Regulation of the mRNAs Encoding Proteins of the BMP Signaling Pathway during the Maternal Stages of Xenopus Development

Abstract

Activation of the Xenopus bone morphogenetic protein (BMP) pathway is coincident with the onset of zygotic transcription but requires maternal signaling proteins. The mechanisms controlling the translation of mRNAs that encode proteins of the BMP pathway were investigated by using polysome association as an assay for translational activity. Our results indicate that five different mRNAs encoding proteins of the BMP pathway were translationally regulated during Xenopus development. These mRNAs were either not associated or inefficiently associated with polysomes in oocytes, and each was recruited to polysomes at a different developmental stage. The Smad1 and ALK-2 mRNAs were recruited to polysomes during oocyte maturation, whereas the BMP-7 and XSTK9 mRNAs were recruited during the early stages of embryogenesis. The ALK-3 mRNA was not efficiently associated with polysomes during any maternal stage of development and was efficiently recruited to polysomes only after the onset of zygotic transcription. In general, for all stages except oocytes, polysome recruitment was associated with the presence of a 3′ poly(A) tail. However, there was not an obvious correlation between the absolute length of poly(A) and the efficiency of polysome recruitment, indicating that the relationship between poly(A) tail length and translation during early frog embryogenesis is complex. We further focused on the BMP-7 mRNA and demonstrated that sequence elements within the 3′UTR were necessary for recruitment of the BMP-7 mRNA to polysomes and sufficient to direct the addition of poly(A) and activate translation of a reporter during embryogenesis. Interestingly, the BMP-7 mRNA lacks the previously defined eCPE sequences proposed to direct poly(A) addition and translational activation during embryogenesis. The implications of our findings for translational regulation of maternal mRNAs during embryogenesis and for the activation of the BMP pathway are discussed.