Advertisement

Glycoconjugate Journal

, Volume 29, Issue 7, pp 525–537 | Cite as

Glycosylation potential of human prostate cancer cell lines

  • Yin Gao
  • Vishwanath B. Chachadi
  • Pi-Wan Cheng
  • Inka BrockhausenEmail author
Article

Abstract

Altered glycosylation is a universal feature of cancer cells and altered glycans can help cancer cells escape immune surveillance, facilitate tumor invasion, and increase malignancy. The goal of this study was to identify specific glycoenzymes, which could distinguish prostate cancer cells from normal prostatic cells. We investigated enzymatic activities and gene expression levels of key glycosyl- and sulfotransferases responsible for the assembly of O- and N-glycans in several prostatic cells. These cells included immortalized RWPE-1 cells derived from normal prostatic tissues, and prostate cancer cells derived from metastasis in bone (PC-3), brain (DU145), lymph node (LNCaP), and vertebra (VCaP). We found that all cells were capable of synthesizing complex N-glycans and O-glycans with the core 1 structure, and each cell line had characteristic biosynthetic pathways to modify these structures. The in vitro measured activities corresponded well to the mRNA levels of glycosyltransferases and sulfotransferases. Lectin and antibody binding to whole cells supported these results, which form the basis for the development of tumor cell-specific targeting strategies.

Keywords

Glycosyltransferase activities N-glycosylation O-glycosylation Real-time PCR Prostate cancer cells 

Abbreviations

FUT

fucosyltransferase

Gal3ST

3-O-sulfotransferase

GalT

galactosyltransferase

GalNAcT

GalNAc-transferase

GAPDH

Glyceraldehyde 3-phosphate dehydrogenase

GnT GlcNAcT

GlcNAc-transferase

GlcNAc6ST

N-acetylglucosaminyl-6-O-sulfotransferase

HPLC

high pressure liquid chromatography

PCR

polymerase chain reaction

ppGalNAcT

polypeptide GalNAc-transferase

PSA

prostate specific antigen

SLex

sialyl-Lewisx

ST3Gal

α2,3-sialyltransferase

ST6Gal(NAc)

α2,6-sialyltransferase

Notes

Acknowledgements

This work was supported by a grant from the Prostate Cancer Fight Foundation, Motorcycle Ride for Dad (to I.B.), and grants from the Office of Research and Development, Medical Research Service, Department of Veterans Affairs (VA 1I1BX000985), the National Institutes of Health (1R21HL097238 and 2RO1HL48282) and the State of Nebraska (LB506)(to P.W.C.).

Supplementary material

10719_2012_9428_MOESM1_ESM.pdf (224 kb)
Supplementary Figure 1 Lectin staining of whole prostatic cells. Lectin binding was carried out as described in the Methods section using Ricin (Ricin A chain lectin), WGA (wheat germ agglutinin), MAAII (Maackia amurensis lectin II), SNA (Sambucus nigra lectin), GSL-1 (Griffonia simplicifolia lectin 1), UEA-1 (Ulex eauropaeus lectin 1), PNA (Peanut agglutinin), HP, (Helix pomatia lectin), ConA (Concanavalin A), BSL-1 (Bandeiraea simplicifolia lectin 1), DSL ( Datura stramonium lectin). The intensity of absorbance at 405 nm was recorded, normalized to the same cell number of 100,000 cells (Intensity). a, Normal prostatic RWPE-1 cells; b, Prostate cancer cells PC-3; c, DU145 cells; d, LNCaP cells; e, VCaP cells. The error bars show the variations among the 7 samples tested. (PDF 223 kb)
10719_2012_9428_MOESM2_ESM.pdf (100 kb)
Supplementary Figure 2 ELISA of whole prostatic cells. Prostatic cells were stained as described in the Materials and Methods section using anti-Tn antibody (Tn) anti-sialyl-Tn (STn), anti-sialyl-Lewisx (SLe x), anti- Lewis y (Le y) and anti-Lewis a (Le a) antibodies. The intensity of staining measured at 405 nm , normalized to the same cell number is shown. a, Normal prostatic RWPE-1 cells; b, Prostate cancer cells PC-3; c, DU145 cells; d, LNCaP cells; e, VCaP cells. (PDF 100 kb)
10719_2012_9428_MOESM3_ESM.pdf (182 kb)
Supplementary Figure 3 Quantitative real time PCR analysis of various glycosyltransferase and sulfotransferase genes in normal and cancerous prostatic cells. The expression levels of glycosyltransferase and sulfotransferase genes are shown. The gene expression levels were calculated by the ΔCt method as described in Materials and Methods and expressed Supplemental Material (Not to be Published) as relative amount to that of GAPDH (100%). The enzyme names are listed in Table 1. Results are shown for B3GNT2 - 5 (Extension β3GlcNAcT), ST3GAL3 - 6 (α2,3-sialyltransferases), GAL3ST1 and 3 (galactosyl-3-O-sulfotransferases); ST6GALNAC1 - 4 (α2,6-sialyltransferases acting on GalNAc) and ST6GAL1 (α2,6-sialyltransferase acting on Gal). The data were obtained from three independent experiments and expressed as mean ± SEM. (PDF 181 kb)
10719_2012_9428_MOESM4_ESM.pdf (38 kb)
ESM 1 (PDF 37 kb)

