Poly(A) removal during oocyte maturation: a default reaction selectively prevented by specific sequences in the 3' UTR of certain maternal mRNAs.

Certain maternal mRNAs lose their poly(A) tails during early development and concomitantly become translationally inactive. In this report we analyze the mechanism of poly(A) removal during frog oocyte maturation by injecting short synthetic RNAs. We demonstrate that removal of poly(A) during oocyte maturation is a default reaction: In the absence of any specific sequence information, poly(A) is removed. However, poly(A) removal can be prevented by specific sequences in the 3'-untranslated regions of certain maternal mRNAs. These sequences are also required for poly(A) addition during oocyte maturation and include AAUAAA and a nearby U-rich element. Mutations in either AAUAAA or the U-rich element cause loss of poly(A) and not merely a failure to extend the poly(A) tail. We infer that poly(A) addition is required to escape poly(A) loss. The enzyme that removes the poly(A) during oocyte maturation appears to be a 3'----5' nuclease that prefers a 3'-terminal poly(A) segment. We discuss possible mechanisms by which poly(A) addition might circumvent default poly(A) removal and consider whether poly(A) removal is also a default reaction in somatic cells. Finally, we consider the possible implications of our results for the selectivity of poly(A) addition and removal, and for translational regulation during early development.