Induction of small cell lung cancer by somatic inactivation of both Trp53 and Rb1 in a conditional mouse model
Open accessAbstract
Small cell lung cancer (SCLC) is a highly aggressive human tumor with a more than 95% mortality rate. Its ontogeny and molecular pathogenesis remains poorly understood. We established a mouse model for neuroendocrine (NE) lung tumors by conditional inactivation of Rb1 and Trp53 in mouse lung epithelial cells. Mice carrying conditional alleles for both Rb1 and Trp53 developed with high incidence aggressive lung tumors with striking morphologic and immunophenotypic similarities to SCLC. Most of these tumors, which we designate MSCLC (murine small cell lung carcinoma), diffusely spread through the lung and gave rise to extrapulmonary metastases. In our model, inactivation of both Rb1 and p53 was a prerequisite for the pathogenesis of SCLC.
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RB is inactivated in more than 90% of human small-cell lung carcinomas.
“RB is inactivated in more than 90% of human small-cell lung carcinomas (SCLC)”
From Cellular mechanisms of tumour suppression by the retinoblastoma gene (2008) · cites this paper as [24]
Mouse genetic studies confirm that RB is crucial in preventing initiation of small-cell lung carcinoma.
“mouse genetic studies have confirmed that RB is crucial in preventing the initiation of this lung cancer sub-type24”
From Cellular mechanisms of tumour suppression by the retinoblastoma gene (2008) · cites this paper as [24]
Combined loss of Trp53 and Rb produces more tumours in mutant mice.
“When loss of Trp53 and Rb are combined, more tumours develop in mutant mice24,147–149 but it becomes difficult to dissect the respective roles of these two potent tumour suppressors.”
From Cellular mechanisms of tumour suppression by the retinoblastoma gene (2008) · cites this paper as [24]
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Bhattacharjee, A., Richards, W. G., Staunton, J. E., Li, C., Monti, S., Vasa, P. P., Ladd, C., Beheshti, J., Bueno, R., Gillette, M. A., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191502998 · Cited by 2,540 · see citing works
Neuroblastoma: biological insights into a clinical enigma
Brodeur, G. M. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1014 · Cited by 2,161 · see citing works
Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-rasPreprint
Jackson, E. L., Willis, N. A., Mercer, K. L., Bronson, R. T., Crowley, D. G., Montoya, R., Jacks, T., & Tuveson, D. A. (2001) · Genes & Development · doi:10.1101/gad.943001 · Cited by 1,877 · see citing works
Effects of an Rb mutation in the mouse
Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A., & Weinberg, R. A. (1992) · Nature · doi:10.1038/359295a0 · Cited by 1,755 · see citing works
The RB and p53 pathways in cancer
Sherr, C. J., & McCormick, F. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00102-2 · Cited by 1,690 · see citing works
Simplified mammalian DNA isolation procedure
Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R., & Berns, A. J. M. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.15.4293 · Cited by 1,497 · see citing works
Self-citationDiversity of gene expression in adenocarcinoma of the lung
Garber, M. E., Troyanskaya, O. G., Schlüns, K., Petersen, S., Thäsler, Z., Pacyna-Gengelbach, M., van de Rijn, M., Rosen, G., Perou, C. M., Whyte, R. I., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.241500798 · Cited by 1,301 · see citing works
Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer
Watkins, D. N., Berman, D. M., Burkholder, S. G., Wang, B., Beachy, P. A., & Baylin, S. B. (2003) · Nature · doi:10.1038/nature01493 · Cited by 1,082 · see citing works
Jonkers, J., Meuwissen, R. L. J., van der Gulden, H. M. L., Peterse, H. L., van der Valk, M., & Berns, A. J. M. (2001) · Nature Genetics · doi:10.1038/ng747 · Cited by 1,053 · see citing works
Self-citationMarino, S., Vooijs, M., van der Gulden, H., Jonkers, J., & Berns, A. (2000) · Genes & Development · doi:10.1101/gad.14.8.994 · Cited by 920 · see citing works
Self-citationThe retinoblastoma tumour suppressor in development and cancer
Classon, M., & Harlow, E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc950 · Cited by 738 · see citing works
Sage, J., Mulligan, G. J., Attardi, L. D., Miller, A., Chen, S., Williams, B., Theodorou, E., & Jacks, T. (2000) · Genes & Development · doi:10.1101/gad.843200 · Cited by 582 · see citing works
Minna, J. D., Roth, J. A., & Gazdar, A. F. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00027-2 · Cited by 553 · see citing works
Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins
Lasorella, A., Noseda, M., Beyna, M., & Iavarone, A. (2000) · Nature · doi:10.1038/35036504 · Cited by 497 · see citing works
The Developmental Biology of Brain Tumors
