Skip to main content
Erschienen in: Virchows Archiv 6/2011

01.06.2011 | Original Article

Claudins and tricellulin in fibrolamellar hepatocellular carcinoma

verfasst von: Attila Patonai, Boglárka Erdélyi-Belle, Anna Korompay, Áron Somorácz, Beate K. Straub, Peter Schirmacher, Ilona Kovalszky, Gábor Lotz, András Kiss, Zsuzsa Schaff

Erschienen in: Virchows Archiv | Ausgabe 6/2011

Einloggen, um Zugang zu erhalten

Abstract

Fibrolamellar hepatocellular carcinoma is a subtype of hepatocellular carcinoma occurring in non-cirrhotic liver at a younger age. The tumor expresses both hepatocellular and cholangiocellular markers. Previously, our group described overexpression of tight junction protein claudin 4 in cholangiocellular carcinoma in contrast to hepatocellular carcinoma. In the present study, tight junction protein expressions were studied to possibly clarify bipotential lineage of fibrolamellar hepatocellular carcinoma. Eleven fibrolamellar hepatocellular carcinomas were compared with seven “conventional” hepatocellular carcinomas, seven cholangiocellular carcinomas, and five normal liver samples. By immunohistochemistry, all fibrolamellar hepatocellular carcinomas were positive for HepPar1 and cytokeratins 7, 8, and 18, but negative for cytokeratin 19. Glypican-3 gave weak staining in two cases. Expression of claudin 1 was lower, while that of claudin 2 was higher in fibrolamellar hepatocellular carcinomas than in other tumors. Claudins 3, 4, and 7 were not detectable in fibrolamellar hepatocellular carcinomas as in the majority of “conventional” hepatocellular carcinomas, contrary to high expression observed in cholangiocellular carcinomas. Focal or diffuse claudin 5 expression was detected in nine of 11 fibrolamellar hepatocellular carcinomas contrary to other tumors. Tricellulin was significantly downregulated in all tumors compared with normal liver. Our findings showed claudins to exhibit specific expression patterns in fibrolamellar hepatocellular carcinomas not observed in other primary liver tumors, with unique claudin 5 expression and pattern features similar to common hepatocellular carcinoma, but different from cholangiocellular carcinoma. This is the first report describing the loss of tricellulin expression in human hepatic tumors.
Literatur
1.
Zurück zum Zitat Abdul-Al HM, Wang G, Makhlouf HR, Goodman ZD (2010) Fibrolamellar hepatocellular carcinoma: an immunohistochemical comparison with conventional hepatocellular carcinoma. Int J Surg Pathol 18:313–318PubMed Abdul-Al HM, Wang G, Makhlouf HR, Goodman ZD (2010) Fibrolamellar hepatocellular carcinoma: an immunohistochemical comparison with conventional hepatocellular carcinoma. Int J Surg Pathol 18:313–318PubMed
2.
Zurück zum Zitat Ishak KG, Goodman ZD, Stocker JT (2001) Tumors of the Liver and Intrahepatic Bile Ducts. Atlas of Tumor Pathology, Third Series, Fascicle 31. Armed Forces Institute of Pathology, Washington, DC Ishak KG, Goodman ZD, Stocker JT (2001) Tumors of the Liver and Intrahepatic Bile Ducts. Atlas of Tumor Pathology, Third Series, Fascicle 31. Armed Forces Institute of Pathology, Washington, DC
3.
Zurück zum Zitat Kannangai R, Vivekanandan P, Martinez-Murillo F, Choti M, Torbenson M (2007) Fibrolamellar carcinomas show overexpression of genes in the RAS, MAPK, PIK3, and xenobiotic degradation pathways. Hum Pathol 38:639–644PubMedCrossRef Kannangai R, Vivekanandan P, Martinez-Murillo F, Choti M, Torbenson M (2007) Fibrolamellar carcinomas show overexpression of genes in the RAS, MAPK, PIK3, and xenobiotic degradation pathways. Hum Pathol 38:639–644PubMedCrossRef
4.
