In the mouse, completion of oocyte maturation and the initiation of preimplantation development occur during transcriptional silence and depend on the presence and translation of stored mRNAs transcribed in the growing oocyte. The Spin gene has three transcripts, each with an identical open reading frame and a different 3′ untranslated region (UTR). (Beta)-galactosidase-tagged reporter transcripts containing each of the different Spin 3′UTRs were injected into oocytes and zygotes and (beta)-galactosidase activity was monitored. Results from these experiments suggest that differential polyadenylation and translation occurs at two critical points in the oocyte-to-embryo transition - upon oocyte maturation and fertilization - and is dependent on sequences in the 3′UTR. The stability and mobility shifts of ten other maternal transcripts were monitored by reprobing a northern blot of oocytes and embryos collected at 12 hour intervals after fertilization. Some are more stable than others and the upward mobility shift associated with polyadenylation correlates with the presence of cytoplasmic polyadenylation elements (CPEs) within about 120 nucleotides of the nuclear polyadenylation signal. A survey of the 3′ UTRs of expressed sequence tag clusters from a mouse 2-cell stage cDNA library indicates that about one third contain CPEs. We suggest that differential transcript stability and a translational control program can supply the diversity of protein products necessary for oocyte maturation and the initiation of development.

REFERENCES

Casanova
J.
,
Struhl
G.
(
1989
)
Localized surface activity of torso, a receptor tyrosine kinase, specifies terminal body pattern in Drosophila.
Genes Dev
3
,
2025
2038
Cibelli
J. B.
,
Stice
S. L.
,
Golueke
P. J.
,
Kane
J. J.
,
Jerry
J.
,
Blackwell
C.
,
Ponce de Leon
F. A.
,
Robl
J. M.
(
1998
)
Cloned transgenic calves produced from nonquiescent fetal fibroblasts.
Science
280
,
1256
1258
Diamond
R. H.
,
Cressman
D. E.
,
Laz
T. M.
,
Abrams
C. S.
,
Taub
R.
(
1994
)
PRL-1, a unique nuclear protein tyrosine phosphatase, affects cell growth.
Mol. Cell. Biol
14
,
3752
3762
Driever
W.
,
Nusslein-Volhard
C.
(
1988
)
A gradient of bicoid protein in Drosophila embryos.
Cell
54
,
83
93
Eppig
J. J.
,
Wigglesworth
K.
(
1994
)
Atypical maturation of oocytes of strain I/LnJ mice.
Human Reprod
9
,
1136
1142
Fox
C. A.
,
Sheets
M. D.
,
Wickens
M. P.
(
1989
)
Poly(A) addition during maturation of frog oocytes: distinct nuclear and cytoplasmic activities and regulation by the sequence UUUUUAU.
Genes Dev
3
,
2151
2162
Gavis
E. R.
,
Lehmann
R.
(
1994
)
Translational regulation of nanos by RNA localization.
Nature
369
,
315
318
Gebauer
F.
,
Xu
W.
,
Cooper
G. M.
,
Richter
J. D.
(
1994
)
Translational control by cytoplasmic polyadenylation of c- Mos mRNA is necessary for oocyte maturation in the mouse.
EMBO J
13
,
5712
5720
Heyer
B. S.
,
Warsowe
J.
,
Solter
D.
,
Knowles
B. B.
,
Ackerman
S. L.
(
1997
)
New member of the Snf1/AMPK kinase family, Melk, is expressed in the mouse egg and preimplantation embryo.
Mol. Reprod. Dev
47
,
148
156
Huarte
J.
,
Belin
D.
,
Vassalli
A.
,
Strickland
S.
,
Vassalli
J.-D.
(
1987
)
Meiotic maturation of mouse oocytes triggers the translation and polyadenylation of dormant tissue-type plasminogen activator mRNA.
Genes Dev
1
,
1201
1211
Hwang
S. Y.
,
Oh
B.
,
Johnson
K.
,
Solter
D.
,
Knowles
B. B.
(
1997
)
Maid: a maternally transcribed novel gene encoding a potential negative regulator of bHLH proteins in the mouse egg and zygote.
Dev. Dyn
209
,
217
226
Kuge
H.
,
Richter
J. D.
(
1995
)
Cytoplasmic 3poly(A) addition induces 5 cap ribose methylation: implications for translational control of maternal mRNA.
EMBO J
14
,
6301
6310
McGrew
L. L.
,
Dworkin-Rastl
E.
,
Dworkin
M. B.
,
Richter
J. D.
(
1989
)
Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element.
Genes Dev
3
,
803
815
McGrew
L. L.
,
Richter
J. D.
(
1990
)
Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: characterization of cis and trans elements and regulation by cyclin/MPF.
EMBO J
9
,
3743
3751
Mendez
R.
,
Hake
L. E.
,
Andresson
T.
,
Littlepage
L. E.
,
Ruderman
J. V.
,
Richter
J. D.
(
2000
)
Phosphorylation of CPE binding factor by Eg2 regulates translation of c- mos mRNA.
