Generic placeholder image

Current Drug Metabolism

Editor-in-Chief

ISSN (Print): 1389-2002
ISSN (Online): 1875-5453

Review Article

The Role of E-cadherin in Helicobacter pylori-Related Gastric Diseases

Author(s): Yunzhan Zhang, Danyan Li, Yunkai Dai, Ruliu Li, Yong Gao* and Ling Hu*

Volume 20, Issue 1, 2019

Page: [23 - 28] Pages: 6

DOI: 10.2174/1389200219666180625113010

Price: $65

Abstract

Background: Helicobacter pylori (H. pylori)-related gastric diseases are a series of gastric mucosal disorders associated with H. pylori infection. Gastric cancer (GC) is widely believed to evolve from gastritis and gastric ulcer. As an important adhesion molecule of epithelial cells, E-cadherin plays a key role in the development of gastric diseases. In this review, we aim to seek the characteristic of E-cadherin expression at different stages of gastric diseases.

Methods: We searched plenty of databases for research literature about E-cadherin expression in H. pylori-related gastric diseases, and reviewed the relationship of E-cadherin and H. pylori, and the role of E-cadherin at different stages of gastric diseases.

Results: H. pylori was shown to decrease E-cadherin expression by various ways in vitro, while most of clinical studies have not found the relationship between H. pylori and E-cadherin expression. It is defined that poor outcome of GC is related to loss expression of E-cadherin, but it is still unclear when qualitative change of E-cadherin expression in gastric mucosa emerges.

Conclusion: Expression level of E-cadherin in gastric cells may be a consequence of injury factors and body’s selfrepairing ability. More studies on E-cadherin expression in gastric mucosa with precancerous lesions need to be performed, which may be potential and useful for early detection, prevention and treatment of GC.

Keywords: E-cadherin, Helicobacter pylori, gastritis, gastric ulcer, gastric cancer, pathology.

