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Erschienen in: Medical Molecular Morphology 1/2019

28.06.2018 | Original Paper

Immunoreactivity patterns of tight junction proteins are useful for differential diagnosis of human salivary gland tumors

verfasst von: Tomoyuki Aoyama, Akira Takasawa, Masaki Murata, Makoto Osanai, Kenichi Takano, Tadashi Hasagawa, Norimasa Sawada

Erschienen in: Medical Molecular Morphology | Ausgabe 1/2019

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Abstract

The expression pattern of tight junction proteins (TJPs) varies among organs and tumor types. In this study, we examined the immunoreactivity of claudin (CLDN)-1, -4, and -7, and JAM-A in salivary gland tumors (SGTs) by histological types and cell types to estimate their usefulness as differential diagnostic markers. Immunoreactivity of CLDN1 was higher in ductal epithelium cells of SGTs than in non-tumor tissues. Conversely, immunoreactivity of CLDN1 was significantly decreased in basal/myoepithelium cells of SGTs compared with that in non-tumor tissues. There was no significant difference between the immunoreactivity of CLDN1 in benign tumors and that in malignant tumors. Immunoreactivity of CLDN4, CLDN7, and JAM-A in ductal epithelium cells was higher in many SGTs than in non-tumor tissues. There was a difference depending on the histological type of SGT in immunoreactivity of CLDN4, CLDN7, and JAM-A in basaloid/myoepithelial cells. It was possible to classify SGTs by a hierarchical clustering using immunoreactivity of TJPs. The results suggest that an immunohistochemical marker panel including these TJPs may be useful for differential diagnosis of SGTs and that CLDN1 is associated with tumorigenesis of SGTs.
Literatur
1.
Zurück zum Zitat Anderson JM, Cereijido M (2001) Tight junctions, 2nd edn. CRC Press, Boca Raton, pp 1–18 Anderson JM, Cereijido M (2001) Tight junctions, 2nd edn. CRC Press, Boca Raton, pp 1–18
2.
Zurück zum Zitat Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293CrossRefPubMed Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293CrossRefPubMed
3.
Zurück zum Zitat Chiba H, Osanai M, Murata M, Kojima T, Sawada N (2008) Transmembrane proteins of tight junctions. Biochim Biophys Acta 1778:588–600CrossRefPubMed Chiba H, Osanai M, Murata M, Kojima T, Sawada N (2008) Transmembrane proteins of tight junctions. Biochim Biophys Acta 1778:588–600CrossRefPubMed
4.
Zurück zum Zitat Severson EA, Parkos C (2009) Structural determinants of junctional adhesion molecule A (JAM-A) function and mechanisms of intracellular signaling. Curr Opin Cell Biol 21:701–707CrossRefPubMedPubMedCentral Severson EA, Parkos C (2009) Structural determinants of junctional adhesion molecule A (JAM-A) function and mechanisms of intracellular signaling. Curr Opin Cell Biol 21:701–707CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Takano K, Kojima T, Sawada N, Himi T (2014) Role of tight junctions in signal transduction: an update. EXCLI J 13:1145–1162PubMedPubMedCentral Takano K, Kojima T, Sawada N, Himi T (2014) Role of tight junctions in signal transduction: an update. EXCLI J 13:1145–1162PubMedPubMedCentral
7.
Zurück zum Zitat Osanai M, Takasawa A, Murata M, Sawada N (2017) Claudins in cancer: bench to bedside. Pflugers Arch 469:55–67CrossRefPubMed Osanai M, Takasawa A, Murata M, Sawada N (2017) Claudins in cancer: bench to bedside. Pflugers Arch 469:55–67CrossRefPubMed
8.
Zurück zum Zitat Katahira J, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N (1997) Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J Cell Biol 136:1239–1247CrossRefPubMedPubMedCentral Katahira J, Inoue N, Horiguchi Y, Matsuda M, Sugimoto N (1997) Molecular cloning and functional characterization of the receptor for Clostridium perfringens enterotoxin. J Cell Biol 136:1239–1247CrossRefPubMedPubMedCentral
9.
