β-Galactoside α2,6-sialyltranferase 1 promotes transforming growth factor-β-mediated epithelial-mesenchymal transition

Journal of Biological Chemistry

Volumn 289, Issue 50, 2014, Pages 34627-34641

  Lu, Jishun ^a   Isaji, Tomoya ^a   Im, Sanghun ^a   Fukuda, Tomohiko ^a   Hashii, Noritaka ^b   Takakura, Daisuke ^b   Kawasaki, Nana ^b   Gu, Jianguo ^a  

^a TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; GLYCOPROTEINS; POLYSACCHARIDES;

ADHERENS JUNCTIONS; E-CADHERIN EXPRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; HUMAN BREAST CANCER CELLS; MALIGNANT PROGRESSION; PLAUSIBLE MECHANISMS; TRANSFORMING GROWTH FACTORS; TUMOR PROGRESSIONS;

CYTOLOGY;

BETA GALACTOSIDE; BETA GALACTOSIDE ALPHA2, 6 SIALYLTRANFERASE 1; INTEGRIN; PROTEIN KINASE B; SIALYLTRANSFERASE; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; CADHERIN; LEUKOCYTE ANTIGEN; ST6GAL1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ARTICLE; BREAST CANCER CELL LINE; CELL ADHESION; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIALYLATION; SIGNAL TRANSDUCTION; ST6GAL1 GENE; UPREGULATION; BINDING SITE; BREAST TUMOR; CELL MOTION; DEFICIENCY; DISEASE COURSE; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

ANTIGENS, CD; BINDING SITES; BREAST NEOPLASMS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE KNOCKDOWN TECHNIQUES; GENE SILENCING; HUMANS; PHENOTYPE; PROMOTER REGIONS, GENETIC; SIALYLTRANSFERASES; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84918561625     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593392     Document Type: Article

References (62)

