ASCL1 and NEUROD1 Reveal Heterogeneity in Pulmonary Neuroendocrine Tumors and Regulate Distinct Genetic Programs

Cell Reports

Volumn 16, Issue 5, 2016, Pages 1259-1272

  Borromeo, Mark D ^a   Savage, Trisha K ^a   Kollipara, Rahul K ^b   He, Min ^a   Augustyn, Alexander ^b   Osborne, Jihan K ^a   Girard, Luc ^a,b,c   Minna, John D ^a,b,c   Gazdar, Adi F ^a,b,c   Cobb, Melanie H ^a,c   Johnson, Jane E ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; NOTCH RECEPTOR; PROTEIN BCL 2; PROTEIN RET; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR SOX2; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; NEUROD1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CARCINOGENESIS; CELL HETEROGENEITY; CONTROLLED STUDY; DLL3 GENE; E BOX ELEMENT; ENHANCER REGION; FEMALE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOCUS; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOLECULAR PATHOLOGY; MOUSE; MYCL1 GENE; NEWBORN; NFIB GENE; NONHUMAN; ONCOGENE; ONCOGENE MYC; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTO ONCOGENE; RET GENE; SMALL CELL LUNG CANCER; SOX2 GENE; ANIMAL; GENE EXPRESSION; GENETICS; LUNG TUMOR; METABOLISM; NEUROENDOCRINE TUMOR; NEUROSECRETORY CELL; TUMOR CELL LINE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; MALE; MICE; NEUROENDOCRINE CELLS; NEUROENDOCRINE TUMORS; ONCOGENES; PROTO-ONCOGENE PROTEINS C-MYC; SMALL CELL LUNG CARCINOMA; TRANSCRIPTION FACTORS;

EID: 84989936333     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.081     Document Type: Article

References (64)

1. Augustyn, A., Borromeo, M., Wang, T., Fujimoto, J., Shao, C., Dospoy, P.D., Lee, V., Tan, C., Sullivan, J.P., Larsen, J.E., et al. ASCL1 is a lineage oncogene providing therapeutic targets for high-grade neuroendocrine lung cancers. Proc. Natl. Acad. Sci. USA 111 (2014), 14788–14793.
2. Badis, G., Berger, M.F., Philippakis, A.A., Talukder, S., Gehrke, A.R., Jaeger, S.A., Chan, E.T., Metzler, G., Vedenko, A., Chen, X., et al. Diversity and complexity in DNA recognition by transcription factors. Science 324 (2009), 1720–1723.
3. Bertrand, N., Castro, D.S., Guillemot, F., Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3 (2002), 517–530.
4. Borges, M., Linnoila, R.I., van de Velde, H.J., Chen, H., Nelkin, B.D., Mabry, M., Baylin, S.B., Ball, D.W., An achaete-scute homologue essential for neuroendocrine differentiation in the lung. Nature 386 (1997), 852–855.
5. Bunt, J., Hasselt, N.E., Zwijnenburg, D.A., Hamdi, M., Koster, J., Versteeg, R., Kool, M., OTX2 directly activates cell cycle genes and inhibits differentiation in medulloblastoma cells. Int. J. Cancer 131 (2012), E21–32.
6. Carney, D.N., Gazdar, A.F., Bepler, G., Guccion, J.G., Marangos, P.J., Moody, T.W., Zweig, M.H., Minna, J.D., Establishment and identification of small cell lung cancer cell lines having classic and variant features. Cancer Res. 45 (1985), 2913–2923.
7. Castro, D.S., Skowronska-Krawczyk, D., Armant, O., Donaldson, I.J., Parras, C., Hunt, C., Critchley, J.A., Nguyen, L., Gossler, A., Göttgens, B., et al. Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev. Cell 11 (2006), 831–844.
8. Cau, E., Gradwohl, G., Fode, C., Guillemot, F., Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124 (1997), 1611–1621.
9. Christensen, C.L., Kwiatkowski, N., Abraham, B.J., Carretero, J., Al-Shahrour, F., Zhang, T., Chipumuro, E., Herter-Sprie, G.S., Akbay, E.A., Altabef, A., et al. Targeting transcriptional addictions in small cell lung cancer with a covalent CDK7 inhibitor. Cancer Cell 26 (2014), 909–922.
10. Dabir, S., Babakoohi, S., Kluge, A., Morrow, J.J., Kresak, A., Yang, M., MacPherson, D., Wildey, G., Dowlati, A., RET mutation and expression in small-cell lung cancer. J. Thorac. Oncol. 9 (2014), 1316–1323.
