2p24 gain region harboring MYCN gene compared with MYCN amplified and nonamplified neuroblastoma: Biological and clinical characteristics

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2616-2625

  Jeison, Marta ^a   Ash, Shifra ^a   Halevy Berko, Gili ^a   Mardoukh, Jacques ^a   Luria, Drorit ^a   Avigad, Smadar ^a   Feinberg Gorenshtein, Galina ^a   Goshen, Yacov ^a   Hertzel, Gabriel ^b   Kapelushnik, Joseph ^c   Barak, Ayelet Ben ^d   Attias, Dina ^e   Steinberg, Ran ^a   Stein, Jerry ^a   Stark, Batia ^a   Yaniv, Isaac ^a  

^a SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^b HAEMEK MEDICAL CENTER   (Israel)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^d MEYER CHILDREN S HOSPITAL   (Israel)

^e TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; MYCN PROTEIN; UNCLASSIFIED DRUG; MYCN PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN;

ADOLESCENT; ARTICLE; CHILD; CHROMOSOME 11Q; CHROMOSOME 17Q; CHROMOSOME 1P; CHROMOSOME 2; CHROMOSOME 2P; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOGENETICS; EVENT FREE SURVIVAL; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE AMPLIFICATION; GENE NUMBER; HUMAN; INFANT; MAJOR CLINICAL STUDY; MALE; NEUROBLASTOMA; NEWBORN; OVERALL SURVIVAL; PREDICTOR VARIABLE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROMOTER REGION; RELAPSE; RETROSPECTIVE STUDY; SCHOOL CHILD; SURVIVAL RATE; DISEASE FREE SURVIVAL; GENE DOSAGE; GENETICS; ONCOGENE MYC; PATHOLOGY; PATHOPHYSIOLOGY;

CHILD; CHROMOSOMES, HUMAN, PAIR 2; DISEASE-FREE SURVIVAL; GENE AMPLIFICATION; GENE DOSAGE; GENES, MYC; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INFANT; NEUROBLASTOMA; NUCLEAR PROTEINS; ONCOGENE PROTEINS;

EID: 77953223713     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090624     Document Type: Article

References (61)

