Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans

被引:84
作者
Sato, Ken
Sato, Miyuki
Audhya, Anjon
Oegema, Karen
Schweinsberg, Peter
Grant, Barth D. [1 ]
机构
[1] Rutgers State Univ, Dept Mol Biol & Biochem, Piscataway, NJ 08854 USA
[2] Gunma Univ, Inst Mol & Cellular Regulat, Lab Mol Traff, Gunma 3718512, Japan
[3] Univ Calif San Diego, Dept Cellular & Mol Med, Ludwig Inst Canc Res, La Jolla, CA 92093 USA
关键词
D O I
10.1091/mbc.E06-03-0211
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Caveolin is the major protein component required for the formation of caveolae on the plasma membrane. Here we show that trafficking of Caenorhabditis elegans caveolin-1 (CAV-1) is dynamically regulated during development of the germ line and embryo. In oocytes a CAV-1-green fluorescent protein (GFP) fusion protein is found on the plasma membrane and in large vesicles (CAV-1 bodies). After ovulation and fertilization the CAV-1 bodies fuse with the plasma membrane in a manner reminiscent of cortical granule exocytosis as described in other species. Fusion of CAV-1 bodies with the plasma membrane appears to be regulated by the advancing cell cycle, and not fertilization per se, because fusion can proceed in spe-9 fertilization mutants but is blocked by RNA interference-mediated knockdown of an anaphase-promoting complex component (EMB-27). After exocytosis, most CAV-1-GFP is rapidly endocytosed and degraded within one cell cycle. CAV-1 bodies in oocytes appear to be produced by the Golgi apparatus in an ARF-1-dependent, clathrin-independent, mechanism. Conversely endocytosis and degradation of CAV-1-GFP in embryos requires clathrin, dynamin, and RAB-5. Our results demonstrate that the distribution of CAV-1 is highly dynamic during development and provides new insights into the sorting mechanisms that regulate CAV-1 localization.
引用
收藏
页码:3085 / 3094
页数:10
相关论文
共 58 条
[31]   Arf and its many interactors [J].
Nie, ZZ ;
Hirsch, DS ;
Randazzo, PA .
CURRENT OPINION IN CELL BIOLOGY, 2003, 15 (04) :396-404
[32]   Lipid rafts and caveolae as portals for endocytosis: New insights and common mechanisms [J].
Parton, RG ;
Richards, AA .
TRAFFIC, 2003, 4 (11) :724-738
[33]   Caveolae and caveolins [J].
Parton, RG .
CURRENT OPINION IN CELL BIOLOGY, 1996, 8 (04) :542-548
[34]   Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae [J].
Pelkmans, L ;
Zerial, M .
NATURE, 2005, 436 (7047) :128-133
[35]   Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic [J].
Pelkmans, L ;
Bürli, T ;
Zerial, M ;
Helenius, A .
CELL, 2004, 118 (06) :767-780
[36]   Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae [J].
Pelkmans, L ;
Püntener, D ;
Helenius, A .
SCIENCE, 2002, 296 (5567) :535-539
[37]   Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER [J].
Pelkmans, L ;
Kartenbeck, J ;
Helenius, A .
NATURE CELL BIOLOGY, 2001, 3 (05) :473-483
[38]   Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis [J].
Pelkmans, L ;
Fava, E ;
Grabner, H ;
Hannus, M ;
Habermann, B ;
Krausz, E ;
Zerial, M .
NATURE, 2005, 436 (7047) :78-86
[39]   Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C-elegans [J].
Pellettieri, J ;
Reinke, V ;
Kim, SK ;
Seydoux, G .
DEVELOPMENTAL CELL, 2003, 5 (03) :451-462
[40]   Dynamic and regulated association of caveolin with lipid bodies: Modulation of lipid body motility and function by a dominant negative mutant [J].
Pol, A ;
Martin, S ;
Fernandez, MA ;
Ferguson, C ;
Carozzi, A ;
Luetterforst, R ;
Enrich, C ;
Parton, RG .
MOLECULAR BIOLOGY OF THE CELL, 2004, 15 (01) :99-110