Zurück zum Zitat Smedley JG III, Uzal FA, McClane BA (2007) Identification of a prepore large-complex stage in the mechanism of action of Clostridium perfringens enterotoxin. Infect Immun 75:2381–2390CrossRefPubMedPubMedCentral Smedley JG III, Uzal FA, McClane BA (2007) Identification of a prepore large-complex stage in the mechanism of action of Clostridium perfringens enterotoxin. Infect Immun 75:2381–2390CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Michl P, Buchholz M, Rolke M, Kunsch S, Löhr M, McClane B, Tsukita S, Leder G, Adler G, Gress TM (2001) Claudin-4: a new target for pancreatic cancer treatment using Clostridium perfringens enterotoxin. Gastroenterology 121:678–684CrossRefPubMed Michl P, Buchholz M, Rolke M, Kunsch S, Löhr M, McClane B, Tsukita S, Leder G, Adler G, Gress TM (2001) Claudin-4: a new target for pancreatic cancer treatment using Clostridium perfringens enterotoxin. Gastroenterology 121:678–684CrossRefPubMed
11.
Zurück zum Zitat Kominsky SL, Vali M, Korz D, Gabig TG, Weitzman SA, Argani P, Sukumar S (2004) Clostridium perfringens enterotoxin elicits rapid and specific cytolysis of breast carcinoma cells mediated through tight junction proteins claudin 3 and 4. Am J Pathol 164:1627–1633CrossRefPubMedPubMedCentral Kominsky SL, Vali M, Korz D, Gabig TG, Weitzman SA, Argani P, Sukumar S (2004) Clostridium perfringens enterotoxin elicits rapid and specific cytolysis of breast carcinoma cells mediated through tight junction proteins claudin 3 and 4. Am J Pathol 164:1627–1633CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Santin AD, Cané S, Bellone S, Palmieri M, Siegel ER, Thomas M, Roman JJ, Burnett A, Cannon MJ, Pecorelli S (2005) Treatment of chemotherapy-resistant human ovarian cancer xenografts in C.B-17/SCID mice by intraperitoneal administration of Clostridium perfringens enterotoxin. Cancer Res 65:4334–4342CrossRefPubMed Santin AD, Cané S, Bellone S, Palmieri M, Siegel ER, Thomas M, Roman JJ, Burnett A, Cannon MJ, Pecorelli S (2005) Treatment of chemotherapy-resistant human ovarian cancer xenografts in C.B-17/SCID mice by intraperitoneal administration of Clostridium perfringens enterotoxin. Cancer Res 65:4334–4342CrossRefPubMed
13.
Zurück zum Zitat Santin AD, Bellone S, Siegel ER, McKenney JK, Thomas M, Roman JJ, Burnett A, Tognon G, Bandiera E, Pecorelli S (2007) Overexpression of Clostridium perfringens enterotoxin receptors claudin-3 and claudin-4 in uterine carcinosarcomas. Clin Cancer Res 13:3339–3346CrossRefPubMed Santin AD, Bellone S, Siegel ER, McKenney JK, Thomas M, Roman JJ, Burnett A, Tognon G, Bandiera E, Pecorelli S (2007) Overexpression of Clostridium perfringens enterotoxin receptors claudin-3 and claudin-4 in uterine carcinosarcomas. Clin Cancer Res 13:3339–3346CrossRefPubMed
14.
Zurück zum Zitat Maeda T, Murata M, Chiba H, Takasawa A, Tanaka S, Kojima T, Masumori N, Tsukamoto T, Sawada N (2012) Claudin-4-targeted therapy using Clostridium perfringens enterotoxin for prostate cancer. Prostate 72:351–360CrossRefPubMed Maeda T, Murata M, Chiba H, Takasawa A, Tanaka S, Kojima T, Masumori N, Tsukamoto T, Sawada N (2012) Claudin-4-targeted therapy using Clostridium perfringens enterotoxin for prostate cancer. Prostate 72:351–360CrossRefPubMed
15.