Graphical Abstract

[1]
An international association between Helicobacter pylori infection and gastric cancer. Lancet, 1993, 341(8857), 1359-1362.
[2]
Correa, P. Human Gastric Carcinoggenesis: A multistep and multifactorial process-first american cancer society award lecture on cancer epidemiology and prevention. Cancer Res., 1992, 52(24), 6735-6740.
[3]
Lau, M.T.; Klausen, C.; Leung, P.C.K. E-cadherin inhibits tumor cell growth by suppressing PI3K/Akt signaling via β-catenin-Egr1-mediated PTEN expression. Oncogene, 2011, 30(24), 2753-2766.
[4]
Chen, Z.; Liu, M.; Liu, X.; Huang, S.; Li, L.; Song, B.; Li, H.; Ren, Q.; Hu, Z.; Zhou, Y.; Qiao, L. COX-2 regulates E-cadherin expression through the NF-κB/Snail signaling pathway in gastric cancer. Int. J. Mol. Med., 2013, 32(1), 93-100.
[5]
Du, J.; Wang, S.; Jing, F.; Zhan, J.; Wang, Y. MicroRNA-203 suppresses invasion of gastric cancer cells by targeting ERK1/2/Slug/E-cadherin signaling. Cancer Biomark., 2017, 19, 1-10.
[6]
Hatakeyama, M.; Higashi, H. Helicobacter pylori CagA: a new paradigm for bacterial carcinogenesis. Cancer Sci., 2005, 96(12), 835-843.
[7]
Kim, J.M.; Kim, J.S.; Lee, J.Y.; Kim, Y.J.; Youn, H.J.; Kim, I.Y.; Chee, Y.J.; Oh, Y.K.; Kim, N.; Jung, H.C.; Song, I.S. Vacuolating cytotoxin in Helicobacter pylori water-soluble proteins upregulates chemokine expression in human eosinophils via Ca2+ influx, mitochondrial reactive oxygen intermediates, and NF-kappaB activation. Infect. Immun., 2007, 75(7), 3373-3381.
[8]
Tp, S. A.H.; S.W. Exploiting the gastric epithelial barrier: Helicobacter pylori’s attack on tight and adherent junctions. Curr. Top Microbiol., 2017, 400, 195-226.
[9]
Peek, R.M., Jr; Crabtree, J.E. Helicobacter infection and gastric neoplasia. J. Pathol., 2006, 208(2), 233-248.
[10]
Blaser, M.J.; Atherton, J.C. Helicobacter pylori persistence: biology and disease. J. Clin. Invest., 2004, 113(3), 321-333.
[11]
Suzuki, M.; Mimuro, H.; Suzuki, T.; Park, M.; Yamamoto, T.; Sasakawa, C. Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J. Exp. Med., 2005, 202(9), 1235-1247.
[12]
Hoy, B.; Löwer, M.; Weydig, C.; Carra, G.; Tegtmeyer, N.; Geppert, T.; Schröder, P.; Sewald, N.; Backert, S.; Schneider, G.; Wessler, S. Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep., 2010, 11(10), 798-804.
[13]
Schmidt, T.P.; Perna, A.M.; Fugmann, T.; Böhm, M. Jan Hiss; Haller, S.; Götz, C.; Tegtmeyer, N.; Hoy, B.; Rau, T.T.; Neri, D.; Backert, S.; Schneider, G.; Wessler, S. Identification of E-cadherin signature motifs functioning as cleavage sites for Helicobacter pylori HtrA. Sci. Rep., 2016, 6, 23264.
[14]
Weydig, C.; Starzinski-Powitz, A.; Carra, G.; Löwer, J.; Wessler, S. CagA-independent disruption of adherence junction complexes involves E-cadherin shedding and implies multiple steps in Helicobacter pylori pathogenicity. Exp. Cell Res., 2007, 313(16), 3459-3471.
[15]
Conlin, V.S.; Curtis, S.B.; Zhao, Y.; Moore, E.D.; Smith, V.C.; Meloche, R.M.; Finlay, B.B.; Buchan, A.M. Helicobacter pylori infection targets adherens junction regulatory proteins and results in increased rates of migration in human gastric epithelial cells. Infect. Immun., 2004, 72(9), 5181-5192.