Wechsler‐Reya, R. J., & Scott, M. P. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.385 · Cited by 458 · see citing works
An achaete-scute homologue essential for neuroendocrine differentiation in the lung
Borges, M. W., Linnoila, R. I., van de Velde, H. J. K., Chen, H., Nelkin, B. D., Mabry, M. H., Baylin, S. B., & Ball, D. W. (1997) · Nature · doi:10.1038/386852a0 · Cited by 455 · see citing works
Self-citationReynolds, S. D., Giangreco, A., Power, J. H. T., & Stripp, B. R. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64727-x · Cited by 449 · see citing works
Molecular genetics of small cell lung carcinoma
Wistuba, I. I., Gazdar, A. F., & Minna, J. D. (2001) · Seminars in Oncology · doi:10.1016/s0093-7754(01)90072-7 · Cited by 421 · see citing works
Dannenberg, J.-H., van Rossum, A., Schuijff, L., & te Riele, H. (2000) · Genes & Development · doi:10.1101/gad.847700 · Cited by 413 · see citing works
The retinoblastoma gene family in differentiation and development
Lipinski, M. M., & Jacks, T. (1999) · Oncogene · doi:10.1038/sj.onc.1203244 · Cited by 404 · see citing works
Ito, T., Udaka, N., Yazawa, T., Okudela, K., Hayashi, H., Sudo, T., Guillemot, F., Kageyama, R., & Kitamura, H. (2000) · Development · doi:10.1242/dev.127.18.3913 · Cited by 403 · see citing works
Cooperative tumorigenic effects of germline mutations in Rb and p53
Williams, B. O., Remington, L., Albert, D. M., Mukai, S., Bronson, R. T., & Jacks, T. (1994) · Nature Genetics · doi:10.1038/ng0894-480 · Cited by 367 · see citing works
Ordóǹez, N. G. (2000) · The American Journal of Surgical Pathology · doi:10.1097/00000478-200009000-00004 · Cited by 341 · see citing works
Molecular Genetics of Lung Cancer
Sekido, Y., Fong, K. M., & Minna, J. D. (2003) · Annual Review of Medicine · doi:10.1146/annurev.med.54.101601.152202 · Cited by 318 · see citing works
N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling
Cavallaro, U., Niedermeyer, J., Fuxa, M., & Christofori, G. (2001) · Nature Cell Biology · doi:10.1038/35083041 · Cited by 307 · see citing works
The p53-deficient mouse: a model for basic and applied cancer studies
Donehower, L. A. (1996) · Seminars in Cancer Biology · doi:10.1006/scbi.1996.0035 · Cited by 268 · see citing works
Developmental rescue of an embryonic‐lethal mutation in the retinoblastoma gene in chimeric mice.
Robanus-Maandag, E. C., van der Valk, M., Vlaar, M., Feltkamp, C. A., O’Brien, J. M., van ROON, M. A., van der Lugt, N. M. T., Berns, A. J. M., & Riele, H. T. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06746.x · Cited by 248 · see citing works
Self-citationLung cancer in Europe in 2000: epidemiology, prevention, and early detection
Tyczynski, J. E., Bray, F., & Parkin, D. M. (2003) · The Lancet Oncology · doi:10.1016/s1470-2045(03)00960-4 · Cited by 239 · see citing works
Reynolds, S. D., Hong, K. U., Giangreco, A., Mango, G. W., Guron, C., Morimoto, Y., & Stripp, B. R. (2000) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.2000.278.6.l1256 · Cited by 238 · see citing works
Meuwissen, R. L. J., Linn, S. C., van der Valk, M., Mooi, W. J., & Berns, A. J. M. (2001) · Oncogene · doi:10.1038/sj.onc.1204837 · Cited by 200 · see citing works
Self-citationIdentification of a human achaete-scute homolog highly expressed in neuroendocrine tumors.
Ball, D. W., Azzoli, C. G., Baylin, S. B., Chi, D., Dou, S., Donis-keller, H., Cumaraswamy, A., Borges, M. W., & Nelkin, B. D. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.12.5648 · Cited by 177 · see citing works
Molecular and Genetic Aspects of Lung Cancer
Rom, W. N., Hay, J. G., Lee, T. C., Jiang, Y., & Tchou-Wong, K.-M. (2000) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.161.4.9908012 · Cited by 162 · see citing works
Shibayama, T., Ueoka, H., Nishii, K., Kiura, K., Tabata, M., 宮武, 和., Kitajima, T., & Harada, M. (2001) · Lung Cancer · doi:10.1016/s0169-5002(00)00205-1 · Cited by 150 · see citing works
Burstein, D., Wu, M., Sabo, E., Wang, B., Miller, L. K., Gan, L., & Gil, J. (2003) · American Journal of Clinical Pathology · doi:10.1309/p5ab-r5kq-89rn-jtfh · Cited by 147 · see citing works
Flp-mediated tissue-specific inactivation of the retinoblastoma tumor suppressor gene in the mouse
Vooijs, M., van der Valk, M., Riele, H. T., & Berns, A. J. M. (1998) · Oncogene · doi:10.1038/sj.onc.1202169 · Cited by 140 · see citing works
Self-citationLinnoila, R. I., Zhao, B., DeMayo, J. L., Nelkin, B. D., Baylin, S. B., DeMayo, F. J., & Ball, D. W. (2000) · PubMed · Cited by 125 · see citing works
Self-citationChemotherapy for small cell lung cancer
Sandler, A. B. (2003) · Seminars in Oncology · doi:10.1053/sonc.2003.50012 · Cited by 116 · see citing works
Wuenschell, C. W., Sunday, M. E., Singh, G., Minoo, P., Slavkin, H. C., & Warburton, D. (1996) · Journal of Histochemistry & Cytochemistry · doi:10.1177/44.2.8609367 · Cited by 109 · see citing works
