Pan-cancer Alterations of the MYC Oncogene and Its Proximal Network across the Cancer Genome Atlas

Cell Systems

Volumn 6, Issue 3, 2018, Pages 282-300.e2

  Schaub, Franz X ^a,b   Dhankani, Varsha ^b   Berger, Ashton C ^c   Trivedi, Mihir ^b   Richardson, Anne B ^b   Shaw, Reid ^b   Zhao, Wei ^d   Zhang, Xiaoyang ^c   Ventura, Andrea ^e   Liu, Yuexin ^d   Ayer, Donald E ^f   Hurlin, Peter J ^g   Cherniack, Andrew D ^c,k   Eisenman, Robert N ^h   Bernard, Brady ^i,j   Grandori, Carla ^a,b   Caesar Johnson, Samantha J ^k   Demchok, John A ^k   Felau, Ina ^k   Kasapi, Melpomeni ^k   Ferguson, Martin L ^k   Hutter, Carolyn M ^k   Sofia, Heidi J ^k   Tarnuzzer, Roy ^k   Wang, Zhining ^k   Yang, Liming ^k   Zenklusen, Jean C ^k   more..

^a Cure First   (United States)

^b Cure First and SEngine Precision Medicine   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^f UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^g OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^h Fred Hutchinson Cancer Research Center   (United States)

ⁱ INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^j Providence Health and Services   (United States)

^k Julia)

more..

Author keywords

MAX; MNT; MYC genomic alterations; TCGA; The Cancer Genome Atlas

Indexed keywords

APC PROTEIN; B RAF KINASE; MICRORNA; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PIK3CA PROTEIN; PROTEIN; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; MGA PROTEIN, HUMAN; MNT PROTEIN, HUMAN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TUMOR MARKER;

ARTICLE; CANCER GENETICS; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; FUNCTIONAL PROTEOMICS; GENE DELETION; GENETIC CONSERVATION; HUMAN; HUMAN GENOME; IMMUNE RESPONSE; MALIGNANT NEOPLASM; ONCOGENE MYC; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; BIOLOGY; CARCINOGENESIS; CHROMATIN; GENETICS; GENOMICS; METABOLISM; NEOPLASM; ONCOGENE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PROTEOMICS;

BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOMARKERS, TUMOR; CARCINOGENESIS; CHROMATIN; COMPUTATIONAL BIOLOGY; GENES, MYC; GENOMICS; HUMANS; NEOPLASMS; ONCOGENES; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 85044336302     PISSN: 24054712     EISSN: 24054720     Source Type: Journal    
DOI: 10.1016/j.cels.2018.03.003     Document Type: Article

References (113)

