Coordinate regulation of N-glycosylation gene DPAGT1, canonical Wnt signaling and E-cadherin adhesion

Journal of Cell Science

Volumn 126, Issue 2, 2013, Pages 484-496

  Sengupta, Pritam K ^a   Bouchie, Meghan P ^a   Nita Lazar, Mihai ^b   Yang, Hsiao Ying ^a   Kukuruzinska, Maria A ^a  

^a BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

catenin; catenin; DPAGT1; E cadherin adhesion; N glycosylation; Wnt signaling

Indexed keywords

BETA CATENIN; MESSENGER RNA; UVOMORULIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CONTACT; CELL DENSITY; CELL JUNCTION; CELL LYSATE; CELL PROLIFERATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOSKELETON; DPAGT1 GENE; GENE; GENE EXPRESSION; GLYCOSYLATION; MDCK CELL; METABOLISM; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; RNA STABILITY; TRANSCRIPTION INITIATION; WNT SIGNALING PATHWAY;

ANIMALS; CADHERINS; CELL ADHESION; DOGS; GLYCOSYLATION; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; N-ACETYLGLUCOSAMINYLTRANSFERASES; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84876071063     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113035     Document Type: Article

References (54)

1. Bradley, R. S., Cowin, P. and Brown, A. M. (1993). Expression of Wnt-1 in PC12 cells results in modulation of plakoglobin and E-cadherin and increased cellular adhesion. J. Cell Biol. 123, 1857-1865.
2. Brembeck, F. H., Rosário, M. and Birchmeier, W. (2006). Balancing cell adhesion and Wnt signaling, the key role of beta-catenin. Curr. Opin. Genet. Dev. 16, 51-59.
3. Chairoungdua, A., Smith, D. L., Pochard, P., Hull, M. and Caplan, M. J. (2010). Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J. Cell Biol. 190, 1079-1091.
4. Clark, G. F., Miller, K. R. and Smith, P. B. (1983). Formation of dolichol-linked sugar intermediates during the postnatal development of skeletal muscle. J. Biol. Chem. 258, 14263-14270.
5. Clevers, H. (2006). Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480.
6. Dignam, J. D., Lebovitz, R. M. and Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.
7. Fernandes, R. P., Cotanche, D. A., Lennon-Hopkins, K., Erkan, F., Menko, A. S. and Kukuruzinska, M. A. (1999). Differential expression of proliferative, cytoskeletal, and adhesive proteins during postnatal development of the hamster submandibular gland. Histochem. Cell Biol. 111, 153-162.
8. Gottardi, C. J. and Gumbiner, B. M. (2004). Role for ICAT in beta-catenin-dependent nuclear signaling and cadherin functions. Am. J. Physiol. Cell Physiol. 286, C747-C756.
9. Gottardi, C. J., Wong, E. and Gumbiner, B. M. (2001). E-cadherin suppresses cellular transformation by inhibiting β-catenin signaling in an adhesion-independent manner. J. Cell Biol. 153, 1049-1060.
10. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
11. Hartsock, A. and Nelson, W. J. (2008). Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim. Biophys. Acta 1778, 660-669.
12. Haÿ, E., Laplantine, E., Geoffroy, V., Frain, M., Kohler, T., Müller, R. and Marie, P. J. (2009). N-cadherin interacts with axin and LRP5 to negatively regulate Wnt/beta-catenin signaling, osteoblast function, and bone formation. Mol. Cell. Biol. 29, 953-964.
13. Hayes, G. R. and Lucas, J. J. (1983). Stimulation of lipid-linked oligosaccharide assembly during oviduct differentiation. J. Biol. Chem. 258, 15095-15100.
14. Helenius, A. and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364-2369.
15. Heuberger, J. and Birchmeier, W. (2010). Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb. Perspect. Biol. 2, a002915.
16. Huang, G. T., Lennon, K. and Kukuruzinska, M. A. (1998). Characterization of multiple transcripts of the hamster dolichol-P-dependent N-acetylglucosamine-1-P transferase suggests functionally complex expression. Mol. Cell. Biochem. 181, 97-106.