Jögi, A., Persson, P., Grynfeld, A., Påhlman, S., & Axelson, H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m107713200 · Cited by 96 · see citing works
Toma, J. G., El-Bizri, H., Barnabé‐Heider, F., Aloyz, R. S., & Miller, F. D. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07648.2000 · Cited by 95 · see citing works
Wu, M., Wang, B., Gil, J., et al. (2003) · American Journal of Clinical Pathology · doi:10.1309/p5abr5kq89rnjtfh · Cited by 82 · see citing works
Mechanism of Retinoblastoma Gene Inactivation in the Spectrum of Neuroendocrine Lung Tumors
Gouyer, V., Gazzéri, S., Bolon, I., Drevet, C., Brambilla, C., & Brambilla, E. M. (1998) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.18.2.3008 · Cited by 77 · see citing works
Pathology of small-cell lung cancer
Junker, K., Wiethege, T., & Müller, K. M. (2000) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/pl00008483 · Cited by 70 · see citing works
Molecular and cellular biology of small cell lung cancer
Sattler, M., & Salgia, R. (2003) · Seminars in Oncology · doi:10.1053/sonc.2003.50019 · Cited by 70 · see citing works
Ferrari, L., Seregni, E. C., Bajetta, E., Martinetti, A., & Bombardieri, E. (1999) · PubMed · Cited by 56 · see citing works
Magdaleno, S. M., Wang, G., Mireles, V. L., Ray, M. K., Finegold, M. J., & DeMayo, F. J. (1997) · PubMed · Cited by 45 · see citing works
Calcitonin driven v-Ha-ras induces multilineage pulmonary epithelial hyperplasias and neoplasms
Sunday, M. E., Haley, K. J., Sikorski, K. A., Graham, S. A., Emanuel, R. L., Zhang, F., Mu, Q., Shahsafaei, A., & Hatzis, D. (1999) · Oncogene · doi:10.1038/sj.onc.1202810 · Cited by 34 · see citing works
Kobayashi, S., Okada, S., Hasumi, T., Sato, N., & Fujimura, S. (1999) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.189.37 · Cited by 8 · see citing works
Flagged first, then by citations
1 of the 49 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Comprehensive genomic profiles of small cell lung cancer
George, J., Lim, J. S., Jang, S. J., Cun, Y., Ozretić, L., Kong, G., Leenders, F., Lu, X. L., Fernandez‐Cuesta, L., Bosco, G., et al. (2015) · Nature · doi:10.1038/nature14664 · Cited by 2,325 · see citing works
Rudin, C. M., Brambilla, E. M., Finn, C. F., & Sage, J. (2021) · Nature Reviews Disease Primers · doi:10.1038/s41572-020-00235-0 · Cited by 1,632 · see citing works
Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer
Peifer, M., Fernandez‐Cuesta, L., Sos, M. L., George, J., Seidel, D., Kasper, L. H., Plenker, D., Leenders, F., Sun, R., Zander, T., et al. (2012) · Nature Genetics · doi:10.1038/ng.2396 · Cited by 1,390 · see citing works
Molecular subtypes of small cell lung cancer: a synthesis of human and mouse model data
Rudin, C. M., Poirier, J. T., Byers, L. A., Dive, C., Dowlati, A., George, J., Heymach, J. V., Johnson, J. E. B., Lehman, J. M., MacPherson, D. P., et al. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0133-9 · Cited by 1,251 · see citing works
LKB1 modulates lung cancer differentiation and metastasis
Ji, H., Ramsey, M. R., Hayes, D. N., Fan, C., McNamara, K., Kozlowski, P., Torrice, C., Wu, M. C., Shimamura, T., Perera, S. A., et al. (2007) · Nature · doi:10.1038/nature06030 · Cited by 1,064 · see citing works
Cellular mechanisms of tumour suppression by the retinoblastoma gene
Burkhart, D. L., & Sage, J. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2399 · Cited by 974 · see citing works
Oser, M. G., Niederst, M. J., Sequist, L. V. D., & Engelman, J. A. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(14)71180-5 · Cited by 939 · see citing works
Small-cell lung cancer: what we know, what we need to know and the path forward
Gazdar, A. F., Bunn, P. A., & Minna, J. D. (2017) · Nature reviews. Cancer · doi:10.1038/nrc.2017.87 · Cited by 900 · see citing works
Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase
DuPage, M. J. P., Dooley, A. L., & Jacks, T. (2009) · Nature Protocols · doi:10.1038/nprot.2009.95 · Cited by 862 · see citing works
Maximizing mouse cancer models
Frese, K. K., & Tuveson, D. A. (2007) · Nature reviews. Cancer · doi:10.1038/nrc2192 · Cited by 711 · see citing works
Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer
Hodgkinson, C. L., Morrow, C. J., Li, Y., Metcalf, R. L., Rothwell, D. G., Trapani, F., Polański, R., Burt, D. J., Simpson, K., Morris, K. L., et al. (2014) · Nature Medicine · doi:10.1038/nm.3600 · Cited by 695 · see citing works
Burr, M. L., Sparbier, C. E., Chan, K. L., Chan, Y.-C., Kersbergen, A. J., Lam, E. Y. N., Azidis-Yates, E., Vassiliadis, D., Bell, C. C., Gilan, O., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.08.008 · Cited by 657 · see citing works
Small cell lung cancer: Where do we go from here?