1. Adhikary, S., Marinoni, F., Hock, A., Hulleman, E., Popov, N., Beier, R., Bernard, S., Quarto, M., Capra, M., Goettig, S., et al. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123 (2005), 409–421.
2. Ayer, D.E., Kretzner, L., Eisenman, R.N., Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell 72 (1993), 211–222.
3. Bahram, F., von der Lehr, N., Cetinkaya, C., Larsson, L.G., c-Myc hot spot mutations in lymphomas result in inefficient ubiquitination and decreased proteasome-mediated turnover. Blood 95 (2000), 2104–2110.
4. Bartel, D.P., MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116 (2004), 281–297.
5. Bazarov, A.V., Adachi, S., Li, S.F., Mateyak, M.K., Wei, S., Sedivy, J.M., A modest reduction in c-myc expression has minimal effects on cell growth and apoptosis but dramatically reduces susceptibility to Ras and Raf transformation. Cancer Res. 61 (2001), 1178–1186.
6. Beroukhim, R., Mermel, C.H., Porter, D., Wei, G., Raychaudhuri, S., Donovan, J., Barretina, J., Boehm, J.S., Dobson, J., Urashima, M., et al. The landscape of somatic copy-number alteration across human cancers. Nature 463 (2010), 899–905.
7. Blackwell, T.K., Huang, J., Ma, A., Kretzner, L., Alt, F.W., Eisenman, R.N., Weintraub, H., Binding of myc proteins to canonical and noncanonical DNA sequences. Mol. Cell. Biol. 13 (1993), 5216–5224.
8. Bouchard, C., Dittrich, O., Kiermaier, A., Dohmann, K., Menkel, A., Eilers, M., Lüscher, B., Regulation of cyclin D2 gene expression by the Myc/Max/Mad network: Myc-dependent TRRAP recruitment and histone acetylation at the cyclin D2 promoter. Genes Dev. 15 (2001), 2042–2047.
9. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., Brabletz, T., A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9 (2008), 582–589.
10. Burnichon, N., Cascón, A., Schiavi, F., Morales, N.P., Comino-Méndez, I., Abermil, N., Inglada-Pérez, L., de Cubas, A.A., Amar, L., Barontini, M., et al. MAX mutations cause hereditary and sporadic pheochromocytoma and paraganglioma. Clin. Cancer Res. 18 (2012), 2828–2837.
11. Cancer Genome Atlas Research Network, Comprehensive molecular profiling of lung adenocarcinoma. Nature 511 (2014), 543–550.
12. Cancer Genome Atlas Research Network, Integrated genomic characterization of papillary thyroid carcinoma. Cell 159 (2014), 676–690.
13. Canisius, S., Martens, J.W., Wessels, L.F., A novel independence test for somatic alterations in cancer shows that biology drives mutual exclusivity but chance explains most co-occurrence. Genome Biol., 17, 2016, 261.
14. Carroll, P.A., Diolaiti, D., McFerrin, L., Gu, H., Djukovic, D., Du, J., Cheng, P.F., Anderson, S., Ulrich, M., Hurley, J.B., et al. Deregulated Myc requires MondoA/Mlx for metabolic reprogramming and tumorigenesis. Cancer Cell 27 (2015), 271–285.
15. Carter, S.L., Cibulskis, K., Helman, E., McKenna, A., Shen, H., Zack, T., Laird, P.W., Onofrio, R.C., Winckler, W., Weir, B.A., et al. Absolute quantification of somatic DNA alterations in human cancer. Nat. Biotechnol. 30 (2012), 413–421.
16. Casey, S.C., Tong, L., Li, Y., Do, R., Walz, S., Fitzgerald, K.N., Gouw, A.M., Baylot, V., Gütgemann, I., Eilers, M., et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science 352 (2016), 227–231.
17. Cermelli, S., Jang, I.S., Bernard, B., Grandori, C., Synthetic lethal screens as a means to understand and treat MYC-driven cancers. Cold Spring Harb. Perspect. Med., 4, 2014, 10.1101/cshperspect.a014209.
18. Chang, T.-C., Wentzel, E.A., Kent, O.A., Ramachandran, K., Mullendore, M., Lee, K.H., Feldmann, G., Yamakuchi, M., Ferlito, M., Lowenstein, C.J., et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26 (2007), 745–752.
