Acquisition of meiotic DNA repair regulators maintain genome stability in glioblastoma

Cell Death and Disease

Volumn 6, Issue 4, 2015, Pages

  Rivera, M ^a,b   Wu, Q ^a   Hamerlik, P ^c   Hjelmeland, A B ^d   Bao, S ^a   Rich, J N ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; DISRUPTED MEIOTIC CDNA1; NUCLEIC ACID BINDING PROTEIN; RECOMBINASE; REPLICATION FACTOR A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SURVIVAL; CELL CYCLE PROGRESSION; CELL DEATH; CELL GROWTH; CELL PROLIFERATION; CLONAL EVOLUTION; CONTROLLED STUDY; DNA DAMAGE RESPONSE; DNA RECOMBINATION; DNA TEMPLATE; ENZYME ACTIVATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IONIZING RADIATION; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RADIOSENSITIVITY; TUMOR GROWTH; ANIMAL; BRAIN TUMOR; DNA REPAIR; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; MEIOSIS; PATHOLOGY; RETROSPECTIVE STUDY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DNA REPAIR; GENE EXPRESSION; GENOMIC INSTABILITY; GLIOBLASTOMA; HEK293 CELLS; HETEROGRAFTS; HUMANS; MEIOSIS; MICE; RETROSPECTIVE STUDIES;

EID: 84989938536     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.75     Document Type: Article

References (53)

1. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M. Epidemiology and molecular pathology of glioma. Nat Clin Pract Neurol 2006; 2: 494-503 quiz 1 p following 516.
2. Ostrom QT, Gittleman H, Farah P, Ondracek A, Chen Y, Wolinsky Y et al. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States 2006-2010. Neuro Oncol 2013; 15(suppl 2): ii1-ii56.
3. Krex D, Klink B, Hartmann C, von Deimling A, Pietsch T, Simon M et al. Long-term survival with glioblastoma multiforme. Brain 2007; 130: 2596-2606.
4. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTCNCIC trial. Lancet Oncol 2009; 10: 459-466.
5. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-996.
6. Gupta T, Dinshaw K. Modified optimal fractionation for poor prognosis malignant gliomas: an elusive search. Acta Oncologica 2005; 44: 105-113.
7. Santivasi WL, Xia F. The role and clinical significance of DNA damage response and repair pathways in primary brain tumors. Cell Biosci 2013; 3: 10.
8. Chang JE, Khuntia D, Robins HI, Mehta M. Radiotherapy and radiosensitizers in the treatment of glioblastoma multiforme. Clin Adv Hematol Oncol 2007; 5: 894-915.
9. Romanelli P, Conti A, Pontoriero A, Ricciardi GK, Tomasello F, De Renzis C et al. Role of stereotactic radiosurgery and fractionated stereotactic radiotherapy for the treatment of recurrent glioblastoma multiforme. Neurosurg Focus 2009; 27: E8.
10. van Gent DC, Hoeijmakers JH, Kanaar R. Chromosomal stability and the DNA doublestranded break connection. Nat Genet 2001; 2: 196-206.
11. Rivera M, Sukhdeo K, Yu J. Ionizing radiation in glioblastoma initiating cells. Front Oncol 2013; 3: 74.
12. Moynahan ME, Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 2010; 11: 196-207.
13. Bishop DK. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 1994; 79: 1081-1092.
14. Hashimoto Y, Ray Chaudhuri A, Lopes M, Costanzo V. Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nat Struct Mol Biol 2010; 17: 1305-1311.
15. Costanzo V. Brca2, Rad51 and Mre11: performing balancing acts on replication forks. DNA Repair 2011; 10: 1060-1065.
16. Yata K, Lloyd J, Maslen S, Bleuyard JY, Skehel M, Smerdon SJ et al. Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Mol Cell 2012; 45: 371-383.
17. Bishop DK, Park D, Xu L, Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 1992; 69: 439-456.
18. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 2012; 337: 1222-1225.
19. Keeney S. Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn Stab 2007: 81-123.
20. Bugreev DV, Pezza RJ, Mazina OM, Voloshin ON, Camerini-Otero RD, Mazin AV et al. The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nat Struct Mol Biol 2011; 18: 56-60.
21. Masson JY, Davies AA, Hajibagheri N, Van Dyck E, Benson FE, Stasiak AZ et al. The meiosis-specific recombinase hDmc1 froms ring structures and interacts with hRad51. EMBO J 1999; 18: 6552-6656.
22. Lao JP, Cloud V, Huang CC, Grubb J, Thacker D, Lee CY et al. Meiotic crossover control by concerted action of Rad51-Dmc1 in homolog template bias and robust homeostatic regulation. PLoS Genet 2013; 9: e1003978.
23. Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature 2012; 481: 287-294.
24. Morales A, Miranda M, Sanchez-Reyes A, Biete A, Fernandez-Checa JC. Oxidate damage of mitochondrial and nuclear DNA induced by ionizing radiation in human hepatoblastoma cells. Int J Radiat Oncol Biol Phys 1998; 42: 191-203.
25. Davis AJ, Chen DJ. DNA double strand break repair via non-homologous end-joining. Transl Cancer Res 2013; 2: 130-143.
26. Iyama T, Wilson DM 3rd. DNA repair mechanisms in dividing and non-dividing cells. DNA Repair 2013; 12: 620-636.
27. Makishima H, Maciejewski JP. Pathogenesis and consequences of uniparental disomy in cancer. Clin Cancer Res 2011; 17: 3913-3923.
28. Lim YC, Roberts TL, Day BW, Harding A, Kozlov S, Kijas AW et al. A role for homologous recombination and abnormal cell-cycle progression in radioresistance of gliomainitiating cells. Mol Cancer Ther 2012; 11: 1863-1872.
29. Short SC, Giampieri S, Worku M, Alcaide-German M, Sioftanos G, Bourne S et al. Rad51 inhibition is an effective means of targeting DNA repair in glioma models and CD133+ tumorderived cells. Neuro-oncology 2011; 13: 487-499.
30. Zheng Z, Ng WL, Zhang X, Olson JJ, Hao C, Curran WJ et al. RNAi-mediated targeting of noncoding and coding sequences in DNA repair gene messages efficiently radiosensitizes human tumor cells. Cancer Res 2012; 72: 1221-1228.
31. Lim YC, Roberts TL, Day BW, Stringer BW, Kozlov S, Fazry S et al. Increased sensitivity to ionizing radiation by targeting the homologous recombination pathway in glioma initiating cells. Mol Oncol 2014; 8: 1603-1615.
32. Westermark UK, Lindberg N, Roswall P, Brasater D, Helgadottir HR, Hede SM et al. RAD51 can inhibit PDGF-B-induced gliomagenesis and genomic instability. Neuro-oncology 2011; 13: 1277-1287.
33. Welsh JW, Ellsworth RK, Kumar R, Fjerstad K, Martinez J, Nagel RB et al. Rad51 protein expression and survival in patients with glioblastoma multiforme. Int J Radiat Oncol Biol Phys 2009; 74: 1251-1255.
34. Bugreev DV, Huang F, Mazina OM, Pezza RJ, Voloshin ON, Camerini-Otero RD et al. HOP2-MND1 modulates RAD51 binding to nucleotides and DNA. Nat Commun 2014; 5: 4198.
35. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 2012; 489: 391-399.
36. Bartkova J, Hamerlik P, Stockhausen MT, Ehrmann J, Hlobilkova A, Laursen H et al. Replication stress and oxidative damage contribute to aberrant constitutive activation of DNA damage signalling in human gliomas. Oncogene 2010; 29: 5095-5102.
37. Sleeth KM, Sorensen CS, Issaeva N, Dziegielewski J, Bartek J, Helleday T et al. RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J Mol Biol 2007; 373: 38-47.
38. Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y et al. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem 2003; 278: 25207-25217.
39. Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res 2010; 108: 73-112.
40. Konca K, Lankoff A, Banasik A, Lisowska H, Kuszewski T, Gozdz S et al. A cross-platform public domain PC image-analysis program for the comet assay. Mutat Res 2003; 534: 15-20.
41. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 2014; 370: 709-722.
42. Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014; 370: 699-708.
43. Nesic D, Hsu Y, Stebbins CE. Assembly and function of a bacterial genotoxin. Nature 2004; 429: 429-433.
44. Kalejs M, Ivanov A, Plakhins G, Cragg MS, Emzinsh D, Illidge TM et al. Upregulation of meiosis-specific genes in lymphoma cell lines following genotoxic insult and induction of mitotic catastrophe. BMC Cancer 2006; 6: 6.
45. Ianzini F, Kosmacek EA, Nelson ES, Napoli E, Erenpreisa J, Kalejs M et al. Activation of meiosis-specific genes is associated with depolyploidization of human tumor cells following radiation-induced mitotic catastrophe. Cancer Res 2009; 69: 2296-2304.
46. Lindsey SF, Byrnes DM, Eller MS, Rosa AM, Dabas N, Escandon J et al. Potential role of meiosis proteins in melanoma chromosomal instability. J Skin Cancer 2013; 2013: 190109.
47. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, Freon K et al. Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell 2010; 39: 346-359.
48. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005; 434: 913-917.
49. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005; 434: 917-921.
50. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med 2009; 361: 123-134.
51. Goudar RK, Shi Q, Hjelmeland MD, Keir ST, McLendon RE, Wikstrand CJ et al. Combination therapy of inhibitors of epidermal growth factor receptor/vascular endothelial growth factor receptor 2 (AEE788) and the mammalian target of rapamycin (RAD001) offers improved glioblastoma tumor growth inhibition. Mol Cancer Ther 2005; 4: 101-112.
52. Shi Q, Hjelmeland AB, Keir ST, Song L, Wickman S, Jackson D et al. A novel low-molecular weight inhibitor of focal adhesion kinase, TAE226, inhibits glioma growth. Mol Carcinogen 2007; 46: 488-496.
53. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.