Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

N-glycans as apical sorting signals in epithelial cells

Abstract

IN epithelial Madin–Darby canine kidney (MDCK) cells newly synthesized molecules are sorted in the trans-Golgi network and directly delivered to their apical and basolateral surface destinations1. Sorting is mediated by signals in the cytoplasmic domains of basolateral transmembrane proteins2–4 whereas gly-cosylphosphatidylinositol-linked proteins have apical sorting information in their glycolipid tails5,6. Signals for apical transmembrane proteins are thought to reside in their ectodomains, because truncated forms lacking the cytoplasmic tail and the membrane anchor are secreted apically7,8. Here we demonstrate that carbohydrates act as an apical targeting signal for secretory proteins. Growth hormone, which is non-glycosylated and secreted from both sides of MDCK cell layers9, is secreted from the apical side when gly-cosylated. Thus glycans not only play a general role in protein folding10 but also appear to function in protein sorting in biosynthetic traffic.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Wandinger-Ness, A., Bennet, M. K., Antony, C. & Simons, K. J. Cell Biol. 111, 987–1000 (1990).

    Article  CAS  PubMed  Google Scholar 

  2. Hunziker, W., Harter, C., Matter, K. & Mellman, I. Cell 66, 1–20 (1991).

    Article  Google Scholar 

  3. Mostov, K. E., Harris, J. M. & Breitfeld, P. P. J. Cell Biol. 105, 2031–2036 (1987).

    Article  CAS  PubMed  Google Scholar 

  4. Matter, K. & Mellman, I. Curr. Opin. Cell Biol. 6, 545–554 (1994).

    Article  CAS  PubMed  Google Scholar 

  5. Brown, D. A., Crise, B. & Rose, J. K. Science 245, 1499–1501 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Lisanti, M. P., Caras, I. W., Davitz, M. A. & Rodriguez-Boulan, E. J. Cell Biol. 109, 2145–2156 (1989).

    Article  CAS  PubMed  Google Scholar 

  7. Corbeil, D., Boileau, G., Lemay, G. & Crine, P. J. biol. Chem. 267, 2798–2801 (1992).

    CAS  PubMed  Google Scholar 

  8. Vogel, L. K., Spiess, M., Sjöström, H. & Norén, O. J. biol. Chem. 267, 2794–2797 (1992).

    CAS  PubMed  Google Scholar 

  9. Gottlieb, T. A. et al. Proc. natn. Acad. Sci. U.S.A. 83, 2100–2104 (1986).

    Article  ADS  CAS  Google Scholar 

  10. Helenius, A. Molec. Biol. Cell 5, 253–265 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Green, R. F., Meiss, H. K. & Rodriguez-Boulan, E. J. J. Cell Biol. 89, 230–239 (1981).

    Article  CAS  PubMed  Google Scholar 

  12. Urban, J., Parczyk, K., Leutz, A., Kayne, M. & Kondor-Koch, C. J. Cell Biol. 105, 2735–2743 (1987).

    Article  CAS  PubMed  Google Scholar 

  13. Guan, J.-L., Machamer, C. E. & Rose, J. K. Cell 42, 489–496 (1985).

    Article  CAS  PubMed  Google Scholar 

  14. Balcarova-Ständer, J., Pfeiffer, S. E., Fuller, S. D. & Simons, K. EMBO J. 3, 2687–2694 (1984).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kondor-Koch, C. B., Bravo, R., Fuller, S. D., Cutler, D. & Garoff, H. Cell 43, 297–306 (1985).

    Article  CAS  PubMed  Google Scholar 

  16. Cunningham, B. C., Mulkerrin, M. G. & Wells, J. A. Science 253, 545–548 (1991).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Chanat, E. & Huttner, W. B. J. Cell Biol. 115, 1505–1519 (1991).

    Article  CAS  PubMed  Google Scholar 

  18. Gonzalez, A., Nicovani, S. & Juica, F. J. biol. Chem. 268, 6662–6667 (1993).

    CAS  PubMed  Google Scholar 

  19. Fiedler, K. & Simons, K. Cell 81, 1–20 (1995).

    Article  Google Scholar 

  20. Musto, N. A. Expl Cell Res. 209, 271–276 (1993).

    Article  CAS  Google Scholar 

  21. Kitagawa, Y. et al. Expl Cell Res. 213, 449–457 (1994).

    Article  CAS  Google Scholar 

  22. Vogel, L. K., Suske, G., Beato, M., Norén, O. & Sjöström, H. FEBS Lett. 330, 293–296 (1993).

    Article  CAS  PubMed  Google Scholar 

  23. Meiss, H. K., Green, R. F. & Rodriguez-Boulan, E., Molec. cell. Biol. 2, 1287–1294 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wagner, M., Morgans, C. & Koch-Brandt, C. Eur. J. Cell Biol. 67, 84–88 (1995).

    CAS  PubMed  Google Scholar 

  25. Fiedler, K., Parton, R. G., Kellner, R., Etzold, T. & Simons, K. EMBO J. 13, 1729–1740 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Caplan, M. J. et al. Nature 329, 632–635 (1987).

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Ragno, P. et al. Expl Cell Res. 203, 236–243 (1992).

    Article  CAS  Google Scholar 

  28. Rodriguez-Boulan, E. & Powell, S. K. A. Rev. Cell Biol. 8, 395–427 (1992).

    Article  CAS  Google Scholar 

  29. Casanova, J. E., Breitfeld, P. P., Ross, S. A. & Mostov, K. E. Science 248, 742–745 (1990).

    Article  ADS  CAS  PubMed  Google Scholar 

  30. Miller, A. D. & Rosman, G. M. Biotechniques 7, 980–990 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scheiffele, P., Peränen, J. & Simons, K. N-glycans as apical sorting signals in epithelial cells. Nature 378, 96–98 (1995). https://doi.org/10.1038/378096a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/378096a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing