Skip to main content
SpringerLink
Log in

Glycosaminoglycan secretion in xyloside treated polarized human colon carcinoma Caco-2 cells

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Polarized epithelial cells like Madin-Darby canine kidney (MDCK) and CaCo-2 cells synthesize and secrete proteoglycans (PGs), mostly of heparan sulphate (HS) type in direction of the basal extracellular matrix, but also some in the apical direction. MDCK cells possess the capacity to synthesize chondroitin sulphate (CS) PGs that are mainly secreted into the apical medium, a process that is enhanced in the presence of hexyl-β-d-xyloside. We have now tested the capacity of several xylosides to enhance glycosaminoglycan (GAG) chain secretion from the human colon carcinoma cell line CaCo-2 in the differentiated and non-differentiated state. In these cells, benzyl-β-d-xyloside was a potent initiator of CS chains, which for these cells were predominantly secreted into the basolateral medium. Xylosides with other aglycone groups mediated only minor changes in GAG secretion. Although benzyl-β-d-xyloside stimulated the basolateral CS-GAG secretion in both differentiated and undifferentiated CaCo-2 cells, basolateral secretion of trypsin-like activity was dramatically enhanced in undifferentiated cells, but not significantly altered in differentiated cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Cheng, F., Johnsson, R., Nilsson, J., Fransson, L.A., Ellervik, U., Mani, K.: Potentiation of naphthoxyloside cytotoxicity on human tumor cells by difluoromethylornithine and spermine-NONOate. Cancer Lett. 273, 148–154 (2009). doi:10.1016/j.canlet.2008.07.036

    Article  CAS  PubMed  Google Scholar 

  2. Dick, G., Grondahl, F., Prydz, K.: Overexpression of the 3’¢-phosphoadenosine 5’¢-phosphosulfate (PAPS) transporter 1 increases sulfation of chondroitin sulfate in the apical pathway of MDCK II cells. Glycobiology 18, 53–65 (2008). doi:10.1093/glycob/cwm121

    Article  CAS  PubMed  Google Scholar 

  3. Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002). doi:10.1146/annurev.biochem.71.110601.135458

    Article  CAS  PubMed  Google Scholar 

  4. Freeze, H.H., Sampath, D., Varki, A.: Alpha- and beta-xylosides alter glycolipid synthesis in human melanoma and Chinese hamster ovary cells. J. Biol. Chem. 268, 1618–1627 (1993)

    CAS  PubMed  Google Scholar 

  5. Gouyer, V., Leteurtre, E., Delmotte, P., Steelant, W.F., Krzewinski-Recchi, M.A., Zanetta, J.P., Lesuffleur, T., Trugnan, G., Delannoy, P., Huet, G.: Differential effect of GalNAcalpha-O-bn on intracellular trafficking in enterocytic HT-29 and Caco-2 cells: correlation with the glycosyltransferase expression pattern. J. Cell Sci. 114, 1455–1471 (2001)

    CAS  PubMed  Google Scholar 

  6. Iozzo, R.V., San Antonio, J.D.: Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena. J. Clin. Invest. 108, 349–355 (2001)

    CAS  PubMed  Google Scholar 

  7. Kolset, S.O., Sakurai, K., Ivhed, I., Overvatn, A., Suzuki, S.: The effect of beta-d-xylosides on the proliferation and proteoglycan biosynthesis of monoblastic U-937 cells. Biochem. J. 265, 637–645 (1990)

    CAS  PubMed  Google Scholar 

  8. Kolset, S.O., Tveit, H.: Serglycin—structure and biology. Cell. Mol. Life Sci. 65, 1073–1085 (2008). doi:10.1007/s00018-007-7455-6

    Article  CAS  PubMed  Google Scholar 

  9. Kolset, S.O., Vuong, T.T., Prydz, K.: Apical secretion of chondroitin sulphate in polarized Madin-Darby canine kidney (MDCK) cells. J. Cell Sci. 112(Pt 11), 1797–1801 (1999)

    CAS  PubMed  Google Scholar 

  10. Lugemwa, F.N., Esko, J.D.: Estradiol beta-d-xyloside, an efficient primer for heparan sulfate biosynthesis. J. Biol. Chem. 266, 6674–6677 (1991)

    CAS  PubMed  Google Scholar 

  11. Malavaki, C., Mizumoto, S., Karamanos, N., Sugahara, K.: Recent Advances in the structural study of functional chondroitin sulfate and dermatan sulfate in health and disease. Connect. Tissue Res. 49, 133–139 (2008). doi:10.1080/03008200802148546