1. Maris JM, Matthay KK: Molecular biology of neuroblastoma. J Clin Oncol 1999, 17:2264-2279
2. Brodeur GM: Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003, 3:203-216
3. London WB, Castleberry RP, Matthay KK, Look AT, Seeger RC, Shimada H, Thorner P, Brodeur G, Maris JM, Reynolds CP, Cohn S: Evidence for an age cut-off greater 365 days for than neuroblastoma risk group stratification in the Children's Oncology Group. J Clin Oncol 2005, 23:6459-6465
4. Brodeur GM, Pritchard J, Berthold F, Carlsen NLT, Castel V, Castelberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F, Kaneko M, Kemshead J, Lampert F, Lee REJ, Look AT, Pearson ADJ, Philip T, Roald B, Sawada T, Seeger RC, Tsuchida Y, Voûte PA: Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 1993, 11:1466-1477
5. Shimada H, Ambros I, Dehner L, Hata J, Joshi VV, Roald B, Stram DO, Gerbing RB, Lukens JN, Matthay KK, Castleberry RP: The International Neuroblastoma Pathology Classification (the Shimada System). Cancer 1999, 86:364-372
6. Look AT, Hayes FA, Shuster JJ, Dougalss EC, Castelberry RP, Bowman LC, Smith EI, Brodeur GM: 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
7. Ladenstein R, Ambros IM, Potschger U, Amann G, Urban C, Fink FM, Schmitt K, Jones R, Slociak M, Schilling F, Ritter J, Berthold F, Gadner H, Ambros PF: Prognostic significance of DNA di-tetraploidy in neuroblastoma. Med Pediatr Oncol 2001, 36:83-92
8. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM: Amplification of N-myc in untreated human neuroblastoma correlate with advance disease stage. Science 1984, 224:1121-1124 (Pubitemid 14106392)
9. Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D: Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastoma. N Engl J Med 1985, 313:1111-1116 (Pubitemid 16216827)
10. Maris JM, White PS, Beltinger CP, Sulman EP, Castleberry RP, Shuster JJ, Look AT, Brodeur GM: Significance of chromosome 1p loss of heterozygosity in neuroblastoma. Cancer Res 1995, 55:4664-4669
11. Gehring M, Berthold F, Edler L, Schwab M, Amler LC: The 1p deletion is not a reliable marker for the prognosis of patients with neuroblastoma. Cancer Res 1995, 15:5366-5399
12. Caron H, van Sluis P, de Kraker J, Bökkerink J, Egeler M, Laureys G, Slater R, Westerveld A, Voûte P, Versteeg R: Allelic loss of chromosome 1p as a predictor of unfavorable outcome in patients with neuroblastoma. N Engl J Med 1996, 334:225-230 (Pubitemid 26030673)
13. Lastowska M, Cotterill S, Pearson ADJ, Roberts P, McGuckin A, Lewis I, Bown N: Gain of chromosome arm 17q predicts unfavourable outcome in neuroblastoma patients. Eur J Cancer 1997, 33:1627-1633
14. Bown N, Cotterill S, Lastowska M, O'Neill S, Pearson AD, Plantaz D, Meddeb M, Danglot G, Brinkschmidt C, Christiansen H, Laureys G, Speleman F, Nicholson J, Bernheim A, Betts DR, Vandesompele J, Van Roy N: Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 1999, 340:1954-1961
15. Bown N, Lastowska M, Cotterill S, O'Neill S, Ellershaw C, Roberts P, Lewis I, Pearson AD, UK Cancer Cytogenetics Group, UK Children's Cancer Study Group: 17q gain in neuroblastoma predicts adverse clinical outcome. Med Pediatr Oncol 2001, 36:14-19
16. Spitz R, Hero B, Ernestus K, Berthold F: Gain of distal chromosome arm 17q is not associated with poor prognosis in neuroblastoma. Clin Cancer Res 2003, 9:4835-4840 (Pubitemid 37323287)
17. Spitz R, Hero B, Ernestus K, Berthold F: Deletions in chromosome arms 3p and 11q are new prognostic markers in localized and 4s neuroblastoma. Clin Cancer Res 2003, 9:52-58 (Pubitemid 36109715)
