Minor changes in expression of the mismatch repair protein MSH2 exert a major impact on glioblastoma response to temozolomide

Cancer Research

Volumn 75, Issue 15, 2015, Pages 3127-3138

  McFaline Figueroa, José L ^a,b   Braun, Christian J ^a   Stanciu, Monica ^a   Nagel, Zachary D ^b   Mazzucato, Patrizia ^b   Sangaraju, Dewakar ^c   Cerniauskas, Edvinas ^b   Barford, Kelly ^b   Vargas, Amanda ^b   Chen, Yimin ^b   Tretyakova, Natalia ^c   Lees, Jacqueline A ^a   Hemann, Michael T ^a   White, Forest M ^a,b   Samson, Leona D ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN MSH2; PROTEIN MSH6; TEMOZOLOMIDE; ALKYLATING AGENT; CARMUSTINE; DACARBAZINE; DNA BINDING PROTEIN; DNA LIGASE; DNA METHYLTRANSFERASE; G-T MISMATCH-BINDING PROTEIN; MGMT PROTEIN, HUMAN; MSH2 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER RECURRENCE; CANCER SURVIVAL; CELL CYCLE; CELL SURVIVAL; CONTROLLED STUDY; DRUG DOSE ESCALATION; DRUG MEGADOSE; DRUG RESISTANCE; DRUG RESPONSE; DRUG SENSITIVITY; DRUG TUMOR LEVEL; GENE EXPRESSION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR REGRESSION; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DOSE RESPONSE; DRUG EFFECTS; DRUG SCREENING; GENE SILENCING; GENETICS; IONIZING RADIATION; METABOLISM; MORTALITY; PATHOLOGY; RADIATION RESPONSE; SURVIVAL; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CARMUSTINE; CELL LINE, TUMOR; DACARBAZINE; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; GENES, P53; GLIOBLASTOMA; HUMANS; MICE, INBRED C57BL; MUTS HOMOLOG 2 PROTEIN; RADIATION, IONIZING; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942865794     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-3616     Document Type: Article

References (39)

