P53-dependent nestin regulation links tumor suppression to cellular plasticity in liver cancer

Cell

Volumn 158, Issue 3, 2014, Pages 579-592

  Tschaharganeh, Darjus F ^a   Xue, Wen ^b   Calvisi, Diego F ^c   Evert, Matthias ^c   Michurina, Tatyana V ^b   Dow, Lukas E ^a   Banito, Ana ^a   Katz, Sarah F ^d   Kastenhuber, Edward R ^a   Weissmueller, Susann ^a,b   Huang, Chun Hao ^a   Lechel, Andre ^d   Andersen, Jesper B ^e,f   Capper, David ^g   Zender, Lars ^b   Longerich, Thomas ^g   Enikolopov, Grigori ^b   Lowe, Scott W ^a,b,h  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^c Medical University of Greifswald   (Germany)

^d UNIVERSITY OF ULM   (Germany)

^e NATIONAL CANCER INSTITUTE   (United States)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^h HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NESTIN; NOTCH RECEPTOR; PROTEIN P53; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3; WNT PROTEIN; NES PROTEIN, HUMAN; SP1 PROTEIN, HUMAN; SP3 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT CARCINOMA; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STEM CELL; CANCER SURVIVAL; CELL DEDIFFERENTIATION; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; FEMALE; GENE LOSS; GENE MUTATION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION TERMINATION; TUMOR SUPPRESSOR GENE; WNT SIGNALING PATHWAY; ANIMAL; CELL TRANSFORMATION; GENETIC TRANSCRIPTION; LIVER TUMOR; METABOLISM; PATHOLOGY; PROGNOSIS;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL TRANSFORMATION, NEOPLASTIC; HEPATOCYTES; HUMANS; LIVER NEOPLASMS; MICE; NESTIN; PROGNOSIS; SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905377981     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.05.051     Document Type: Article

References (58)

