Neuroblastoma genetics and phenotype: A tale of heterogeneity

Seminars in Cancer Biology

Volumn 21, Issue 4, 2011, Pages 238-244

  Speleman, Frank ^a   de Preter, Katleen ^a   Vandesompele, Jo ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

Genetics; Genomics; Neuroblastoma

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; BMI1 PROTEIN; CHECKPOINT KINASE 1; CLUSTERIN; CYCLIN DEPENDENT KINASE INHIBITOR 1C; CYCLIN DEPENDENT KINASE INHIBITOR 2A; LIM KINASE 1; MESSENGER RNA; MICRORNA; MIXED LINEAGE LEUKEMIA PROTEIN; MYC PROTEIN; PROTEIN MDM2; PROTEIN P53; PROTEIN TYROSINE KINASE A; TRANSCRIPTOME;

BACTERIAL ARTIFICIAL CHROMOSOME; CANCER GENETICS; CARCINOGENESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME 17; CHROMOSOME ADDITION; CHROMOSOME REARRANGEMENT; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; CYTOGENETICS; GENE AMPLIFICATION; GENE DELETION; GENE DOSAGE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC PREDISPOSITION; HOMOZYGOSITY; HUMAN; MOLECULAR GENETICS; MOLECULAR INTERACTION; MYCN GENE; NEUROBLASTOMA; NONHUMAN; ONCOGENE; PHENOTYPE; PROGNOSIS; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR GENE; TUMOR SUPPRESSOR GENE;

ANIMALS; HUMANS; NEUROBLASTOMA; PHENOTYPE;

EID: 80655149031     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2011.07.003     Document Type: Review

References (114)

1. Schwab M., Alitalo K., Klempnauer K.H., Varmus H.E., Bishop J.M., Gilbert F., et al. Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour. Nature 1983, 305:245-248.
2. Brodeur G.M. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003, 3:203-216.
3. Brodeur G.M., Green A.A., Hayes F.A., Williams K.J., Williams D.L., Tsiatis A.A. Cytogenetic features of human neuroblastomas and cell lines. Cancer Res 1981, 41:4678-4686.
4. Kaneko Y., Kanda N., Maseki N., Sakurai M., Tsuchida Y., Takeda T., et al. Different karyotypic patterns in early and advanced stage neuroblastomas. Cancer Res 1987, 47:311-318.
5. Look A.T., Hayes F.A., Shuster J.J., Douglass E.C., Castleberry R.P., Bowman L.C., et al. Clinical relevance of tumor cell ploidy and N-myc gene amplification in childhood neuroblastoma: a pediatric oncology group study. J Clin Oncol 1991, 9:581-591.
6. Van Roy N., Laureys G., Cheng N.C., Willem P., Opdenakker G., Versteeg R., et al. 1;17 translocations and other chromosome 17 rearrangements in human primary neuroblastoma tumors and cell lines. Genes Chromosomes Cancer 1994, 10:103-114.
7. Caron H., van Sluis P., van Roy N., de Kraker J., Speleman F., Voûte P.A., et al. Recurrent 1;17 translocations in human neuroblastoma reveal nonhomologous mitotic recombination during the S/G2 phase as a novel mechanism for loss of heterozygosity. Am J Hum Genet 1994, 55:341-347.
8. Vandesompele J., Van Roy N., Van Gele M., Laureys G., Ambros P., Heimann P., et al. Genetic heterogeneity of neuroblastoma studied by comparative genomic hybridization. Genes Chromosomes Cancer 1998, 23:141-152.
9. Bown N., Cotterill S., Lastowska M., O'Neill S., Pearson A., Plantaz D., et al. Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 1999, 340:1954-1961.
10. Plantaz D., Vandesompele J., Van Roy N., Lastowska M., Bown N., Combaret V., et al. Comparative genomic hybridization (CGH) analysis of stage 4 neuroblastoma reveals high frequency of 11q deletion in tumors lacking MYCN amplification. Int J Cancer 2001, 91:680-686.
11. Vandesompele J., Baudis M., De Preter K., Van Roy N., Ambros P., Bown N., et al. Unequivocal delineation of clinicogenetic subgroups and development of a new model for improved outcome prediction in neuroblastoma. J Clin Oncol 2005, 23:2280-2299.
