Multi-platform molecular profiling of a large cohort of glioblastomas reveals potential therapeutic strategies

Oncotarget

Volumn 7, Issue 16, 2016, Pages 21556-21569

  Xiu, Joanne ^a   Piccioni, David ^b   Juarez, Tiffany ^b   Pingle, Sandeep C ^b   Hu, Jethro ^c   Rudnick, Jeremy ^c   Fink, Karen ^d   Spetzler, David B ^a   Maney, Todd ^a   Ghazalpour, Anatole ^a   Bender, Ryan ^a   Gatalica, Zoran ^a   Reddy, Sandeep ^a   Sanai, Nader ^e   Idbaih, Ahmed ^f,g,h,i   Glantz, Michael ^j   Kesari, Santosh ^b,k,l  

^a CARIS LIFE SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^e BARROW NEUROLOGICAL INSTITUTE   (United States)

^f PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^g SORBONNE UNIVERSITÉ   (France)

^h INSERM   (France)

ⁱ CNRS   (France)

^j PENN STATE COLLEGE OF MEDICINE   (United States)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l JOHN WAYNE CANCER INSTITUTE   (United States)

more..

Author keywords

EGFRvIII; Glioblastoma; IDH1; MGMT promoter methylation; Tumor profiling

Indexed keywords

ISOCITRATE DEHYDROGENASE 1; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN P53; TUMOR MARKER; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; CANCER GRADING; CANCER PROGNOSIS; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; DNA METHYLATION; EGFRVIII GENE; FEMALE; GENE; GENE AMPLIFICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC ASSOCIATION; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; IDH1 GENE; INDEL MUTATION; MAJOR CLINICAL STUDY; MALE; MGMT GENE; MIDDLE AGED; MOLECULAR BIOLOGY; MOLECULAR PROFILING; MUTATIONAL ANALYSIS; PD 1 GENE; PD L1 GENE; POINT MUTATION; PR GENE; PREDICTIVE VALUE; PROMOTER REGION; PROTEIN EXPRESSION; SURVIVAL PREDICTION; SURVIVAL TIME; TOPO1 GENE; TP53 GENE; TUMOR DIFFERENTIATION; AGE; BRAIN TUMOR; GENETICS; METABOLISM; MUTATION; PROGNOSIS; SURVIVAL ANALYSIS; VERY ELDERLY; YOUNG ADULT;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; BRAIN NEOPLASMS; DNA METHYLATION; GENE AMPLIFICATION; GLIOBLASTOMA; HUMANS; MIDDLE AGED; MUTATION; PROGNOSIS; PROMOTER REGIONS, GENETIC; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEINS; YOUNG ADULT;

EID: 84965036990     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7722     Document Type: Article

References (53)