Nature
404
,
302
307
Mercer
J. F.
,
Wake
S. A.
(
1985
)
An analysis of the rate of metallothionein mRNA poly(A)-shortening using RNA blot hybridization.
Nucl. Acids Res
13
,
7929
7943
Newport
J.
,
Kirschner
M.
(
1982
)
A major developmental transition in early Xenopus embryos: 1. Characterization and timing of cellular changes at the midblastula stage.
Cell
30
,
675
686
Newport
J.
,
Kirschner
N.
(
1982
)
A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription.
Cell
30
,
687
696
Oh
B.
,
Hwang
S.-Y.
,
Solter
D.
,
Knowles
B. B.
(
1997
)
Spindlin, a major maternal transcript expressed on the mouse during the transition from oocyte-to-embryo.
Dev
124
,
493
503
Oh
B.
,
Hampl
A.
,
Eppig
J. J.
,
Solter
D.
,
Knowles
B. B.
(
1998
)
SPIN, a substrate in the MAP kinase pathway in mouse oocytes.
Mol. Reprod. Dev
50
,
240
249
Rickles
R. J.
,
Darrow
A. L.
,
Strickland
S.
(
1988
)
Molecular cloning of complementary DNA to mouse tissue plasminogen activator mRNA and its expression during F9 teratocarcinoma cell differentiation.
J. Biol. Chem
263
,
1563
1569
Rosenthal
E. T.
,
Ruderman
J. V.
(
1987
)
Widespread changes in the translation and adenylation of maternal messenger RNAs following fertilization of Spisula oocytes.
Dev. Biol
121
,
237
246
Rothstein
J. L.
,
Johnson
D. K.
,
DeLoia
J. A.
,
Skowronski
J.
,
Solter
D.
,
Knowles
B. B.
(
1992
)
Gene expression during preimplantation mouse development.
Genes Dev
6
,
1190
1201
Schultz
R. M.
(
1993
)
Regulation of zygotic gene activation in the mouse.
BioEssays
15
,
531
538
Simon
R.
,
Tassan
J. P.
,
Richter
J. D.
(
1992
)
Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element.
Genes Dev
6
,
2580
2591
Simon
R.
,
Richter
J. D.
(
1994
)
Further analysis of cytoplasmic polyadenylation in Xenopus embryos and identification of embryoniccytoplasmic polyadenylation element-binding proteins.
Mol. Cell. Biol
14
,
7867
7875
Stutz
A.
,
Conne
B.
,
Huarte
J.
,
Gubler
P.
,
Volkel
V.
,
Flandin
P.
,
Vassalli
J. D.
(
1998
)
Masking, unmasking, and regulated polyadenylation cooperate in the translational control of a dormant mRNA in mouse oocytes.
Genes Dev
12
,
2535
2548
Tay
J.
,
Hodgman
R.
,
Richter
J. D.
(
2000
)
The control of cyclin B1 in mRNA translation during mouse oocyte maturation.
Dev. Biol
221
,
1
9
Telford
N. A.
,
Watson
A. J.
,
Schultz
G. A.
(
1990
)
Transition from maternal to embryonic control in early mammalian development: a comparison of several species.
Mol. Reprod. Dev
26
,
90
100
Vassalli
J. D.
,
Huarte
J.
,
Belin
D.
,
Gubler
P.
,
Vassalli
A.
,
O'Connell
M. L.
,
Parton
L. A.
,
Rickles
R. J.
,
Strickland
S.
(
1989
)
Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes.
Genes Dev
3
,
2163
2171
Verrotti
A. C.
,
Thompson
S. R.
,
Wreden
C.
,
Strickland
S.
,
Wickens
M.
(
1996
)
Evolutionary conservation of sequence elements controlling cytoplasmic polyadenylation.
Proc. Natl. Acad. Sci. USA
93
,
9027
9032
Wakayama
T.
,
Perry
A. C.
,
Zuccotti
M.
,
Johnson
K. R.
,
Yanagimachi
R.
(
1998
)
Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei.
Nature
394
,
369
374
Wassarman
P. M.
,
Schultz
R. M.
,
Letourneau
G. E.
,
LaMarca
M. J.
,
Josefowicz
W. J.
,
Bleil
J.D.
(
1979
)
Meiotic maturation of mouse oocytes in vitro.
Adv. Exp. Med. Biol
112
,
251
268
West
M. F.
,
Verrotti
A. C.
,
Salles
F. J.
,
Tsirka
S. E.
,
Strickland
S.
(
1996
)
Isolation and characterization of two novel cytoplasmically polyadenylated, oocyte-specific, mouse maternal RNAs.
Dev. Biol
175
,
132
141
Wilmut
I.
,
Schnieke
A. E.
,
McWhir
J.
,
Kind
A. J.
,
Campbell
K. H. S.
(
1997
)
Viable offspring derived from fetal and adult mammalian cells.
Nature
385
,
810
813
Wilt
F. H.
(
1973
)
Polyadenylation of maternal RNA of sea urchin eggs after fertilization.
Proc. Natl. Acad. Sci. USA
70
,
2345
2349
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