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

Abstract

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).

Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2

“…GLD-2 was identified as a regulatory cytoplasmic poly(A) polymerase that controls germline progression through meiosis in C. elegans and Schizosaccharomyces pombe (Read et al 2002;Saitoh et al 2002;Wang et al 2002). Recently, it was reported that in Drosophila a GLD-2 homolog is required for long-term memory (Kwak et al 2008) and oogenesis (Cui et al 2008). Mammalian GLD-2 is expressed in many tissues and localizes in both the nucleus and cytoplasm (Nakanishi et al 2006).…”

Regulation of Cyclin A protein in meiosis and early embryogenesis

“…The poly(A) tail of cyclin A mRNA is short during prophase I arrest, and its lengthening correlates with appearance of the protein at oocyte maturation. It remains to be determined how this polyadenylation is controlled, but a likely possibility is that it may involve the GLD2 poly(A) polymerase shown to polyadenylate other mRNAs at maturation (2,33). The poly(A) tail is further increased at egg activation in a mechanism that requires active PNG kinase, and this may contribute to efficient translation of Cyclin A during early embryogenesis.…”

Translational regulation of the cell cycle: when, where, how and why?

“…Translation of Cyclin B also is promoted by Drosophila CPEB, called ORB ( figure 2c). In addition, a GLD-2 homologue is required at maturation for polyadenylation and translation of many proteins, including the Drosophila orthologue of Mos and a meiosis-specific activator of the APC/C called Cortex [42,101,102].…”