Notch signaling is activated in human hepatocellular carcinoma and induces tumor formation in mice

Gastroenterology

Volumn 143, Issue 6, 2012, Pages

  Villanueva, Augusto ^a,b,c   Alsinet, Clara ^a,b,c   Yanger, Kilangsungla ^d,e   Hoshida, Yujin ^f,g,h   Zong, Yiwei ^d,e   Toffanin, Sara ^h,i   Rodriguez Carunchio, Leonardo ^j   Solé, Manel ^j   Thung, Swan ^h   Stanger, Ben Z ^d,e   Llovet, Josep M ^a,b,c,h,k  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

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

^g HARVARD MEDICAL SCHOOL   (United States)

^h MOUNT SINAI MEDICAL CENTER   (United States)

ⁱ NATIONAL CANCER INSTITUTE   (Italy)

^j HOSPITAL CLÍNIC   (Spain)

^k INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

more..

Author keywords

Gene Expression Profiling; Genetically Engineered Mouse Model; Notch Activation

Indexed keywords

ALPHA FETOPROTEIN; CYCLIN A2; CYCLIN B2; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYTOCHROME P450; DEOXYRIBONUCLEASE I; GAMMA SECRETASE INHIBITOR; MESSENGER RNA; NOTCH RECEPTOR; OSTEOPONTIN; SOMATOMEDIN B; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER DEVELOPMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84869774410     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2012.09.002     Document Type: Article

References (64)

