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(American Journal of Pathology. 1998;153:333-339.)
© 1998 American Society for Investigative Pathology

Reviews

Inactivation of the E-Cadherin-Mediated Cell Adhesion System in Human Cancers

Setsuo Hirohashi

From the Pathology Division, National Cancer Center Research Institute, 1-1, Tsukiji 5-chome, Chuo-ku, Tokyo 104, and Hirohashi Cell Configuration Project, ERATO, Japan Scientific and Technology Corporation, Tsukuba Research Consortium, 9-4, Tokodai 5-chome, Tsukuba 300-26, Japan

Abstract

It has long been known that cell-cell adhesiveness is generally reduced in human cancers. Tumor cells are dissociated throughout the entire tumor masses of diffuse-type cancers, whereas those of solid tumors with high metastatic potentials are often focally dissociated or dedifferentiated at the invading fronts. Thus, both irreversible and reversible mechanisms for inactivating the cell adhesion system appear to exist. This paper focuses on the cadherin system, which mediates Ca2+-dependent homophilic cell-cell adhesion. The E (epithelial)-cadherin-mediated cell adhesion system in cancer cells is inactivated by multiple mechanisms corresponding to the pathological features described above. Mutations have been found in the genes for E-cadherin and its undercoat proteins, {alpha}- and ß-catenins, which connect cadherins to actin filaments and establish firm cell-cell adhesion. Transcriptional inactivation of E-cadherin expression was shown to occur frequently in tumor progression. E-cadherin expression in human cancer cells is regulated by CpG methylation around the promoter region. The cadherin system interacts directly with products of oncogenes, eg, c-erbB-2 protein and the epidermal growth factor receptor, and of the tumor suppressor gene, adenomatous polyposis coli (APC) protein, through ß-catenin, which may be important in signal transduction pathways contributing to the determination of the biological properties of human cancers. In conclusion, inactivation of the E-cadherin system by multiple mechanisms, including both genetic and epigenetic events, plays a significant role in multistage carcinogenesis.




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 Cancer Res.Home page
K. Nakanishi, M. Sakamoto, J. Yasuda, M. Takamura, N. Fujita, T. Tsuruo, S. Todo, and S. Hirohashi
Critical Involvement of the Phosphatidylinositol 3-Kinase/Akt Pathway in Anchorage-independent Growth and Hematogeneous Intrahepatic Metastasis of Liver Cancer
Cancer Res., May 1, 2002; 62(10): 2971 - 2975.
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 Am. J. Pathol.Home page
N. A. C. S. Wong and M. Pignatelli
{beta}-Catenin--A Linchpin in Colorectal Carcinogenesis?
Am. J. Pathol., February 1, 2002; 160(2): 389 - 401.
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 CROBMHome page
G. Li, K. Satyamoorthy, and M. Herlyn
DYNAMICS OF CELL INTERACTIONS AND COMMUNICATIONS DURING MELANOMA DEVELOPMENT
Critical Reviews in Oral Biology & Medicine, January 1, 2002; 13(1): 62 - 70.
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 Am. J. Pathol.Home page
T. Saito, Y. Oda, K. Sugimachi, K.-i. Kawaguchi, S. Tamiya, K. Tanaka, S. Matsuda, A. Sakamoto, Y. Iwamoto, and M. Tsuneyoshi
E-Cadherin Gene Mutations Frequently Occur in Synovial Sarcoma as a Determinant of Histological Features
Am. J. Pathol., December 1, 2001; 159(6): 2117 - 2124.
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 Am. J. Pathol.Home page
A. Jung, M. Schrauder, U. Oswald, C. Knoll, P. Sellberg, R. Palmqvist, G. Niedobitek, T. Brabletz, and T. Kirchner
The Invasion Front of Human Colorectal Adenocarcinomas Shows Co-Localization of Nuclear {beta}-Catenin, Cyclin D1, and p16INK4A and Is a Region of Low Proliferation
Am. J. Pathol., November 1, 2001; 159(5): 1613 - 1617.
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 Proc. Natl. Acad. Sci. USAHome page
T. Brabletz, A. Jung, S. Reu, M. Porzner, F. Hlubek, L. A. Kunz-Schughart, R. Knuechel, and T. Kirchner
Variable beta -catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment
PNAS, August 28, 2001; 98(18): 10356 - 10361.
[Abstract] [Full Text] [PDF]