18. Plantaz D, Vandesompele J, Van Roy N, Lastowska M, Bown N, Combaret V, Favrot MC, Delattre O, Michon J, Bénard J, Hartmann O, Nicholson JC, Ross FM, Brinkschmidt C, Laureys G, Caron H, Matthay KK, Feuerstein BG, Speelman F: Comparative genomic hybridization (CGH) analysis of stage 4 neuroblastoma revealed high frequency of 11q deletion in tumors lacking MYCN amplifications. Int J Cancer 2001, 91:680-686
19. Attiyeh EF, London WB, Mossé YP, Wang Q, Winter C, Khazi D, McGrady PW, Seeger RC, Look AT, Shimada H, Brodeur GM, Cohn SL, Matthay KK, Maris JM, Children's Oncology Group: Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med 2005, 353:2243-2253
20. Lastowska M, Viprey V, Santibanez-Koref M, Wappler I, Peters H, Cullinane C, Roberts P, Hall AG, Tweddle DA, Pearson ADJ, Lewis I, Burchill SA, Jackson MS: Identification of candidate genes involved in neuroblastoma progression by combining genomic and expression microarrays with survival data. Oncogene 2007, 1-13
21. Cohn SL, Pearson ADJ, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D, Mosseri V, Simon T, Garaventa A, Castel V, Matthay KK: The International Neuroblastoma Risk Group (INRG) Classification System: an INRG Task Force Report. J Clin Oncol 2009, 27:289-297
22. Schleiermacher G, Michon J, Huon I, Duboisd'Enghien C, Klijanienko J, Brisse H, Ribeiro A, Mosseri V, Rubie H, Munzer C, Thomas C, Valtau-Couanet D, Avrignon A, Plantaz D, Delattre O, Couturier J: Chromosomal CGH identifies patients with higher risk of relapse in neuroblastoma without MYCN amplification. Br J Cancer 2007, 97:238-246
23. Janoueix-Lerosey I, Schleiermacher G, Michels E, Veronique Mosseri V, Ribeiro A, Lequin D, Vermeulen J, Couturier J, Peuchmaur M, Valent A, Plantaz D, Rubie H, Valteau-Couanet D, Thomas C, Combaret C, Rousseau R, Eggert A, Michon J, Speleman F, Delattre O: Overall genomic pattern is a predictor of outcome in neuroblastoma. J Clin Oncol 2009, 27:1026-1033
24. Ohali A, Avigad S, Ash S, Goshen Y, Luria D, Feinmesser M, Zaizov R, Yaniv I: Telomere length is a prognostic factor in neuroblastoma. Cancer 2006, 15:1391-1399
25. Schwab M, Ellison J, Busch M, Rosenau W, Varmus HE, Bishop JM: Enhanced expression of the human gene N-myc consequent to amplification of DNA may contribute to malignant progression of neuroblastoma. Proc Natl Acad Sci USA 1984, 81:4940-4944
26. Hogarty MD, Brodeur GM: Wild type sequence of MYCN in neuroblastoma cell lines. Int J Cancer 1999, 80:630-631
27. Ambros IM, Benard J, Boavida M, Bown N, Caron H, Combaret V, Couturier J, Darnfors C, Delattre O, Freeman-Edward J, Gambini C, Gross N, Hattinger CM, Luegmayr A, Lunec J, MartinssonT, Mazzoco K, Navarro S, Noguera R, O'Neill S, Pötschger U, Rumpler S, Speleman F, Tonini GP, Valent A, Van Roy N, Amann G, De Bernardi B, Kogner P, Ladenstein R, Michon J, Pearson ADJ, Ambros PF: Quality Assessment of genetic markers used for therapy stratification. J Clin Oncol 2003, 21:2077-2084
28. Shapiro DN, Valentine MB, Rowe ST, Sinclair AE, Suublett JE, Roberts WM, Look AT: Detection of N-myc gene amplification by fluorescence in situ hybridization. Am J Pathol 1993, 142:1339-1346
29. Theissen J, Boensch M, Spitz R, Betts D, Stegmaier S, Christiansen H, Niggli F, Schilling F, Schwab M, Simon T, Westermann F, Berthold F, Hero B: Heterogeneity of the MYCN oncogene in neuroblastoma. Clin Cancer Res 2009, 15:2085-2090
30. Ambors PF, Ambros IN, Brodeur GM, Haber M, Jhan J, Nakagawara A, Schleiermacher G, Speleman F, Spitz R, London WB, Pearson ADJ, Maris JM: International consensus for neuroblastoma molecular diagnostic: report from the International Neuroblastoma Risk Group (INRG) Biology Committee. Br J Cancer 2009, 100:1471-1482