1. A. Jemal, F. Bray, M.M. Centers Global cancer statistics CA Cancer J Clin 61 2011 69 90
2. S.F. Altekruse, K.A. Mcglynn, M.E. Reichman Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005 J Clin Oncol 27 2009 1485 1491
3. J.M. Llovet, A. Burroughs, J. Bruix Hepatocellular carcinoma Lancet 362 2003 1907 1917
4. J.M. Llovet, S. Ricci, V. Mazzaferro Sorafenib in advanced hepatocellular carcinoma N Engl J Med 359 2008 378 390
5. K.S. Zaret Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation Nat Rev Genet 9 2008 329 340
6. Y. Zong, A. Panikkar, J. Xu Notch signaling controls liver development by regulating biliary differentiation Development 136 2009 1727 1739
7. P. Ranganathan, K.L. Weaver, A.J. Capobianco Notch signalling in solid tumours: a little bit of everything but not all the time Nat Rev Cancer 11 2011 336 351
8. B. Westhoff, I.N. Colaluca, G. D'Ario Alterations of the Notch pathway in lung cancer Proc Natl Acad Sci U S A 106 2009 22293 22298
9. S. Santagata, F. Demichelis, A. Riva JAGGED1 expression is associated with prostate cancer metastasis and recurrence Cancer Res 64 2004 6854 6857
10. C. Wang, R. Qi, N. Li Notch1 signaling sensitizes tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in human hepatocellular carcinoma cells by inhibiting Akt/Hdm2-mediated p53 degradation and up-regulating p53-dependent DR5 expression J Biol Chem 284 2009 16183 16190
11. R. Qi, H. An, Y. Yu Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis Cancer Res 63 2003 8323 8329
12. C. Giovannini, L. Gramantieri, P. Chieco Selective ablation of Notch3 in HCC enhances doxorubicin's death promoting effect by a p53 dependent mechanism J Hepatol 50 2009 969 979
13. L.C. Murtaugh, B.Z. Stanger, K.M. Kwan Notch signaling controls multiple steps of pancreatic differentiation Proc Natl Acad Sci U S A 100 2003 14920 14925
14. C. Kellendonk, C. Opherk, K. Anlag Hepatocyte-specific expression of Cre recombinase Genesis 26 2000 151 153
15. D.Y. Chiang, A. Villanueva, Y. Hoshida Focal gains of VEGFA and molecular classification of hepatocellular carcinoma Cancer Res 68 2008 6779 6788
16. E. Wurmbach, Y.-B. Chen, G. Khitrov Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma Hepatology 45 2007 938 947
17. A. Villanueva, Y. Hoshida, C. Battiston Combining clinical, pathology, and gene expression data to predict recurrence of hepatocellular carcinoma Gastroenterology 140 2011 1501 1512.e2
18. Y. Hoshida, S.M.B. Nijman, M. Kobayashi Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma Cancer Res 69 2009 7385 7392
19. J. Barretina, G. Caponigro, N. Stransky The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity Nature 483 2012 603 607
20. A. Villanueva, D.Y. Chiang, P. Newell Pivotal role of mTOR signaling in hepatocellular carcinoma Gastroenterology 135 2008 1972 1983e1-11
21. I. Maillard, U. Koch, A. Dumortier Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells Cell Stem Cell 2 2008 356 366
22. M. Reich, T. Liefeld, J. Gould GenePattern 2.0 Nat Genet 38 2006 500 501
23. V.G. Tusher, R. Tibshirani, G. Chu Significance analysis of microarrays applied to the ionizing radiation response Proc Natl Acad Sci U S A 98 2001 5116 5121
24. Y. Hochberg, Y. Benjamini More powerful procedures for multiple significance testing Stat Med 9 1990 811 818
25. Y. Hoshida Nearest template prediction: a single-sample-based flexible class prediction with confidence assessment PLoS ONE 5 2010 e15543
26. M. Kanehisa, S. Goto KEGG: Kyoto encyclopedia of genes and genomes Nucleic Acids Res 28 2000 27 30
27. M.E. Higgins, M. Claremont, J.E. Major CancerGenes: a gene selection resource for cancer genome projects Nucleic Acids Res 35 2007 D721 D726
28. R.L. Seal, S.M. Gordon, M.J. Lush genenames.org: the HGNC resources in 2011 Nucleic Acids Res 39 2010 D514 D519
29. V. Tovar, C. Alsinet, A. Villanueva IGF activation in a molecular subclass of hepatocellular carcinoma and pre-clinical efficacy of IGF-1R blockage J Hepatol 52 2010 550 559
30. G. Nardone, M. Romano, A. Calabrò Activation of fetal promoters of insulin-like growth factors II gene in hepatitis C virus-related chronic hepatitis, cirrhosis, and hepatocellular carcinoma Hepatology 23 1996 1304 1312
31. P.A. Seymour, K.K. Freude, M.N. Tran SOX9 is required for maintenance of the pancreatic progenitor cell pool Proc Natl Acad Sci U S A 104 2007 1865 1870
32. K. Furuyama, Y. Kawaguchi, H. Akiyama Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine Nat Genet 43 2010 34 41
33. W. Guo, Z. Keckesova, J.L. Donaher Slug and Sox9 cooperatively determine the mammary stem cell state Cell 148 2012 1015 1028