19. Ciriello, G., Miller, M.L., Aksoy, B.A., Senbabaoglu, Y., Schultz, N., Sander, C., Emerging landscape of oncogenic signatures across human cancers. Nat. Genet. 45 (2013), 1127–1133.
20. Comino-Méndez, I., Gracia-Aznárez, F.J., Schiavi, F., Landa, I., Leandro-García, L.J., Letón, R., Honrado, E., Ramos-Medina, R., Caronia, D., Pita, G., et al. Exome sequencing identifies MAX mutations as a cause of hereditary pheochromocytoma. Nat. Genet. 43 (2011), 663–667.
21. Conacci-Sorrell, M., McFerrin, L., Eisenman, R.N., An overview of MYC and its interactome. Cold Spring Harb. Perspect. Med., 4, 2014, a014357.
22. Cowling, V.H., Cole, M.D., The Myc transactivation domain promotes global phosphorylation of the RNA polymerase II carboxy-terminal domain independently of direct DNA binding. Mol. Cell. Biol. 27 (2007), 2059–2073.
23. Dalla-Favera, R., Westin, E., Gelmann, E.P., Martinotti, S., Bregni, M., Wong-Staal, F., Gallo, R.C., The human onc gene c-myc: structure, expression, and amplification in the human promyelocytic leukemia cell line HL-60. Haematol. Blood Transfus. 28 (1983), 247–254.
24. Dang, C.V., Eisenman, R.N., Myc and the Pathway to Cancer. 2014, Cold Spring Harbor.
25. De Paoli, L., Cerri, M., Monti, S., Rasi, S., Spina, V., Bruscaggin, A., Greco, M., Ciardullo, C., Famà, R., Cresta, S., et al. MGA, a suppressor of MYC, is recurrently inactivated in high risk chronic lymphocytic leukemia. Leuk. Lymphoma 54 (2013), 1087–1090.
26. de Pretis, S., Kress, T.R., Morelli, M.J., Sabo, A., Locarno, C., Verrecchia, A., Doni, M., Campaner, S., Amati, B., Pelizzola, M., Integrative analysis of RNA polymerase II and transcriptional dynamics upon MYC activation. Genome Res. 27 (2017), 1658–1664.
27. Dezfouli, S., Bakke, A., Huang, J., Wynshaw-Boris, A., Hurlin, P.J., Inflammatory disease and lymphomagenesis caused by deletion of the Myc antagonist Mnt in T cells. Mol. Cell. Biol. 26 (2006), 2080–2092.
28. Diolaiti, D., McFerrin, L., Carroll, P.A., Eisenman, R.N., Functional interactions among members of the MAX and MLX transcriptional network during oncogenesis. Biochim. Biophys. Acta 1849 (2015), 484–500.
29. Dominguez-Sola, D., Gautier, J., MYC and the control of DNA replication. Cold Spring Harb. Perspect. Med., 4, 2014, 10.1101/cshperspect.a014423.
30. Dominguez-Sola, D., Ying, C.Y., Grandori, C., Ruggiero, L., Chen, B., Li, M., Galloway, D.A., Gu, W., Gautier, J., Dalla-Favera, R., Non-transcriptional control of DNA replication by c-Myc. Nature 448 (2007), 445–451.
31. Edelmann, J., Tausch, E., Landau, D.A., Robrecht, S., Bahlo, J., Fischer, K., Fink, A.M., Bloehdorn, J., Holzmann, K., Böttcher, S., et al. Frequent evolution of copy number alterations in CLL following first-line treatment with FC(R) is enriched with TP53 alterations: results from the CLL8 trial. Leukemia 31 (2017), 734–738.
32. Fernandez, P.C., Frank, S.R., Wang, L., Schroeder, M., Liu, S., Greene, J., Cocito, A., Amati, B., Genomic targets of the human c-Myc protein. Genes Dev. 17 (2003), 1115–1129.
33. Fero, M.L., Randel, E., Gurley, K.E., Roberts, J.M., Kemp, C.J., The murine gene p27Kip1 is haplo-insufficient for tumour suppression. Nature 396 (1998), 177–180.
34. Frank, S.R., Schroeder, M., Fernandez, P., Taubert, S., Amati, B., Binding of c-Myc to chromatin mediates mitogen-induced acetylation of histone H4 and gene activation. Genes Dev. 15 (2001), 2069–2082.
35. Gabay, M., Li, Y., Felsher, D.W., MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb. Perspect. Med., 4, 2014.
36. Gomez-Roman, N., Felton-Edkins, Z.A., Kenneth, N.S., Goodfellow, S.J., Athineos, D., Zhang, J., Ramsbottom, B.A., Innes, F., Kantidakis, T., Kerr, E.R., et al. Activation by c-Myc of transcription by RNA polymerases I, II and III. Biochem. Soc. Symp., 2006, 141–154.