References

  1. 1.
    Bresalier, R.S., Ho, S.B., Schoeppner, H.L., Kim, Y.S., Sleisenger, M.H., Brodt, P., Byrd, J.C.: Enhanced sialylation of mucin-associated carbohydrate structures in human colon cancer metastasis. Gastroenterology 110, 1354–1367 (1996)PubMedCrossRefGoogle Scholar
  2. 2.
    Burke, P.A., Gregg, J.P., Bakhtiar, B., Beckett, L.A., Denardo, G.L., Albrecht, H., De Vere White, R.W., De Nardo, S.J.: Characterization of MUC1 glycoprotein on prostate cancer for selection of targeting molecules. Int. J. Oncol. 29, 49–55 (2006)PubMedGoogle Scholar
  3. 3.
    Garbar, C., Mascaux, C., Wespes, E.: Expression of MUC1 and sialyl-Tn in benign prostatic glands, high-grade prostate intraepithelial neoplasia and malignant prostatic glands: a preliminary study. Anal. Quant. Cytol. Histol. 30, 71–77 (2008)PubMedGoogle Scholar
  4. 4.
    Tabarés, G., Radcliffe, C.M., Barrabés, S., Ramírez, M., Aleixandre, R.N., Hoesel, W., Dwek, R.A., Rudd, P.M., Peracaula, R., de Llorens, R.: Different glycan structures in prostate-specific antigen from prostate cancer sera in relation to seminal plasma PSA. Glycobiology 16, 132–145 (2006)PubMedCrossRefGoogle Scholar
  5. 5.
    Barthel, S.R., Gavino, J.D., Wiese, G.K., Jaynes, J.M., Siddiqui, J., Dimitroff, C.J.: Analysis of glycosyltransferase expression in metastatic prostate cancer cells capable of rolling activity on microvascular endothelial (E)-selectin. Glycobiology 18, 806–817 (2008)PubMedCrossRefGoogle Scholar
  6. 6.
    Barthel, S.R., Wiese, G.K., Cho, J., Opperman, M.J., Hays, D.L., Siddiqui, J., Pienta, K.J., Furie, B., Dimitroff, C.J.: Alpha 1,3 fucosyltransferases are master regulators of prostate cancer cell trafficking. Proc. Natl. Acad. Sci. U. S. A. 106, 19491–19496 (2009)PubMedCrossRefGoogle Scholar
  7. 7.
    Brockhausen, I.: Mucin-type O-glycans in human colon and breast cancer: glycodynamics and functions. EMBO Rep. 7, 599–604 (2006)PubMedCrossRefGoogle Scholar
  8. 8.
    Carraway, K.L., Fregien, N., Carraway, C.A.: Tumor sialomucin complexes as tumor antigens and modulators of cellular interactions and proliferation. J. Cell Sci. 103(Pt 2), 299–307 (1992)PubMedGoogle Scholar
  9. 9.
    David, L., Nesland, J.M., Clausen, H., Carneiro, F., Sobrinho-Simões, M.: Simple mucin-type carbohydrate antigens (Tn, sialosyl-Tn and T) in gastric mucosa, carcinomas and metastases. APMIS Suppl. 27, 162–172 (1992)PubMedGoogle Scholar
  10. 10.
    Hoff, S.D., Matsushita, Y., Ota, D.M., Cleary, K.R., Yamori, T., Hakomori, S., Irimura, T.: Increased expression of sialyl-dimeric LeX antigen in liver metastases of human colorectal carcinoma. Cancer Res. 49, 6883–6888 (1989)PubMedGoogle Scholar
  11. 11.
    Kojima, N., Handa, K., Newman, W., Hakomori, S.: Inhibition of selectin-dependent tumor cell adhesion to endothelial cells and platelets by blocking O-glycosylation of these cells. Biochem. Biophys. Res. Commun. 182, 1288–1295 (1992)PubMedCrossRefGoogle Scholar
  12. 12.
