Keratin 19 epithelial patterns in cirrhotic stroma parallel hepatocarcinogenesis

American Journal of Pathology

Volumn 179, Issue 2, 2011, Pages 1015-1029

  Lennerz, Jochen K M ^a,b   Chapman, William C ^b   Brunt, Elizabeth M ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALVASCULIN; CYTOKERATIN 19; SMAD3 PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UVOMORULIN; VIMENTIN;

ANTIBODY LABELING; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER STAGING; CELL DEATH; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; IMMUNOREACTIVITY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER NODULE; PARACRINE SIGNALING; PRIORITY JOURNAL;

APOPTOSIS; BIOPSY; CARCINOMA, HEPATOCELLULAR; EPITHELIUM; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; KERATIN-19; LIVER CIRRHOSIS; LIVER NEOPLASMS; MODELS, BIOLOGICAL; NECROSIS; PREDICTIVE VALUE OF TESTS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 80052503938     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.04.040     Document Type: Article

References (99)

1. T. Roskams, and V. Desmet Ductular reaction and its diagnostic significance Semin Diagn Pathol 15 1998 259 269 (Pubitemid 28536759)
2. V. Desmet, T. Roskams, and P. Van Eyken Ductular reaction in the liver Pathol Res Pract 191 1995 513 524
3. H. Popper, G. Kent, and R. Stein Ductular cell reaction in the liver in hepatic injury J Mt Sinai Hosp NY 24 1957 551 556
4. K.A. Rygiel, H. Robertson, H.L. Marshall, M. Pekalski, L. Zhao, T.A. Booth, D.E. Jones, A.D. Burt, and J.A. Kirby Epithelial-mesenchymal transition contributes to portal tract fibrogenesis during human chronic liver disease Lab Invest 88 2008 112 123 (Pubitemid 351161272)
5. J.A. Kirby, H. Robertson, H.L. Marshall, K.A. Rygiel, M. Hudson, D.E. Jones, and A.D. Burt Epithelial to mesenchymal transition in primary sclerosing cholangitis Liver Int 28 2008 1176 1177
6. Kojiro M: Pathological diagnosis at early stage: reaching international consensus. Oncology 78(Suppl 1):3135
7. Y.N. Park, M. Kojiro, L. Di Tommaso, A.P. Dhillon, F. Kondo, M. Nakano, M. Sakamoto, N.D. Theise, and M. Roncalli Ductular reaction is helpful in defining early stromal invasion, small hepatocellular carcinomas, and dysplastic nodules Cancer 109 2007 915 923 (Pubitemid 46333533)
8. F. van Zijl, M. Mair, A. Csiszar, D. Schneller, G. Zulehner, H. Huber, R. Eferl, H. Beug, H. Dolznig, and W. Mikulits Hepatic tumor-stroma crosstalk guides epithelial to mesenchymal transition at the tumor edge Oncogene 28 2009 4022 4033
9. J.K. Lennerz, J.S. Crippin, and E.M. Brunt Diagnostic considerations of nodules in the cirrhotic liver: a case-based perspective Pathol Case Rev 14 2009 3 12
10. International Working Party: Terminology of nodular hepatocellular lesions Hepatology 22 1995 983 993
11. P. Hytiroglou, Y.N. Park, G. Krinsky, and N.D. Theise Hepatic precancerous lesions and small hepatocellular carcinoma Gastroenterol Clin North Am 36 2007 867 887 (Pubitemid 350051705)
12. J.H. Lefkowitch Hepatobiliary pathology Curr Opin Gastroenterol 24 2008 269 277 (Pubitemid 351535885)
13. R. Moll, W.W. Franke, D.L. Schiller, B. Geiger, and R. Krepler The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells Cell 31 1982 11 24 (Pubitemid 13215192)
14. J. Tan, P. Hytiroglou, R. Wieczorek, Y.N. Park, S.N. Thung, B. Arias, and N.D. Theise Immunohistochemical evidence for hepatic progenitor cells in liver diseases Liver 22 2002 365 373 (Pubitemid 35331396)
