Previous Article | Next Article 
Molecular and Cellular Biology, March 1999, p. 1990-1999, Vol. 19, No. 3
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The Mitogen-Activated Protein Kinase Signaling
Pathway Stimulates Mos mRNA Cytoplasmic Polyadenylation during
Xenopus Oocyte Maturation
Emily L.
Howard,1,2
Amanda
Charlesworth,1
Joseph
Welk,1 and
Angus M.
MacNicol1,2,3,*
Department of
Medicine1 and Committees on
Developmental Biology2 and Cancer
Biology,3 The University of Chicago,
Chicago, Illinois 60637
Received 2 September 1998/Returned for modification 19 October
1998/Accepted 17 November 1998
The Mos protein kinase is a key regulator of vertebrate oocyte
maturation. Oocyte-specific Mos protein expression is subject to
translational control. In the frog Xenopus, the translation of Mos protein requires the progesterone-induced polyadenylation of the
maternal Mos mRNA, which is present in the oocyte cytoplasm. Both the
Xenopus p42 mitogen-activated protein kinase (MAPK) and maturation-promoting factor (MPF) signaling pathways have been proposed
to mediate progesterone-stimulated oocyte maturation. In this study, we
have determined the relative contributions of the MAPK and MPF
signaling pathways to Mos mRNA polyadenylation. We report that
progesterone-induced Mos mRNA polyadenylation was attenuated in oocytes
expressing the MAPK phosphatase rVH6. Moreover, inhibition of MAPK
signaling blocked progesterone-induced Mos protein accumulation.
Activation of the MAPK pathway by injection of RNA encoding Mos was
sufficient to induce both the polyadenylation of synthetic Mos mRNA
substrates and the accumulation of endogenous Mos protein in the
absence of MPF signaling. Activation of MPF, by injection of cyclin B1
RNA or purified cyclin B1 protein, also induced both Mos protein
accumulation and Mos mRNA polyadenylation. However, this action of MPF
required MAPK activity. By contrast, the cytoplasmic polyadenylation of
maternal cyclin B1 mRNA was stimulated by MPF in a MAPK-independent
manner, thus revealing a differential regulation of maternal mRNA
polyadenylation by the MAPK and MPF signaling pathways. We propose that
MAPK-stimulated Mos mRNA cytoplasmic polyadenylation is a key component
of the positive-feedback loop, which contributes to the all-or-none
process of oocyte maturation.
*
Corresponding author. Mailing address: Department of
Medicine, MC 6088, The University of Chicago, 5841 S. Maryland Ave., Chicago, IL 60637. Phone: (773) 702 2676. Fax: (773) 702 2681. E-mail: amacnico{at}medicine.bsd.uchicago.edu.
Molecular and Cellular Biology, March 1999, p. 1990-1999, Vol. 19, No. 3
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Liang, C.-G., Su, Y.-Q., Fan, H.-Y., Schatten, H., Sun, Q.-Y.
(2007). Mechanisms Regulating Oocyte Meiotic Resumption: Roles of Mitogen-Activated Protein Kinase. Mol. Endocrinol.
21: 2037-2055
[Abstract]
[Full Text]
-
Keady, B. T., Kuo, P., Martinez, S. E., Yuan, L., Hake, L. E.
(2007). MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J. Cell Sci.
120: 1093-1103
[Abstract]
[Full Text]
-
Rasar, M., DeFranco, D. B., Hammes, S. R.
(2006). Paxillin Regulates Steroid-triggered Meiotic Resumption in Oocytes by Enhancing an All-or-None Positive Feedback Kinase Loop. J. Biol. Chem.
281: 39455-39464
[Abstract]
[Full Text]
-
Soundararajan, R., Zhang, T. T., Wang, J., Vandewalle, A., Pearce, D.
(2005). A Novel Role for Glucocorticoid-induced Leucine Zipper Protein in Epithelial Sodium Channel-mediated Sodium Transport. J. Biol. Chem.
280: 39970-39981
[Abstract]
[Full Text]
-
Martinez, S. E., Yuan, L., Lacza, C., Ransom, H., Mahon, G. M., Whitehead, I. P., Hake, L. E.
(2005). XGef Mediates Early CPEB Phosphorylation during Xenopus Oocyte Meiotic Maturation. Mol. Biol. Cell
16: 1152-1164
[Abstract]
[Full Text]
-
Charlesworth, A., Cox, L. L., MacNicol, A. M.