[16]
O’Connor, P.M.; Lapointe, T.K.; Jackson, S.; Beck, P.L.; Jones, N.L.; Buret, A.G. Helicobacter pylori activates calpain via toll-like receptor 2 to disrupt adherens junctions in human gastric epithelial cells. Infect. Immun., 2011, 79(10), 3887-3894.
[17]
Bhardwaj, V.; Noto, J.M.; Wei, J.; Andl, C.; El-Rifai, W.; Peek, R.M.; Zaika, A.I. Helicobacter pylori bacteria alter the p53 stress response via ERK-HDM2 pathway. Oncotarget, 2015, 6(3), 1531-1543.
[18]
Chan, A.O.O.; Lam, S.K.; Wong, B.C.Y.; Wong, W.M.; Yuen, M.F.; Yeung, Y.H.; Hui, W.M.; Rashid, A.; Kwong, Y.L. Promoter methylation of E-cadherin gene in gastric mucosa associated with Helicobacter pylori infection and in gastric cancer. Gut, 2003, 52(4), 502-506.
[19]
Leung, W.K.; Man, E.P.S.; Yu, J.; Go, M.Y.Y.; To, K.F.; Yamaoka, Y.; Cheng, V.Y.Y.; Ng, E.K.W.; Sung, J.J.Y. Effects of Helicobacter pylori eradication on methylation status of E-cadherin gene in noncancerous stomach. Clin. Cancer Res., 2006, 12(10), 3216-3221.
[20]
Kague, E.; Thomazini, C.M.; Pardini, M.I.D.C.M.; Carvalho, Fd.; Leite, C.V.; Pinheiro, N.A. Methylation status of CDH1 gene in samples of gastric mucous from Brazilian patients with chronic gastritis infected by Helicobacter pylori. Arq. Gastroenterol., 2010, 47(1), 7-12.
[21]
Huang, F.Y.; Chan, A.O.; Rashid, A.; Wong, D.K.; Cho, C.H.; Yuen, M.F. Helicobacter pylori induces promoter methylation of E-cadherin via interleukin-1β activation of nitric oxide production in gastric cancer cells. Cancer, 2012, 118(20), 4969-4980.
[22]
Ito, T.; Kobayashi, D.; Uchida, K.; Takemura, T.; Nagaoka, S.; Kobayashi, I.; Yokoyama, T.; Ishige, I.; Ishige, Y.; Ishida, N.; Furukawa, A.; Muraoka, H.; Ikeda, S.; Sekine, M.; Ando, N.; Suzuki, Y.; Yamada, T.; Suzuki, T.; Eishi, Y. Helicobacter pylori invades the gastric mucosa and translocates to the gastric lymph nodes. Lab. Invest., 2008, 88(6), 664-681.
[23]
Eida, M.; Deib, A.E.E.; Saad, A.E.D.; Jankowski, J.A. Down-regulation of E-cadherin and β-catenin in Helicobacter pylori associated gastritis and gastric carcinoma: an immunohistochemical study. Gastrointest. Oncol., 2002, 4, 203-208.
[24]
Schirrmeister, W.; Gnad, T.; Wex, T.; Higashiyama, S.; Wolke, C.; Naumann, M.; Lendeckel, U. Ectodomain shedding of E-cadherin and c-Met is induced by Helicobacter pylori infection. Exp. Cell Res., 2009, 315(20), 3500-3508.
[25]
Ferraz, M.A.; Zabaglia, L.M.; Pereira, W.N.; Orcini, W.A.; de Labio, R.W.; Caleman Neto, A.; Wisnieski, F.; Calcagno, D.Q.; Santos, L.C.; Assumpção, P.P.; Burbano, R.R.; Artigiani, R. Smith, Mde.A.; Payão, S.L.; Rasmussen, L.T. C.; Payão S.L.M.; Rasmussen L.T. Downregulated expression of E-cadherin and TP53 in patients with gastric diseases: the involvement of H. pylori infection and its virulence markers. J. Gastrointest. Cancer, 2016, 47(1), 20-26.
[26]