1. Dolecek TA, Propp JM, Stroup NE and Kruchko C. CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2005-2009. Neuro-oncology. 2012; 14 Suppl 5:v1-49.
2. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA: a cancer journal for clinicians. 2014; 64(1):9-29.
3. Furnari FB, Cloughesy TF, Cavenee WK and Mischel PS. Heterogeneity of epidermal growth factor receptor signalling networks in glioblastoma. Nat Rev Cancer. 2015; 15(5):302-310.
4. Kesari S. Understanding glioblastoma tumor biology: the potential to improve current diagnosis and treatments. Seminars in oncology. 2011; 38 Suppl 4:S2-10.
5. Agnihotri S, Burrell KE, Wolf A, Jalali S, Hawkins C, Rutka JT and Zadeh G. Glioblastoma, a brief review of history, molecular genetics, animal models and novel therapeutic strategies. Archivum immunologiae et therapiae experimentalis. 2013; 61(1):25-41.
6. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. The New England journal of medicine. 2005; 352(10):987-996.
7. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, Alexe G, Lawrence M, O'Kelly M, Tamayo P, Weir BA, Gabriel S, 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.
8. Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu CJ, Genovese G, Shmulevich I, Barnholtz-Sloan J, et al. The somatic genomic landscape of glioblastoma. Cell. 2013; 155(2):462-477.
9. Crespo I, Vital AL, Gonzalez-Tablas M, Patino Mdel C, Otero A, Lopes MC, de Oliveira C, Domingues P, Orfao A and Tabernero MD. Molecular and Genomic Alterations in Glioblastoma Multiforme. The American journal of pathology. 2015; 185(7):1820-1833.
10. Malmstrom A, Gronberg BH, Marosi C, Stupp R, Frappaz D, Schultz H, Abacioglu U, Tavelin B, Lhermitte B, Hegi ME, Rosell J and Henriksson R. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: the Nordic randomised, phase 3 trial. The Lancet Oncology. 2012; 13(9):916-926.
11. Wick W, Platten M, Meisner C, Felsberg J, Tabatabai G, Simon M, Nikkhah G, Papsdorf K, Steinbach JP, Sabel M, Combs SE, Vesper J, Braun C, Meixensberger J, Ketter R, Mayer-Steinacker R, et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. The Lancet Oncology. 2012; 13(7):707-715.
12. Olar A and Aldape KD. Using the molecular classification of glioblastoma to inform personalized treatment. The Journal of pathology. 2014; 232(2):165-177.
13. Gan HK, Cvrljevic AN and Johns TG. The epidermal growth factor receptor variant III (EGFRvIII): where wild things are altered. The FEBS journal. 2013; 280(21):5350-5370.
14. 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, et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science (New York, NY). 2014; 343(6167):189-193.
15. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. The New England journal of medicine. 2012; 366(26):2443-2454.
16. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, et al. IDH1 and IDH2 mutations in gliomas. The New England journal of medicine. 2009; 360(8):765-773.
17. Von HoffDD, Stephenson JJ, Jr., Rosen P, Loesch DM, Borad MJ, Anthony S, Jameson G, Brown S, Cantafio N, Richards DA, Fitch TR, Wasserman E, Fernandez C, Green S, Sutherland W, Bittner M, et al. Pilot study using molecular profiling of patients' tumors to find potential targets and select treatments for their refractory cancers. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2010; 28(33):4877-4883.
18. Tsimberidou AM, Iskander NG, Hong DS, Wheler JJ, Falchook GS, Fu S, Piha-Paul S, Naing A, Janku F, Luthra R, Ye Y, Wen S, Berry D and Kurzrock R. Personalized medicine in a phase I clinical trials program: the MD Anderson Cancer Center initiative. Clinical cancer research: an official journal of the American Association for Cancer Research. 2012; 18(22):6373-6383.
19. Jameson GS, Petricoin EF, Sachdev J, Liotta LA, Loesch DM, Anthony SP, Chadha MK, Wulfkuhle JD, Gallagher RI, Reeder KA, Pierobon M, Fulk MR, Cantafio NA, Dunetz B, Mikrut WD, Von HoffDD, et al. A pilot study utilizing multi-omic molecular profiling to find potential targets and select individualized treatments for patients with previously treated metastatic breast cancer. Breast cancer research and treatment. 2014; 147(3):579-588.
20. Tsimberidou AM, Wen S, Hong DS, Wheler JJ, Falchook GS, Fu S, Piha-Paul S, Naing A, Janku F, Aldape K, Ye Y, Kurzrock R and Berry D. Personalized medicine for patients with advanced cancer in the phase I program at MD anderson: validation and landmark analyses. Clinical cancer research: an official journal of the American Association for Cancer Research. 2014; 20(18):4827-4836.