(2004). Cytoplasmic Polyadenylation Element (CPE)- and CPE-binding Protein (CPEB)-independent Mechanisms Regulate Early Class Maternal mRNA Translational Activation in Xenopus Oocytes. J. Biol. Chem.
279: 17650-17659
[Abstract]
[Full Text]
-
Sun, L., Machaca, K.
(2004). Ca2+cyt negatively regulates the initiation of oocyte maturation. JCB
165: 63-75
[Abstract]
[Full Text]
-
Francois, P., Hakim, V.
(2004). Design of genetic networks with specified functions by evolution in silico. Proc. Natl. Acad. Sci. USA
101: 580-585
[Abstract]
[Full Text]
-
Baert, F., Bodart, J.-F., Bocquet-Muchembled, B., Lescuyer-Rousseau, A., Vilain, J.-P.
(2003). Xp42Mpk1 Activation Is Not Required for Germinal Vescicle Breakdown but for Raf Complete Phosphorylation in Insulin-stimulated Xenopus Oocytes. J. Biol. Chem.
278: 49714-49720
[Abstract]
[Full Text]
-
Schmitt, A., Nebreda, A. R.
(2002). Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A. Proc. Natl. Acad. Sci. USA
99: 4361-4366
[Abstract]
[Full Text]
-
Lazar, S., Galiani, D., Dekel, N.
(2002). cAMP-Dependent PKA Negatively Regulates Polyadenylation of c-mos mRNA in Rat Oocytes. Mol. Endocrinol.
16: 331-341
[Abstract]
[Full Text]
-
Peter, M., Labbe, J.-C., Doree, M., Mandart, E.
(2002). A new role for Mos in Xenopus oocyte maturation: targeting Myt1 independently of MAPK. Development
129: 2129-2139
[Abstract]
[Full Text]
-
Palancade, B., Bellier, S., Almouzni, G., Bensaude, O.
(2001). Incomplete RNA polymerase II phosphorylation in Xenopus laevis early embryos. J. Cell Sci.
114: 2483-2489
[Abstract]
[Full Text]
-
Abrieu, A, Doree, M, Fisher, D
(2001). The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J. Cell Sci.
114: 257-267
[Abstract]
-
MacNicol, M. C., Muslin, A. J., MacNicol, A. M.
(2000). Disruption of the 14-3-3 Binding Site within the B-Raf Kinase Domain Uncouples Catalytic Activity from PC12 Cell Differentiation. J. Biol. Chem.
275: 3803-3809
[Abstract]
[Full Text]
-
Gavin, A.-C., Ainle, A. N., Chierici, E., Jones, M., Nebreda, A. R.
(1999). A p90rsk Mutant Constitutively Interacting with MAP Kinase Uncouples MAP Kinase from p34cdc2/Cyclin B Activation in Xenopus Oocytes. Mol. Biol. Cell
10: 2971-2986
[Abstract]
[Full Text]
-
Nakahata, S., Katsu, Y., Mita, K., Inoue, K., Nagahama, Y., Yamashita, M.
(2001). Biochemical Identification of Xenopus Pumilio as a Sequence-specific Cyclin B1 mRNA-binding Protein That Physically Interacts with a Nanos Homolog, Xcat-2, and a Cytoplasmic Polyadenylation Element-binding Protein. J. Biol. Chem.
276: 20945-20953
[Abstract]
[Full Text]
-
Schmitt, A., Nebreda, A. R.
(2002). Inhibition of Xenopus oocyte meiotic maturation by catalytically inactive protein kinase A. Proc. Natl. Acad. Sci. USA
99: 4361-4366
[Abstract]
[Full Text]
-
Machaca, K., Haun, S.
(2002). Induction of maturation-promoting factor during Xenopus oocyte maturation uncouples Ca2+ store depletion from store-operated Ca2+ entry. JCB
156: 75-86
[Abstract]
[Full Text]
-
Sohaskey, M. L., Ferrell, J. E. Jr.
(2002). Activation of p42 Mitogen-activated Protein Kinase (MAPK), but not c-Jun NH2-Terminal Kinase, Induces Phosphorylation and Stabilization of MAPK Phosphatase XCL100 in Xenopus Oocytes. Mol. Biol. Cell
13: 454-468
[Abstract]
[Full Text]