Recent insights into the biology of neuroblastoma

International Journal of Cancer

Volumn 135, Issue 10, 2014, Pages 2249-2261

  Schleiermacher, Gudrun ^a,b   Janoueix Lerosey, Isabelle ^b   Delattre, Olivier ^b  

^a Arvalis Institut du Vegetal   (France)

^b INSTITUT CURIE   (France)

Author keywords

Animal models; Expression signatures; Genetic alterations; Neuroblastoma; Progression; Susceptibility

Indexed keywords

ANTINEOPLASTIC AGENT; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; CRIZOTINIB; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MICRORNA; PROTEIN TYROSINE PHOSPHATASE SHP 2; TORIN2; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ALLELE; AUTOLOGOUS STEM CELL TRANSPLANTATION; CANCER CLASSIFICATION; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CARCINOGENESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME 11P; CHROMOSOME 11Q; CHROMOSOME 17P; CHROMOSOME 2P; CHROMOSOME 6P; CHROMOSOME LOSS; CHROMOTHRIPSIS; CONGENITAL CENTRAL HYPOVENTILATION SYNDROME; COPY NUMBER VARIATION; CYTOTOXICITY; DISEASE ASSOCIATION; DNA METHYLATION; DRUG SENSITIVITY; EVENT FREE SURVIVAL; GENE AMPLIFICATION; GENE DOSAGE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCUS; GENE REARRANGEMENT; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; GENETIC PREDISPOSITION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HEREDITY; HETEROZYGOSITY; HIGH RISK PATIENT; HOMOZYGOSITY; HUMAN; LOW RISK PATIENT; MACROPHAGE; MALIGNANT TRANSFORMATION; MURINAE; NEUROBLASTOMA; NEUROFIBROMATOSIS; NONHUMAN; ONCOGENE; ONCOGENE ALK; ONCOGENE ARID1A; ONCOGENE ATRX; ONCOGENE BARD1; ONCOGENE BARD1 BETA; ONCOGENE CD16; ONCOGENE CD33; ONCOGENE CDK4; ONCOGENE CDKN2A; ONCOGENE CHD5; ONCOGENE CREBBP; ONCOGENE CSMD1; ONCOGENE DB1; ONCOGENE DDX1; ONCOGENE DUSP12; ONCOGENE EP300; ONCOGENE FCGR3; ONCOGENE FLJ22536; ONCOGENE FLJ44180; ONCOGENE HACE1; ONCOGENE HSD17B12; ONCOGENE IKZF1; ONCOGENE IL10; ONCOGENE IL6R; ONCOGENE LET 7; ONCOGENE LIN28B; ONCOGENE LMO1; ONCOGENE MDM2; ONCOGENE MEIS1; ONCOGENE MLH1; ONCOGENE MYCN; ONCOGENE N RAS; ONCOGENE NAG; ONCOGENE NBPF23; ONCOGENE NME1; ONCOGENE ODZ3; ONCOGENE PAFAH1B1; ONCOGENE PHOX2B; ONCOGENE PTPN11; ONCOGENE PTPRD; ONCOGENE TIAM1; ONCOGENE TTF2; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRACTICE GUIDELINE; PROGRESSION FREE SURVIVAL; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; ZEBRA FISH; ANIMAL MODELS; EXPRESSION SIGNATURES; GENETIC ALTERATIONS; GENETICS; PATHOLOGY; PROGRESSION; SUSCEPTIBILITY;

ANIMAL MODELS; EXPRESSION SIGNATURES; GENETIC ALTERATIONS; NEUROBLASTOMA; PROGRESSION; SUSCEPTIBILITY;

HUMANS; NEUROBLASTOMA;

EID: 84909957043     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29077     Document Type: Review

References (92)