12. Michels E., Vandesompele J., Hoebeeck J., Menten B., De Preter K., Laureys G., et al. Genome wide measurement of DNA copy number changes in neuroblastoma: dissecting amplicons and mapping losses, gains and breakpoints. Cytogenet Genome Res 2006, 115:273-282.
13. Van Roy N., De Preter K., Hoebeeck J., Van Maerken T., Pattyn F., Mestdagh P., et al. The emerging molecular pathogenesis of neuroblastoma: implications for improved risk assessment and targeted therapy. Genome Med 2009, 1:74.
14. Janoueix-Lerosey I., Schleiermacher G., Michels E., Mosseri V., Ribeiro A., Lequin D., et al. Overall genomic pattern is a predictor of outcome in neuroblastoma. J Clin Oncol 2009, 27:1026-1033.
15. Janoueix-Lerosey I., Lequin D., Brugières L., Ribeiro A., de Pontual L., Combaret V., et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008, 455:967-970.
16. Mossé Y.P., Laudenslager M., Longo L., Cole Ka, Wood A., Attiyeh E.F., et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008, 455:930-935.
17. Chen Y., Takita J., Choi Y.L., Kato M., Ohira M., Sanada M., et al. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008, 455:971-974.
18. George R.E., Sanda T., Hanna M., Frohling S., Luther W., Zhang J., et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 2008, 455:975-978.
19. Stallings R.L., Nair P., Maris J.M., Catchpoole D., McDermott M., O'Meara A., et al. High-resolution analysis of chromosomal breakpoints and genomic instability identifies PTPRD as a candidate tumor suppressor gene in neuroblastoma. Cancer Res 2006, 66:3673-3680.
20. Kumps C, Fieuw A, Mestdagh P, Menten B, Lefever S, Pattyn F, et al. Rare recurrent DNA copy number alterations in neuroblastoma target MYCN pathway component genes, in preparation.
21. Stratton M.R. Exploring the genomes of cancer cells: progress and promise. Science 2011, 331:1553-1558.
22. Ali M.A., Sjöblom T. Molecular pathways in tumor progression: from discovery to functional understanding. Mol Biosyst 2009, 5:902-908.
23. Carén H., Kryh H., Nethander M., Sjöberg R-M., Träger C., Nilsson S., et al. High-risk neuroblastoma tumors with 11q-deletion display a poor prognostic, chromosome instability phenotype with later onset. Proc Natl Acad Sci USA 2010, 107:4323-4328.
24. Fieuw A, Kumps C, Schramm A, Pattyn F, Menten B, Antonacci F, et al. Identification of a novel recurrent 1q42.2-1qter deletion in high risk MYCN single copy 11q deleted neuroblastomas. Int J Cancer, in press. doi:10.1002/ijc.26317.
25. Johansson P., Wei J., Chen Q., Bowden N., Badgett T., Song Y., et al. A genomic portrait of tumor progression using next-generation sequencing. Orlando, Florida, Philadelphia, PA, April 2-6 2011.
26. Morozova O., Birol I., Corbett R., Mungall K., Attiyeh E.F., Asgharzadeh S., et al. Proceedings of the 102nd Annual Meeting of the American Association for Cancer Research. Whole genome and transcriptome sequencing defines the spectrum of somatic changes in high-risk neuroblastoma 2011.
27. Pugh T.J., Lawrence M., Sougnez C., Getz G., Attiyeh E., Hogarty M., et al. Exome sequencing of 81 neuroblastomas identifies a wide diversity of somatic mutation. Orlando, Florida, Philadelphia (PA), April 2-6 2011.
28. Bell E., Chen L., Liu T., Marshall G.M., Lunec J., Tweddle D.A. MYCN oncoprotein targets and their therapeutic potential. Cancer Lett 2010, 293:144-157.
29. Hogarty M.D., Norris M.D., Davis K., Liu X., Evageliou N.F., Hayes C.S., et al. ODC1 is a critical determinant of MYCN oncogenesis and a therapeutic target in neuroblastoma. Cancer Res 2008, 68:9735-9745.