Byers, L. A., & Rudin, C. M. (2014) · Cancer · doi:10.1002/cncr.29098 · Cited by 631 · see citing works
Pocket proteins and cell cycle control
Cobrinik, D. (2005) · Oncogene · doi:10.1038/sj.onc.1208619 · Cited by 601 · see citing works
Mollaoglu, G., Guthrie, M. R., Böhm, S., Brägelmann, J., Can, İ., Ballieu, P. M., Marx, A., George, J., Heinen, C., Chalishazar, M. D., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2016.12.005 · Cited by 594 · see citing works
BACH1 Stabilization by Antioxidants Stimulates Lung Cancer Metastasis
Wiel, C., Le Gal, K., Ibrahim, M. X., Jahangir, C. A., Kashif, M., Yao, H., Ziegler, D. V., Xu, X., Ghosh, T., Mondal, T., et al. (2019) · Cell · doi:10.1016/j.cell.2019.06.005 · Cited by 579 · see citing works
The Differential Effects of Mutant <i>p53</i> Alleles on Advanced Murine Lung Cancer
Jackson, E. L., Olive, K. P., Tuveson, D. A., Bronson, R., Crowley, D., Brown, M., & Jacks, T. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-2193 · Cited by 553 · see citing works
Yachida, S., Vakiani, E., White, C. M., Zhong, Y., Saunders, T., Morgan, R., de Wilde, R. F., Maitra, A., Hicks, J. L., Marzo, A. M. D., et al. (2012) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3182417d36 · Cited by 536 · see citing works
Sutherland, K. D., Proost, N., Brouns, I., Adriaensen, D., Song, J.-Y., & Berns, A. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.04.019 · Cited by 534 · see citing works
Self-citationIreland, A. S., Micinski, A. M., Kastner, D. W., Guo, B., Wait, S. J., Spainhower, K. B., Conley, C. C., Chen, O. S., Guthrie, M. R., Soltero, D., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.05.001 · Cited by 506 · see citing works
Borromeo, M. D., Savage, T. K., Kollipara, R. K., He, M. Y., Augustyn, A., Osborne, J. K., Girard, L., Minna, J. D., Gazdar, A. F., Cobb, M. H., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.081 · Cited by 502 · see citing works
Unravelling the biology of SCLC: implications for therapy
Sabari, J. K., Lok, B. H., Laird, J. H., Poirier, J. T., & Rudin, C. M. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.71 · Cited by 488 · see citing works
Epidermal Growth Factor Receptor Tyrosine Kinase Inhibitor–Resistant Disease
Ohashi, K., Maruvka, Y. E., Michor, F., & Pao, W. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.43.3912 · Cited by 467 · see citing works
Boire, A. A., Brastianos, P. K., Garzia, L., & Valiente, M. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0220-y · Cited by 455 · see citing works
INK4a/ARF: A multifunctional tumor suppressor locus
Sharpless, N. E. (2005) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/j.mrfmmm.2004.08.021 · Cited by 442 · see citing works
Targeting Transcriptional Addictions in Small Cell Lung Cancer with a Covalent CDK7 Inhibitor
Christensen, C. L., Kwiatkowski, N. P., Abraham, B. J., Carretero, J., Al‐Shahrour, F., Zhang, T., Chipumuro, E., Herter-Sprie, G. S., Akbay, E. A., Altabef, A. B., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.019 · Cited by 435 · see citing works
Lung Cancers: Molecular Characterization, Clonal Heterogeneity and Evolution, and Cancer Stem Cells
Testa, U., Castelli, G., & Pelosi, E. (2018) · Cancers · doi:10.3390/cancers10080248 · Cited by 406 · see citing works
Megyesfalvi, Z., Gay, C. M., Popper, H., Pirker, R., Ostoros, G., Heeke, S., Lang, C., Höetzenecker, K., Solta, A., Boettiger, K., et al. (2023) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21785 · Cited by 390 · see citing works
A Functional Role for Tumor Cell Heterogeneity in a Mouse Model of Small Cell Lung Cancer
Calbó, J., van Montfort, E. H. N., Proost, N., van Drunen, E., Beverloo, H. B., Meuwissen, R. L. J., & Berns, A. J. M. (2011) · Cancer Cell · doi:10.1016/j.ccr.2010.12.021 · Cited by 366 · see citing works
Self-citationNfib Promotes Metastasis through a Widespread Increase in Chromatin Accessibility
Denny, S. K., Yang, D., Chuang, C.-H., Brady Jennifer, J., Lim, J. S., Grüner, B. M., Chiou, S., Schep, A. N., Baral, J., Hamard, C., et al. (2016) · Cell · doi:10.1016/j.cell.2016.05.052 · Cited by 358 · see citing works
Contributions of Human Tumor Xenografts to Anticancer Drug Development
Sausville, E. A., & Burger, A. M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3627 · Cited by 348 · see citing works
Rb Loss Is Characteristic of Prostatic Small Cell Neuroendocrine Carcinoma
Tan, H., Sood, A., Rahimi, H. A., Wang, W., Gupta, N., Hicks, J. L., Mosier, S. L., Gocke, C. D., Epstein, J. I., Netto, G. J., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-1982 · Cited by 344 · see citing works