15. P. Van Eyken, and V.J. Desmet Cytokeratins and the liver Liver 13 1993 113 122 (Pubitemid 23228705)
16. T. Terada, M. Hoso, and Y. Nakanuma Distribution of cytokeratin 19positive biliary cells in cirrhotic nodules, hepatic borderline nodules (atypical adenomatous hyperplasia), and small hepatocellular carcinomas Mod Pathol 8 1995 371 379
17. H. Malhi, G.J. Gores, and J.J. Lemasters Apoptosis and necrosis in the liver: a tale of two deaths Hepatology 43 2006 S31 S44
18. R.S. Hotchkiss, A. Strasser, J.E. McDunn, and P.E. Swanson Cell death N Engl J Med 361 2009 1570 1583
19. B. Zhivotovsky, and S. Orrenius Assessment of apoptosis and necrosis by DNA fragmentation and Morphological Criteria Curr Protoc Cell Biol 2001 Chapter 18: Unit 18.3
20. I.D. Bowen Techniques for demonstrating cell death Cell Death in Biology and Pathology I.D. Bowen, R.A. Lockshin, 1981 Chapman & Hall London-New York 379 444
21. J.F. Kerr, A.H. Wyllie, and A.R. Currie Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 1972 239 257
22. Y. Gavrieli, Y. Sherman, and S.A. Ben-Sasson Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation J Cell Biol 119 1992 493 501
23. M. Zeisberg, and E.G. Neilson Biomarkers for epithelial-mesenchymal transitions J Clin Invest 119 2009 1429 1437
24. J.K. Lennerz, S.H. Kim, E.L. Oates, W.J. Huh, J.M. Doherty, X. Tian, A.J. Bredemeyer, J.R. Goldenring, G.Y. Lauwers, Y.K. Shin, and J.C. Mills The transcription factor MIST1 is a novel human gastric chief cell marker whose expression is lost in metaplasia, dysplasia, and carcinoma Am J Pathol 177 2010 1514 1533
25. J.K. Lennerz, V. Ruhle, E.P. Ceppa, W.L. Neuhuber, N.W. Bunnett, E.F. Grady, and K. Messlinger Calcitonin receptor-like receptor (CLR), receptor activity-modifying protein 1 (RAMP1), and calcitonin gene-related peptide (CGRP) immunoreactivity in the rat trigeminovascular system: differences between peripheral and central CGRP receptor distribution J Comp Neurol 507 2008 1277 1299 (Pubitemid 351413572)
26. L. Berglund, E. Bjorling, P. Oksvold, L. Fagerberg, A. Asplund, C.A. Szigyarto, A. Persson, J. Ottosson, H. Wernerus, P. Nilsson, E. Lundberg, A. Sivertsson, S. Navani, K. Wester, C. Kampf, S. Hober, F. Ponten, and M. Uhlen A genecentric human protein atlas for expression profiles based on antibodies Mol Cell Proteomics 7 2008 2019 2027
27. P.B. Silcocks Measuring repeatability and validity of histological diagnosis: a brief review with some practical examples J Clin Pathol 36 1983 1269 1275 (Pubitemid 14205410)
28. J. Pupure, S. Isajevs, E. Skapare, J. Rumaks, S. Svirskis, D. Svirina, I. Kalvinsh, and V. Klusa Neuroprotective properties of mildronate, a mitochondria-targeted small molecule Neurosci Lett 470 2010 100 105
29. M.S. Aguzzi, P. Fortugno, C. Giampietri, G. Ragone, M.C. Capogrossi, and A. Facchiano Intracellular targets of RGDS peptide in melanoma cells Mol Cancer 9 2010 84
30. D. Tarin, E.W. Thompson, and D.F. Newgreen The fallacy of epithelial mesenchymal transition in neoplasia Cancer Res 65 2005 5996 6000 (Pubitemid 40994379)
31. Zhang DW, Bian H: No contribution to liver fibrosis, but possible carcinogenesis? Hepatology 51:14681469; author reply 1469
32. R. Kuwahara, A.V. Kofman, C.S. Landis, E.S. Swenson, E. Barendswaard, and N.D. Theise The hepatic stem cell niche: identification by label-retaining cell assay Hepatology 47 2008 1994 2002 (Pubitemid 351945566)