30. Tsai H.-Y., Hsi B.-L., Hung I.-J., Yang C.-P., Lin J.-N., Chen J.-C., et al. Correlation of MYCN amplification with MCM7 protein expression in neuroblastomas: a chromogenic in situ hybridization study in paraffin sections. Hum Pathol 2004, 35:1397-1403.
31. Krams M., Hero B., Berthold F., Parwaresch R., Harms D., Rudolph P. Full-length telomerase reverse transcriptase messenger RNA is an independent prognostic factor in neuroblastoma. Am J Pathol 2003, 162:1019-1026.
32. Iraci N., Diolaiti D., Papa A., Porro A., Valli E., Gherardi S., et al. A SP1/MIZ1/MYCN repression complex recruits HDAC1 at the TRKA and p75NTR promoters and affects neuroblastoma malignancy by inhibiting the cell response to NGF. Cancer Res 2011, 71:404-412.
33. Westermann F., Muth D., Benner A., Bauer T., Henrich K.-O., Oberthuer A., et al. Distinct transcriptional MYCN/c-MYC activities are associated with spontaneous regression or malignant progression in neuroblastomas. Genome Biol 2008, 9:R150.
34. Mestdagh P., Fredlund E., Pattyn F., Schulte J.H., Muth D., Vermeulen J., et al. MYCN/c-MYC-induced microRNAs repress coding gene networks associated with poor outcome in MYCN/c-MYC-activated tumors. Oncogene 2010, 29:1394-1404.
35. Mestdagh P., Boström A-K., Impens F., Fredlund E., Van Peer G., De Antonellis P., et al. The miR-17-92 microRNA cluster regulates multiple components of the TGF-B pathway in neuroblastoma. Mol Cell 2010, 40:762-773.
36. Schulte J.H., Horn S., Otto T., Samans B., Heukamp L.C., Eilers U.C., et al. MYCN regulates oncogenic microRNAs in neuroblastoma. Int J Cancer 2008, 122:699-704.
37. De Brouwer S., De Preter K., Kumps C., Zabrocki P., Porcu M., Westerhout E.M., et al. Meta-analysis of neuroblastomas reveals a skewed ALK mutation spectrum in tumors with MYCN amplification. Clin Cancer Res 2010, 16:4353-4362.
38. Vandesompele J., Michels E., De Preter K., Menten B., Schramm A., Eggert A., et al. Identification of 2 putative critical segments of 17q gain in neuroblastoma through integrative genomics. Int J Cancer 2008, 122:1177-1182.
39. Islam A., Kageyama H., Takada N., Kawamoto T., Takayasu H., Isogai E., et al. High expression of survivin, mapped to 17q25, is significantly associated with poor prognostic factors and promotes cell survival in human neuroblastoma. Oncogene 2000, 19:617-623.
40. Saito-Ohara F., Imoto I., Inoue J., Hosoi H., Nakagawara A., Sugimoto T., et al. PPM1D is a potential target for 17q gain in neuroblastoma. Cancer Res 2003, 63:1876-1883.
41. Hailat N., Keim D.R., Melhem R.F., Zhu X.X., Eckerskorn C., Brodeur G.M., et al. High levels of p19/nm23 protein in neuroblastoma are associated with advanced stage disease and with N-myc gene amplification. J Clin Invest 1991, 88:341-345.
42. Chen Q.R., Bilke S., Wei J.S., Greer B.T., Steinberg S.M., Westermann F., et al. Increased WSB1 copy number correlates with its over-expression which associates with increased survival in neuroblastoma. Genes Chromosomes Cancer 2006, 45:856-862.
43. De Preter K., Vandesompele J., Heimann P., Yigit N., Beckman S., Schramm A., et al. Human fetal neuroblast and neuroblastoma transcriptome analysis confirms neuroblast origin and highlights neuroblastoma candidate genes. Genome Biol 2006, 7:R84.
44. Carr-Wilkinson J., O'Toole K., Wood K.M., Challen C.C., Baker A.G., Board J.R., et al. High frequency of p53/MDM2/p14ARF pathway abnormalities in relapsed neuroblastoma. Clin Cancer Res 2010, 16:1108-1118.