Zurück zum Zitat Liu S, Chan KW, Wang B, Qiao L (2009) Fibrolamellar hepatocellular carcinoma. Am J Gastroenterol 104:2617–2624PubMedCrossRef Liu S, Chan KW, Wang B, Qiao L (2009) Fibrolamellar hepatocellular carcinoma. Am J Gastroenterol 104:2617–2624PubMedCrossRef
5.
Zurück zum Zitat Torbenson M (2007) Review of the clinicopathologic features of fibrolamellar carcinoma. Adv Anat Pathol 14:217–223PubMedCrossRef Torbenson M (2007) Review of the clinicopathologic features of fibrolamellar carcinoma. Adv Anat Pathol 14:217–223PubMedCrossRef
6.
Zurück zum Zitat Ward SC, Huang J, Tickoo SK, Thung SN, Ladanyi M, Klimstra DS (2010) Fibrolamellar carcinoma of the liver exhibits immunohistochemical evidence of both hepatocyte and bile duct differentiation. Mod Pathol 23:1180–1190PubMedCrossRef Ward SC, Huang J, Tickoo SK, Thung SN, Ladanyi M, Klimstra DS (2010) Fibrolamellar carcinoma of the liver exhibits immunohistochemical evidence of both hepatocyte and bile duct differentiation. Mod Pathol 23:1180–1190PubMedCrossRef
7.
Zurück zum Zitat Craig JR, Peters RL, Edmondson HA, Omata M (1980) Fibrolamellar carcinoma of the liver: a tumor of adolescents and young adults with distinctive clinico-pathologic features. Cancer 46:372–379PubMedCrossRef Craig JR, Peters RL, Edmondson HA, Omata M (1980) Fibrolamellar carcinoma of the liver: a tumor of adolescents and young adults with distinctive clinico-pathologic features. Cancer 46:372–379PubMedCrossRef
8.
Zurück zum Zitat El-Serag HB, Davila JA (2004) Is fibrolamellar carcinoma different from hepatocellular carcinoma? A US population-based study. Hepatology 39:798–803PubMedCrossRef El-Serag HB, Davila JA (2004) Is fibrolamellar carcinoma different from hepatocellular carcinoma? A US population-based study. Hepatology 39:798–803PubMedCrossRef
9.
Zurück zum Zitat Arista-Nasr J, Gutierrez-Villalobos L, Nuncio J, Maldonaldo H, Bornstein-Quevedo L (2002) Fibrolamellar hepatocellular carcinoma in Mexican patients. Pathol Oncol Res 8:133–137PubMedCrossRef Arista-Nasr J, Gutierrez-Villalobos L, Nuncio J, Maldonaldo H, Bornstein-Quevedo L (2002) Fibrolamellar hepatocellular carcinoma in Mexican patients. Pathol Oncol Res 8:133–137PubMedCrossRef
10.
Zurück zum Zitat Górnicka B, Ziarkiewicz-Wróblewska B, Wróblewski T, Wilczynski GM, Koperski L, Krawczyk M, Wasiutynski A (2005) Carcinoma, a fibrolamellar variant—immunohistochemical analysis of 4 cases. Hepatogastroenterology 52:519–523PubMed Górnicka B, Ziarkiewicz-Wróblewska B, Wróblewski T, Wilczynski GM, Koperski L, Krawczyk M, Wasiutynski A (2005) Carcinoma, a fibrolamellar variant—immunohistochemical analysis of 4 cases. Hepatogastroenterology 52:519–523PubMed
11.
Zurück zum Zitat Chang YC, Dai YC, Chow NH (2003) Fibrolamellar hepatocellular carcinoma with a recurrence of classic hepatocellular carcinoma: a case report and review of Oriental cases. Hepatogastroenterology 50:1637–1640PubMed Chang YC, Dai YC, Chow NH (2003) Fibrolamellar hepatocellular carcinoma with a recurrence of classic hepatocellular carcinoma: a case report and review of Oriental cases. Hepatogastroenterology 50:1637–1640PubMed
12.
Zurück zum Zitat Davison FD, Fagan EA, Portmann B, Williams R (1990) HBV-DNA sequences in tumor and nontumor tissue in a patient with the fibrolamellar variant of hepatocellular carcinoma. Hepatology 12:676–679PubMedCrossRef Davison FD, Fagan EA, Portmann B, Williams R (1990) HBV-DNA sequences in tumor and nontumor tissue in a patient with the fibrolamellar variant of hepatocellular carcinoma. Hepatology 12:676–679PubMedCrossRef
13.