33. T.A. Roskams, N.D. Theise, C. Balabaud, G. Bhagat, P.S. Bhathal, P. Bioulac-Sage, E.M. Brunt, J.M. Crawford, H.A. Crosby, V. Desmet, M.J. Finegold, S.A. Geller, A.S. Gouw, P. Hytiroglou, A.S. Knisely, M. Kojiro, J.H. Lefkowitch, Y. Nakanuma, J.K. Olynyk, Y.N. Park, B. Portmann, R. Saxena, P.J. Scheuer, A.J. Strain, S.N. Thung, I.R. Wanless, and A.B. West Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers Hepatology 39 2004 1739 1745 (Pubitemid 38702678)
34. K. Taura, K. Miura, K. Iwaisako, C.H. Osterreicher, Y. Kodama, M. Penz-Osterreicher, and D.A. Brenner Hepatocytes do not undergo epithelial-mesenchymal transition in liver fibrosis in mice Hepatology 51 2010 1027 1036
35. G. Giannelli The epithelial-mesenchymal transition: fact or fiction in cancer Hepatology 50 2009 1344 1346
36. R.G. Wells The epithelial-to-mesenchymal transition in liver fibrosis: here today, gone tomorrow Hepatology 51 2010 737 740
37. D. Scholten, A. Scholten, D.A. Brenner, and T. Kisseleva Epithelial-to-mesenchymal transition (EMT) in cholangiocytes does not contribute to liver fibrosis Hepatology 50 Suppl 2009 818A
38. H. Robertson, J.A. Kirby, W.W. Yip, D.E. Jones, and A.D. Burt Biliary epithelial-mesenchymal transition in posttransplantation recurrence of primary biliary cirrhosis Hepatology 45 2007 977 981 (Pubitemid 46631566)
39. A. Omenetti, A. Porrello, Y. Jung, L. Yang, Y. Popov, S.S. Choi, R.P. Witek, G. Alpini, J. Venter, H.M. Vandongen, W.K. Syn, G.S. Baroni, A. Benedetti, D. Schuppan, and A.M. Diehl Hedgehog signaling regulates epithelial-mesenchymal transition during biliary fibrosis in rodents and humans J Clin Invest 118 2008 3331 3342
40. M. Zeisberg, C. Yang, M. Martino, M.B. Duncan, F. Rieder, H. Tanjore, and R. Kalluri Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition J Biol Chem 282 2007 23337 23347 (Pubitemid 47311952)
41. S.S. Choi, A. Omenetti, R.P. Witek, C.A. Moylan, W.K. Syn, Y. Jung, L. Yang, D.L. Sudan, J.K. Sicklick, G.A. Michelotti, M. Rojkind, and A.M. Diehl Hedgehog pathway activation and epithelial-to-mesenchymal transitions during myofibroblastic transformation of rat hepatic cells in culture and cirrhosis Am J Physiol Gastrointest Liver Physiol 297 2009 G1093 G1106
42. L. Fabris, and M. Strazzabosco Epithelial-mesenchymal interactions in biliary diseases Semin Liver Dis 31 2011 11 32
43. F. Strutz, H. Okada, C.W. Lo, T. Danoff, R.L. Carone, J.E. Tomaszewski, and E.G. Neilson Identification and characterization of a fibroblast marker: fSP1 J Cell Biol 130 1995 393 405
44. L. Mazzucchelli Protein S100A4: too long overlooked by pathologists Am J Pathol 160 2002 7 13 (Pubitemid 34052259)
45. M.H. Yang, C.L. Chen, G.Y. Chau, S.H. Chiou, C.W. Su, T.Y. Chou, W.L. Peng, and J.C. Wu Comprehensive analysis of the independent effect of Twist and Snail in promoting metastasis of hepatocellular carcinoma Hepatology 50 2009 1464 1474
46. M.A. Nieto The snail superfamily of zinc-finger transcription factors Nat Rev Mol Cell Biol 3 2002 155 166
47. M. Le Hir, I. Hegyi, D. Cueni-Loffing, J. Loffing, and B. Kaissling Characterization of renal interstitial fibroblast-specific protein 1/S100A4positive cells in healthy and inflamed rodent kidneys Histochem Cell Biol 123 2005 335 346 (Pubitemid 40922217)
48. H. Robertson, S. Ali, B.J. McDonnell, A.D. Burt, and J.A. Kirby Chronic renal allograft dysfunction: the role of T cellmediated tubular epithelial to mesenchymal cell transition J Am Soc Nephrol 15 2004 390 397 (Pubitemid 38140779)