45. Chen L., Iraci N., Gherardi S., Gamble L.D., Wood K.M., Perini G., et al. p53 is a direct transcriptional target of MYCN in neuroblastoma. Cancer Res 2010, 70:1377-1388.
46. Tweddle D.A., Pearson A.D.J., Haber M., Norris M.D., Xue C., Flemming C., et al. The p53 pathway and its inactivation in neuroblastoma. Cancer Lett 2003, 197:93-98.
47. Van Maerken T., Vandesompele J., Rihani A., De Paepe A., Speleman F. Escape from p53-mediated tumor surveillance in neuroblastoma: switching off the p14(ARF)-MDM2-p53 axis. Cell Death Differ 2009, 16:1563-1572.
48. Van Maerken T., Ferdinande L., Taildeman J., Lambertz I., Yigit N., Vercruysse L., et al. Antitumor activity of the selective MDM2 antagonist nutlin-3 against chemoresistant neuroblastoma with wild-type p53. J Natl Cancer Inst 2009, 101:1562-1574.
49. Van Maerken T., Speleman F., Vermeulen J., Lambertz I., De Clercq S., De Smet E., et al. Small-molecule MDM2 antagonists as a new therapy concept for neuroblastoma. Cancer Res 2006, 66:9646-9655.
50. Kim E., Shohet J. Targeted molecular therapy for neuroblastoma: the ARF/MDM2/p53 axis. J Natl Cancer Inst 2009, 101:1527-1529.
51. Fujita T., Igarashi J., Okawa E.R., Gotoh T., Manne J., Kolla V., et al. CHD5, a tumor suppressor gene deleted from 1p36.31 in neuroblastomas. J Natl Cancer Inst 2008, 100:940-949.
52. Thompson P.M., Gotoh T., Kok M., White P.S., Brodeur G.M. CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system. Oncogene 2003, 22:1002-1011.
53. Munirajan A.K., Ando K., Mukai A., Takahashi M., Suenaga Y., Ohira M., et al. KIF1Bbeta functions as a haploinsufficient tumor suppressor gene mapped to chromosome 1p36.2 by inducing apoptotic cell death. J Biol Chem 2008, 283:24426-24434.
54. Ochiai H., Takenobu H., Nakagawa A., Yamaguchi Y., Kimura M., Ohira M., et al. Bmi1 is a MYCN target gene that regulates tumorigenesis through repression of KIF1Bbeta and TSLC1 in neuroblastoma. Oncogene 2010, 29:2681-2690.
55. Henrich K-O., Fischer M., Mertens D., Benner A., Wiedemeyer R., Brors B., et al. Reduced expression of CAMTA1 correlates with adverse outcome in neuroblastoma patients. Clin Cancer Res 2006, 12:131-138.
56. Henrich K-O., Bauer T., Schulte J.H., Ehemann V., Deubzer H.E., Gogolin S., et al. CAMTA1, a 1p36 tumor suppressor candidate, inhibits growth and activates differentiation programmes in neuroblastoma cells. Cancer Res 2011, 71:3142-3151.
57. Meister G. Argonaute function in glioblastoma. Banff, Alberta, Canada, February 11-16 2011.
58. De Brouwer S, Mestdagh P, Lambertz I, Pattyn F, De Paepe A, Westermann F, et al. Dickkopf-3 is regulated by the MYCN-induced miR-17-92 cluster in neuroblastoma. Int J Cancer, in press. doi:10.1002/ijc.26295.
59. Vandepoele K., Staes K., Andries V., van Roy F. Chibby interacts with NBPF1 and clusterin, two candidate tumor suppressors linked to neuroblastoma. Exp Cell Res 2010, 316:1225-1233.
60. Diskin S.J., Hou C., Glessner J.T., Attiyeh E.F., Laudenslager M., Bosse K., et al. Copy number variation at 1q21.1 associated with neuroblastoma. Nature 2009, 459:987-991.
61. Chayka O., Corvetta D., Dews M., Caccamo A.E., Piotrowska I., Santilli G., et al. Clusterin, a haploinsufficient tumor suppressor gene in neuroblastomas. J Natl Cancer Inst 2009, 101:663-677.