Zurück zum Zitat Morin PJ (2005) Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res 65:9603–9606CrossRefPubMed Morin PJ (2005) Claudin proteins in human cancer: promising new targets for diagnosis and therapy. Cancer Res 65:9603–9606CrossRefPubMed
16.
Zurück zum Zitat Kominsky SL (2006) Claudins: emerging targets for cancer therapy. Expert Rev Mol Med 8:1–11CrossRefPubMed Kominsky SL (2006) Claudins: emerging targets for cancer therapy. Expert Rev Mol Med 8:1–11CrossRefPubMed
17.
Zurück zum Zitat Goetsch L, Haeuw JF, Bear-Larvor C, Gonzalez A, Zanna L, Malissard M, Lepecquet AM, Robert A, Bailly C, Broussas M, Corvaia N (2012) A novel role for junctional adhesion moleculea-A in tumor proliferation: modulation by an anti-JAM-A monoclonal antibody. Int J Cancer 132:1463–1474CrossRefPubMed Goetsch L, Haeuw JF, Bear-Larvor C, Gonzalez A, Zanna L, Malissard M, Lepecquet AM, Robert A, Bailly C, Broussas M, Corvaia N (2012) A novel role for junctional adhesion moleculea-A in tumor proliferation: modulation by an anti-JAM-A monoclonal antibody. Int J Cancer 132:1463–1474CrossRefPubMed
18.
Zurück zum Zitat Murakami M, Giampietro C, Giannotta M, Corada M, Torselli I, Orsenigo F, Cocito A, d’Ario G, Mazzarol G, Confalonieri S, Di Fiore PP, Dejana E (2011) Abrogation of junctional adhesion molecule-A expression induces cell apoptosis and reduces breast cancer progression. PLoS One 6:e21242CrossRefPubMedPubMedCentral Murakami M, Giampietro C, Giannotta M, Corada M, Torselli I, Orsenigo F, Cocito A, d’Ario G, Mazzarol G, Confalonieri S, Di Fiore PP, Dejana E (2011) Abrogation of junctional adhesion molecule-A expression induces cell apoptosis and reduces breast cancer progression. PLoS One 6:e21242CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat El-Naggar AK (2017) Tumors of the salivary glands. In: El-Naggar AK, Chan JKC, Grandis JR, Takata T, Slootweg PJ (eds) World Health Organization Classification of Tumors. WHO classification of head and neck tumours, 4th edn. International Agency for Research on Cancer Press, Lyon, pp 160–202 El-Naggar AK (2017) Tumors of the salivary glands. In: El-Naggar AK, Chan JKC, Grandis JR, Takata T, Slootweg PJ (eds) World Health Organization Classification of Tumors. WHO classification of head and neck tumours, 4th edn. International Agency for Research on Cancer Press, Lyon, pp 160–202
23.
Zurück zum Zitat Kriegs JO, Homann V, Kinne-Saffran E, Kinne RK (2007) Identification and subcellular localization of paracellin-1 (claudin-16) in human salivary glands. Histochem Cell Biol 128:45–53CrossRefPubMed Kriegs JO, Homann V, Kinne-Saffran E, Kinne RK (2007) Identification and subcellular localization of paracellin-1 (claudin-16) in human salivary glands. Histochem Cell Biol 128:45–53CrossRefPubMed
24.
Zurück zum Zitat Lourenço SV, Coutinho-Camillo CM, Buim ME, Uyekita SH, Soares FA (2007) Human salivary gland branching morphogenesis: morphological localization of claudins and its parallel relation with developmental stages revealed by expression of cytoskeleton and secretion markers. Histochem Cell Biol 128:361–369CrossRefPubMed Lourenço SV, Coutinho-Camillo CM, Buim ME, Uyekita SH, Soares FA (2007) Human salivary gland branching morphogenesis: morphological localization of claudins and its parallel relation with developmental stages revealed by expression of cytoskeleton and secretion markers. Histochem Cell Biol 128:361–369CrossRefPubMed
25.