Zurück zum Zitat Lapis K, Zs S, Kopper L, Karácsonyi S, Ormos J (1990) Fibrolamellar carcinomas of the liver. Zentralbl Allg Pathol Pathol Anat 136:135–149 Lapis K, Zs S, Kopper L, Karácsonyi S, Ormos J (1990) Fibrolamellar carcinomas of the liver. Zentralbl Allg Pathol Pathol Anat 136:135–149
14.
Zurück zum Zitat Malouf G, Falissard B, Azoulay D, Callea F, Ferrell LD, Goodman ZD, Hayashi Y, Hsu HC, Hubscher SG, Kojiro M, Ng IO, Paterson AC, Reynes M, Zafrani ES, Emile JF (2009) Is histological diagnosis of primary liver carcinomas with fibrous stroma reproducible among experts? J Clin Pathol 62:519–524PubMedCrossRef Malouf G, Falissard B, Azoulay D, Callea F, Ferrell LD, Goodman ZD, Hayashi Y, Hsu HC, Hubscher SG, Kojiro M, Ng IO, Paterson AC, Reynes M, Zafrani ES, Emile JF (2009) Is histological diagnosis of primary liver carcinomas with fibrous stroma reproducible among experts? J Clin Pathol 62:519–524PubMedCrossRef
15.
Zurück zum Zitat Lee J-S, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, Mikaelyan A, Roberts LR, Demetris AJ, Sun Z, Nevens F, Roskams T, Thorgeirsson SS (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12:410–416PubMedCrossRef Lee J-S, Heo J, Libbrecht L, Chu IS, Kaposi-Novak P, Calvisi DF, Mikaelyan A, Roberts LR, Demetris AJ, Sun Z, Nevens F, Roskams T, Thorgeirsson SS (2006) A novel prognostic subtype of human hepatocellular carcinoma derived from hepatic progenitor cells. Nat Med 12:410–416PubMedCrossRef
16.
Zurück zum Zitat Kakar S, Chen X, Ho C, Burgart LJ, Sahai V, Dachrut S, Yabes A, Jain D, Ferrell LD (2009) Chromosomal changes in fibrolamellar hepatocellular carcinoma detected by array comparative genomic hybridization. Hum Pathol 22:134–141 Kakar S, Chen X, Ho C, Burgart LJ, Sahai V, Dachrut S, Yabes A, Jain D, Ferrell LD (2009) Chromosomal changes in fibrolamellar hepatocellular carcinoma detected by array comparative genomic hybridization. Hum Pathol 22:134–141
17.
Zurück zum Zitat International Consensus Group for Hepatocellular Neoplasia (2009) Pathologic diagnosis of early hepatocellular carcinoma: a report of the International Consensus Group for Hepatocellular Neoplasia. Hepatology 49:658–664CrossRef International Consensus Group for Hepatocellular Neoplasia (2009) Pathologic diagnosis of early hepatocellular carcinoma: a report of the International Consensus Group for Hepatocellular Neoplasia. Hepatology 49:658–664CrossRef
18.
Zurück zum Zitat Libbrecht L, Severi T, Cassiman D, Vander Borght S, Pirenne J, Nevens F, Verslype C, van Pelt J, Roskams T (2006) Glypican-3 expression distinguishes small hepatocellular carcinomas from cirrhosis, dysplastic nodules, and focal nodular hyperplasia-like nodules. Am J Surg Pathol 30:1405–1411PubMedCrossRef Libbrecht L, Severi T, Cassiman D, Vander Borght S, Pirenne J, Nevens F, Verslype C, van Pelt J, Roskams T (2006) Glypican-3 expression distinguishes small hepatocellular carcinomas from cirrhosis, dysplastic nodules, and focal nodular hyperplasia-like nodules. Am J Surg Pathol 30:1405–1411PubMedCrossRef
19.
Zurück zum Zitat Cs L, Szabó E, Holczbauer Á, Batmunkh E, Szíjártó A, Kupcsulik P, Kovalszky I, Paku S, Illyés G, Kiss A, Schaff Z (2006) Claudin-4 differentiates biliary tract cancers from hepatocellular carcinomas. Mod Pathol 19:460–469CrossRef Cs L, Szabó E, Holczbauer Á, Batmunkh E, Szíjártó A, Kupcsulik P, Kovalszky I, Paku S, Illyés G, Kiss A, Schaff Z (2006) Claudin-4 differentiates biliary tract cancers from hepatocellular carcinomas. Mod Pathol 19:460–469CrossRef
20.