    Radhakrishnan, P., Lin, M.F., Cheng, P.W.: Elevated expression of L-selectin ligand in lymph node-derived human prostate cancer cells correlates with increased tumorigenicity. Glycoconj. J. 26, 75–81 (2009)PubMedCrossRefGoogle Scholar
  13. 13.
    Takano, R., Muchmore, E., Dennis, J.W.: Sialylation and malignant potential in tumour cell glycosylation mutants. Glycobiology 4, 665–674 (1994)PubMedCrossRefGoogle Scholar
  14. 14.
    Itzkowitz, S.H., Bloom, E.J., Kokal, W.A., Modin, G., Hakomori, S., Kim, Y.S.: Sialosyl-Tn. A novel mucin antigen associated with prognosis in colorectal cancer patients. Cancer 66, 1960–1966 (1990)PubMedCrossRefGoogle Scholar
  15. 15.
    Janković, M.M., Kosanović, M.M.: Glycosylation of urinary prostate-specific antigen in benign hyperplasia and cancer: assessment by lectin-binding patterns. Clin. Biochem. 38, 58–65 (2005)PubMedCrossRefGoogle Scholar
  16. 16.
    Peracaula, R., Tabarés, G., Royle, L., Harvey, D.J., Dwek, R.A., Rudd, P.M., de Llorens, R.: Altered glycosylation pattern allows the distinction between prostate-specific antigen (PSA) from normal and tumor origins. Glycobiology 13, 457–470 (2003)PubMedCrossRefGoogle Scholar
  17. 17.
    Cozzi, P.J., Wang, J., Delprado, W., Perkins, A.C., Allen, B.J., Russell, P.J., Li, Y.: MUC1, MUC2, MUC4, MUC5AC and MUC6 expression in the progression of prostate cancer. Clin. Exp. Metastasis 22, 565–573 (2005)PubMedCrossRefGoogle Scholar
  18. 18.
    Singh, A.P., Chauhan, S.C., Bafna, S., Johansson, S.L., Smith, L.M., Moniaux, N., Lin, M.F., Batra, S.K.: Aberrant expression of transmembrane mucins, MUC1 and MUC4, in human prostate carcinomas. Prostate 66, 421–429 (2006)PubMedCrossRefGoogle Scholar
  19. 19.
    Wu, G.J., Peng, Q., Fu, P., Wang, S.W., Chiang, C.F., Dillehay, D.L., Wu, M.W.: Ectopical expression of human MUC18 increases metastasis of human prostate cancer cells. Gene 327, 201–213 (2004)PubMedCrossRefGoogle Scholar
  20. 20.
    Bélanger, A., van Halbeek, H., Graves, H.C., Grandbois, K., Stamey, T.A., Huang, L., Poppe, I., Labrie, F.: Molecular mass and carbohydrate structure of prostate specific antigen: studies for establishment of an international PSA standard. Prostate 27, 187–197 (1995)PubMedCrossRefGoogle Scholar
  21. 21.
    Meany, D.L., Zhang, Z., Sokoll, L.J., Zhang, H., Chan, D.W.: Glycoproteomics for prostate cancer detection: changes in serum PSA glycosylation patterns. J. Proteome Res. 8, 613–619 (2009)PubMedCrossRefGoogle Scholar
  22. 22.
    Ohyama, C., Hosono, M., Nitta, K., Oh-eda, M., Yoshikawa, K., Habuchi, T., Arai, Y., Fukuda, M.: Carbohydrate structure and differential binding of prostate specific antigen to Maackia amurensis lectin between prostate cancer and benign prostate hypertrophy. Glycobiology 14, 671–679 (2004)PubMedCrossRefGoogle Scholar
  23. 23.
