Human monocytes undergo excessive apoptosis following temozolomide activating the ATM/ATR pathway while dendritic cells and macrophages are resistant

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Bauer, Martina ^a   Goldstein, Michael ^a   Heylmann, Daniel ^a   Kaina, Bernd ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CASPASE; CELL PROTEIN; CELL RECEPTOR; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYTOKINE; DOUBLE STRANDED DNA; FAS RECEPTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 4; LIGASE IIIALPHA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; SINGLE STRANDED DNA; TEMOZOLOMIDE; UNCLASSIFIED DRUG; XRCC1 PROTEIN;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL ISOLATION; CELL KILLING; CELL MATURATION; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DENDRITIC CELL; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; DRUG ACTIVITY; ENZYME ACTIVATION; EXCISION REPAIR; HUMAN; HUMAN CELL; MACROPHAGE; MITOCHONDRION; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIZATION; SINGLE STRANDED DNA BREAK; UPREGULATION;

ANTIGENS, CD95; APOPTOSIS; CASPASES; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; DACARBAZINE; DENDRITIC CELLS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; ENZYME ACTIVATION; HISTONES; HUMANS; MACROPHAGES; MITOCHONDRIA; MONOCYTES; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84863096016     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039956     Document Type: Article

References (41)

1. Hume DA, (2006) The mononuclear phagocyte system. Curr Opin Immunol 18: 49-53.
2. Wyatt MD, Pittman DL, (2006) Methylating agents and DNA repair responses: Methylated bases and sources of strand breaks. Chem Res Toxicol 19: 1580-1594.
3. Kaina B, Christmann M, Naumann S, Roos WP, (2007) MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair 6: 1079-1099.
4. Roos W, Baumgartner M, Kaina B, (2004) Apoptosis triggered by DNA damage O6-methylguanine in human lymphocytes requires DNA replication and is mediated by p53 and Fas/CD95/Apo-1. Oncogene 23: 359-367.
5. Christmann M, Tomicic MT, Roos WP, Kaina B, (2003) Mechanisms of human DNA repair: an update. Toxicology 193: 3-34.
6. Briegert M, Kaina B, (2007) Human monocytes, but not dendritic cells derived from them, are defective in base excision repair and hypersensitive to methylating agents. Cancer Res 67: 26-31.
7. Harper JW, Elledge SJ, (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745.
8. Iliakis G, (2009) Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother Oncol 92: 310-315.
9. Wang H, Rosidi B, Perrault R, Wang MC, Zhang L, et al. (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res 65: 4020-4030.
10. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, et al. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661.
11. Briegert M, Enk AH, Kaina B, (2007) Change in expression of MGMT during maturation of human monocytes into dendritic cells. DNA Repair (Amst) 6: 1255-1263.
12. Menear KA, Adcock C, Boulter R, Cockroft X, Copsey L, et al. (2008) 4-(3-(4-Cyclopropanecarbonylpiperazine-1-carbonyl)-4-fluorobenzyl)-2H-phthalazin-1-one: A Novel Bioavailable Inhibitor of Poly(ADP-ribose) Polymerase-1. J Med Chem 51: 6581-6591.
13. Nikolova T, Ensminger M, Löbrich M, Kaina B, (2010) Homologous recombination protects mammalian cells from replication-associated DNA double-strand breaks arising in response to methyl methanesulfonat. DNA repair (Amst) 9: 1050-1063.
14. Kinner A, Wu W, Staudt C, Iliakis G, (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 36: 5678-5694.
15. Gottipati P, Helleday T, (2009) Transcription-associated recombination in eukaryotes: link between transcription, replication and recombination. Mutagenesis 24: 203-210.
16. Parchment RE, Gordon M, Grieshaber CK, Sessa C, Volpe D, et al. (1998) Predicting hematological toxicity (myelosuppression) of cytotoxic drug therapy from in vitro tests. Ann Oncol 9: 357-364.
17. Quiros S, Roos WP, Kaina B, (2010) Processing of O6-methylguanine into DNA double-strand breaks requires two rounds of replication whereas apoptosis is also induced in subsequent cell cycles. Cell Cycle 9: 168-178.
