Transcript signatures that predict outcome and identify targetable pathways in MYCN-amplified neuroblastoma

Molecular Oncology

Volumn 10, Issue 9, 2016, Pages 1461-1472

  Hallett, Robin M ^a   Seong, Alex B K ^a,b,c   Kaplan, David R ^a,c   Irwin, Meredith S ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Biomarkers; Confounding variables; Gene signatures; MYCN; Networks; Neuroblastoma

Indexed keywords

MYCN PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN; UNCLASSIFIED DRUG; MESSENGER RNA; MYCN PROTEIN, HUMAN; N MYC PROTO ONCOGENE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR;

ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; GENE AMPLIFICATION; GENE EXPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; NEUROBLASTOMA; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; TREATMENT OUTCOME; COHORT ANALYSIS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PHENOTYPE; PROBABILITY; PROGNOSIS; REPRODUCIBILITY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; COHORT STUDIES; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; N-MYC PROTO-ONCOGENE PROTEIN; NEUROBLASTOMA; PHENOTYPE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; PROBABILITY; PROGNOSIS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

EID: 84995480852     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2016.07.012     Document Type: Article

References (65)

1. Abel, F., Dalevi, D., Nethander, M., Jornsten, R., De Preter, K., Vermeulen, J., Stallings, R., Kogner, P., Maris, J., Nilsson, S., A 6-gene signature identifies four molecular subgroups of neuroblastoma. Cancer Cell Int., 11, 2011, 9.
2. Asgharzadeh, S., Pique-Regi, R., Sposto, R., Wang, H., Yang, Y., Shimada, H., Matthay, K., Buckley, J., Ortega, A., Seeger, R.C., Prognostic significance of gene expression profiles of metastatic neuroblastomas lacking MYCN gene amplification. J. Natl. Cancer Inst. 98 (2006), 1193–1203.
3. Asgharzadeh, S., Salo, J.A., Ji, L., Oberthuer, A., Fischer, M., Berthold, F., Hadjidaniel, M., Liu, C.W., Metelitsa, L.S., Pique-Regi, R., Wakamatsu, P., Villablanca, J.G., Kreissman, S.G., Matthay, K.K., Shimada, H., London, W.B., Sposto, R., Seeger, R.C., Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J. Clin. Oncol. 30 (2012), 3525–3532.
4. Attiyeh, E.F., London, W.B., Mosse, Y.P., Wang, Q., Winter, C., Khazi, D., McGrady, P.W., Seeger, R.C., Look, A.T., Shimada, H., Brodeur, G.M., Cohn, S.L., Matthay, K.K., Maris, J.M., Chromosome 1p and 11q deletions and outcome in neuroblastoma. N. Engl. J. Med. 353 (2005), 2243–2253.
5. Barbieri, E., De Preter, K., Capasso, M., Johansson, P., Man, T.K., Chen, Z., Stowers, P., Tonini, G.P., Speleman, F., Shohet, J.M., A p53 drug response signature identifies prognostic genes in high-risk neuroblastoma. PLoS One, 8, 2012, e79843.
6. Bown, N., Cotterill, S., Lastowska, M., O'Neill, S., Pearson, A.D., Plantaz, D., Meddeb, M., Danglot, G., Brinkschmidt, C., Christiansen, H., Laureys, G., Speleman, F., Nicholson, J., Bernheim, A., Betts, D.R., Vandesompele, J., Van Roy, N., Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N. Engl. J. Med. 340 (1999), 1954–1961.
7. Bresler, S.C., Weiser, D.A., Huwe, P.J., Park, J.H., Krytska, K., Ryles, H., Laudenslager, M., Rappaport, E.F., Wood, A.C., McGrady, P.W., Hogarty, M.D., London, W.B., Radhakrishnan, R., Lemmon, M.A., Mosse, Y.P., ALK mutations confer differential oncogenic activation and sensitivity to ALK inhibition therapy in neuroblastoma. Cancer Cell 26 (2014), 682–694.
8. Brodeur, G.M., Pritchard, J., Berthold, F., Carlsen, N.L., Castel, V., Castelberry, R.P., De Bernardi, B., Evans, A.E., Favrot, M., Hedborg, F., et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J. Clin. Oncol. 11 (1993), 1466–1477.
9. Brodeur, G.M., Seeger, R.C., Schwab, M., Varmus, H.E., Bishop, J.M., Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 224 (1984), 1121–1124.