49. A. Cano, M.A. Perez-Moreno, I. Rodrigo, A. Locascio, M.J. Blanco, M.G. del Barrio, F. Portillo, and M.A. Nieto The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat Cell Biol 2 2000 76 83
50. M.A. Huber, N. Kraut, and H. Beug Molecular requirements for epithelial-mesenchymal transition during tumor progression Curr Opin Cell Biol 17 2005 548 558 (Pubitemid 41267170)
51. R. Kalluri, and E.G. Neilson Epithelial-mesenchymal transition and its implications for fibrosis J Clin Invest 112 2003 1776 1784 (Pubitemid 38063698)
52. H. Okada, T.M. Danoff, R. Kalluri, and E.G. Neilson Early role of Fsp1 in epithelial-mesenchymal transformation Am J Physiol 273 1997 F563 F574
53. S. Wasilenko, and A.L. Mason New insights from recurrent primary biliary cirrhosis in liver transplantation: the paradox of becoming a fibroblast Hepatology 45 2007 837 840 (Pubitemid 46631550)
54. M. Iwano, D. Plieth, T.M. Danoff, C. Xue, H. Okada, and E.G. Neilson Evidence that fibroblasts derive from epithelium during tissue fibrosis J Clin Invest 110 2002 341 350 (Pubitemid 34847966)
55. J.R. Tyler, H. Robertson, T.A. Booth, A.D. Burt, and J.A. Kirby Chronic allograft nephropathy: intraepithelial signals generated by transforming growth factor-beta and bone morphogenetic protein-7 Am J Transplant 6 2006 1367 1376 (Pubitemid 44030319)
56. L.E. Greenbaum Hedgehog signaling in biliary fibrosis J Clin Invest 118 2008 3263 3265
57. N. Fausto, and J.S. Campbell Mouse models of hepatocellular carcinoma Semin Liver Dis 30 2010 87 98
58. S.S. Glaser, E. Gaudio, T. Miller, D. Alvaro, and G. Alpini Cholangiocyte proliferation and liver fibrosis Exp Rev Mol Med 11 2009 e7
59. A. Kiss, J. Schnur, Z. Szabo, and P. Nagy Immunohistochemical analysis of atypical ductular reaction in the human liver, with special emphasis on the presence of growth factors and their receptors Liver 21 2001 237 246 (Pubitemid 32677379)
60. J.M. Llovet, and J. Bruix Molecular targeted therapies in hepatocellular carcinoma Hepatology 48 2008 1312 1327
61. A.M. Gressner, R. Weiskirchen, K. Breitkopf, and S. Dooley Roles of TGF-beta in hepatic fibrosis Front Biosci 7 2002 d793 d807
62. C.E. Tan, V.S. Chan, R.Y. Yong, V. Vijayan, W.L. Tan, S.M. Fook Chong, J.M. Ho, and H.H. Cheng Distortion in TGF beta 1 peptide immunolocalization in biliary atresia: comparison with the normal pattern in the developing human intrahepatic bile duct system Pathol Int 45 1995 815 824
63. P. ten Dijke, and C.S. Hill New insights into TGF-beta-Smad signalling Trends Biochem Sci 29 2004 265 273
64. S. Dooley, J. Hamzavi, L. Ciuclan, P. Godoy, I. Ilkavets, S. Ehnert, E. Ueberham, R. Gebhardt, S. Kanzler, A. Geier, K. Breitkopf, H. Weng, and P.R. Mertens Hepatocyte-specific Smad7 expression attenuates TGF-beta-mediated fibrogenesis and protects against liver damage Gastroenterology 135 2008 642 659
65. M. Stopa, D. Anhuf, L. Terstegen, P. Gatsios, A.M. Gressner, and S. Dooley Participation of Smad2, Smad3, and Smad4 in transforming growth factor beta (TGF-beta)-induced activation of Smad7 THE TGF-beta response element of the promoter requires functional Smad binding element and E-box sequences for transcriptional regulation J Biol Chem 275 2000 29308 29317 (Pubitemid 32043801)
66. M. Zeisberg, J. Hanai, H. Sugimoto, T. Mammoto, D. Charytan, F. Strutz, and R. Kalluri BMP-7 counteracts TGF-beta1induced epithelial-to-mesenchymal transition and reverses chronic renal injury Nat Med 9 2003 964 968 (Pubitemid 36889942)