Bebb, J.R.; Leach, L.; Zaitoun, A.; Hand, N.; Letley, D.P.; Thomas, R.; Atherton, J.C. Effects of Helicobacter pylori on the cadherin-catenin complex. J. Clin. Pathol., 2006, 59(12), 1261-1266.
[27]
Murakami, M.; Fukuzawa, M.; Yamamoto, M.; Hamaya, K.; Tamura, Y.; Sugiyama, A.; Takahashi, R.; Murakami, T.; Amagase, K.; Takeuchi, K. Effects of Helicobacter pylori infection on gastric parietal cells and E-cadherin in Mongolian gerbils. J. Pharmacol. Sci., 2013, 121(4), 305-311.
[28]
Yu, X.W.; Xu, Q.; Gong, Y.H.; Dong, N.N.; Yuan, Y. Detection in situ of E-cadherin, β-catenin, TCF4 and CDX2 in various gastric diseases. Chin. J. Cancer Res., 2009, 21, 185-193.
[29]
Zali, M.R.; Moaven, O.; Asadzadeh Aghdaee, H.; Ghafarzadegan, K.; Ahmadi, K.J.; Farzadnia, M.; Arabi, A.; Abbaszadegan, M.R. Clinicopathological significance of E-cadherin, β-catenin and p53 expression in gastric adenocarinoma. J. Res. Med. Sci., 2009, 14(4), 239-247.
[30]
Lazăr, D.; Tăban, S.; Ardeleanu, C.; Dema, A.; Sporea, I.; Cornianu, M.; Lazăr, E.; Vernic, C. The immunohistochemical expression of E-cadherin in gastric cancer; correlations with clinicopathological factors and patients’ survival. Rom. J. Morphol. Embryol., 2008, 49(4), 459-467.
[31]
Yu, X.W.; Xu, Q.; Xu, Y.; Gong, Y.H.; Yuan, Y. Expression of the E-cadherin/β-catenin/tcf-4 pathway in gastric diseases with relation to Helicobacter pylori infection: clinical and pathological implications. Asian Pac. J. Cancer Prev., 2014, 15(1), 215-220.
[32]
Lin, J.T.; Wang, J.T.; Wang, T.H.; Wu, M.S.; Lee, T.K.; Chen, C.J. Helicobacter pylori infection in a randomly selected population, healthy volunteers, and patients with gastric ulcer and gastric adenocarcinoma. A seroprevalence study in Taiwan. Scand. J. Gastroenterol., 1993, 28(12), 1067-1072.
[33]
Xueqin, W.; Kefeng, J.; Xiaoyun, W. Effect of eradication of Helicobacter pylori on healing and recurrence of peptic ulcer. J. Ningxia Med. Univ., 2009, 31, 106-108.
[34]
Aihara, E.; Matthis, A.L.; Karns, R.A.; Engevik, K.A.; Jiang, P.; Wang, J.; Yacyshyn, B.R.; Montrose, M.H. Epithelial regeneration after gastric ulceration causes prolonged cell-type alterations. Cell. Mol. Gastroenterol. Hepatol., 2016, 2(5), 625-647.
[35]
Xinmin, D.; Huiming, L. The mechanisms of gastric ulcer. Chin. J. Integr. Tradit. West. Med. Dig., 2001, 9, 155-159.
[36]
Hanby, A.M.; Chinery, R.; Poulsom, R.; Playford, R.J.; Pignatelli, M. Downregulation of E-cadherin in the reparative epithelium of the human gastrointestinal tract. Am. J. Pathol., 1996, 148(3), 723-729.
[37]
Zullo, A.; Hassan, C.; Romiti, A.; Giusto, M.; Guerriero, C.; Lorenzetti, R.; Campo, S.M.; Tomao, S. Follow-up of intestinal metaplasia in the stomach: When, how and why. World J. Gastrointest. Oncol., 2012, 4(3), 30-36.
[38]
Sun, G.Y.; Wu, J.X.; Wu, J.S.; Pan, Y.T.; Jin, R. Caveolin-1, E-cadherin and beta-catenin in gastric carcinoma, precancerous tissues and chronic non-atrophic gastritis. Chin. J. Cancer Res., 2012, 24(1), 23-28.
[39]
