Emerging roles of transmembrane-type tight junction proteins in cancers.
aberrant expression
cancer
claudin
diagnostic marker
junctional adhesion molecule
malignant potential
therapeutic target
tight junction
transmembrane protein
Journal
Pathology international
ISSN: 1440-1827
Titre abrégé: Pathol Int
Pays: Australia
ID NLM: 9431380
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
19
04
2023
accepted:
06
06
2023
medline:
14
8
2023
pubmed:
14
7
2023
entrez:
14
7
2023
Statut:
ppublish
Résumé
Tight junctions (TJs) are the most apical components of the cell-cell adhesion machinery in epithelial and endothelial cells and they play essential roles in homeostasis. Recent studies have revealed that aberrant expression of tight junction proteins (TJPs) is frequently observed in various type of cancers. Here we review cancer-associated aberrant expression of TJPs with focus on transmembrane-type TJPs including claudins, junctional adhesion molecule-A (JAM-A), and occludin. Some transmembrane-type TJPs are upregulated at the early neoplastic stage and their expression persists during dedifferentiation. Aberrant expression of TJPs contributes to proliferation, invasion, and dysregulated signaling of cancer cells. In addition to an increase in their expression level, their localization is altered from a TJ-restricted pattern to distribution throughout the whole cell membrane, making them suitable as therapeutic targets. Extracellular domains of transmembrane-type TJPs can be approached by target drugs not only from the lumen side (apical side) but also from the extracellular matrix side (basal side), including blood vessels. Aberrantly expressed TJPs are potential useful diagnostic markers as well as therapeutic targets for cancers.
Substances chimiques
Tight Junction Proteins
0
Claudins
0
Occludin
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
331-340Subventions
Organisme : Japan Society for the Promotion of Science
ID : 24790355
Organisme : Japan Society for the Promotion of Science
ID : 26460421
Organisme : Japan Society for the Promotion of Science
ID : JP17K08698
Organisme : Japan Society for the Promotion of Science
ID : JP20K07409
Organisme : Ono Cancer Research Fund
Organisme : Suhara Foundation
Organisme : Kurozumi Medical Foundation
Informations de copyright
© 2023 Japanese Society of Pathology and John Wiley & Sons Australia, Ltd.
Références
Sawada N. Tight junction-related human diseases. Pathol Int. 2013;63:1-12.
Otani T, Furuse M. Tight junction structure and function revisited. Trends Cell Biol. 2020;30:805-17.
Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE. Structure and function of claudins. Biochim Biophys Acta Biomembr. 2008;1778(3):631-45.
Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol. 2006;68:403-29.
Birukova AA, Birukov KG, Adyshev D, Usatyuk P, Natarajan V, Garcia JGN, et al. Involvement of microtubules and Rho pathway in TGF-β1-induced lung vascular barrier dysfunction. J Cell Physiol. 2005;204:934-47.
Oshima T, Miwa H. Gastrointestinal mucosal barrier function and diseases. J Gastroenterol. 2016;51(8):768-78.
Assimakopoulos SF, Scopa CD, Vagianos CE. Pathophysiology of increased intestinal permeability in obstructive jaundice. World J Gastroenterol. 2007;13(48):6458-64.
Daneman R, Prat A. The blood-brain barrier. Cold Spring Harbor Perspect Biol. 2015;7(1):a020412.
Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37(1):13-25.
Tsukita S, Furuse M. Claudin-based barrier in simple and stratified cellular sheets. Curr Opin Cell Biol. 2002;14:531-6.
Tsukita S, Yamazaki Y, Katsuno T, Tamura A, Tsukita S. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene. 2008;27:6930-8.
Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol. 1998;141(7):1539-50.
Schilpp C, Lochbaum R, Braubach P, Jonigk D, Frick M, Dietl P, et al. TGF-β1 increases permeability of ciliated airway epithelia via redistribution of claudin 3 from tight junction into cell nuclei. Pflügers Arch Eur J Physiol. 2021;473(2):287-311.
Higashi T, Tokuda S, Kitajiri S, Masuda S, Nakamura H, Oda Y, et al. Analysis of the ‘angulin’ proteins LSR, ILDR1 and ILDR2-tricellulin recruitment, epithelial barrier function and implication in deafness pathogenesis. J Cell Sci. 2013;126(Pt 4):3797-97.
Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol. 2001;2:285-93.