    St Hill, C.A., Farooqui, M., Mitcheltree, G., Gulbahce, H.E., Jessurun, J., Cao, Q., Walcheck, B.: The high affinity selectin glycan ligand C2-O-SLex and mRNA transcripts of the core 2 beta-1,6-N-acetylglucosaminyltransferase (C2GnT1) gene are highly expressed in human colorectal adenocarcinomas. BMC Cancer 9, 79 (2009)PubMedCrossRefGoogle Scholar
  24. 24.
    Shimodaira, K., Nakayama, J., Nakamura, N., Hasebe, O., Katsuyama, T., Fukuda, M.: Carcinoma-associated expression of core 2 beta-1,6-N-acetylglucosaminyltransferase gene in human colorectal cancer: role of O-glycans in tumor progression. Cancer Res. 57, 5201–5206 (1997)PubMedGoogle Scholar
  25. 25.
    Hanski, C., Klussmann, E., Wang, J., Böhm, C., Ogorek, D., Hanski, M.L., Krüger-Krasagakes, S., Eberle, J., Schmitt-Gräff, A., Riecken, E.O.: Fucosyltransferase III and sialyl-Le(x) expression correlate in cultured colon carcinoma cells but not in colon carcinoma tissue. Glycoconj. J. 13, 727–733 (1996)PubMedCrossRefGoogle Scholar
  26. 26.
    Ito, H., Hiraiwa, N., Sawada-Kasugai, M., Akamatsu, S., Tachikawa, T., Kasai, Y., Akiyama, S., Ito, K., Takagi, H., Kannagi, R.: Altered mRNA expression of specific molecular species of fucosyl- and sialyl-transferases in human colorectal cancer tissues. Int. J. Cancer 71, 556–564 (1997)PubMedCrossRefGoogle Scholar
  27. 27.
    Nakamori, S., Kameyama, M., Imaoka, S., Furukawa, H., Ishikawa, O., Sasaki, Y., Kabuto, T., Iwanaga, T., Matsushita, Y., Irimura, T.: Increased expression of sialyl Lewisx antigen correlates with poor survival in patients with colorectal carcinoma: clinicopathological and immunohistochemical study. Cancer Res. 53, 3632–3637 (1993)PubMedGoogle Scholar
  28. 28.
    Machida, E., Nakayama, J., Amano, J., Fukuda, M.: Clinicopathological significance of core 2 beta1,6-N-acetylglucosaminyltransferase messenger RNA expressed in the pulmonary adenocarcinoma determined by in situ hybridization. Cancer Res. 61, 2226–2231 (2001)PubMedGoogle Scholar
  29. 29.
    Hagisawa, S., Ohyama, C., Takahashi, T., Endoh, M., Moriya, T., Nakayama, J., Arai, Y., Fukuda, M.: Expression of core 2 beta1,6-N-acetylglucosaminyltransferase facilitates prostate cancer progression. Glycobiology 15, 1016–1024 (2005)PubMedCrossRefGoogle Scholar
  30. 30.
    Valenzuela, H.F., Pace, K.E., Cabrera, P.V., White, R., Porvari, K., Kaija, H., Vihko, P., Baum, L.G.: O-glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1. Cancer Res. 67, 6155–6162 (2007)PubMedCrossRefGoogle Scholar
  31. 31.
    Brockhausen, I.: Pathways of O-glycan biosynthesis in cancer cells. Biochim. Biophys. Acta 1473, 67–95 (1999)PubMedCrossRefGoogle Scholar
  32. 32.
    Brockhausen, I.: Comprehensive Natural Products II Chemistry and Biology. In: Mander, L., Lui, H.-W., Wang, P.G. (eds.) Biosynthesis of complex mucin-type O-glycans. Carbohydrates, nucleosides and nucleic acids, vol. 6, pp. 315–350. Elsevier, Oxford (2010). Chapter 11Google Scholar
  33. 33.
    Burchell, J., Poulsom, R., Hanby, A., Whitehouse, C., Cooper, L., Clausen, H., Miles, D., Taylor-Papadimitriou, J.: An alpha2,3 sialyltransferase (ST3Gal I) is elevated in primary breast carcinomas. Glycobiology 9, 1307–1311 (1999)PubMedCrossRefGoogle Scholar