10. Capasso, M., Devoto, M., Hou, C., Asgharzadeh, S., Glessner, J.T., Attiyeh, E.F., Mosse, Y.P., Kim, C., Diskin, S.J., Cole, K.A., Bosse, K., Diamond, M., Laudenslager, M., Winter, C., Bradfield, J.P., Scott, R.H., Jagannathan, J., Garris, M., McConville, C., London, W.B., Seeger, R.C., Grant, S.F., Li, H., Rahman, N., Rappaport, E., Hakonarson, H., Maris, J.M., Common variations in BARD1 influence susceptibility to high-risk neuroblastoma. Nat. Genet. 41 (2009), 718–723.
11. Caron, H., van Sluis, P., de Kraker, J., Bokkerink, J., Egeler, M., Laureys, G., Slater, R., Westerveld, A., Voute, P.A., Versteeg, R., Allelic loss of chromosome 1p as a predictor of unfavorable outcome in patients with neuroblastoma. N. Engl. J. Med. 334 (1996), 225–230.
12. Cohn, S.L., Pearson, A.D., London, W.B., Monclair, T., Ambros, P.F., Brodeur, G.M., Faldum, A., Hero, B., Iehara, T., Machin, D., Mosseri, V., Simon, T., Garaventa, A., Castel, V., Matthay, K.K., The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J. Clin. Oncol. 27 (2009), 289–297.
13. Cole, K.A., Huggins, J., Laquaglia, M., Hulderman, C.E., Russell, M.R., Bosse, K., Diskin, S.J., Attiyeh, E.F., Sennett, R., Norris, G., Laudenslager, M., Wood, A.C., Mayes, P.A., Jagannathan, J., Winter, C., Mosse, Y.P., Maris, J.M., RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc. Natl. Acad. Sci. U. S. A 108 (2011), 3336–3341.
14. De Preter, K., Vermeulen, J., Brors, B., Delattre, O., Eggert, A., Fischer, M., Janoueix-Lerosey, I., Lavarino, C., Maris, J.M., Mora, J., Nakagawara, A., Oberthuer, A., Ohira, M., Schleiermacher, G., Schramm, A., Schulte, J.H., Wang, Q., Westermann, F., Speleman, F., Vandesompele, J., Accurate outcome prediction in neuroblastoma across independent data sets using a multigene signature. Clin. Cancer Res. 16 (2010), 1532–1541.
15. Fardin, P., Barla, A., Mosci, S., Rosasco, L., Verri, A., Versteeg, R., Caron, H.N., Molenaar, J.J., Ora, I., Eva, A., Puppo, M., Varesio, L., A biology-driven approach identifies the hypoxia gene signature as a predictor of the outcome of neuroblastoma patients. Mol. Cancer, 9, 2010, 185.
16. Fardin, P., Cornero, A., Barla, A., Mosci, S., Acquaviva, M., Rosasco, L., Gambini, C., Verri, A., Varesio, L., Identification of multiple hypoxia signatures in neuroblastoma cell lines by l1-l2 regularization and data reduction. J. Biomed. Biotechnol., 2010, 2009, 878709.
17. Fischer, M., Oberthuer, A., Brors, B., Kahlert, Y., Skowron, M., Voth, H., Warnat, P., Ernestus, K., Hero, B., Berthold, F., Differential expression of neuronal genes defines subtypes of disseminated neuroblastoma with favorable and unfavorable outcome. Clin. Cancer Res. 12 (2006), 5118–5128.
18. Garcia, I., Mayol, G., Rios, J., Domenech, G., Cheung, N.K., Oberthuer, A., Fischer, M., Maris, J.M., Brodeur, G.M., Hero, B., Rodriguez, E., Sunol, M., Galvan, P., de Torres, C., Mora, J., Lavarino, C., A three-gene expression signature model for risk stratification of patients with neuroblastoma. Clin. Cancer Res. 18 (2012), 2012–2023.
19. Guo, C., White, P.S., Weiss, M.J., Hogarty, M.D., Thompson, P.M., Stram, D.O., Gerbing, R., Matthay, K.K., Seeger, R.C., Brodeur, G.M., Maris, J.M., Allelic deletion at 11q23 is common in MYCN single copy neuroblastomas. Oncogene 18 (1999), 4948–4957.
20. Hallett, R.M., Dvorkin-Gheva, A., Bane, A., Hassell, J.A., A gene signature for predicting outcome in patients with basal-like breast cancer. Sci. Rep., 2, 2012, 227.
