Skip to main content
Erschienen in: Acta Neuropathologica 4/2015

01.04.2015 | Original Paper

Evolution of DNA repair defects during malignant progression of low-grade gliomas after temozolomide treatment

verfasst von: Hinke F. van Thuijl, Tali Mazor, Brett E. Johnson, Shaun D. Fouse, Koki Aihara, Chibo Hong, Annika Malmström, Martin Hallbeck, Jan J. Heimans, Jenneke J. Kloezeman, Marie Stenmark-Askmalm, Martine L. M. Lamfers, Nobuhito Saito, Hiroyuki Aburatani, Akitake Mukasa, Mitchell S. Berger, Peter Söderkvist, Barry S. Taylor, Annette M. Molinaro, Pieter Wesseling, Jaap C. Reijneveld, Susan M. Chang, Bauke Ylstra, Joseph F. Costello

Erschienen in: Acta Neuropathologica | Ausgabe 4/2015

Einloggen, um Zugang zu erhalten

Abstract

Temozolomide (TMZ) increases the overall survival of patients with glioblastoma (GBM), but its role in the clinical management of diffuse low-grade gliomas (LGG) is still being defined. DNA hypermethylation of the O 6 -methylguanine-DNA methyltransferase (MGMT) promoter is associated with an improved response to TMZ treatment, while inactivation of the DNA mismatch repair (MMR) pathway is associated with therapeutic resistance and TMZ-induced mutagenesis. We previously demonstrated that TMZ treatment of LGG induces driver mutations in the RB and AKT–mTOR pathways, which may drive malignant progression to secondary GBM. To better understand the mechanisms underlying TMZ-induced mutagenesis and malignant progression, we explored the evolution of MGMT methylation and genetic alterations affecting MMR genes in a cohort of 34 treatment-naïve LGGs and their recurrences. Recurrences with TMZ-associated hypermutation had increased MGMT methylation compared to their untreated initial tumors and higher overall MGMT methylation compared to TMZ-treated non-hypermutated recurrences. A TMZ-associated mutation in one or more MMR genes was observed in five out of six TMZ-treated hypermutated recurrences. In two cases, pre-existing heterozygous deletions encompassing MGMT, or an MMR gene, were followed by TMZ-associated mutations in one of the genes of interest. These results suggest that tumor cells with methylated MGMT may undergo positive selection during TMZ treatment in the context of MMR deficiency.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068 Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061–1068
2.
Zurück zum Zitat Bady P, Sciuscio D, Diserens AC, Bloch J, van den Bent MJ, Marosi C, Dietrich PY, Weller M, Mariani L, Heppner FL, Mcdonald DR, Lacombe D, Stupp R, Delorenzi M, Hegi ME (2012) MGMT methylation analysis of glioblastoma on the Infinium methylation BeadChip identifies two distinct CpG regions associated with gene silencing and outcome, yielding a prediction model for comparisons across datasets, tumor grades, and CIMP-status. Acta Neuropathol 124:547–560CrossRefPubMedCentralPubMed Bady P, Sciuscio D, Diserens AC, Bloch J, van den Bent MJ, Marosi C, Dietrich PY, Weller M, Mariani L, Heppner FL, Mcdonald DR, Lacombe D, Stupp R, Delorenzi M, Hegi ME (2012) MGMT methylation analysis of glioblastoma on the Infinium methylation BeadChip identifies two distinct CpG regions associated with gene silencing and outcome, yielding a prediction model for comparisons across datasets, tumor grades, and CIMP-status. Acta Neuropathol 124:547–560CrossRefPubMedCentralPubMed
3.
Zurück zum Zitat Baumert B, Mason WP, Ryan G, Bromberg JE, van den Bent M, Hoang-Xuan K, Brandes AA, Kantor G, Taphoorn MJ, Ben Hassel M, Rees J, Wick W, von DA, Hartmann C, Kros JM, Hegi ME, Dif N, Lacombe D, Gorlia T, Stupp R (2013) The international EORTC/NCIC-CTG/TROG/MRC-CTU low grade trial: temozolomide chemotherapy versus radiotherapy in molecularly characterized (1p loss) LGG. 4th Quadrennial Meeting of the World Federation of Neuro-Oncology. San Francisco, CA, USA Baumert B, Mason WP, Ryan G, Bromberg JE, van den Bent M, Hoang-Xuan K, Brandes AA, Kantor G, Taphoorn MJ, Ben Hassel M, Rees J, Wick W, von DA, Hartmann C, Kros JM, Hegi ME, Dif N, Lacombe D, Gorlia T, Stupp R (2013) The international EORTC/NCIC-CTG/TROG/MRC-CTU low grade trial: temozolomide chemotherapy versus radiotherapy in molecularly characterized (1p loss) LGG. 4th Quadrennial Meeting of the World Federation of Neuro-Oncology. San Francisco, CA, USA
4.
Zurück zum Zitat Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, Vivanco I, Lee JC, Huang JH, Alexander S, Du J, Kau T, Thomas RK, Shah K, Soto H, Perner S, Prensner J, Debiasi RM, Demichelis F, Hatton C, Rubin MA, Garraway LA, Nelson SF, Liau L, Mischel PS, Cloughesy TF, Meyerson M, Golub TA, Lander ES, Mellinghoff IK, Sellers WR (2007) Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci 104:20007–20012CrossRefPubMedCentralPubMed Beroukhim R, Getz G, Nghiemphu L, Barretina J, Hsueh T, Linhart D, Vivanco I, Lee JC, Huang JH, Alexander S, Du J, Kau T, Thomas RK, Shah K, Soto H, Perner S, Prensner J, Debiasi RM, Demichelis F, Hatton C, Rubin MA, Garraway LA, Nelson SF, Liau L, Mischel PS, Cloughesy TF, Meyerson M, Golub TA, Lander ES, Mellinghoff IK, Sellers WR (2007) Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci 104:20007–20012CrossRefPubMedCentralPubMed
5.