37. Grandori, C., Gomez-Roman, N., Felton-Edkins, Z.A., Ngouenet, C., Galloway, D.A., Eisenman, R.N., White, R.J., c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat. Cell Biol. 7 (2005), 311–318.
38. Grandori, C., Mac, J., Siebelt, F., Ayer, D.E., Eisenman, R.N., Myc-Max heterodimers activate a DEAD box gene and interact with multiple E box-related sites in vivo. EMBO J. 15 (1996), 4344–4357.
39. Grandori, C., Wu, K.-J., Fernandez, P., Ngouenet, C., Grim, J., Clurman, B.E., Moser, M.J., Oshima, J., Russell, D.W., Swisshelm, K., et al. Werner syndrome protein limits MYC-induced cellular senescence. Genes Dev. 17 (2003), 1569–1574.
40. Gregory, P.A., Bert, A.G., Paterson, E.L., Barry, S.C., Tsykin, A., Farshid, G., Vadas, M.A., Khew-Goodall, Y., Goodall, G.J., The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10 (2008), 593–601.
41. Grewal, S.S., Li, L., Orian, A., Eisenman, R.N., Edgar, B.A., Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat. Cell Biol. 7 (2005), 295–302.
42. Guccione, E., Martinato, F., Finocchiaro, G., Luzi, L., Tizzoni, L., Dall' Olio, V., Zardo, G., Nervi, C., Bernard, L., Amati, B., Myc-binding-site recognition in the human genome is determined by chromatin context. Nat. Cell Biol. 8 (2006), 764–770.
43. Han, Y.C., Vidigal, J.A., Mu, P., Yao, E., Singh, I., González, A.J., Concepcion, C.P., Bonetti, C., Ogrodowski, P., Carver, B., et al. An allelic series of miR-17∼92-mutant mice uncovers functional specialization and cooperation among members of a microRNA polycistron. Nat. Genet. 47 (2015), 766–775.
44. Hayward, W.S., Neel, B.G., Astrin, S.M., Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290 (1981), 475–480.
45. He, L., Liu, J., Collins, I., Sanford, S., O'Connell, B., Benham, C.J., Levens, D., Loss of FBP function arrests cellular proliferation and extinguishes c-myc expression. EMBO J. 19 (2000), 1034–1044.
46. He, L., Thomson, J.M., Hemann, M.T., Hernando-Monge, E., Mu, D., Goodson, S., Powers, S., Cordon-Cardo, C., Lowe, S.W., Hannon, G.J., et al. A microRNA polycistron as a potential human oncogene. Nature 435 (2005), 828–833.
47. Hedges, L.V., Distribution theory for glass's estimator of effect size and related estimators. J. Educ. Behav. Stat. 6 (1981), 107–128.
48. Hemann, M.T., Bric, A., Teruya-Feldstein, J., Herbst, A., Nilsson, J.A., Cordon-Cardo, C., Cleveland, J.L., Tansey, W.P., Lowe, S.W., Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436 (2005), 807–811.
49. Herranz, D., Ambesi-Impiombato, A., Palomero, T., Schnell, S.A., Belver, L., Wendorff, A.A., Xu, L., Castillo-Martin, M., Llobet-Navás, D., Cordon-Cardo, C., et al. A NOTCH1-driven MYC enhancer promotes T cell development, transformation and acute lymphoblastic leukemia. Nat. Med. 20 (2014), 1130–1137.
50. Hnisz, D., Abraham, B.J., Lee, T.I., Lau, A., Saint-André, V., Sigova, A.A., Hoke, H.A., Young, R.A., Super-enhancers in the control of cell identity and disease. Cell 155 (2013), 934–947.
51. Hofmann, J.W., Zhao, X., De Cecco, M., Peterson, A.L., Pagliaroli, L., Manivannan, J., Hubbard, G.B., Ikeno, Y., Zhang, Y., Feng, B., et al. Reduced expression of MYC increases longevity and enhances healthspan. Cell 160 (2015), 477–488.
52. Huang, M., Weiss, W.A., G34, another connection between MYCN and a pediatric tumor. Cancer Discov. 3 (2013), 484–486.
53. Hurlin, P.J., Quéva, C., Eisenman, R.N., Mnt, a novel Max-interacting protein is coexpressed with Myc in proliferating cells and mediates repression at Myc binding sites. Genes Dev. 11 (1997), 44–58.