17. Jamal, B. T., Nita-Lazar, M., Gao, Z., Amin, B., Walker, J. and Kukuruzinska, M. A. (2009). N-glycosylation status of E-cadherin controls cytoskeletal dynamics through the organization of distinct β-catenin- and γ-catenin-containing AJs. Cell Health Cytoskelet. 2009, 67-80.
18. Jamal, B., Sengupta, P. K., Gao, Z. N., Nita-Lazar, M., Amin, B., Jalisi, S., Bouchie, M. P. and Kukuruzinska, M. A. (2012). Aberrant amplification of the crosstalk between canonical Wnt signaling and N-glycosylation gene DPAGT1 promotes oral cancer. Oral Oncol. 48, 523-529.
19. Jamora, C. and Fuchs, E. (2002). Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4, E101-E108.
20. Jung, H., Lee, S. K. and Jho, E. H. (2011). Mest/Peg1 inhibits Wnt signalling through regulation of LRP6 glycosylation. Biochem. J. 436, 263-269.
21. Khan, Z., Vijayakumar, S., de la Torre, T. V., Rotolo, S. and Bafico, A. (2007). Analysis of endogenous LRP6 function reveals a novel feedback mechanism by which Wnt negatively regulates its receptor. Mol. Cell. Biol. 27, 7291-7301.
22. Kimelman, D. and Xu, W. (2006). beta-catenin destruction complex: insights and questions from a structural perspective. Oncogene 25, 7482-7491.
23. Kobielak, A. and Fuchs, E. (2004). Alpha-catenin: at the junction of intercellular adhesion and actin dynamics. Nat. Rev. Mol. Cell Biol. 5, 614-625.
24. Komekado, H., Yamamoto, H., Chiba, T. and Kikuchi, A. (2007). Glycosylation and palmitoylation of Wnt-3a are coupled to produce an active form of Wnt-3a. Genes Cells 12, 521-534.
25. Kukuruzinska, M. A. and Lennon, K. (1998). Protein N-glycosylation: molecular genetics and functional significance. Crit. Rev. Oral Biol. Med. 9, 415-448.
26. Kuroda, S., Fukata, M., Nakagawa, M., Fujii, K., Nakamura, T., Ookubo, T., Izawa, I., Nagase, T., Nomura, N., Tani, H. et al. (1998). Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 281, 832-835.
27. Lee, E., Salic, A., Krüger, R., Heinrich, R. and Kirschner, M. W. (2003). The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol. 1, E10.
28. Leonard, M., Chan, Y. and Menko, A. S. (2008). Identification of a novel intermediate filament-linked N-cadherin/gamma-catenin complex involved in the establishment of the cytoarchitecture of differentiated lens fiber cells. Dev. Biol. 319, 298-308.
29. Liwosz, A., Lei, T. and Kukuruzinska, M. A. (2006). N-glycosylation affects the molecular organization and stability of E-cadherin junctions. J. Biol. Chem. 281, 23138-23149.
30. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
31. Maeda, O., Usami, N., Kondo, M., Takahashi, M., Goto, H., Shimokata, K., Kusugami, K. and Sekido, Y. (2004). Plakoglobin (gamma-catenin) has TCF/LEF family-dependent transcriptional activity in beta-catenin-deficient cell line. Oncogene 23, 964-972.
32. Maher, M. T., Flozak, A. S., Stocker, A. M., Chenn, A. and Gottardi, C. J. (2009). Activity of the beta-catenin phosphodestruction complex at cell-cell contacts is enhanced by cadherin-based adhesion. J. Cell Biol. 186, 219-228.
33. Meissner, J. D., Naumann, A., Mueller, W. H. and Scheibe, R. J. (1999). Regulation of UDP-N-acetylglucosamine:dolichyl-phosphate N-acetylglucosamine-1-phosphate transferase by retinoic acid in P19 cells. Biochem. J. 338, 561-568.
34. Mendelsohn, R. D., Helmerhorst, E. J., Cipollo, J. F. and Kukuruzinska, M. A. (2005). A hypomorphic allele of the first N-glycosylation gene, ALG7, causes mitochondrial defects in yeast. Biochim. Biophys. Acta 1723, 33-44.
35. Miravet, S., Piedra, J., Miró, F., Itarte, E., García de Herreros, A. and Duñach, M. (2002). The transcriptional factor Tcf-4 contains different binding sites for betacatenin and plakoglobin. J. Biol. Chem. 277, 1884-1891.