Zurück zum Zitat Bodell WJ, Gaikwad NW, Miller D, Berger MS (2003) Formation of DNA adducts and induction of lacI mutations in Big Blue Rat-2 cells treated with temozolomide: implications for the treatment of low-grade adult and pediatric brain tumors. Cancer Epidemiol Biomarkers Prev 12:545–551PubMed Bodell WJ, Gaikwad NW, Miller D, Berger MS (2003) Formation of DNA adducts and induction of lacI mutations in Big Blue Rat-2 cells treated with temozolomide: implications for the treatment of low-grade adult and pediatric brain tumors. Cancer Epidemiol Biomarkers Prev 12:545–551PubMed
6.
Zurück zum Zitat Brada M, Viviers L, Abson C, Hines F, Britton J, Ashley S, Sardell S, Traish D, Gonsalves A, Wilkins P, Westbury C (2003) Phase II study of primary temozolomide chemotherapy in patients with WHO grade II gliomas. Ann Oncol 14:1715–1721CrossRefPubMed Brada M, Viviers L, Abson C, Hines F, Britton J, Ashley S, Sardell S, Traish D, Gonsalves A, Wilkins P, Westbury C (2003) Phase II study of primary temozolomide chemotherapy in patients with WHO grade II gliomas. Ann Oncol 14:1715–1721CrossRefPubMed
7.
Zurück zum Zitat Brandes AA, Franceschi E, Tosoni A, Bartolini S, Bacci A, Agati R, Ghimenton C, Turazzi S, Talacchi A, Skrap M, Marucci G, Volpin L, Morandi L, Pizzolitto S, Gardiman M, Andreoli A, Calbucci F, Ermani M (2010) O(6)-methylguanine DNA-methyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neuro Oncol 12:283–288CrossRefPubMedCentralPubMed Brandes AA, Franceschi E, Tosoni A, Bartolini S, Bacci A, Agati R, Ghimenton C, Turazzi S, Talacchi A, Skrap M, Marucci G, Volpin L, Morandi L, Pizzolitto S, Gardiman M, Andreoli A, Calbucci F, Ermani M (2010) O(6)-methylguanine DNA-methyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neuro Oncol 12:283–288CrossRefPubMedCentralPubMed
8.
Zurück zum Zitat Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, Batchelor TT, Futreal PA, Stratton MR, Curry WT, Iafrate AJ, Louis DN (2007) Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 13:2038–2045CrossRefPubMedCentralPubMed Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, Batchelor TT, Futreal PA, Stratton MR, Curry WT, Iafrate AJ, Louis DN (2007) Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 13:2038–2045CrossRefPubMedCentralPubMed
9.
Zurück zum Zitat Cankovic M, Mikkelsen T, Rosenblum ML, Zarbo RJ (2007) A simplified laboratory validated assay for MGMT promoter hypermethylation analysis of glioma specimens from formalin-fixed paraffin-embedded tissue. Lab Invest 87:392–397PubMed Cankovic M, Mikkelsen T, Rosenblum ML, Zarbo RJ (2007) A simplified laboratory validated assay for MGMT promoter hypermethylation analysis of glioma specimens from formalin-fixed paraffin-embedded tissue. Lab Invest 87:392–397PubMed
10.
Zurück zum Zitat Chao EC, Velasquez JL, Witherspoon MS, Rozek LS, Peel D, Ng P, Gruber SB, Watson P, Rennert G, Anton-Culver H, Lynch H, Lipkin SM (2008) Accurate classification of MLH1/MSH2 missense variants with multivariate analysis of protein polymorphisms-mismatch repair (MAPP-MMR). Hum Mutat 29:852–860CrossRefPubMed Chao EC, Velasquez JL, Witherspoon MS, Rozek LS, Peel D, Ng P, Gruber SB, Watson P, Rennert G, Anton-Culver H, Lynch H, Lipkin SM (2008) Accurate classification of MLH1/MSH2 missense variants with multivariate analysis of protein polymorphisms-mismatch repair (MAPP-MMR). Hum Mutat 29:852–860CrossRefPubMed
11.
Zurück zum Zitat Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, Gabriel S, Meyerson M, Lander ES, Getz G (2013) Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 31:213–219CrossRefPubMed Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, Gabriel S, Meyerson M, Lander ES, Getz G (2013) Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 31:213–219CrossRefPubMed
12.
Zurück zum Zitat Costello JF, Futscher BW, Kroes RA, Pieper RO (1994) Methylation-related chromatin structure is associated with exclusion of transcription factors from and suppressed expression of the O-6-methylguanine DNA methyltransferase gene in human glioma cell lines. Mol Cell Biol 14:6515–6521PubMedCentralPubMed Costello JF, Futscher BW, Kroes RA, Pieper RO (1994) Methylation-related chromatin structure is associated with exclusion of transcription factors from and suppressed expression of the O-6-methylguanine DNA methyltransferase gene in human glioma cell lines. Mol Cell Biol 14:6515–6521PubMedCentralPubMed
13.