1. Tarin, D., Thompson, E. W., and Newgreen, D. F. (2005) The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res. 65, 5996-6000; discussion 6000-6001
2. Thiery, J. P., and Sleeman, J. P. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142
3. Greenburg, G., and Hay, E. D. (1982) Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells. J. Cell Biol. 95, 333-339
4. Hay, E. D. (1995) An overview of epithelio-mesenchymal transformation. Acta Anat. 154, 8-20
5. Hugo, H., Ackland, M. L., Blick, T., Lawrence, M. G., Clements, J. A., Williams, E. D., and Thompson, E. W. (2007) Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J. Cell. Physiol. 213, 374-383
6. Roberts, A. B., and Wakefield, L. M. (2003) The two faces of transforming growth factor β in carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 8621-8623
7. Kalluri, R., and Weinberg, R. A. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428
8. Valcourt, U., Kowanetz, M., Niimi, H., Heldin, C. H., and Moustakas, A. (2005) TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol. Biol. Cell 16, 1987-2002
9. Derynck, R., and Zhang, Y. E. (2003) Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577-584
10. Wu, G., Chen, Y. G., Ozdamar, B., Gyuricza, C. A., Chong, P. A., Wrana, J. L., Massagué, J., and Shi, Y. (2000) Structural basis of Smad2 recognition by the Smad anchor for receptor activation. Science 287, 92-97
11. Maupin, K. A., Sinha, A., Eugster, E., Miller, J., Ross, J., Paulino, V., Keshamouni, V. G., Tran, N., Berens, M., Webb, C., and Haab, B. B. (2010) Glycogene expression alterations associated with pancreatic cancer epithelial-mesenchymal transition in complementary model systems. PLoS One 5, e13002
12. Tan, Z., Lu, W., Li, X., Yang, G., Guo, J., Yu, H., Li, Z., and Guan, F. (2014) Altered N-glycan expression profile in epithelial-to-mesenchymal transition of NMuMG cells revealed by an integrated strategy using mass spectrometry and glycogene and lectin microarray analysis. J. Proteome Res. 13, 2783-2795
13. Li, S., Mo, C., Peng, Q., Kang, X., Sun, C., Jiang, K., Huang, L., Lu, Y., Sui, J., Qin, X., and Liu, Y. (2013) Cell surface glycan alterations in epithelial mesenchymal transition process of Huh7 hepatocellular carcinoma cell. PLoS One 8, e71273
14. Swindall, A. F., and Bellis, S. L. (2011) Sialylation of the Fas death receptor by ST6Gal-I provides protection against Fas-mediated apoptosis in colon carcinoma cells. J. Biol. Chem. 286, 22982-22990
15. Liu, Z., Swindall, A. F., Kesterson, R. A., Schoeb, T. R., Bullard, D. C., and Bellis, S. L. (2011) ST6Gal-I regulates macrophage apoptosis via α2-6 sialylation of the TNFR1 death receptor. J. Biol. Chem. 286, 39654-39662
16. Crespo, H. J., Cabral, M. G., Teixeira, A. V., Lau, J. T., Trindade, H., and Videira, P. A. (2009) Effect of sialic acid loss on dendritic cell maturation. Immunology 128, e621-e631
17. Taniguchi, A., Higai, K., Hasegawa, Y., Utsumi, K., and Matsumoto, K. (1998) Differentiation elicits negative regulation of human β-galactoside α2,6-sialyltransferase at the mRNA level in the HL-60 cell line. FEBS Lett. 441, 191-194
18. Büll, C., Boltje, T. J., Wassink, M., de Graaf, A. M., van Delft, F. L., den Brok, M. H., and Adema, G. J. (2013) Targeting aberrant sialylation in cancer cells using a fluorinated sialic acid analog impairs adhesion, migration, and in vivo tumor growth. Mol. Cancer Ther. 12, 1935-1946
19. Seales, E. C., Jurado, G. A., Brunson, B. A., Wakefield, J. K., Frost, A. R., and Bellis, S. L. (2005) Hypersialylation of β1 integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer Res. 65, 4645-4652
20. Xu, Q., Isaji, T., Lu, Y., Gu, W., Kondo, M., Fukuda, T., Du, Y., and Gu, J. (2012) Roles of N-acetylglucosaminyltransferase III in epithelial-to-mesenchymal transition induced by transforming growth factor β1 (TGF-β1) in epithelial cell lines. J. Biol. Chem. 287, 16563-16574
21. Isaji, T., Im, S., Gu, W., Wang, Y., Hang, Q., Lu, J., Fukuda, T., Hashii, N., Takakura, D., Kawasaki, N., Miyoshi, H., and Gu, J. (2014) An oncogenic protein Golgi phosphoprotein 3 up-regulates cell migration via sialylation. J. Biol. Chem. 289, 20694-20705
22. Ranjan, A., and Kalraiya, R. D. (2013) α2,6 sialylation associated with increased β1,6-branched N-oligosaccharides influences cellular adhesion and invasion. J. Biosci. 38, 867-876
23. Jungert, K., Buck, A., von Wichert, G., Adler, G., König, A., Buchholz, M., Gress, T. M., and Ellenrieder, V. (2007) Sp1 is required for transforming growth factor-β-induced mesenchymal transition and migration in pancreatic cancer cells. Cancer Res. 67, 1563-1570