18. Roos W, Baumgartner M, Kaina B, (2004) Apoptosis triggered by DNA damage O6-methylguanine in human lymphocytes requires DNA replication and is mediated by p53 and Fas/CD95/Apo-1. Oncogene 23: 359-367.
19. Bauer M, Goldstein M, Christmann M, Becker H, Heylmann D, et al. (2011) Human monocytes are severely impaired in base and DNA double-strand break repair that renders them vulnerable to oxidative stress. Proc Natl Acad Sci U S A 108: 21105-21110.
20. Chen D, Yu Z, Zhu Z, Lopez CD, (2008) E2F1 regulates the base excision repair gene XRCC1 and promotes DNA repair. J Biol Chem 283: 15381-15389.
21. Audebert M, Salles B, Calsou P, (2004) Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 279: 55117-55126.
22. Roos WP, Kaina B, (2006) DNA damage-induced cell death by apoptosis. Trends Mol Med 12: 440-450.
23. Goldstein M, Roos WP, Kaina B, (2008) Apoptotic death induced by the cyclophosphamide analogue mafosfamide in human lymphoblastoid cells: contribution of DNA replication, transcription inhibition and Chk/p53 signaling. Toxicol Appl Pharmacol 229: 20-32.
24. Roos WP, Kaina B, (2012) DNA damage-induced apoptosis: from specific DNA lesions to the DNA damage response and apoptosis. Cancer Letters in press.
25. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, et al. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352: 987-996.
26. Voss CY, Albertini MR, Malter JS, (2004) Dendritic cell-based immunotherapy for cancer and relevant challenges for transfusion medicine. Transfus Med Rev 18: 189-202.
27. Melief CJ, (2008) Cancer immunotherapy by dendritic cells. Immunity 29: 372-383.
28. Nardin A, Abastado JP, (2008) Macrophages and cancer. Front Biosci 13: 3495-3505.
29. De Vleeschouwer S, Fieuws S, Rutkowski S, Van Calenbergh F, Van Loon J, et al. (2008) Postoperative adjuvant dendritic cell-based immunotherapy in patients with relapsed glioblastoma multiforme. Clin Cancer Res 14: 3098-3104.
30. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, et al. (1997) Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 27: 3135-3142.
31. Ashwell S, Zabludoff S, (2008) DNA damage detection and repair pathways-recent advances with inhibitors of checkpoint kinases in cancer therapy. Clin Cancer Res 14: 4032-4037.
32. Chen J, Kastan MB, (2010) 5′-3′-UTR interactions regulate p53 mRNA translation and provide a target for modulating p53 induction after DNA damage. Genes Dev 24: 2146-2156.
33. Roos WP, Nikolova T, Quiros S, Naumann SC, Kiedron O, et al. (2009) Brca2/Xrcc2 dependent HR, but not NHEJ, is required for protection against O(6)-methylguanine triggered apoptosis, DSBs and chromosomal aberrations by process leading to SCEs. DNA Repair (Amst) 8: 72-86.
34. Hazeki O, Hazeki K, Katada T, Ui M, (1996) Inhibitory effect of wortmannin on phosphatidylinositol 3-kinase-mediated cellular events. J Lipid Mediat Cell Signal 14: 259-261.
35. Pereg Y, Shkedy D, de Graaf P, Meulmeester E, Edelson-Averbukh M, et al. (2005) Phosphorylation of Hdmx mediates its Hdm2- and ATM-dependent degradation in response to DNA damage. Proc Natl Acad Sci U S A 102: 5056-5061.
36. Lau A, Swinbank KM, Ahmed PS, Taylor DL, Jackson SP, et al. (2005) Suppression of HIV-1 infection by a small molecule inhibitor of the ATM kinase. Nat Cell Biol 7: 493-500.
37. Jiang X, Zhao B, Britton R, Lim LY, Leong D, et al. (2004) Inhibition of Chk1 by the G2 DNA damage checkpoint inhibitor isogranulatimide. Mol Cancer Ther 3: 1221-1227.
38. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, et al. (1999) A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285: 1733-1737.
39. Bürkle A, Chen G, Küpper JH, Grube K, Zeller WJ, (1993) Increased poly(ADP-ribosyl)ation in intact cells by cisplatin treatment. Carcinogenesis 14: 559-561.
40. Eich M, Roos WP, Dianov GL, Digweed M, Kaina B, (2010) Nijmegen breakage syndrome protein (NBN) causes resistance to methylating anticancer drugs such as temozolomide. Mol Pharmacol 78: 943-951.
41. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.