Zurück zum Zitat Zs N, Szász AM, Tátrai P, Németh J, Gyorffy H, Somorácz A, Szíjártó A, Kupcsulik P, Kiss A, Schaff Z (2009) Claudin-1, -2, -3, -4, -7, -8, and -10 protein expression in biliary tract cancers. J Histochem Cytochem 57:113–121 Zs N, Szász AM, Tátrai P, Németh J, Gyorffy H, Somorácz A, Szíjártó A, Kupcsulik P, Kiss A, Schaff Z (2009) Claudin-1, -2, -3, -4, -7, -8, and -10 protein expression in biliary tract cancers. J Histochem Cytochem 57:113–121
21.
Zurück zum Zitat Nishino R, Honda M, Yamashita T, Takatori H, Minato H, Zen Y, Sasaki M, Takamura H, Horimoto K, Ohta T, Nakanuma Y, Kaneko S (2008) Identification of novel candidate tumour marker genes for intrahepatic cholangiocarcinoma. J Hepatol 49:207–216PubMedCrossRef Nishino R, Honda M, Yamashita T, Takatori H, Minato H, Zen Y, Sasaki M, Takamura H, Horimoto K, Ohta T, Nakanuma Y, Kaneko S (2008) Identification of novel candidate tumour marker genes for intrahepatic cholangiocarcinoma. J Hepatol 49:207–216PubMedCrossRef
22.
Zurück zum Zitat Balda MS, Matter K (2008) Tight junctions and the regulation of gene expression. Biochim Biophys Acta 1788:761–767PubMed Balda MS, Matter K (2008) Tight junctions and the regulation of gene expression. Biochim Biophys Acta 1788:761–767PubMed
24.
Zurück zum Zitat Saeki R, Kondoh M, Kakutani H (2009) A novel tumor-targeted therapy using a claudin-4-targeting molecule. Mol Pharmacol 76:918–926PubMedCrossRef Saeki R, Kondoh M, Kakutani H (2009) A novel tumor-targeted therapy using a claudin-4-targeting molecule. Mol Pharmacol 76:918–926PubMedCrossRef
25.
Zurück zum Zitat Tsukita S, Yamazaki Y, Katsuno T, Tamura A, Tsukita S (2008) Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 27:6930–6938PubMedCrossRef Tsukita S, Yamazaki Y, Katsuno T, Tamura A, Tsukita S (2008) Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 27:6930–6938PubMedCrossRef
26.
Zurück zum Zitat Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801–805PubMedCrossRef Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM (2007) Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446:801–805PubMedCrossRef
27.
Zurück zum Zitat Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, Cosset FL, Dragic T (2008) The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 82:3555–3560PubMedCrossRef Meertens L, Bertaux C, Cukierman L, Cormier E, Lavillette D, Cosset FL, Dragic T (2008) The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. J Virol 82:3555–3560PubMedCrossRef
28.
Zurück zum Zitat Higashi Y, Suzuki S, Sakaguchi T, Nakamura T, Baba S, Reinecker HC, Nakamura S, Konno H (2007) Loss of claudin-1 expression correlates with malignancy of hepatocellular carcinoma. J Surg Res 139:68–76PubMedCrossRef Higashi Y, Suzuki S, Sakaguchi T, Nakamura T, Baba S, Reinecker HC, Nakamura S, Konno H (2007) Loss of claudin-1 expression correlates with malignancy of hepatocellular carcinoma. J Surg Res 139:68–76PubMedCrossRef
29.
Zurück zum Zitat Shen L, Weber CR, Turner JR (2008) The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J Cell Biol 181:683–695PubMedCrossRef Shen L, Weber CR, Turner JR (2008) The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state. J Cell Biol 181:683–695PubMedCrossRef
30.
Zurück zum Zitat Steed E, Balda MS, Matter K (2010) Dynamics and functions of tight junctions. Trends Cell Biol 20:142–149PubMedCrossRef Steed E, Balda MS, Matter K (2010) Dynamics and functions of tight junctions. Trends Cell Biol 20:142–149PubMedCrossRef
31.
Zurück zum Zitat Förster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130:55–70PubMedCrossRef Förster C (2008) Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 130:55–70PubMedCrossRef
32.
