Clathrin- and caveolin-1-independent endocytosis: Entry of simian virus 40 into cells devoid of caveolae

Journal of Cell Biology

Volumn 168, Issue 3, 2005, Pages 477-488

  Damm, Eva Maria ^a   Pelkmans, Lucas ^b   Kartenbeck, Jürgen ^c   Mezzacasa, Anna ^a   Kurzchalia, Teymuras ^b   Helenius, Ari ^a  

^a ETH ZURICH   (Switzerland)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CAVEOLIN 1; CAVEOLIN 2; CHOLESTEROL; CLATHRIN; DYNAMIN II; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; CAVEOLA; CELL LINE; CELL ORGANELLE; CELL TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; EMBRYO CELL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; FIBROBLAST; HEPATOMA CELL; HUMAN; HUMAN CELL; INTERNALIZATION; KNOCKOUT MOUSE; MEMBRANE BINDING; MEMBRANE TRANSPORT; MICROTUBULE; NONHUMAN; PH; PRIORITY JOURNAL; SIMIAN VIRUS 40; TIME; VIRUS INFECTION; WILD TYPE;

ADP-RIBOSYLATION FACTORS; ANIMALS; ANTIGENS, VIRAL, TUMOR; BICYCLO COMPOUNDS, HETEROCYCLIC; BREFELDIN A; CALCIUM-BINDING PROTEINS; CAVEOLAE; CAVEOLIN 1; CAVEOLIN 2; CAVEOLINS; CELL LINE; CELL LINE, TUMOR; CHOLESTEROL; CLATHRIN; DETERGENTS; DYNAMIN II; EMBRYO; ENDOCYTOSIS; ENDOPLASMIC RETICULUM, SMOOTH; FIBROBLASTS; GENE EXPRESSION; GENISTEIN; HUMANS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROFILAMENTS; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROTUBULES; NOCODAZOLE; PHOSPHOPROTEINS; SEMLIKI FOREST VIRUS; SIMIAN VIRUS 40; THIAZOLES; THIAZOLIDINES; TRANSFERRIN; TRANSPORT VESICLES; TUBULIN; VESICULAR TRANSPORT PROTEINS;

ANIMALIA; DNA VIRUSES; SIMIAE; SIMIAN VIRUS 40;

EID: 13444273098     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200407113     Document Type: Article

References (46)

