Galectin-3 regulates desmoglein-2 and intestinal epithelial intercellular adhesion

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10510-10517

  Jiang, Kun ^a   Rankin, Carl R ^a   Nava, Porfirio ^a,b   Sumagin, Ronen ^a   Kamekura, Ryuta ^a   Stowell, Sean R ^a   Feng, Mingli ^a   Parkos, Charles A ^a   Nusrat, Asma ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; CELL MEMBRANES;

CELL SURFACES; DESMOSOME; ECTODOMAIN; INTERCELLULAR ADHESION; INTESTINAL EPITHELIAL CELLS;

ADHESION;

CADHERIN; DESMOGLEIN 2; GALECTIN 3; LACTOSE; PROTEASOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MEMBRANE; CONTROLLED STUDY; DOWN REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN SYNTHESIS;

CELL-CELL INTERACTION; DESMOGLEIN-2; DESMOSOME; GALECTIN; GALECTIN-3F; INTESTINAL EPITHELIUM; PROTEIN STABILITY;

ANIMALS; CELL ADHESION; CELL COMMUNICATION; CELL LINE; CELL PROLIFERATION; DESMOGLEIN 2; EPITHELIAL CELLS; EPITHELIUM; GALACTOSE; GALECTIN 3; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; INTESTINES; LACTOSE; MEMBRANE MICRODOMAINS; MICE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STRUCTURE, TERTIARY; PROTEOMICS; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING;

EID: 84898653028     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.538538     Document Type: Article

References (59)