67. B. Grasl-Kraupp, B. Ruttkay-Nedecky, H. Koudelka, K. Bukowska, W. Bursch, and R. Schulte-Hermann In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note Hepatology 21 1995 1465 1468
68. N. Kanno, G. LeSage, S. Glaser, D. Alvaro, and G. Alpini Functional heterogeneity of the intrahepatic biliary epithelium Hepatology 31 2000 555 561 (Pubitemid 30118620)
69. K.L. Cepek, S.K. Shaw, C.M. Parker, G.J. Russell, J.S. Morrow, D.L. Rimm, and M.B. Brenner Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin Nature 372 1994 190 193
70. S. Fu, N. Zhang, A.C. Yopp, D. Chen, M. Mao, H. Zhang, Y. Ding, and J.S. Bromberg TGF-beta induces Foxp3 + T-regulatory cells from CD4+CD25- precursors Am J Transplant 4 2004 1614 1627 (Pubitemid 39312295)
71. T. Kisseleva, H. Uchinami, N. Feirt, O. Quintana-Bustamante, J.C. Segovia, R.F. Schwabe, and D.A. Brenner Bone marrowderived fibrocytes participate in pathogenesis of liver fibrosis J Hepatol 45 2006 429 438 (Pubitemid 44142115)
72. S.J. Forbes, F.P. Russo, V. Rey, P. Burra, M. Rugge, N.A. Wright, and M.R. Alison A significant proportion of myofibroblasts are of bone marrow origin in human liver fibrosis Gastroenterology 126 2004 955 963 (Pubitemid 38451166)
73. S.M. Frisch, and R.A. Screaton Anoikis mechanisms Curr Opin Cell Biol 13 2001 555 562 (Pubitemid 32817013)
74. L. Di Tommaso, A. Destro, J.Y. Seok, E. Balladore, L. Terracciano, A. Sangiovanni, M. Iavarone, M. Colombo, J.J. Jang, E. Yu, S.Y. Jin, E. Morenghi, Y.N. Park, and M. Roncalli The application of markers (HSP70 GPC3 and GS) in liver biopsies is useful for detection of hepatocellular carcinoma J Hepatol 50 2009 746 754
75. L. Di Tommaso, G. Franchi, Y.N. Park, B. Fiamengo, A. Destro, E. Morenghi, M. Montorsi, G. Torzilli, M. Tommasini, L. Terracciano, L. Tornillo, R. Vecchione, and M. Roncalli Diagnostic value of HSP70, glypican 3, and glutamine synthetase in hepatocellular nodules in cirrhosis Hepatology 45 2007 725 734 (Pubitemid 46450624)
76. Y.N. Park, C.P. Yang, G.J. Fernandez, O. Cubukcu, S.N. Thung, and N.D. Theise Neoangiogenesis and sinusoidal "capillarization" in dysplastic nodules of the liver Am J Surg Pathol 22 1998 656 662 (Pubitemid 28280267)
77. M. Roncalli, M. Borzio, and L. Di Tommaso Hepatocellular dysplastic nodules Hepatol Res 37 Suppl 2 2007 S125 S134
78. I.R. Wanless Liver biopsy in the diagnosis of hepatocellular carcinoma Clin Liver Dis 9 2005 281 285
79. O. Falkowski, H.J. An, I.A. Ianus, L. Chiriboga, H. Yee, A.B. West, and N.D. Theise Regeneration of hepatocyte "buds" in cirrhosis from intrabiliary stem cells J Hepatol 39 2003 357 364 (Pubitemid 37070252)
80. S.M. Yoon, D. Gerasimidou, R. Kuwahara, P. Hytiroglou, J.E. Yoo, Y.N. Park, and N.D. Theise Epithelial cell adhesion molecule (EpCAM) marks hepatocytes newly derived from stem/progenitor cells in humans Hepatology 53 2011 964 973
81. J. Bruix, and M. Sherman Management of hepatocellular carcinoma Hepatology 42 2005 1208 1236 (Pubitemid 43112690)
82. T. Kalinski, and A. Roessner Hepatocellular carcinoma: pathology and liver biopsy Dig Dis 27 2009 102 108
83. M. Roncalli Hepatocellular nodules in cirrhosis: focus on diagnostic criteria on liver biopsy: a Western experience Liver Transpl 10 2004 S9 S15
84. R. Jain, S. Fischer, S. Serra, and R. Chetty The use of cytokeratin 19 (CK19) immunohistochemistry in lesions of the pancreas, gastrointestinal tract, and liver Appl Immunohistochem Mol Morphol 18 2010 9 15
