E-cadherin and adherens-junctions stability in gastric carcinoma: Functional implications of glycosyltransferases involving N-glycan branching biosynthesis, N-acetylglucosaminyltransferases III and v

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 3, 2013, Pages 2690-2700

  Pinho, Salomé S ^a   Figueiredo, Joana ^a,c   Cabral, Joana ^a   Carvalho, Sandra ^a   Dourado, Joana ^a   Magalhães, Ana ^a   Gärtner, Fátima ^a   Mendonça, Ana Maria ^a   Isaji, Tomoya ^b   Gu, Jianguo ^b   Carneiro, Fátima ^a,c,d   Seruca, Raquel ^a,c   Taniguchi, Naoyuki ^e   Reis, Celso A ^a,c  

^a UNIVERSITY OF PORTO   (Portugal)

^b TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^c University of Porto   (Portugal)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

^e RIKEN   (Japan)

Author keywords

Adherens junctions; E cadherin; Gastric cancer; Glycosyltransferases; N glycosylation

Indexed keywords

ALPHA 1,3(6) MANNOSYLGLYCOPROTEIN BETA 1,6 N ACETYLGLUCOSAMINYLTRANSFERASE; CLATHRIN; GLYCAN; GLYCOSYLTRANSFERASE; MESSENGER RNA; N ACETYLGLUCOSAMINYLTRANSFERASE; N ACETYLGLUCOSAMINYLTRANSFERASE III; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CANCER INHIBITION; CANCER INVASION; CANCER TISSUE; CARBOHYDRATE SYNTHESIS; CATALYSIS; CELL ADHESION; CELL JUNCTION; CELL MEMBRANE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN STABILITY; REAL TIME POLYMERASE CHAIN REACTION; STOMACH CARCINOGENESIS; STOMACH CARCINOMA;

ADHERENS JUNCTIONS; CADHERINS; CARCINOMA; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; ENDOCYTOSIS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOSAMINOGLYCANS; HUMANS; KINETICS; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

EID: 84873589547     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.10.021     Document Type: Article

References (48)