62. Michels E., Hoebeeck J., De Preter K., Schramm A., Brichard B., De Paepe A., et al. CADM1 is a strong neuroblastoma candidate gene that maps within a 3.72 Mb critical region of loss on 11q23. BMC Cancer 2008, 8:173.
63. Nowacki S., Skowron M., Oberthuer A., Fagin A., Voth H., Brors B., et al. Expression of the tumour suppressor gene CADM1 is associated with favourable outcome and inhibits cell survival in neuroblastoma. Oncogene 2008, 27:3329-3338.
64. Masuda M., Yageta M., Fukuhara H., Kuramochi M., Maruyama T., Nomoto A., et al. The tumor suppressor protein TSLC1 is involved in cell-cell adhesion. J Biol Chem 2002, 277:31014-31019.
65. Yageta M., Kuramochi M., Masuda M., Fukami T., Fukuhara H., Maruyama T., et al. Direct association of TSLC1 and DAL-1, two distinct tumor suppressor proteins in lung cancer. Cancer Res 2002, 62:5129-5133.
66. Berger M.F., Lawrence M.S., Demichelis F., Drier Y., Cibulskis K., Sivachenko A.Y., et al. The genomic complexity of primary human prostate cancer. Nature 2011, 470:214-220.
67. Parsons D.W., Li M., Zhang X., Jones S., Leary R.J., Lin JC-H., et al. The genetic landscape of the childhood cancer medulloblastoma. Science 2011, 331:435-439.
68. Lam M.H., Liu Q., Elledge S.J., Rosen J.M. Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 2004, 6:45-59.
69. Cole K.A., Huggins J., Laquaglia M., Hulderman C.E., Russell M.R., Bosse K., et al. RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc Natl Acad Sci USA 2011, 108:3336-3341.
70. Alaminos M., Davalos V., Cheung N-KV, Gerald W.L., Esteller M. Clustering of gene hypermethylation associated with clinical risk groups in neuroblastoma. J Natl Cancer Inst 2004, 96:1208-1219.
71. Michalowski M.B., de Fraipont F., Plantaz D., Michelland S., Combaret V., Favrot M-C. Methylation of tumor-suppressor genes in neuroblastoma: The RASSF1A gene is almost always methylated in primary tumors. Pediatr Blood Cancer 2008, 50:29-32.
72. Lázcoz P., Muñoz J., Nistal M., Pestaña A., Encío I., Castresana J.S. Frequent promoter hypermethylation of RASSF1A and CASP8 in neuroblastoma. BMC Cancer 2006, 6:254.
73. Gonzalez-Gomez P., Bello M.J., Lomas J., Arjona D., Alonso M.E., Amiñoso C., et al. Aberrant methylation of multiple genes in neuroblastic tumours. relationship with MYCN amplification and allelic status at 1p. Eur J Cancer 2003, 39:1478-1485.
74. Yang Q., Kiernan C.M., Tian Y., Salwen H.R., Chlenski A., Brumback B.A., et al. Methylation of CASP8, DCR2, and HIN-1 in neuroblastoma is associated with poor outcome. Clin Cancer Res 2007, 13:3191-3197.
75. Hoebeeck J., Michels E., Pattyn F., Combaret V., Vermeulen J., Yigit N., et al. Aberrant methylation of candidate tumor suppressor genes in neuroblastoma. Cancer Lett 2009, 273:336-346.
76. Yagyu S., Gotoh T., Iehara T., Miyachi M., Katsumi Y., Tsubai-Shimizu S., et al. Circulating methylated-DCR2 gene in serum as an indicator of prognosis and therapeutic efficacy in patients with MYCN nonamplified neuroblastoma. Clin Cancer Res 2008, 14:7011-7019.
77. Grau E., Martinez F., Orellana C., Canete A., Yañez Y., Oltra S., et al. Hypermethylation of apoptotic genes as independent prognostic factor in neuroblastoma disease. Mol Carcinog 2010, 50:153-162.
78. Banelli B., Bonassi S., Casciano I., Mazzocco K., Di Vinci A., Scaruffi P., et al. Outcome prediction and risk assessment by quantitative pyrosequencing methylation analysis of the SFN gene in advanced stage, high-risk, neuroblastic tumor patients. Int J Cancer 2010, 126:656-668.