  34. 34.
    Petretti, T., Kemmner, W., Schulze, B., Schlag, P.M.: Altered mRNA expression of glycosyltransferases in human colorectal carcinomas and liver metastases. Gut 46, 359–366 (2000)PubMedCrossRefGoogle Scholar
  35. 35.
    Seko, A., Ohkura, T., Kitamura, H., Yonezawa, S., Sato, E., Yamashita, K.: Quantitative differences in GlcNAc:beta1– > 3 and GlcNAc:beta1– > 4 galactosyltransferase activities between human colonic adenocarcinomas and normal colonic mucosa. Cancer Res. 56, 3468–3473 (1996)PubMedGoogle Scholar
  36. 36.
    Yang, J.M., Byrd, J.C., Siddiki, B.B., Chung, Y.S., Okuno, M., Sowa, M., Kim, Y.S., Matta, K.L., Brockhausen, I.: Alterations of O-glycan biosynthesis in human colon cancer tissues. Glycobiology 4, 873–884 (1994)PubMedCrossRefGoogle Scholar
  37. 37.
    Vavasseur, F., Dole, K., Yang, J., Matta, K.L., Myerscough, N., Corfield, A., Paraskeva, C., Brockhausen, I.: O-glycan biosynthesis in human colorectal adenoma cells during progression to cancer. Eur. J. Biochem. 222, 415–424 (1994)PubMedCrossRefGoogle Scholar
  38. 38.
    Vavasseur, F., Yang, J.M., Dole, K., Paulsen, H., Brockhausen, I.: Synthesis of O-glycan core 3: characterization of UDP-GlcNAc: GalNAc-R beta 3-N-acetyl-glucosaminyltransferase activity from colonic mucosal tissues and lack of the activity in human cancer cell lines. Glycobiology 5, 351–357 (1995)PubMedCrossRefGoogle Scholar
  39. 39.
    Brockhausen, I., Romero, P., Herscovics, A.: Glycosyltransferase changes upon differentiation of CaCo-2 human colonic adenocarcinoma Cells. Cancer Res. 51, 3136–3142 (1991)PubMedGoogle Scholar
  40. 40.
    Brockhausen, I., Benn, M., Bhat, S., Marone, S., Riley, J.G., Montoya-Peleaz, P., Vlahakis, J.Z., Paulsen, H., Schutzbach, J.S., Szarek, W.A.: UDP-Gal: GlcNAc-R beta1,4-galactosyltransferase–a target enzyme for drug design. Acceptor specificity and inhibition of the enzyme. Glycoconj. J. 23, 525–541 (2006)PubMedCrossRefGoogle Scholar
  41. 41.
    Brockhausen, I., Reck, F., Kuhns, W., Khan, S., Matta, K.L., Meinjohanns, E., Paulsen, H., Shah, R.N., Baker, M.A., Schachter, H.: Substrate specificity and inhibition of UDP-GlcNAc:GlcNAc beta 1-2Man alpha 1-6R beta 1,6-N-acetylglucosaminyltransferase V using synthetic substrate analogues. Glycoconj. J. 12, 371–379 (1995)PubMedCrossRefGoogle Scholar
  42. 42.
    Brockhausen, I., Dowler, T., Paulsen, H.: Site directed processing: role of amino acid sequences and glycosylation of acceptor glycopeptides in the assembly of extended mucin type O-glycan core 2. Biochim. Biophys. Acta 1790, 1244–1257 (2009)PubMedCrossRefGoogle Scholar
  43. 43.
    Tassone, F., Hagerman, R.J., Taylor, A.K., Gane, L.W., Godfrey, T.E., Hagerman, P.J.: Elevated levels of FMR1 mRNA in carrier males: a new mechanism of involvement in the fragile-X syndrome. Am. J. Hum. Genet. 66, 6–15 (2000)PubMedCrossRefGoogle Scholar