1. Anderson, H.A., Y. Chen, and L.C. Norkin. 1996. Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. Mol. Biol. Cell. 7:1825-1834.
2. Anderson, R.G. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67:199-225.
3. Arnaoutova, I., C.L. Jackson, O.S. Al-Awar, J.G. Donaldson, and Y.P. Loh. 2003. Recycling of Raft-associated prohormone sorting receptor carboxypeptidase E requires interaction with ARF6. Mol. Biol. Cell. 14:4448-4457.
4. Benlimame, N., P.U. Le, and I.R. Nabi. 1998. Localization of autocrine motility factor receptor to caveolae and clathrin-independent internalization of its ligand to smooth endoplasmic reticulum. Mol. Biol. Cell. 9:1773-1786.
5. Benmerah, A., M. Bayrou, N. Cerf-Bensussan, and A. Dautry-Varsat. 1999. Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J. Cell Sci. 112:1303-1311.
6. Brown, D.A., and J.K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
7. Conner, S.D., and S.L. Schmid. 2003. Regulated portals of entry into the cell. Nature. 422:37-44.
8. Dautry-Varsat, A. 2000. Clathrin-independent endocytosis. In Endocytosis. M. Marsh, editor. Oxford University Press, Oxford. 26-57.
9. De Camilli, P., K. Takei, and P.S. McPherson. 1995. The function of dynamin in endocytosis. Curr. Opin. Neurobiol. 5:559-565.
10. Drab, M., P. Verkade, M. Elger, M. Kasper, M. Lohn, B. Lauterbach, J. Menne, C. Lindschau, F. Mende, F.C. Luft, et al. 2001. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 293:2449-2452.
11. Fish, K.N., S.L. Schmid, and H. Damke. 2000. Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell Biol. 150:145-154.
12. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1995. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA. 92:8655-8659.
13. Gilbert, J.M., and T.L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588.
14. Hammond, C., and A. Helenius. 1994. Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126:41-52.
15. Johannes, L., and C. Lamaze. 2002. Clathrin-dependent or not: is it still the question? Traffic. 3:443-451.
16. Kartenbeck, J., H. Stukenbrok, and A. Helenius. 1989. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109:2721-2729.
17. Kasamatsu, H., and A. Nakanishi. 1998. How do animal DNA viruses get to the nucleus? Annu. Rev. Microbiol. 52:627-686.
18. Kurzchalia, T.V., and R.G. Parton. 1999. Membrane microdomains and caveolae. Curr. Opin. Cell Biol. 11:424-431.
19. Lamaze, C., A. Dujeancourt, T. Baba, C.G. Lo, A. Benmerah, and A. Dautry-Varsat. 2001. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell. 7:661-671.
20. Le, P.U., G. Guay, Y. Altschuler, and I.R. Nabi. 2002. Caveolin-1 is a negative regulator of caveolae-mediated endocytosis to the endoplasmic reticulum. J. Biol. Chem. 277:3371-3379.
21. Marsh, M., and A. Helenius. 1989. Virus entry into animal cells. Adv. Virus Res. 36:107-151.
22. Nabi, I.R., and P.U. Le. 2003. Caveolae/raft-dependent endocytosis. J. Cell Biol. 161:673-677.
23. Naslavsky, N., R. Weigert, and J.G. Donaldson. 2003. Convergence of nonclathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol. Biol. Cell. 14:417-431.
24. Naslavsky, N., R. Weigert, and J.G. Donaldson. 2004. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell. 15:3542-3552.
25. Nichols, B. 2003. Caveosomes and endocytosis of lipid rafts. J. Cell Sci. 116:4707-4714.
26. Nichols, B.J. 2002. A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4:374-378.
27. Norkin, L.C. 2001. Caveolae in the uptake and targeting of infectious agents and secreted toxins. Adv. Drug Deliv. Rev. 49:301-315.
28. Oh, P., D.P. McIntosh, and J.E. Schnitzer. 1998. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141:101-114.
29. Parolini, I., M. Sargiacomo, F. Galbiati, G. Rizzo, F. Grignani, J.A. Engelman, T. Okamoto, T. Ikezu, P.E. Scherer, R. Mora, et al. 1999. Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the golgi complex. J. Biol. Chem. 274:25718-25725.
30. Parton, R.G. 1994. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J. Histochem. Cytochem. 42:155-166.
31. Parton, R.G., and M. Lindsay. 1999. Exploitation of major histocompatibility complex class I molecules and caveolae by simian virus 40. Immunol. Rev. 168:23-31.
32. Parton, R.G., and A.A. Richards. 2003. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic. 4:724-738.
33. Pelkmans, L., and A. Helenius. 2003. Insider information: what viruses tell us about endocytosis. Curr. Opin. Cell Biol. 15:414-422.
34. Pelkmans, L., J. Kartenbeck, and A. Helenius. 2001. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3:473-483.
35. Pelkmans, L., D. Puntener, and A. Helenius. 2002. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science. 296:535-539.
36. Peters, P.J., A. Mironov Jr., D. Peretz, E. van Donselaar, E. Leclerc, S. Erpel, S.J. DeArmond, D.R. Burton, R.A. Williamson, M. Vey, and S.B. Prusiner. 2003. Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J. Cell Biol. 162:703-717.
37. Razani, B., T.P. Combs, X.B. Wang, P.G. Frank, D.S. Park, R.G. Russell, M. Li, B. Tang, L.A. Jelicks, P.E. Scherer, and M.P. Lisanti. 2002. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277:8635-8647.
38. Rothberg, K.G., J.E. Heuser, W.C. Donzell, Y.S. Ying, J.R. Glenney, and R.G. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell. 68:673-682.
39. Sabharanjak, S., P. Sharma, R.G. Parton, and S. Mayor. 2002. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell. 2:411-423.
40. Sieczkarski, S.B., and G.R. Whittaker. 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545.
41. Simons, K., and E. Ikonen. 2000. How cells handle cholesterol. Science. 290:1721-1726.
42. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
43. Steegmaier, M., V. Oorschot, J. Klumperman, and R.H. Scheller, 2000. Syntaxin 17 is abundant in steroidogenic cells and implicated in smooth endoplasmic reticulum membrane dynamics. Mol. Biol. Cell. 11:2719-2731.
44. Thomsen, P., K. Roepstorff, M. Stahlhut, and B. van Deurs. 2002. Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell. 13:238-250.
45. Vainio, S., S. Heino, J.E. Mansson, P. Fredman, E. Kuismanen, O. Vaarala, and E. Ikonen. 2002. Dynamic association of human insulin receptor with lipid rafts in cells lacking caveolae. EMBO Rep. 3:95-100.
46. Williams, T.M., and M.P. Lisanti. 2004. The caveolin proteins. Genome Biol. 5:214.