79. Banelli B., Gelvi I., Di Vinci A., Scaruffi P., Casciano I., Allemanni G., et al. Distinct CpG methylation profiles characterize different clinical groups of neuroblastic tumors. Oncogene 2005, 24:5619-5628.
80. Abe M., Ohira M., Kaneda A., Yagi Y., Yamamoto S., Kitano Y., et al. CpG island methylator phenotype is a strong determinant of poor prognosis in neuroblastomas. Cancer Res 2005, 65:828-834.
81. Caren H., Djos A., Nethander M., Sjoberg R-M., Kogner P., Enstrom C., et al. Identification of epigenetically regulated genes that predict patient outcome in neuroblastoma. BMC Cancer 2011, 11:66.
82. Misawa A., Tanaka S., Yagyu S., Tsuchiya K., Iehara T., Sugimoto T., et al. RASSF1A hypermethylation in pretreatment serum DNA of neuroblastoma patients: a prognostic marker. Br J Cancer 2009, 100:399-404.
83. Bourdeaut F., Trochet D., Janoueix-Lerosey I., Ribeiro A., Deville A., Coz C., et al. Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma. Cancer Lett 2005, 228:51-58.
84. Perri P., Bachetti T., Longo L., Matera I., Seri M., Tonini G.P., et al. PHOX2B mutations and genetic predisposition to neuroblastoma. Oncogene 2005, 24:3050-3053.
85. Alam G., Cui H., Shi H., Yang L., Ding J., Mao L., et al. MYCN promotes the expansion of Phox2B-positive neuronal progenitors to drive neuroblastoma development. Am J Pathol 2009, 175:856-866.
86. Capasso M., Devoto M., Hou C., Asgharzadeh S., Glessner J.T., Attiyeh E.F., et al. Common variations in BARD1 influence susceptibility to high-risk neuroblastoma. Nat Genet 2009, 41:718-723.
87. Wang K., Diskin S.J., Zhang H., Attiyeh E.F., Winter C., Hou C., et al. Integrative genomics identifies LMO1 as a neuroblastoma oncogene. Nature 2011, 469:216-220.
88. Nguyen L.B., Diskin S.J., Capasso M., Wang K., Diamond M.A., Glessner J., et al. Phenotype restricted genome-wide association study using a gene-centric approach identifies three low-risk neuroblastoma susceptibility loci. PLoS Genet 2011, 7:e1002026.
89. Deyell R.J., Attiyeh E.F. Advances in the understanding of constitutional and somatic genomic alterations in neuroblastoma. Cancer Genetics 2011, 204:113-121.
90. Buckley P.G., Alcock L., Bryan K., Bray I., Schulte J.H., Schramm A., et al. Chromosomal and microRNA expression patterns reveal biologically distinct subgroups of 11q- neuroblastoma. Clin Cancer Res 2010, 16:2971-2978.
91. Berwanger B., Hartmann O., Bergmann E., Bernard S., Nielsen D., Krause M., et al. Loss of a FYN-regulated differentiation and growth arrest pathway in advanced stage neuroblastoma. Cancer Cell 2002, 2:377-386.
92. Schulte J.H., Schowe B., Mestdagh P., Kaderali L., Kalaghatgi P., Schlierf S., et al. Accurate prediction of neuroblastoma outcome based on miRNA expression profiles. Int J Cancer 2010, 127:2374-2385.
93. Oberthuer A., Hero B., Berthold F., Juraeva D., Faldum A., Kahlert Y., et al. Prognostic impact of gene expression-based classification for neuroblastoma. J Clin Oncol 2010, 28:3506-3515.
94. Oberthuer A., Berthold F., Warnat P., Hero B., Kahlert Y., Spitz R., et al. Customized oligonucleotide microarray gene expression-based classification of neuroblastoma patients outperforms current clinical risk stratification. J Clin Oncol 2006, 24:5070-5078.
95. Ohira M., Oba S., Nakamura Y., Isogai E., Kaneko S., Nakagawa A., et al. Expression profiling using a tumor-specific cDNA microarray predicts the prognosis of intermediate risk neuroblastomas. Cancer Cell 2005, 7:337-350.
