The chloroethylating anticancer drug ACNU induces FRA1 that is involved in drug resistance of glioma cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 7, 2012, Pages 1199-1207

  Meise, Ruth ^a   Tomicic, Maja T ^a   Kaina, Bernd ^a   Christmann, Markus ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

ACNU; AP 1; FRA1; Glioma; Sensitivity

Indexed keywords

ANTINEOPLASTIC AGENT; CHECKPOINT KINASE 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NIMUSTINE; PROTEIN C JUN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1;

APOPTOSIS; ARTICLE; ATTENUATION; CELL CYCLE PROGRESSION; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC TRANSFECTION; GLIOMA CELL; HUMAN; HUMAN CELL; MESSENGER RNA SYNTHESIS; MOLECULAR CLONING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; DNA REPAIR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; FAS LIGAND PROTEIN; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; GLIOMA; HUMANS; MICE; NIMUSTINE; PROTO-ONCOGENE PROTEINS C-FOS; TRANSCRIPTION FACTOR AP-1;

EID: 84861706181     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.05.008     Document Type: Article

References (44)

1. Christmann M., Tomicic M.T., Roos W.P., Kaina B. Mechanisms of human DNA repair: an update. Toxicology 2003, 193:3-34.
2. Chiu R., Boyle W.J., Meek J., Smeal T., Hunter T., Karin M. The c-Fos protein interacts with c-Jun/AP-1 to stimulate transcription of AP-1 responsive genes. Cell 1988, 54:541-552.
3. Rauscher F.J., Sambucetti L.C., Curran T., Distel R.J., Spiegelman B.M. Common DNA binding site for Fos protein complexes and transcription factor AP-1. Cell 1988, 52:471-480.
4. Milde-Langosch K. The Fos family of transcription factors and their role in tumourigenesis. Eur. J. Cancer 2005, 41:2449-2461.
5. Christmann M., Tomicic M.T., Aasland D., Berdelle N., Kaina B. Three prime exonuclease I (TREX1) is Fos/AP-1 regulated by genotoxic stress and protects against ultraviolet light and benzo(a)pyrene-induced DNA damage. Nucleic Acids Res. 2010, 38:6418-6432.
6. Christmann M., Tomicic M.T., Origer J., Aasland D., Kaina B. c-Fos is required for excision repair of UV-light induced DNA lesions by triggering the re-synthesis of XPF. Nucleic Acids Res. 2006, 34:6530-6539.
7. Tomicic M.T., Reischmann P., Rasenberger B., Meise R., Kaina B., Christmann M. Delayed c-Fos activation in human cells triggers XPF induction and an adaptive response to UVC-induced DNA damage and cytotoxicity. Cell Mol. Life Sci. 2011, 68:1785-1798.
8. Chiappetta G., Ferraro A., Botti G., Monaco M., Pasquinelli R., Vuttariello E., Arnaldi L., Di Bonito M., D'Aiuto G., Pierantoni G.M., Fusco A. FRA-1 protein overexpression is a feature of hyperplastic and neoplastic breast disorders. BMC Cancer 2007, 7:17.
9. Baan B., Pardali E., ten Dijke P., van Dam H. In situ proximity ligation detection of c-Jun/AP-1 dimers reveals increased levels of c-Jun/Fra1 complexes in aggressive breast cancer cell lines in vitro and in vivo. Mol. Cell. Proteomics 2010, 9:1982-1990.
10. Belguise K., Kersual N., Galtier F., Chalbos D. FRA-1 expression level regulates proliferation and invasiveness of breast cancer cells. Oncogene 2005, 24:1434-1444.
11. Debinski W., Gibo D.M. Fos-related antigen 1 modulates malignant features of glioma cells. Mol. Cancer Res. 2005, 3:237-249.
