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Caveolae/raft-dependent endocytosis.

Nabi IR, Le PU - J. Cell Biol. (2003)

Bottom Line: Although caveolae are well-characterized subdomains of glycolipid rafts, their distinctive morphology and association with caveolins has led to their internalization being considered different from that of rafts.In this review, we propose that caveolae and rafts are internalized via a common pathway, caveolae/raft-dependent endocytosis, defined by its clathrin independence, dynamin dependence, and sensitivity to cholesterol depletion.The regulatory role of caveolin-1 and ligand sorting in this complex endocytic pathway are specifically addressed.

View Article: PubMed Central - PubMed

Affiliation: Département de Pathologie et Biologie Cellulaire, Université de Montréal, C.P. 6128, Succursale A, Montréal, Québec, Canada H3C 3J7. ivan.robert.nabi@umontreal.ca

ABSTRACT
Although caveolae are well-characterized subdomains of glycolipid rafts, their distinctive morphology and association with caveolins has led to their internalization being considered different from that of rafts. In this review, we propose that caveolae and rafts are internalized via a common pathway, caveolae/raft-dependent endocytosis, defined by its clathrin independence, dynamin dependence, and sensitivity to cholesterol depletion. The regulatory role of caveolin-1 and ligand sorting in this complex endocytic pathway are specifically addressed.

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Caveolae/raft-mediated endocytosis. (A) The cholesterol-dependent invagination of glycolipid rafts occurs independently of caveolin-1 expression and results in the formation of caveolar invaginations that remain only transiently associated with the plasma membrane. Caveolin-1 is a negative regulator of the budding of caveolar invaginations, and caveolin-1–expressing stable cell surface caveolae can become endocytosis competent aftert specific signaling events. Caveolar invaginations bud in a dynamin-dependent manner from the plasma membrane to form caveolar vesicles. (B) COP- dependent pathways target CTX (blue) and SV40 (green) via the caveosome for delivery to the Golgi and ER, respectively, whereas AMF (red) is targeted via a distinct pathway that is apparently direct to the ER. CTX and SV40 could alternatively be targeted to a common caveosome (gray) and subsequently segregated for delivery to the Golgi and ER, respectively (dashed lines).
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fig2: Caveolae/raft-mediated endocytosis. (A) The cholesterol-dependent invagination of glycolipid rafts occurs independently of caveolin-1 expression and results in the formation of caveolar invaginations that remain only transiently associated with the plasma membrane. Caveolin-1 is a negative regulator of the budding of caveolar invaginations, and caveolin-1–expressing stable cell surface caveolae can become endocytosis competent aftert specific signaling events. Caveolar invaginations bud in a dynamin-dependent manner from the plasma membrane to form caveolar vesicles. (B) COP- dependent pathways target CTX (blue) and SV40 (green) via the caveosome for delivery to the Golgi and ER, respectively, whereas AMF (red) is targeted via a distinct pathway that is apparently direct to the ER. CTX and SV40 could alternatively be targeted to a common caveosome (gray) and subsequently segregated for delivery to the Golgi and ER, respectively (dashed lines).

Mentions: Although raft-derived smooth vesicles are technically “raft invaginations,” use of this nomenclature implies that raft-derived smooth invaginations mediate different endocytic processes than do caveolae. We propose that the term “caveolar” be used as a morphological descriptor for endocytic raft-derived invaginations. Caveolar invaginations and caveolar vesicles therefore encompass both endocytosis-competent caveolin-positive caveolae and more transient caveolin-negative raft-derived morphological equivalents. This represents a nomenclature that reflects the similar morphology, lipid composition, and role in endocytosis of these domains. It nevertheless recognizes that stable cell surface–associated caveolae are a functionally distinct organelle whose expression and function are associated with caveolin-1 expression (Fig. 2 A). Caveolae are not observed in endothelial cells of caveolin-1 knock-out mice, although some smooth caveolae-like invaginations were reported (Drab et al., 2001; Razani et al., 2001; Zhao et al., 2002). The extent to which the caveolae/raft-dependent pathway functions in caveolin-1 cells and whether expression of the dynK44A mutant induces the expression of caveolar invaginations in these cells represent critical experiments that remain to be performed.


Caveolae/raft-dependent endocytosis.