Tobioka H, Isomura H, Kokai Y, Tokunaga Y, Yamaguchi J, Sawada N. Occludin expression decreases with the progression of human endometrial carcinoma. Hum Pathol. 2004;35(2):159-64.
Agarwal R, D'Souza T, Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res. 2005;65(16):7378-85.
Michl P, Barth C, Buchholz M, Lerch MM, Rolke M, Holzmann KH, et al. Claudin-4 expression decreases invasiveness and metastatic potential of pancreatic cancer. Cancer Res. 2003;63(19):6265-71.
Osanai M, Takasawa A, Murata M, Sawada N. Claudins in cancer: bench to bedside. Pflügers Arch Eur J Physiol. 2017;469(1):55-67.
Ono Y, Hiratsuka Y, Murata M, Takasawa A, Fukuda R, Nojima M, et al. Claudins-4 and -7 might be valuable markers to distinguish hepatocellular carcinoma from cholangiocarcinoma. Virchows Arch. 2016;469(4):417-26.
Rohde C, Yamaguchi R, Mukhina S, Sahin U, Itoh K, Türeci Ö. Comparison of Claudin 18.2 expression in primary tumors and lymph node metastases in Japanese patients with gastric adenocarcinoma. Jpn J Clin Oncol. 2019;49(9):870-6.
Bhat AA, Syed N, Therachiyil L, Nisar S, Hashem S, Macha MA, et al. Claudin-1, a double-edged sword in cancer. Int J Mol Sci. 2020;21(2):569.
Lauko A, Mu Z, Gutmann DH, Naik UP, Lathia JD. Junctional adhesion molecules in cancer: a paradigm for the diverse functions of cell-cell interactions in tumor progression. Cancer Res. 2020;80(22):4878-85.
Sugimoto H, Nagahara M, Bae Y, Nakagawa T, Ishikawa T, Sato T, et al. Clinicopathologic relevance of claudin 5 expression in breast cancer. Am J Clin Path. 2015;143(4):540-6.
Aoyama T, Takasawa A, Murata M, Osanai M, Takano K, Hasagawa T, et al. Immunoreactivity patterns of tight junction proteins are useful for differential diagnosis of human salivary gland tumors. Med Mol Morphol. 2019;52(1):23-35.
Dottermusch M, Krüger S, Behrens HM, Halske C, Röcken C. Expression of the potential therapeutic target claudin-18.2 is frequently decreased in gastric cancer: results from a large Caucasian cohort study. Virchows Arch. 2019;475(5):563-71.
Miwa N, Furuse M, Tsukita S, Niikawa N, Nakamura Y, Furukawa Y. Involvement of claudin-1 in the β-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol Res. 2001;12(11-12):469-76.
Oshima T, Shan J, Okugawa T, Chen X, Hori K, Tomita T, et al. Down-regulation of claudin-18 is associated with the proliferative and invasive potential of gastric cancer at the invasive front. PLoS One. 2013;8(9):e74757.
Martin TA. Loss of occludin leads to the progression of human breast cancer. Int J Mol Med. 2010;26(5):723-34.
de Oliveira SS, de Oliveira IM, De Souza W, Morgado-Díaz JA. Claudins upregulation in human colorectal cancer. FEBS Lett. 2005;579(27):6179-85.
Dhawan P. Claudin-1 regulates cellular transformation and metastatic behavior in colon cancer. J Clin Invest. 2005;115(7):1765-76.
Kinugasa T, Huo Q, Higashi D, Shibaguchi H, Kuroki M, Tanaka T, et al. Selective up-regulation of claudin-1 and claudin-2 in colorectal cancer. Anticancer Res. 2007;27(6A):3729-34.
Yadav R, Kumar Y, Dahiya D, Bhatia A. Claudins: the newly emerging targets in breast cancer. Clin Breast Cancer. 2022;22(8):737-52.
Huang J, Li J, Qu Y, Zhang J, Zhang L, Chen X, et al. The expression of claudin 1 correlates with β-catenin and is a prognostic factor of poor outcome in gastric cancer. Int J Oncol. 2014;44(4):1293-301.
Shinozaki A, Shibahara J, Noda N, Tanaka M, Aoki T, Kokudo N, et al. Claudin-18 in biliary neoplasms. Its significance in the classification of intrahepatic cholangiocarcinoma. Virchows Arch. 2011;459(1):73-80.