Jeong, Y., Hoang, N. T., Lovejoy, A. F., Stehr, H., Newman, A. M., Gentles, A. J., Kong, W. W., Truong, D., Martin, S. A., Chaudhuri, A. A., et al. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0127 · Cited by 348 · see citing works
Classification of Proliferative Pulmonary Lesions of the Mouse
Nikitin, A. Y., Alcaraz, A., Anver, M. R., Bronson, R. T., Cardiff, R. D., Dixon, D., Fraire, A. E., Gabrielson, E. W., Gunning, W. T., Haines, D. C., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3376 · Cited by 334 · see citing works
Self-citationSynergy of p53 and Rb Deficiency in a Conditional Mouse Model for Metastatic Prostate Cancer
Zhou, Z., Flesken‐Nikitin, A., Corney, D. C., Wang, W., Goodrich, D. W., Roy‐Burman, P., & Nikitin, A. Y. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0486 · Cited by 315 · see citing works
Song, H., Yao, E., Lin, C., Gacayan, R., Chen, M.-H., & Chuang, P. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207238109 · Cited by 313 · see citing works
The Evolving Landscape of Brain Metastasis
Valiente, M., Ahluwalia, M. S., Boire, A. A., Brastianos, P. K., Goldberg, S. B., Lee, E. Q., Rhun, É. L., Preusser, M., Winkler, F., & Soffietti, R. (2018) · Trends in cancer · doi:10.1016/j.trecan.2018.01.003 · Cited by 310 · see citing works
Stem Cells and Cell Therapies in Lung Biology and Lung Diseases
Weiss, D. J., Kolls, J. K., Ortiz, L. A., Panoskaltsis‐Mortari, A., & Prockop, D. J. (2008) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200804-037dw · Cited by 308 · see citing works
Mouse models for human lung cancerPreprint
Meuwissen, R. L. J., & Berns, A. J. M. (2005) · Genes & Development · doi:10.1101/gad.1284505 · Cited by 301 · see citing works
Self-citationA Translational View of the Molecular Pathogenesis of Lung Cancer
Sato, M., Shames, D. S., Gazdar, A. F., & Minna, J. D. (2007) · Journal of Thoracic Oncology · doi:10.1097/01.jto.0000263718.69320.4c · Cited by 296 · see citing works
Genetic and Clonal Dissection of Murine Small Cell Lung Carcinoma Progression by Genome Sequencing
McFadden, D. G., Papagiannakopoulos, T. Y., Taylor-Weiner, A. N., Stewart, C., Carter, S. L., Cibulskis, K., Bhutkar, A. J., McKenna, A., Dooley, A. L., Vernon, A. N., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.031 · Cited by 289 · see citing works
Tracing the cellular origin of cancer
Blanpain, C. (2013) · Nature Cell Biology · doi:10.1038/ncb2657 · Cited by 275 · see citing works
Smoking, p53 Mutation, and Lung Cancer
Gibbons, D. L., Byers, L. A., & Kurie, J. M. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0539 · Cited by 255 · see citing works
LOSS OF P130 ACCELERATES TUMOR DEVELOPMENT IN A MOUSE MODEL FOR HUMAN SMALL CELL LUNG CARCINOMA
Schaffer, B. E., Park, K.-S., Yiu, G., Conklin, J. F., Lin, C., Burkhart, D. L., Karnezis, A., Sweet-Cordero, A., & Sage, J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-4228 · Cited by 235 · see citing works
Poirier, J. T., Gardner, E. E., Connis, N., Moreira, A. L., de Stanchina, E., Hann, C. L., & Rudin, C. M. (2015) · Oncogene · doi:10.1038/onc.2015.38 · Cited by 247 · see citing works
Origins, genetic landscape, and emerging therapies of small cell lung cancerPreprint
Semenova, E. A., Nagel, R., & Berns, A. J. M. (2015) · Genes & Development · doi:10.1101/gad.263145.115 · Cited by 247 · see citing works
Self-citationA crucial requirement for Hedgehog signaling in small cell lung cancer
Park, K.-S., Martelotto, L. G., Peifer, M., Sos, M. L., Karnezis, A. N., Mahjoub, M. R., Bernard, K., Conklin, J. F., Szczepny, A., Yuan, J., et al. (2011) · Nature Medicine · doi:10.1038/nm.2473 · Cited by 247 · see citing works
Molecular Biology of Lung Cancer: Clinical Implications
Larsen, J. E., & Minna, J. D. (2011) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2011.08.003 · Cited by 247 · see citing works
An Organoid Biobank of Neuroendocrine Neoplasms Enables Genotype-Phenotype Mapping
Kawasaki, K., Toshimitsu, K., Matano, M., Fujita, M., Fujii, M., Togasaki, K., Ebisudani, T., Shimokawa, M., Takano, A., Takahashi, S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.023 · Cited by 238 · see citing works
Mechanisms of small cell lung cancer metastasis
Ko, J. H., Winslow, M. M., & Sage, J. (2020) · EMBO Molecular Medicine · doi:10.15252/emmm.202013122 · Cited by 232 · see citing works
Biology and evolution of poorly differentiated neuroendocrine tumors
Rickman, D. S., Beltran, H., Demichelis, F., & Rubin, M. A. (2017) · Nature Medicine · doi:10.1038/nm.4341 · Cited by 230 · see citing works
Small Cell Lung Cancer: Will Recent Progress Lead to Improved Outcomes?