1. Maris JM, Hogarty MD, Bagatell R, et al. Neuroblastoma. Lancet 2007;369:2106-20.
2. La situation du cancer en France en 2011. INCa Report. 2011;36-7.
3. Cohn SL, Pearson AD, London WB, et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 2009;27:289-97.
4. London WB, Castleberry RP, Matthay KK, et al. Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children's Oncology Group. J Clin Oncol 2005;23:6459-65.
5. Brems H, Beert E, de Ravel T, et al. Mechanisms in the pathogenesis of malignant tumours in neurofibromatosis type 1. Lancet Oncol 2009;10:508-15.
6. Shojaei-Brosseau T, Chompret A, Abel A, et al. Genetic epidemiology of neuroblastoma: a study of 426 cases at the Institut Gustave-Roussy in France. Pediatr Blood Cancer 2004;42:99-105.
7. Trochet D, Bourdeaut F, Janoueix-Lerosey I, et al. Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma. Am J Hum Genet 2004;74:761-4.
8. Trochet D, O'Brien LM, Gozal D, et al. PHOX2B genotype allows for prediction of tumor risk in congenital central hypoventilation syndrome. Am J Hum Genet 2005;76:421-6.
9. Janoueix-Lerosey I, Lequin D, Brugieres L, et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008;455:967-70.
10. Mosse YP, Laudenslager M, Longo L, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008;455:930-5.
11. Bourdeaut F, Ferrand S, Brugieres L, et al. ALK germline mutations in patients with neuroblastoma: a rare and weakly penetrant syndrome. Eur J Hum Genet 2012;20:291-7.
12. Devoto M, Specchia C, Laudenslager M, et al. Genome-wide linkage analysis to identify genetic modifiers of ALK mutation penetrance in familial neuroblastoma. Hum Hered 2011;71:135-9.
13. De Pontual L, Kettaneh D, Gordon CT, et al. Germline gain-of-function mutations of ALK disrupt central nervous system development. Hum Mutat 2011;32:272-6.
14. Diskin SJ, Hou C, Glessner JT, et al. Copy number variation at 1q21.1 associated with neuroblastoma. Nature 2009;459:987-91.
15. Nguyen le B, Diskin SJ, Capasso M, 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.
16. Capasso M, Devoto M, Hou C, et al. Common variations in BARD1 influence susceptibility to high-risk neuroblastoma. Nat Genet 2009;41:718-23.
17. Maris JM, Mosse YP, Bradfield JP, et al. Chromosome 6p22 locus associated with clinically aggressive neuroblastoma. N Engl J Med 2008;358:2585-93.
18. Diskin SJ, Capasso M, Schnepp RW, et al. Common variation at 6q16 within HACE1 and LIN28B influences susceptibility to neuroblastoma. Nat Genet 2012;44:1126-30.
19. Wang K, Diskin SJ, Zhang H, et al. Integrative genomics identifies LMO1 as a neuroblastoma oncogene. Nature 2011;469:216-20.
20. Vandepoele K, Andries V, Van Roy N, et al. A constitutional translocation t(1;17)(p36.2;q11.2) in a neuroblastoma patient disrupts the human NBPF1 and ACCN1 genes. PLoS One 2008;3:e2207.
21. Bosse KR, Diskin SJ, Cole KA, et al. Common variation at BARD1 results in the expression of an oncogenic isoform that influences neuroblastoma susceptibility and oncogenicity. Cancer Res 2012;72:2068-78.
22. Molenaar JJ, Domingo-Fernández R, Ebus ME, et al. LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat Genet 2012;44:1199-206.
23. Cheung N-KV, Dyer MA. Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer 2013;13:397-411.
24. Brodeur GM, Seeger RC, Schwab M, et al. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 1984;224:1121-4.
25. Guimier A, Ferrand S, Pierron G, et al. Clinical characteristics and outcome of patients with neuroblastoma presenting genomic amplification of loci other than MYCN. PLoS One, 2014;9:e101990.
26. Fix A, Lucchesi C, Ribeiro A, et al. Characterization of amplicons in neuroblastoma: high-resolution mapping using DNA microarrays, relationship with outcome, and identification of overexpressed genes. Genes Chromosomes Cancer 2008;47:819-34.