  44. 44.
    Yang, X., Yip, J., Harrison, M., Brockhausen, I.: Primary human osteoblasts and bone cancer cells as models to study glycodynamics in bone. Int. J. Biochem. Cell Biol. 40, 471–483 (2008)PubMedCrossRefGoogle Scholar
  45. 45.
    Brown, J.R., Fuster, M.M., Li, R., Varki, N., Glass, C.A., Esko, J.D.: A disaccharide-based inhibitor of glycosylation attenuates metastatic tumor cell dissemination. Clin. Cancer Res. 12, 2894–2901 (2006)PubMedCrossRefGoogle Scholar
  46. 46.
    Brockhausen, I., Williams, D., Matta, K.L., Orr, J., Schachter, H.: Mucin Synthesis III: UDP-GlcNAc:Galβ1-3(GlcNAcβ1-6)GalNAc-R (GlcNAc to Gal) β3-N-acetylglucosaminyltransferase, an enzyme in porcine gastric mucosa involved in the elongation of mucin-type oligosaccharides. Can. J. Biochem. Cell Biol. 61, 1322–1333 (1983)PubMedCrossRefGoogle Scholar
  47. 47.
    Gao, Y., Lazar, C., Szarek, W.A., Brockhausen, I.: Specificity of β4galactosyltransferase inhibitor 2-naphthyl 2-butanamido-2-deoxy-1-thio-β-D-glucopyranoside. Glycoconj. J. 27, 673–684 (2010)PubMedCrossRefGoogle Scholar
  48. 48.
    Huang, J., Liang, J.T., Huang, H.C., Shen, T.L., Chen, H.Y., Lin, N.Y., Che, M.I., Lin, W.C., Huang, M.C.: Beta1,4-N-acetylgalactosaminyltransferase III enhances malignant phenotypes of colon cancer cells. Mol. Cancer Res. 5, 543–552 (2007)PubMedCrossRefGoogle Scholar
  49. 49.
    Yao, M., Zhou, D.P., Jiang, S.M., Wang, Q.H., Zhou, X.D., Tang, Z.Y., Gu, J.X.: Elevated activity of N-acetylglucosaminyltransferase V in human hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 124, 27–30 (1998)PubMedCrossRefGoogle Scholar
  50. 50.
    Tsui, K.H., Chang, P.L., Feng, T.H., Chung, L.C., Sung, H.C., Juang, H.H.: Evaluating the function of matriptase and N-acetylglucosaminyltransferase V in prostate cancer metastasis. Anticancer. Res. 28, 1993–1999 (2008)PubMedGoogle Scholar
  51. 51.
    Premaratne, P., Wélen, K., Damber, J.-E., Hansson, G., Bäckström, M.: O-glycosylation of MUC1 mucin in prostate cancer and the effects of its expression on tumor growth in a prostate cancer xenograft model. Tumor Biol. 32, 203–213 (2011)CrossRefGoogle Scholar
  52. 52.
    Pinho, S., Marcos, N.T., Ferreira, B., Carvalho, A.S., Oliveira, M.J., Santos-Silva, F., Harduin-Lepers, A., Reis, C.A.: Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett. 249, 157–170 (2007)PubMedCrossRefGoogle Scholar
  53. 53.
    Lise, M., Belluco, C., Perera, S.P., Patel, R., Thomas, P., Ganguly, A.: Clinical correlations of alpha2,6-sialyltransferase expression in colorectal cancer patients. Hybridoma 19, 281–286 (2000)PubMedCrossRefGoogle Scholar
  54. 54.
    Dalziel, M., Whitehouse, C., McFarlane, I., Brockhausen, I., Gschmeissner, S., Schwientek, T., Clausen, H., Burchell, J.M., Taylor-Papadimitriou, J.: The relative activities of the C2GnT1 and ST3Gal-I glycosyltransferases determine O-glycan structure and expression of a tumor-associated epitope on MUC1. J. Biol. Chem. 276, 11007–11015 (2001)PubMedCrossRefGoogle Scholar