    Article  CAS  PubMed  Google Scholar 

  12. Mani, K., Havsmark, B., Persson, S., Kaneda, Y., Yamamoto, H., Sakurai, K., Ashikari, S., Habuchi, H., Suzuki, S., Kimata, K., Malmstrom, A., Westergren-Thorsson, G., Fransson, L.A.: Heparan/chondroitin/dermatan sulfate primer 2-(6-hydroxynaphthyl)-O-beta-d-xylopyranoside preferentially inhibits growth of transformed cells. Cancer Res. 58, 1099–1104 (1998)

    CAS  PubMed  Google Scholar 

  13. Moses, J., Oldberg, A., Fransson, L.A.: Initiation of galactosaminoglycan biosynthesis. Separate galactosylation and dephosphorylation pathways for phosphoxylosylated decorin protein and exogenous xyloside. Eur. J. Biochem. 260, 879–884 (1999). doi:10.1046/j.1432-1327.1999.00228.x

    Article  CAS  PubMed  Google Scholar 

  14. Pejler, G., Abrink, M., Ringvall, M., Wernersson, S.: Mast cell proteases. Adv. Immunol. 95, 167–255 (2007). doi:10.1016/S0065-2776(07)95006-3

    Article  CAS  PubMed  Google Scholar 

  15. Pejler, G., Winberg, J.O., Vuong, T.T., Henningsson, F., Uhlin-Hansen, L., Kimata, K., Kolset, S.O.: Secretion of macrophage urokinase plasminogen activator is dependent on proteoglycans. Eur. J. Biochem. 270, 3971–3980 (2003). doi:10.1046/j.1432-1033.2003.03785.x

    Article  CAS  PubMed  Google Scholar 

  16. Prydz, K., Dalen, K.T.: Synthesis and sorting of proteoglycans. J. Cell Sci. 113(Pt 2), 193–205 (2000)

    CAS  PubMed  Google Scholar 

  17. Prydz, K., Dick, G., Tveit, H.: How many ways through the Golgi maze? Traffic 9, 299–304 (2008). doi:10.1111/j.1600-0854.2007.00690.x

    Article  CAS  PubMed  Google Scholar 

  18. Ristamäki, R., Joensuu, H., Jalkanen, S.: Serum CD44 in Non-Hodgkin’s Lymphoma. Leuk. Lymphoma 33, 433–440 (1999)

    PubMed  Google Scholar 

  19. Salmivirta, M., Safaiyan, F., Prydz, K., Andresen, M.S., Aryan, M., Kolset, S.O.: Differentiation-associated modulation of heparan sulfate structure and function in CaCo-2 colon carcinoma cells. Glycobiology 8, 1029–1036 (1998). doi:10.1093/glycob/8.10.1029

    Article  CAS  PubMed  Google Scholar 

  20. Shively, J.E., Conrad, H.E.: Formation of anhydrosugars in the chemical depolymerization of heparin. Biochemistry 15, 3932–3942 (1976). doi:10.1021/bi00663a005

    Article  CAS  PubMed  Google Scholar 

  21. Simon-Assmann, P., Kedinger, M., De Arcangelis, A., Rousseau, V., Simo, P.: Extracellular matrix components in intestinal development. Experientia 51, 883–900 (1995). doi:10.1007/BF01921739

    Article  CAS  PubMed  Google Scholar 

  22. Tveit, H., Dick, G., Skibeli, V., Prydz, K.: A proteoglycan undergoes different modifications en route to the apical and basolateral surfaces of Madin-Darby canine kidney cells. J. Biol. Chem. 280, 29596–29603 (2005). doi:10.1074/jbc.M503691200

    Article  CAS  PubMed  Google Scholar 

  23. Vuong, T.T., Prydz, K., Tveit, H.: Differences in the apical and basolateral pathways for glycosaminoglycan biosynthesis in Madin-Darby canine kidney cells. Glycobiology 16, 326–332 (2006). doi:10.1093/glycob/cwj075

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from The Norwegian Cancer Society and The Throne Holst Foundation

Author information

Authors and Affiliations

  1. Department of Molecular Biosciences, University of Oslo, Box 1041, Blindern, 0316, Oslo, Norway

    Kristian Prydz

  2. Department of Pathology, Rikshospitalet University Hospital, 0027, Oslo, Norway

    Tram T. Vuong

  3. Department of Nutrition, University of Oslo, Box 1046, Blindern, 0316, Oslo, Norway

    Svein O. Kolset

Authors
  1. Kristian Prydz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tram T. Vuong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Svein O. Kolset
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Svein O. Kolset.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prydz, K., Vuong, T.T. & Kolset, S.O. Glycosaminoglycan secretion in xyloside treated polarized human colon carcinoma Caco-2 cells. Glycoconj J 26, 1117–1124 (2009). https://doi.org/10.1007/s10719-009-9232-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-009-9232-2

Keywords

Search

Navigation