27. Caren H, Erichsen J, Olsson L, et al. High-resolution array copy number analyses for detection of deletion, gain, amplification and copy-neutral LOH in primary neuroblastoma tumors: four cases of homozygous deletions of the CDKN2A gene. BMC Genomics 2008;9:353.
28. Caron H, van Sluis P, van Roy N, 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;55:341-7.
29. Schleiermacher G, Janoueix-Lerosey I, Combaret V, et al. Combined 24-color karyotyping and comparative genomic hybridization analysis indicates predominant rearrangements of early replicating chromosome regions in neuroblastoma. Cancer Genet Cytogenet 2003;141:32-42.
30. Bown N, Cotterill S, Lastowska M, et al. Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 1999;340:1954-61.
31. Attiyeh EF, London WB, Mosse YP, et al. Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med 2005;353:2243-53.
32. Schleiermacher G, Janoueix-Lerosey I, Ribeiro A, et al. Accumulation of segmental alterations determines progression in neuroblastoma. J Clin Oncol 2010;28:3122-30.
33. Coco S, Theissen J, Scaruffi P, et al. Age-dependent accumulation of genomic aberrations and deregulation of cell cycle and telomerase genes in metastatic neuroblastoma. Int J Cancer 2012;131:1591-600.
34. Caren H, Kryh H, Nethander M, 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;107:4323-8.
35. Janoueix-Lerosey I, Schleiermacher G, Michels E, et al. Overall genomic pattern is a predictor of outcome in neuroblastoma. J Clin Oncol 2009;27:1026-33.
36. Kumps C, Fieuw A, Mestdagh P, et al. Focal DNA copy number changes in neuroblastoma target MYCN regulated genes. PLoS One 2013;8:e52321.
37. Cobrinik D, Ostrovnaya I, Hassimi M, et al. Recurrent pre-existing and acquired DNA copy number alterations, including focal TERT gains, in neuroblastoma central nervous system metastases. Genes Chromosomes Cancer 2013;52:1150-66.
38. Stallings RL, Nair P, Maris JM, et al. High-resolution analysis of chromosomal breakpoints and genomic instability identifies PTPRD as a candidate tumor suppressor gene in neuroblastoma. Cancer Res 2006;66:3673-80.
39. Janoueix-Lerosey I, Novikov E, Monteiro M, et al. Gene expression profiling of 1p35-36 genes in neuroblastoma. Oncogene 2004;23:5912-22.
40. Stigliani S, Coco S, Moretti S, et al. High genomic instability predicts survival in metastatic high-risk neuroblastoma. Neoplasia 2012;14:823-32.
41. Kryh H, Carén H, Erichsen J, et al. Comprehensive SNP array study of frequently used neuroblastoma cell lines; copy neutral loss of heterozygosity is common in the cell lines but uncommon in primary tumors. BMC Genomics 2011;12:443.
42. Lastowska M, Cullinane C, Variend S, et al. Comprehensive genetic and histopathologic study reveals three types of neuroblastoma tumors. J Clin Oncol 2001;19:3080-90.
43. Vandesompele J, Baudis M, De Preter K, et al. Unequivocal delineation of clinicogenetic subgroups and development of a new model for improved outcome prediction in neuroblastoma. J Clin Oncol 2005;23:2280-99.
44. Schleiermacher G, Michon J, Ribeiro A, et al. Segmental chromosomal alterations lead to a higher risk of relapse in infants with MYCN-non-amplified localised unresectable/disseminated neuroblastoma (a SIOPEN collaborative study). Br J Cancer 2011;105:1940-8.
45. Tomioka N, Oba S, Ohira M, et al. Novel risk stratification of patients with neuroblastoma by genomic signature, which is independent of molecular signature. Oncogene 2008;27:441-9.
46. Chen Y, Takita J, Choi YL, et al. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008;455:971-4.
