The fully linked HTML version of this article has now been published.
JCS ePress
online publication date 29 Jan 2003
doi: 10.1242/jcs.00327
Research Article
Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum
Phuong U. Le
and
Ivan R. Nabi*
* Author for correspondence (e-mail: ivan.robert.nabi{at}umontreal.ca)
Internalization of autocrine motility factor (AMF) into the endoplasmic reticulum is sensitive to the cholesterol-extracting reagent methyl-
-cyclodextrin, inhibited by the dynamin-1 K44A mutant and negatively regulated by caveolin-1. Thus, AMF internalization requires a caveolae-mediated endocytic pathway. Similarly, we show here that endocytosis of cholera toxin (CTX) in NIH-3T3 fibroblasts is inhibited by adenoviral expression of the dynamin-1 K44A mutant but only partially by expression of the clathrin hub. Treatment with methyl--cyclodextrin and overexpression of caveolin-1, but not the clathrin hub, selectively diminishes CTX endocytosis to the Golgi apparatus but not to endosomes. CTX is therefore targeted via a caveolin-1-regulated caveolae-mediated pathway to the Golgi. Disruption of Golgi-, caveosome- or endosome-mediated trafficking with brefeldin A, nocodazole or a 20°C temperature block, respectively, inhibit CTX endocytosis to the Golgi but do not affect AMF delivery to the endoplasmic reticulum. Following an incubation of only five minutes in the presence of the clathrin hub, AMF and CTX are not cointernalized, and AMF is delivered to the AMF-R-positive smooth ER. The internalization of both ligands is nevertheless sensitive to the tyrosine kinase inhibitor genistein, confirming that they are both internalized via caveolae/raft pathways. Two distinct caveolae-mediated endocytic pathways therefore exist, including a novel direct pathway to the ER from the plasma membrane.
This article has been cited by other articles:
|
|
|
|
 
Y. Pu and X. Zhang
Mouse Hepatitis Virus Type 2 Enters Cells through a Clathrin-Mediated Endocytic Pathway Independent of Eps15
J. Virol.,
August 15, 2008;
82(16):
8112 - 8123.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Delva, J. M. Jennings, C. C. Calkins, M. D. Kottke, V. Faundez, and A. P. Kowalczyk
Pemphigus Vulgaris IgG-induced Desmoglein-3 Endocytosis and Desmosomal Disassembly Are Mediated by a Clathrin- and Dynamin-independent Mechanism
J. Biol. Chem.,
June 27, 2008;
283(26):
18303 - 18313.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Saavedra, A. Mohamed, V. Ma, S. Kar, and E. P. de Chaves
Internalization of -Amyloid Peptide by Primary Neurons in the Absence of Apolipoprotein E
J. Biol. Chem.,
December 7, 2007;
282(49):
35722 - 35732.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. D. Kojic, B. Joshi, P. Lajoie, P. U. Le, M. E. Cox, D. A. Turbin, S. M. Wiseman, and I. R. Nabi
Raft-dependent Endocytosis of Autocrine Motility Factor Is Phosphatidylinositol 3-Kinase-dependent in Breast Carcinoma Cells
J. Biol. Chem.,
October 5, 2007;
282(40):
29305 - 29313.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. W. Wong, S. J. Scales, and D. E. Reilly
DNA Internalized via Caveolae Requires Microtubule-dependent, Rab7-independent Transport to the Late Endocytic Pathway for Delivery to the Nucleus
J. Biol. Chem.,
August 3, 2007;
282(31):
22953 - 22963.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Schilling, N. Opitz, A. Wiesenthal, S. Oess, R. Tikkanen, W. Muller-Esterl, and A. Icking
Translocation of Endothelial Nitric-Oxide Synthase Involves a Ternary Complex with Caveolin-1 and NOSTRIN
Mol. Biol. Cell,
September 1, 2006;
17(9):
3870 - 3880.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Wang, D. Li, H. Fan, L. Tian, Y. Zhong, Y. Zhang, L. Yuan, C. Jin, C. Yin, and D. Ma
Cellular Uptake of Exogenous Human PDCD5 Protein
J. Biol. Chem.,
August 25, 2006;
281(34):
24803 - 24817.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z.-J. Cheng, R. D. Singh, D. K. Sharma, E. L. Holicky, K. Hanada, D. L. Marks, and R. E. Pagano
Distinct Mechanisms of Clathrin-independent Endocytosis Have Unique Sphingolipid Requirements
Mol. Biol. Cell,
July 1, 2006;
17(7):
3197 - 3210.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Tomasinsig, B. Skerlavaj, N. Papo, B. Giabbai, Y. Shai, and M. Zanetti
Mechanistic and Functional Studies of the Interaction of a Proline-rich Antimicrobial Peptide with Mammalian Cells
J. Biol. Chem.,
January 6, 2006;
281(1):
383 - 391.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J.-X. Zhu, S. Goldoni, G. Bix, R. T. Owens, D. J. McQuillan, C. C. Reed, and R. V. Iozzo
Decorin Evokes Protracted Internalization and Degradation of the Epidermal Growth Factor Receptor via Caveolar Endocytosis
J. Biol. Chem.,
September 16, 2005;
280(37):
