Mutation and expression analysis in medulloblastoma yields prognostic variants and a putative mechanism of disease for i17q tumors

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Bien Willner, Gabriel A ^a,b   Mitra, Robi D ^b  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Expression; Fluidigm; Group 4; I17q; Medulloblastoma; Next generation sequencing; Outcomes

Indexed keywords

BIOLOGICAL MARKER; PROTEIN P53; TP53 PROTEIN, HUMAN;

CEREBELLAR NEOPLASMS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME 17; CHROMOSOME ABERRATION; GENE EXPRESSION PROFILING; GENETICS; HUMAN; MALE; MEDULLOBLASTOMA; MUTATION; PROGNOSIS; SURVIVAL;

BIOLOGICAL MARKERS; CEREBELLAR NEOPLASMS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME ABERRATIONS; CHROMOSOMES, HUMAN, PAIR 17; GENE EXPRESSION PROFILING; HUMANS; MALE; MEDULLOBLASTOMA; MUTATION; PROGNOSIS; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84929939479     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/s40478-014-0074-1     Document Type: Article

References (56)

1. Gurney JG, Smith MA, Bunin GR: CNS and miscellaneous intracranial and intraspinal neoplasms. In Cancer incidence and survival among children and adolescents: United States SEER program 1975-1995, vol NIH Pub. No. 99-4649. Edited by: Reis LAG, Smith MA, Gurney JG. National Cancer Research Institute Cancer Surveillance Research Program, NIH Pub. No. 99-4649, Bethesda, MD; 1999:51-63.
2. Gurney JG, Kadan-Lottick N: Brain and other central nervous system tumors: rates, trends, and epidemiology. Curr Opin Oncol 2001, 13(3):160-166. 10.1097/00001622-200105000-00005
3. Packer RJ, Gajjar A, Vezina G, Rorke-Adams L, Burger PC, Robertson PL, Bayer L, LaFond D, Donahue BR, Marymont MH, Muraszko K, Langston J, Sposto R: Phase III study of craniospinal radiation therapy followed by adjuvant chemotherapy for newly diagnosed average-risk medulloblastoma. J Clin Oncol 2006, 24(25):4202-4208. doi:24/25/4202 10.1200/JCO.2006.06.4980
4. Packer RJ, Sutton LN, Elterman R, Lange B, Goldwein J, Nicholson HS, Mulne L, Boyett J, D'Angio G, Wechsler-Jentzsch K, Reaman G, Cohen BH, Bruce DA, Rorke LB, Molloy P, Ryan J, LaFond D, Evans A, Schut L: Outcome for children with medulloblastoma treated with radiation and cisplatin, CCNU, and vincristine chemotherapy. J Neurosurg 1994, 81(5):690-698. doi:10.3171/jns.1994.81.5.0690 10.3171/jns.1994.81.5.0690
5. Gajjar A, Chintagumpala M, Ashley D, Kellie S, Kun LE, Merchant TE, Woo S, Wheeler G, Ahern V, Krasin MJ, Fouladi M, Broniscer A, Krance R, Hale GA, Stewart CF, Dauser R, Sanford RA, Fuller C, Lau C, Boyett JM, Wallace D, Gilbertson RJ: Risk-adapted craniospinal radiotherapy followed by high-dose chemotherapy and stem-cell rescue in children with newly diagnosed medulloblastoma (St Jude Medulloblastoma-96): long-term results from a prospective, multicentre trial. Lancet Oncol 2006, 7(10):813-820. doi:S1470-2045(06)70867-1 10.1016/S1470-2045(06)70867-1
6. Polkinghorn WR, Tarbell NJ: Medulloblastoma: tumorigenesis, current clinical paradigm, and efforts to improve risk stratification. Nat Clin Pract Oncol 2007, 4(5):295-304. doi:ncponc0794 10.1038/ncponc0794
7. Ellison DW, Kocak M, Dalton J, Megahed H, Lusher ME, Ryan SL, Zhao W, Nicholson SL, Taylor RE, Bailey S, Clifford SC: Definition of disease-risk stratification groups in childhood medulloblastoma using combined clinical, pathologic, and molecular variables. J Clin Oncol 2010, 29(11):1400-1407. doi:JCO.2010.30.2810 10.1200/JCO.2010.30.2810