Zurück zum Zitat Maria OM, Kim JW, Gerstenhaber JA, Baum BJ, Tran SD (2008) Distribution of tight junction proteins in adult human salivary glands. J Histochem Cytochem 56:1093–1098CrossRefPubMedPubMedCentral Maria OM, Kim JW, Gerstenhaber JA, Baum BJ, Tran SD (2008) Distribution of tight junction proteins in adult human salivary glands. J Histochem Cytochem 56:1093–1098CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Ewert P, Aguilera S, Alliende C, Kwon YJ, Albornoz A, Molina C, Urzúa U, Quest AF, Olea N, Pérez P, Castro I, Barrera MJ, Romo R, Hermoso M, Leyton C, González MJ (2010) Disruption of tight junction structure in salivary glands from Sjögren’s syndrome patients is linked to proinflammatory cytokine exposure. Arthritis Rheum 62:1280–1289CrossRefPubMed Ewert P, Aguilera S, Alliende C, Kwon YJ, Albornoz A, Molina C, Urzúa U, Quest AF, Olea N, Pérez P, Castro I, Barrera MJ, Romo R, Hermoso M, Leyton C, González MJ (2010) Disruption of tight junction structure in salivary glands from Sjögren’s syndrome patients is linked to proinflammatory cytokine exposure. Arthritis Rheum 62:1280–1289CrossRefPubMed
27.
Zurück zum Zitat Mellas RE, Leigh NJ, Nelson JW, McCall AD, Baker OJ (2015) Zonula occludens-1, occludin and E-cadherin expression and organization in salivary glands with Sjögren’s Syndrome. J Histochem Cytochem 63:45–56CrossRefPubMedPubMedCentral Mellas RE, Leigh NJ, Nelson JW, McCall AD, Baker OJ (2015) Zonula occludens-1, occludin and E-cadherin expression and organization in salivary glands with Sjögren’s Syndrome. J Histochem Cytochem 63:45–56CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Abe A, Takano K, Kojima T, Nomura K, Kakuki T, Kaneko Y, Yamamoto M, Takahashi H, Himi T (2016) Interferon-gamma increased epithelial barrier function via upregulating claudin-7 expression in human submandibular gland duct epithelium. J Mol Histol 47:353–363CrossRefPubMed Abe A, Takano K, Kojima T, Nomura K, Kakuki T, Kaneko Y, Yamamoto M, Takahashi H, Himi T (2016) Interferon-gamma increased epithelial barrier function via upregulating claudin-7 expression in human submandibular gland duct epithelium. J Mol Histol 47:353–363CrossRefPubMed
29.
Zurück zum Zitat Aro K, Rosa LE, Bello IO, Soini Y, Mäkitie AA, Salo T, Leivo I (2011) Expression pattern of claudins 1 and 3—an auxiliary tool in predicting behavior of mucoepidermoid carcinoma of salivary gland origin. Virchows Arch 458:341–348CrossRefPubMed Aro K, Rosa LE, Bello IO, Soini Y, Mäkitie AA, Salo T, Leivo I (2011) Expression pattern of claudins 1 and 3—an auxiliary tool in predicting behavior of mucoepidermoid carcinoma of salivary gland origin. Virchows Arch 458:341–348CrossRefPubMed
30.
Zurück zum Zitat Abd El-Ghani SF, Kasem RF, Ghallab NA, Shaker OG (2013) Detection of claudin-4 in salivary gland neoplasms (a study utilizing RT-PCR and immunohistochemistry). J Oral Pathol Med 42:781–787CrossRefPubMed Abd El-Ghani SF, Kasem RF, Ghallab NA, Shaker OG (2013) Detection of claudin-4 in salivary gland neoplasms (a study utilizing RT-PCR and immunohistochemistry). J Oral Pathol Med 42:781–787CrossRefPubMed
31.