Ogawa M, Kojima T, Someya M, Nomura K, Takasawa A, Murata M, et al. Epidermal growth factor modulates claudins and tight junctional functions in ovarian cancer cell lines. Histochem Cell Biol. 2012;138(2):323-38.
Soini Y, Eskelinen M, Juvonen P, Kärjä V, Haapasaari KM, Saarela A, et al. Strong claudin 5 expression is a poor prognostic sign in pancreatic adenocarcinoma. Tumor Biol. 2014;35(4):3803-8.
Moentenich V, Gebauer F, Comut E, Tuchscherer A, Bruns C, Schroeder W, et al. Claudin 18.2 expression in esophageal adenocarcinoma and its potential impact on future treatment strategies. Oncol Lett. 2020;19(6):3665-70.
Bornholdt J, Friis S, Godiksen S, Poulsen SS, Santoni-Rugiu E, Bisgaard HC, et al. The level of claudin-7 is reduced as an early event in colorectal carcinogenesis. BMC Cancer. 2011;11:65.
Konecny GE, Agarwal R, Keeney GA, Winterhoff B, Jones MB, Mariani A, et al. Claudin-3 and claudin-4 expression in serous papillary, clear-cell, and endometrioid endometrial cancer. Gynecol Oncol. 2008;109(2):263-9.
Lee JW, Lee SJ, Seo J, Song SY, Ahn G, Park CS, et al. Increased expressions of claudin-1 and claudin-7 during the progression of cervical neoplasia. Gynecol Oncol. 2005;97(1):53-9.
Tsujiwaki M, Murata M, Takasawa A, Hiratsuka Y, Fukuda R, Sugimoto K, et al. Aberrant expression of claudin-4 and -7 in hepatocytes in the cirrhotic human liver. Med Mol Morphol. 2015;48(1):33-43.
Akimoto T, Takasawa A, Murata M, Kojima Y, Takasawa K, Nojima M, et al. 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. 2016;31(8):921-31.
Soini Y, Takasawa A, Eskelinen M, Juvonen P, Kärjä V, Hasegawa T, et al. Expression of claudins 7 and 18 in pancreatic ductal adenocarcinoma: association with features of differentiation. J Clin Pathol. 2012;65(5):431-6.
Yamada G, Murata M, Takasawa A, Nojima M, Mori Y, Sawada N, et al. Increased expressions of claudin 4 and 7 in atypical adenomatous hyperplasia and adenocarcinoma of the lung. Med Mol Morphol. 2016;49(3):163-9.
Keira Y, Takasawa A, Murata M, Nojima M, Takasawa K, Ogino J, et al. 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. 2015;466(3):265-77.
Ito Y, Takasawa A, Takasawa K, Murakami T, Akimoto T, Kyuno D, et al. Aberrant expression of claudin-6 contributes to malignant potentials and drug resistance of cervical adenocarcinoma. Cancer Sci. 2022;113(4):1519-30.
Kojima M, Sugimoto K, Tanaka M, Endo Y, Kato H, Honda T, et al. Prognostic significance of aberrant claudin-6 expression in endometrial cancer. Cancers. 2020;12(10):2748.
Soini Y, Pirinen R, Takasawa K, Osanai M, Takasawa A. Claudin 6 is associated with a short survival and a short recurrent free interval in non-small cell lung carcinoma. Pol J Pathol. 2022;73(1):1-5.
Matsuda M, Sentani K, Noguchi T, Hinoi T, Okajima M, Matsusaki K, et al. Immunohistochemical analysis of colorectal cancer with gastric phenotype: claudin-18 is associated with poor prognosis. Pathol Int. 2010;60(10):673-80.
Yu S, Zhang Y, Li Q, Zhang Z, Zhao G, Xu J. CLDN6 promotes tumor progression through the YAP1-snail1 axis in gastric cancer. Cell Death Dis. 2019;10(12):949.
Lu Y, Dang Q, Bo Y, Su X, Wang L, Sun J, et al. The expression of CLDN6 in hepatocellular carcinoma tissue and the effects of CLDN6 on biological phenotypes of hepatocellular carcinoma cells. J Cancer. 2021;12(18):5454-63.
Wang L, Jin X, Lin D, Liu Z, Zhang X, Lu Y, et al. Clinicopathologic significance of claudin-6, occludin, and matrix metalloproteinases-2 expression in ovarian carcinoma. Diagn Pathol. 2013;8:190.