21. Febbo PG, Ladanyi M, Aldape KD, De Marzo AM, Hammond ME, Hayes DF, Iafrate AJ, Kelley RK, Marcucci G, Ogino S, Pao W, Sgroi DC and Birkeland ML. NCCN Task Force report: Evaluating the clinical utility of tumor markers in oncology. Journal of the National Comprehensive Cancer Network: JNCCN. 2011; 9 Suppl 5:S1-32; quiz S33.
22. 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, MirimanoffRO, Cairncross JG, Janzer RC and Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. The New England journal of medicine. 2005; 352(10):997-1003.
23. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, 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. The Lancet Oncology. 2009; 10(5):459-466.
24. Sampson JH, Aldape KD, Archer GE, Coan A, Desjardins A, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling R, Shi W, Vredenburgh JJ, et al. Greater chemotherapy-induced lymphopenia enhances tumorspecific immune responses that eliminate EGFRvIIIexpressing tumor cells in patients with glioblastoma. Neurooncology. 2011; 13(3):324-333.
25. Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE, 2nd, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling RJ, Shi W, Vredenburgh JJ and Bigner DD. Immunologic escape after prolonged progressionfree survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2010; 28(31):4722-4729.
26. Schuster J, Lai RK, Recht LD, Reardon DA, Paleologos NA, Groves MD, Mrugala MM, Jensen R, Baehring JM, Sloan A, Archer GE, Bigner DD, Cruickshank S, Green JA, Keler T, Davis TA, et al. A phase II, multicenter trial of rindopepimut (CDX-110) in newly diagnosed glioblastoma: the ACT III study. Neuro-oncology. 2015; 17(6):854-861.
27. Gong W, Zhang X, Wu J, Chen L, Li L, Sun J, Lv Y, Wei X, Du Y, Jin H and Dong J. RRM1 expression and clinical outcome of gemcitabine-containing chemotherapy for advanced non-small-cell lung cancer: a meta-analysis. Lung cancer (Amsterdam, Netherlands). 2012; 75(3):374-380.
28. Qiu LX, Tang QY, Bai JL, Qian XP, Li RT, Liu BR and Zheng MH. Predictive value of thymidylate synthase expression in advanced colorectal cancer patients receiving fluoropyrimidine-based chemotherapy: evidence from 24 studies. International journal of cancer Journal international du cancer. 2008; 123(10):2384-2389.
29. Metro G, Fabi A, Mirri MA, Vidiri A, Pace A, Carosi M, Russillo M, Maschio M, Giannarelli D, Pellegrini D, Pompili A, Cognetti F and Carapella CM. Phase II study of fixed dose rate gemcitabine as radiosensitizer for newly diagnosed glioblastoma multiforme. Cancer chemotherapy and pharmacology. 2010; 65(2):391-397.
30. Grunda JM, Fiveash J, Palmer CA, Cantor A, Fathallah-Shaykh HM, Nabors LB and Johnson MR. Rationally designed pharmacogenomic treatment using concurrent capecitabine and radiotherapy for glioblastoma; gene expression profiles associated with outcome. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16(10):2890-2898.
31. BerghoffAS, Kiesel B, Widhalm G, Rajky O, Ricken G, Wohrer A, Dieckmann K, Filipits M, Brandstetter A, Weller M, Kurscheid S, Hegi ME, Zielinski CC, Marosi C, Hainfellner JA, Preusser M, et al. Programmed death ligand 1 expression and tumor-infiltrating lymphocytes in glioblastoma. Neuro-oncology. 2015; 17(8):1064-1075.
32. Barazzuol L, Jena R, Burnet NG, Meira LB, Jeynes JC, Kirkby KJ and Kirkby NF. Evaluation of poly (ADP-ribose) polymerase inhibitor ABT-888 combined with radiotherapy and temozolomide in glioblastoma. Radiation oncology (London, England). 2013; 8:65.
33. Gan H. A phase 1 study evaluating ABT-414 in combination with temozolomide (TMZ) for subjects with recurrent or unresectable glioblastoma (GBM). Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2015; 32(5s):suppl; abstr 2021.
34. Wiestler B, Capper D, Sill M, Jones DT, Hovestadt V, Sturm D, Koelsche C, Bertoni A, Schweizer L, Korshunov A, Weiss EK, Schliesser MG, Radbruch A, Herold-Mende C, Roth P, Unterberg A, et al. Integrated DNA methylation and copy-number profiling identify three clinically and biologically relevant groups of anaplastic glioma. Acta neuropathologica. 2014; 128(4):561-571.