Zurück zum Zitat Remmele W, Hildebrand U, Hienz HA, Klein PJ, Vierbuchen M, Behnken LJ, Heicke B, Scheidt E (1986) Comparative histological, histochemical, immunohistochemical and biochemical studies on oestrogen receptors, lectin receptors, and Barr bodies in human breast cancer. Virchows Arch A Pathol Anat Histopahtol 409:127–147CrossRef Remmele W, Hildebrand U, Hienz HA, Klein PJ, Vierbuchen M, Behnken LJ, Heicke B, Scheidt E (1986) Comparative histological, histochemical, immunohistochemical and biochemical studies on oestrogen receptors, lectin receptors, and Barr bodies in human breast cancer. Virchows Arch A Pathol Anat Histopahtol 409:127–147CrossRef
32.
Zurück zum Zitat Keira Y, Takasawa A, Murata M, Nojima M, Takasawa K, Ogino J, Higashiura Y, Sasaki A, Kimura Y, Mizuguchi T, Tanaka S, Hirata K, Sawada N, Hasegawa T (2015) An immunohistochemical marker panel including claudin-18, maspin, and p53 improves diagnostic accuracy of bile duct neoplasms in surgical and presurgical biopsy specimens. Virchows Arch 466:265–277CrossRefPubMed Keira Y, Takasawa A, Murata M, Nojima M, Takasawa K, Ogino J, Higashiura Y, Sasaki A, Kimura Y, Mizuguchi T, Tanaka S, Hirata K, Sawada N, Hasegawa T (2015) An immunohistochemical marker panel including claudin-18, maspin, and p53 improves diagnostic accuracy of bile duct neoplasms in surgical and presurgical biopsy specimens. Virchows Arch 466:265–277CrossRefPubMed
34.
Zurück zum Zitat Huang J, Zhang L, He C, Qu Y, Li J, Zhang J, Du T, Chen X, Yu Y, Liu B, Zhu Z (2015) Claudin-1 enhances tumor proliferation and metastasis by regulating cell anoikis in gastric cancer. Oncotarget 6:1652–1665PubMed Huang J, Zhang L, He C, Qu Y, Li J, Zhang J, Du T, Chen X, Yu Y, Liu B, Zhu Z (2015) Claudin-1 enhances tumor proliferation and metastasis by regulating cell anoikis in gastric cancer. Oncotarget 6:1652–1665PubMed
35.
Zurück zum Zitat Chang TL, Ito K, Ko TK, Liu Q, Salto-Tellez M, Yeoh KG, Fukamachi H, Ito Y (2010) Claudin-1 has tumor suppressive activity and is a direct target of RUNX3 in gastric epithelial cells. Gastroenterology 138:255–265CrossRefPubMed Chang TL, Ito K, Ko TK, Liu Q, Salto-Tellez M, Yeoh KG, Fukamachi H, Ito Y (2010) Claudin-1 has tumor suppressive activity and is a direct target of RUNX3 in gastric epithelial cells. Gastroenterology 138:255–265CrossRefPubMed
36.