Zurück zum Zitat Costello JF, Futscher BW, Tano K, Graunke DM, Pieper RO (1994) Graded methylation in the promoter and body of the O6-methylguanine DNA methyltransferase (MGMT) gene correlates with MGMT expression in human glioma cells. J Biol Chem 269:17228–17237PubMed Costello JF, Futscher BW, Tano K, Graunke DM, Pieper RO (1994) Graded methylation in the promoter and body of the O6-methylguanine DNA methyltransferase (MGMT) gene correlates with MGMT expression in human glioma cells. J Biol Chem 269:17228–17237PubMed
14.
Zurück zum Zitat Douw L, Klein M, Fagel SS, van den Heuvel J, Taphoorn MJ, Aaronson NK, Postma TJ, Vandertop WP, Mooij JJ, Boerman RH, Beute GN, Sluimer JD, Slotman BJ, Reijneveld JC, Heimans JJ (2009) Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8:810–818CrossRefPubMed Douw L, Klein M, Fagel SS, van den Heuvel J, Taphoorn MJ, Aaronson NK, Postma TJ, Vandertop WP, Mooij JJ, Boerman RH, Beute GN, Sluimer JD, Slotman BJ, Reijneveld JC, Heimans JJ (2009) Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: long-term follow-up. Lancet Neurol 8:810–818CrossRefPubMed
15.
Zurück zum Zitat Dunn J, Baborie A, Alam F, Joyce K, Moxham M, Sibson R, Crooks D, Husband D, Shenoy A, Brodbelt A, Wong H, Liloglou T, Haylock B, Walker C (2009) Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 101:124–131CrossRefPubMedCentralPubMed Dunn J, Baborie A, Alam F, Joyce K, Moxham M, Sibson R, Crooks D, Husband D, Shenoy A, Brodbelt A, Wong H, Liloglou T, Haylock B, Walker C (2009) Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 101:124–131CrossRefPubMedCentralPubMed
16.
Zurück zum Zitat Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797PubMed Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793–797PubMed
17.
Zurück zum Zitat Everhard S, Tost J, El AH, Criniere E, Busato F, Marie Y, Gut IG, Sanson M, Mokhtari K, Laigle-Donadey F, Hoang-Xuan K, Delattre JY, Thillet J (2009) Identification of regions correlating MGMT promoter methylation and gene expression in glioblastomas. Neuro Oncol 11:348–356CrossRefPubMedCentralPubMed Everhard S, Tost J, El AH, Criniere E, Busato F, Marie Y, Gut IG, Sanson M, Mokhtari K, Laigle-Donadey F, Hoang-Xuan K, Delattre JY, Thillet J (2009) Identification of regions correlating MGMT promoter methylation and gene expression in glioblastomas. Neuro Oncol 11:348–356CrossRefPubMedCentralPubMed
18.
Zurück zum Zitat Felsberg J, Thon N, Eigenbrod S, Hentschel B, Sabel MC, Westphal M, Schackert G, Kreth FW, Pietsch T, Loffler M, Weller M, Reifenberger G, Tonn JC (2011) 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 129:659–670CrossRefPubMed Felsberg J, Thon N, Eigenbrod S, Hentschel B, Sabel MC, Westphal M, Schackert G, Kreth FW, Pietsch T, Loffler M, Weller M, Reifenberger G, Tonn JC (2011) 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 129:659–670CrossRefPubMed
19.
Zurück zum Zitat Fritz G, Kaina B (1992) Genomic differences between O6-methylguanine-DNA methyltransferase proficient (Mex+) and deficient (Mex−) cell lines: possible role of genetic and epigenetic changes in conversion of Mex+ into Mex−. Biochem Biophys Res Commun 183:1184–1190CrossRefPubMed Fritz G, Kaina B (1992) Genomic differences between O6-methylguanine-DNA methyltransferase proficient (Mex+) and deficient (Mex−) cell lines: possible role of genetic and epigenetic changes in conversion of Mex+ into Mex−. Biochem Biophys Res Commun 183:1184–1190CrossRefPubMed
20.
Zurück zum Zitat Giraldo A, Gomez A, Salguero G, Garcia H, Aristizabal F, Gutierrez O, Angel LA, Padron J, Martinez C, Martinez H, Malaver O, Florez L, Barvo R (2005) MLH1 and MSH2 mutations in Colombian families with hereditary nonpolyposis colorectal cancer (Lynch syndrome)–description of four novel mutations. Fam Cancer 4:285–290CrossRefPubMed Giraldo A, Gomez A, Salguero G, Garcia H, Aristizabal F, Gutierrez O, Angel LA, Padron J, Martinez C, Martinez H, Malaver O, Florez L, Barvo R (2005) MLH1 and MSH2 mutations in Colombian families with hereditary nonpolyposis colorectal cancer (Lynch syndrome)–description of four novel mutations. Fam Cancer 4:285–290CrossRefPubMed
21.
Zurück zum Zitat Grasbon-Frodl EM, Kreth FW, Ruiter M, Schnell O, Bise K, Felsberg J, Reifenberger G, Tonn JC, Kretzschmar HA (2007) Intratumoral homogeneity of MGMT promoter hypermethylation as demonstrated in serial stereotactic specimens from anaplastic astrocytomas and glioblastomas. Int J Cancer 121:2458–2464CrossRefPubMed Grasbon-Frodl EM, Kreth FW, Ruiter M, Schnell O, Bise K, Felsberg J, Reifenberger G, Tonn JC, Kretzschmar HA (2007) Intratumoral homogeneity of MGMT promoter hypermethylation as demonstrated in serial stereotactic specimens from anaplastic astrocytomas and glioblastomas. Int J Cancer 121:2458–2464CrossRefPubMed
22.