1. J.B. Andersen, B. Spee, B.R. Blechacz, I. Avital, M. Komuta, A. Barbour, E.A. Conner, M.C. Gillen, T. Roskams, and L.R. Roberts et al. Genomic and genetic characterization of cholangiocarcinoma identifies therapeutic targets for tyrosine kinase inhibitors Gastroenterology 142 2012 1021 1031.e1015
2. J.B. Bell, K.M. Podetz-Pedersen, E.L. Aronovich, L.R. Belur, R.S. McIvor, and P.B. Hackett Preferential delivery of the Sleeping Beauty transposon system to livers of mice by hydrodynamic injection Nat. Protoc. 2 2007 3153 3165
3. G.L. Bond, W. Hu, E.E. Bond, H. Robins, S.G. Lutzker, N.C. Arva, J. Bargonetti, F. Bartel, H. Taubert, and P. Wuerl et al. A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans Cell 119 2004 591 602
4. L. Boulter, O. Govaere, T.G. Bird, S. Radulescu, P. Ramachandran, A. Pellicoro, R.A. Ridgway, S.S. Seo, B. Spee, and N. Van Rooijen et al. Macrophage-derived Wnt opposes Notch signaling to specify hepatic progenitor cell fate in chronic liver disease Nat. Med. 18 2012 572 579
5. C.A. Brady, D. Jiang, S.S. Mello, T.M. Johnson, L.A. Jarvis, M.M. Kozak, D. Kenzelmann Broz, S. Basak, E.J. Park, and M.E. McLaughlin et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression Cell 145 2011 571 583
6. J. Chen, Y. Li, T.S. Yu, R.M. McKay, D.K. Burns, S.G. Kernie, and L.F. Parada A restricted cell population propagates glioblastoma growth after chemotherapy Nature 488 2012 522 526
7. L. Cheng, Z. Jin, L. Liu, Y. Yan, T. Li, X. Zhu, and N. Jing Characterization and promoter analysis of the mouse nestin gene FEBS Lett. 565 2004 195 202
8. J. Dong, G. Feldmann, J. Huang, S. Wu, N. Zhang, S.A. Comerford, M.F. Gayyed, R.A. Anders, A. Maitra, and D. Pan Elucidation of a universal size-control mechanism in Drosophila and mammals Cell 130 2007 1120 1133
9. B. Fan, Y. Malato, D.F. Calvisi, S. Naqvi, N. Razumilava, S. Ribback, G.J. Gores, F. Dombrowski, M. Evert, X. Chen, and H. Willenbring Cholangiocarcinomas can originate from hepatocytes in mice J. Clin. Invest. 122 2012 2911 2915
10. T.G. Fellous, S. Islam, P.J. Tadrous, G. Elia, H.M. Kocher, S. Bhattacharya, L. Mears, D.M. Turnbull, R.W. Taylor, and L.C. Greaves et al. Locating the stem cell niche and tracing hepatocyte lineages in human liver Hepatology 49 2009 1655 1663
11. D. Friedmann-Morvinski, E.A. Bushong, E. Ke, Y. Soda, T. Marumoto, O. Singer, M.H. Ellisman, and I.M. Verma Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice Science 338 2012 1080 1084
12. A.S. Gleiberman, J.M. Encinas, J.L. Mignone, T. Michurina, M.G. Rosenfeld, and G. Enikolopov Expression of nestin-green fluorescent protein transgene marks oval cells in the adult liver Dev. Dyn. 234 2005 413 421
13. S. Godar, T.A. Ince, G.W. Bell, D. Feldser, J.L. Donaher, J. Bergh, A. Liu, K. Miu, R.S. Watnick, and F. Reinhardt et al. Growth-inhibitory and tumor- suppressive functions of p53 depend on its repression of CD44 expression Cell 134 2008 62 73
14. D. Grimm, K.L. Streetz, C.L. Jopling, T.A. Storm, K. Pandey, C.R. Davis, P. Marion, F. Salazar, and M.A. Kay Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways Nature 441 2006 537 541
15. J. Hanna, K. Saha, B. Pando, J. van Zon, C.J. Lengner, M.P. Creyghton, A. van Oudenaarden, and R. Jaenisch Direct cell reprogramming is a stochastic process amenable to acceleration Nature 462 2009 595 601
16. D.M. Harvey, and A.J. Levine p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts Genes Dev. 5 12B 1991 2375 2385
17. J. Ho, and S. Benchimol Transcriptional repression mediated by the p53 tumour suppressor Cell Death Differ. 10 2003 404 408
18. H. Hong, K. Takahashi, T. Ichisaka, T. Aoi, O. Kanagawa, M. Nakagawa, K. Okita, and S. Yamanaka Suppression of induced pluripotent stem cell generation by the p53-p21 pathway Nature 460 2009 1132 1135