Murakami T, Takasawa A, Takasawa K, Akimoto T, Aoyama T, Magara K, et al. Aberrant expression of junctional adhesion molecule-A contributes to the malignancy of cervical adenocarcinoma by interaction with poliovirus receptor/CD155. Cancer Sci. 2021;112(2):906-17.
Akimoto T, Takasawa A, Takasawa K, Aoyama T, Murata M, Osanai M, et al. Estrogen/GPR30 signaling contributes to the malignant potentials of ER-negative cervical adenocarcinoma via regulation of claudin-1 expression. Neoplasia. 2018;20(10):1083-93.
Takasawa K, Takasawa A, Osanai M, Aoyama T, Ono Y, Kono T, et al. Claudin-18 coupled with EGFR/ERK signaling contributes to the malignant potentials of bile duct cancer. Cancer Lett. 2017;403:66-73.
Magara K, Takasawa A, Osanai M, Ota M, Tagami Y, Ono Y, et al. Elevated expression of JAM-A promotes neoplastic properties of lung adenocarcinoma. Cancer Sci. 2017;108(11):2306-14.
Facchetti F, Lonardi S, Gentili F, Bercich L, Falchetti M, Tardanico R, et al. Claudin 4 identifies a wide spectrum of epithelial neoplasms and represents a very useful marker for carcinoma versus mesothelioma diagnosis in pleural and peritoneal biopsies and effusions. Virchows Arch. 2007;451(3):669-80.
Rahman A, Kobayashi M, Sugimoto K, Endo Y, Kojima M, Furukawa S, et al. Reduced claudin-12 expression predicts poor prognosis in cervical cancer. Int J Mol Sci. 2021;22(7):3774.
Virman J, Soini Y, Kujala P, Luukkaala T, Salminen T, Sunela K, et al. Claudins as prognostic factors for renal cell cancer. Anticancer Res. 2014;34(8):4181-7.
Watanabe M, Higashi T, Ozeki K, Higashi AY, Sugimoto K, Mine H, et al. CLDN15 is a novel diagnostic marker for malignant pleural mesothelioma. Sci Rep. 2021;11(1):12554.
Ito T, Kojima T, Yamaguchi H, Kyuno D, Kimura Y, Imamura M, et al. Transcriptional regulation of claudin-18 via specific protein kinase C signaling pathways and modification of DNA methylation in human pancreatic cancer cells. JCB. 2011;112(7):1761-72.
Takasawa A, Murata M, Takasawa K, Ono Y, Osanai M, Tanaka S, et al. Nuclear localization of tricellulin promotes the oncogenic property of pancreatic cancer. Sci Rep. 2016;6:33582.
Saito Y, Takasawa A, Takasawa K, Aoyama T, Akimoto T, Ota M, et al. Aldolase A promotes epithelial-mesenchymal transition to increase malignant potentials of cervical adenocarcinoma. Cancer Sci. 2020;111(8):3071-81.
Liu F, Koval M, Ranganathan S, Fanayan S, Hancock WS, Lundberg EK, et al. Systems proteomics view of the endogenous human claudin protein family. J Proteome Res. 2016;15(2):339-59.
Takasawa K, Takasawa A, Akimoto T, Magara K, Aoyama T, Kitajima H, et al. Regulatory roles of claudin-1 in cell adhesion and microvilli formation. Biochem Biophys Res Commun. 2021;565:36-42.
Fujiwara-Tani R, Sasaki T, Luo Y, Goto K, Kawahara I, Nishiguchi Y, et al. Anti-claudin-4 extracellular domain antibody enhances the antitumoral effects of chemotherapeutic and antibody drugs in colorectal cancer. Oncotarget. 2018;9:37367-78.
Gowrikumar S, Singh AB, Dhawan P. Role of claudin proteins in regulating cancer stem cells and chemoresistance-potential implication in disease prognosis and therapy. Int J Mol Sci. 2019;21(1):53.
Baumgartner HK, Beeman N, Hodges RS, Neville MC. A D-peptide analog of the second extracellular loop of claudin-3 and -4 leads to mislocalized claudin and cellular apoptosis in mammary epithelial cells. Chem Biol Drug Des. 2011;77(2):124-36.
Nishiguchi Y, Fujiwara-Tani R, Sasaki T, Luo Y, Ohmori H, Kishi S, et al. Targeting claudin-4 enhances CDDP-chemosensitivity in gastric cancer. Oncotarget. 2019;10:2189-202.
