Changes in bicoid mRNA anchoring highlight conserved mechanisms during the oocyte-to-embryo transition

被引:53
作者
Weil, Timothy T. [1 ]
Parton, Richard [2 ]
Davis, Ilan [2 ]
Gavis, Elizabeth R. [1 ]
机构
[1] Princeton Univ, Dept Mol Biol, Princeton, NJ 08544 USA
[2] Univ Edinburgh, Wellcome Trust Ctr Cell Biol, Edinburgh EH9 3JR, Midlothian, Scotland
基金
英国医学研究理事会; 英国惠康基金;
关键词
D O I
10.1016/j.cub.2008.06.046
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Intracellular mRNA localization directs protein synthesis to particular subcellular domains to establish embryonic polarity in a variety of organisms. In Drosophila, bicoid (bcd) mRNA is prelocalized at the oocyte anterior. After fertilization, translation of this RNA produces a Bcd protein gradient that determines anterior cell fates [1, 2]. Analysis of bcd mRNA during late stages of oogenesis suggested a model for steady-state bcd localization by continual active transport [3). However, this mechanism cannot explain maintenance of bcd localization throughout the end of oogenesis, when microtubules; disassemble in p reparation for embryogenesis [4, 5], or retention of bcd at the anterior in mature oocytes, which can remain dormant for weeks before fertilization [6]. Here, we elucidate the path and mechanism of sustained bcd mRNA transport by direct observation of bcd RNA particle translocation in living oocytes. We show that bcd mRNA shifts from continuous active transport to stable actin-dependent anchoring at the end of oogenesis. Egg activation triggers bcd release from the anterior cortex for proper deployment in the embryo, probably through reorganization of the actin cytoskeleton. These findings uncover a surprising parallel between flies and frogs, as cortically tethered Xenopus Vg1 mRNA undergoes a similar redistribution during oocyte maturation [7]. Our results thus highlight a conserved mechanism for regulating mRNA anchoring and redeployment during the oocyte-to-embryo transition.
引用
收藏
页码:1055 / 1061
页数:7
相关论文
共 31 条
[1]   THE ROLE OF LOCALIZATION OF BICOID RNA IN ORGANIZING THE ANTERIOR PATTERN OF THE DROSOPHILA EMBRYO [J].
BERLETH, T ;
BURRI, M ;
THOMA, G ;
BOPP, D ;
RICHSTEIN, S ;
FRIGERIO, G ;
NOLL, M ;
NUSSLEINVOLHARD, C .
EMBO JOURNAL, 1988, 7 (06) :1749-1756
[2]   Vg1 is an essential signaling molecule in Xenopus development [J].
Birsoy, B ;
Kofron, M ;
Schaible, K ;
Wylie, C ;
Heasman, J .
DEVELOPMENT, 2006, 133 (01) :15-20
[3]   Spatial regulation of nanos is required for its function in dendrite morphogenesis [J].
Brechbiel, Jillian L. ;
Gavis, Elizabeth R. .
CURRENT BIOLOGY, 2008, 18 (10) :745-750
[4]   Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family [J].
Chu, T ;
Henrion, G ;
Haegeli, V ;
Strickland, S .
GENESIS, 2001, 29 (03) :141-152
[5]   A Dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte [J].
Clark, Alejandra ;
Meignin, Carine ;
Davis, Ilan .
DEVELOPMENT, 2007, 134 (10) :1955-1965
[6]   THE BICOID PROTEIN DETERMINES POSITION IN THE DROSOPHILA EMBRYO IN A CONCENTRATION-DEPENDENT MANNER [J].
DRIEVER, W ;
NUSSLEINVOLHARD, C .
CELL, 1988, 54 (01) :95-104
[7]   Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila [J].
Forrest, KM ;
Gavis, ER .
CURRENT BIOLOGY, 2003, 13 (14) :1159-1168
[8]  
Gavis ER, 2007, TRANSLATIONAL CONTRO, V48, P687
[9]   Force-induced bidirectional stepping of cytoplasmic dynein [J].
Gennerich, Arne ;
Carter, Andrew P. ;
Reck-Peterson, Samara L. ;
Vale, Ronald D. .
CELL, 2007, 131 (05) :952-965
[10]  
Gepner J, 1996, GENETICS, V142, P865