Pietanza, M. C., Byers, L. A., Minna, J. D., & Rudin, C. M. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-2958 · Cited by 228 · see citing works
Characterization of the cell of origin for small cell lung cancer
Park, K.-S., Liang, M., Raiser, D. M., Zamponi, R., Roach, R. R., Curtis, S. J., Walton, Z. E., Schaffer, B. E., Roake, C. M., Zmoos, A., et al. (2011) · Cell Cycle · doi:10.4161/cc.10.16.17012 · Cited by 225 · see citing works
Chiaverotti, T. A., Couto, S. S., Donjacour, A. A., Mao, J., Nagase, H., Cardiff, R. D., Cunha, G. R., & Balmain, A. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2008.070602 · Cited by 228 · see citing works
Wang, Q., Gumus, Z. H., Colarossi, C., Memeo, L., Wang, X., Kong, C. Y., & Boffetta, P. (2022) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2022.10.002 · Cited by 226 · see citing works
Kim, S. Y., Park, H. S.-M., & Chiang, A. C. (2025) · JAMA · doi:10.1001/jama.2025.0560 · Cited by 219 · see citing works
Molecular biology of lung cancer: Clinical implications
Fong, K. M., & Minna, J. D. (2002) · Clinics in Chest Medicine · doi:10.1016/s0272-5231(03)00062-5 · Cited by 210 · see citing works
Functional facets of the pulmonary neuroendocrine system
Linnoila, R. I. (2006) · Laboratory Investigation · doi:10.1038/labinvest.3700412 · Cited by 207 · see citing works
Self-citationCancer cell plasticity: Impact on tumor progression and therapy response
da Silva-Diz, V., Lorenzo-Sanz, L., Bernat‐Peguera, A., Lopez-Cerda, M., & Muñoz, P. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.08.009 · Cited by 202 · see citing works
Molecular heterogeneity in lung cancer: from mechanisms of origin to clinical implications
Marino, F. Z., Bianco, R., Accardo, M., Ronchi, A., Cozzolino, I., Morgillo, F., Rossi, G., & Franco, R. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.34739 · Cited by 203 · see citing works
Chinnam, M., & Goodrich, D. W. (2011) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-380916-2.00005-x · Cited by 200 · see citing works
Oronsky, B. T., Reid, T. R., Oronsky, A. L., & Carter, C. A. (2017) · Neoplasia · doi:10.1016/j.neo.2017.07.007 · Cited by 197 · see citing works
Crebbp Loss Drives Small Cell Lung Cancer and Increases Sensitivity to HDAC Inhibition
Jia, D., Augert, A., Kim, D. W., Eastwood, E., Wu, N., Ibrahim, A. H., Kim, K., Dunn, C. T., Pillai, S. P. S., Gazdar, A. F., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-0385 · Cited by 195 · see citing works
Jiang, T., Collins, B. J., Jin, N. Y., Watkins, D. N., Brock, M. V., Matsui, W. H., Nelkin, B. D., & Ball, D. W. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2762 · Cited by 186 · see citing works
Treatment advances in small cell lung cancer (SCLC)
Waqar, S. N., & Morgensztern, D. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.06.002 · Cited by 184 · see citing works
Bunn, P. A., Minna, J. D., Augustyn, A., Gazdar, A. F., Ouadah, Y., Krasnow, M. A., Berns, A. J. M., Brambilla, E. M., Rekhtman, N., Massion, P. P., et al. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.01.012 · Cited by 180 · see citing works
Self-citationMeder, L., König, K., Ozretić, L., Schultheis, A. M., Ueckeroth, F., Ade, C. P., Albus, K., Boehm, D., Rommerscheidt‐Fuss, U., Florin, A., et al. (2015) · International Journal of Cancer · doi:10.1002/ijc.29835 · Cited by 179 · see citing works
Sutherland, K. D., & Berns, A. J. M. (2010) · Molecular Oncology · doi:10.1016/j.molonc.2010.05.002 · Cited by 176 · see citing works
Self-citationPearson, J. D., Huang, K., Pacal, M., McCurdy, S. R., Lü, S., Aubry, A., Yu, T., Wadosky, K. M., Zhang, L., Wang, T., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.06.016 · Cited by 172 · see citing works
Cells Lacking the RB1 Tumor Suppressor Gene Are Hyperdependent on Aurora B Kinase for Survival
Oser, M. G., Fonseca, R., Chakraborty, A. A., Brough, R., Spektor, A., Jennings, R. B., Flaifel, A., Novak, J. S. S., Gulati, A., Buss, E. J., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-0389 · Cited by 174 · see citing works
New Approaches to SCLC Therapy: From the Laboratory to the Clinic