47. George RE, Sanda T, Hanna M, et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 2008;455:975-8.
48. De Brouwer S, De Preter K, Kumps C, et al. Meta-analysis of neuroblastomas reveals a skewed ALK mutation spectrum in tumors with MYCN amplification. Clin Cancer Res 2010;16:4353-62.
49. Molenaar JJ, Koster J, Zwijnenburg DA, et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012;483:589-93.
50. Sausen M, Leary RJ, Jones S, et al. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat Genet 2013;45:12-7.
51. Cheung N-KV, Zhang J, Lu C, et al. Association of age at diagnosis and genetic mutations in patients with neuroblastoma. J Am Med Assoc 2012;307:1062-71.
52. Pugh TJ, Morozova O, Attiyeh EF, et al. The genetic landscape of high-risk neuroblastoma. Nat Genet 2013;45:279-84.
53. Boeva V, Jouannet S, Daveau R, et al. Breakpoint features of genomic rearrangements in neuroblastoma with unbalanced translocations and chromothripsis. PLoS One 2013;8:e72182.
54. Stephens PJ, Greenman CD, Fu B, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 2011;144:27-40.
55. Ciriello G, Miller ML, Aksoy BA, et al. Emerging landscape of oncogenic signatures across human cancers. Nat Genet 2013;45:1127-33.
56. Oberthuer A, Hero B, Berthold F, et al. Prognostic impact of gene expression-based classification for neuroblastoma. J Clin Oncol 2010;28:3506-15.
57. Vermeulen J, De Preter K, Naranjo A, et al. Predicting outcomes for children with neuroblastoma using a multigene-expression signature: a retrospective SIOPEN/COG/GPOH study. Lancet Oncol 2009;10:663-71.
58. Garcia I, Mayol G, Ríos J, et al. A three-gene expression signature model for risk stratification of patients with neuroblastoma. Clin Cancer Res 2012;18:2012-23.
59. Asgharzadeh S, Pique-Regi R, Sposto R, et al. Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J Natl Cancer Inst 2006;98:1193-203.
60. Fardin P, Barla A, Mosci S, et al. A biologydriven approach identifies the hypoxia gene signature as a predictor of the outcome of neuroblastoma patients. Mol Cancer 2010;9:185.
61. Asgharzadeh S, Salo JA, Ji L, et al. Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol 2012;30:3525-32.
62. Valentijn LJ, Koster J, Haneveld F, et al. Functional MYCN signature predicts outcome of neuroblastoma irrespective of MYCN amplification. Proc Natl Acad Sci USA 2012;109:19190-5.
63. Mestdagh P, Fredlund E, Pattyn F, et al. An integrative genomics screen uncovers ncRNA T-UCR functions in neuroblastoma tumours. Oncogene 2010;29:3583-92.
64. Schulte JH, Schowe B, Mestdagh P, et al. Accurate prediction of neuroblastoma outcome based on miRNA expression profiles. Int J Cancer 2010;127:2374-85.
65. De Preter K, Mestdagh P, Vermeulen J, et al. miRNA expression profiling enables risk stratification in archived and fresh neuroblastoma tumor samples. Clin Cancer Res 2011;17:7684-92.
66. Decock A, Ongenaert M, Hoebeeck J, et al. Genome-wide promoter methylation analysis in neuroblastoma identifies prognostic methylation biomarkers. Genome Biol 2012;13:R95.
67. Barone G, Anderson J, Pearson ADJ, et al. New strategies in neuroblastoma: therapeutic targeting of MYCN and ALK. Clin Cancer Res 2013;19:5814-21.
68. Mossé YP, Lim MS, Voss SD, et al. Safety and activity of crizotinib for paediatric patients with refractory solid tumours or anaplastic large-cell lymphoma: a Children's Oncology Group phase 1 consortium study. Lancet Oncol 2013;14:472-80.
69. Woods WG, Tuchman M, Robison LL, et al. Screening for neuroblastoma is ineffective in reducing the incidence of unfavourable advanced stage disease in older children. Eur J Cancer 1997;33:2106-12.
70. Raabe EH, Laudenslager M, Winter C, et al. Prevalence and functional consequence of PHOX2B mutations in neuroblastoma. Oncogene 2008;27:469-76.