Zurück zum Zitat Pope JL, Ahmad R, Bhat AA, Washington MK, Singh AB, Dhawan P (2014) Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenomatous polyposis coli-mediated colon tumorigenesis. Mol Cancer 13:167CrossRefPubMedPubMedCentral Pope JL, Ahmad R, Bhat AA, Washington MK, Singh AB, Dhawan P (2014) Claudin-1 overexpression in intestinal epithelial cells enhances susceptibility to adenomatous polyposis coli-mediated colon tumorigenesis. Mol Cancer 13:167CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Bezdekova M, Brychtova S, Sedlakova E, Langova K, Brychta T, Belej K (2012) Analysis of Snail-1, E-cadherin and claudin-1 expression in colorectal adenomas and carcinomas. Int J Mol Sci 13:1632–1643CrossRefPubMedPubMedCentral Bezdekova M, Brychtova S, Sedlakova E, Langova K, Brychta T, Belej K (2012) Analysis of Snail-1, E-cadherin and claudin-1 expression in colorectal adenomas and carcinomas. Int J Mol Sci 13:1632–1643CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Huo Q, Kinugasa T, Wang L, Huang J, Zhao J, Shibaguchi H, Kuroki M, Tanaka T, Yamashita Y, Nabeshima K, Iwasaki H, Kuroki M (2009) Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res 29:851–857PubMed Huo Q, Kinugasa T, Wang L, Huang J, Zhao J, Shibaguchi H, Kuroki M, Tanaka T, Yamashita Y, Nabeshima K, Iwasaki H, Kuroki M (2009) Claudin-1 protein is a major factor involved in the tumorigenesis of colorectal cancer. Anticancer Res 29:851–857PubMed
39.
Zurück zum Zitat Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR (2008) Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 88:1110–1120CrossRefPubMedPubMedCentral Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR (2008) Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 88:1110–1120CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat Tőkés A-M, Kulka J, Paku S, Szik Á, 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–R305CrossRefPubMedPubMedCentral Tőkés A-M, Kulka J, Paku S, Szik Á, 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–R305CrossRefPubMedPubMedCentral
41.
Zurück zum Zitat Myal Y, Leygue E, Blanchard AA (2010) Claudin 1 in breast tumorigenesis: revelation of a possible novel “claudin high” subset of breast cancers. J Biomed Biotechnol 2010:956897CrossRefPubMedPubMedCentral Myal Y, Leygue E, Blanchard AA (2010) Claudin 1 in breast tumorigenesis: revelation of a possible novel “claudin high” subset of breast cancers. J Biomed Biotechnol 2010:956897CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat Tokés 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–R305CrossRefPubMedPubMedCentral Tokés 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–R305CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ (2009) Claudin-1 acts through c-ABl-PKCdelta signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 285:226–233CrossRefPubMedPubMedCentral Yoon CH, Kim MJ, Park MJ, Park IC, Hwang SG, An S, Choi YH, Yoon G, Lee SJ (2009) Claudin-1 acts through c-ABl-PKCdelta signaling and has a causal role in the acquisition of invasive capacity in human liver cells. J Biol Chem 285:226–233CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Suh Y, Yoon CH, Kim RK, Lim EJ, Oh YS, Hwang SG, An S, Yoon G, Gye MC, Yi JM, Kim MJ, Lee SJ (2012) Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells. Oncogene 32:4873–4882CrossRefPubMed Suh Y, Yoon CH, Kim RK, Lim EJ, Oh YS, Hwang SG, An S, Yoon G, Gye MC, Yi JM, Kim MJ, Lee SJ (2012) Claudin-1 induces epithelial-mesenchymal transition through activation of the c-Abl-ERK signaling pathway in human liver cells. Oncogene 32:4873–4882CrossRefPubMed
45.
Zurück zum Zitat Chao YC, Pan SH, Yang SC, Yu SL, Che TF, Lin CW, Tsai MS, Chang GC, Wu CH, Wu YY, Lee YC, Hong TM, Yang PC (2009) Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma. Am J Respir Crit Care Med 179:123–133CrossRefPubMed Chao YC, Pan SH, Yang SC, Yu SL, Che TF, Lin CW, Tsai MS, Chang GC, Wu CH, Wu YY, Lee YC, Hong TM, Yang PC (2009) Claudin-1 is a metastasis suppressor and correlates with clinical outcome in lung adenocarcinoma. Am J Respir Crit Care Med 179:123–133CrossRefPubMed
46.
Zurück zum Zitat Tzelepi VN, Tsamandas AC, Vlotinou HD, Vagianos CE, Scopa CD (2008) Tight junctions in thyroid carcinogenesis: diverse expression of claudin-1, claudin-4, claudin-7 and occludin in thyroid neoplasms. Mod Pathol 21:22–30CrossRefPubMed Tzelepi VN, Tsamandas AC, Vlotinou HD, Vagianos CE, Scopa CD (2008) Tight junctions in thyroid carcinogenesis: diverse expression of claudin-1, claudin-4, claudin-7 and occludin in thyroid neoplasms. Mod Pathol 21:22–30CrossRefPubMed
47.