54. Hurlin, P.J., Quéva, C., Koskinen, P.J., Steingrímsson, E., Ayer, D.E., Copeland, N.G., Jenkins, N.A., Eisenman, R.N., Mad3 and Mad4: novel Max-interacting transcriptional repressors that suppress c-myc dependent transformation and are expressed during neural and epidermal differentiation. EMBO J. 14 (1995), 5646–5659.
55. Hurlin, P.J., Steingrìmsson, E., Copeland, N.G., Jenkins, N.A., Eisenman, R.N., Mga, a dual-specificity transcription factor that interacts with Max and contains a T-domain DNA-binding motif. EMBO J. 18 (1999), 7019–7028.
56. Ilic, N., Utermark, T., Widlund, H.R., Roberts, T.M., PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis. Proc. Natl. Acad. Sci. USA 108 (2011), E699–E708.
57. Johnston, L.A., Prober, D.A., Edgar, B.A., Eisenman, R.N., Gallant, P., Drosophila myc regulates cellular growth during development. Cell 98 (1999), 779–790.
58. Kedde, M., van Kouwenhove, M., Zwart, W., Oude Vrielink, J.A.F., Elkon, R., Agami, R., A Pumilio-induced RNA structure switch in p27-3' UTR controls miR-221 and miR-222 accessibility. Nat. Cell Biol. 12 (2010), 1014–1020.
59. Kim, Y.K., Yu, J., Han, T.S., Park, S.Y., Namkoong, B., Kim, D.H., Hur, K., Yoo, M.W., Lee, H.J., Yang, H.K., et al. Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res. 37 (2009), 1672–1681.
60. Korpal, M., Lee, E.S., Hu, G., Kang, Y., The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283 (2008), 14910–14914.
61. Kress, T.R., Sabò, A., Amati, B., MYC: connecting selective transcriptional control to global RNA production. Nat. Rev. Cancer 15 (2015), 593–607.
62. le Sage, C., Nagel, R., Egan, D.A., Schrier, M., Mesman, E., Mangiola, A., Anile, C., Maira, G., Mercatelli, N., Ciafrè, S.A., et al. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26 (2007), 3699–3708.
63. Li, Y., Choi, P.S., Casey, S.C., Dill, D.L., Felsher, D.W., MYC through miR-17-92 suppresses specific target genes to maintain survival, autonomous proliferation, and a neoplastic state. Cancer Cell 26 (2014), 262–272.
64. Lin, C.Y., Lovén, J., Rahl, P.B., Paranal, R.M., Burge, C.B., Bradner, J.E., Lee, T.I., Young, R.A., Transcriptional amplification in tumor cells with elevated c-Myc. Cell 151 (2012), 56–67.
65. Link, J.M., Hurlin, P.J., The activities of MYC, MNT and the MAX-interactome in lymphocyte proliferation and oncogenesis. Biochim. Biophys. Acta 1849 (2015), 554–562.
66. Link, J.M., Ota, S., Zhou, Z.Q., Daniel, C.J., Sears, R.C., Hurlin, P.J., A critical role for Mnt in Myc-driven T-cell proliferation and oncogenesis. Proc. Natl. Acad. Sci. USA 109 (2012), 19685–19690.
67. Little, C.D., Nau, M.M., Carney, D.N., Gazdar, A.F., Minna, J.D., Amplification and expression of the c-myc oncogene in human lung cancer cell lines. Nature 306 (1983), 194–196.
68. Lüscher, B., Vervoorts, J., Regulation of gene transcription by the oncoprotein MYC. Gene 494 (2012), 145–160.
69. Medina, P.P., Nolde, M., Slack, F.J., OncomiR addiction in an in vivo model of microRNA-21-induced pre-B-cell lymphoma. Nature 467 (2010), 86–90.
70. Mermel, C.H., Schumacher, S.E., Hill, B., Meyerson, M.L., Beroukhim, R., Getz, G., GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol., 12, 2011, R41.
71. Meroni, G., Reymond, A., Alcalay, M., Borsani, G., Tanigami, A., Tonlorenzi, R., Lo Nigro, C., Messali, S., Zollo, M., Ledbetter, D.H., et al. Rox, a novel bHLHZip protein expressed in quiescent cells that heterodimerizes with Max, binds a non-canonical E box and acts as a transcriptional repressor. EMBO J. 16 (1997), 2892–2906.
72. Mootha, V.K., Lindgren, C.M., Eriksson, K.F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstråle, M., Laurila, E., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34 (2003), 267–273.