Zurück zum Zitat Groenendijk FH, Taal W, Dubbink HJ, Haarloo CR, Kouwenhoven MC, van den Bent MJ, Kros JM, Dinjens WN (2011) MGMT promoter hypermethylation is a frequent, early, and consistent event in astrocytoma progression, and not correlated with TP53 mutation. J Neurooncol 101:405–417CrossRefPubMedCentralPubMed Groenendijk FH, Taal W, Dubbink HJ, Haarloo CR, Kouwenhoven MC, van den Bent MJ, Kros JM, Dinjens WN (2011) MGMT promoter hypermethylation is a frequent, early, and consistent event in astrocytoma progression, and not correlated with TP53 mutation. J Neurooncol 101:405–417CrossRefPubMedCentralPubMed
23.
Zurück zum Zitat Hamilton MG, Roldan G, Magliocco A, McIntyre JB, Parney I, Easaw JC (2011) Determination of the methylation status of MGMT in different regions within glioblastoma multiforme. J Neurooncol 102:255–260CrossRefPubMed Hamilton MG, Roldan G, Magliocco A, McIntyre JB, Parney I, Easaw JC (2011) Determination of the methylation status of MGMT in different regions within glioblastoma multiforme. J Neurooncol 102:255–260CrossRefPubMed
24.
Zurück zum Zitat Harris LC, Remack JS, Brent TP (1994) Identification of a 59 bp enhancer located at the first exon/intron boundary of the human O6-methylguanine DNA methyltransferase gene. Nucleic Acids Res 22:4614–4619CrossRefPubMedCentralPubMed Harris LC, Remack JS, Brent TP (1994) Identification of a 59 bp enhancer located at the first exon/intron boundary of the human O6-methylguanine DNA methyltransferase gene. Nucleic Acids Res 22:4614–4619CrossRefPubMedCentralPubMed
25.
Zurück zum Zitat Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003CrossRefPubMed Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003CrossRefPubMed
26.
Zurück zum Zitat Hunter C, Smith R, Cahill DP, Stephens P, Stevens C, Teague J, Greenman C, Edkins S, Bignell G, Davies H, O’Meara S, Parker A, Avis T, Barthorpe S, Brackenbury L, Buck G, Butler A, Clements J, Cole J, Dicks E, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Kosmidou V, Laman R, Lugg R, Menzies A, Perry J, Petty R, Raine K, Richardson D, Shepherd R, Small A, Solomon H, Tofts C, Varian J, West S, Widaa S, Yates A, Easton DF, Riggins G, Roy JE, Levine KK, Mueller W, Batchelor TT, Louis DN, Stratton MR, Futreal PA, Wooster R (2006) A hypermutation phenotype and somatic MSH6 mutations in recurrent human malignant gliomas after alkylator chemotherapy. Cancer Res 66:3987–3991CrossRefPubMed Hunter C, Smith R, Cahill DP, Stephens P, Stevens C, Teague J, Greenman C, Edkins S, Bignell G, Davies H, O’Meara S, Parker A, Avis T, Barthorpe S, Brackenbury L, Buck G, Butler A, Clements J, Cole J, Dicks E, Forbes S, Gorton M, Gray K, Halliday K, Harrison R, Hills K, Hinton J, Jenkinson A, Jones D, Kosmidou V, Laman R, Lugg R, Menzies A, Perry J, Petty R, Raine K, Richardson D, Shepherd R, Small A, Solomon H, Tofts C, Varian J, West S, Widaa S, Yates A, Easton DF, Riggins G, Roy JE, Levine KK, Mueller W, Batchelor TT, Louis DN, Stratton MR, Futreal PA, Wooster R (2006) A hypermutation phenotype and somatic MSH6 mutations in recurrent human malignant gliomas after alkylator chemotherapy. Cancer Res 66:3987–3991CrossRefPubMed
27.
28.
Zurück zum Zitat Johnson BE, Mazor T, Hong C, Barnes M, Aihara K, McLean CY, Fouse SD, Yamamoto S, Ueda H, Tatsuno K, Asthana S, Jalbert LE, Nelson SJ, Bollen AW, Gustafson WC, Charron E, Weiss WA, Smirnov IV, Song JS, Olshen AB, Cha S, Zhao Y, Moore RA, Mungall AJ, Jones SJ, Hirst M, Marra MA, Saito N, Aburatani H, Mukasa A, Berger MS, Chang SM, Taylor BS, Costello JF (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 343:189–193CrossRefPubMedCentralPubMed Johnson BE, Mazor T, Hong C, Barnes M, Aihara K, McLean CY, Fouse SD, Yamamoto S, Ueda H, Tatsuno K, Asthana S, Jalbert LE, Nelson SJ, Bollen AW, Gustafson WC, Charron E, Weiss WA, Smirnov IV, Song JS, Olshen AB, Cha S, Zhao Y, Moore RA, Mungall AJ, Jones SJ, Hirst M, Marra MA, Saito N, Aburatani H, Mukasa A, Berger MS, Chang SM, Taylor BS, Costello JF (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 343:189–193CrossRefPubMedCentralPubMed
29.
