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J. Biol. Chem., Vol. 276, Issue 45, 41810-41816, November 9, 2001
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From the Department of Biochemistry, College of Agriculture and
Life Sciences, University of Wisconsin, Madison, Wisconsin 53706
Translational activation
in oocytes and embryos is often regulated via increases in poly(A)
length. Cleavage and polyadenylation specificity factor (CPSF),
cytoplasmic polyadenylation element binding protein (CPEB), and poly(A)
polymerase (PAP) have each been implicated in cytoplasmic
polyadenylation in Xenopus laevis oocytes. Cytoplasmic
polyadenylation activity first appears in vertebrate oocytes during
meiotic maturation. Data presented here shows that complexes containing
both CPSF and CPEB are present in extracts of X. laevis
oocytes prepared before or after meiotic maturation. Assessment of a
variety of RNA sequences as polyadenylation substrates indicates that
the sequence specificity of polyadenylation in egg extracts is
comparable to that observed with highly purified mammalian CPSF and
recombinant PAP. The two in vitro systems exhibit a
sequence specificity that is similar, but not identical, to that
observed in vivo, as assessed by injection of the same RNAs into the oocyte. These findings imply that CPSFs intrinsic RNA sequence
preferences are sufficient to account for the specificity of
cytoplasmic polyadenylation of some mRNAs. We discuss the
hypothesis that CPSF is required for all polyadenylation reactions, but
that the polyadenylation of some mRNAs may require additional
factors such as CPEB. To test the consequences of PAP binding to
mRNAs in vivo, PAP was tethered to a reporter mRNA
in resting oocytes using MS2 coat protein. Tethered PAP catalyzed
polyadenylation and stimulated translation ~40-fold; stimulation was
exclusively cis-acting, but was independent of a CPE and
AAUAAA. Both polyadenylation and translational stimulation required
PAPs catalytic core, but did not require the putative CPSF interaction
domain of PAP. These results demonstrate that premature recruitment of
PAP can cause precocious polyadenylation and translational stimulation
in the resting oocyte, and can be interpreted to suggest that the role of other factors is to deliver PAP to the mRNA.
Poly(A) Polymerase and the Regulation of Cytoplasmic
Polyadenylation*
,
*
This work was supported by National Institutes of Health
Grant RO1 GM31892 (to M. W.), a University of Wisconsin Molecular Biosciences Training Grant Predoctoral Fellowship and EMBO Long Term
Fellowship (to K. S. D.), and by the Medical Research Council (to N. K. G.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Current address: Dept. of Neuroscience, University of Edinburgh,
Edinburgh, Scotland EH9 3JQ, United Kingdom.
§
Current address: Dept. of Microbiology and Immunology, Stanford
University School of Medicine, Stanford, CA 94305.
¶
MRC Human Genetics Unit, Western General Hospital, Edinburgh,
Scotland EH4 2XU, United Kingdom.
To whom correspondence should be addressed. Tel.:
608-262-8007; Fax: 608-262-9108; E-mail:
wickens@biochem.wisc.edu.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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