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 Genes Dev.Home page
A. Prokhortchouk, B. Hendrich, H. Jorgensen, A. Ruzov, M. Wilm, G. Georgiev, A. Bird, and E. Prokhortchouk
The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor
Genes & Dev., July 1, 2001; 15(13): 1613 - 1618.
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 Cancer Res.Home page
K. O. Toyooka, S. Toyooka, A. K. Virmani, U. G. Sathyanarayana, D. M. Euhus, M. Gilcrease, J. D. Minna, and A. F. Gazdar
Loss of Expression and Aberrant Methylation of the CDH13 (H-Cadherin) Gene in Breast and Lung Carcinomas
Cancer Res., June 1, 2001; 61(11): 4556 - 4560.
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 Cancer Res.Home page
A. Menke, C. Philippi, R. Vogelmann, B. Seidel, M. P. Lutz, G. Adler, and D. Wedlich
Down-Regulation of E-Cadherin Gene Expression by Collagen Type I and Type III in Pancreatic Cancer Cell Lines
Cancer Res., April 1, 2001; 61(8): 3508 - 3517.
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 Cancer Res.Home page
Y. Naishiro, T. Yamada, A. S. Takaoka, R. Hayashi, F. Hasegawa, K. Imai, and S. Hirohashi
Restoration of Epithelial Cell Polarity in a Colorectal Cancer Cell Line by Suppression of {beta}-catenin/T-Cell Factor 4-mediated Gene Transactivation
Cancer Res., March 1, 2001; 61(6): 2751 - 2758.
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 CarcinogenesisHome page
C. A. Blum, M. Xu, G. A. Orner, A. T. Fong, G. S. Bailey, G. D. Stoner, D. T. Horio, and R. H. Dashwood
{beta}-Catenin mutation in rat colon tumors initiated by 1,2-dimethylhydrazine and 2-amino-3-methylimidazo[4,5-f]quinoline, and the effect of post-initiation treatment with chlorophyllin and indole-3-carbinol
Carcinogenesis, February 1, 2001; 22(2): 315 - 320.
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 JNCI J Natl Cancer InstHome page
E. R. Fearon
BRCA1 and E-Cadherin Promoter Hypermethylation and Gene Inactivation in Cancer--Association or Mechanism?
J Natl Cancer Inst, April 5, 2000; 92(7): 515 - 517.
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 JNCI J Natl Cancer InstHome page
G. Tamura, J. Yin, S. Wang, A. S. Fleisher, T. Zou, J. M. Abraham, D. Kong, K. N. Smolinski, K. T. Wilson, S. P. James, et al.
E-Cadherin Gene Promoter Hypermethylation in Primary Human Gastric Carcinomas
J Natl Cancer Inst, April 5, 2000; 92(7): 569 - 573.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
H. Huang, B. M. Mahler-Araujo, A. Sankila, L. Chimelli, Y. Yonekawa, P. Kleihues, and H. Ohgaki
APC Mutations in Sporadic Medulloblastomas
Am. J. Pathol., February 1, 2000; 156(2): 433 - 437.
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 Am. J. Pathol.Home page
H. Huang, H. Fujii, A. Sankila, B. M. Mahler-Araujo, M. Matsuda, G. Cathomas, and H. Ohgaki
{beta}-Catenin Mutations Are Frequent in Human Hepatocellular Carcinomas Associated with Hepatitis C Virus Infection
Am. J. Pathol., December 1, 1999; 155(6): 1795 - 1801.
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 Am. J. Pathol.Home page
K.-F. Becker, E. Kremmer, M. Eulitz, I. Becker, G. Handschuh, C. Schuhmacher, W. Muller, H. E. Gabbert, A. Ochiai, S. Hirohashi, et al.
Analysis of E-Cadherin in Diffuse-Type Gastric Cancer Using a Mutation-Specific Monoclonal Antibody
Am. J. Pathol., December 1, 1999; 155(6): 1803 - 1809.
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 Am. J. Pathol.Home page
C. Gamallo, J. Palacios, G. Moreno, J. Calvo de Mora, A. Suarez, and A. Armas
{beta}-Catenin Expression Pattern in Stage I and II Ovarian Carcinomas : Relationship with {beta}-Catenin Gene Mutations,Clinicopathological Features, and Clinical Outcome
Am. J. Pathol., August 1, 1999; 155(2): 527 - 536.
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 Am. J. Pathol.Home page
Y. Maeno, S. Moroi, H. Nagashima, T. Noda, H. Shiozaki, M. Monden, S. Tsukita, and A. Nagafuchi
{alpha}-Catenin-Deficient F9 Cells Differentiate into Signet Ring Cells
Am. J. Pathol., May 1, 1999; 154(5): 1323 - 1328.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
J. A. Efstathiou and M. Pignatelli
Modulation of Epithelial Cell Adhesion in Gastrointestinal Homeostasis
Am. J. Pathol., August 1, 1998; 153(2): 341 - 347.
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 J. Biol. Chem.Home page
A. L. Giannini, M. d. M. Vivanco, and R. M. Kypta
alpha -Catenin Inhibits beta -Catenin Signaling by Preventing Formation of a beta -Catenin{middle dot}T-cell Factor{middle dot}DNA Complex
J. Biol. Chem., July 14, 2000; 275(29): 21883 - 21888.
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 J. Biol. Chem.Home page
I. Poser, D. Dominguez, A. G. de Herreros, A. Varnai, R. Buettner, and A. K Bosserhoff
Loss of E-cadherin Expression in Melanoma Cells Involves Up-regulation of the Transcriptional Repressor Snail
J. Biol. Chem., June 29, 2001; 276(27): 24661 - 24666.
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 Proc. Natl. Acad. Sci. USAHome page
Y. Ino, M. Gotoh, M. Sakamoto, K. Tsukagoshi, and S. Hirohashi
Dysadherin, a cancer-associated cell membrane glycoprotein, down-regulates E-cadherin and promotes metastasis
PNAS, January 8, 2002; 99(1): 365 - 370.
[Abstract] [Full Text] [PDF]


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