Insulinoma-associated protein 1 is a crucial regulator of neuroendocrine differentiation in lung cancer

American Journal of Pathology

Volumn 185, Issue 12, 2015, Pages 3164-3177

  Fujino, Kosuke ^a   Motooka, Yamato ^a   Hassan, Wael A ^a,c   Ali Abdalla, Mohamed O ^b,c   Sato, Yonosuke ^a   Kudoh, Shinji ^a   Hasegawa, Koki ^a   Niimori Kita, Kanako ^a   Kobayashi, Hironori ^d   Kubota, Ichiro ^e   Wakimoto, Joeji ^e   Suzuki, Makoto ^a   Ito, Takaaki ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

^c Suez Canal University Faculty of Medicine   (Egypt)

^d NATIONAL HOSPITAL ORGANIZATION   (Japan)

^e Minami Kyushu Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOGRANIN A; INSULINOMA ASSOCIATED PROTEIN 1; NERVE CELL ADHESION MOLECULE; SMALL INTERFERING RNA; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ASCL1 PROTEIN, HUMAN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; INSM1 PROTEIN, HUMAN; NOTCH1 PROTEIN, HUMAN; NOTCH1 RECEPTOR; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR BRN-2; TRANSCRIPTION FACTOR POU; TUMOR PROTEIN;

ADENOCARCINOMA CELL LINE; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULINOMA; LUNG CANCER; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; PROMOTER REGION; SMALL CELL LUNG CANCER; ADENOCARCINOMA; ANIMAL; APOPTOSIS; CANCER TRANSPLANTATION; CELL PROLIFERATION; GENE SILENCING; GENETICS; INBRED MOUSE STRAIN; LUNG TUMOR; METABOLISM; NEUROSECRETORY CELL; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; XENOGRAFT;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; GENE KNOCKDOWN TECHNIQUES; HETEROGRAFTS; HOMEODOMAIN PROTEINS; HUMANS; LUNG NEOPLASMS; MICE, INBRED STRAINS; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEUROENDOCRINE CELLS; POU DOMAIN FACTORS; RECEPTOR, NOTCH1; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMALL CELL LUNG CARCINOMA;

EID: 84947763328     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.08.018     Document Type: Article

References (40)