12. Hamdi M., Popeijus H.E., Carlotti F., Janssen J.M., van der Burgt C., Cornelissen-Steijger P., van de Water B., Hoeben R.C., Matsuo K., van Dam H. ATF3 and Fra1 have opposite functions in JNK- and ERK-dependent DNA damage responses. DNA Repair (Amst) 2008, 7:487-496.
13. Wischhusen J., Naumann U., Ohgaki H., Rastinejad F., Weller M. CP-31398, a novel p53-stabilizing agent, induces p53-dependent and p53-independent glioma cell death. Oncogene 2003, 22:8233-8245.
14. Christmann M., Kaina B. Nuclear translocation of mismatch repair proteins MSH2 and MSH6 as a response of cells to alkylating agents. J. Biol. Chem. 2000, 275:36256-36262.
15. Sijbers A.M., de Laat W.L., Ariza R.R., Biggerstaff M., Wei Y.F., Moggs J.G., Carter K.C., Shell B.K., Evans E., de Jong M.C., Rademakers S., de Rooij J., Jaspers N.G., Hoeijmakers J.H., Wood R.D. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 1996, 86:811-822.
16. Tomicic M.T., Thust R., Sobol R.W., Kaina B. DNA polymerase beta mediates protection of mammalian cells against ganciclovir-induced cytotoxicity and DNA breakage. Cancer Res. 2001, 61:7399-7403.
17. Tomicic M.T., Bey E., Wutzler P., Thust R., Kaina B. Comparative analysis of DNA breakage, chromosomal aberrations and apoptosis induced by the anti-herpes purine nucleoside analogues aciclovir, ganciclovir and penciclovir. Mutat. Res. 2002, 505:1-11.
18. Tomicic M.T., Friedrichs C., Christmann M., Wutzler P., Thust R., Kaina B. Apoptosis induced by (E)-5-(2-bromovinyl)-2'-deoxyuridine in varicella zoster virus thymidine kinase-expressing cells is driven by activation of c-Jun/activator protein-1 and Fas ligand/caspase-8. Mol. Pharmacol. 2003, 63:439-449.
19. Faris M., Latinis K.M., Kempiak S.J., Koretzky G.A., Nel A. Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol. Cell. Biol. 1998, 18:5414-5424.
20. Youn C.K., Kim M.H., Cho H.J., Kim H.B., Chang I.Y., Chung M.H., You H.J. Oncogenic H-Ras up-regulates expression of ERCC1 to protect cells from platinum-based anticancer agents. Cancer Res. 2004, 64:4849-4857.
21. Usanova S., Piee-Staffa A., Sied U., Schneider A., Thomale J., Kaina B., Koberle B. Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression. Mol. Cancer 2010, 9:248.
22. Debinski W., Gibo D.M. Fos-related antigen 1 (Fra-1) pairing with and transactivation of JunB in GBM cells. Cancer Biol. Ther. 2011, 11:254-262.
23. Kaina B., Christmann M., Naumann S., Roos W.P. MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst) 2007, 6:1079-1099.
24. Adiseshaiah P., Peddakama S., Zhang Q., Kalvakolanu D.V., Reddy S.P. Mitogen regulated induction of FRA-1 proto-oncogene is controlled by the transcription factors binding to both serum and TPA response elements. Oncogene 2005, 24:4193-4205.
25. Casalino L., De Cesare D., Verde P. Accumulation of Fra-1 in ras-transformed cells depends on both transcriptional autoregulation and MEK-dependent posttranslational stabilization. Mol. Cell. Biol. 2003, 23:4401-4415.
26. Vial E., Marshall C.J. Elevated ERK-MAP kinase activity protects the FOS family member FRA-1 against proteasomal degradation in colon carcinoma cells. J. Cell Sci. 2003, 116:4957-4963.
27. Tower G.B., Coon C.I., Belguise K., Chalbos D., Brinckerhoff C.E. Fra-1 targets the AP-1 site/2G single nucleotide polymorphism (ETS site) in the MMP-1 promoter. Eur. J. Biochem. 2003, 270:4216-4225.