21. Hallett, R.M., Pond, G., Hassell, J.A., A target based approach identifies genomic predictors of breast cancer patient response to chemotherapy. BMC Med. Genomics, 5, 2012, 16.
22. Ham, J., Costa, C., Sano, R., Lochmann, T.L., Sennott, E.M., Patel, N.U., Dastur, A., Gomez-Caraballo, M., Krytska, K., Hata, A.N., Floros, K.V., Hughes, M.T., Jakubik, C.T., Heisey, D.A., Ferrell, J.T., Bristol, M.L., March, R.J., Yates, C., Hicks, M.A., Nakajima, W., Gowda, M., Windle, B.E., Dozmorov, M.G., Garnett, M.J., McDermott, U., Harada, H., Taylor, S.M., Morgan, I.M., Benes, C.H., Engelman, J.A., Mosse, Y.P., Faber, A.C., Exploitation of the apoptosis-primed state of MYCN-amplified neuroblastoma to develop a potent and specific targeted therapy combination. Cancer Cell 29 (2016), 159–172.
23. Huang, M., Weiss, W.A., Neuroblastoma and MYCN. Cold Spring Harb. Perspect. Med., 3, 2013, a014415.
24. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., Speed, T.P., Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 (2003), 249–264.
25. Irwin, M.S., Park, J.R., Neuroblastoma: paradigm for precision medicine. Pediatr. Clin. North Am. 62 (2015), 225–256.
26. Johnson, W.E., Li, C., Rabinovic, A., Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8 (2007), 118–127.
27. Kaufman, B., Shapira-Frommer, R., Schmutzler, R.K., Audeh, M.W., Friedlander, M., Balmana, J., Mitchell, G., Fried, G., Stemmer, S.M., Hubert, A., Rosengarten, O., Steiner, M., Loman, N., Bowen, K., Fielding, A., Domchek, S.M., Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation. J. Clin. Oncol. 33 (2015), 244–250.
28. Kushner, B.H., Modak, S., Kramer, K., LaQuaglia, M.P., Yataghene, K., Basu, E.M., Roberts, S.S., Cheung, N.K., Striking dichotomy in outcome of MYCN-amplified neuroblastoma in the contemporary era. Cancer 120 (2014), 2050–2059.
29. Ladenstein, R., Ambros, I.M., Potschger, U., Amann, G., Urban, C., Fink, F.M., Schmitt, K., Jones, R., Slociak, M., Schilling, F., Ritter, J., Berthold, F., Gadner, H., Ambros, P.F., Prognostic significance of DNA di-tetraploidy in neuroblastoma. Med. Pediatr. Oncol. 36 (2001), 83–92.
30. Liang, J., Tong, P., Zhao, W., Li, Y., Zhang, L., Xia, Y., Yu, Y., The REST gene signature predicts drug sensitivity in neuroblastoma cell lines and is significantly associated with neuroblastoma tumor stage. Int. J. Mol. Sci. 15 (2014), 11220–11233.
31. Maris, J.M., Recent advances in neuroblastoma. N. Engl. J. Med. 362 (2010), 2202–2211.
32. Mateo, J., Carreira, S., Sandhu, S., Miranda, S., Mossop, H., Perez-Lopez, R., Nava Rodrigues, D., Robinson, D., Omlin, A., Tunariu, N., Boysen, G., Porta, N., Flohr, P., Gillman, A., Figueiredo, I., Paulding, C., Seed, G., Jain, S., Ralph, C., Protheroe, A., Hussain, S., Jones, R., Elliott, T., McGovern, U., Bianchini, D., Goodall, J., Zafeiriou, Z., Williamson, C.T., Ferraldeschi, R., Riisnaes, R., Ebbs, B., Fowler, G., Roda, D., Yuan, W., Wu, Y.M., Cao, X., Brough, R., Pemberton, H., A'Hern, R., Swain, A., Kunju, L.P., Eeles, R., Attard, G., Lord, C.J., Ashworth, A., Rubin, M.A., Knudsen, K.E., Feng, F.Y., Chinnaiyan, A.M., Hall, E., de Bono, J.S., DNA-repair defects and olaparib in metastatic prostate cancer. N. Engl. J. Med. 373 (2015), 1697–1708.
33. Meddeb, M., Danglot, G., Chudoba, I., Venuat, A.M., Benard, J., Avet-Loiseau, H., Vasseur, B., Le Paslier, D., Terrier-Lacombe, M.J., Hartmann, O., Bernheim, A., Additional copies of a 25 Mb chromosomal region originating from 17q23.1-17qter are present in 90% of high-grade neuroblastomas. Genes Chromosomes Cancer 17 (1996), 156–165.