73. Moser, R., Toyoshima, M., Robinson, K., Gurley, K.E., Howie, H.L., Davison, J., Morgan, M., Kemp, C.J., Grandori, C., MYC-driven tumorigenesis is inhibited by WRN syndrome gene deficiency. Mol. Cancer Res. 10 (2012), 535–545.
74. Mu, P., Han, Y.C., Betel, D., Yao, E., Squatrito, M., Ogrodowski, P., de Stanchina, E., D'Andrea, A., Sander, C., Ventura, A., Genetic dissection of the miR-17 92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 23 (2009), 2806–2811.
75. Muncan, V., Sansom, O.J., Tertoolen, L., Phesse, T.J., Begthel, H., Sancho, E., Cole, A.M., Gregorieff, A., de Alboran, I.M., Clevers, H., et al. Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Mol. Cell. Biol. 26 (2006), 8418–8426.
76. Murphy, D.J., Junttila, M.R., Pouyet, L., Karnezis, A., Shchors, K., Bui, D.A., Brown-Swigart, L., Johnson, L., Evan, G.I., Distinct thresholds govern Myc's biological output in vivo. Cancer Cell 14 (2008), 447–457.
77. Nakagawara, A., Ikeda, K., Tsuda, T., Higashi, K., N-myc oncogene amplification and prognostic factors of neuroblastoma in children. J. Pediatr. Surg. 22 (1987), 895–898.
78. Nesbit, C.E., Tersak, J.M., Prochownik, E.V., MYC oncogenes and human neoplastic disease. Oncogene 18 (1999), 3004–3016.
79. Nie, Z., Hu, G., Wei, G., Cui, K., Yamane, A., Resch, W., Wang, R., Green, D.R., Tessarollo, L., Casellas, R., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 151 (2012), 68–79.
80. Nilsson, J.A., Maclean, K.H., Keller, U.B., Pendeville, H., Baudino, T.A., Cleveland, J.L., Mnt loss triggers Myc transcription targets, proliferation, apoptosis, and transformation. Mol. Cell. Biol. 24 (2004), 1560–1569.
81. Nowell, P., Finan, J., Dalla-Favera, R., Gallo, R.C., ar-Rushdi, A., Romanczuk, H., Selden, J.R., Emanuel, B.S., Rovera, G., Croce, C.M., Association of amplified oncogene c-myc with an abnormally banded chromosome 8 in a human leukaemia cell line. Nature 306 (1983), 494–497.
82. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V., Mendell, J.T., c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435 (2005), 839–843.
83. O'Neil, J., Grim, J., Strack, P., Rao, S., Tibbitts, D., Winter, C., Hardwick, J., Welcker, M., Meijerink, J.P., Pieters, R., et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 204 (2007), 1813–1824.
84. O'Shea, J.M., Ayer, D.E., Coordination of nutrient availability and utilization by MAX- and MLX-centered transcription networks. Cold Spring Harb. Perspect. Med., 3, 2013, a014258.
85. Olive, V., Bennett, M.J., Walker, J.C., Ma, C., Jiang, I., Cordon-Cardo, C., Li, Q.-J., Lowe, S.W., Hannon, G.J., He, L., miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 23 (2009), 2839–2849.
86. Pantaleo, M.A., Urbini, M., Indio, V., Ravegnini, G., Nannini, M., De Luca, M., Tarantino, G., Angelini, S., Gronchi, A., Vincenzi, B., et al. Genome-wide analysis identifies MEN1 and MAX mutations and a neuroendocrine-like molecular heterogeneity in quadruple WT GIST. Mol. Cancer Res. 15 (2017), 553–562.
87. Park, S.-M., Gaur, A.B., Lengyel, E., Peter, M.E., The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22 (2008), 894–907.
88. Payne, S.R., Kemp, C.J., Tumor suppressor genetics. Carcinogenesis 26 (2005), 2031–2045.
89. Robinson, K., Asawachaicharn, N., Galloway, D.A., Grandori, C., c-Myc accelerates S-phase and requires WRN to avoid replication stress. PLoS One, 4, 2009, e5951.
90. Rohban, S., Campaner, S., Myc induced replicative stress response: how to cope with it and exploit it. Biochim. Biophys. Acta 1849 (2015), 517–524.
91. Roussel, M.F., Robinson, G.W., Role of MYC in medulloblastoma. Cold Spring Harb. Perspect. Med., 3, 2013.