1. M.G. Kris, S.I. Benowitz, S. Adams, L. Diller, P. Ganz, M.S. Kahlenberg, Q.T. Le, M. Markman, G.A. Masters, L. Newman, J.C. Obel, A.D. Seidman, S.M. Smith, N. Vogelzang, and N.J. Petrelli Clinical cancer advances 2010: annual report on progress against cancer from the American Society of Clinical Oncology J Clin Oncol 28 2010 5327 5347
2. E. Rodriguez, and R.C. Lilenbaum Small cell lung cancer: past, present, and future Curr Oncol Rep 12 2010 327 334
3. T. Mitsudomi, S. Morita, Y. Yatabe, S. Negoro, I. Okamoto, J. Tsurutani, T. Seto, M. Satouchi, H. Tada, T. Hirashima, K. Asami, N. Katakami, M. Takada, H. Yoshioka, K. Shibata, S. Kudoh, E. Shimizu, H. Saito, S. Toyooka, K. Nakagawa, and M. Fukuoka Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial Lancet Oncol 11 2010 121 128
4. E.L. Kwak, Y.J. Bang, D.R. Camidge, A.T. Shaw, B. Solomon, R.G. Maki, S.H. Ou, B.J. Dezube, P.A. Janne, D.B. Costa, M. Varella-Garcia, W.H. Kim, T.J. Lynch, P. Fidias, H. Stubbs, J.A. Engelman, L.V. Sequist, W. Tan, L. Gandhi, M. Mino-Kenudson, G.C. Wei, S.M. Shreeve, M.J. Ratain, J. Settleman, J.G. Christensen, D.A. Haber, K. Wilner, R. Salgia, G.I. Shapiro, J.W. Clark, and A.J. Iafrate Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer N Engl J Med 363 2010 1693 1703
5. M. May, M. Siegsmund, F. Hammermann, V. Loy, and S. Gunia Prognostic significance of proliferation activity and neuroendocrine differentiation to predict treatment failure after radical prostatectomy Scand J Urol Nephrol 41 2007 375 381
6. R.I. Linnoila, B. Zhao, J.L. DeMayo, B.D. Nelkin, S.B. Baylin, F.J. DeMayo, and D.W. Ball Constitutive achaete-scute homologue-1 promotes airway dysplasia and lung neuroendocrine tumors in transgenic mice Cancer Res 60 2000 4005 4009
7. W.D. Travis Pathology and diagnosis of neuroendocrine tumors: lung neuroendocrine Thorac Surg Clin 24 2014 257 266
8. D.W. Ball, C.G. Azzoli, S.B. Baylin, D. Chi, S. Dou, H. Donis-Keller, A. Cumaraswamy, M. Borges, and B.D. Nelkin Identification of a human achaete-scute homolog highly expressed in neuroendocrine tumors Proc Natl Acad Sci U S A 90 1993 5648 5652
9. N. Pedersen, S. Mortensen, S.B. Sorensen, M.W. Pedersen, K. Rieneck, L.F. Bovin, and H.S. Poulsen Transcriptional gene expression profiling of small cell lung cancer cells Cancer Res 63 2003 1943 1953
10. M. Taniwaki, Y. Daigo, N. Ishikawa, A. Takano, T. Tsunoda, W. Yasui, K. Inai, N. Kohno, and Y. Nakamura Gene expression profiles of small-cell lung cancers: molecular signatures of lung cancer Int J Oncol 29 2006 567 575
11. T. Ito, N. Udaka, T. Yazawa, K. Okudela, H. Hayashi, T. Sudo, F. Guillemot, R. Kageyama, and H. Kitamura Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium Development 127 2000 3913 3921
12. H. Osada, S. Tomida, Y. Yatabe, Y. Tatematsu, T. Takeuchi, H. Murakami, Y. Kondo, Y. Sekido, and T. Takahashi Roles of achaete-scute homologue 1 in DKK1 and E-cadherin repression and neuroendocrine differentiation in lung cancer Cancer Res 68 2008 1647 1655
13. H. Osada, Y. Tatematsu, Y. Yatabe, Y. Horio, and T. Takahashi ASH1 gene is a specific therapeutic target for lung cancers with neuroendocrine features Cancer Res 65 2005 10680 10685
14. J. Ishii, H. Sato, M. Sakaeda, Y. Shishido-Hara, C. Hiramatsu, H. Kamma, H. Shimoyamada, M. Fujiwara, T. Endo, I. Aoki, and T. Yazawa POU domain transcription factor BRN2 is crucial for expression of ASCL1, ND1 and neuroendocrine marker molecules and cell growth in small cell lung cancer Pathol Int 63 2013 158 168
15. th Edition. Edited by Travis WD, Brambilla E, Burke AP, Marx A, Nicholson AG. Lyon, France, IARC, 2015, pp. 63-68
16. W. Hamanaka, N. Motoi, S. Ishikawa, M. Ushijima, K. Inamura, S. Hatano, H. Uehara, S. Okumura, K. Nakagawa, M. Nishio, T. Horai, H. Aburatani, M. Matsuura, A. Iwasaki, and Y. Ishikawa A subset of small cell lung cancer with low neuroendocrine expression and good prognosis: a comparison study of surgical and inoperable cases with biopsy Hum Pathol 45 2014 1045 1056
17. H. Wael, R. Yoshida, S. Kudoh, K. Hasegawa, K. Niimori-Kita, and T. Ito Notch1 signaling controls cell proliferation, apoptosis and differentiation in lung carcinoma Lung Cancer 85 2014 131 140
18. L. Shan, J.C. Aster, J. Sklar, and M.E. Sunday Notch-1 regulates pulmonary neuroendocrine cell differentiation in cell lines and in transgenic mice Am J Physiol Lung Cell Mol Physiol 292 2007 L500 L509
19. V. Sriuranpong, M.W. Borges, C.L. Strock, E.K. Nakakura, D.N. Watkins, C.M. Blaumueller, B.D. Nelkin, and D.W. Ball Notch signaling induces rapid degradation of achaete-scute homolog 1 Mol Cell Biol 22 2002 3129 3139
20. Y. Goto, M.G. De Silva, A. Toscani, B.S. Prabhakar, A.L. Notkins, and M.S. Lan A novel human insulinoma-associated cDNA, IA-1, encodes a protein with "zinc-finger" DNA-binding motifs J Biol Chem 267 1992 15252 15257