Romiti, A.; Zullo, A.; Tomao, S.; Hassan, C.; Sarcina, I.; De Francesco, V.; Ierardi, E.; Tomao, F.; Vecchione, A.; Morini, S. Gastric mucosa alterations in first-degree relatives of gastric cancer patients. Anticancer Res., 2005, 25(3c), 2567-2572.
[40]
Rui, W.; Zheng-Yu, S.; Yong-Qiang, Y.; Jie-Lin, Y. Correlation between E-cadherin and VEGF expression of the gastric mucosa. Mod. Digestion Interv., 2015, 20, 319-322.
[41]
Lin, S.; Yan, X. Clinicopathological significance and expression of E-cadherin and FSP-1/S100A4 in gastric carcinoma and the precancerous lesions. Mod. Oncol., 2014, 22, 2903-2908.
[42]
Jianping, Z.; Peiliang, Y.; Qingyuan, Y.; Ming, Y.; Yan, W.; Xiaoling, L.; Wenjun, L. A study of intestinal metaplasia of gastric mucosa and its relationship to gastric carcinoma. Acta. Acad. Med. Shandong, 1997, 35, 203-206.
[43]
Yao, Z.; Jian-Ping, Z.; Feng-Jun, L.; Jing-Yan, Y.; Lin, W. Relationship of expressions of E-cadherin and β-catenin proteins and gastric mucosa intestinal metaplasia and gastric carcinoma. Chin. J. Curr. Adv. Gen. Surg., 2009, 12, 858-860.
[44]
Murata-Kamiya, N.; Kurashima, Y.; Teishikata, Y.; Yamahashi, Y.; Saito, Y.; Higashi, H.; Aburatani, H.; Akiyama, T.; Peek, R.M., Jr; Azuma, T.; Hatakeyama, M. Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene, 2007, 26(32), 4617-4626.
[45]
Zullo, A.; Romiti, A.; Borrini, F.; Hassan, C.; Stella, F.; Sarcina, I.; Martini, M.E.; Tomao, S.; Morini, S.; Mingazzini, P. Alteration of E-cadherin expression in gastric mucosa: role of intestinal metaplasia and Helicobacter pylori infection. Anticancer Res., 2004, 24(3a), 1603-1607.
[46]
Chan, A.O-O.; Wong, B.C-Y.; Lan, H-Y.; Loke, S-L.; Chan, W-K.; Hui, W-M.; Yuen, Y-H.; Ng, I.; Hou, L.; Wong, W-M.; Yuen, M-F.; Luk, J.M-C.; Lam, S-K. Deregulation of E-cadherin-catenin complex in precancerous lesions of gastric adenocarcinoma. J. Gastroenterol. Hepatol., 2003, 18(5), 534-539.
[47]
Wagih, H.M.; El-Ageery, S.M.; Alghaithy, A.A. A study of RUNX3, E-cadherin and β-catenin in CagA-positive Helicobacter pylori associated chronic gastritis in Saudi patients. Eur. Rev. Med. Pharmacol. Sci., 2015, 19(8), 1416-1429.
[48]
Zhou, Y-N.; Xu, C-P.; Han, B.; Li, M.; Qiao, L.; Fang, D-C.; Yang, J-M. Expression of E-cadherin and β-catenin in gastric carcinoma and its correlation with the clinicopathological features and patient survival. World J. Gastroenterol., 2002, 8(6), 987-993.
[49]
Zheng, Z.H.; Sun, X.J.; Ma, M.C.; Hao, D.M.; Liu, Y.H.; Sun, K.L. [Studies of promoter methylation status and protein expression of E-cadherin gene in associated progression stages of gastric cancer] Yi Chuan Xue Bao, 2003, 30(2), 103-108.
[50]
Ahmadi, L.; Kamkari, S.; Mokarram, P.; Lankarani, K.B.; Tabibi, N.; Ashktorab, H.; Vasei, M. HER-2-neu and E-cadherin expression and microsatellite instability in gastric dysplasia. Middle East J. Dig. Dis., 2011, 3(1), 20-27.
[51]
Wang, L.L.; Yao, G.Y.; Zhang, B.Y.; Zhang, X.M.; Zhao, M. [Expression and significance of CD147 and E-cadherin in human gastric carcinoma] Zhonghua Zhong Liu Za Zhi, 2009, 31(7), 515-519.
[52]