Zurück zum Zitat Koekkoek JA, Dirven L, Heimans JJ, Postma TJ, Vos MJ, Reijneveld JC, Taphoorn MJ (2014) Seizure reduction in a low-grade glioma: more than a beneficial side effect of temozolomide. J Neurol Neurosurg Psychiatry. doi:10.1136/jnnp-2014-308136 PubMed Koekkoek JA, Dirven L, Heimans JJ, Postma TJ, Vos MJ, Reijneveld JC, Taphoorn MJ (2014) Seizure reduction in a low-grade glioma: more than a beneficial side effect of temozolomide. J Neurol Neurosurg Psychiatry. doi:10.​1136/​jnnp-2014-308136 PubMed
30.
Zurück zum Zitat Komine C, Watanabe T, Katayama Y, Yoshino A, Yokoyama T, Fukushima T (2003) Promoter hypermethylation of the DNA repair gene O6-methylguanine-DNA methyltransferase is an independent predictor of shortened progression free survival in patients with low-grade diffuse astrocytomas. Brain Pathol 13:176–184CrossRefPubMed Komine C, Watanabe T, Katayama Y, Yoshino A, Yokoyama T, Fukushima T (2003) Promoter hypermethylation of the DNA repair gene O6-methylguanine-DNA methyltransferase is an independent predictor of shortened progression free survival in patients with low-grade diffuse astrocytomas. Brain Pathol 13:176–184CrossRefPubMed
32.
Zurück zum Zitat Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109CrossRefPubMedCentralPubMed Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109CrossRefPubMedCentralPubMed
33.
Zurück zum Zitat Malley DS, Hamoudi RA, Kocialkowski S, Pearson DM, Collins VP, Ichimura K (2011) A distinct region of the MGMT CpG island critical for transcriptional regulation is preferentially methylated in glioblastoma cells and xenografts. Acta Neuropathol 121:651–661CrossRefPubMed Malley DS, Hamoudi RA, Kocialkowski S, Pearson DM, Collins VP, Ichimura K (2011) A distinct region of the MGMT CpG island critical for transcriptional regulation is preferentially methylated in glioblastoma cells and xenografts. Acta Neuropathol 121:651–661CrossRefPubMed
34.
Zurück zum Zitat McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefPubMedCentralPubMed McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefPubMedCentralPubMed
35.
Zurück zum Zitat Nakamura M, Watanabe T, Yonekawa Y, Kleihues P, Ohgaki H (2001) Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G: C–>A: T mutations of the TP53 tumor suppressor gene. Carcinogenesis 22:1715–1719CrossRefPubMed Nakamura M, Watanabe T, Yonekawa Y, Kleihues P, Ohgaki H (2001) Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G: C–>A: T mutations of the TP53 tumor suppressor gene. Carcinogenesis 22:1715–1719CrossRefPubMed
36.
Zurück zum Zitat Nguyen SA, Stechishin OD, Luchman HA, Lun XQ, Senger DL, Robbins SM, Cairncross G, Weiss S (2014) Novel MSH6 mutations in treatment naive glioblastoma and anaplastic oligodendroglioma influence temozolomide resistance independently of MGMT methylation. Clin Cancer Res Nguyen SA, Stechishin OD, Luchman HA, Lun XQ, Senger DL, Robbins SM, Cairncross G, Weiss S (2014) Novel MSH6 mutations in treatment naive glioblastoma and anaplastic oligodendroglioma influence temozolomide resistance independently of MGMT methylation. Clin Cancer Res
37.
Zurück zum Zitat Pace A, Vidiri A, Galie E, Carosi M, Telera S, Cianciulli AM, Canalini P, Giannarelli D, Jandolo B, Carapella CM (2003) Temozolomide chemotherapy for progressive low-grade glioma: clinical benefits and radiological response. Ann Oncol 14:1722–1726CrossRefPubMed Pace A, Vidiri A, Galie E, Carosi M, Telera S, Cianciulli AM, Canalini P, Giannarelli D, Jandolo B, Carapella CM (2003) Temozolomide chemotherapy for progressive low-grade glioma: clinical benefits and radiological response. Ann Oncol 14:1722–1726CrossRefPubMed
38.
Zurück zum Zitat Parkinson JF, Wheeler HR, Clarkson A, McKenzie CA, Biggs MT, Little NS, Cook RJ, Messina M, Robinson BG, McDonald KL (2008) Variation of O(6)-methylguanine-DNA methyltransferase (MGMT) promoter methylation in serial samples in glioblastoma. J Neurooncol 87:71–78CrossRefPubMed Parkinson JF, Wheeler HR, Clarkson A, McKenzie CA, Biggs MT, Little NS, Cook RJ, Messina M, Robinson BG, McDonald KL (2008) Variation of O(6)-methylguanine-DNA methyltransferase (MGMT) promoter methylation in serial samples in glioblastoma. J Neurooncol 87:71–78CrossRefPubMed
39.
Zurück zum Zitat Peltomaki P (2003) Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21:1174–1179CrossRefPubMed Peltomaki P (2003) Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21:1174–1179CrossRefPubMed
40.
Zurück zum Zitat Pieper RO, Costello JF, Kroes RA, Futscher BW, Marathi U, Erickson LC (1991) Direct correlation between methylation status and expression of the human O-6-methylguanine DNA methyltransferase gene. Cancer Commun 3:241–253PubMed Pieper RO, Costello JF, Kroes RA, Futscher BW, Marathi U, Erickson LC (1991) Direct correlation between methylation status and expression of the human O-6-methylguanine DNA methyltransferase gene. Cancer Commun 3:241–253PubMed
41.