1. Kamekura, R., Kolegraff, K. N., Nava, P., Hilgarth, R. S., Feng, M., Parkos, C. A., and Nusrat, A. (2013) Loss of the desmosomal cadherin desmoglein- 2 suppresses colon cancer cell proliferation through EGFR signaling. Oncogene 10.1038/onc.2013.442
2. Nava, P., Laukoetter, M. G., Hopkins, A. M., Laur, O., Gerner-Smidt, K., Green, K. J., Parkos, C. A., and Nusrat, A. (2007) Desmoglein-2: a novel regulator of apoptosis in the intestinal epithelium. Mol. Biol. Cell 18, 4565-4578
3. Eshkind, L., Tian, Q., Schmidt, A., Franke, W. W., Windoffer, R., and Leube, R. E. (2002) Loss of desmoglein 2 suggests essential functions for early embryonic development and proliferation of embryonal stem cells. Eur. J. Cell Biol. 81, 592-598
4. Schlegel, N., Meir, M., Heupel, W. M., Holthöfer, B., Leube, R. E., and Waschke, J. (2010) Desmoglein 2-mediated adhesion is required for intestinal epithelial barrier integrity. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G774-G783
5. Chen, J., Nekrasova, O. E., Patel, D. M., Klessner, J. L., Godsel, L. M., Koetsier, J. L., Amargo, E. V., Desai, B. V., and Green, K. J. (2012) The C-terminal unique region of desmoglein 2 inhibits its internalization via tail-tail interactions. J. Cell Biol. 199, 699-711
6. Wang, H., Yumul, R., Cao, H., Ran, L., Fan, X., Richter, M., Epstein, F., Gralow, J., Zubieta, C., Fender, P., and Lieber, A. (2013) Structural and functional studies on the interaction of adenovirus fiber knobs and desmoglein 2. J. Virol. 87, 11346-11362
7. Brooke, M. A., Nitoiu, D., and Kelsell, D. P. (2012) Cell-cell connectivity: desmosomes and disease. J. Pathol. 226, 158-171
8. Dusek, R. L., and Attardi, L. D. (2011) Desmosomes: new perpetrators in tumour suppression. Nat. Rev. Cancer 11, 317-323
9. Kolegraff, K., Nava, P., Helms, M. N., Parkos, C. A., and Nusrat, A. (2011) Loss of desmocollin-2 confers a tumorigenic phenotype to colonic epithelial cells through activation of Akt/β-catenin signaling. Mol. Biol. Cell 22, 1121-1134
10. Yashiro, M., Nishioka, N., and Hirakawa, K. (2006) Decreased expression of the adhesion molecule desmoglein-2 is associated with diffuse-type gastric carcinoma. Eur. J. Cancer 42, 2397-2403
11. Fukushima, K., Yonezawa, H., and Fiocchi, C. (2003) Inflammatory bowel disease-associated gene expression in intestinal epithelial cells by differential cDNA screening and mRNA display. Inflamm. Bowel Dis. 9, 290-301
12. Klessner, J. L., Desai, B. V., Amargo, E. V., Getsios, S., and Green, K. J. (2009) EGFR and ADAMs cooperate to regulate shedding and endocytic trafficking of the desmosomal cadherin desmoglein 2. Mol. Biol. Cell 20, 328-337
13. Marcozzi, C., Burdett, I. D., Buxton, R. S., and Magee, A. I. (1998) Coexpression of both types of desmosomal cadherin and plakoglobin confers strong intercellular adhesion. J. Cell Sci. 111, 495-509
14. Vasioukhin, V., Bowers, E., Bauer, C., Degenstein, L., and Fuchs, E. (2001) Desmoplakin is essential in epidermal sheet formation. Nat. Cell Biol. 3, 1076-1085
15. Cheng, X., and Koch, P. J. (2004) In vivo function of desmosomes. J. Dermatol. 31, 171-187
16. Garrod, D. R., Merritt, A. J., and Nie, Z. (2002) Desmosomal cadherins. Curr. Opin. Cell Biol. 14, 537-545
17. Green, K. J., and Simpson, C. L. (2007) Desmosomes: new perspectives on a classic. J. Invest. Dermatol. 127, 2499-2515
18. Mahoney, M. G., Hu, Y., Brennan, D., Bazzi, H., Christiano, A. M., and Wahl, J. K., 3rd (2006) Delineation of diversified desmoglein distribution in stratified squamous epithelia: implications in diseases. Exp. Dermatol. 15, 101-109
19. Holthöfer, B., Windoffer, R., Troyanovsky, S., and Leube, R. E. (2007) Structure and function of desmosomes. Int. Rev. Cytol. 264, 65-163
20. Chen, R., Jiang, X., Sun, D., Han, G., Wang, F., Ye, M., Wang, L., and Zou, H. (2009) Glycoproteomics analysis of human liver tissue by combination of multiple enzyme digestion and hydrazide chemistry. J. Proteome Res. 8, 651-661
21. Wollscheid, B., Bausch-Fluck, D., Henderson, C., O'Brien, R., Bibel, M., Schiess, R., Aebersold, R., and Watts, J. D. (2009) Mass-spectrometric identification and relative quantification ofN-linked cell surface glycoproteins. Nat. Biotechnol. 27, 378-386