Jawhari, A.U.; Noda, M.; Farthing, M.J.; Pignatelli, M. Abnormal expression and function of the E-cadherin-catenin complex in gastric carcinoma cell lines. Br. J. Cancer, 1999, 80(3-4), 322-330.
[53]
Long-Cheng Li, R.M.C. Masahiro Sasaki; Koichi Nakajima; Geetha Perinchery; Harry C. Au; Dana Nojima; Peter Carroll; Rajvir Dahiya. A single nucleotide polymorphism in the E-cadherin gene promoter alters trancscriptional activities. Cancer Res., 2000, 60, 873-876.
[54]
Shin, Y.; Kim, I-J.; Kang, H.C.; Park, J.H.; Park, H.R.; Park, H.W.; Park, M.A.; Lee, J.S.; Yoon, K.A.; Ku, J.L.; Park, J.G. The E-cadherin -347G->GA promoter polymorphism and its effect on transcriptional regulation. Carcinogenesis, 2004, 25(6), 895-899.
[55]
Kaurah, P.; MacMillan, A.; Boyd, N.; Senz, J.; De Luca, A.; Chun, N.; Suriano, G.; Zaor, S.; Van Manen, L.; Gilpin, C.; Nikkel, S.; Connolly-Wilson, M.; Weissman, S.; Rubinstein, W.S.; Sebold, C.; Greenstein, R.; Stroop, J.; Yim, D.; Panzini, B.; McKinnon, W.; Greenblatt, M.; Wirtzfeld, D.; Fontaine, D.; Coit, D.; Yoon, S.; Chung, D.; Lauwers, G.; Pizzuti, A.; Vaccaro, C.; Redal, M.A.; Oliveira, C.; Tischkowitz, M.; Olschwang, S.; Gallinger, S.; Lynch, H.; Green, J.; Ford, J.; Pharoah, P.; Fernandez, B.; Huntsman, D.; Huntsman, D. Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. JAMA, 2007, 297(21), 2360-2372.
[56]
Zeng, W.; Zhu, J.; Shan, L.; Han, Z.; Aerxiding, P.; Quhai, A.; Zeng, F.; Wang, Z.; Li, H. The clinicopathological significance of CDH1 in gastric cancer: a meta-analysis and systematic review. Drug Des. Devel. Ther., 2015, 9, 2149-2157.
[57]
Kuraoka, K.; Oue, N.; Yokozaki, H.; Kitadai, Y.; Ito, R.; Nakayama, H.; Yasui, W. Correlation of a single nucleotide polymorphism in the E-cadherin gene promoter with tumorigenesis and progression of gastric carcinoma in Japan. Int. J. Oncol., 2003, 23(2), 421-427.
[58]
Chen, B.; Zhou, Y.; Yang, P.; Liu, L.; Qin, X.P.; Wu, X.T. CDH1 -160C>A gene polymorphism is an ethnicity-dependent risk factor for gastric cancer. Cytokine, 2011, 55(2), 266-273.
[59]
Borges, B.D.N. Santos, Eda.S.; Bastos, C.E.M.C.; Pinto, L.C.; Anselmo, N.P.; Quaresma, J.A.; Calcagno, D.Q.; Burbano, R.M.; Harada, M.L. Promoter polymorphisms and methylation of E-cadherin (CDH1) and KIT in gastric cancer patients from northern Brazil. Anticancer Res., 2010, 30(6), 2225-2233.
[60]
Pereira, E.D.S.; Silva-Fernandes, I.D.L.; Costa, D.M.D.; Burbano, R.M.R.; Rabenhorst, S.H.B. Association of the polymorphism in DNA repair enzymes and E-cadherin gene with gastric carcinoma risk in population from Brazil. Eur. Acad. Res., 2015, 3, 2286-4822.
[61]
Liu, Y-C.; Shen, C-Y.; Wu, H-S.; Chan, D-C.; Chen, C-J.; Yu, J-C.; Yu, C-P.; Harn, H-J.; Shyu, R-Y.; Shih, Y-L.; Hsieh, C-B.; Hsu, H-M. Helicobacter pylori infection in relation to E-cadherin gene promoter polymorphism and hypermethylation in sporadic gastric carcinomas. World J. Gastroenterol., 2005, 11(33), 5174-5179.
[62]
Batlle, E.; Sancho, E.; Francí, C.; Domínguez, D.; Monfar, M.; Baulida, J.; García De Herreros, A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol., 2000, 2(2), 84-89.