19. S.P. Hussain, J. Schwank, F. Staib, X.W. Wang, and C.C. Harris TP53 mutations and hepatocellular carcinoma: insights into the etiology and pathogenesis of liver cancer Oncogene 26 2007 2166 2176
20. S.F. Katz, A. Lechel, A.C. Obenauf, Y. Begus-Nahrmann, J.M. Kraus, E.M. Hoffmann, J. Duda, P. Eshraghi, D. Hartmann, and B. Liss et al. Disruption of Trp53 in livers of mice induces formation of carcinomas with bilineal differentiation Gastroenterology 142 2012 1229 1239
21. T. Kawamura, J. Suzuki, Y.V. Wang, S. Menendez, L.B. Morera, A. Raya, G.M. Wahl, and J.C. Izpisúa Belmonte Linking the p53 tumour suppressor pathway to somatic cell reprogramming Nature 460 2009 1140 1144
22. D. Kenzelmann Broz, and L.D. Attardi In vivo analysis of p53 tumor suppressor function using genetically engineered mouse models Carcinogenesis 31 2010 1311 1318
23. O. Krupkova Jr., T. Loja, I. Zambo, and R. Veselska Nestin expression in human tumors and tumor cell lines Neoplasma 57 2010 291 298
24. H. Li, A. Wolfe, S. Septer, G. Edwards, X. Zhong, A.B. Abdulkarim, S. Ranganathan, and U. Apte Deregulation of Hippo kinase signalling in human hepatic malignancies Liver Int. 32 2012 38 47
25. T. Lin, C. Chao, S. Saito, S.J. Mazur, M.E. Murphy, E. Appella, and Y. Xu p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression Nat. Cell Biol. 7 2005 165 171
26. W.J. Lu, F. Lan, Q. He, A. Lee, C.Z. Tang, L. Dong, B. Lan, X. Ma, J.C. Wu, and L. Shen Inducible expression of stem cell associated intermediate filament nestin reveals an important role in glioblastoma carcinogenesis Int. J. Cancer 128 2011 343 351
27. A. Lujambio, L. Akkari, J. Simon, D. Grace, D.F. Tschaharganeh, J.E. Bolden, Z. Zhao, V. Thapar, J.A. Joyce, V. Krizhanovsky, and S.W. Lowe Non-cell-autonomous tumor suppression by p53 Cell 153 2013 449 460
28. S.G. Lutzker, and A.J. Levine A functionally inactive p53 protein in teratocarcinoma cells is activated by either DNA damage or cellular differentiation Nat. Med. 2 1996 804 810
29. R.M. Marión, K. Strati, H. Li, M. Murga, R. Blanco, S. Ortega, O. Fernandez-Capetillo, M. Serrano, and M.A. Blasco A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity Nature 460 2009 1149 1153
30. E.K. Markert, H. Mizuno, A. Vazquez, and A.J. Levine Molecular classification of prostate cancer using curated expression signatures Proc. Natl. Acad. Sci. USA 108 2011 21276 21281
31. J.L. Mignone, V. Kukekov, A.S. Chiang, D. Steindler, and G. Enikolopov Neural stem and progenitor cells in nestin-GFP transgenic mice J. Comp. Neurol. 469 2004 311 324
32. H. Mizuno, B.T. Spike, G.M. Wahl, and A.J. Levine Inactivation of p53 in breast cancers correlates with stem cell transcriptional signatures Proc. Natl. Acad. Sci. USA 107 2010 22745 22750
33. J.C. Nault, and J. Zucman-Rossi Genetics of hepatobiliary carcinogenesis Semin. Liver Dis. 31 2011 173 187
34. O. Neumann, M. Kesselmeier, R. Geffers, R. Pellegrino, B. Radlwimmer, K. Hoffmann, V. Ehemann, P. Schemmer, P. Schirmacher, J. Lorenzo Bermejo, and T. Longerich Methylome analysis and integrative profiling of human HCCs identify novel protumorigenic factors Hepatology 56 2012 1817 1827
35. T. Roskams Liver stem cells and their implication in hepatocellular and cholangiocarcinoma Oncogene 25 2006 3818 3822
36. P.C. Rumsby, M.J. Davies, and J.G. Evans Screening for p53 mutations in C3H/He mouse liver tumors derived spontaneously or induced with diethylnitrosamine or phenobarbitone Mol. Carcinog. 9 1994 71 75
37. A. Saborowski, M. Saborowski, M.A. Davare, B.J. Druker, D.S. Klimstra, and S.W. Lowe Mouse model of intrahepatic cholangiocarcinoma validates FIG-ROS as a potent fusion oncogene and therapeutic target Proc. Natl. Acad. Sci. 110 2013 19513 19518