Zurück zum Zitat Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084CrossRefPubMed Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084CrossRefPubMed
42.
Zurück zum Zitat Quinn JA, Reardon DA, Friedman AH, Rich JN, Sampson JH, Provenzale JM, McLendon RE, Gururangan S, Bigner DD, Herndon JE, Avgeropoulos N, Finlay J, Tourt-Uhlig S, Affronti ML, Evans B, Stafford-Fox V, Zaknoen S, Friedman HS (2003) Phase II trial of temozolomide in patients with progressive low-grade glioma. J Clin Oncol 21:646–651CrossRefPubMed Quinn JA, Reardon DA, Friedman AH, Rich JN, Sampson JH, Provenzale JM, McLendon RE, Gururangan S, Bigner DD, Herndon JE, Avgeropoulos N, Finlay J, Tourt-Uhlig S, Affronti ML, Evans B, Stafford-Fox V, Zaknoen S, Friedman HS (2003) Phase II trial of temozolomide in patients with progressive low-grade glioma. J Clin Oncol 21:646–651CrossRefPubMed
43.
Zurück zum Zitat Raevaara TE, Korhonen MK, Lohi H, Hampel H, Lynch E, Lonnqvist KE, Holinski-Feder E, Sutter C, McKinnon W, Duraisamy S, Gerdes AM, Peltomaki P, Kohonen-Ccorish M, Mangold E, Macrae F, Greenblatt M, de la Chapelle A, Nystrom M (2005) Functional significance and clinical phenotype of nontruncating mismatch repair variants of MLH1. Gastroenterology 129:537–549PubMed Raevaara TE, Korhonen MK, Lohi H, Hampel H, Lynch E, Lonnqvist KE, Holinski-Feder E, Sutter C, McKinnon W, Duraisamy S, Gerdes AM, Peltomaki P, Kohonen-Ccorish M, Mangold E, Macrae F, Greenblatt M, de la Chapelle A, Nystrom M (2005) Functional significance and clinical phenotype of nontruncating mismatch repair variants of MLH1. Gastroenterology 129:537–549PubMed
44.
Zurück zum Zitat Ramalho-Carvalho J, Pires M, Lisboa S, Graca I, Rocha P, Barros-Silva JD, Savva-Bordalo J, Mauricio J, Resende M, Teixeira MR, Honavar M, Henrique R, Jeronimo C (2013) Altered expression of MGMT in high-grade gliomas results from the combined effect of epigenetic and genetic aberrations. PLoS One 8:e58206CrossRefPubMedCentralPubMed Ramalho-Carvalho J, Pires M, Lisboa S, Graca I, Rocha P, Barros-Silva JD, Savva-Bordalo J, Mauricio J, Resende M, Teixeira MR, Honavar M, Henrique R, Jeronimo C (2013) Altered expression of MGMT in high-grade gliomas results from the combined effect of epigenetic and genetic aberrations. PLoS One 8:e58206CrossRefPubMedCentralPubMed
45.
Zurück zum Zitat Reijneveld JC, Bottomley A, Taphoorn MJ, Coens C, Bromberg JE, Mason, Hoang-Xuan K, Brandes AA, Stupp R, Kantor G, Ben Hassel M, Ryan G, Wick W, Theissen B, Lacombe D, Gorlia T, Baumert B. (2013) Health related Quality of Life results from temozolomide chemotherapy vs. radiotherapy in molecularly characterized (1p loss) low-grade glioma. A randomized phase III Intergroup study by the EORTC/NCIC-CTG/TROG/MRC-CTU (EORTC 22033-26033). Neuro Oncol 15. 4th Quadrennial Meeting of the World Federation of Neuro-Oncology. San Francisco, CA, USA Reijneveld JC, Bottomley A, Taphoorn MJ, Coens C, Bromberg JE, Mason, Hoang-Xuan K, Brandes AA, Stupp R, Kantor G, Ben Hassel M, Ryan G, Wick W, Theissen B, Lacombe D, Gorlia T, Baumert B. (2013) Health related Quality of Life results from temozolomide chemotherapy vs. radiotherapy in molecularly characterized (1p loss) low-grade glioma. A randomized phase III Intergroup study by the EORTC/NCIC-CTG/TROG/MRC-CTU (EORTC 22033-26033). Neuro Oncol 15. 4th Quadrennial Meeting of the World Federation of Neuro-Oncology. San Francisco, CA, USA
46.
Zurück zum Zitat Rodriguez-Hernandez I, Garcia JL, Santos-Briz A, Hernandez-Lain A, Gonzalez-Valero JM, Gomez-Moreta JA, Toldos-Gonzalez O, Cruz JJ, Martin-Vallejo J, Gonzalez-Sarmiento R (2013) Integrated analysis of mismatch repair system in malignant astrocytomas. PLoS One 8:e76401CrossRefPubMedCentralPubMed Rodriguez-Hernandez I, Garcia JL, Santos-Briz A, Hernandez-Lain A, Gonzalez-Valero JM, Gomez-Moreta JA, Toldos-Gonzalez O, Cruz JJ, Martin-Vallejo J, Gonzalez-Sarmiento R (2013) Integrated analysis of mismatch repair system in malignant astrocytomas. PLoS One 8:e76401CrossRefPubMedCentralPubMed
47.