85. Y.J. Choi, M.M. Pinto, L. Hao, and A.K. Riba Interobserver variability and aberrant E-cadherin immunostaining of lobular neoplasia and infiltrating lobular carcinoma Mod Pathol 21 2008 1224 1237
86. R. Bergstrom, K. Savary, A. Moren, S. Guibert, C.H. Heldin, R. Ohlsson, and A. Moustakas Transforming growth factor beta promotes complexes between Smad proteins and the CCCTC-binding factor on the H19 imprinting control region chromatin J Biol Chem 285 2010 19727 19737
87. K. Baghy, K. Dezso, V. Laszlo, A. Fullar, B. Peterfia, S. Paku, P. Nagy, Z. Schaff, R.V. Iozzo, and I. Kovalszky Ablation of the decorin gene enhances experimental hepatic fibrosis and impairs hepatic healing in mice Lab Invest 91 2011 439 451
88. H.J. Kahn, A. Marks, H. Thom, and R. Baumal Role of antibody to S100 protein in diagnostic pathology Am J Clin Pathol 79 1983 341 347 (Pubitemid 13164114)
89. T. Vincent, E.P. Neve, J.R. Johnson, A. Kukalev, F. Rojo, J. Albanell, K. Pietras, I. Virtanen, L. Philipson, P.L. Leopold, R.G. Crystal, A.G. de Herreros, A. Moustakas, R.F. Pettersson, and J. Fuxe A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition Nat Cell Biol 11 2009 943 950
90. Q. Li, S.A. Pangas, C.J. Jorgez, J.M. Graff, M. Weinstein, and M.M. Matzuk Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo Mol Cell Biol 28 2008 7001 7011
91. N. Bardeesy, K.H. Cheng, J.H. Berger, G.C. Chu, J. Pahler, P. Olson, A.F. Hezel, J. Horner, G.Y. Lauwers, D. Hanahan, and R.A. DePinho Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer Genes Dev 20 2006 3130 3146 (Pubitemid 44790628)
92. J.L. Hornick, G.Y. Lauwers, and R.D. Odze Immunohistochemistry can help distinguish metastatic pancreatic adenocarcinomas from bile duct adenomas and hamartomas of the liver Am J Surg Pathol 29 2005 381 389 (Pubitemid 40321975)
93. C. Van Themsche, P. Chaudhry, V. Leblanc, S. Parent, and E. Asselin XIAP gene expression and function is regulated by autocrine and paracrine TGF-beta signaling Mol Cancer 9 2010 216
94. F. Louafi, R.T. Martinez-Nunez, and T. Sanchez-Elsner MicroRNA-155 targets SMAD2 and modulates the response of macrophages to transforming growth factor-{beta} J Biol Chem 285 2010 41328 41336
95. M. Kondo, E. Cubillo, K. Tobiume, T. Shirakihara, N. Fukuda, H. Suzuki, K. Shimizu, K. Takehara, A. Cano, M. Saitoh, and K. Miyazono A role for Id in the regulation of TGF-beta-induced epithelial-mesenchymal transdifferentiation Cell Death Differ 11 2004 1092 1101 (Pubitemid 39341635)
96. Rachakonda G, Sekhar KR, Jowhar D, Samson PC, Wikswo JP, Beauchamp RD, Datta PK, Freeman ML: Increased cell migration and plasticity in Nrf2-deficient cancer cell lines. Oncogene 29:37033714
97. W. Huang, Y. Zhang, S. Varambally, A.M. Chinnaiyan, M. Banerjee, S.D. Merajver, and C.G. Kleer Inhibition of CCN6 (Wnt-1-induced signaling protein 3) down-regulates E-cadherin in the breast epithelium through induction of snail and ZEB1 Am J Pathol 172 2008 893 904 (Pubitemid 351519987)
98. G. Tzur, A. Israel, A. Levy, H. Benjamin, E. Meiri, Y. Shufaro, K. Meir, E. Khvalevsky, Y. Spector, N. Rojansky, Z. Bentwich, B.E. Reubinoff, and E. Galun Comprehensive gene and microRNA expression profiling reveals a role for microRNA in human liver development PLoS One 4 2009 e7511
99. N. Azumi, and H. Battifora The distribution of vimentin and keratin in epithelial and nonepithelial neoplasms: a comprehensive immunohistochemical study on formalin- and alcohol-fixed tumors Am J Clin Pathol 88 1987 286 296 (Pubitemid 17145592)