24. Zhao, Y., Li, Y., Ma, H., Dong, W., Zhou, H., Song, X., Zhang, J., and Jia, L. (2014) Modification of sialylation mediates the invasive properties and chemosensitivity of human hepatocellular carcinoma. Mol. Cell Proteomics 13, 520-536
25. Zheng, G., Lyons, J. G., Tan, T. K., Wang, Y., Hsu, T. T., Min, D., Succar, L., Rangan, G. K., Hu, M., Henderson, B. R., Alexander, S. I., and Harris, D. C. (2009) Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-β1 in renal tubular epithelial cells. Am. J. Pathol. 175, 580-591
26. Cha, S. K., Ortega, B., Kurosu, H., Rosenblatt, K. P., Kuro-O, M., and Huang, C. L. (2008) Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1. Proc. Natl. Acad. Sci. U.S.A. 105, 9805-9810
27. Kitazume, S., Imamaki, R., Ogawa, K., Komi, Y., Futakawa, S., Kojima, S., Hashimoto, Y., Marth, J. D., Paulson, J. C., and Taniguchi, N. (2010) α2,6-Sialic acid on platelet endothelial cell adhesion molecule (PECAM) regulates its homophilic interactions and downstream antiapoptotic signaling. J. Biol. Chem. 285, 6515-6521
28. Zhu, Y., Srivatana, U., Ullah, A., Gagneja, H., Berenson, C. S., and Lance, P. (2001) Suppression of a sialyltransferase by antisense DNA reduces invasiveness of human colon cancer cells in vitro. Biochim. Biophys. Acta 1536, 148-160
29. Lin, S., Kemmner, W., Grigull, S., and Schlag, P. M. (2002) Cell surface α2,6 sialylation affects adhesion of breast carcinoma cells. Exp. Cell Res. 276, 101-110
30. 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
31. de Oliveira, J. T., de Matos, A. J., Santos, A. L., Pinto, R., Gomes, J., Hespanhol, V., Chammas, R., Manninen, A., Bernardes, E. S., Albuquerque Reis, C., Rutteman, G., and Gärtner, F. (2011) Sialylation regulates galectin-3/ligand interplay during mammary tumour progression: a case of targeted uncloaking. Int. J. Dev. Biol. 55, 823-834
32. Zhuo, Y., Chammas, R., and Bellis, S. L. (2008) Sialylation of β1 integrins blocks cell adhesion to galectin-3 and protects cells against galectin-3-induced apoptosis. J. Biol. Chem. 283, 22177-22185
33. Zhuo, Y., and Bellis, S. L. (2011) Emerging role of α2,6-sialic acid as a negative regulator of galectin binding and function. J. Biol. Chem. 286, 5935-5941
34. Lee, M., Lee, H. J., Bae, S., and Lee, Y. S. (2008) Protein sialylation by sialyltransferase involves radiation resistance. Mol Cancer Res. 6, 1316-1325
35. Ma, H., Zhou, H., Song, X., Shi, S., Zhang, J., and Jia, L. (2014) Modification of sialylation is associated with multidrug resistance in human acute myeloid leukemia. Oncogene 10.1038/onc.2014.7
36. Bae, G. Y., Choi, S. J., Lee, J. S., Jo, J., Lee, J., Kim, J., and Cha, H. J. (2013) Loss of E-cadherin activates EGFR-MEK/ERK signaling, which promotes invasion via the ZEB1/MMP2 axis in non-small cell lung cancer. Oncotarget 4, 2512-2522
37. Bakin, A. V., Tomlinson, A. K., Bhowmick, N. A., Moses, H. L., and Arteaga, C. L. (2000) Phosphatidylinositol 3-kinase function is required for transforming growth factor β-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem. 275, 36803-36810
38. Kattla, J. J., Carew, R. M., Heljic, M., Godson, C., and Brazil, D. P. (2008) Protein kinase B/Akt activity is involved in renal TGF-β1-driven epithelial-mesenchymal transition in vitro and in vivo. Am. J. Physiol. Renal Physiol 295, F215-F225
39. Christie, D. R., Shaikh, F. M., Lucas, J. A., 4th, Lucas, J. A., 3rd, and Bellis, S. L. (2008) ST6Gal-I expression in ovarian cancer cells promotes an invasive phenotype by altering integrin glycosylation and function. J. Ovarian Res. 1, 3
40. Shaikh, F. M., Seales, E. C., Clem, W. C., Hennessy, K. M., Zhuo, Y., and Bellis, S. L. (2008) Tumor cell migration and invasion are regulated by expression of variant integrin glycoforms. Exp. Cell Res. 314, 2941-2950
41. Chen, Q., Manning, C. D., Millar, H., McCabe, F. L., Ferrante, C., Sharp, C., Shahied-Arruda, L., Doshi, P., Nakada, M. T., and Anderson, G. M. (2008) CNTO 95, a fully human anti αv integrin antibody, inhibits cell signaling, migration, invasion, and spontaneous metastasis of human breast cancer cells. Clin. Exp. Metastasis 25, 139-148
42. Thomas, G. J., Lewis, M. P., Hart, I. R., Marshall, J. F., and Speight, P. M. (2001) αVβ6 integrin promotes invasion of squamous carcinoma cells through up-regulation of matrix metalloproteinase-9. Int. J. Cancer 92, 641-650
43. Thomas, G. J., Lewis, M. P., Whawell, S. A., Russell, A., Sheppard, D., Hart, I. R., Speight, P. M., and Marshall, J. F. (2001) Expression of the alphavbeta6 integrin promotes migration and invasion in squamous carcinoma cells. J. Invest. Dermatol. 117, 67-73