31. Valent A, Le Roux G, Barrois M, Terrier-Lacombe MJ, Valteau-Couanet D, Léon B, Spengler B, Lenoir G, Bénard J, Bernheim A: MYCN gene overrepresentation detected in primary neuroblastoma tumour cells without amplification. J Patholy 2002, 198:495-501
32. Spitz R, Hero B, Skowron M, Ernestus K, Berthold F: MYCN-status in neuroblastoma: characteristics of tumors showing amplification, gain and non-amplification. Eur J Cancer 2004, 40:2753-2759
33. Stallings RL, Carty P, McArdle L, Mullarkey M, McDermott M, O'Meara A, Ryan E, Catchpoole D, Breatnach F: Evolution of unbalanced gain of distal chromosome 2p in neuroblastoma. Cytogenet Genome Res 2004, 106:49-54
34. Noguera R, Cañete A, Pellín A, Ruiz A, Tasso M, Navarro S, Castel V, Llombart-Bosch A: MYCN gain and MYCN amplification in a stage 4S neuroblastoma. Cancer Genet Cytogenet 2003, 140:157-161
35. Stark B, Jeison M, Gobuzov R, Grug H, Glaser-Gabay L, Luria D, El-Hasid R, Ben Harush M, Avrahami G, Fisher S, Stein J, Zaizov R, Yaniv I: Near haploid childhood acute lymphoblastic leukemia masked by hyperdiploid line: detection by fluorescence in situ hybridization. Cancer Genet Cytogenet 2001, 128:108-113
36. Schouten JP, McElgunn CJ, Waajer R, Zwijnenburg D, Diepvens F, Pals G: Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acid Res 2002, 30:e57
37. van Dijk MC, Rombout PD, Boots-Sprenger SH, Straatman H, Bernsen M, Ruiter DJ, Jeuken JW: Multiplex-ligation-dependent probe amplification for the detection of chromosomal gain and losses in formalin-fixed tissue. Diagn Mol Pathol 2005, 14:9-16
38. Schwab M: Oncogene amplification in solid tumors. Semin Cancer Biol 1999, 9:319-325
39. Savelyeva L, Schwab M: Amplification of oncogenes revisited: from expression profiling to clinical application. Cancer Letters 2001, 167:115-123
40. Corvi R, Savalyeva L, Schwab M: Duplication of N-myc gene at its resident site 2p24 may be a mechanism of activation alternative to amplification in human neuroblastoma cells. Cancer Res 1995, 55:3471-3474
41. Van Roy N, Van Limbergen H, Vandesompele J, Van Gele M, Poppe B, Laureys G, De Paepe A, Speleman F: Chromosome 2 short arm translocations revealed by M-FISH analysis of neuroblastoma cell lines. Med Pediatr Oncol 2000, 35:538-540
42. Valent A, Guillaud-Bataille M, Farra Ch, Lozach F, Spengler B, Terrier-Lacombe MJ, Valteau-Couanet D, Danglot G, Lenoir G, Brison O, Bénard J, Bernheim A: Alternative pathways of MYCN gene copy number increase in primary neuroblastoma tumors. Cancer Genet Cytogenet 2004, 153:10-15
43. Schleiermacher G, Janoueix-Lerosey I, Combaret V, Derré J, Couturier J, Aurias A, Delattre O: Combined 24-color karyotype and comparative genomic hybridization analysis indicates predominant rearrangements of early replicating chromosome regions in neuroblastoma. Cancer Genet Cytogenet 2003, 141:23-42
44. Villamon E, Piqueras M, Mackintosh C, Alonso J, de Alava E, Navarro S, Noguera R: Comparisson of different techniques for the detection of genetic risk-identifying chromosomal gains and losses in neuroblastoma. Virchows Arch 2008, 453:47-55
45. Chen Q-R, Bilke S, Khan J: High-resolution cDNA microarray-based comparative genomic hybridization analysis in neuroblastoma. Cancer Lett 2005, 228:71-81 (Pubitemid 41188427)
46. Mossé YP, Greshock J, Weber BL, Maris JM: Measurement and relevance of neuroblastoma DNA copy number changes in the postgenome era. Cancer Lett 2005, 228:83-90