Nabi IR, Le PU - J. Cell Biol. (2003)

Caveolae/raft-mediated endocytosis. (A) The cholesterol-dependent invagination of glycolipid rafts occurs independently of caveolin-1 expression and results in the formation of caveolar invaginations that remain only transiently associated with the plasma membrane. Caveolin-1 is a negative regulator of the budding of caveolar invaginations, and caveolin-1–expressing stable cell surface caveolae can become endocytosis competent aftert specific signaling events. Caveolar invaginations bud in a dynamin-dependent manner from the plasma membrane to form caveolar vesicles. (B) COP- dependent pathways target CTX (blue) and SV40 (green) via the caveosome for delivery to the Golgi and ER, respectively, whereas AMF (red) is targeted via a distinct pathway that is apparently direct to the ER. CTX and SV40 could alternatively be targeted to a common caveosome (gray) and subsequently segregated for delivery to the Golgi and ER, respectively (dashed lines).
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Related In: Results  -  Collection

Show All Figures
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fig2: Caveolae/raft-mediated endocytosis. (A) The cholesterol-dependent invagination of glycolipid rafts occurs independently of caveolin-1 expression and results in the formation of caveolar invaginations that remain only transiently associated with the plasma membrane. Caveolin-1 is a negative regulator of the budding of caveolar invaginations, and caveolin-1–expressing stable cell surface caveolae can become endocytosis competent aftert specific signaling events. Caveolar invaginations bud in a dynamin-dependent manner from the plasma membrane to form caveolar vesicles. (B) COP- dependent pathways target CTX (blue) and SV40 (green) via the caveosome for delivery to the Golgi and ER, respectively, whereas AMF (red) is targeted via a distinct pathway that is apparently direct to the ER. CTX and SV40 could alternatively be targeted to a common caveosome (gray) and subsequently segregated for delivery to the Golgi and ER, respectively (dashed lines).
Mentions: Although raft-derived smooth vesicles are technically “raft invaginations,” use of this nomenclature implies that raft-derived smooth invaginations mediate different endocytic processes than do caveolae. We propose that the term “caveolar” be used as a morphological descriptor for endocytic raft-derived invaginations. Caveolar invaginations and caveolar vesicles therefore encompass both endocytosis-competent caveolin-positive caveolae and more transient caveolin-negative raft-derived morphological equivalents. This represents a nomenclature that reflects the similar morphology, lipid composition, and role in endocytosis of these domains. It nevertheless recognizes that stable cell surface–associated caveolae are a functionally distinct organelle whose expression and function are associated with caveolin-1 expression (Fig. 2 A). Caveolae are not observed in endothelial cells of caveolin-1 knock-out mice, although some smooth caveolae-like invaginations were reported (Drab et al., 2001; Razani et al., 2001; Zhao et al., 2002). The extent to which the caveolae/raft-dependent pathway functions in caveolin-1 cells and whether expression of the dynK44A mutant induces the expression of caveolar invaginations in these cells represent critical experiments that remain to be performed.

Bottom Line: Although caveolae are well-characterized subdomains of glycolipid rafts, their distinctive morphology and association with caveolins has led to their internalization being considered different from that of rafts.In this review, we propose that caveolae and rafts are internalized via a common pathway, caveolae/raft-dependent endocytosis, defined by its clathrin independence, dynamin dependence, and sensitivity to cholesterol depletion.The regulatory role of caveolin-1 and ligand sorting in this complex endocytic pathway are specifically addressed.

View Article: PubMed Central - PubMed

Affiliation: Département de Pathologie et Biologie Cellulaire, Université de Montréal, C.P. 6128, Succursale A, Montréal, Québec, Canada H3C 3J7. ivan.robert.nabi@umontreal.ca

ABSTRACT
Although caveolae are well-characterized subdomains of glycolipid rafts, their distinctive morphology and association with caveolins has led to their internalization being considered different from that of rafts. In this review, we propose that caveolae and rafts are internalized via a common pathway, caveolae/raft-dependent endocytosis, defined by its clathrin independence, dynamin dependence, and sensitivity to cholesterol depletion. The regulatory role of caveolin-1 and ligand sorting in this complex endocytic pathway are specifically addressed.

Show MeSH
Related in: MedlinePlus