Zurück zum Zitat Martin TA, Jiang WG (2009) Loss of tight junction barrier function and its role in cancer metastasis. Biochim Biophys Acta 1788:872–891PubMedCrossRef Martin TA, Jiang WG (2009) Loss of tight junction barrier function and its role in cancer metastasis. Biochim Biophys Acta 1788:872–891PubMedCrossRef
33.
Zurück zum Zitat Ouban A, Ahmed AA (2010) Claudins in human cancer: a review. Histol Histopathol 25:83–90PubMed Ouban A, Ahmed AA (2010) Claudins in human cancer: a review. Histol Histopathol 25:83–90PubMed
34.
Zurück zum Zitat Sawada N, Murata M, Kikuchi K, Osanai M, Tobioka H, Kojima T, Chiba H (2003) Tight junctions and human diseases. Med Electron Microsc 36:147–156PubMedCrossRef Sawada N, Murata M, Kikuchi K, Osanai M, Tobioka H, Kojima T, Chiba H (2003) Tight junctions and human diseases. Med Electron Microsc 36:147–156PubMedCrossRef
35.
Zurück zum Zitat Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ (2010) Claudin-1 acts through c-Abl-protein kinase Cdelta (PKCdelta) signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 285:226–233PubMedCrossRef Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ (2010) Claudin-1 acts through c-Abl-protein kinase Cdelta (PKCdelta) signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 285:226–233PubMedCrossRef
36.
Zurück zum Zitat Kojima T, Murata M, Yamamoto T, Lan M, Imamura M, Son S, Takano K, Yamaguchi H, Ito T, Tanaka S, Chiba H, Hirata K, Sawada N (2009) Tight junction proteins and signal transduction pathways in hepatocytes. Histol Histopathol 24:1463–1472PubMed Kojima T, Murata M, Yamamoto T, Lan M, Imamura M, Son S, Takano K, Yamaguchi H, Ito T, Tanaka S, Chiba H, Hirata K, Sawada N (2009) Tight junction proteins and signal transduction pathways in hepatocytes. Histol Histopathol 24:1463–1472PubMed
37.
Zurück zum Zitat Rahner C, Mitic LL, Anderson JM (2001) Heterogeneity in expression and Subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas and gut. Gastroenterology 120:411–422PubMedCrossRef Rahner C, Mitic LL, Anderson JM (2001) Heterogeneity in expression and Subcellular localization of claudins 2, 3, 4, and 5 in the rat liver, pancreas and gut. Gastroenterology 120:411–422PubMedCrossRef
38.
Zurück zum Zitat Ikari A, Atomi K, Takiguchi A, Yamazaki Y, Miwa M, Sugatani J (2009) Epidermal growth factor increases claudin-4 expression mediated by Sp1 elevation in MDCK cells. Biochem Biophys Res Commun 384:306–310PubMedCrossRef Ikari A, Atomi K, Takiguchi A, Yamazaki Y, Miwa M, Sugatani J (2009) Epidermal growth factor increases claudin-4 expression mediated by Sp1 elevation in MDCK cells. Biochem Biophys Res Commun 384:306–310PubMedCrossRef
39.
Zurück zum Zitat Bello IO, Vilen S-T, Niinimaa A, Kantola S, Soini Y, Salo T (2008) Expression of claudins 1, 4, 5, and 7 and occludin, and relationship with prognosis in squamous cell carcinoma of the tongue. Hum Pathol 39:1212–1220PubMedCrossRef Bello IO, Vilen S-T, Niinimaa A, Kantola S, Soini Y, Salo T (2008) Expression of claudins 1, 4, 5, and 7 and occludin, and relationship with prognosis in squamous cell carcinoma of the tongue. Hum Pathol 39:1212–1220PubMedCrossRef
40.
Zurück zum Zitat Dos Reis PP, Bharadwaj RR, Machado J, Macmillan C, Pintilie M, Sukhai MA, Perez-Ordonez B, Gullane P, Irish J, Kamel-Reid S (2008) Claudin 1 overexpression increases invasion and is associated with aggressive histological features in oral squamous cell carcinoma. Cancer 113:3169–3180PubMedCrossRef Dos Reis PP, Bharadwaj RR, Machado J, Macmillan C, Pintilie M, Sukhai MA, Perez-Ordonez B, Gullane P, Irish J, Kamel-Reid S (2008) Claudin 1 overexpression increases invasion and is associated with aggressive histological features in oral squamous cell carcinoma. Cancer 113:3169–3180PubMedCrossRef
41.