28. Kasibhatla S., Brunner T., Genestier L., Echeverri F., Mahboubi A., Green D.R. DNA damaging agents induce expression of Fas ligand and subsequent apoptosis in T lymphocytes via the activation of NF-kappa B and AP-1. Mol. Cell 1998, 1:543-551.
29. Alderson M.R., Tough T.W., Davis-Smith T., Braddy S., Falk B., Schooley K.A., Goodwin R.G., Smith C.A., Ramsdell F., Lynch D.H. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 1995, 181:71-77.
30. Brunner T., Mogil R.J., LaFace D., Yoo N.J., Mahboubi A., Echeverri F., Martin S.J., Force W.R., Lynch D.H., Ware C.F., et al. Cell-autonomous Fas (CD95)/Fas-ligand interaction mediates activation-induced apoptosis in T-cell hybridomas. Nature 1995, 373:441-444.
31. Faris M., Kokot N., Latinis K., Kasibhatla S., Green D.R., Koretzky G.A., Nel A. The c-Jun N-terminal kinase cascade plays a role in stress-induced apoptosis in Jurkat cells by up-regulating Fas ligand expression. J. Immunol. 1998, 160:134-144.
32. Baumann S., Hess J., Eichhorst S.T., Krueger A., Angel P., Krammer P.H., Kirchhoff S. An unexpected role for FosB in activation-induced cell death of T cells. Oncogene 2003, 22:1333-1339.
33. Kolbus A., Herr I., Schreiber M., Debatin K.M., Wagner E.F., Angel P. c-Jun-dependent CD95-L expression is a rate-limiting step in the induction of apoptosis by alkylating agents. Mol. Cell. Biol. 2000, 20:575-582.
34. Christmann M., Tomicic M.T., Aasland D., Kaina B. A role for UV-light-induced c-Fos: stimulation of nucleotide excision repair and protection against sustained JNK activation and apoptosis. Carcinogenesis 2007, 28:183-190.
35. Kirschner K., Melton D.W. Multiple roles of the ERCC1-XPF endonuclease in DNA repair and resistance to anticancer drugs. Anticancer. Res. 2010, 30:3223-3232.
36. Peng C.Y., Graves P.R., Thoma R.S., Wu Z., Shaw A.S., Piwnica-Worms H. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 1997, 277:1501-1505.
37. Sanchez Y., Wong C., Thoma R.S., Richman R., Wu Z., Piwnica-Worms H., Elledge S.J. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 1997, 277:1497-1501.
38. Dalal S.N., Schweitzer C.M., Gan J., DeCaprio J.A. Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 1999, 19:4465-4479.
39. Christmann M., Verbeek B., Roos W.P., Kaina B. O(6)-Methylguanine-DNA methyltransferase (MGMT) in normal tissues and tumors: enzyme activity, promoter methylation and immunohistochemistry. Biochim. Biophys. Acta 2011, 1816:179-190.
40. Chen C.C., Taniguchi T., D'Andrea A. The Fanconi anemia (FA) pathway confers glioma resistance to DNA alkylating agents. J. Mol. Med. (Berl) 2007, 85:497-509.
41. Kondo N., Takahashi A., Mori E., Noda T., Zdzienicka M.Z., Thompson L.H., Helleday T., Suzuki M., Kinashi Y., Masunaga S., Ono K., Hasegawa M., Ohnishi T. FANCD1/BRCA2 plays predominant role in the repair of DNA damage induced by ACNU or TMZ. PLoS One 2011, 6:e19659.
42. Batista L.F., Roos W.P., Christmann M., Menck C.F., Kaina B. Differential sensitivity of malignant glioma cells to methylating and chloroethylating anticancer drugs: p53 determines the switch by regulating xpc, ddb2, and DNA double-strand breaks. Cancer Res. 2007, 67:11886-11895.
43. Helleday T., Petermann E., Lundin C., Hodgson B., Sharma R.A. DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 2008, 8:193-204.
44. Hosoya N., Miyagawa K. Clinical importance of DNA repair inhibitors in cancer therapy. Mag. Eur. Med. Oncol. 2009, 2:9-14.