34. Nevo, I., Oberthuer, A., Botzer, E., Sagi-Assif, O., Maman, S., Pasmanik-Chor, M., Kariv, N., Fischer, M., Yron, I., Witz, I.P., Gene-expression-based analysis of local and metastatic neuroblastoma variants reveals a set of genes associated with tumor progression in neuroblastoma patients. Int. J. Cancer 126 (2009), 1570–1581.
35. Newman, E.A., Lu, F., Bashllari, D., Wang, L., Opipari, A.W., Castle, V.P., Alternative NHEJ pathway components are therapeutic targets in high-risk neuroblastoma. Mol. Cancer Res. 13 (2015), 470–482.
36. Norris, R.E., Adamson, P.C., Nguyen, V.T., Fox, E., Preclinical evaluation of the PARP inhibitor, olaparib, in combination with cytotoxic chemotherapy in pediatric solid tumors. Pediatr. Blood Cancer 61 (2014), 145–150.
37. Oberthuer, A., Berthold, F., Warnat, P., Hero, B., Kahlert, Y., Spitz, R., Ernestus, K., Konig, R., Haas, S., Eils, R., Schwab, M., Brors, B., Westermann, F., Fischer, M., Customized oligonucleotide microarray gene expression-based classification of neuroblastoma patients outperforms current clinical risk stratification. J. Clin. Oncol. 24 (2006), 5070–5078.
38. Ohira, M., Oba, S., Nakamura, Y., Isogai, E., Kaneko, S., Nakagawa, A., Hirata, T., Kubo, H., Goto, T., Yamada, S., Yoshida, Y., Fuchioka, M., Ishii, S., Nakagawara, A., Expression profiling using a tumor-specific cDNA microarray predicts the prognosis of intermediate risk neuroblastomas. Cancer Cell 7 (2005), 337–350.
39. Park, J.R., Bagatell, R., London, W.B., Maris, J.M., Cohn, S.L., Mattay, K.K., Hogarty, M., Children's Oncology Group's 2013 blueprint for research: neuroblastoma. Pediatr. Blood Cancer 60 (2013), 985–993.
40. Peifer, M., Hertwig, F., Roels, F., Dreidax, D., Gartlgruber, M., Menon, R., Kramer, A., Roncaioli, J.L., Sand, F., Heuckmann, J.M., Ikram, F., Schmidt, R., Ackermann, S., Engesser, A., Kahlert, Y., Vogel, W., Altmuller, J., Nurnberg, P., Thierry-Mieg, J., Thierry-Mieg, D., Mariappan, A., Heynck, S., Mariotti, E., Henrich, K.O., Gloeckner, C., Bosco, G., Leuschner, I., Schweiger, M.R., Savelyeva, L., Watkins, S.C., Shao, C., Bell, E., Hofer, T., Achter, V., Lang, U., Theissen, J., Volland, R., Saadati, M., Eggert, A., de Wilde, B., Berthold, F., Peng, Z., Zhao, C., Shi, L., Ortmann, M., Buttner, R., Perner, S., Hero, B., Schramm, A., Schulte, J.H., Herrmann, C., O'Sullivan, R.J., Westermann, F., Thomas, R.K., Fischer, M., Telomerase activation by genomic rearrangements in high-risk neuroblastoma. Nature 526 (2015), 700–704.
41. Pinto, N.R., Applebaum, M.A., Volchenboum, S.L., Matthay, K.K., London, W.B., Ambros, P.F., Nakagawara, A., Berthold, F., Schleiermacher, G., Park, J.R., Valteau-Couanet, D., Pearson, A.D., Cohn, S.L., Advances in risk classification and treatment strategies for neuroblastoma. J. Clin. Oncol. 33 (2015), 3008–3017.