38. C.M. Sahlgren, H.M. Pallari, T. He, Y.H. Chou, R.D. Goldman, and J.E. Eriksson A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death EMBO J. 25 2006 4808 4819
39. S. Schwitalla, A.A. Fingerle, P. Cammareri, T. Nebelsiek, S.I. Göktuna, P.K. Ziegler, O. Canli, J. Heijmans, D.J. Huels, and G. Moreaux et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties Cell 152 2013 25 38
40. S. Sekiya, and A. Suzuki Intrahepatic cholangiocarcinoma can arise from Notch-mediated conversion of hepatocytes J. Clin. Invest. 122 2012 3914 3918
41. S. Soddu, G. Blandino, G. Citro, R. Scardigli, G. Piaggio, A. Ferber, B. Calabretta, and A. Sacchi Wild-type p53 gene expression induces granulocytic differentiation of HL-60 cells Blood 83 1994 2230 2237
42. B.T. Spike, and G.M. Wahl p53, Stem Cells, and Reprogramming: Tumor Suppression beyond Guarding the Genome Genes Cancer 2 2011 404 419
43. K. Sugimoto, S.P. Gordon, and E.M. Meyerowitz Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation? Trends Cell Biol. 21 2011 212 218
44. O. Takakuwa, K. Maeno, E. Kunii, H. Ozasa, H. Hijikata, T. Uemura, D. Kasai, H. Ohkubo, M. Miyazaki, T. Oguri, and A. Niimi Involvement of intermediate filament nestin in cell growth of small-cell lung cancer Lung Cancer 81 2013 174 179
45. A. Tapias, C.J. Ciudad, I.B. Roninson, and V. Noé Regulation of Sp1 by cell cycle related proteins Cell Cycle 7 2008 2856 2867
46. P.R. Tata, H. Mou, A. Pardo-Saganta, R. Zhao, M. Prabhu, B.M. Law, V. Vinarsky, J.L. Cho, S. Breton, and A. Sahay et al. Dedifferentiation of committed epithelial cells into stem cells in vivo Nature 503 2013 218 223
47. K.H. Vousden, and D.P. Lane p53 in health and disease Nat. Rev. Mol. Cell Biol. 8 2007 275 283
48. K.H. Vousden, and C. Prives Blinded by the Light: The Growing Complexity of p53 Cell 137 2009 413 431
49. D.Y. Wu, and Z. Yao Functional analysis of two Sp1/Sp3 binding sites in murine Nanog gene promoter Cell Res. 16 2006 319 322
50. W. Xue, L. Zender, C. Miething, R.A. Dickins, E. Hernando, V. Krizhanovsky, C. Cordon-Cardo, and S.W. Lowe Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas Nature 445 2007 656 660
51. S.R. Yant, L. Meuse, W. Chiu, Z. Ivics, Z. Izsvak, and M.A. Kay Somatic integration and long-term transgene expression in normal and haemophilic mice using a DNA transposon system Nat. Genet. 25 2000 35 41
52. M.H. Yun, P.B. Gates, and J.P. Brockes Regulation of p53 is critical for vertebrate limb regeneration Proc. Natl. Acad. Sci. USA 110 2013 17392 17397
53. L. Zender, M.S. Spector, W. Xue, P. Flemming, C. Cordon-Cardo, J. Silke, S.T. Fan, J.M. Luk, M. Wigler, and G.J. Hannon et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach Cell 125 2006 1253 1267
54. L. Zhang, D. Yu, M. Hu, S. Xiong, A. Lang, L.M. Ellis, and R.E. Pollock Wild-type p53 suppresses angiogenesis in human leiomyosarcoma and synovial sarcoma by transcriptional suppression of vascular endothelial growth factor expression Cancer Res. 60 2000 3655 3661
55. Y. Zhao, W. Zhang, Z. Guo, F. Ma, Y. Wu, Y. Bai, W. Gong, Y. Chen, T. Cheng, and F. Zhi et al. Inhibition of the transcription factor Sp1 suppresses colon cancer stem cell growth and induces apoptosis in vitro and in nude mouse xenografts Oncol. Rep. 30 2013 1782 1792
56. O. Aksoy, A. Chicas, T. Zeng, Z. Zhao, M. McCurrach, X. Wang, and S.W. Lowe The atypical E2F family member E2F7 couples the p53 and RB pathways during cellular senescence Genes Dev. 26 2012 1546 1557
57. T.R. Brummelkamp, R. Bernards, and R. Agami A system for stable expression of short interfering RNAs in mammalian cells Science 296 2002 550 553
58. P.K. Premsrirut, L.E. Dow, S.Y. Kim, M. Camiolo, C.D. Malone, C. Miething, C. Scuoppo, J. Zuber, R.A. Dickins, and S.C. Kogan et al. A rapid and scalable system for studying gene function in mice using conditional RNA interference Cell 145 2011 145 158