Zurück zum Zitat Rohde C, Zhang Y, Reinhardt R, Jeltsch A (2010) BISMA–fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinform 11:230CrossRef Rohde C, Zhang Y, Reinhardt R, Jeltsch A (2010) BISMA–fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinform 11:230CrossRef
48.
Zurück zum Zitat Ruda R, Magliola U, Bertero L, Trevisan E, Bosa C, Mantovani C, Ricardi U, Castiglione A, Monagheddu C, Soffietti R (2013) Seizure control following radiotherapy in patients with diffuse gliomas: a retrospective study. Neuro Oncol 15:1739–1749CrossRefPubMedCentralPubMed Ruda R, Magliola U, Bertero L, Trevisan E, Bosa C, Mantovani C, Ricardi U, Castiglione A, Monagheddu C, Soffietti R (2013) Seizure control following radiotherapy in patients with diffuse gliomas: a retrospective study. Neuro Oncol 15:1739–1749CrossRefPubMedCentralPubMed
49.
Zurück zum Zitat Scheinin I, Sie D, Bengtsson H, van de Wiel MA, Olshen AB, van Thuijl HF, van Essen HF, Eijk PP, Rustenburg F, Meijer GA, Reijneveld JC, Wesseling P, Pinkel D, Albertson DG, Ylstra B (2014) DNA copy number analysis of fresh and formalin-fixed specimens by shallow whole-genome sequencing with identification and exclusion of problematic regions in the genome assembly. Genome Res 24:2022–2032CrossRefPubMedCentralPubMed Scheinin I, Sie D, Bengtsson H, van de Wiel MA, Olshen AB, van Thuijl HF, van Essen HF, Eijk PP, Rustenburg F, Meijer GA, Reijneveld JC, Wesseling P, Pinkel D, Albertson DG, Ylstra B (2014) DNA copy number analysis of fresh and formalin-fixed specimens by shallow whole-genome sequencing with identification and exclusion of problematic regions in the genome assembly. Genome Res 24:2022–2032CrossRefPubMedCentralPubMed
50.
Zurück zum Zitat Shaw EG, Wang M, Coons SW, Brachman DG, Buckner JC, Stelzer KJ, Barger GR, Brown PD, Gilbert MR, Mehta MP (2012) Randomized trial of radiation therapy plus procarbazine, lomustine, and vincristine chemotherapy for supratentorial adult low-grade glioma: initial results of RTOG 9802. J Clin Oncol 30:3065–3070CrossRefPubMedCentralPubMed Shaw EG, Wang M, Coons SW, Brachman DG, Buckner JC, Stelzer KJ, Barger GR, Brown PD, Gilbert MR, Mehta MP (2012) Randomized trial of radiation therapy plus procarbazine, lomustine, and vincristine chemotherapy for supratentorial adult low-grade glioma: initial results of RTOG 9802. J Clin Oncol 30:3065–3070CrossRefPubMedCentralPubMed
51.
Zurück zum Zitat Shin YK, Heo SC, Shin JH, Hong SH, Ku JL, Yoo BC, Kim IJ, Park JG (2004) Germline mutations in MLH1, MSH2 and MSH6 in Korean hereditary non-polyposis colorectal cancer families. Hum Mutat 24:351CrossRefPubMed Shin YK, Heo SC, Shin JH, Hong SH, Ku JL, Yoo BC, Kim IJ, Park JG (2004) Germline mutations in MLH1, MSH2 and MSH6 in Korean hereditary non-polyposis colorectal cancer families. Hum Mutat 24:351CrossRefPubMed
52.
Zurück zum Zitat Silber JR, Blank A, Bobola MS, Ghatan S, Kolstoe DD, Berger MS (1999) O6-methylguanine-DNA methyltransferase-deficient phenotype in human gliomas: frequency and time to tumor progression after alkylating agent-based chemotherapy. Clin Cancer Res 5:807–814PubMed Silber JR, Blank A, Bobola MS, Ghatan S, Kolstoe DD, Berger MS (1999) O6-methylguanine-DNA methyltransferase-deficient phenotype in human gliomas: frequency and time to tumor progression after alkylating agent-based chemotherapy. Clin Cancer Res 5:807–814PubMed
53.
Zurück zum Zitat Taal W, Dubbink HJ, Zonnenberg CB, Zonnenberg BA, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Kros JM, Kouwenhoven MC, van Marion R, van Heuvel I, van der Holt B, Bromberg JE, Sillevis Smitt PA, Dinjens WN, van den Bent MJ (2011) First-line temozolomide chemotherapy in progressive low-grade astrocytomas after radiotherapy: molecular characteristics in relation to response. Neuro Oncol 13:235–241CrossRefPubMedCentralPubMed Taal W, Dubbink HJ, Zonnenberg CB, Zonnenberg BA, Postma TJ, Gijtenbeek JM, Boogerd W, Groenendijk FH, Kros JM, Kouwenhoven MC, van Marion R, van Heuvel I, van der Holt B, Bromberg JE, Sillevis Smitt PA, Dinjens WN, van den Bent MJ (2011) First-line temozolomide chemotherapy in progressive low-grade astrocytomas after radiotherapy: molecular characteristics in relation to response. Neuro Oncol 13:235–241CrossRefPubMedCentralPubMed
54.