47. Spitz R, Oberthuer A, Zapatka M, Brors B, Hero B, Ernestus K, Oestreich J, Fischer M, Simon T, Berthold F: Oligonucleotide array-based comparative genomic hybridization (aCGH) of 90 neuroblastomas reveals aberration patterns closely associated with relapse pattern and outcome. Genes Chromosomes Cancer 2006, 45:1130-1142
48. George RE, Attiyeh EF, Shuli L, Moreau LA, Neuberg D, Cheng L, Fox EA, Meyerson M, Diller L, Fortina P, Look AT, Maris JM: Genome-wide analysis of neuroblastomas using high-density single nucleotide polymorphism arrays. PLoS One 2007, 2:e255
49. Carén H, Abel F, Kogner P, Martinsson T: High incidence of DNA mutations and gene amplifications of the ALK gene in advanced sporadic neuroblastoma tumors. Biochem J 2008, 416:153-159
50. Chen Y, Takita J, Choi YL, Kato M, Ohira M, Sanada M, Wang L, Soda M, Kikuchi A, Igarashi T, Nakagawara A, Hayashi Y, Mano H, Ogawa S: Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008, 455:971-974
51. Janoueix-Lerosey I, Lequin D, Brugières L, Ribeiro A, de Pontual L, Combaret V, Raynal V, Puisieux A, Schleiermacher G, Pierron G, Valteau-Couanet D, Frebourg T, Michon J, Lyonnet S, Amiel J, Delattre O: Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008, 455:967-970
52. Mossé YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, Laquaglia MJ, Sennett R, Lynch JE, Perri P, Laureys G, Speleman F, Kim C, Hou C, Hakonarson H, Torkamani A, Schork NJ, Brodeur GM, Tonini GP, Rappaport E, Devoto M, Maris JM: Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008, 455:930-935
53. Cohn SL, London WB, Huang D, Katzenstein HM, Salwen HR, Reinhart T, Madafiglio J, Marshall GM, Norris MD, Haber M: MYCN expression is not prognostic of adverse outcome in advanced-stage neuroblastoma with nonamplified MYCN. J Clin Oncol 2000, 18:3604-3613
54. Tajiri T, Tanaka S, Higashi M, Kinoshita Y, Takahashi Y, Tatsuta K, Sachiyo S: Biological diagnosis for neuroblastoma using the combination of highly sensitive analysis of prognostic factors. J Pediatr Surg 2006, 41:560-566
55. Stock C, Bozarsky E, Watzinger F, Poetschger U, Orel L, Lion T, Kowalska A, Ambros P: Genes proximal and distal to MYCN are highly expressed in human neuroblastoma as visualized by comparative expressed sequence hybridization. Am J Pathol 2008, 172:203-214
56. Guo C, White PS, Weiss MJ, Hogarty MD, Thompson PM, Stram DO, Gerbing R, Matthay KK, Seeger RC, Brodeur GM, Maris JM: Allelic deletion at 11q23 is common in MYCN single copy neuroblastomas. Oncogene 1999, 18:4948-4957
57. Guo C, White PS, Hogarty MD, Brodeur GM, Gerbing R, Stram DO, Maris JM: Deletion of 11q23 is a frequent event in the evolution of MYCN single-copy high-risk neuroblastomas. Med Pediatr Oncol 2000, 35:544-546
58. Stark B, Jeison M, Bar-Am I, Glaser-Gabay L, Mordoukh J, Luria D, Feinmeser M, Goshen Y, Stein J, Abramov A, Zaizov R, Yaniv I: Distinct cytogenetic pathways of advanced-stage neuroblastoma tumors, detected by spectral karyotyping. Genes Chromosomes Cancer 2002, 34:313-324
59. Stark B, Jeison M, Glaser-Gabay L, Bar-Am I, Mordoukh J, Ash SH, Atias D, Stein J, Zaizov R, Yaniv I: der(11)t(11;17): a distinct cytogenetic pathway of advanced stage neuroblastoma (NBL) detected by spectral karyotype (SKY). Cancer Lett 2003, 19:75-79
60. Lastowska M, Van Roy N, Bown N, Speelmanm F, Lunec J, Strachan T, Pearson ADJ, Jackson MS: Molecular cytogenetic delineation of 17q translocation breakpoints in neuroblastoma cell lines. Genes Chromosomes Cancer 1998, 23:116-122 (Pubitemid 28402337)
61. Stallings RL, Carty P, McArdle L, Mullarkey M, McDermott M, Breatnach F, O'Meara A: Molecular cytogenetic analysis of recurrent unbalanced t(11;17) in neuroblastoma. Cancer Genet Cytogenet 2004, 154:44-51