36. Mota, O. M., Huang, G. T. and Kukuruzinska, M. A. (1994). Developmental regulation and tissue-specific expression of hamster dolichol-P-dependent Nacetylglucosamine- 1-P transferase (GPT). Biochem. Biophys. Res. Commun. 204, 284-291.
37. Nita-Lazar, M., Noonan, V., Rebustini, I., Walker, J., Menko, A. S. and Kukuruzinska, M. A. (2009). Overexpression of DPAGT1 leads to aberrant Nglycosylation of E-cadherin and cellular discohesion in oral cancer. Cancer Res. 69, 5673-5680.
38. Nita-Lazar, M., Rebustini, I., Walker, J. and Kukuruzinska, M. A. (2010). Hypoglycosylated E-cadherin promotes the assembly of tight junctions through the recruitment of PP2A to adherens junctions. Exp. Cell Res. 316, 1871-1884.
39. Sengupta, P. K., Bouchie, M. P. and Kukuruzinska, M. A. (2010). N-glycosylation gene DPAGT1 is a target of the Wnt/beta-catenin signaling pathway. J. Biol. Chem. 285, 31164-31173.
40. Sharova, L. V., Sharov, A. A., Nedorezov, T., Piao, Y., Shaik, N. and Ko, M. S. (2009). Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 16, 45-58.
41. Shimizu, M., Fukunaga, Y., Ikenouchi, J. and Nagafuchi, A. (2008). Defining the roles of beta-catenin and plakoglobin in LEF/T-cell factor-dependent transcription using beta-catenin/plakoglobin-null F9 cells. Mol. Cell. Biol. 28, 825-835.
42. Steel, M. D., Puddicombe, S. M., Hamilton, L. M., Powell, R. M., Holloway, J. W., Holgate, S. T., Davies, D. E. and Collins, J. E. (2005). Beta-catenin/T-cell factormediated transcription is modulated by cell density in human bronchial epithelial cells. Int. J. Biochem. Cell Biol. 37, 1281-1295.
43. Stefanovic, B., Lindquist, J. and Brenner, D. A. (2000). The 5' stem-loop regulates expression of collagen alpha1(I) mRNA in mouse fibroblasts cultured in a threedimensional matrix. Nucleic Acids Res. 28, 641-647.
44. Stockinger, A., Eger, A., Wolf, J., Beug, H. and Foisner, R. (2001). E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J. Cell Biol. 154, 1185-1196.
45. Takeichi, M. (1995). Morphogenetic roles of classical cadherins. Curr. Opin. Cell Biol. 7, 619-627.
46. Vagin, O., Tokhtaeva, E., Yakubov, I., Shevchenko, E. and Sachs, G. (2008). 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, 2192-2202.
47. van Amerongen, R. and Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214.
48. Walker, J. L., Menko, A. S., Khalil, S., Rebustini, I., Hoffman, M. P., Kreidberg, J. A. and Kukuruzinska, M. A. (2008). Diverse roles of E-cadherin in the morphogenesis of the submandibular gland: insights into the formation of acinar and ductal structures. Dev. Dyn. 237, 3128-3141.
49. Welply, J. K., Lau, J. T. and Lennarz, W. J. (1985). Developmental regulation of glycosyltransferases involved in synthesis of N-linked glycoproteins in sea urchin embryos. Dev. Biol. 107, 252-258.
50. Wheelock, M. J. and Johnson, K. R. (2003). Cadherins as modulators of cellular phenotype. Annu. Rev. Cell Dev. Biol. 19, 207-235.
51. Wu, Z.,Zheng,S., Li, Z.,Tan, J. andYu, Q. (2011). E2F1 suppressesWnt/β-catenin activity through transactivation of β-catenin interacting protein ICAT. Oncogene 30, 3979-3984.
52. Zhao, Y. Y., Takahashi, M., Gu, J. G., Miyoshi, E., Matsumoto, A., Kitazume, S. and Taniguchi, N. (2008). Functional roles of N-glycans in cell signaling and cell adhesion in cancer. Cancer Sci. 99, 1304-1310.
53. Zhurinsky, J., Shtutman, M. and Ben-Ze'ev, A. (2000a). Differential mechanisms of LEF/TCF family-dependent transcriptional activation by beta-catenin and plakoglobin. Mol. Cell. Biol. 20, 4238-4252.
54. Zhurinsky, J., Shtutman, M. and Ben-Ze'ev, A. (2000b). Plakoglobin and beta-catenin: protein interactions, regulation and biological roles. J. Cell Sci. 113, 3127-3139