34. S. Toffanin, Y. Hoshida, A. Lachenmayer MicroRNA-based classification of hepatocellular carcinoma and oncogenic role of miR-517a Gastroenterology 140 2011 1618 1628.e16
35. J.B. Andersen, R. Loi, A. Perra Progenitor-derived hepatocellular carcinoma model in the rat Hepatology 51 2010 1401 1409
36. H.G. Woo, J.H. Lee, J.H. Yoon Identification of a cholangiocarcinoma-like gene expression trait in hepatocellular carcinoma Cancer Res 70 2010 3034 3041
37. C. Coulouarn, V.M. Factor, S.S. Thorgeirsson Transforming growth factor-β gene expression signature in mouse hepatocytes predicts clinical outcome in human cancer Hepatology 47 2008 2059 2067
38. S.-O. Lim, Y.M. Park, H.S. Kim Notch1 differentially regulates oncogenesis by wild-type p53 overexpression and p53 mutation in grade III hepatocellular carcinoma Hepatology 53 2011 1382 1392
39. M. Liu, D.-F. Lee, C.-T. Chen IKKα; activation of NOTCH links tumorigenesis via FOXA2 Suppression Mol Cell 45 2012 171 184
40. P. Viatour, U. Ehmer, L.A. Saddic Notch signaling inhibits hepatocellular carcinoma following inactivation of the RB pathway J Exp Med 208 2011 1963 1976
41. S. Weijzen, P. Rizzo, M. Braid Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells Nat Med 8 2002 979 986
42. J-S. Lee, I.-S. Chu, A. Mikaelyan Application of comparative functional genomics to identify best-fit mouse models to study human cancer Nat Genet 36 2004 1306 1311
43. D. Jia, L. Wei, W. Guo Genome-wide copy number analyses identified novel cancer genes in hepatocellular carcinoma Hepatology 54 2011 1227 1236
44. P. Kaposi-Novak Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype J Clin Invest 116 2006 1582 1595
45. J-S. Lee, J. Heo, L. Libbrecht A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells Nat Med 12 2006 410 416
46. P.B. Chapman, A. Hauschild, C. Robert Improved survival with vemurafenib in melanoma with BRAF V600E mutation N Engl J Med 364 2011 2507 2516
47. E.L. Kwak, Y.-J. Bang, D.R. Camidge Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer N Engl J Med 363 2010 1693 1703
48. V. Mazzaferro, R. Romito, M. Schiavo Prevention of hepatocellular carcinoma recurrence with α-interferon after liver resection in HCV cirrhosis Hepatology 44 2006 1543 1554
49. Y. Zong, A. Panikkar, J. Xu Notch signaling controls liver development by regulating biliary differentiation Development 136 2009 1727 1739
50. L.C. Murtaugh, B.Z. Stanger, K.M. Kwan Notch signaling controls multiple steps of pancreatic differentiation Proc Natl Acad Sci U S A 100 2003 14920 14925
51. C. Kellendonk, C. Opherk, K. Anlag Hepatocyte-specific expression of Cre recombinase Genesis 26 2000 151 153
52. D.Y. Chiang, A. Villanueva, Y. Hoshida Focal gains of VEGFA and molecular classification of hepatocellular carcinoma Cancer Res 68 2008 6779 6788
53. E. Wurmbach, Y.-B. Chen, G. Khitrov Genome-wide molecular profiles of HCV-induced dysplasia and hepatocellular carcinoma Hepatology 45 2007 938 947
54. A. Villanueva, Y. Hoshida, C. Battiston Combining clinical, pathology, and gene expression data to predict recurrence of hepatocellular carcinoma Gastroenterology 140 2011 1501 1512.e2
55. Y. Hoshida, S.M.B. Nijman, M. Kobayashi Integrative transcriptome analysis reveals common molecular subclasses of human hepatocellular carcinoma Cancer Res 69 2009 7385 7392
56. M. Reich, T. Liefeld, J. Gould GenePattern 2.0 Nat Genet 38 2006 500 501
57. V.G. Tusher, R. Tibshirani, G. Chu Significance analysis of microarrays applied to the ionizing radiation response Proc Natl Acad Sci U S A 98 2001 5116 5121
58. Y. Hochberg, Y. Benjamini More powerful procedures for multiple significance testing Stat Med 9 1990 811 818
59. Y. Hoshida Nearest template prediction: a single-sample-based flexible class prediction with confidence assessment PLoS ONE 5 2010 e15543
60. Y. Hoshida, A. Villanueva, M. Kobayashi Gene expression in fixed tissues and outcome in hepatocellular carcinoma N Engl J Med 359 2008 1995 2004
61. M. Kanehisa, S. Goto KEGG: kyoto encyclopedia of genes and genomes Nucleic Acids Res 28 2000 27 30
62. M.E. Higgins, M. Claremont, J.E. Major CancerGenes: a gene selection resource for cancer genome projects Nucleic Acids Res 35 2007 D721 D726
63. R.L. Seal, S.M. Gordon, M.J. Lush genenames.org: the HGNC resources in 2011 Nucleic Acids Res 39 2010 D514 D519
64. S. Toffanin, Y. Hoshida, A. Lachenmayer MicroRNA-based classification of hepatocellular carcinoma and oncogenic role of miR-517a Gastroenterology 140 2011 1618 1628