32468 - 32479.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Lagana, J. G. Goetz, N. Y, Y. Altschuler, and I. R. Nabi
pH-specific sequestration of phosphoglucose isomerase/autocrine motility factor by fibronectin and heparan sulphate
J. Cell Sci.,
September 15, 2005;
118(18):
4175 - 4185.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Alcon-LePoder, M.-T. Drouet, P. Roux, M.-P. Frenkiel, M. Arborio, A.-M. Durand-Schneider, M. Maurice, I. Le Blanc, J. Gruenberg, and M. Flamand
The Secreted Form of Dengue Virus Nonstructural Protein NS1 Is Endocytosed by Hepatocytes and Accumulates in Late Endosomes: Implications for Viral Infectivity
J. Virol.,
September 1, 2005;
79(17):
11403 - 11411.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Beer, D. S. Andersen, A. Rojek, and L. Pedersen
Caveola-Dependent Endocytic Entry of Amphotropic Murine Leukemia Virus
J. Virol.,
August 15, 2005;
79(16):
10776 - 10787.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Morinaga, Y. Iwamaru, K. Yahiro, M. Tagashira, J. Moss, and M. Noda
Differential Activities of Plant Polyphenols on the Binding and Internalization of Cholera Toxin in Vero Cells
J. Biol. Chem.,
June 17, 2005;
280(24):
23303 - 23309.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. R. Pendleton and C. E. Machamer
Infectious Bronchitis Virus 3a Protein Localizes to a Novel Domain of the Smooth Endoplasmic Reticulum
J. Virol.,
May 15, 2005;
79(10):
6142 - 6151.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Sauvonnet, A. Dujeancourt, and A. Dautry-Varsat
Cortactin and dynamin are required for the clathrin-independent endocytosis of {gamma}c cytokine receptor
J. Cell Biol.,
January 3, 2005;
168(1):
155 - 163.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Gilbert and T. Benjamin
Uptake Pathway of Polyomavirus via Ganglioside GD1a
J. Virol.,
November 15, 2004;
78(22):
12259 - 12267.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Eash, W. Querbes, and W. J. Atwood
Infection of Vero Cells by BK Virus Is Dependent on Caveolae
J. Virol.,
November 1, 2004;
78(21):
11583 - 11590.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Pietiainen, V. Marjomaki, P. Upla, L. Pelkmans, A. Helenius, and T. Hyypia
Echovirus 1 Endocytosis into Caveosomes Requires Lipid Rafts, Dynamin II, and Signaling Events
Mol. Biol. Cell,
November 1, 2004;
15(11):
4911 - 4925.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. A. Khine, P. Tam, A. Nutikka, and C. A. Lingwood
Brefeldin A and filipin distinguish two globotriaosyl ceramide/verotoxin-1 intracellular trafficking pathways involved in Vero cell cytotoxicity
Glycobiology,
August 1, 2004;
14(8):
701 - 712.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. H. Massol, J. E. Larsen, Y. Fujinaga, W. I. Lencer, and T. Kirchhausen
Cholera Toxin Toxicity Does Not Require Functional Arf6- and Dynamin-dependent Endocytic Pathways
Mol. Biol. Cell,
August 1, 2004;
15(8):
3631 - 3641.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. W. McL. Rixon, G. Brown, J. Aitken, T. McDonald, S. Graham, and R. J. Sugrue
The small hydrophobic (SH) protein accumulates within lipid-raft structures of the Golgi complex during respiratory syncytial virus infection
J. Gen. Virol.,
May 1, 2004;
85(5):
1153 - 1165.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. E. Smith and A. Helenius
How Viruses Enter Animal Cells
Science,
April 9, 2004;
304(5668):
237 - 242.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Pang, P. U. Le, and I. R. Nabi
Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus
J. Cell Sci.,
March 15, 2004;
117(8):
1421 - 1430.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Nichols
Caveosomes and endocytosis of lipid rafts
J. Cell Sci.,
December 1, 2003;
116(23):
4707 - 4714.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Amraei, Z. Jia, P. Reboul, and I. R. Nabi
Acid-induced Conformational Changes in Phosphoglucose Isomerase Result in Its Increased Cell Surface Association and Deposition on Fibronectin Fibrils
J. Biol. Chem.,
October 3, 2003;
278(40):
38935 - 38941.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. D. Singh, V. Puri, J. T. Valiyaveettil, D. L. Marks, R. Bittman, and R. E. Pagano
Selective Caveolin-1-dependent Endocytosis of Glycosphingolipids
Mol. Biol. Cell,
August 1, 2003;
14(8):
3254 - 3265.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Venkatesan, J. J. Rose, R. Lodge, P. M. Murphy, and J. F. Foley
Distinct Mechanisms of Agonist-induced Endocytosis for Human Chemokine Receptors CCR5 and CXCR4
Mol. Biol. Cell,
August 1, 2003;
14(8):
3305 - 3324.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. R. Nabi and P. U. Le
Caveolae/raft-dependent endocytosis
J. Cell Biol.,
May 26, 2003;
161(4):
673 - 677.
[Abstract]
[Full Text]
[PDF]
|
|
|
© The Company of Biologists Ltd 2003