1. A. Hartsock, and W.J. Nelson Adherens and tight junctions: structure, function and connections to the actin cytoskeleton Biochim. Biophys. Acta 1778 2008 660 669
2. M. Takeichi Morphogenetic roles of classic cadherins Curr. Opin. Cell Biol. 7 1995 619 627
3. W.J. Nelson Regulation of cell-cell adhesion by the cadherin-catenin complex Biochem. Soc. Trans. 36 2008 149 155
4. F. van Roy, and G. Berx The cell-cell adhesion molecule E-cadherin Cell. Mol. Life Sci. 65 2008 3756 3788
5. K. Xiao, R.G. Oas, C.M. Chiasson, and A.P. Kowalczyk Role of p120-catenin in cadherin trafficking Biochim. Biophys. Acta 1773 2007 8 16
6. K. Xiao, J. Garner, K.M. Buckley, P.A. Vincent, C.M. Chiasson, E. Dejana, V. Faundez, and A.P. Kowalczyk p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin Mol. Biol. Cell 16 2005 5141 5151
7. W. Birchmeier, and J. Behrens Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness Biochim. Biophys. Acta 1198 1994 11 26
8. G. Berx, K.F. Becker, H. Hofler, and F. van Roy Mutations of the human E-cadherin (CDH1) gene Hum. Mutat. 12 1998 226 237
9. C. Oliveira, S. Sousa, H. Pinheiro, R. Karam, R. Bordeira-Carrico, J. Senz, P. Kaurah, J. Carvalho, R. Pereira, L. Gusmao, X. Wen, M.A. Cipriano, J. Yokota, F. Carneiro, D. Huntsman, and R. Seruca Quantification of epigenetic and genetic 2nd hits in CDH1 during hereditary diffuse gastric cancer syndrome progression Gastroenterology 136 2009 2137 2148
10. J. Simoes-Correia, J. Figueiredo, C. Oliveira, J. van Hengel, R. Seruca, F. van Roy, and G. Suriano Endoplasmic reticulum quality control: a new mechanism of E-cadherin regulation and its implication in cancer Hum. Mol. Genet. 17 2008 3566 3576
11. J. Figueiredo, J. Simoes-Correia, O. Soderberg, G. Suriano, and R. Seruca ADP-ribosylation factor 6 mediates E-cadherin recovery by chemical chaperones PLoS One 6 2011 e23188
12. C.C. Alves, F. Carneiro, H. Hoefler, and K.F. Becker Role of the epithelial-mesenchymal transition regulator Slug in primary human cancers Front. Biosci. 14 2009 3035 3050
13. P.A. Gregory, A.G. Bert, E.L. Paterson, S.C. Barry, A. Tsykin, G. Farshid, M.A. Vadas, Y. Khew-Goodall, and G.J. Goodall The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1 Nat. Cell Biol. 10 2008 593 601
14. C.J. Bosques, S. Raguram, and R. Sasisekharan The sweet side of biomarker discovery Nat. Biotechnol. 24 2006 1100 1101
15. A. Helenius, and M. Aebi Intracellular functions of N-linked glycans Science 291 2001 2364 2369
16. S.S. Pinho, R. Seruca, F. Gartner, Y. Yamaguchi, J. Gu, N. Taniguchi, and C.A. Reis Modulation of E-cadherin function and dysfunction by N-glycosylation Cell. Mol. Life Sci. 68 2011 1011 1020
17. M. Yoshimura, Y. Ihara, Y. Matsuzawa, and N. Taniguchi Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis J. Biol. Chem. 271 1996 13811 13815
18. A. Liwosz, T. Lei, and M.A. Kukuruzinska N-glycosylation affects the molecular organization and stability of E-cadherin junctions J. Biol. Chem. 281 2006 23138 23149
19. F. Zhou, J. Su, L. Fu, Y. Yang, L. Zhang, L. Wang, H. Zhao, D. Zhang, Z. Li, and X. Zha Unglycosylation at Asn-633 made extracellular domain of E-cadherin folded incorrectly and arrested in endoplasmic reticulum, then sequentially degraded by ERAD Glycoconj. J. 25 2008 727 740
20. J.C. de Freitas Junior, R. Silva Bdu, W.F. de Souza, W.M. de Araujo, E.S. Abdelhay, and J.A. Morgado-Diaz Inhibition of N-linked glycosylation by tunicamycin induces E-cadherin-mediated cell-cell adhesion and inhibits cell proliferation in undifferentiated human colon cancer cells Cancer Chemother. Pharmacol. 68 2011 227 238
21. M. Przybylo, D. Hoja-Lukowicz, A. Litynska, and P. Laidler Different glycosylation of cadherins from human bladder non-malignant and cancer cell lines Cancer Cell Int. 2 2002 6
22. S.S. Pinho, H. Osorio, M. Nita-Lazar, J. Gomes, C. Lopes, F. Gartner, and C.A. Reis Role of E-cadherin N-glycosylation profile in a mammary tumor model Biochem. Biophys. Res. Commun. 379 2009 1091 1096
23. S.S. Pinho, C.A. Reis, J. Paredes, A.M. Magalhaes, A.C. Ferreira, J. Figueiredo, W. Xiaogang, F. Carneiro, F. Gartner, and R. Seruca The role of N-acetylglucosaminyltransferase III and V in the post-transcriptional modifications of E-cadherin Hum. Mol. Genet. 18 2009 2599 2608
24. Y. Zhao, T. Nakagawa, S. Itoh, K. Inamori, T. Isaji, Y. Kariya, A. Kondo, E. Miyoshi, K. Miyazaki, N. Kawasaki, N. Taniguchi, and J. Gu N-acetylglucosaminyltransferase III antagonizes the effect of N-acetylglucosaminyltransferase V on alpha3beta1 integrin-mediated cell migration J. Biol. Chem. 281 2006 32122 32130
25. M. Yoshimura, A. Nishikawa, Y. Ihara, S. Taniguchi, and N. Taniguchi Suppression of lung metastasis of B16 mouse melanoma by N- acetylglucosaminyltransferase III gene transfection Proc. Natl. Acad. Sci. U. S. A. 92 1995 8754 8758
26. M. Granovsky, J. Fata, J. Pawling, W.J. Muller, R. Khokha, and J.W. Dennis Suppression of tumor growth and metastasis in Mgat5-deficient mice Nat. Med. 6 2000 306 312