11. Dooley, A.L., Winslow, M.M., Chiang, D.Y., Banerji, S., Stransky, N., Dayton, T.L., Snyder, E.L., Senna, S., Whittaker, C.A., Bronson, R.T., et al. Nuclear factor I/B is an oncogene in small cell lung cancer. Genes Dev. 25 (2011), 1470–1475.
12. DuPage, M., Dooley, A.L., Jacks, T., Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat. Protoc. 4 (2009), 1064–1072.
13. Fujino, K., Motooka, Y., Hassan, W.A., Ali Abdalla, M.O., Sato, Y., Kudoh, S., Hasegawa, K., Niimori-Kita, K., Kobayashi, H., Kubota, I., et al. Insulinoma-Associated Protein 1 Is a Crucial Regulator of Neuroendocrine Differentiation in Lung Cancer. Am. J. Pathol. 185 (2015), 3164–3177.
14. Gazdar, A.F., Carney, D.N., Nau, M.M., Minna, J.D., Characterization of variant subclasses of cell lines derived from small cell lung cancer having distinctive biochemical, morphological, and growth properties. Cancer Res. 45 (1985), 2924–2930.
15. Gazdar, A.F., Girard, L., Lockwood, W.W., Lam, W.L., Minna, J.D., Lung cancer cell lines as tools for biomedical discovery and research. J. Natl. Cancer Inst. 102 (2010), 1310–1321.
16. Gazdar, A.F., Savage, T.K., Johnson, J.E., Berns, A., Sage, J., Linnoila, R.I., MacPherson, D., McFadden, D.G., Farago, A., Jacks, T., et al. The comparative pathology of genetically engineered mouse models for neuroendocrine carcinomas of the lung. J. Thorac. Oncol. 10 (2015), 553–564.
17. George, J., Lim, J.S., Jang, S.J., Cun, Y., Ozretić, L., Kong, G., Leenders, F., Lu, X., Fernández-Cuesta, L., Bosco, G., et al. Comprehensive genomic profiles of small cell lung cancer. Nature 524 (2015), 47–53.
18. Goebbels, S., Bode, U., Pieper, A., Funfschilling, U., Schwab, M.H., Nave, K.A., Cre/loxP-mediated inactivation of the bHLH transcription factor gene NeuroD/BETA2. Genesis 42 (2005), 247–252.
19. Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., Nowak, N.J., Joyner, A., Leblanc, G., Hatten, M.E., Heintz, N., A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425 (2003), 917–925.
20. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., Glass, C.K., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38 (2010), 576–589.
21. Henke, R.M., Meredith, D.M., Borromeo, M.D., Savage, T.K., Johnson, J.E., Ascl1 and Neurog2 form novel complexes and regulate Delta-like3 (Dll3) expression in the neural tube. Dev. Biol. 328 (2009), 529–540.
22. 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.
23. Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T., Guillemot, F., Kageyama, R., Kitamura, H., Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127 (2000), 3913–3921.
24. Jiang, T., Collins, B.J., Jin, N., Watkins, D.N., Brock, M.V., Matsui, W., Nelkin, B.D., Ball, D.W., Achaete-scute complex homologue 1 regulates tumor-initiating capacity in human small cell lung cancer. Cancer Res. 69 (2009), 845–854.
25. Johnson, B.E., Russell, E., Simmons, A.M., Phelps, R., Steinberg, S.M., Ihde, D.C., Gazdar, A.F., MYC family DNA amplification in 126 tumor cell lines from patients with small cell lung cancer. J. Cell. Biochem. Suppl. 24 (1996), 210–217.
26. Kamburov, A., Pentchev, K., Galicka, H., Wierling, C., Lehrach, H., Herwig, R., ConsensusPathDB: toward a more complete picture of cell biology. Nucleic Acids Res. 39 (2011), D712–D717.
27. Kim, Y.H., Girard, L., Giacomini, C.P., Wang, P., Hernandez-Boussard, T., Tibshirani, R., Minna, J.D., Pollack, J.R., Combined microarray analysis of small cell lung cancer reveals altered apoptotic balance and distinct expression signatures of MYC family gene amplification. Oncogene 25 (2006), 130–138.
28. Kim, E.J., Battiste, J., Nakagawa, Y., Johnson, J.E., Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol. Cell. Neurosci. 38 (2008), 595–606.
29. Kim, E.J., Ables, J.L., Dickel, L.K., Eisch, A.J., Johnson, J.E., Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS ONE, 6, 2011, e18472.