Zurück zum Zitat Paschoud S, Bongiovanni M, Pache J-C, Citi S (2007) Claudin-1 and claudin-5 expression patterns differentiate lung squamous cell carcinomas from adenocarcinomas. Mod Pathol 20:947–954PubMedCrossRef Paschoud S, Bongiovanni M, Pache J-C, Citi S (2007) Claudin-1 and claudin-5 expression patterns differentiate lung squamous cell carcinomas from adenocarcinomas. Mod Pathol 20:947–954PubMedCrossRef
42.
Zurück zum Zitat Sobel G, Cs P, Szabó I, Kiss A, Kádár A, Schaff Z (2005) Increased expression of claudins in cervical squamous intraepithelial neoplasia and invasive carcinoma. Hum Pathol 36:162–169PubMedCrossRef Sobel G, Cs P, Szabó I, Kiss A, Kádár A, Schaff Z (2005) Increased expression of claudins in cervical squamous intraepithelial neoplasia and invasive carcinoma. Hum Pathol 36:162–169PubMedCrossRef
43.
Zurück zum Zitat Tőkés AM, Kulka J, Paku S, Szik A, Páska C, Novák PK, Szilák L, Kiss A, Bögi K, Schaff Z (2005) Claudin −1, -3 and -4 proteins and mRNA expression in benign and malignant breast lesions: a research study. Breast Cancer Res 7:R296–R305PubMedCrossRef Tőkés AM, Kulka J, Paku S, Szik A, Páska C, Novák PK, Szilák L, Kiss A, Bögi K, Schaff Z (2005) Claudin −1, -3 and -4 proteins and mRNA expression in benign and malignant breast lesions: a research study. Breast Cancer Res 7:R296–R305PubMedCrossRef
44.
Zurück zum Zitat Szabó I, Kiss A, Zs S, Sobel G (2009) Claudins as diagnostic and prognostic markers in gynecological cancer. Histol Histopathol 24:1607–1615PubMed Szabó I, Kiss A, Zs S, Sobel G (2009) Claudins as diagnostic and prognostic markers in gynecological cancer. Histol Histopathol 24:1607–1615PubMed
45.
Zurück zum Zitat Resnick MB, Konkin T, Routhier J, Sabo E, Pricolo VE (2005) Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod Pathol 18:511–518PubMedCrossRef Resnick MB, Konkin T, Routhier J, Sabo E, Pricolo VE (2005) Claudin-1 is a strong prognostic indicator in stage II colonic cancer: a tissue microarray study. Mod Pathol 18:511–518PubMedCrossRef
46.
Zurück zum Zitat Soini Y (2004) Claudins 2, 3, 4, and 5 in Paget’s disease and breast carcinoma. Hum Pathol 35:1531–1536PubMedCrossRef Soini Y (2004) Claudins 2, 3, 4, and 5 in Paget’s disease and breast carcinoma. Hum Pathol 35:1531–1536PubMedCrossRef
47.
Zurück zum Zitat Soini Y (2005) Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours. Histopathology 46:551–560PubMedCrossRef Soini Y (2005) Expression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours. Histopathology 46:551–560PubMedCrossRef
48.
Zurück zum Zitat Van Itallie CM, Holmes J, Bridges A, Anderson JM (2009) Claudin-2-dependent changes in noncharged solute flux are mediated by the extracellular domains and require attachment to the PDZ-scaffold. Ann NY Acad Sci 1165:82–87PubMedCrossRef Van Itallie CM, Holmes J, Bridges A, Anderson JM (2009) Claudin-2-dependent changes in noncharged solute flux are mediated by the extracellular domains and require attachment to the PDZ-scaffold. Ann NY Acad Sci 1165:82–87PubMedCrossRef
49.
Zurück zum Zitat Sobel G, Németh J, Kiss A, Lotz G, Szabó I, Udvarhelyi N, Schaff Z, Páska C (2006) Claudin 1 differentiates endometrioid and serous papillary endometrial adenocarcinoma. Gynecol Oncol 103:591–598PubMedCrossRef Sobel G, Németh J, Kiss A, Lotz G, Szabó I, Udvarhelyi N, Schaff Z, Páska C (2006) Claudin 1 differentiates endometrioid and serous papillary endometrial adenocarcinoma. Gynecol Oncol 103:591–598PubMedCrossRef
50.