22. Syed, S. E., Trinnaman, B., Martin, S., Major, S., Hutchinson, J., and Magee, A. I. (2002) Molecular interactions between desmosomal cadherins. Biochem. J. 362, 317-327
23. Moutsatsos, I. K., Davis, J. M., and Wang, J. L. (1986) Endogenous lectins from cultured cells: subcellular localization of carbohydrate-binding protein 35 in 3T3 fibroblasts. J. Cell Biol. 102, 477-483
24. Cho, M., and Cummings, R. D. (1995) Galectin-1, aβ-galactoside- binding lectin in Chinese hamster ovary cells. II. Localization and biosynthesis. J. Biol. Chem. 270, 5207-5212
25. Danielsen, E. M., and van Deurs, B. (1997) Galectin-4 and small intestinal brush border enzymes form clusters. Mol. Biol. Cell 8, 2241-2251
26. Thomsen, M. K., Hansen, G. H., and Danielsen, E. M. (2009) Galectin-2 at the enterocyte brush border of the small intestine. Mol. Membr. Biol. 26, 347-355
27. Chabot, S., Kashio, Y., Seki, M., Shirato, Y., Nakamura, K., Nishi, N., Nakamura, T., Matsumoto, R., and Hirashima, M. (2002) Regulation of galectin- 9 expression and release in Jurkat T cell line cells. Glycobiology 12, 111-118
28. Cherayil, B. J., Chaitovitz, S., Wong, C., and Pillai, S. (1990) Molecular cloning of a human macrophage lectin specific for galactose. Proc. Natl. Acad. Sci. U.S.A. 87, 7324-7328
29. Ahmad, N., Gabius, H. J., André, S., Kaltner, H., Sabesan, S., Roy, R., Liu, B., Macaluso, F., and Brewer, C. F. (2004) Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heterogeneous cross-linked complexes. J. Biol. Chem. 279, 10841-10847
30. Lepur, A., Salomonsson, E., Nilsson, U. J., and Leffler, H. (2012) Ligand induced galectin-3 protein self-association. J. Biol. Chem. 287, 21751-21756
31. Morris, S., Ahmad, N., André, S., Kaltner, H., Gabius, H. J., Brenowitz, M., and Brewer, F. (2004) Quaternary solution structures of galectins-1, -3, and -7. Glycobiology 14, 293-300
32. Inohara, H., and Raz, A. (1995) Functional evidence that cell surface galectin- 3 mediates homotypic cell adhesion. Cancer Res. 55, 3267-3271
33. Partridge, E. A., Le Roy, C., Di Guglielmo, G. M., Pawling, J., Cheung, P., Granovsky, M., Nabi, I. R., Wrana, J. L., and Dennis, J. W. (2004) Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306, 120-124
34. Boscher, C., and Nabi, I. R. (2013) Galectin-3- and phospho-caveolin-1- dependent outside-in integrin signaling mediates the EGF motogenic response in mammary cancer cells. Mol. Biol. Cell 24, 2134-2145
35. Boscher, C., Zheng, Y. Z., Lakshminarayan, R., Johannes, L., Dennis, J. W., Foster, L. J., and Nabi, I. R. (2012) Galectin-3 protein regulates mobility of N-cadherin and GM1 ganglioside at cell-cell junctions of mammary carcinoma cells. J. Biol. Chem. 287, 32940-32952
36. Lajoie, P., Partridge, E. A., Guay, G., Goetz, J. G., Pawling, J., Lagana, A., Joshi, B., Dennis, J. W., and Nabi, I. R. (2007) Plasma membrane domain organization regulates EGFR signaling in tumor cells. J. Cell Biol. 179, 341-356
37. Friedrichs, J., Manninen, A., Muller, D. J., and Helenius, J. (2008) Galectin- 3 regulates integrinα2β1-mediated adhesion to collagen-I and -IV. J. Biol. Chem. 283, 32264-32272
38. Furtak, V., Hatcher, F., and Ochieng, J. (2001) Galectin-3 mediates the endocytosis ofβ-1 integrins by breast carcinoma cells. Biochem. Biophys. Res. Commun. 289, 845-850
39. Lau, K. S., Partridge, E. A., Grigorian, A., Silvescu, C. I., Reinhold, V. N., Demetriou, M., and Dennis, J. W. (2007) Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129, 123-134
40. Rankin, C. R., Hilgarth, R. S., Leoni, G., Kwon, M., Den Beste, K. A., Parkos, C. A., and Nusrat, A. (2013) Annexin A2 regulatesβ1 integrin internalization and intestinal epithelial cell migration. J. Biol. Chem. 288, 15229-15239
41. Kolegraff, K., Nava, P., Laur, O., Parkos, C. A., and Nusrat, A. (2011) Characterization of full-length and proteolytic cleavage fragments of desmoglein- 2 in native human colon and colonic epithelial cell lines. Cell Adh. Migr. 5, 306-314
42. Shimoyama, Y., Hirohashi, S., Hirano, S., Noguchi, M., Shimosato, Y., Takeichi, M., and Abe, O. (1989) Cadherin cell-adhesion molecules in human epithelial tissues and carcinomas. Cancer Res. 49, 2128-2133
