Evolutionary analysis and molecular dissection of caveola biogenesis

Kirkham, Matthew; Nixon, Susan J.; Howes, Mark T.; Abi-Rached, Laurent; Wakeham, Diane E.; Hanzal-Bayer, Michael; Ferguson, Charles; Hill, Michelle M.; Brown, Deborah A.; Hancock, John F.; Brodsky, Frances M.; Parton, Robert G.

doi:10.1242/jcs.024588

Cited by 111 publications

(144 citation statements)

References 69 publications

(97 reference statements)

Supporting

Mentioning

136

Contrasting

Unclassified

Order By: Relevance

“…The ability of CAV-2 to induce the formation of caveolae has not been tested. Kirkham et al, (2008) have shown that C. elegans CAV-1 does not induce caveolae in mammalian cells and have used phylogenetic analysis to indentify amino acid changes that may underlie this difference (Kirkham et al, 2008). In particular they identified two key regions: one involving residues 56 -59 and another involving residues S104, F12, and A129 in the human caveolin 1 sequence (Supplementary Figure S4), which may determine the ability of caveolins to form caveolae.…”

Section: Discussionmentioning

confidence: 99%

“…The behavior of CAV-1 in the germ line and embryos is highly dynamic . Phylogenetic analysis and expression studies of CAV-1 and CAV-1-mammalian caveolin hybrids in mammalian cells suggest that CAV-1 does not induce caveola biogenesis (Kirkham et al, 2008) and so may have a different role to mammalian caveolins. The function of CAV-2 has not previously been investigated.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Caveolin-2 Is Required for Apical Lipid Trafficking and Suppresses Basolateral Recycling Defects in the Intestine ofCaenorhabditis elegans

Parker

Walker

et al. 2009

MBoC

View full text Add to dashboard Cite

Caveolins are plasma membrane-associated proteins that colocalize with, and stabilize caveolae. Their functions remain unclear although they are known to be involved in specific events in cell signaling and endocytosis. Caenorhabditis elegans encodes two caveolin genes, cav-1 and cav-2. We show that cav-2 is expressed in the intestine where it is localized to the apical membrane and in intracellular bodies. Using the styryl dye FM4-64 and BODIPY-labeled lactosylceramide, we show that the intestinal cells of cav-2 animals are defective in the apical uptake of lipid markers. These results suggest parallels with the function of caveolins in lipid homeostasis in mammals. We also show that CAV-2 depletion suppresses the abnormal accumulation of vacuoles that result from defective basolateral recycling in rme-1 and rab-10 mutants. Analysis of fluorescent markers of basolateral endocytosis and recycling suggest that endocytosis is normal in cav-2 mutants and thus, that the suppression of basolateral recycling defects in cav-2 mutants is due to changes in intracellular trafficking pathways. Finally, cav-2 mutants also have abnormal trafficking of yolk proteins. Taken together, these data indicate that caveolin-2 is an integral component of the trafficking network in the intestinal cells of C. elegans. INTRODUCTIONCaveolae are 50 -100-nm invaginations located on the plasma membrane of many cell types (Anderson, 1998). They are enriched in lipid raft-associated molecules: cholesterol, sphingolipids, glycosphingolipids, and many signaling and receptor proteins. Although identified more than 50 years ago, their functions have remained elusive. However, they are known to play roles in specific cell-signaling processes, and it is clear that endocytosis through caveolae is an important clathrin-independent endocytic pathway (Parton and Richards, 2003;Parton and Simons, 2007). A range of molecules including glycosphingolipids, glycosylphosphatidylinositol (GPI)-anchored proteins, cholera toxin B, and SV40 virus have been shown to traffic through caveolaedependent endocytosis pathways (see Marsh and Helenius, 2006;Mayor and Pagano, 2007; Parton and Simons, 2007 for reviews).Caveolae require caveolin proteins for formation so that depletion of caveolins results in loss of morphologically detectable caveolae (Drab et al., 2001;Galbiati et al., 2001). Furthermore, introduction of caveolin into cells that do not produce caveolae stimulates caveolar biogenesis (Lipardi et al., 1998). The majority of caveolin appears to traffic to the plasma membrane and is relatively immobile; however, internal caveolin-containing structures, named caveosomes, have been visualized (Parton and Simons, 2007) and appear to be an integral part of the caveolin-dependent endocytic machinery (Nichols, 2003). Mammalian cells have three caveolin subtypes: caveolin 1 is widely expressed, but is found at particularly high levels in adipocytes, endothelial cells, and fibroblasts. Caveolin 2 interacts with caveolin 1, whereas caveolin 3 is expressed in myocytes ...

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Caveolin-2 Is Required for Apical Lipid Trafficking and Suppresses Basolateral Recycling Defects in the Intestine ofCaenorhabditis elegans

Parker

Walker

et al. 2009

MBoC

View full text Add to dashboard Cite

show abstract

“…It is unclear whether the effect results from increased levels of CAV-1 in tissues which normally express the CAV-1 protein or , is due to ectopic expression. It has recently been suggested that C. elegans CAV-1 is unlikely to form caveolae, 23 thus making its role in this and other processes in C. elegans enigmatic.…”

Section: Article Addendummentioning

confidence: 99%

“…Egg laying in C. elegans is under neuronal control thus changes in egg laying may be the result of changes in neuronal function brought about by the presence of ectopic CAV-2 protein. The ability of CAV-2 to form caveolae has not been tested; 23 however, bioinformatic analysis Overexpression of caveolins in C. elegans Figure 1. Overexpression of CAV-1 improves fecundity in heat-shocked worms carrying extrachromosomal arrays.…”

Section: Overexpression Of Caveolin-2 Causes Increased Egg Layingmentioning

confidence: 99%