Zurück zum Zitat Amasheh S, Schmidt T, Mahn M, Florian P, Mankertz J, Tavalali S, Gitter AH, Schulzke JD, Fromm M (2005) Expression of claudin-5 contributes to barrier properties in tight junctions of epithelial cells. Cell Tissue Res 321:89–96PubMedCrossRef Amasheh S, Schmidt T, Mahn M, Florian P, Mankertz J, Tavalali S, Gitter AH, Schulzke JD, Fromm M (2005) Expression of claudin-5 contributes to barrier properties in tight junctions of epithelial cells. Cell Tissue Res 321:89–96PubMedCrossRef
51.
Zurück zum Zitat Kojima S, Rahner C, Peng S, Rizzolo LJ (2002) Claudin 5 is transiently expressed during the development of the retinal pigment epithelium. J Membr Biol 186:81–88PubMedCrossRef Kojima S, Rahner C, Peng S, Rizzolo LJ (2002) Claudin 5 is transiently expressed during the development of the retinal pigment epithelium. J Membr Biol 186:81–88PubMedCrossRef
52.
Zurück zum Zitat Jakab C, Rusvai M, Gálfi P, Mándoki M, Demeter Z, Szabó Z, Kulka J (2009) Expression of claudin-5 in hepatoid gland biopsies. Vet Dermatol 21:276–281CrossRef Jakab C, Rusvai M, Gálfi P, Mándoki M, Demeter Z, Szabó Z, Kulka J (2009) Expression of claudin-5 in hepatoid gland biopsies. Vet Dermatol 21:276–281CrossRef
53.
Zurück zum Zitat Comper F, Antonello D, Beghelli S, Gobbo S, Montagna L, Pederzoli P, Chilosi M, Scarpa A (2009) Expression pattern of claudins 5 and 7 distinguishes solid-pseudopapillary from pancreatoblastoma, acinar cell and endocrine tumors of the pancreas. Am J Surg Pathol 33:768–774PubMedCrossRef Comper F, Antonello D, Beghelli S, Gobbo S, Montagna L, Pederzoli P, Chilosi M, Scarpa A (2009) Expression pattern of claudins 5 and 7 distinguishes solid-pseudopapillary from pancreatoblastoma, acinar cell and endocrine tumors of the pancreas. Am J Surg Pathol 33:768–774PubMedCrossRef
54.
Zurück zum Zitat Burek M, Arias-Loza PA, Roewer N, Förster CY (2010) Claudin-5 as a novel estrogen target in vascular endothelium. Arterioscler Thromb Vasc Biol 30:298–304PubMedCrossRef Burek M, Arias-Loza PA, Roewer N, Förster CY (2010) Claudin-5 as a novel estrogen target in vascular endothelium. Arterioscler Thromb Vasc Biol 30:298–304PubMedCrossRef
55.
Zurück zum Zitat Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S (2005) Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171:939–945PubMedCrossRef Ikenouchi J, Furuse M, Furuse K, Sasaki H, Tsukita S, Tsukita S (2005) Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 171:939–945PubMedCrossRef
56.
Zurück zum Zitat Westphal JK, Dörfel MJ, Krug SM, Cording JD, Piontek J, Blasig IE, Tauber R, Fromm M, Huber O (2010) Tricellulin forms homomeric and heteromeric tight junctional complexes. Cell Mol Life Sci 67:2057–2068PubMedCrossRef Westphal JK, Dörfel MJ, Krug SM, Cording JD, Piontek J, Blasig IE, Tauber R, Fromm M, Huber O (2010) Tricellulin forms homomeric and heteromeric tight junctional complexes. Cell Mol Life Sci 67:2057–2068PubMedCrossRef
57.
Zurück zum Zitat Krug SM, Amasheh S, Richter JF, Milatz S, Günzel D, Westphal JK, Huber O, Schulzke JD, Fromm M (2009) Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol Biol 20:3713–3724 Krug SM, Amasheh S, Richter JF, Milatz S, Günzel D, Westphal JK, Huber O, Schulzke JD, Fromm M (2009) Tricellulin forms a barrier to macromolecules in tricellular tight junctions without affecting ion permeability. Mol Biol 20:3713–3724
Metadaten
Titel
Claudins and tricellulin in fibrolamellar hepatocellular carcinoma
verfasst von
Attila Patonai
Boglárka Erdélyi-Belle
Anna Korompay
Áron Somorácz
Beate K. Straub
Peter Schirmacher
Ilona Kovalszky
Gábor Lotz
András Kiss
Zsuzsa Schaff
Publikationsdatum
01.06.2011
Verlag
Springer-Verlag
Erschienen in
Virchows Archiv / Ausgabe 6/2011
Print ISSN: 0945-6317
Elektronische ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-011-1077-y