21. M.S. Gierl, N. Karoulias, H. Wende, M. Strehle, and C. Birchmeier The zinc-finger factor Insm1 (IA-1) is essential for the development of pancreatic beta cells and intestinal endocrine cells Genes Dev 20 2006 2465 2478
22. H. Wildner, M.S. Gierl, M. Strehle, P. Pla, and C. Birchmeier Insm1 (IA-1) is a crucial component of the transcriptional network that controls differentiation of the sympatho-adrenal lineage Development 135 2008 473 481
23. J.N. Rosenbaum, A. Duggan, and J. Garcia-Anoveros Insm1 promotes the transition of olfactory progenitors from apical and proliferative to basal, terminally dividing and neuronogenic Neural Dev 6 2011 6
24. L.M. Farkas, C. Haffner, T. Giger, P. Khaitovich, K. Nowick, C. Birchmeier, S. Paabo, and W.B. Huttner Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex Neuron 60 2008 40 55
25. J. Xie, T. Cai, H. Zhang, M.S. Lan, and A.L. Notkins The zinc-finger transcription factor INSM1 is expressed during embryo development and interacts with the Cbl-associated protein Genomics 80 2002 54 61
26. M. Zhu, M.B. Breslin, and M.S. Lan Expression of a novel zinc-finger cDNA, IA-1, is associated with rat AR42J cells differentiation into insulin-positive cells Pancreas 24 2002 139 145
27. M.B. Breslin, M. Zhu, and M.S. Lan NeuroD1/E47 regulates the E-box element of a novel zinc finger transcription factor, IA-1, in developing nervous system J Biol Chem 278 2003 38991 38997
28. M.S. Lan, and M.B. Breslin Structure, expression, and biological function of INSM1 transcription factor in neuroendocrine differentiation FASEB J 23 2009 2024 2033
29. M.S. Lan, E.K. Russell, J. Lu, B.E. Johnson, and A.L. Notkins IA-1, a new marker for neuroendocrine differentiation in human lung cancer cell lines Cancer Res 53 1993 4169 4171
30. C.L. Christensen, T. Gjetting, T.T. Poulsen, F. Cramer, J.A. Roth, and H.S. Poulsen Targeted cytosine deaminase-uracil phosphoribosyl transferase suicide gene therapy induces small cell lung cancer-specific cytotoxicity and tumor growth delay Clin Cancer Res 16 2010 2308 2319
31. S.R. Michaelsen, C.L. Christensen, M. Sehested, F. Cramer, T.T. Poulsen, A.V. Patterson, and H.S. Poulsen Single agent- and combination treatment with two targeted suicide gene therapy systems is effective in chemoresistant small cell lung cancer cells J Gene Med 14 2012 445 458
32. R. Yoshida, M. Nagata, H. Nakayama, K. Niimori-Kita, W. Hassan, T. Tanaka, M. Shinohara, and T. Ito The pathological significance of Notch1 in oral squamous cell carcinoma Lab Invest 93 2013 1068 1081
33. A. Augustyn, M. Borromeo, T. Wang, J. Fujimoto, C. Shao, P.D. Dospoy, V. Lee, C. Tan, J.P. Sullivan, J.E. Larsen, L. Girard, C. Behrens, I.I. Wistuba, Y. Xie, M.H. Cobb, A.F. Gazdar, J.E. Johnson, and J.D. Minna ASCL1 is a lineage oncogene providing therapeutic targets for high-grade neuroendocrine lung cancers Proc Natl Acad Sci U S A 111 2014 14788 14793
34. M. Peifer, L. Fernández-Cuesta, M.L. Sos, J. George, D. Seidel, L.H. Kasper, and et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer Nat Genet 44 2012 1104 1110
35. C.M. Rudin, S. Durinck, E.W. Stawiski, J.T. Poirier, Z. Modrusan, D.S. Shames, and et al. Comprehensive genomic analysis identifies SOX2 as a frequently amplified gene in small-cell lung cancer Nat Genet 44 2012 1111 1116
36. R. Meuwissen, S.C. Linn, R.I. Linnoila, J. Zevenhoven, W.J. Mooi, and A. Berns 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
37. L.A. Byers, J. Wang, M.B. Nilsson, J. Fujimoto, P. Saintigny, J. Yordy, U. Giri, M. Peyton, Y.H. Fan, L. Diao, F. Masrorpour, L. Shen, W. Liu, B. Duchemann, P. Tumula, V. Bhardwaj, J. Welsh, S. Weber, B.S. Glisson, N. Kalhor, I.I. Wistuba, L. Girard, S.M. Lippman, G.B. Mills, K.R. Coombes, J.N. Weinstein, J.D. Minna, and J.V. Heymach Proteomic profiling identifies dysregulated pathways in small cell lung cancer and novel therapeutic targets including PARP1 Cancer Discov 2 2012 798 811
38. K.A. Wikenheiser-Brokamp Rb family proteins differentially regulate distinct cell lineages during epithelial development Development 131 2004 4299 4310
39. M.G. Oser, M.J. Niederst, L.V. Sequist, and J.A. Engelman Transformation from non-small-cell lung cancer to small-cell lung cancer: molecular drivers and cells of origin Lancet Oncol 16 2015 e165 e172
40. M.J. Niederst, L.V. Sequist, J.T. Poirier, C.H. Mermel, E.L. Lockerman, A.R. Garcia, R. Katayama, C. Costa, K.N. Ross, T. Moran, E. Howe, L.E. Fulton, H.E. Mulvey, L.A. Bernardo, F. Mohamoud, N. Miyoshi, P.A. VanderLaan, D.B. Costa, P.A. Jänne, D.R. Borger, S. Ramaswamy, T. Shioda, A.J. Iafrate, G. Getz, C.M. Rudin, M. Mino-Kenudson, and J.A. Engelman RB loss in resistant EGFR mutant lung adenocarcinomas that transform to small-cell lung cancer Nat Commun 6 2015 6377