P-Body Loss Is Concomitant with Formation of a Messenger RNA Storage Domain in Mouse Oocytes

被引:118
作者
Flemr, Matyas [1 ]
Ma, Jun [2 ]
Schultz, Richard M. [2 ]
Svoboda, Petr [1 ]
机构
[1] Acad Sci Czech Republ, Inst Mol Genet, CR-14220 Prague 4, Czech Republic
[2] Univ Penn, Dept Biol, Philadelphia, PA 19104 USA
关键词
DDX6; gene regulation; maternal mRNA; miRNA; oocyte; oocyte development; P-body; RNA granule; YBX2; PROCESSING BODIES; TRANSLATIONAL CONTROL; BINDING PROTEIN; EXPRESSION; MSY2; GENE; ARGONAUTE; COMPONENT; ROLES; GW182;
D O I
10.1095/biolreprod.109.082057
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
In mammalian somatic cells, several pathways that converge on deadenylation, decapping, and 5'-3' degradation are found in cytoplasmic foci known as P-bodies. Because controlled mRNA stability is essential for oocyte-to-zygote transition, we examined the dynamics of P-body components in mouse oocytes. We report that oocyte growth is accompanied by loss of P-bodies and a subcortical accumulation of several RNA-binding proteins, including DDX6, CPEB, YBX2 (MSY2), and the exon junction complex. These proteins form transient RNA-containing aggregates in fully grown oocytes with a surrounded nucleolus chromatin configuration. These aggregates disperse during oocyte maturation, consistent with recruitment of maternal mRNAs that occurs during this time. In contrast, levels of DCP1A are low during oocyte growth, and DCP1A does not colocalize with DDX6 in the subcortical aggregates. The amount of DCP1A markedly increases during meiosis, which correlates with the first wave of destabilization of maternal mRNAs. We propose that the cortex of growing oocytes serves as an mRNA storage compartment, which contains a novel type of RNA granule related to P-bodies.
引用
收藏
页码:1008 / 1017
页数:10
相关论文
共 46 条
[21]   Expression of rck/p54, a DEAD-box RNA helicase, in gametogenesis and early embryogenesis of mice [J].
Matsumoto, K ;
Kwon, OY ;
Kim, H ;
Akao, Y .
DEVELOPMENTAL DYNAMICS, 2005, 233 (03) :1149-1156
[22]   Primordial germ cells in the mouse [J].
McLaren, A .
DEVELOPMENTAL BIOLOGY, 2003, 262 (01) :1-15
[23]   Critical roles for Dicer in the female germline [J].
Murchison, Elizabeth P. ;
Stein, Paula ;
Xuan, Zhenyu ;
Pan, Hua ;
Zhang, Michael Q. ;
Schultz, Richard M. ;
Hannon, Gregory J. .
GENES & DEVELOPMENT, 2007, 21 (06) :682-693
[24]   Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development [J].
Noble, Scott L. ;
Allen, Brittany L. ;
Goh, Lai Kuan ;
Nordick, Kristen ;
Evans, Thomas C. .
JOURNAL OF CELL BIOLOGY, 2008, 182 (03) :559-572
[25]   P bodies and the control of mRNA translation and degradation [J].
Parker, Roy ;
Sheth, Ujwal .
MOLECULAR CELL, 2007, 25 (05) :635-646
[26]   Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body [J].
Pepling, Melissa E. ;
Wilhelm, James E. ;
O'Hara, Ashley L. ;
Gephardt, Grant W. ;
Spradling, Allan C. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (01) :187-192
[27]   Translational control by cytoplasmic polyadenylation in Xenopus oocytes [J].
Radford, Helois E. ;
Meijer, Hedda A. ;
de Moor, Comelia H. .
BIOCHIMICA ET BIOPHYSICA ACTA-GENE REGULATORY MECHANISMS, 2008, 1779 (04) :217-229
[28]   CGH-1 and the control of maternal mRNAs [J].
Rajyaguru, Purusharth ;
Parker, Roy .
TRENDS IN CELL BIOLOGY, 2009, 19 (01) :24-28
[29]   CPEB: a life in translation [J].
Richter, Joel D. .
TRENDS IN BIOCHEMICAL SCIENCES, 2007, 32 (06) :279-285
[30]   Processing bodies are not required for mammalian nonsense-mediated mRNA decay [J].
Stalder, Lukas ;
Muehlemann, Oliver .
RNA, 2009, 15 (07) :1265-1273