42. Pugh, T.J., Morozova, O., Attiyeh, E.F., Asgharzadeh, S., Wei, J.S., Auclair, D., Carter, S.L., Cibulskis, K., Hanna, M., Kiezun, A., Kim, J., Lawrence, M.S., Lichenstein, L., McKenna, A., Pedamallu, C.S., Ramos, A.H., Shefler, E., Sivachenko, A., Sougnez, C., Stewart, C., Ally, A., Birol, I., Chiu, R., Corbett, R.D., Hirst, M., Jackman, S.D., Kamoh, B., Khodabakshi, A.H., Krzywinski, M., Lo, A., Moore, R.A., Mungall, K.L., Qian, J., Tam, A., Thiessen, N., Zhao, Y., Cole, K.A., Diamond, M., Diskin, S.J., Mosse, Y.P., Wood, A.C., Ji, L., Sposto, R., Badgett, T., London, W.B., Moyer, Y., Gastier-Foster, J.M., Smith, M.A., Guidry Auvil, J.M., Gerhard, D.S., Hogarty, M.D., Jones, S.J., Lander, E.S., Gabriel, S.B., Getz, G., Seeger, R.C., Khan, J., Marra, M.A., Meyerson, M., Maris, J.M., The genetic landscape of high-risk neuroblastoma. Nat. Genet. 45 (2013), 279–284.
43. Puissant, A., Frumm, S.M., Alexe, G., Bassil, C.F., Qi, J., Chanthery, Y.H., Nekritz, E.A., Zeid, R., Gustafson, W.C., Greninger, P., Garnett, M.J., McDermott, U., Benes, C.H., Kung, A.L., Weiss, W.A., Bradner, J.E., Stegmaier, K., Targeting MYCN in neuroblastoma by BET bromodomain inhibition. Cancer Discov. 3 (2013), 308–323.
44. Schleiermacher, G., Janoueix-Lerosey, I., Ribeiro, A., Klijanienko, J., Couturier, J., Pierron, G., Mosseri, V., Valent, A., Auger, N., Plantaz, D., Rubie, H., Valteau-Couanet, D., Bourdeaut, F., Combaret, V., Bergeron, C., Michon, J., Delattre, O., Accumulation of segmental alterations determines progression in neuroblastoma. J. Clin. Oncol. 28 (2010), 3122–3130.
45. Schleiermacher, G., Mosseri, V., London, W.B., Maris, J.M., Brodeur, G.M., Attiyeh, E., Haber, M., Khan, J., Nakagawara, A., Speleman, F., Noguera, R., Tonini, G.P., Fischer, M., Ambros, I., Monclair, T., Matthay, K.K., Ambros, P., Cohn, S.L., Pearson, A.D., Segmental chromosomal alterations have prognostic impact in neuroblastoma: a report from the INRG project. Br. J. Cancer 107 (2012), 1418–1422.
46. Schramm, A., Mierswa, I., Kaderali, L., Morik, K., Eggert, A., Schulte, J.H., Reanalysis of neuroblastoma expression profiling data using improved methodology and extended follow-up increases validity of outcome prediction. Cancer Lett. 282 (2009), 55–62.
47. Schramm, A., Schulte, J.H., Klein-Hitpass, L., Havers, W., Sieverts, H., Berwanger, B., Christiansen, H., Warnat, P., Brors, B., Eils, J., Eils, R., Eggert, A., Prediction of clinical outcome and biological characterization of neuroblastoma by expression profiling. Oncogene 24 (2005), 7902–7912.
48. Schramm, A., Vandesompele, J., Schulte, J.H., Dreesmann, S., Kaderali, L., Brors, B., Eils, R., Speleman, F., Eggert, A., Translating expression profiling into a clinically feasible test to predict neuroblastoma outcome. Clin. Cancer Res. 13 (2007), 1459–1465.
49. Schwab, M., Alitalo, K., Klempnauer, K.H., Varmus, H.E., Bishop, J.M., Gilbert, F., Brodeur, G., Goldstein, M., Trent, J., Amplified DNA with limited homology to myc cellular oncogene is shared by human neuroblastoma cell lines and a neuroblastoma tumour. Nature 305 (1983), 245–248.
50. Seong, B.K., Lau, J., Adderley, T., Kee, L., Chaukos, D., Pienkowska, M., Malkin, D., Thorner, P., Irwin, M.S., SATB2 enhances migration and invasion in osteosarcoma by regulating genes involved in cytoskeletal organization. Oncogene 34 (2015), 3582–3592.
51. Slavc, I., Ellenbogen, R., Jung, W.H., Vawter, G.F., Kretschmar, C., Grier, H., Korf, B.R., myc gene amplification and expression in primary human neuroblastoma. Cancer Res. 50 (1990), 1459–1463.