1. Johnson DR, O'Neill BP. Glioblastoma survival in the United States before and during the temozolomide era. J Neurooncol 2012;107: 359-64.
2. 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;352:987-96.
3. Li GM. Mechanisms and functions of DNA mismatch repair. Cell Res 2008;18:85-98.
4. Pegg AE. Multifaceted roles of alkyltransferase and related proteins in DNA repair, DNA damage, resistance to chemotherapy, and research tools. Chem Res Toxicol 2011;24:618-39.
5. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003.
6. van Nifterik KA, van den Berg J, van derMeideWF, Ameziane N, Wedekind LE, Steenbergen RD, et al. Absence of the MGMT protein as well as methylation of the MGMT promoter predict the sensitivity for temozolomide. Br J Cancer 2010;103:29-35.
7. Mojas N, Lopes M, Jiricny J. Mismatch repair-dependent processing of methylation damage gives rise to persistent single-stranded gaps in newly replicated DNA. Genes Dev 2007;21:3342-55.
8. Quiros S, Roos WP, Kaina B. 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 2010;9: 168-78.
9. Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, et al. Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 2007;13:2038-45.
10. The Cancer Genome Atlas Research Network T. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008;455:1061-8.
11. Yip S, Miao J, Cahill DP, Iafrate AJ, Aldape K, Nutt CL, et al. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 2009;15: 4622-9.
12. Maxwell JA, Johnson SP, McLendon RE, Lister DW, Horne KS, Rasheed A, et al. Mismatch repair deficiency does not mediate clinical resistance to temozolomide in malignant glioma. Clin Cancer Res 2008;14:4859-68.
13. Felsberg J, Thon N, Eigenbrod S, Hentschel B, Sabel MC, Westphal M, et al. Promoter methylation and expression of MGMT and the DNA mismatch repair genes MLH1, MSH2, MSH6 and PMS2 in paired primary and recurrent glioblastomas. Int J Cancer 2011;129:659-70.
14. Stark AM, Doukas A, Hugo HH, Hedderich J, Hattermann K, Maximilian Mehdorn H, et al. Expression of DNA mismatch repair proteins MLH1, MSH2, andMSH6 in recurrent glioblastoma. Neurol Res 2015;37:95-105.
15. NewcombEW, Zagzag D. The murine Gl261 glioma experimentalmodel to assess novel brain tumor treatments. In: Van Meir EG, editor. CNS cancer: models, markers, prognostic factors, targets, and therapeutic approaches. Volume 12. New York: Humana Press; 2009. p 227-41.
16. Valiathan C, McFaline JL, Samson LD. A rapid survival assay to measure drug-induced cytotoxicity and cell cycle effects.DNARepair 2012;11:92-8.
17. Noonan EM, Shah D, Yaffe MB, Lauffenburger DA, Samson LD. O6- Methylguanine DNA lesions induce an intra-S-phase arrest from which cells exit into apoptosis governed by early and late multi-pathway signaling network activation. Integr Biol 2012;4:1237-55.
18. Nagel ZD, Margulies CM, Chaim IA, McRee SK, Mazzucato P, Ahmad A, et al. Multiplexed DNA repair assays for multiple lesions and multiple doses via transcription inhibition and transcriptional mutagenesis. Proc Natl Acad Sci U S A 2014;111:E1823-32.
19. Ostermann S, Csajka C, Buclin T, Leyvraz S, Lejeune F, Decosterd LA, et al. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res 2004;10:3728-36.
20. Newlands ES, Blackledge GR, Slack JA, Rustin GJ, Smith DB, Stuart NS, et al. Phase I trial of temozolomide (CCRG 81045: M&B 39831: NSC 362856). Br J Cancer 1992;65:287-91.
21. Rudek MA, Donehower RC, Statkevich P, Batra VK, Cutler DL, Baker SD. Temozolomide in patients with advanced cancer: phase I and pharmacokinetic study. Pharmacotherapy 2004;24:16-25.
22. Schneider SW, Ludwig T, Tatenhorst L, Braune S, OberleithnerH, Senner V, et al. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathol 2004;107:272-6.
23. BloughMD, Beauchamp DC, Westgate MR, Kelly JJ, Cairncross JG. Effect of aberrant p53 function on temozolomide sensitivity of glioma cell lines and brain tumor initiating cells from glioblastoma. J Neurooncology 2011; 102:1-7.
24. Hirose Y, Berger MS, Pieper RO. p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 2001;61:1957-63.
25. Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol Biol Cell 2001;12:1315-28.
26. Samson L, Derfler B, Waldstein EA. Suppression of humanDNAalkylationrepair defects by Escherichia coli DNA-repair genes. Proc Natl Acad Sci U S A 1986;83:5607-10.
27. Yan L, Donze JR, Liu LL. Inactivated MGMT by O-6-benzylguanine is associated with prolongedG(2)/M arrest in cancer cells treatedwith BCNU. Oncogene 2005;24:2175-83.
28. Lorente A, Mueller W, Urdangarin E, Lazcoz P, von Deimling A, Castresana JS. Detection of methylation in promoter sequences by melting curve analysis-based semiquantitative real time PCR. BMC Cancer 2008;8:61.
29. Agnihotri S, Gajadhar AS, Ternamian C, Gorlia T, Diefes KL, Mischel PS, et al. Alkylpurine-DNA-N-glycosylase confers resistance to temozolomide in xenograft models of glioblastoma multiforme and is associated with poor survival in patients. J Clin Invest 2012;122:253-66.
30. Fu D, Calvo JA, Samson LD. Balancing repair and tolerance ofDNAdamage caused by alkylating agents. Nat Rev Cancer 2012;12:104-20.
31. Halabi A, Ditch S, Wang J, Grabczyk E. DNA mismatch repair complex MutSbeta promotes GAA.TTC repeat expansion in human cells. J Biol Chem 2012;287:29958-67.
32. Jiricny J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 2006;7:335-46.
33. Walid MS. Prognostic factors for long-term survival after glioblastoma. Perm J 2008;12:45-8.
34. Barber A. The roles of MLH1 and MSH2 in growth and drug resistance in human colorectal cancer cells [dissertation]. Guelph, (Ontario, Canada): University of Guelph; 2012.
35. Shin KH, Park JG. Microsatellite instability is associated with genetic alteration but not with low levels of expression of the human mismatch repair proteins hMSH2 and hMLH1. Eur J Cancer 2000;36:925-31.
36. ClaijN, Riele HT.Methylation tolerance in mismatch repair proficient cells with low MSH2 protein level. Oncogene 2002;21:2873-79.
37. de Wind N, Dekker M, Berns A, Radman M, te Riele H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell 1995; 82:321-30.
38. Andrew SE, McKinnon M, Cheng BS, Francis A, Penney J, Reitmair AH, et al. Tissues of MSH2-deficient mice demonstrate hypermutability on exposure to a DNA methylating agent. Proc Natl Acad Sci U S A 1998;95:1126-30.
39. Marra G, D'Atri S, Corti C, Bonmassar L, CattaruzzaMS, Schweizer P, et al. Tolerance of human MSH2+/- lymphoblastoid cells to the methylating agent temozolomide. Proc Natl Acad Sci U S A 2001;98:7164-9.