96. Wei J.S., Greer B.T., Westermann F., Steinberg S.M., Son C.G., Chen Q.R., et al. Prediction of clinical outcome using gene expression profiling and artificial neural networks for patients with neuroblastoma. Cancer Res 2004, 64:6883-6891.
97. Asgharzadeh S., Pique-Regi R., Sposto R., Wang H., Yang Y., Shimada H., et al. Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J Natl Cancer Inst 2006, 98:1193-1203.
98. Chen Q.R., Song Y.K., Wei J.S., Bilke S., Asgharzadeh S., Seeger R.C., et al. An integrated cross-platform prognosis study on neuroblastoma patients. Genomics 2008, 92:195-203.
99. Fan C., Oh D.S., Wessels L., Weigelt B., Nuyten DSa, Nobel A.B., et al. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med 2006, 355:560-569.
100. De Preter K., De Brouwer S., Van Maerken T., Pattyn F., Schramm A., Eggert A., et al. Meta-mining of neuroblastoma and neuroblast gene expression profiles reveals candidate therapeutic compounds. Clin Cancer Res 2009, 15:3690-3696.
101. Vermeulen J., De Preter K., Naranjo A., Vercruysse L., Van Roy N., Hellemans J., et al. Predicting outcomes for children with neuroblastoma using a multigene-expression signature: a retrospective SIOPEN/COG/GPOH study. Lancet Oncol 2009, 10:663-671.
102. Mestdagh P, Lefever S, Pattyn F, Ridzon D, Fredlund E, Fieuw A, et al. The microRNA body map: dissecting microRNA function through integrative genomics. Nucleic Acids Res, in press. doi:10.1093/nar/gkr646.
103. Bray I., Bryan K., Prenter S., Buckley P.G., Foley N.H., Murphy D.M., et al. Widespread dysregulation of MiRNAs by MYCN amplification and chromosomal imbalances in neuroblastoma: association of miRNA expression with survival. PLoS One 2009, 4:e7850.
104. Cohn S.L., Pearson A.D.J., London W.B., Monclair T., Ambros P.F., Brodeur G.M., et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 2009, 27:289-297.
105. Vandewoestyne M., Kumps C., Swerts K., Menten B., Lammens T., Philippe J., et al. Isolation of disseminated neuroblastoma cells from bone marrow aspirates for pre-treatment risk assessment by array comparative genomic hybridization. Int J Cancer 2011.
106. De Preter K., Vandesompele J., Heimann P., Kockx M.M., Van Gele M., Hoebeeck J., et al. Application of laser capture microdissection in genetic analysis of neuroblastoma and neuroblastoma precursor cells. Cancer Lett 2003, 197:53-61.
107. Nair P., De Preter K., Vandesompele J., Speleman F., Stallings R.L. Aberrant splicing of the PTPRD gene mimics microdeletions identified at this locus in neuroblastomas. Genes Chromosomes Cancer 2008, 47:197-202.
108. Pattyn F, De Preter K, Van Maerken T, Vermeulen J, Hoebeeck J, Mestdagh P, et al. Discovering hidden significance in neuroblastoma gene expression studies using the neuroblastoma gene server, submitted for publication.
109. Lee Y., Miller H.L., Jensen P., Hernan R., Connelly M., Wetmore C., et al. A molecular fingerprint for medulloblastoma. Cancer Res 2009, 542:8-37.
110. Maurer J., Fuchs S., Jager R., Kurz B., Sommer L., Schorle H. Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation 2007, 75:580-591.
111. Schulte J, Bohrer A, Lindner S, Mauer J, De Preter K, Lefever S, et al. Neuroblastoma develops from neural crest stem cells, submitted for publication.
112. Balamuth N.J., Wood A., Wang Q., Jagannathan J., Mayes P., Zhang Z., et al. Serial transcriptome analysis and cross-species integration identifies centromere-associated protein E as a novel neuroblastoma target. Cancer Res 2010, 70:2749-2758.
113. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010, 11:597-610.
114. Mavrakis KJ, Van der Meulen J, Wolfe AL, Mets E, Taghon T, Khan AA, et al. A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL). Nat Genetics [2nd revision].