Poirier, J. T., George, J., Owonikoko, T. K., Berns, A. J. M., Brambilla, E. M., Byers, L. A., Carbone, D. P., Chen, H. J., Christensen, C. L., Dive, C., et al. (2020) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2020.01.016 · Cited by 173 · see citing works
Self-citationNuclear factor I/B is an oncogene in small cell lung cancerPreprint
Dooley, A. L., Winslow, M. M., Chiang, D. Y., Banerji, S. O., Stransky, N., Dayton, T. L., Snyder, E. L., Senna, S., Whittaker, C. A., Bronson, R. T., et al. (2011) · Genes & Development · doi:10.1101/gad.2046711 · Cited by 172 · see citing works
Simpson, K., Stoney, R., Frese, K. K., Simms, N., Rowe, W., Pearce, S. P., Humphrey, S., Booth, L., Morgan, D., Dynowski, M., et al. (2020) · Nature Cancer · doi:10.1038/s43018-020-0046-2 · Cited by 173 · see citing works
Meder, L., Schuldt, P., Thelen, M., Schmitt, A., Dietlein, F., Klein, S., Borchmann, S., Wennhold, K., Vlašić, I., Oberbeck, S., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2176 · Cited by 172 · see citing works
Lung Cancer and Lung Stem Cells
Giangreco, A., Groot, K. R., & Janes, S. M. (2006) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200607-984pp · Cited by 170 · see citing works
Preclinical Murine Models for Lung Cancer: Clinical Trial Applications
Kellar, A., Egan, C., & Morris, D. G. (2015) · BioMed Research International · doi:10.1155/2015/621324 · Cited by 170 · see citing works
Lung Cancer Signatures in Plasma Based on Proteome Profiling of Mouse Tumor Models
Taguchi, A., Politi, K. A., Pitteri, S. J., Lockwood, W. W., Faça, V. M., Kelly‐Spratt, K. S., Wong, C., Zhang, Q. H., Chin, A. P., Park, K.-S., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.08.007 · Cited by 167 · see citing works
The role of p53 in treatment responses of lung cancer
Viktorsson, K., Petris, L. D., & Lewensohn, R. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.03.192 · Cited by 161 · see citing works
Intertumoral Heterogeneity in SCLC Is Influenced by the Cell Type of Origin
Yang, D., Denny, S. K., Greenside, P., Chaikovsky, A. C., Brady Jennifer, J., Ouadah, Y., Granja, J. M., Jahchan, N. S., Lim, J. S., Kwok, S., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0987 · Cited by 158 · see citing works
Semenova, E. A., Kwon, M.-C., Monkhorst, K., Song, J., Bhaskaran, R., Krijgsman, O., Kuilman, T., Peters, D. D. G. C., Buikhuisen, W. A., Smit, E. F., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.020 · Cited by 159 · see citing works
Self-citationChuang, C.-H., Greenside, P., Rogers, Z. N., Brady Jennifer, J., Yang, D., Ma, R. K., Caswell, D. R., Chiou, S., Winters, A. F., Grüner, B. M., et al. (2017) · Nature Medicine · doi:10.1038/nm.4285 · Cited by 151 · see citing works
Kwon, M.-C., & Berns, A. J. M. (2013) · Molecular Oncology · doi:10.1016/j.molonc.2013.02.010 · Cited by 145 · see citing works
Self-citationIntravital microscopy: new insights into metastasis of tumors
Beerling, E., Ritsma, L., Vrisekoop, N., Derksen, P. W. B., & van Rheenen, J. (2011) · Journal of Cell Science · doi:10.1242/jcs.072728 · Cited by 148 · see citing works
Lung Cancer Subtypes Generate Unique Immune Responses
Busch, S., Hanke, M. L., Kargl, J., Metz, H. E., MacPherson, D. P., & Houghton, A. M. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600576 · Cited by 147 · see citing works
Rogers, Z. N., McFarland, C. D., Winters, I. P., Naranjo, S., Chuang, C.-H., Petrov, D. A., & Winslow, M. M. (2017) · Nature Methods · doi:10.1038/nmeth.4297 · Cited by 139 · see citing works
Kim, C. H., Lee, Y.-C. A., Hung, R. J., McNallan, S. R., Coté, M. L., Lim, W., Chang, S., Kim, J. H., Ugolini, D., Chen, Y., et al. (2014) · International Journal of Cancer · doi:10.1002/ijc.28835 · Cited by 147 · see citing works
Ferroptosis response segregates small cell lung cancer (SCLC) neuroendocrine subtypes
Bebber, C. M., Thomas, E. S., Stroh, J., Chen, Z., Androulidaki, A., Schmitt, A., Höhne, M. N., Stüker, L., Alves, C. D. P., Khonsari, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22336-4 · Cited by 143 · see citing works
Intracellular and extracellular TGF-β signaling in cancer: some recent topics
Miyazono, K., Katsuno, Y., Koinuma, D., Ehata, S., & Morikawa, M. (2018) · Frontiers of Medicine · doi:10.1007/s11684-018-0646-8 · Cited by 141 · see citing works