[63]
Moreno-Bueno, G.; Cubillo, E.; Sarrio, D.; Peinado, H.C. Rodrı’Guez-Pinilla S.M.A.; Villa S.; Bolo´S. V.; Jorda M.; Fabra A.; Portillo F.; Palacios J.; Cano A. The Slug zinc-finger protein represses E-cadherin in breast cancer. Cancer Res., 2006, 66, 9543-9556.
[64]
Castro Alves, C.; Rosivatz, E.; Schott, C.; Hollweck, R.; Becker, I.; Sarbia, M.; Carneiro, F.; Becker, K-F. Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the down-regulation of E-cadherin. J. Pathol., 2007, 211(5), 507-515.
[65]
Perez-Moreno, M.A.; Locascio, A.; Rodrigo, I.; Dhondt, G.; Portillo, F.; Nieto, M.A.; Cano, A. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem., 2001, 276(29), 27424-27431.
[66]
Vesuna, F.; van Diest, P.; Chen, J.H.; Raman, V. Twist is a transcriptional repressor of E-cadherin gene expression in breast cancer. Biochem. Biophys. Res. Commun., 2008, 367(2), 235-241.
[67]
Jianfeng, Z. 2016.
[68]
Ma, L.; Young, J.; Prabhala, H.; Pan, E.; Mestdagh, P.; Muth, D.; Teruya-Feldstein, J.; Reinhardt, F.; Onder, T.T.; Valastyan, S.; Westermann, F.; Speleman, F.; Vandesompele, J.; Weinberg, R.A. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat. Cell Biol., 2010, 12(3), 247-256.
[69]
Caldeira, J.; Figueiredo, J.; Brás-Pereira, C.; Carneiro, P.; Moreira, A.M.; Pinto, M.T.; Relvas, J.B.; Carneiro, F.; Barbosa, M.; Casares, F.; Janody, F.; Seruca, R. E-cadherin-defective gastric cancer cells depend on Laminin to survive and invade. Hum. Mol. Genet., 2015, 24(20), 5891-5900.
[70]
Anbiaee, R.; Mojir Sheibani, K.; Torbati, P.; Jaam, H. Abnormal expression of e-cadherin in gastric adenocarcinoma, and its correlation with tumor histopathology and helicobacter pylori infection. Iran. Red Crescent Med. J., 2013, 15(3), 218-222.
[71]
Torabizadeh, Z.; Nosrati, A.; Sajadi Saravi, S.N.; Yazdani Charati, J.; Janbabai, G. Evaluation of E-cadherin expression in gastric cancer and its correlation with clinicopathologic parameters. Int. J. Hematol. Oncol. Stem Cell Res., 2017, 11(2), 158-164.
[72]
Awad, H.; Salih, N.; Adam, E.A.; Gamal, A.; Ellaithi, M. Expression of E-Cadherin and H.pylori in Sudanese patients with gastric adenocarcinoma and gastrointestinal stromal tumors. AI Neelain. Med. J., 2016, 4, 12-30.
[73]
Zhang, J.; Chen, X.Y.; Huang, K.J.; Wu, W.D.; Jiang, T.; Cao, J.; Zhou, L.S.; Qiu, Z.J.; Huang, C. Expression of FoxM1 and the EMT-associated protein E-cadherin in gastric cancer and its clinical significance. Oncol. Lett., 2016, 12(4), 2445-2450.
[74]
Xing, X.; Tang, Y.B.; Yuan, G.; Wang, Y.; Wang, J.; Yang, Y.; Chen, M. The prognostic value of E-cadherin in gastric cancer: a meta-analysis. Int. J. Cancer, 2013, 132(11), 2589-2596.
[75]
Zhong, X-Y.; Zhang, L-H.; Jia, S-Q.; Shi, T.; Niu, Z-J.; Du, H.; Zhang, G-G.; Hu, Y.; Lu, A-P.; Li, J-Y.; Ji, J-F. Positive association of up-regulated Cripto-1 and down-regulated E-cadherin with tumour progression and poor prognosis in gastric cancer. Histopathology, 2008, 52(5), 560-568.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy