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

被引:86
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
[1]   Calcium and the control of mammalian cortical granule exocytosis [J].
Abbott, AL ;
Ducibella, T .
FRONTIERS IN BIOSCIENCE, 2001, 6 :D792-D806
[2]   The caveolae membrane system [J].
Anderson, RGW .
ANNUAL REVIEW OF BIOCHEMISTRY, 1998, 67 :199-225
[3]   A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans [J].
Audhya, A ;
Hyndman, F ;
McLeod, IX ;
Maddox, AS ;
Yates, JR ;
Desai, A ;
Oegema, K .
JOURNAL OF CELL BIOLOGY, 2005, 171 (02) :267-279
[4]   The GGA proteins: Adaptors on the move [J].
Bonifacino, JS .
NATURE REVIEWS MOLECULAR CELL BIOLOGY, 2004, 5 (01) :23-32
[5]  
BRENNER S, 1974, GENETICS, V77, P71
[6]   Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization [J].
del Pozo, MA ;
Balasubramanian, N ;
Alderson, NB ;
Kiosses, WB ;
Grande-García, A ;
Anderson, RGW ;
Schwartz, MA .
NATURE CELL BIOLOGY, 2005, 7 (09) :901-U57
[7]   Localization and function of Arf family GTPases [J].
Donaldson, JG ;
Honda, A .
BIOCHEMICAL SOCIETY TRANSACTIONS, 2005, 33 :639-642
[8]   Multiple activities for Arf1 at the Golgi complex [J].
Donaldson, JG ;
Honda, A ;
Weigert, R .
BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR CELL RESEARCH, 2005, 1744 (03) :364-373
[9]   Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice [J].
Drab, M ;
Verkade, P ;
Elger, M ;
Kasper, M ;
Lohn, M ;
Lauterbach, B ;
Menne, J ;
Lindschau, C ;
Mende, F ;
Luft, FC ;
Schedl, A ;
Haller, H ;
Kurzchalia, TV .
SCIENCE, 2001, 293 (5539) :2449-2452
[10]   Mechanism of caveolin filament assembly [J].
Fernandez, I ;
Ying, YS ;
Albanesi, J ;
Anderson, RGW .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (17) :11193-11198