8. Pfister S, Remke M, Benner A, Mendrzyk F, Toedt G, Felsberg J, Wittmann A, Devens F, Gerber NU, Joos S, Kulozik A, Reifenberger G, Rutkowski S, Wiestler OD, Radlwimmer B, Scheurlen W, Lichter P, Korshunov A: Outcome prediction in pediatric medulloblastoma based on DNA copy-number aberrations of chromosomes 6q and 17q and the MYC and MYCN loci. J Clin Oncol 2009, 27(10):1627-1636. doi:JCO.2008.17.9432 10.1200/JCO.2008.17.9432
9. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, Stolovitzky G, Louis DN, Mesirov JP, Lander ES, Golub TR: Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 2002, 415(6870):436-442. doi:10.1038/415436a 10.1038/415436a
10. Eberhart CG, Kepner JL, Goldthwaite PT, Kun LE, Duffner PK, Friedman HS, Strother DR, Burger PC: Histopathologic grading of medulloblastomas: a pediatric oncology group study. Cancer 2002, 94(2):552-560. doi:10.1002/cncr.10189 10.1002/cncr.10189
11. Perry A: Medulloblastomas with favorable versus unfavorable histology: how many small blue cell tumor types are there in the brain? Adv Anat Pathol 2002, 9(6):345-350. 10.1097/00125480-200211000-00003
12. Brown HG, Kepner JL, Perlman EJ, Friedman HS, Strother DR, Duffner PK, Kun LE, Goldthwaite PT, Burger PC: "Large cell/anaplastic" medulloblastomas: a pediatric oncology group study. J Neuropathol Exp Neurol 2000, 59(10):857-865.
13. Bayani J, Zielenska M, Marrano P, Kwan Ng Y, Taylor MD, Jay V, Rutka JT, Squire JA: Molecular cytogenetic analysis of medulloblastomas and supratentorial primitive neuroectodermal tumors by using conventional banding, comparative genomic hybridization, and spectral karyotyping. J Neurosurg 2000, 93(3):437-448. doi:10.3171/jns.2000.93.3.0437 10.3171/jns.2000.93.3.0437
14. Nicholson J, Wickramasinghe C, Ross F, Crolla J, Ellison D: Imbalances of chromosome 17 in medulloblastomas determined by comparative genomic hybridisation and fluorescence in situ hybridisation. Mol Pathol 2000, 53(6):313-319. 10.1136/mp.53.6.313
15. McCabe MG, Ichimura K, Liu L, Plant K, Backlund LM, Pearson DM, Collins VP: High-resolution array-based comparative genomic hybridization of medulloblastomas and supratentorial primitive neuroectodermal tumors. J Neuropathol Exp Neurol 2006, 65(6):549-561. 10.1097/00005072-200606000-00003
16. Mendrzyk F, Korshunov A, Toedt G, Schwarz F, Korn B, Joos S, Hochhaus A, Schoch C, Lichter P, Radlwimmer B: Isochromosome breakpoints on 17p in medulloblastoma are flanked by different classes of DNA sequence repeats. Genes Chromosomes Cancer 2006, 45(4):401-410. 10.1002/gcc.20304
17. Carvalho CM, Lupski JR: Copy number variation at the breakpoint region of isochromosome 17q. Genome Res 2008, 18(11):1724-1732. doi:gr.080697.108 10.1101/gr.080697.108
18. Shaw CJ, Lupski JR: Implications of human genome architecture for rearrangement-based disorders: the genomic basis of disease. Hum Mol Genet 2004, 13(1):R57-64. 10.1093/hmg/ddh073
19. Bien-Willner GA, Lopez-Terrada D, Bhattacharjee MB, Patel KU, Stankiewicz P, Lupski JR, Pfeifer JD, Perry A: Early recurrence in standard-risk medulloblastoma patients with the common idic(17)(p11.2) rearrangement. Neuro Oncol 2012, 14(7):831-840. doi:10.1093/neuonc/nos086 10.1093/neuonc/nos086
20. Min HS, Lee JY, Kim SK, Park SH: Genetic grouping of medulloblastomas by representative markers in pathologic diagnosis. Transl Oncol 2013, 6(3):265-272. 10.1593/tlo.12382
21. Scheurlen WG, Schwabe GC, Joos S, Mollenhauer J, Sorensen N, Kuhl J: Molecular analysis of childhood primitive neuroectodermal tumors defines markers associated with poor outcome. J Clin Oncol 1998, 16(7):2478-2485.