Zurück zum Zitat Zwanziger D, Badziong J, Ting S, Moeller LC, Schmid KW, Siebolts U, Wickenhauser C, Dralle H, Fuehrer D (2015) The impact of CLAUDIN-1 on follicular thyroid carcinoma aggressiveness. Endocr Relat Cancer 22:819–830CrossRefPubMed Zwanziger D, Badziong J, Ting S, Moeller LC, Schmid KW, Siebolts U, Wickenhauser C, Dralle H, Fuehrer D (2015) The impact of CLAUDIN-1 on follicular thyroid carcinoma aggressiveness. Endocr Relat Cancer 22:819–830CrossRefPubMed
48.
Zurück zum Zitat Goetsch L, Haeuw JF, Beau-Larvor C, Gonzalez A, Zanna L, Malissard M, Lepecquet AM, Robert A, Bailly C, Broussas M, Corvaia N (2013) A novel role for junctional adhesion molecule-A in tumor proliferation: modulation by an anti-JAM-A monoclonal antibody. Int J Cancer 132:1463–1474CrossRefPubMed Goetsch L, Haeuw JF, Beau-Larvor C, Gonzalez A, Zanna L, Malissard M, Lepecquet AM, Robert A, Bailly C, Broussas M, Corvaia N (2013) A novel role for junctional adhesion molecule-A in tumor proliferation: modulation by an anti-JAM-A monoclonal antibody. Int J Cancer 132:1463–1474CrossRefPubMed
49.
Zurück zum Zitat Takasawa A, Murata M, Takasawa K, Ono Y, Osanai M, Tanaka S, Nojima M, Kono T, Hirata K, Kojima T, Sawada N (2016) Nuclear localization of tricellulin promotes the oncogenic property of pancreatic cancer. Sci Rep 6:33582CrossRefPubMedPubMedCentral Takasawa A, Murata M, Takasawa K, Ono Y, Osanai M, Tanaka S, Nojima M, Kono T, Hirata K, Kojima T, Sawada N (2016) Nuclear localization of tricellulin promotes the oncogenic property of pancreatic cancer. Sci Rep 6:33582CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Akimoto T, Takasawa A, Murata M, Kojima Y, Takasawa K, Nojima M, Aoyama T, Hiratsuka Y, Ono Y, Tanaka S, Osanai M, Hasegawa T, Saito T, Sawada N (2016) Analysis of the expression and localization of tight junction transmembrane proteins, claudin-1, -4, -7, occludin and JAM-A, in human cervical adenocarcinoma. Histol Histopathol 31:921–931PubMed Akimoto T, Takasawa A, Murata M, Kojima Y, Takasawa K, Nojima M, Aoyama T, Hiratsuka Y, Ono Y, Tanaka S, Osanai M, Hasegawa T, Saito T, Sawada N (2016) Analysis of the expression and localization of tight junction transmembrane proteins, claudin-1, -4, -7, occludin and JAM-A, in human cervical adenocarcinoma. Histol Histopathol 31:921–931PubMed
Metadaten
Titel
Immunoreactivity patterns of tight junction proteins are useful for differential diagnosis of human salivary gland tumors
verfasst von
Tomoyuki Aoyama
Akira Takasawa
Masaki Murata
Makoto Osanai
Kenichi Takano
Tadashi Hasagawa
Norimasa Sawada
Publikationsdatum
28.06.2018
Verlag
Springer Japan
Erschienen in
Medical Molecular Morphology / Ausgabe 1/2019
Print ISSN: 1860-1480
Elektronische ISSN: 1860-1499
DOI
https://doi.org/10.1007/s00795-018-0199-6

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