30. Leung, C.T., Coulombe, P.A., Reed, R.R., Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10 (2007), 720–726.
31. Li, H.J., Johnston, B., Aiello, D., Caffrey, D.R., Giel-Moloney, M., Rindi, G., Leiter, A.B., Distinct cellular origins for serotonin-expressing and enterochromaffin-like cells in the gastric corpus. Gastroenterology 146 (2014), 754–764.
32. 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.
33. Linnoila, R.I., Zhao, B., DeMayo, J.L., Nelkin, B.D., Baylin, S.B., DeMayo, F.J., Ball, D.W., Constitutive achaete-scute homologue-1 promotes airway dysplasia and lung neuroendocrine tumors in transgenic mice. Cancer Res. 60 (2000), 4005–4009.
34. Lovén, J., Hoke, H.A., Lin, C.Y., Lau, A., Orlando, D.A., Vakoc, C.R., Bradner, J.E., Lee, T.I., Young, R.A., Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153 (2013), 320–334.
35. Ma, Q., Kintner, C., Anderson, D.J., Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87 (1996), 43–52.
36. McFadden, D.G., Papagiannakopoulos, T., Taylor-Weiner, A., Stewart, C., Carter, S.L., Cibulskis, K., Bhutkar, A., McKenna, A., Dooley, A., Vernon, A., et al. Genetic and clonal dissection of murine small cell lung carcinoma progression by genome sequencing. Cell 156 (2014), 1298–1311.
37. McLean, C.Y., Bristor, D., Hiller, M., Clarke, S.L., Schaar, B.T., Lowe, C.B., Wenger, A.M., Bejerano, G., GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28 (2010), 495–501.
38. Meuwissen, R., Linn, S.C., Linnoila, R.I., Zevenhoven, J., Mooi, W.J., Berns, A., Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model. Cancer Cell 4 (2003), 181–189.
39. Minoo, P., Su, G., Drum, H., Bringas, P., Kimura, S., Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev. Biol. 209 (1999), 60–71.
40. Myatt, S.S., Lam, E.W., The emerging roles of forkhead box (Fox) proteins in cancer. Nat. Rev. Cancer 7 (2007), 847–859.
41. Neptune, E.R., Podowski, M., Calvi, C., Cho, J.H., Garcia, J.G., Tuder, R., Linnoila, R.I., Tsai, M.J., Dietz, H.C., Targeted disruption of NeuroD, a proneural basic helix-loop-helix factor, impairs distal lung formation and neuroendocrine morphology in the neonatal lung. J. Biol. Chem. 283 (2008), 21160–21169.
42. Osada, H., Tatematsu, Y., Yatabe, Y., Horio, Y., Takahashi, T., ASH1 gene is a specific therapeutic target for lung cancers with neuroendocrine features. Cancer Res. 65 (2005), 10680–10685.
43. Osada, H., Tomida, S., Yatabe, Y., Tatematsu, Y., Takeuchi, T., Murakami, H., Kondo, Y., Sekido, Y., Takahashi, T., Roles of achaete-scute homologue 1 in DKK1 and E-cadherin repression and neuroendocrine differentiation in lung cancer. Cancer Res. 68 (2008), 1647–1655.
44. Osborne, J.K., Larsen, J.E., Shields, M.D., Gonzales, J.X., Shames, D.S., Sato, M., Kulkarni, A., Wistuba, I.I., Girard, L., Minna, J.D., Cobb, M.H., NeuroD1 regulates survival and migration of neuroendocrine lung carcinomas via signaling molecules TrkB and NCAM. Proc. Natl. Acad. Sci. USA 110 (2013), 6524–6529.
45. Pacary, E., Heng, J., Azzarelli, R., Riou, P., Castro, D., Lebel-Potter, M., Parras, C., Bell, D.M., Ridley, A.J., Parsons, M., Guillemot, F., Proneural transcription factors regulate different steps of cortical neuron migration through Rnd-mediated inhibition of RhoA signaling. Neuron 69 (2011), 1069–1084.
46. Park, K.S., Liang, M.C., Raiser, D.M., Zamponi, R., Roach, R.R., Curtis, S.J., Walton, Z., Schaffer, B.E., Roake, C.M., Zmoos, A.F., et al. Characterization of the cell of origin for small cell lung cancer. Cell Cycle 10 (2011), 2806–2815.
47. Pedersen, N., Pedersen, M.W., Lan, M.S., Breslin, M.B., Poulsen, H.S., The insulinoma-associated 1: a novel promoter for targeted cancer gene therapy for small-cell lung cancer. Cancer Gene Ther. 13 (2006), 375–384.