Zurück zum Zitat van de Wiel MA, Kim KI, Vosse SJ, van Wieringen WN, Wilting SM, Ylstra B (2007) CGHcall: calling aberrations for array CGH tumor profiles. Bioinformatics 23:892–894CrossRefPubMed van de Wiel MA, Kim KI, Vosse SJ, van Wieringen WN, Wilting SM, Ylstra B (2007) CGHcall: calling aberrations for array CGH tumor profiles. Bioinformatics 23:892–894CrossRefPubMed
55.
Zurück zum Zitat van Thuijl HF, Scheinin I, Sie D, Alentorn A, van Essen HF, Cordes M, Fleischeuer R, Gijtenbeek AM, Beute G, van den Brink WA, Meijer GA, Havenith M, Idbaih A, Hoang-Xuan K, Mokhtari K, Verhaak R, van der Valk P, van de Wiel MA, Heimans JJ, Aronica E, Reijneveld JC, Wesseling P, Ylstra B (2014) Spatial and temporal evolution of distal 10q deletion, a prognostically unfavorable event in diffuse low-grade gliomas. Genome Biol 15:471CrossRefPubMedCentralPubMed van Thuijl HF, Scheinin I, Sie D, Alentorn A, van Essen HF, Cordes M, Fleischeuer R, Gijtenbeek AM, Beute G, van den Brink WA, Meijer GA, Havenith M, Idbaih A, Hoang-Xuan K, Mokhtari K, Verhaak R, van der Valk P, van de Wiel MA, Heimans JJ, Aronica E, Reijneveld JC, Wesseling P, Ylstra B (2014) Spatial and temporal evolution of distal 10q deletion, a prognostically unfavorable event in diffuse low-grade gliomas. Genome Biol 15:471CrossRefPubMedCentralPubMed
56.
Zurück zum Zitat Venkatraman ES, Olshen AB (2007) A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23:657–663CrossRefPubMed Venkatraman ES, Olshen AB (2007) A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23:657–663CrossRefPubMed
57.
Zurück zum Zitat Weber RG, Sabel M, Reifenberger J, Sommer C, Oberstrass J, Reifenberger G, Kiessling M, Cremer T (1996) Characterization of genomic alterations associated with glioma progression by comparative genomic hybridization. Oncogene 13:983–994PubMed Weber RG, Sabel M, Reifenberger J, Sommer C, Oberstrass J, Reifenberger G, Kiessling M, Cremer T (1996) Characterization of genomic alterations associated with glioma progression by comparative genomic hybridization. Oncogene 13:983–994PubMed
58.
Zurück zum Zitat Wick W, Meisner C, Hentschel B, Platten M, Schilling A, Wiestler B, Sabel MC, Koeppen S, Ketter R, Weiler M, Tabatabai G, von DA, Gramatzki D, Westphal M, Schackert G, Loeffler M, Simon M, Reifenberger G, Weller M (2013) Prognostic or predictive value of MGMT promoter methylation in gliomas depends on IDH1 mutation. Neurology 81:1515–1522CrossRefPubMed Wick W, Meisner C, Hentschel B, Platten M, Schilling A, Wiestler B, Sabel MC, Koeppen S, Ketter R, Weiler M, Tabatabai G, von DA, Gramatzki D, Westphal M, Schackert G, Loeffler M, Simon M, Reifenberger G, Weller M (2013) Prognostic or predictive value of MGMT promoter methylation in gliomas depends on IDH1 mutation. Neurology 81:1515–1522CrossRefPubMed
59.
Zurück zum Zitat www.clinicaltrials.gov (2013) NCT00003375, observation or radiation therapy with or without combination chemotherapy in treating patients with low-grade glioma www.​clinicaltrials.​gov (2013) NCT00003375, observation or radiation therapy with or without combination chemotherapy in treating patients with low-grade glioma
61.
Zurück zum Zitat Ye K, Schulz MH, Long Q, Apweiler R, Ning Z (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25:2865–2871CrossRefPubMedCentralPubMed Ye K, Schulz MH, Long Q, Apweiler R, Ning Z (2009) Pindel: a pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics 25:2865–2871CrossRefPubMedCentralPubMed
62.
Zurück zum Zitat Yip S, Miao J, Cahill DP, Iafrate AJ, Aldape K, Nutt CL, Louis DN (2009) MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 15:4622–4629CrossRefPubMedCentralPubMed Yip S, Miao J, Cahill DP, Iafrate AJ, Aldape K, Nutt CL, Louis DN (2009) MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 15:4622–4629CrossRefPubMedCentralPubMed
Metadaten
Titel
Evolution of DNA repair defects during malignant progression of low-grade gliomas after temozolomide treatment
verfasst von
Hinke F. van Thuijl
Tali Mazor
Brett E. Johnson
Shaun D. Fouse
Koki Aihara
Chibo Hong
Annika Malmström
Martin Hallbeck
Jan J. Heimans
Jenneke J. Kloezeman
Marie Stenmark-Askmalm
Martine L. M. Lamfers
Nobuhito Saito
Hiroyuki Aburatani
Akitake Mukasa
Mitchell S. Berger
Peter Söderkvist
Barry S. Taylor
Annette M. Molinaro
Pieter Wesseling
Jaap C. Reijneveld
Susan M. Chang
Bauke Ylstra
Joseph F. Costello
Publikationsdatum
01.04.2015
Verlag
Springer Berlin Heidelberg
Erschienen in
Acta Neuropathologica / Ausgabe 4/2015
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-015-1403-6

Weitere Artikel der Ausgabe 4/2015

Acta Neuropathologica 4/2015 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Neu im Fachgebiet Neurologie

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.