92. Ruggero, D., The role of Myc-induced protein synthesis in cancer. Cancer Res. 69 (2009), 8839–8843.
93. Sabo, A., Amati, B., Genome recognition by MYC. Cold Spring Harb. Perspect. Med., 4, 2014.
94. Sabò, A., Kress, T.R., Pelizzola, M., de Pretis, S., Gorski, M.M., Tesi, A., Morelli, M.J., Bora, P., Doni, M., Verrecchia, A., et al. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 511 (2014), 488–492.
95. Salghetti, S.E., Kim, S.Y., Tansey, W.P., Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J. 18 (1999), 717–726.
96. Schaefer, I.M., Wang, Y., Liang, C.W., Bahri, N., Quattrone, A., Doyle, L., Mariño-Enríquez, A., Lauria, A., Zhu, M., Debiec-Rychter, M., et al. MAX inactivation is an early event in GIST development that regulates p16 and cell proliferation. Nat. Commun., 8, 2017, 14674.
97. 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.
98. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
99. Sur, I.K., Hallikas, O., Vähärautio, A., Yan, J., Turunen, M., Enge, M., Taipale, M., Karhu, A., Aaltonen, L.A., Taipale, J., Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science 338 (2012), 1360–1363.
100. Ventura, A., Jacks, T., MicroRNAs and cancer: short RNAs go a long way. Cell 136 (2009), 586–591.
101. Vidotto, T., Tiezzi, D.G., Squire, J.A., Distinct subtypes of genomic PTEN deletion size influence the landscape of aneuploidy and outcome in prostate cancer. Mol. Cytogenet., 11, 2018, 1.
102. Vita, M., Henriksson, M., The Myc oncoprotein as a therapeutic target for human cancer. Semin. Cancer Biol. 16 (2006), 318–330.
103. Vo, B.T., Wolf, E., Kawauchi, D., Gebhardt, A., Rehg, J.E., Finkelstein, D., Walz, S., Murphy, B.L., Youn, Y.H., Han, Y.-G., et al. The interaction of myc with Miz1 defines medulloblastoma subgroup identity. Cancer Cell 29 (2016), 5–16.
104. Walter, W., Sánchez-Cabo, F., Ricote, M., GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31 (2015), 2912–2914.
105. Walz, S., Lorenzin, F., Morton, J., Wiese, K.E., von Eyss, B., Herold, S., Rycak, L., Dumay-Odelot, H., Karim, S., Bartkuhn, M., et al. Activation and repression by oncogenic MYC shape tumour-specific gene expression profiles. Nature 511 (2014), 483–487.
106. Washkowitz, A.J., Schall, C., Zhang, K., Wurst, W., Floss, T., Mager, J., Papaioannou, V.E., Mga is essential for the survival of pluripotent cells during peri-implantation development. Development 142 (2015), 31–40.
107. Weng, A.P., Millholland, J.M., Yashiro-Ohtani, Y., Arcangeli, M.L., Lau, A., Wai, C., Del Bianco, C., Rodriguez, C.G., Sai, H., Tobias, J., et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20 (2006), 2096–2109.
108. Wilde, B.R., Ayer, D.E., Interactions between Myc and MondoA transcription factors in metabolism and tumourigenesis. Br. J. Cancer 113 (2015), 1529–1533.
109. Yang, G., Hurlin, P.J., MNT and emerging concepts of MNT-MYC antagonism. Genes (Basel), 8, 2017, 10.3390/genes8020083.
110. Zack, T.I., Schumacher, S.E., Carter, S.L., Cherniack, A.D., Saksena, G., Tabak, B., Lawrence, M.S., Zhsng, C.Z., Wala, J., Mermel, C.H., Pan-cancer patterns of somatic copy number alteration. Nat. Genet. 45 (2013), 1134–1140.
111. Zervos, A.S., Gyuris, J., Brent, R., Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites. Cell 72 (1993), 223–232.
112. Zhang, Q., Spears, E., Boone, D.N., Li, Z., Gregory, M.A., Hann, S.R., Domain-specific c-Myc ubiquitylation controls c-Myc transcriptional and apoptotic activity. Proc. Natl. Acad. Sci. USA 110 (2013), 978–983.
113. Zhang, X., Choi, P.S., Francis, J.M., Imielinski, M., Watanabe, H., Cherniack, A.D., Meyerson, M., Identification of focally amplified lineage-specific super-enhancers in human epithelial cancers. Nat. Genet. 48 (2016), 176–182.