Maeda T, Murata M, Chiba H, Takasawa A, Tanaka S, Kojima T, et al. Claudin-4-targeted therapy using Clostridium perfringens enterotoxin for prostate cancer. Prostate. 2012;72(4):351-60.
Kuwada M, Chihara Y, Luo Y, Li X, Nishiguchi Y, Fujiwara R, et al. Pro-chemotherapeutic effects of antibody against extracellular domain of claudin-4 in bladder cancer. Cancer Lett. 2015;369(1):212-21.
Nasako H, Takashina Y, Eguchi H, Ito A, Ishikawa Y, Matsunaga T, et al. Increase in toxicity of anticancer drugs by PMTPV, a claudin-1-binding peptide, mediated via down-regulation of claudin-1 in human lung adenocarcinoma A549 cells. Int J Mol Sci. 2020;21(16):5909.
Nasako H, Akizuki R, Takashina Y, Ishikawa Y, Shinoda T, Shirouzu M, et al. Claudin-2 binding peptides, VPDSM and DSMKF, down-regulate claudin-2 expression and anticancer resistance in human lung adenocarcinoma A549 cells. Biochim Biophys Acta Mol Cell Res. 2020;1867(4):118642.
Maruhashi R, Akizuki R, Sato T, Matsunaga T, Endo S, Yamaguchi M, et al. Elevation of sensitivity to anticancer agents of human lung adenocarcinoma A549 cells by knockdown of claudin-2 expression in monolayer and spheroid culture models. Biochim Biophys Acta Mol Cell Res. 2018;1865(3):470-9.
Luo Y, Kishi S, Sasaki T, Ohmori H, Fujiwara-Tani R, Mori S, et al. Targeting claudin-4 enhances chemosensitivity in breast cancer. Cancer Sci. 2020;111(5):1840-50.
Ikari A, Taga S, Watanabe R, Sato T, Shimobaba S, Sonoki H, et al. Clathrin-dependent endocytosis of claudin-2 by DFYSP peptide causes lysosomal damage in lung adenocarcinoma A549 cells. Biochim Biophys Acta Biomembr. 2015;1848(10 Pt A):2326-36.
Singh P, Toom S, Huang Y. Anti-claudin 18.2 antibody as new targeted therapy for advanced gastric cancer. J Hematol Oncol. 2017;10(1):105.
Türeci O, Sahin U, Schulze-Bergkamen H, Zvirbule Z, Lordick F, Koeberle D, et al. A multicentre, phase IIa study of zolbetuximab as a single agent in patients with recurrent or refractory advanced adenocarcinoma of the stomach or lower oesophagus: the MONO study. Ann Oncol. 2019;30(9):1487-95.
Türeci Ӧ, Mitnacht-Kraus R, Wöll S, Yamada T, Sahin U. Characterization of zolbetuximab in pancreatic cancer models. Oncoimmunology. 2018;8(1):e1523096.
Wöll S, Schlitter AM, Dhaene K, Roller M, Esposito I, Sahin U, et al. Claudin 18.2 is a target for IMAB362 antibody in pancreatic neoplasms. Int J Cancer. 2014;134(3):731-9.
Lordick F, Al-Batran SE, Ganguli A, Morlock R, Sahin U, Türeci Ö. Patient-reported outcomes from the phase II FAST trial of zolbetuximab plus EOX compared to EOX alone as first-line treatment of patients with metastatic CLDN18.2+ gastroesophageal adenocarcinoma. Gastric Cancer. 2021;24(3):721-30.
Hashizume A, Ueno T, Furuse M, Tsukita S, Nakanishi Y, Hieda Y. Expression patterns of claudin family of tight junction membrane proteins in developing mouse submandibular gland. Dev Dyn. 2004;231(2):425-31.
Stadler CR, Bähr-Mahmud H, Plum LM, Schmoldt K, Kölsch AC, Türeci, Ö, et al. Characterization of the first-in-class T-cell-engaging bispecific single-chain antibody for targeted immunotherapy of solid tumors expressing the oncofetal protein claudin 6. Oncoimmunology. 2015;5(3):e1091555.
Reinhard K, Rengstl B, Oehm P, Michel K, Billmeier A, Hayduk N, et al. An RNA vaccine drives expansion and efficacy of claudin-CAR-T cells against solid tumors. Science. 2020;367(6476):446-53.