Recurrent glioblastomas reveal molecular subtypes associated with mechanistic implications of drug-resistance

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Kwon, So Mee ^a   Kang, Shin Hyuk ^b   Park, Chul Kee ^c   Jung, Shin ^d   Park, Eun Sung ^e   Lee, Ju Seog ^f   Kim, Se Hyuk ^a   Woo, Hyun Goo ^a  

^a Ajou University School of Medicine   (South Korea)

^b Korea University College of Medicine   (South Korea)

^c Seoul National University College of Medicine   (South Korea)

^d Chonnam National University Hwasun Hospital and Medical School   (South Korea)

^e Yonsei University College of Medicine   (South Korea)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOX PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROTEIN MSH6; TEMOZOLOMIDE; ANTINEOPLASTIC AGENT; DNA BINDING PROTEIN; DNA LIGASE; DNA METHYLTRANSFERASE; G-T MISMATCH-BINDING PROTEIN; MGMT PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ARTICLE; CANCER CLASSIFICATION; CANCER RECURRENCE; CANCER RESISTANCE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA REPAIR; FEMALE; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETIC TRAIT; GENETIC VARIABILITY; GLIOBLASTOMA; HUMAN; MALE; ONCOGENE; OUTCOME ASSESSMENT; PERSONALIZED MEDICINE; TRANSCRIPTOMICS; BRAIN NEOPLASMS; CANCER STEM CELL; CELL SELF-RENEWAL; CLUSTER ANALYSIS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; REPRODUCIBILITY; TUMOR RECURRENCE; TUMOR VOLUME; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL SELF RENEWAL; CLUSTER ANALYSIS; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NEOPLASTIC STEM CELLS; REPRODUCIBILITY OF RESULTS; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEINS;

EID: 84949008680     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140528     Document Type: Article

References (44)

1. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta neuropathologica. 2007; 114(2):97-109. doi: 10. 1007/s00401-007-0243-4 PMID: 17618441; PubMed Central PMCID: PMC1929165.
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(10):987-96. doi: 10. 1056/NEJMoa043330 PMID: 15758009.
3. Dennis G Jr., Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003; 4(5):P3. Epub 2003/05/08. PMID: 12734009; PubMed Central PMCID: PMC3720094.
4. Giese A, Kucinski T, Knopp U, Goldbrunner R, Hamel W, Mehdorn HM, et al. Pattern of recurrence following local chemotherapy with biodegradable carmustine (BCNU) implants in patients with glioblastoma. Journal of neuro-oncology. 2004; 66(3):351-60. PMID: 15015668.
5. Warde-Farley D, Donaldson SL, Comes O, Zuberi K, Badrawi R, Chao P, et al. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 2010; 38(Web Server issue):W214-20. Epub 2010/07/02. doi: 10.1093/nar/gkq537 PMID: 20576703; PubMed Central PMCID: PMC2896186.
6. Brennan CW, Verhaak RGW, McKenna A, Campos B, Noushmehr H, Salama SR, et al. XThe somatic genomic landscape of glioblastoma. Cell. 2013; 155(2):X462-77.
7. Maher EA, Brennan C, Wen PY, Durso L, Ligon KL, Richardson A, et al. Marked genomic differences characterize primary and secondary glioblastoma subtypes and identify two distinct molecular and clinical secondary glioblastoma entities. Cancer Research. 2006; 66(23):11502-13. doi: 10.1158/0008-5472.CAN-06-2072 PMID: 17114236
8. Shen R, Mo Q, Schultz N, Seshan VE, Olshen AB, Huse J, et al. Integrative subtype discovery in glioblastoma using iCluster. PLoS ONE. 2012; 7(4). doi: 10.1371/journal.pone.0035236
9. Verhaak RGW, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated Genomic Analysis Identifies Clinically Relevant Subtypes of Glioblastoma Characterized by Abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010; 17(1):98-110. doi: 10.1016/j.ccr.2009.12.020 PMID: 20129251
10. Cancer Genome Atlas Research N. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008; 455(7216):1061-8. doi: 10.1038/nature07385 PMID: 18772890; PubMed Central PMCID: PMC2671642.
11. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010; 17(1):98-110. doi: 10.1016/j.ccr.2009.12.020 PMID: 20129251; PubMed Central PMCID: PMC2818769.
12. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006; 9(3):157-73. doi: 10.1016/j.ccr.2006.02.019 PMID: 16530701.
13. Yoshimoto K, Mizoguchi M, Hata N, Murata H, Hatae R, Amano T, et al. Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Frontiers in oncology. 2012; 2:186. doi: 10.3389/fonc.2012.00186 PMID: 23227453; PubMed Central PMCID: PMC3514620.
14. Madhavan S, Zenklusen JC, Kotliarov Y, Sahni H, Fine HA, Buetow K. Rembrandt: helping personalized medicine become a reality through integrative translational research. Mol Cancer Res. 2009; 7 (2):157-67. doi: 10.1158/1541-7786.MCR-08-0435 PMID: 19208739; PubMed Central PMCID: PMC2645472.
15. Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010; 26(12):1572-3. doi: 10.1093/bioinformatics/btq170 PMID: 20427518; PubMed Central PMCID: PMC2881355.
16. Hoshida Y. Nearest template prediction: a single-sample-based flexible class prediction with confidence assessment. PLoS One. 2010; 5(11):e15543. doi: 10.1371/journal.pone.0015543 PMID: 21124904; PubMed Central PMCID: PMC2990751.
17. Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ, et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. The Lancet Oncology. 2006; 7(5):392-401. doi: 10.1016/S1470-2045(06) 70665-9 PMID: 16648043.
18. Zhou H, Kuang J, Zhong L, Kuo WL, Gray JW, Sahin A, et al. Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet. 1998; 20(2):189-93. doi: 10.1038/2496 PMID: 9771714.
19. Xia Z, Wei P, Zhang H, Ding Z, Yang L, Huang Z, et al. AURKA governs self-renewal capacity in glioma-initiating cells via stabilization/activation of beta-catenin/Wnt signaling. Mol Cancer Res. 2013; 11 (9):1101-11. doi: 10.1158/1541-7786.MCR-13-0044 PMID: 23761169.
20. Lehman NL, O'Donnell JP, Whiteley LJ, Stapp RT, Lehman TD, Roszka KM, et al. Aurora A is differentially expressed in gliomas, is associated with patient survival in glioblastoma and is a potential chemotherapeutic target in gliomas. Cell Cycle. 2012; 11(3):489-502. doi: 10.4161/cc.11.3.18996 PMID: 22274399; PubMed Central PMCID: PMC3315093.
21. Barton VN, Foreman NK, Donson AM, Birks DK, Handler MH, Vibhakar R. Aurora kinase A as a rational target for therapy in glioblastoma. Journal of neurosurgery Pediatrics. 2010; 6(1):98-105. doi: 10.3171/2010.3.PEDS10120 PMID: 20593995.
22. Mannino M, Gomez-Roman N, Hochegger H, Chalmers AJ. Differential sensitivity of Glioma stem cells to Aurora kinase A inhibitors: implications for stem cell mitosis and centrosome dynamics. Stem cell research. 2014; 13(1):135-43. doi: 10.1016/j.scr.2014.05.001 PMID: 24879067; PubMed Central PMCID: PMC4085484.
