Premature Translation of <i>oskar</i> in Oocytes Lacking the RNA-Binding Protein Bicaudal-C

Saffman, Emma E.; Styhler, Sylvia; Rother, Katherine; Li, Weihua; Richard, Stéphane; Lasko, Paul

doi:10.1128/mcb.18.8.4855

Cited by 98 publications

(82 citation statements)

References 50 publications

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“…Drosophila Bic-C has been shown to bind to poly(G) and poly(U) RNAs in pull-down experiments in vitro (Saffman et al 1998;Braddock et al 2002) and a similar preference in RNA binding has been reported for mouse Bic-C (Bouvrette et al 2008). While Bic-C proteins contain several GxxG motifs that are involved in nucleic acid binding in canonical KH domains (Braddock et al 2002), the KH domains of GLD-3 are degenerate in that none features the GxxG sequence (Fig.…”

Section: Rna-binding Properties Of the Gld-3 Kh Regionmentioning

confidence: 99%

Four KH domains of the C. elegans Bicaudal-C ortholog GLD-3 form a globular structural platform

Nakel¹,

Hartung²,

Bonneau³

et al. 2010

RNA

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Caenorhabditis elegans GLD-3 is a five K homology (KH) domain-containing protein involved in the translational control of germline-specific mRNAs during embryogenesis. GLD-3 interacts with the cytoplasmic poly(A)-polymerase GLD-2. The two proteins cooperate to recognize target mRNAs and convert them into a polyadenylated, translationally active state. We report the 2.8-Å -resolution crystal structure of a proteolytically stable fragment encompassing the KH2, KH3, KH4, and KH5 domains of C. elegans GLD-3. The structure reveals that the four tandem KH domains are organized into a globular structural unit. The domains are involved in extensive side-by-side interactions, similar to those observed in previous structures of dimeric KH domains, as well as head-to-toe interactions. Small-angle X-ray scattering reconstructions show that the N-terminal KH domain (KH1) forms a thumb-like protrusion on the KH2-KH5 unit. Although KH domains are putative RNA-binding modules, the KH region of GLD-3 is unable in isolation to cross-link RNA. Instead, the KH1 domain mediates the direct interaction with the poly(A)-polymerase GLD-2, pointing to a function of the KH region as a protein-protein interaction platform.

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Section: Rna-binding Properties Of the Gld-3 Kh Regionmentioning

confidence: 99%

Four KH domains of the C. elegans Bicaudal-C ortholog GLD-3 form a globular structural platform

Nakel¹,

Hartung²,

Bonneau³

et al. 2010

RNA

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“…For example, Bic-C mutant mice develop renal cysts, providing a model for polycystic kidney disease (Maisonneuve et al 2009;Tran et al 2010). In Drosophila, where Bic-C was first identified, Bic-C contributes to patterning of the early embryo by repressing specific maternal mRNAs, such as oskar (Saffman et al 1998;Chicoine et al 2007). However, in vertebrates the mechanisms of Bic-C action have not been identified nor have mRNA targets been identified systematically.…”

Section: Introductionmentioning

confidence: 99%

“…Bicaudal-C (Bic-C) RNA binding proteins have vital roles in vertebrate embryogenesis and also in adult tissues, including the kidney, heart, and pancreas (Saffman et al 1998;Chicoine et al 2007;Gamberi and Lasko 2012). For example, Bic-C mutant mice develop renal cysts, providing a model for polycystic kidney disease (Maisonneuve et al 2009;Tran et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Bicaudal-C spatially controls translation of vertebrate maternal mRNAs

Zhang

Cooke

Park

et al. 2013

RNA

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The Xenopus Cripto-1 protein is confined to the cells of the animal hemisphere during early embryogenesis where it regulates the formation of anterior structures. Cripto-1 protein accumulates only in animal cells because cripto-1 mRNA in cells of the vegetal hemisphere is translationally repressed. Here, we show that the RNA binding protein, Bicaudal-C (Bic-C), functioned directly in this vegetal cell-specific repression. While Bic-C protein is normally confined to vegetal cells, ectopic expression of Bic-C in animal cells repressed a cripto-1 mRNA reporter and associated with endogenous cripto-1 mRNA. Repression by Bic-C required its N-terminal domain, comprised of multiple KH motifs, for specific binding to relevant control elements within the cripto-1 mRNA and a functionally separable C-terminal translation repression domain. Bic-C-mediated repression required the 5 ′ CAP and translation initiation factors, but not a poly(A) tail or the conserved SAM domain within Bic-C. Bic-C-directed immunoprecipitation followed by deep sequencing of associated mRNAs identified multiple Bic-C-regulated mRNA targets, including cripto-1 mRNA, providing new insights and tools for understanding the role of Bic-C in vertebrate development.

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“…Drosophila has homologs of some of these proteins, and Drosophila's CPEB (named Orb) has been shown to interact with Bic-C, the Drosophila homolog of GLD-3 (Castagnetti and Ephrussi 2003). Bic-C, which is present in oocytes and early embryos like wisp, is required for anteriorposterior patterning during oogenesis (Mahone et al 1995;Saffman et al 1998). In the germline, Bic-C has been recently reported to regulate the expression of specific mRNAs by participating in control of their poly(A) tail length (Chicoine et al 2007).…”

mentioning

confidence: 99%

Wispy, the Drosophila Homolog of GLD-2, Is Required During Oogenesis and Egg Activation

et al. 2008

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Egg activation is the process that modifies mature, arrested oocytes so that embryo development can proceed. One key aspect of egg activation is the cytoplasmic polyadenylation of certain maternal mRNAs to permit or enhance their translation. wispy (wisp) maternal-effect mutations in Drosophila block development during the egg-to-embryo transition. We show here that the wisp gene encodes a member of the GLD-2 family of cytoplasmic poly(A) polymerases (PAPs). The WISP protein is required for poly(A) tail elongation of bicoid, Toll, and torso mRNAs upon egg activation. In Drosophila, WISP and Smaug (SMG) have previously been reported to be required to trigger the destabilization of maternal mRNAs during egg activation. SMG is the major regulator of this activity. We report here that SMG is still translated in activated eggs from wisp mutant mothers, indicating that WISP does not regulate mRNA stability by controlling the translation of smg mRNA. We have also analyzed in detail the very early developmental arrest associated with wisp mutations. Pronuclear migration does not occur in activated eggs laid by wisp mutant females. Finally, we find that WISP function is also needed during oogenesis to regulate the poly(A) tail length of dmos during oocyte maturation and to maintain a high level of active (phospho-) mitogen-activated protein kinases (MAPKs).

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Premature Translation of oskar in Oocytes Lacking the RNA-Binding Protein Bicaudal-C

Cited by 98 publications

References 50 publications

Four KH domains of the C. elegans Bicaudal-C ortholog GLD-3 form a globular structural platform

Four KH domains of the C. elegans Bicaudal-C ortholog GLD-3 form a globular structural platform

Bicaudal-C spatially controls translation of vertebrate maternal mRNAs

Wispy, the Drosophila Homolog of GLD-2, Is Required During Oogenesis and Egg Activation

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