52. Stricker, T.P., Morales La Madrid, A., Chlenski, A., Guerrero, L., Salwen, H.R., Gosiengfiao, Y., Perlman, E.J., Furman, W., Bahrami, A., Shohet, J.M., Zage, P.E., Hicks, M.J., Shimada, H., Suganuma, R., Park, J.R., So, S., London, W.B., Pytel, P., Maclean, K.H., Cohn, S.L., Validation of a prognostic multi-gene signature in high-risk neuroblastoma using the high throughput digital NanoString nCounter system. Mol. Oncol. 8 (2014), 669–678.
53. Thompson, D., Vo, K.T., London, W.B., Fischer, M., Ambros, P.F., Nakagawara, A., Brodeur, G.M., Matthay, K.K., DuBois, S.G., Identification of patient subgroups with markedly disparate rates of MYCN amplification in neuroblastoma: a report from the International Neuroblastoma Risk Group project. Cancer 122:6 (2016 Mar 15), 935–945.
54. Tofigh, A., Suderman, M., Paquet, E.R., Livingstone, J., Bertos, N., Saleh, S.M., Zhao, H., Souleimanova, M., Cory, S., Lesurf, R., Shahalizadeh, S., Garcia Lopez, N., Riazalhosseini, Y., Omeroglu, A., Ursini-Siegel, J., Park, M., Dumeaux, V., Hallett, M., The prognostic ease and difficulty of invasive breast carcinoma. Cell Rep. 9 (2014), 129–142.
55. Valentijn, L.J., Koster, J., Haneveld, F., Aissa, R.A., van Sluis, P., Broekmans, M.E., Molenaar, J.J., van Nes, J., Versteeg, R., Functional MYCN signature predicts outcome of neuroblastoma irrespective of MYCN amplification. Proc. Natl. Acad. Sci. U. S. A 109 (2012), 19190–19195.
56. van Nes, J., Chan, A., van Groningen, T., van Sluis, P., Koster, J., Versteeg, R., A NOTCH3 transcriptional module induces cell motility in neuroblastoma. Clin. Cancer Res. 19 (2013), 3485–3494.
57. Venet, D., Dumont, J.E., Detours, V., Most random gene expression signatures are significantly associated with breast cancer outcome. PLoS Comput. Biol., 7, 2011, e1002240.
58. Vermeulen, J., De Preter, K., Laureys, G., Speleman, F., Vandesompele, J., 59-gene prognostic signature sub-stratifies high-risk neuroblastoma patients. Lancet Oncol., 10, 2009, 1030.
59. von Stedingk, K., Koster, J., Piqueras, M., Noguera, R., Navarro, S., Pahlman, S., Versteeg, R., Ora, I., Gisselsson, D., Lindgren, D., Axelson, H., snoRNPs regulate telomerase activity in neuroblastoma and are associated with poor prognosis. Transl. Oncol. 6 (2013), 447–457.
60. Wang, L.L., Teshiba, R., Ikegaki, N., Tang, X.X., Naranjo, A., London, W.B., Hogarty, M.D., Gastier-Foster, J.M., Look, A.T., Park, J.R., Maris, J.M., Cohn, S.L., Seeger, R.C., Asgharzadeh, S., Shimada, H., Augmented expression of MYC and/or MYCN protein defines highly aggressive MYC-driven neuroblastoma: a Children's Oncology Group study. Br. J. Cancer 113 (2015), 57–63.
61. Wei, J.S., Greer, B.T., Westermann, F., Steinberg, S.M., Son, C.G., Chen, Q.R., Whiteford, C.C., Bilke, S., Krasnoselsky, A.L., Cenacchi, N., Catchpoole, D., Berthold, F., Schwab, M., Khan, J., Prediction of clinical outcome using gene expression profiling and artificial neural networks for patients with neuroblastoma. Cancer Res. 64 (2004), 6883–6891.
62. Weiss, W.A., Aldape, K., Mohapatra, G., Feuerstein, B.G., Bishop, J.M., Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J. 16 (1997), 2985–2995.
63. Wu, G., Feng, X., Stein, L., A human functional protein interaction network and its application to cancer data analysis. Genome Biol., 11, 2010, R53.
64. Wu, G., Stein, L., A network module-based method for identifying cancer prognostic signatures. Genome Biol., 13, 2012, R112.
65. Zhu, S., Lee, J.S., Guo, F., Shin, J., Perez-Atayde, A.R., Kutok, J.L., Rodig, S.J., Neuberg, D.S., Helman, D., Feng, H., Stewart, R.A., Wang, W., George, R.E., Kanki, J.P., Look, A.T., Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell 21 (2012), 362–373.