71. Peuchmaur M, d'Amore ESG, Joshi VV, et al. Revision of the International Neuroblastoma Pathology Classification: confirmation of favorable and unfavorable prognostic subsets in ganglioneuroblastoma, nodular. Cancer 2003;98:2274-81.
72. Bourdeaut F, Ribeiro A, Paris R, et al. In neuroblastic tumours, Schwann cells do not harbour the genetic alterations of neuroblasts but may nevertheless share the same clonal origin. Oncogene 2008;27:3066-71.
73. Schleiermacher G, Javanmardi N, Bernard V, et al. Emergence of new ALK mutations at relapse of neuroblastoma. J Clin Oncol, in press.
74. Weiss WA, Aldape K, Mohapatra G, et al. Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J 1997;16:2985-95.
75. Hackett CS, Hodgson JG, Law ME, et al. Genome-wide array CGH analysis of murine neuroblastoma reveals distinct genomic aberrations which parallel those in human tumors. Cancer Res 2003;63:5266-73.
76. Grau E, Martinez F, Orellana C, et al. Hypermethylation of apoptotic genes as independent prognostic factor in neuroblastoma disease. Mol Carcinog 2011;50:153-62.
77. Teitz T, Inoue M, Valentine MB, et al. Th-MYCN mice with caspase-8 deficiency develop advanced neuroblastoma with bone marrow metastasis. Cancer Res 2013;73:4086-97.
78. Heukamp LC, Thor T, Schramm A, et al. Targeted expression of mutated ALK induces neuroblastoma in transgenic mice. Sci Transl Med 2012;4:141ra91.
79. Berry T, Luther W, Bhatnagar N, et al. The ALK(F1174L) mutation potentiates the oncogenic activity of MYCN in neuroblastoma. Cancer Cell 2012;22:117-30.
80. Reiff T, Huber L, Kramer M, et al. Midkine and Alk signaling in sympathetic neuron proliferation and neuroblastoma predisposition. Development 2011;138:4699-708.
81. Schönherr C, Ruuth K, Kamaraj S, et al. Anaplastic lymphoma kinase (ALK) regulates initiation of transcription of MYCN in neuroblastoma cells. Oncogene 2012;31:5193-200.
82. Bresler SC, Wood AC, Haglund EA, et al. Differential inhibitor sensitivity of anaplastic lymphoma kinase variants found in neuroblastoma. Sci Transl Med 2011;3:108ra114.
83. Schulte JH, Bachmann HS, Brockmeyer B, et al. High ALK receptor tyrosine kinase expression supersedes ALK mutation as a determining factor of an unfavorable phenotype in primary neuroblastoma. Clin Cancer Res 2011;17:5082-92.
84. Cazes A, Lopez-Delisle L, Tsarovina K, et al. Activated Alk triggers prolonged neurogenesis and Ret upregulation providing a therapeutic target in ALK-mutated neuroblastoma. Oncotarget 2014;5:2688-702.
85. Enomoto H, Crawford PA, Gorodinsky A, et al. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 2001;128:3963-74.
86. Lopez-Delisle L, Pierre-Eugène C, Bloch-Gallego E, et al. Hyperactivation of Alk induces neonatal lethality in knock-in AlkF1178L mice. Oncotarget 2014;5:2703-13.
87. Zhu S, Lee JS, Guo F, et al. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell 2012;21:362-73.
88. Rodrigues FSLM, Yang X, Nikaido M, et al. A simple, highly visual in vivo screen for anaplastic lymphoma kinase inhibitors. ACS Chem Biol 2012;7:1968-74.
89. Amiel J, Laudier B, Attie-Bitach T, et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nat Genet 2003;33:459-61.
90. Mosse YP, Laudenslager M, Khazi D, et al. Germline PHOX2B mutation in hereditary neuroblastoma. Am J Hum Genet 2004;75:727-30.
91. Nagashimada M, Ohta H, Li C, et al. Autonomic neurocristopathy-associated mutations in PHOX2B dysregulate Sox10 expression. J Clin Invest 2012;122:3145-58.
92. Pei D, Luther W, Wang W, et al. Distinct neuroblastoma-associated alterations of PHOX2B impair sympathetic neuronal differentiation in zebrafish models. PLoS Genet 2013;9:e1003533.