22. Gilbertson R, Wickramasinghe C, Hernan R, Balaji V, Hunt D, Jones-Wallace D, Crolla J, Perry R, Lunec J, Pearson A, Ellison D: Clinical and molecular stratification of disease risk in medulloblastoma. Br J Cancer 2001, 85(5):705-712. doi:10.1054/bjoc.2001.1987 10.1054/bjoc.2001.1987
23. Cogen PH, McDonald JD: Tumor suppressor genes and medulloblastoma. J Neurooncol 1996, 29(1):103-112. 10.1007/BF00165523
24. Shih DJ, Northcott PA, Remke M, Korshunov A, Ramaswamy V, Kool M, Luu B, Yao Y, Wang X, Dubuc AM, Garzia L, Peacock J, Mack SC, Wu X, Rolider A, Morrissy AS, Cavalli FM, Jones DT, Zitterbart K, Faria CC, Schuller U, Kren L, Kumabe T, Tominaga T, Shin Ra Y, Garami M, Hauser P, Chan JA, Robinson S, Bognar L et al (2014) Cytogenetic prognostication within medulloblastoma subgroups. J Clin Oncol doi:10.1200/JCO.2013.50.9539
25. Castellino RC, De Bortoli M, Lu X, Moon SH, Nguyen TA, Shepard MA, Rao PH, Donehower LA, Kim JY: Medulloblastomas overexpress the p53-inactivating oncogene WIP1/PPM1D. J Neurooncol 2008, 86(3):245-256. doi:10.1007/s11060-007-9470-8 10.1007/s11060-007-9470-8
26. Tabori U, Baskin B, Shago M, Alon N, Taylor MD, Ray PN, Bouffet E, Malkin D, Hawkins C: Universal poor survival in children with medulloblastoma harboring somatic TP53 mutations. J Clin Oncol 2010, 28(8):1345-1350. doi:10.1200/JCO.2009.23.5952 10.1200/JCO.2009.23.5952
27. de Bont JM, Packer RJ, Michiels EM, den Boer ML, Pieters R: Biological background of pediatric medulloblastoma and ependymoma: a review from a translational research perspective. Neuro Oncol 2008, 10(6):1040-1060. doi:10.1215/15228517-2008-059 10.1215/15228517-2008-059
28. Northcott PA, Korshunov A, Witt H, Hielscher T, Eberhart CG, Mack S, Bouffet E, Clifford SC, Hawkins CE, French P, Rutka JT, Pfister S, Taylor MD: Medulloblastoma comprises four distinct molecular variants. J Clin Oncol 2011, 29(11):1408-1414. doi:10.1200/JCO.2009.27.4324 10.1200/JCO.2009.27.4324
29. Taylor MD, Northcott PA, Korshunov A, Remke M, Cho YJ, Clifford SC, Eberhart CG, Parsons DW, Rutkowski S, Gajjar A, Ellison DW, Lichter P, Gilbertson RJ, Pomeroy SL, Kool M, Pfister SM (2011) Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol doi:10.1007/s00401-011-0922-z
30. Pei Y, Moore CE, Wang J, Tewari AK, Eroshkin A, Cho YJ, Witt H, Korshunov A, Read TA, Sun JL, Schmitt EM, Miller CR, Buckley AF, McLendon RE, Westbrook TF, Northcott PA, Taylor MD, Pfister SM, Febbo PG, Wechsler-Reya RJ: An animal model of MYC-driven medulloblastoma. Cancer Cell 2012, 21(2):155-167. doi:10.1016/j.ccr.2011.12.021 10.1016/j.ccr.2011.12.021
31. Kawauchi D, Robinson G, Uziel T, Gibson P, Rehg J, Gao C, Finkelstein D, Qu C, Pounds S, Ellison DW, Gilbertson RJ, Roussel MF: A mouse model of the most aggressive subgroup of human medulloblastoma. Cancer Cell 2012, 21(2):168-180. doi:10.1016/j.ccr.2011.12.023 10.1016/j.ccr.2011.12.023
32. Northcott PA, Shih DJ, Peacock J, Garzia L, Morrissy AS, Zichner T, Stutz AM, Korshunov A, Reimand J, Schumacher SE, Beroukhim R, Ellison DW, Marshall CR, Lionel AC, Mack S, Dubuc A, Yao Y, Ramaswamy V, Luu B, Rolider A, Cavalli FM, Wang X, Remke M, Wu X, Chiu RY, Chu A, Chuah E, Corbett RD, Hoad GR, Jackman SD, et al.: Subgroup-specific structural variation across 1,000 medulloblastoma genomes. Nature 2012, 488(7409):49-56. doi:10.1038/nature11327 10.1038/nature11327
33. Robinson G, Parker M, Kranenburg TA, Lu C, Chen X, Ding L, Phoenix TN, Hedlund E, Wei L, Zhu X, Chalhoub N, Baker SJ, Huether R, Kriwacki R, Curley N, Thiruvenkatam R, Wang J, Wu G, Rusch M, Hong X, Becksfort J, Gupta P, Ma J, Easton J, Vadodaria B, Onar-Thomas A, Lin T, Li S, Pounds S, Paugh S, et al.: Novel mutations target distinct subgroups of medulloblastoma. Nature 2012, 488(7409):43-48. doi:10.1038/nature11213 10.1038/nature11213
34. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, Greulich H, Lawrence MS, Lennon NJ, McKenna A, Meldrim J, Ramos AH, Ross MG, Russ C, Shefler E, Sivachenko A, Sogoloff B, Stojanov P, Tamayo P, Mesirov JP, Amani V, Teider N, Sengupta S, Francois JP, Northcott PA, Taylor MD, et al.: Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012, 488(7409):106-110. doi:10.1038/nature11329 10.1038/nature11329
35. Squire SE, Chan MD, Marcus KJ: Atypical teratoid/rhabdoid tumor: the controversy behind radiation therapy. J Neurooncol 2007, 81(1):97-111. doi:10.1007/s11060-006-9196-z 10.1007/s11060-006-9196-z
36. Grill J, Sainte-Rose C, Jouvet A, Gentet JC, Lejars O, Frappaz D, Doz F, Rialland X, Pichon F, Bertozzi AI, Chastagner P, Couanet D, Habrand JL, Raquin MA, Le Deley MC, Kalifa C: Treatment of medulloblastoma with postoperative chemotherapy alone: an SFOP prospective trial in young children. Lancet Oncol 2005, 6(8):573-580. doi:10.1016/S1470-2045(05)70252-7 10.1016/S1470-2045(05)70252-7
37. Jakacki RI, Feldman H, Jamison C, Boaz JC, Luerssen TG, Timmerman R: A pilot study of preirradiation chemotherapy and 1800cGy craniospinal irradiation in young children with medulloblastoma. Int J Radiat Oncol Biol Phys 2004, 60(2):531-536. doi:10.1016/j.ijrobp.2004.03.027 10.1016/j.ijrobp.2004.03.027
38. (2012) Haplotype-based variant detection from short-read sequencing., [http://arxiv.org/abs/1207.3907]
39. Wang K, Li M, Hakonarson H: ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 2010, 38(16):e164. doi:10.1093/nar/gkq603 10.1093/nar/gkq603
40. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE, Kang HM, Marth GT, McVean GA: An integrated map of genetic variation from 1,092 human genomes. Nature 2012, 491(7422):56-65. doi:10.1038/nature11632 10.1038/nature11632
41. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K: dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 2001, 29(1):308-311. 10.1093/nar/29.1.308
42. Do H, Wong SQ, Li J, Dobrovic A: Reducing sequence artifacts in amplicon-based massively parallel sequencing of formalin-fixed paraffin-embedded DNA by enzymatic depletion of uracil-containing templates. Clin Chem 2013, 59(9):1376-1383. doi:10.1373/clinchem.2012.202390 10.1373/clinchem.2012.202390
43. Robasky K, Lewis NE, Church GM: The role of replicates for error mitigation in next-generation sequencing. Nat Rev Genet 2014, 15(1):56-62. doi:10.1038/nrg3655 10.1038/nrg3655
44. Thorvaldsdottir H, Robinson JT, Mesirov JP: Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013, 14(2):178-192. doi:10.1093/bib/bbs017 10.1093/bib/bbs017
45. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013.