43. Monteiro, A. C., Sumagin, R., Rankin, C. R., Leoni, G., Mina, M. J., Reiter, D. M., Stehle, T., Dermody, T. S., Schaefer, S. A., Hall, R. A., Nusrat, A., and Parkos, C. A. (2013) JAM-A associates with ZO-2, afadin, and PDZ-GEF1 to activate Rap2c and regulate epithelial barrier function. Mol. Biol. Cell 24, 2849-2860
44. Sumagin, R., Robin, A. Z., Nusrat, A., and Parkos, C. A. (2013) Transmigrated neutrophils in the intestinal lumen engage ICAM-1 to regulate the epithelial barrier and neutrophil recruitment. Mucosal Immunol. 10.1038/mi.2013.106
45. Hirabayashi, J., Hashidate, T., Arata, Y., Nishi, N., Nakamura, T., Hi- rashima, M., Urashima, T., Oka, T., Futai, M., Muller, W. E., Yagi, F., and Kasai, K. (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim. Biophys. Acta 1572, 232-254
46. Ho, M. K., and Springer, T. A. (1982) Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J. Immunol. 128, 1221-1228
47. Kowalczyk, A. P., Bornslaeger, E. A., Norvell, S. M., Palka, H. L., and Green, K. J. (1999) Desmosomes: intercellular adhesive junctions specialized for attachment of intermediate filaments. Int. Rev. Cytol. 185, 237-302
48. Langer, M. D., Guo, H., Shashikanth, N., Pierce, J. M., and Leckband, D. E. (2012) N-Glycosylation alters cadherin-mediated intercellular binding kinetics. J. Cell Sci. 125, 2478-2485
49. Inohara, H., Akahani, S., Koths, K., and Raz, A. (1996) Interactions between galectin-3 and Mac-2-binding protein mediate cell-cell adhesion. Cancer Res. 56, 4530-4534
50. Zou, J., Glinsky, V. V., Landon, L. A., Matthews, L., and Deutscher, S. L. (2005) Peptides specific to the galectin-3 carbohydrate recognition domain inhibit metastasis-associated cancer cell adhesion. Carcinogenesis 26, 309-318
51. Hartsock, A., and Nelson, W. J. (2012) Competitive regulation of E-cadherin juxtamembrane domain degradation by p120-catenin binding and Hakai-mediated ubiquitination. PLoS One 7, e37476
52. Brennan, D., Peltonen, S., Dowling, A., Medhat, W., Green, K. J., Wahl, J. K., 3rd, Del Galdo, F., and Mahoney, M. G. (2012) A role for caveolin-1 in desmoglein binding and desmosome dynamics. Oncogene 31, 1636-1648
53. Resnik, N., Sepcic, K., Plemenitas, A., Windoffer, R., Leube, R., and Veranic, P. (2011) Desmosome assembly and cell-cell adhesion are membrane raft-dependent processes. J. Biol. Chem. 286, 1499-1507
54. Jensen-Jarolim, E., Gscheidlinger, R., Oberhuber, G., Neuchrist, C., Lucas, T., Bises, G., Radauer, C., Willheim, M., Scheiner, O., Liu, F. T., and Boltz- Nitulescu, G. (2002) The constitutive expression of galectin-3 is downregulated in the intestinal epithelia of Crohn's disease patients, and tumour necrosis factorα decreases the level of galectin-3-specific mRNA in HCT-8 cells. Eur. J. Gastroenterol. Hepatol. 14, 145-152
55. Brazowski, E., Dotan, I., Tulchinsky, H., Filip, I., and Eisenthal, A. (2009) Galectin-3 expression in pouchitis in patients with ulcerative colitis who underwent ileal pouch-anal anastomosis (IPAA). Pathol. Res. Pract. 205, 551-558
56. Jensen-Jarolim, E., Neumann, C., Oberhuber, G., Gscheidlinger, R., Neuchrist, C., Reinisch, W., Zuberi, R. I., Penner, E., Liu, F. T., and Boltz- Nitulescu, G. (2001) Anti-Galectin-3 IgG autoantibodies in patients with Crohn's disease characterized by means of phage display peptide libraries. J. Clin. Immunol. 21, 348-356
57. Campbell, B. J., Yu, L. G., and Rhodes, J. M. (2001) Altered glycosylation in inflammatory bowel disease: a possible role in cancer development. Glycoconj. J. 18, 851-858
58. Bodger, K., Halfvarson, J., Dodson, A. R., Campbell, F., Wilson, S., Lee, R., Lindberg, E., Järnerot, G., Tysk, C., and Rhodes, J. M. (2006) Altered colonic glycoprotein expression in unaffected monozygotic twins of inflammatory bowel disease patients. Gut 55, 973-977
59. Shinzaki, S., Kuroki, E., Iijima, H., Tatsunaka, N., Ishii, M., Fujii, H., Kamada, Y., Kobayashi, T., Shibukawa, N., Inoue, T., Tsujii, M., Takeishi, S., Mizushima, T., Ogata, A., Naka, T., Plevy, S. E., Takehara, T., and Miyoshi, E. (2013) Lectin-based immunoassay for aberrant IgG glycosylation as the biomarker for Crohn's disease. Inflamm. Bowel Dis. 19, 321-331