Identification of DHODH as a therapeutic target in small cell lung cancer
Li, L., Ng, S. R., Colón, C. I., Drapkin, B. J., Hsu, P. P., Li, Z., Nabel, C. S., Lewis, C. A., Romero, R., Mercer, K. L., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aaw7852 · Cited by 141 · see citing works
Emerging advances in defining the molecular and therapeutic landscape of small-cell lung cancer
Sen, T., Takahashi, N., Chakraborty, S., Takebe, N., Nassar, A. H., Karim, N. A., Puri, S., & Naqash, A. R. (2024) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-024-00914-x · Cited by 139 · see citing works
Dannenberg, J.-H., Schuijff, L., Dekker, M., van der Valk, M., & Riele, H. T. (2004) · Genes & Development · doi:10.1101/gad.322004 · Cited by 137 · see citing works
Fujino, K., Motooka, Y., Hassan, W. A., Abdalla, M. O. A., Sato, Y., Kudoh, S., Hasegawa, K., Niimori‐Kita, K., Kobayashi, H., Kubota, I., et al. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.08.018 · Cited by 137 · see citing works
Remón, J., Morán, T., Majem, M., Reguart, N., Dalmau, E., Márquez-Medina, D., & LIANES, P. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.06.002 · Cited by 135 · see citing works
Hollander, M. C., Philburn, R. T., Patterson, A. D., Velasco-Miguel, S., Friedberg, E. C., Linnoila, R. I., & Fornace, A. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503133102 · Cited by 135 · see citing works
Self-citationTransformation to SCLC after Treatment with the ALK Inhibitor Alectinib
Fujita, S., Masago, K., Katakami, N., & Yatabe, Y. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2015.12.105 · Cited by 133 · see citing works
Oser, M. G., Sabet, A. H., Gao, W., Chakraborty, A. A., Schinzel, A. C., Jennings, R. B., Fonseca, R., Bonal, D. M., Booker, M. A., Flaifel, A., et al. (2019) · Genes & Development · doi:10.1101/gad.328336.119 · Cited by 134 · see citing works
Miller, Y. E. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2005-0158oe · Cited by 132 · see citing works
PTEN Is a Potent Suppressor of Small Cell Lung Cancer
Cui, M., Augert, A., Rongione, M. A., Conkrite, K. L., Parazzoli, S. D., Nikitin, A. Y., Ingolia, N. T., & MacPherson, D. P. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0554 · Cited by 131 · see citing works
Faber, A. C., Farago, A. F., Costa, C., Dastur, A., Gomez-Caraballo, M., Robbins, R., Wagner, B. L., Rideout, W. M., Jakubik, C. T., Ham, J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411848112 · Cited by 127 · see citing works
Nadauld, L. D., Garcia, S., Natsoulis, G., Bell, J., Miotke, L. K., Hopmans, E. S., Xu, H., Pai, R. K., Palm, C., Regan, J. F., et al. (2014) · Genome biology · doi:10.1186/s13059-014-0428-9 · Cited by 126 · see citing works
- Authors
- Meuwissen, R., Linn, S. C., Linnoila, R. I., Zevenhoven, J., Mooi, W. J., & Berns, A.
- Affiliations
- The Netherlands Cancer Institute (NL)
- National Cancer Institute (US)
- Corresponding author
- Berns, Anton
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2003-09
- Volume
- 4
- Issue
- 3
- Pages
- 181-189
- ISSN
- 1535-6108 (ISSN-L)
- OpenAlex
- W1978286483
- Cited by
- 643
- References
- 49
- Citations by year
- 2026: 22 · 2025: 41 · 2024: 30 · 2023: 43 · 2022: 43 · 2021: 40 · 2020: 33 · 2019: 43 · 2018: 34 · 2017: 34 · 2016: 27 · 2015: 31 · 2014: 27 · 2013: 24 · 2012: 16
- FWCI
- 8.70
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- KWF Kankerbestrijding
- Topics
- Health Sciences › Medicine › Oncology › Lung Cancer Research Studies
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Occupational and environmental lung diseases
- Keywords
- small cell lung cancer, lung neuroendocrine tumors, Trp53, RB1, conditional knockout mice, carcinogenesis, p53, retinoblastoma protein, lung epithelial cells, metastasis, mouse model
- MeSH terms
- Animals, DNA-Binding Proteins, Lung Neoplasms, Mice, Transgenic, Transcription Factors, Gene Expression Regulation, Neoplastic, Genes, p53, Tumor Suppressor Protein p53, Retinoblastoma Protein, Carcinoma, Small Cell, Mice, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins
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