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We have examined the relationship between the newly synthesized mRNA that enters polysomes in sea urchin embryos and the messengerlike RNA that enters the pool of ribosome-free ribonucleoprotein particles (free RNPs or informosomes). Although the RNA in the free RNPs turns over 25% more rapidly than in the polysomes, labeling kinetics indicate that the RNA containing poly(A) [poly(A)(+)RNA] and the RNA not containing poly(A) [poly(A)(-)RNA] within each cytoplasmic compartment have very similar half-lives. The poly(A)(+)RNA from both free RNPs and polysomes binds ribosomes almost equally well in a reticulocyte lysate, and this binding is sensitive to inhibitors of initiation. The poly(A)(-)RNA from polysomes initiates as well as poly(A)(+)RNA; however, poly(A)(-)RNA from free RNPs is only half as efficient in binding to ribosomes, and by this criterion is only 50% mRNA. We have also examined the size and dynamics of shortening of the poly(A) tails of poly(A)(+)RNA from free RNPs and polysomes. Pulse-labeled poly(A) from both free RNPs and polysomes is about 180 nucleotides in length. Poly(A) shortening is very rapid in polysomes; steady-state labeled polysomal RNA is largely devoid of the 180-nucleotide-long poly(A) segments. Poly(A) shortening in free RNPs is slower; half of the poly(A) derived from steady-state free RNPs is still 180 nucleotides long. Despite this difference in the rates of poly(A) shortening, polysomes and free RNPs have very similar half-lives. There is, then, no obvious relationship between poly(A) shortening and turnover of mRNA in these embryos. The data are interpreted to mean that poly(A)(+)RNA from free RNPs is enriched for a class of mRNA that initiates less frequently in vivo than the bulk of the cellular mRNA.
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