Intratumoral heterogeneity identified at the epigenetic, genetic and transcriptional level in glioblastoma

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Parker, Nicole R ^a,b,c   Hudson, Amanda L ^a,b,c   Khong, Peter ^a,b,c   Parkinson, Jonathon F ^a,b,c   Dwight, Trisha ^a,b,c   Ikin, Rowan J ^a,b,c   Zhu, Ying ^b,c,d   Cheng, Zhangkai Jason ^e   Vafaee, Fatemeh ^e   Chen, Jason ^f   Wheeler, Helen R ^a,b,c   Howell, Viive M ^a,b,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b Northern Sydney Local Health District ^*  (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d Hunter New England Area Health Service   (Australia)

^e UNIVERSITY OF SYDNEY   (Australia)

^f CENTRAL SYDNEY AREA HEALTH SERVICE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; DACARBAZINE; DNA LIGASE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; PHARMACOLOGICAL BIOMARKER; TEMOZOLOMIDE; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ANALOGS AND DERIVATIVES; BIOPSY; BRAIN NEOPLASMS; DNA METHYLATION; FEMALE; FOLLOW UP; GENE EXPRESSION PROFILING; GENETICS; GLIOBLASTOMA; HIGH THROUGHPUT SEQUENCING; HUMAN; MALE; MIDDLE AGED; PROMOTER REGION; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS, ALKYLATING; BIOMARKERS, PHARMACOLOGICAL; BIOMARKERS, TUMOR; BIOPSY; BRAIN NEOPLASMS; DACARBAZINE; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION PROFILING; GLIOBLASTOMA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MALE; MIDDLE AGED; PROMOTER REGIONS, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84960517189     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22477     Document Type: Article

References (48)

1. Stupp, R. 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 EORTC-NCIC trial. Lancet Oncol 10, 459-466 (2009).
2. Omuro, A. & DeAngelis, L. M. Glioblastoma and other malignant gliomas: a clinical review. JAMA 310, 1842-1850 (2013).
3. Patel, A. P. et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science 344, 1396-1401 (2014).
4. Nabilsi, N. H. et al. Multiplex mapping of chromatin accessibility and DNA methylation within targeted single molecules identifies epigenetic heterogeneity in neural stem cells and glioblastoma. Genome Res 24, 329-339 (2014).
5. Szerlip, N. J. et al. Intratumoral heterogeneity of receptor tyrosine kinases EGFR and PDGFRA amplification in glioblastoma defines subpopulations with distinct growth factor response. Proc Natl Acad Sci USA 109, 3041-3046 (2012).
6. Snuderl, M. et al. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20, 810-817 (2011).
7. Nickel, G. C. et al. Characterizing mutational heterogeneity in a glioblastoma patient with double recurrence. PLoS One 7, e35262 (2012).
8. Bonavia, R., Inda, M. M., Cavenee, W. K. & Furnari, F. B. Heterogeneity maintenance in glioblastoma: a social network. Cancer Res 71, 4055-4060 (2011).
9. Shapiro, J. R., Yung, W. K. & Shapiro, W. R. Isolation, karyotype, and clonal growth of heterogeneous subpopulations of human malignant gliomas. Cancer Res 41, 2349-2359 (1981).
10. Sottoriva, A. et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci USA 110, 4009-4014 (2013).
11. Little, S. E. et al. Receptor tyrosine kinase genes amplified in glioblastoma exhibit a mutual exclusivity in variable proportions reflective of individual tumor heterogeneity. Cancer Res 72, 1614-1620 (2012).
12. Johnson, B. E. et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 343, 189-193 (2014).
13. Nathanson, D. A. et al. Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science 343, 72-76 (2014).
14. Hegi, M. E. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352, 997-1003 (2005).
15. Verhaak, R. G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110 (2010).
16. Colman, H. et al. A multigene predictor of outcome in glioblastoma. Neuro Oncol 12, 49-57 (2010).
17. Bhat, K. P. et al. Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma. Cancer Cell 24, 331-346 (2013).
18. Phillips, H. S. et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9, 157-173 (2006).
19. Brennan, C. et al. Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS One 4, e7752 (2009).
20. Bady, P. et al. 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, 547-560 (2012).
21. Yung, W. K., Shapiro, J. R. & Shapiro, W. R. Heterogeneous chemosensitivities of subpopulations of human glioma cells in culture. Cancer Res 42, 992-998 (1982).
22. Parkinson, J. F. et al. Variation of O(6)-methylguanine-DNA methyltransferase (MGMT) promoter methylation in serial samples in glioblastoma. J Neurooncol 87, 71-78 (2008).
23. Grasbon-Frodl, E. M. et al. Intratumoral homogeneity of MGMT promoter hypermethylation as demonstrated in serial stereotactic specimens from anaplastic astrocytomas and glioblastomas. Int J Cancer 121, 2458-2464 (2007).
24. Mollemann, M., Wolter, M., Felsberg, J., Collins, V. P. & Reifenberger, G. Frequent promoter hypermethylation and low expression of the MGMT gene in oligodendroglial tumors. Int J Cancer 113, 379-385 (2005).
25. Hegi, M. E. et al. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol 26, 4189-4199 (2008).
26. Hermanson, M. et al. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 52, 3213-3219 (1992).
27. Nabeshima, K. et al. Expression of c-Met correlates with grade of malignancy in human astrocytic tumours: an immunohistochemical study. Histopathology 31, 436-443 (1997).
28. Koga, K. et al. Expression of angiopoietin-2 in human glioma cells and its role for angiogenesis. Cancer Res 61, 6248-6254 (2001).
29. Bello, L. et al. Alpha(v)beta3 and alpha(v)beta5 integrin expression in glioma periphery. Neurosurgery 49, 380-389; discussion 390 (2001).
30. Nishikawa, R. et al. Immunohistochemical analysis of the mutant epidermal growth factor, deltaEGFR, in glioblastoma. Brain Tumor Pathol 21, 53-56 (2004).
31. Jung, V. et al. Evidence of focal genetic microheterogeneity in glioblastoma multiforme by area-specific CGH on microdissected tumor cells. J Neuropathol Exp Neurol 58, 993-999 (1999).
32. Silber, J. R. et al. The apurinic/apyrimidinic endonuclease activity of Ape1/Ref-1 contributes to human glioma cell resistance to alkylating agents and is elevated by oxidative stress. Clin Cancer Res 8, 3008-3018 (2002).
33. Bobola, M. S., Kolstoe, D. D., Blank, A., Chamberlain, M. C. & Silber, J. R. Repair of 3-methyladenine and abasic sites by base excision repair mediates glioblastoma resistance to temozolomide. Front Oncol 2, 176 (2012).
34. Jiricny, J. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7, 335-346 (2006).
35. Yip, S. et al. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 15, 4622-4629 (2009).
36. Cahill, D. P. et al. Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 13, 2038-2045 (2007).
37. Felsberg, J. 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 129, 659-670 (2011).
38. Shinsato, Y. et al. Reduction of MLH1 and PMS2 confers temozolomide resistance and is associated with recurrence of glioblastoma. Oncotarget (2013).
39. Nguyen, S. A. et al. Novel MSH6 Mutations in Treatment-Naive Glioblastoma and Anaplastic Oligodendroglioma Contribute to Temozolomide Resistance Independently of MGMT Promoter Methylation. Clin Cancer Res 20, 4894-4903 (2014).
40. Venere, M. et al. Therapeutic targeting of constitutive PARP activation compromises stem cell phenotype and survival of glioblastoma-initiating cells. Cell Death Differ 21, 258-269 (2014).
41. Tang, J. B. et al. N-methylpurine DNA glycosylase and DNA polymerase beta modulate BER inhibitor potentiation of glioma cells to temozolomide. Neuro Oncol 13, 471-486 (2011).
42. Barazzuol, L. et al. Evaluation of poly (ADP-ribose) polymerase inhibitor ABT-888 combined with radiotherapy and temozolomide in glioblastoma. Radiat Oncol 8, 65 (2013).
43. Mohammed, M. Z. et al. Development and evaluation of human AP endonuclease inhibitors in melanoma and glioma cell lines. Br J Cancer 104, 653-663 (2011).
44. Dunn, J. et al. Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 101, 124-131 (2009).
45. Andersen, C. L., Jensen, J. L. & Orntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64, 5245-5250 (2004).
46. Dvinge, H. & Bertone, P. HTqPCR: high-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics 25, 3325-3326 (2009).
47. Verhaak, R. G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98-110 (2010).
48. Choi, Y. A Fast Computation of Pairwise Sequence Alignment Scores Between a Protein and a Set of Single-Locus Variants of Another Protein. In: In Proceedings of the ACM Conference on Bioinformatics, Computational Biology and Biomedicine (BCB' 12) Edited by ACM, vol. 12. New York, NY, USA, 414-417 (2012).