  55. 55.
    Hatakeyama, S., Kyan, A., Yamamoto, H., Okamoto, A., Sugiyama, N., Suzuki, Y., Yoneyama, T., Hashimoto, Y., Koie, T., Yamada, S., Saito, H., Arai, Y., Fukuda, M., Ohyama, C.: Core 2 N-acetylglucosaminyltransferase-1 expression induces aggressive potential of testicular germ cell tumor. Int. J. Cancer 127, 1052–1059 (2010)PubMedCrossRefGoogle Scholar
  56. 56.
    Iwai, T., Kudo, T., Kawamoto, R., Kubota, T., Togayachi, A., Hiruma, T., Okada, T., Kawamoto, T., Morozumi, K., Narimatsu, H.: Core 3 synthase is down-regulated in colon carcinoma and profoundly suppresses the metastatic potential of carcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 102, 4572–4577 (2005)PubMedCrossRefGoogle Scholar
  57. 57.
    Lee, S.H., Hatakeyama, S., Yu, S.Y., Bao, X., Ohyama, C., Khoo, K.H., Fukuda, M.N., Fukuda, M.: Core 3 O-glycan synthase suppresses tumor formation and metastasis of prostate carcinoma PC3 and LNCaP cells through down-regulation of alpha2beta1 integrin complex. J. Biol. Chem. 284, 17157–17169 (2009)PubMedCrossRefGoogle Scholar
  58. 58.
    An, G., Wei, B., Xia, B., McDaniel, J.M., Ju, T., Cummings, R.D., Braun, J., Xia, L.: Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp. Med. 240, 1417–1429 (2007)CrossRefGoogle Scholar
  59. 59.
    Brockhausen, I., Yang, J.M., Burchell, J., Whitehouse, C., Taylor-Papadimitriou, J.: Mechanisms underlying aberrant glycosylation of MUC1 mucin in breast cancer cells. Eur. J. Biochem. 233, 607–617 (1995)PubMedCrossRefGoogle Scholar
  60. 60.
    Cazet, A., Julien, S., Bobowski, M., Krzewinski-Recchi, M.A., Harduin-Lepers, A., Groux-Degroote, S., Delannoy, P.: Consequences of the expression of sialylated antigens in breast cancer. Carbohydr. Res. 345, 1377–1383 (2010)PubMedCrossRefGoogle Scholar
  61. 61.
    Mungul, A., Cooper, L., Brockhausen, I., Ryder, K., Mandel, U., Clausen, H., Rughetti, A., Miles, D.W., Taylor-Papadimitriou, J., Burchell, J.M.: Sialylated core 1 based O-linked glycans enhance the growth rate of mammary carcinoma cells in MUC1 transgenic mice. Int. J. Oncol. 25, 937–943 (2004)PubMedGoogle Scholar
  62. 62.
    Picco, G., Julien, S., Brockhausen, I., Beatson, R., Antonopoulos, A., Haslam, S., Mandel, U., Dell, A., Pinder, S., Taylor-Papadimitriou, J., Burchell, J.: Over-expression of ST3Gal-I promotes mammary tumorigenesis. Glycobiology 20, 1241–1250 (2010)PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Yin Gao
    • 1
  • Vishwanath B. Chachadi
    • 2
    • 3
  • Pi-Wan Cheng
    • 2
    • 3
  • Inka Brockhausen
    • 1
    Email author
  1. 1.Department of Medicine, Division of Rheumatology, and Department of Biomedical and Molecular SciencesQueen’s UniversityKingstonCanada
  2. 2.VA Nebraska-Western Iowa Health Care System, Research ServiceOmahaUSA
  3. 3.Department of Biochemistry and Molecular Biology, College of MedicineUniversity of Nebraska Medical CenterOmahaUSA

Personalised recommendations