Weitere Artikel der Ausgabe 6/2011

Virchows Archiv 6/2011 Zur Ausgabe

Neu im Fachgebiet Pathologie

Molekularpathologische Untersuchungen im Wandel der Zeit

Open Access Biomarker Leitthema

Um auch an kleinen Gewebeproben zuverlässige und reproduzierbare Ergebnisse zu gewährleisten ist eine strenge Qualitätskontrolle in jedem Schritt des Arbeitsablaufs erforderlich. Eine nicht ordnungsgemäße Prüfung oder Behandlung des …

Vergleichende Pathologie in der onkologischen Forschung

Pathologie Leitthema

Die vergleichende experimentelle Pathologie („comparative experimental pathology“) ist ein Fachbereich an der Schnittstelle von Human- und Veterinärmedizin. Sie widmet sich der vergleichenden Erforschung von Gemeinsamkeiten und Unterschieden von …

Gastrointestinale Stromatumoren

Open Access GIST CME-Artikel

Gastrointestinale Stromatumoren (GIST) stellen seit über 20 Jahren ein Paradigma für die zielgerichtete Therapie mit Tyrosinkinaseinhibitoren dar. Eine elementare Voraussetzung für eine mögliche neoadjuvante oder adjuvante Behandlung bei …

Personalisierte Medizin in der Onkologie

Aufgrund des erheblichen technologischen Fortschritts in der molekularen und genetischen Diagnostik sowie zunehmender Erkenntnisse über die molekulare Pathogenese von Krankheiten hat in den letzten zwei Jahrzehnten ein grundlegender …