35. Suzuki H, Aoki K, Chiba K, Sato Y, Shiozawa Y, Shiraishi Y, Shimamura T, Niida A, Motomura K, Ohka F, Yamamoto T, Tanahashi K, Ranjit M, Wakabayashi T, Yoshizato T, Kataoka K, et al. Mutational landscape and clonal architecture in grade II and III gliomas. Nature genetics. 2015; 47(5):458-468.
36. Park CK, Kim JE, Kim JY, Song SW, Kim JW, Choi SH, Kim TM, Lee SH, Kim IH and Park SH. The Changes in MGMT Promoter Methylation Status in Initial and Recurrent Glioblastomas. Translational oncology. 2012; 5(5):393-397.
37. 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, et al. O(6)-methylguanine DNAmethyltransferase methylation status can change between first surgery for newly diagnosed glioblastoma and second surgery for recurrence: clinical implications. Neurooncology. 2010; 12(3):283-288.
38. Tonn J. MGMT promoter methylation status and DNA mismatch repair genes in paired primary and recurrent glioblastoma: A translational study of the German Glioma Network. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2010; 28(2076).
39. Su KY, Chen HY, Li KC, Kuo ML, Yang JC, Chan WK, Ho BC, Chang GC, Shih JY, Yu SL and Yang PC. Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2012; 30(4):433-440.
40. Yasuda H, Kobayashi S and Costa DB. EGFR exon 20 insertion mutations in non-small-cell lung cancer: preclinical data and clinical implications. The Lancet Oncology. 2012; 13(1):e23-e31.
41. Raizer JJ, Abrey LE, Lassman AB, Chang SM, Lamborn KR, Kuhn JG, Yung WK, Gilbert MR, Aldape KA, Wen PY, Fine HA, Mehta M, Deangelis LM, Lieberman F, Cloughesy TF, Robins HI, et al. A phase II trial of erlotinib in patients with recurrent malignant gliomas and nonprogressive glioblastoma multiforme postradiation therapy. Neuro-oncology. 2010; 12(1):95-103.
42. Hanel W and Moll UM. Links between mutant p53 and genomic instability. Journal of cellular biochemistry. 2012; 113(2):433-439.
43. Sun Z, Huang C, He J, Lamb KL, Kang X, Gu T, Shen WH and Yin Y. PTEN C-terminal deletion causes genomic instability and tumor development. Cell reports. 2014; 6(5):844-854.
44. Gilbert MR, Wang M, Aldape KD, Stupp R, Hegi ME, Jaeckle KA, Armstrong TS, Wefel JS, Won M, Blumenthal DT, Mahajan A, Schultz CJ, Erridge S, Baumert B, Hopkins KI, Tzuk-Shina T, et al. Dose-dense temozolomide for newly diagnosed glioblastoma: a randomized phase III clinical trial. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2013; 31(32):4085-4091.
45. Gilbert MR DJ. RTOG 0825: Phase III double-blind placebo-controlled trial evaluating bevacizumab (Bev) in patients (Pts) with newly diagnosed glioblastoma (GBM). J Clin Oncol 31, 2013b (suppl; abstr 1).
46. Network. NCC. NCCN Clinical Practice Guidelines in Oncology. Central Nervous System Cancers. National Comprehensive Cancer Network. Version 1.2014;.
47. Hsu DW, Efird JT and Hedley-Whyte ET. Progesterone and estrogen receptors in meningiomas: prognostic considerations. Journal of neurosurgery. 1997; 86(1):113-120.
48. Kabat GC, Etgen AM and Rohan TE. Do steroid hormones play a role in the etiology of glioma? Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2010; 19(10):2421-2427.
49. Assimakopoulou M, Sotiropoulou-Bonikou G, Maraziotis T and Varakis J. Does sex steroid receptor status have any prognostic or predictive significance in brain astrocytic tumors? Clinical neuropathology. 1998; 17(1):27-34.
50. Atif F, Patel NR, Yousuf S and Stein DG. The Synergistic Effect of Combination Progesterone and Temozolomide on Human Glioblastoma Cells. PloS one. 2015; 10(6):e0131441.
51. Braun MS, Richman SD, Quirke P, Daly C, Adlard JW, Elliott F, Barrett JH, Selby P, Meade AM, Stephens RJ, Parmar MK and Seymour MT. Predictive biomarkers of chemotherapy efficacy in colorectal cancer: results from the UK MRC FOCUS trial. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2008; 26(16):2690-2698.
52. Sun JM, Ahn JS, Jung SH, Sun J, Ha SY, Han J, Park K and Ahn MJ. Pemetrexed Plus Cisplatin Versus Gemcitabine Plus Cisplatin According to Thymidylate Synthase Expression in Nonsquamous Non-Small-Cell Lung Cancer: A Biomarker-Stratified Randomized Phase II Trial. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2015; 33(22):2450-2456.
53. Millis SZ, Bryant D, Basu G, Bender R, Vranic S, Gatalica Z and Vogelzang NJ. Molecular profiling of infiltrating urothelial carcinoma of bladder and nonbladder origin. Clinical genitourinary cancer. 2015; 13(1):e37-49.