemann H.P. O-Phospho-l-tyrosine protects TP53 wild-type cells against ionizing radiation. Int J Cancer 96 (2001) 1-6
20. Dittmann K., Mayer C., Wanner G., Kehlbach R., and Rodemann H.P. The radioprotector O-phospho-tyrosine stimulates DNA repair via epidermal growth factor receptor- and DNA-dependent kinase phosphorylation. Radiother Oncol 84 (2007) 328-334
21. Dittmann K., Mayer C., Fehrenbacher B., et al. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 280 (2005) 31182-31189
22. Gueven N., Dittmann K., Mayer C., and Rodemann H.P. Bowman-Birk protease inhibitor reduces the radiation-induced activation of the EGF receptor and induces tyrosine phosphatase activity. Int J Radiat Biol 73 (1998) 157-162
23. Xu K.P., Yin J., and Yu F.S. SRC-family tyrosine kinases in wound- and ligand-induced epidermal growth factor receptor activation in human corneal epithelial cells. Invest Ophthalmol Vis Sci 47 (2006) 2832-2839
24. Khan E.M., Heidinger J.M., Levy M., et al. Epidermal growth factor receptor exposed to oxidative stress undergoes Src- and caveolin-1-dependent perinuclear trafficking. J Biol Chem 281 (2006) 14486-14493
25. Das A.K., Chen B.P., Story M.D., et al. Somatic mutations in the tyrosine kinase domain of epidermal growth factor receptor (EGFR) abrogate EGFR-mediated radioprotection in non-small cell lung carcinoma. Cancer Res 67 (2007) 5267-5274
26. Friedmann B.J., Caplin M., Savic B., et al. Interaction of the epidermal growth factor receptor and the DNA-dependent protein kinase pathway following gefitinib treatment. Mol Cancer Ther 5 (2006) 209-218
27. Szumiel I. Epidermal growth factor receptor and DNA double strand break repair: the cell's self-defence. Cell Signal 18 (2006) 1537-1548
28. Goodarzi A.A., Yu Y., Riballo E., et al. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J 25 (2006) 3880-3889
29. Hsu S.C., and Hung M.C. Characterization of a novel tripartite nuclear localization sequence in the EGFR family. J Biol Chem 282 (2007) 10432-10440
30. Lo H.W., Hsu S.C., and Hung M.C. EGFR signaling pathway in breast cancers: from traditional signal transduction to direct nuclear translocalization. Breast Cancer Res Treat 95 (2006) 211-218
31. Lin S.Y., Makino K., Xia W., et al. Nuclear localization of EGF receptor and its potential new role as a transcription factor [see comment]. Nat Cell Biol 3 (2001) 802-808
32. Lo H.W., Xia W., Wei Y., et al. Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer [erratum appears in Cancer Res 2005;65(5):2045]. Cancer Res 65 (2005) 338-348
33. Psyrri A., Yu Z., Weinberger P.M., et al. Quantitative determination of nuclear and cytoplasmic epidermal growth factor receptor expression in oropharyngeal squamous cell cancer by using automated quantitative analysis. Clin Cancer Res 11 (2005) 5856-5862
34. Baumann M., Krause M., Dikomey E., et al. EGFR-targeted anti-cancer drugs in radiotherapy: preclinical evaluation of mechanisms. Radiother Oncol 83 (2007) 238-248
35. Lo H.W., Ali-Seyed M., Wu Y., et al. Nuclear-cytoplasmic transport of EGFR involves receptor endocytosis, importin beta1 and CRM1. J Cell Biochem 98 (2006) 1570-1583
36. Gueven N., Dittmann K., Mayer C., and Rodemann H.P. The radioprotective potential of the Bowman-Birk protease inhibitor is independent of its secondary structure. Cancer Lett 125 (1998) 77-82
37. Aboytes-Torres R., and Buening G.M. Development of a recombinant Anaplasma marginale DNA probe. Vet Microbiol 24 (1990) 391-408
38. Tice D.A., Biscardi J.S., Nickles A.L., and Parsons S.J. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci USA 96 (1999) 1415-1420
39. Zhang X., Gureasko J., Shen K., Cole P.A., and Kuriyan J. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor [see comment]. Cell 125 (2006) 1137-1149
40. Virsik-Kopp P., Rave-Frank M., Hofman-Huther H., and Schmidberger H. Role of DNA-PK in the process of aberration formation as studied in irradiated human glioblastoma cell lines M059K and M059J. Int J Radiat Biol 79 (2003) 61-68
41. Shin K.H., Kim R.H., Kang M.K., et al. p53 promotes the fidelity of DNA end-joining activity by, in part, enhancing the expression of heterogeneous nuclear ribonucleoprotein G. DNA Repair (Amst) 6 (2007) 830-840
42. Dahm-Daphi J., Hubbe P., Horvath F., et al. Nonhomologous end-joining of site-specific but not of radiation-induced DNA double-strand breaks is reduced in the presence of wild-type p53. Oncogene 24 (2005) 1663-1672
43. Stucki M., and Jackson S.P. MDC1/NFBD1: a key regulator of the DNA damage response in higher eukaryotes. DNA Repair (Amst) 3 (2004) 953-957
44. Dimitrova N., and de Lange T. MDC1 accelerates nonhomologous end-joining of dysfunctional telomeres. Genes Dev 20 (2006) 3238-3243
45. Bartkova J., Horej Sbreve I.Z., Sehested M., et al. DNA damage response mediators MDC1 and 53BP1: constitutive activation and aberrant loss in breast and lung cancer, but not in testicular germ cell tumours. Oncogene (2007)
46. Akyuz N., Boehden G.S., Susse S., et al. DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol Cell Biol 22 (2002) 6306-6317
47. Gatz S.A., and Wiesmuller L. p53 in recombination and repair. Cell Death Differ 13 (2006) 1003-1016