48. Peifer, M., Fernández-Cuesta, L., Sos, M.L., George, J., Seidel, D., Kasper, L.H., Plenker, D., Leenders, F., Sun, R., Zander, T., et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat. Genet. 44 (2012), 1104–1110.
49. Poirier, J.T., Dobromilskaya, I., Moriarty, W.F., Peacock, C.D., Hann, C.L., Rudin, C.M., Selective tropism of Seneca Valley virus for variant subtype small cell lung cancer. J. Natl. Cancer Inst. 105 (2013), 1059–1065.
50. Poirier, J.T., Gardner, E.E., Connis, N., Moreira, A.L., de Stanchina, E., Hann, C.L., Rudin, C.M., DNA methylation in small cell lung cancer defines distinct disease subtypes and correlates with high expression of EZH2. Oncogene 34 (2015), 5869–5878.
51. Roulet, E., Busso, S., Camargo, A.A., Simpson, A.J., Mermod, N., Bucher, P., High-throughput SELEX SAGE method for quantitative modeling of transcription-factor binding sites. Nat. Biotechnol. 20 (2002), 831–835.
52. Rudin, C.M., Durinck, S., Stawiski, E.W., Poirier, J.T., Modrusan, Z., Shames, D.S., Bergbower, E.A., Guan, Y., Shin, J., Guillory, J., et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer. Nat. Genet. 44 (2012), 1111–1116.
53. Saunders, L.R., Bankovich, A.J., Anderson, W.C., Aujay, M.A., Bheddah, S., Black, K., Desai, R., Escarpe, P.A., Hampl, J., Laysang, A., et al. A DLL3-targeted antibody-drug conjugate eradicates high-grade pulmonary neuroendocrine tumor-initiating cells in vivo. Sci. Transl. Med., 7, 2015, 302ra136.
54. Schaffer, B.E., Park, K.S., Yiu, G., Conklin, J.F., Lin, C., Burkhart, D.L., Karnezis, A.N., Sweet-Cordero, E.A., Sage, J., Loss of p130 accelerates tumor development in a mouse model for human small-cell lung carcinoma. Cancer Res. 70 (2010), 3877–3883.
55. Siegel, R., Naishadham, D., Jemal, A., Cancer statistics, 2013. CA Cancer J. Clin. 63 (2013), 11–30.
56. Stergachis, A.B., Neph, S., Reynolds, A., Humbert, R., Miller, B., Paige, S.L., Vernot, B., Cheng, J.B., Thurman, R.E., Sandstrom, R., et al. Developmental fate and cellular maturity encoded in human regulatory DNA landscapes. Cell 154 (2013), 888–903.
57. Stovold, R., Blackhall, F., Meredith, S., Hou, J., Dive, C., White, A., Biomarkers for small cell lung cancer: neuroendocrine, epithelial and circulating tumour cells. Lung Cancer 76 (2012), 263–268.
58. Sutherland, K.D., Proost, N., Brouns, I., Adriaensen, D., Song, J.Y., Berns, A., Cell of origin of small cell lung cancer: inactivation of Trp53 and Rb1 in distinct cell types of adult mouse lung. Cancer Cell 19 (2011), 754–764.
59. Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.
60. Tse, C., Shoemaker, A.R., Adickes, J., Anderson, M.G., Chen, J., Jin, S., Johnson, E.F., Marsh, K.C., Mitten, M.J., Nimmer, P., et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 68 (2008), 3421–3428.
61. Van Lommel, A., Pulmonary neuroendocrine cells (PNEC) and neuroepithelial bodies (NEB): chemoreceptors and regulators of lung development. Paediatr. Respir. Rev. 2 (2001), 171–176.
62. Webb, A.E., Pollina, E.A., Vierbuchen, T., Urbán, N., Ucar, D., Leeman, D.S., Martynoga, B., Sewak, M., Rando, T.A., Guillemot, F., et al. FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep. 4 (2013), 477–491.
63. Whyte, W.A., Orlando, D.A., Hnisz, D., Abraham, B.J., Lin, C.Y., Kagey, M.H., Rahl, P.B., Lee, T.I., Young, R.A., Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153 (2013), 307–319.
64. Zhou, L., Dey, C.R., Wert, S.E., Yan, C., Costa, R.H., Whitsett, J.A., Hepatocyte nuclear factor-3beta limits cellular diversity in the developing respiratory epithelium and alters lung morphogenesis in vivo. Dev. Dyn. 210 (1997), 305–314.