44. Sloan, E. K., Pouliot, N., Stanley, K. L., Chia, J., Moseley, J. M., Hards, D. K., and Anderson, R. L. (2006) Tumor-specific expression of αvβ3 integrin promotes spontaneous metastasis of breast cancer to bone. Breast Cancer Res. 8, R20
45. Mamuya, F. A., and Duncan, M. K. (2012) aV integrins and TGF-β-induced EMT: a circle of regulation. J. Cell Mol. Med. 16, 445-455
46. Hinek, A., Bodnaruk, T. D., Bunda, S., Wang, Y., and Liu, K. (2008) Neuraminidase-1, a subunit of the cell surface elastin receptor, desialylates and functionally inactivates adjacent receptors interacting with the mitogenic growth factors PDGF-BB and IGF-2. Am. J. Pathol. 173, 1042-1056
47. Lillehoj, E. P., Hyun, S. W., Feng, C., Zhang, L., Liu, A., Guang, W., Nguyen, C., Luzina, I. G., Atamas, S. P., Passaniti, A., Twaddell, W. S., Puché, A. C., Wang, L. X., Cross, A. S., and Goldblum, S. E. (2012) NEU1 sialidase expressed in human airway epithelia regulates epidermal growth factor receptor (EGFR) and MUC1 protein signaling. J. Biol. Chem. 287, 8214-8231
48. Shen, L., Qu, X., Ma, Y., Zheng, J., Chu, D., Liu, B., Li, X., Wang, M., Xu, C., Liu, N., Yao, L., and Zhang, J. (2014) Tumor suppressor NDRG2 tips the balance of oncogenic TGF-β via EMT inhibition in colorectal cancer. Oncogenesis 3, e86
49. Taniguchi, A., Hasegawa, Y., Higai, K., and Matsumoto, K. (2000) Transcriptional regulation of human β-galactoside α2, 6-sialyltransferase (hST6Gal I) gene during differentiation of the HL-60 cell line. Glycobiology 10, 623-628
50. Gu, J., Nishikawa, A., Tsuruoka, N., Ohno, M., Yamaguchi, N., Kangawa, K., and Taniguchi, N. (1993) Purification and characterization of UDP-N-acetylglucosamine: α-6-D-mannoside β 1-6N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113, 614-619
51. Schachter, H. (1986) Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Adv. Exp. Med. Biol. 205, 53-85
52. Schachter, H., Narasimhan, S., Gleeson, P., and Vella, G. (1983) Control of branching during the biosynthesis of asparagine-linked oligosaccharides. Can. J. Biochem. Cell Biol. 61, 1049-1066
53. Pinho, S. S., Osório, H., Nita-Lazar, M., Gomes, J., Lopes, C., Gärtner, F., and Reis, C. A. (2009) Role of E-cadherin N-glycosylation profile in a mammary tumor model. Biochem. Biophys. Res. Commun. 379, 1091-1096
54. Saldova, R., Piccard, H., Pérez-Garay, M., Harvey, D. J., Struwe, W. B., Galligan, M. C., Berghmans, N., Madden, S. F., Peracaula, R., Opdenakker, G., and Rudd, P. M. (2013) Increase in sialylation and branching in the mouse serum N-glycome correlates with inflammation and ovarian tumour progression. PLoS One 8, e71159
55. Granovsky, M., Fata, J., Pawling, J., Muller, W. J., Khokha, R., and Dennis, J. W. (2000) Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat. Med. 6, 306-312
56. Zhang, Z., Sun, J., Hao, L., Liu, C., Ma, H., and Jia, L. (2013) Modification of glycosylation mediates the invasive properties of murine hepatocarcinoma cell lines to lymph nodes. PLoS One 8, e65218
57. Woodard-Grice, A. V., McBrayer, A. C., Wakefield, J. K., Zhuo, Y., and Bellis, S. L. (2008) Proteolytic shedding of ST6Gal-I by BACE1 regulates the glycosylation and function of α4β1 integrins. J. Biol. Chem. 283, 26364-26373
58. Amano, M., Galvan, M., He, J., and Baum, L. G. (2003) The ST6Gal I sialyltransferase selectively modifies N-glycans on CD45 to negatively regulate galectin-1-induced CD45 clustering, phosphatase modulation, and T cell death. J. Biol. Chem. 278, 7469-7475
59. Liu, Y. C., Yen, H. Y., Chen, C. Y., Chen, C. H., Cheng, P. F., Juan, Y. H., Chen, C. H., Khoo, K. H., Yu, C. J., Yang, P. C., Hsu, T. L., and Wong, C. H. (2011) Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc. Natl. Acad. Sci. U.S.A. 108, 11332-11337
60. Meng, L., Forouhar, F., Thieker, D., Gao, Z., Ramiah, A., Moniz, H., Xiang, Y., Seetharaman, J., Milaninia, S., Su, M., Bridger, R., Veillon, L., Azadi, P., Kornhaber, G., Wells, L., Montelione, G. T., Woods, R. J., Tong, L., and Moremen, K. W. (2013) Enzymatic basis for N-glycan sialylation: structure of rat α2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation. J. Biol. Chem. 288, 34680-34698
61. Swindall, A. F., Londoño-Joshi, A. I., Schultz, M. J., Fineberg, N., Buchsbaum, D. J., and Bellis, S. L. (2013) ST6Gal-I protein expression is upregulated in human epithelial tumors and correlates with stem cell markers in normal tissues and colon cancer cell lines. Cancer Res. 73, 2368-2378
62. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715