Abstract
Mammalian cells endocytose a variety of proteins and lipids without utilising clathrin-coated pits1,2,3,4,5. Detailed molecular mechanisms for clathrin-independent endocytosis are unclear. Several markers for this process, including glycosphingolipid-binding bacterial toxin subunits such as cholera toxin B subunit (CTxB), and glycosyl-phosphatidyl-inositol (GPI)-anchored proteins, are found in detergent-resistant membrane fractions (DRMs), or 'lipid rafts'2,3,5,6,7. The Golgi complex constitutes one principal intracellular destination for these markers2. Uptake of both CTxB and GPI-anchored proteins may involve caveolae, small invaginations in the plasma membrane (PM)8,9,10,11,12,13. However, the identity of intermediate organelles involved in PM to Golgi trafficking, as well as the function of caveolins, defining protein components of caveolae12,13, are unclear. This paper shows that molecules which partition into DRMs and are endocytosed in a clathrin-independent fashion, accumulate in a discrete population of endosomes en route to the Golgi complex. These endosomes are devoid of markers for classical early and recycling endosomes, but do contain caveolin-1. Caveolin-1-positive endosomes are sites for the sorting of caveolin-1 away from Golgi-bound cargoes, although caveolin-1 itself is unlikely to have a direct function in PM to Golgi transport.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Puri, V. et al. J. Cell Biol. 154, 535–547 (2001).
Nichols, B. J. et al. J. Cell Biol. 153, 529–541 (2001).
Nichols, B. J. & Lippincott-Schwartz, J. Trends Cell Biol. 11, 406–412 (2001).
Iversen, T. G. et al. Mol. Biol. Cell 12, 2099–2107 (2001).
Lamaze, C. et al. Mol. Cell 7, 661–671 (2001).
Brown, D,A. & London, E. Annu. Rev. Cell. Dev. Biol. 14, 111–136 (1998).
Simons, K. & Ikonen, E. Nature 387, 569–572 (1997).
Orlandi, P. A. & Fishman, P. H. J. Cell Biol. 141, 905–915 (1998).
Torgersen, M. L., Skretting, G., van Deurs, B. & Sandvig, K. J. Cell Sci. 114, 3737–3747 (2001).
Henley, J. R., Krueger, E. W., Oswald, B. J. & McNiven, M. A. J. Cell Biol. 141, 85–99 (1998).
Oh, P., McIntosh, D. P. & Schnitzer, J. E. J. Cell Biol. 141, 101–114 (1998).
Razani, B. & Lisanti, M. P. Exp. Cell Res. 271, 36–44 (2001).
Kurzchalia, T. V. & Parton, R. G. Curr. Opin. Cell Biol. 11, 424–431 (1999).
Pelkmans, L., Kartenbeck, J. & Helenius, A. Nature Cell Biol. 3, 473–483 (2001).
Scheiffele, P. et al. J. Cell Biol. 140, 795–806 (1998).
Shogomori, H. & Futerman, A. H. J. Biol. Chem. 276, 9182–9188 (2001).
Ford, M. G., et al. Science 291, 1051–1055 (2001).
Stenmark, H., Aasland, R., Toh, B. H. and D'Arrigo, A. J. Biol. Chem. 271, 24048–24054 (1996).
Elbashir, S. M. et al. Nature 411, 494–498 (2001).
Razani, B. et al. J. Biol. Chem. 276, 38121–38138 (2001).
Drab, M. et al. Science 293, 2449–2452 (2001).
Schubert, W. et al. J. Biol. Chem. 276, 48619–48622 (2001).
Chatterjee, S., Smith, E. R., Hanada, K., Stevens, V. L. & Mayor, S. EMBO J. 20, 1583–1592 (2001).
Lipardi, C. Nitsch, L. & Zurzolo, C. Mol. Biol. Cell 11, 531–542 (2000).
Benting, J. H., Rietveld, A. G. & Simons, K. J. Cell. Biol. 146, 313–320 (1999).
Abrami, L. et al. J. Biol. Chem. 276, 30729–30736 (2001).
Oh, P. & Schnitzer, J. E. Mol. Biol. Cell 12, 685–698 (2001).
Schnitzer, J. E., Oh, P. & McIntosh, D. P. Science 274, 239–242 (1996).
Acknowledgements
Many thanks to P. Pipkin for assistance with SV40 infection, A. Helenius and L. Pelkmans for caveolin-1–GFP and the anti-SV40 antibodies, H. McMahon for the AP180-C construct, and H. Pelham and S. Munro for comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nichols, B. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat Cell Biol 4, 374–378 (2002). https://doi.org/10.1038/ncb787
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ncb787
This article is cited by
-
Directing the Way—Receptor and Chemical Targeting Strategies for Nucleic Acid Delivery
Pharmaceutical Research (2023)
-
Plasmalogens Inhibit Endocytosis of Toll-like Receptor 4 to Attenuate the Inflammatory Signal in Microglial Cells
Molecular Neurobiology (2019)
-
ROR1 sustains caveolae and survival signalling as a scaffold of cavin-1 and caveolin-1
Nature Communications (2016)
-
Dynamic caveolae exclude bulk membrane proteins and are required for sorting of excess glycosphingolipids
Nature Communications (2015)
-
The Role of Endocytic Pathways in TGF-β Signaling
Pathology & Oncology Research (2013)