27. S. Ihara, E. Miyoshi, J.H. Ko, K. Murata, S. Nakahara, K. Honke, R.B. Dickson, C.Y. Lin, and N. Taniguchi Prometastatic effect of N- acetylglucosaminyltransferase V is due to modification and stabilization of active matriptase by adding beta 1-6 GlcNAc branching J. Biol. Chem. 277 2002 16960 16967
28. H. Saito, A. Nishikawa, J. Gu, Y. Ihara, H. Soejima, Y. Wada, C. Sekiya, N. Niikawa, and N. Taniguchi cDNA cloning and chromosomal mapping of human N-acetylglucosaminyltransferase V + Biochem. Biophys. Res. Commun. 198 1994 318 327
29. I. Weibrecht, K.J. Leuchowius, C.M. Clausson, T. Conze, M. Jarvius, W.M. Howell, M. Kamali-Moghaddam, and O. Soderberg Proximity ligation assays: a recent addition to the proteomics toolbox Expert Rev. Proteomics 7 2010 401 409
30. K.J. Leuchowius, I. Weibrecht, and O. Soderberg In situ proximity ligation assay for microscopy and flow cytometry Curr. Protoc. Cytom. 56 2011 9.36.1 9.36.15
31. G. Suriano, C. Oliveira, P. Ferreira, J.C. Machado, M.C. Bordin, O. De Wever, E.A. Bruyneel, N. Moguilevsky, N. Grehan, T.R. Porter, F.M. Richards, R.H. Hruban, F. Roviello, D. Huntsman, M. Mareel, F. Carneiro, C. Caldas, and R. Seruca Identification of CDH1 germline missense mutations associated with functional inactivation of the E-cadherin protein in young gastric cancer probands Hum. Mol. Genet. 12 2003 575 582
32. P. Lauren The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. an attempt at a histo-clinical classification Acta Pathol. Microbiol. Scand. 64 1965 31 49
33. F. Carneiro, M. Seixas, and M. Sobrinho-Simoes New elements for an updated classification of the carcinomas of the stomach Pathol. Res. Pract. 191 1995 571 584
34. D. Osumi, M. Takahashi, E. Miyoshi, S. Yokoe, S.H. Lee, K. Noda, S. Nakamori, J. Gu, Y. Ikeda, Y. Kuroki, K. Sengoku, M. Ishikawa, and N. Taniguchi Core fucosylation of E-cadherin enhances cell-cell adhesion in human colon carcinoma WiDr cells Cancer Sci. 100 2009 888 895
35. Q. Xu, T. Isaji, Y. Lu, W. Gu, M. Kondo, T. Fukuda, Y. Du, and J. Gu Roles of N-acetylglucosaminyltransferase III in epithelial-to-mesenchymal transition induced by TGF-beta1 in epithelial cell lines J. Biol. Chem. 287 2012 16563 16574
36. Y. Mosesson, G.B. Mills, and Y. Yarden Derailed endocytosis: an emerging feature of cancer Nat. Rev. Cancer 8 2008 835 850
37. Y. Zhao, Y. Sato, T. Isaji, T. Fukuda, A. Matsumoto, E. Miyoshi, J. Gu, and N. Taniguchi Branched N-glycans regulate the biological functions of integrins and cadherins FEBS J. 275 2008 1939 1948
38. Y.Y. Zhao, M. Takahashi, J.G. Gu, E. Miyoshi, A. Matsumoto, S. Kitazume, and N. Taniguchi Functional roles of N-glycans in cell signaling and cell adhesion in cancer Cancer Sci. 99 2008 1304 1310
39. H.B. Guo, H. Johnson, M. Randolph, T. Nagy, R. Blalock, and M. Pierce Specific posttranslational modification regulates early events in mammary carcinoma formation Proc. Natl. Acad. Sci. U. S. A. 107 2010 21116 21121
40. H.B. Guo, I. Lee, M. Kamar, and M. Pierce N-acetylglucosaminyltransferase V expression levels regulate cadherin-associated homotypic cell-cell adhesion and intracellular signaling pathways J. Biol. Chem. 278 2003 52412 52424
41. H.B. Guo, H. Johnson, M. Randolph, and M. Pierce Regulation of homotypic cell-cell adhesion by branched N-glycosylation of N-cadherin extracellular EC2 and EC3 domains J. Biol. Chem. 284 2009 34986 34997
42. M. Nita-Lazar, V. Noonan, I. Rebustini, J. Walker, A.S. Menko, and M.A. Kukuruzinska Overexpression of DPAGT1 leads to aberrant N-glycosylation of E-cadherin and cellular discohesion in oral cancer Cancer Res. 69 2009 5673 5680
43. O. Vagin, E. Tokhtaeva, I. Yakubov, E. Shevchenko, and G. Sachs Inverse correlation between the extent of N-glycan branching and intercellular adhesion in epithelia. Contribution of the Na, K-ATPase beta1 subunit J. Biol. Chem. 283 2008 2192 2202
44. Y. Song, J.A. Aglipay, J.D. Bernstein, S. Goswami, and P. Stanley The bisecting GlcNAc on N-glycans inhibits growth factor signaling and retards mammary tumor progression Cancer Res. 70 2010 3361 3371
45. P. Stanley Biological consequences of overexpressing or eliminating N-acetylglucosaminyltransferase-TIII in the mouse Biochim. Biophys. Acta 1573 2002 363 368
46. S.S. Pinho, P. Oliveira, J. Cabral, S. Carvalho, D. Huntsman, F. Gartner, R. Seruca, C.A. Reis, and C. Oliveira Loss and recovery of Mgat3 and GnT-III mediated E-cadherin N-glycosylation is a mechanism involved in epithelial-mesenchymal-epithelial transitions PLoS One 7 2012 e33191
47. M. Terao, A. Ishikawa, S. Nakahara, A. Kimura, A. Kato, K. Moriwaki, Y. Kamada, H. Murota, N. Taniguchi, I. Katayama, and E. Miyoshi Enhanced epithelial-mesenchymal transition-like phenotype in N- acetylglucosaminyltransferase V transgenic mouse skin promotes wound healing J. Biol. Chem. 286 2011 28303 28311
48. K. Polyak, and R.A. Weinberg Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits Nat. Rev. Cancer 9 2009 265 273