23. Borges KS, Castro-Gamero AM, Moreno DA, da Silva Silveira V, Brassesco MS, de Paula Queiroz RG, et al. Inhibition of Aurora kinases enhances chemosensitivity to temozolomide and causes radiosensitization in glioblastoma cells. Journal of cancer research and clinical oncology. 2012; 138(3):405-14. doi: 10.1007/s00432-011-1111-0 PMID: 22160182.
24. Zeng WF, Navaratne K, Prayson RA, Weil RJ. Aurora B expression correlates with aggressive behaviour in glioblastoma multiforme. J Clin Pathol. 2007; 60(2):218-21. doi: 10.1136/jcp.2006.036806 PMID: 17264249; PubMed Central PMCID: PMC1860618.
25. Zhang WW, Zhang XJ, Liu HX, Chen J, Ren YH, Huang DG, et al. Cdk1 is required for the self-renewal of mouse embryonic stem cells. J Cell Biochem. 2011; 112(3):942-8. doi: 10.1002/jcb.23010 PMID: 21328468.
26. Cheng CK, Gustafson WC, Charron E, Houseman BT, Zunder E, Goga A, et al. Dual blockade of lipid and cyclin-dependent kinases induces synthetic lethality in malignant glioma. Proc Natl Acad Sci U S A. 2012; 109(31):12722-7. doi: 10.1073/pnas.1202492109 PMID: 22802621; PubMed Central PMCID: PMC3411950.
27. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet. 2008; 40 (5):499-507. PMID: 18443585. doi: 10.1038/ng.127
28. Tilghman J, Wu H, Sang Y, Shi X, Guerrero-Cazares H, Quinones-Hinojosa A, et al. HMMR maintains the stemness and tumorigenicity of glioblastoma stem-like cells. Cancer Res. 2014; 74(11):3168-79. doi: 10.1158/0008-5472.CAN-13-2103 PMID: 24710409; PubMed Central PMCID: PMC4059010.
29. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, et al. Stem cell-related "selfrenewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J Clin Oncol. 2008; 26(18):3015-24. doi: 10.1200/JCO.2007.15.7164 PMID: 18565887.
30. Gaspar N, Marshall L, Perryman L, Bax DA, Little SE, Viana-Pereira M, et al. MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res. 2010; 70(22):9243-52. doi: 10.1158/0008-5472.CAN-10-1250 PMID: 20935218; PubMed Central PMCID: PMC3935452.
31. Kim JW, Kim JY, Kim JE, Kim SK, Chung HT, Park CK. HOXA10 is associated with temozolomide resistance through regulation of the homologous recombinant DNA repair pathway in glioblastoma cell lines. Genes & cancer. 2014; 5(5-6):165-74. PMID: 25061500; PubMed Central PMCID: PMC4104759.
32. 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(2):287-91. PMID: 1739631; PubMed Central PMCID: PMC1977719.
33. 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(10):997-1003. doi: 10.1056/NEJMoa043331 PMID: 15758010.
34. Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res. 2000; 6(7):2585-97. PMID: 10914698.
35. Kondo N, Takahashi A, Ono K, Ohnishi T. DNA damage induced by alkylating agents and repair pathways. Journal of nucleic acids. 2010; 2010:543531. doi: 10.4061/2010/543531 PMID: 21113301; PubMed Central PMCID: PMC2989456.
36. Alexander BM, Pinnell N, Wen PY, D'Andrea A. Targeting DNA repair and the cell cycle in glioblastoma. Journal of neuro-oncology. 2012; 107(3):463-77. doi: 10.1007/s11060-011-0765-4 PMID: 22113697.
37. Bartek J Jr., Ng K, Bartek J, FischerW, Carter B, Chen CC. Key concepts in glioblastoma therapy. J Neurol Neurosurg Psychiatry. 2012; 83(7):753-60. doi: 10.1136/jnnp-2011-300709 PMID: 22396442.
38. Kinsella TJ. Coordination of DNA mismatch repair and base excision repair processing of chemotherapy and radiation damage for targeting resistant cancers. Clin Cancer Res. 2009; 15(6):1853-9. doi: 10.1158/1078-0432.CCR-08-1307 PMID: 19240165.
39. Caldera V, Mellai M, Annovazzi L, Monzeglio O, Piazzi A, Schiffer D. MGMT hypermethylation and MDR system in glioblastoma cancer stem cells. Cancer Genomics Proteomics. 2012; 9(4):171-8. PMID: 22798502.
40. Madhusudan S, Hickson ID. DNA repair inhibition: a selective tumour targeting strategy. Trends Mol Med. 2005; 11(11):503-11. doi: 10.1016/j.molmed.2005.09.004 PMID: 16214418.
41. Raza SM, Fuller GN, Rhee CH, Huang S, Hess K, Zhang W, et al. Identification of necrosis-associated genes in glioblastoma by cDNA microarray analysis. Clin Cancer Res. 2004; 10(1 Pt 1):212-21. PMID: 14734472.
42. Park ES, Kim SJ, Kim SW, Yoon SL, Leem SH, Kim SB, et al. Cross-species hybridization of microarrays for studying tumor transcriptome of brain metastasis. Proc Natl Acad Sci U S A. 2011; 108 (42):17456-61. Epub 2011/10/12. doi: 10.1073/pnas.1114210108 PMID: 21987811; PubMed Central PMCID: PMC3198333.
43. Johnson BE, Mazor T, Hong C, Barnes M, Aihara K, McLean CY, et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science. 2014; 343(6167):189-93. doi: 10. 1126/science.1239947 PMID: 24336570; PubMed Central PMCID: PMC3998672.
44. Kim J, Lee IH, Cho HJ, Park CK, Jung YS, Kim Y, et al. Spatiotemporal Evolution of the Primary Glioblastoma Genome. Cancer Cell. 2015; 28(3):318-28. doi: 10.1016/j.ccell.2015.07.013 PMID: 26373279.