46. Maechler M, Rousseeuw P, Struyf A, Hubert M, Hornik K: cluster: Cluster Analysis Basics and Extensions. Therneau TMG, Patricia M (2013) A Package for Survival Analysis in S. R package version 2.37-4 edn 2013. [ http://CRAN.R-project.org/package=survival ] http://CRAN.R-project.org/package=survival. Version 1.14.4
47. Hemming S, Cakouros D, Isenmann S, Cooper L, Menicanin D, Zannettino A, Gronthos S: EZH2 and KDM6A act as an epigenetic switch to regulate mesenchymal stem cell lineage specification. Stem Cells 2014, 32(3):802-815. doi:10.1002/stem.1573 10.1002/stem.1573
48. Lu X, Nguyen TA, Moon SH, Darlington Y, Sommer M, Donehower LA: The type 2C phosphatase Wip1: an oncogenic regulator of tumor suppressor and DNA damage response pathways. Cancer Metastasis Rev 2008, 27(2):123-135. doi:10.1007/s10555-008-9127-x 10.1007/s10555-008-9127-x
49. Takekawa M, Adachi M, Nakahata A, Nakayama I, Itoh F, Tsukuda H, Taya Y, Imai K: p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. Embo J 2000, 19(23):6517-6526. doi:10.1093/emboj/19.23.6517 10.1093/emboj/19.23.6517
50. Saldana-Meyer R, Recillas-Targa F: Transcriptional and epigenetic regulation of the p53 tumor suppressor gene. Epigenetics 2011, 6(9):1068-1077. doi:10.4161/epi.6.9.16683 10.4161/epi.6.9.16683
51. Riley T, Sontag E, Chen P, Levine A: Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 2008, 9(5):402-412. doi:10.1038/nrm2395 10.1038/nrm2395
52. Courant F, Aksglaede L, Antignac JP, Monteau F, Sorensen K, Andersson AM, Skakkebaek NE, Juul A, Bizec BL: Assessment of circulating sex steroid levels in prepubertal and pubertal boys and girls by a novel ultrasensitive gas chromatography-tandem mass spectrometry method. J Clin Endocrinol Metab 2010, 95(1):82-92. doi:10.1210/jc.2009-1140 10.1210/jc.2009-1140
53. Fernandez-Cuesta L, Anaganti S, Hainaut P, Olivier M: Estrogen levels act as a rheostat on p53 levels and modulate p53-dependent responses in breast cancer cell lines. Breast Cancer Res Treat 2011, 125(1):35-42. doi:10.1007/s10549-010-0819-x 10.1007/s10549-010-0819-x
54. Yamamoto T, Mori T, Sawada M, Kuroboshi H, Tatsumi H, Yoshioka T, Matsushima H, Iwasaku K, Kitawaki J: Estrogen-related receptor-gamma regulates estrogen receptor-alpha responsiveness in uterine endometrial cancer. Int J Gynecol Cancer 2012, 22(9):1509-1516. doi:10.1097/IGC.0b013e31826fd623
55. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, Gallia GL, Jallo GI, Binder ZA, Nikolsky Y, Hartigan J, Smith DR, Gerhard DS, Fults DW, VandenBerg S, Berger MS, Marie SK, Shinjo SM, Clara C, Phillips PC, Minturn JE, Biegel JA, Judkins AR, Resnick AC, Storm PB, Curran T, et al.: The genetic landscape of the childhood cancer medulloblastoma. Science 2011, 331(6016):435-439. doi:10.1126/science.1198056 10.1126/science.1198056
56. Hakimi AA, Chen YB, Wren J, Gonen M, Abdel-Wahab O, Heguy A, Liu H, Takeda S, Tickoo SK, Reuter VE, Voss MH, Motzer RJ, Coleman JA, Cheng EH, Russo P, Hsieh JJ: Clinical and pathologic impact of select chromatin-modulating tumor suppressors in clear cell renal cell carcinoma. Eur Urol 2013, 63(5):848-854. doi:10.1016/j.eururo.2012.09.005 10.1016/j.eururo.2012.09.005