Coordinate Control of Translation and Localization of Vg1 MRNA in Xenopus Oocytes

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2000 Nov 23

PMID 11087864

Citations 9

Authors

J E Wilhelm

R D Vale

R S Hegde

Affiliations

Soon will be listed here.

Abstract

Vg1, a member of the transforming growth factor-beta family involved in mesoderm induction, is translated subsequent to the localization of its mRNA to the vegetal pole of Xenopus oocytes. Whereas the localization of Vg1 mRNA is known to be directed by the 3' untranslated region (UTR), the basis of its translational regulation is unknown. We show here that the 3' UTR of Vg1 causes translational repression of two different reporter mRNAs in Xenopus oocytes. A 350-nucleotide region of the 3' UTR, which is distinct from the localization element, is necessary and sufficient for mediating translational repression and specifically binds to a 38-kDa polypeptide. The translational repression activity is found throughout the oocyte and at all stages of oogenesis. These results suggest that factors colocalized with Vg1 mRNA at the vegetal pole relieve translational repression to allow expression of Vg1 protein.

Citing Articles

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References

Smibert C, Lie Y, Shillinglaw W, Henzel W, Macdonald P . Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA. 1999; 5(12):1535-47. PMC: 1369876. DOI: 10.1017/s1355838299991392. View

Cote C, Gautreau D, Denegre J, Kress T, TERRY N, Mowry K . A Xenopus protein related to hnRNP I has a role in cytoplasmic RNA localization. Mol Cell. 1999; 4(3):431-7. DOI: 10.1016/s1097-2765(00)80345-7. View

Rebagliati M, Weeks D, Harvey R, Melton D . Identification and cloning of localized maternal RNAs from Xenopus eggs. Cell. 1985; 42(3):769-77. DOI: 10.1016/0092-8674(85)90273-9. View

Melton D . Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes. Nature. 1987; 328(6125):80-2. DOI: 10.1038/328080a0. View

Berleth T, Burri M, Thoma G, Bopp D, Richstein S, Frigerio G . The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. EMBO J. 1988; 7(6):1749-56. PMC: 457163. DOI: 10.1002/j.1460-2075.1988.tb03004.x. View

Yisraeli J, Melton D . The material mRNA Vg1 is correctly localized following injection into Xenopus oocytes. Nature. 1988; 336(6199):592-5. DOI: 10.1038/336592a0. View

Andrews D, Lauffer L, Walter P, Lingappa V . Evidence for a two-step mechanism involved in assembly of functional signal recognition particle receptor. J Cell Biol. 1989; 108(3):797-810. PMC: 2115407. DOI: 10.1083/jcb.108.3.797. View

Dale L, Matthews G, Tabe L, Colman A . Developmental expression of the protein product of Vg1, a localized maternal mRNA in the frog Xenopus laevis. EMBO J. 1989; 8(4):1057-65. PMC: 400914. DOI: 10.1002/j.1460-2075.1989.tb03473.x. View

Yisraeli J, Sokol S, Melton D . A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. Development. 1990; 108(2):289-98. DOI: 10.1242/dev.108.2.289. View

10.

Kim-Ha J, Smith J, Macdonald P . oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell. 1991; 66(1):23-35. DOI: 10.1016/0092-8674(91)90136-m. View

11.

Ephrussi A, Dickinson L, Lehmann R . Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 1991; 66(1):37-50. DOI: 10.1016/0092-8674(91)90137-n. View

12.

Lehmann R, Nusslein-Volhard C . The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. Development. 1991; 112(3):679-91. DOI: 10.1242/dev.112.3.679. View

13.

Mowry K, Melton D . Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. Science. 1992; 255(5047):991-4. DOI: 10.1126/science.1546297. View

14.

Heasman J, Holwill S, Wylie C . Fertilization of cultured Xenopus oocytes and use in studies of maternally inherited molecules. Methods Cell Biol. 1991; 36:213-30. DOI: 10.1016/s0091-679x(08)60279-4. View

15.

Smith L, Xu W, Varnold R . Oogenesis and oocyte isolation. Methods Cell Biol. 1991; 36:45-60. DOI: 10.1016/s0091-679x(08)60272-1. View

16.

SCHWARTZ S, Aisenthal L, Elisha Z, Oberman F, Yisraeli J . A 69-kDa RNA-binding protein from Xenopus oocytes recognizes a common motif in two vegetally localized maternal mRNAs. Proc Natl Acad Sci U S A. 1992; 89(24):11895-9. PMC: 50664. DOI: 10.1073/pnas.89.24.11895. View

17.

Tannahill D, Melton D . Localized synthesis of the Vg1 protein during early Xenopus development. Development. 1989; 106(4):775-85. DOI: 10.1242/dev.106.4.775. View

18.

Kim-Ha J, Webster P, Smith J, Macdonald P . Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. Development. 1993; 119(1):169-78. DOI: 10.1242/dev.119.1.169. View

19.

Ostareck-Lederer A, Ostareck D, Standart N, Thiele B . Translation of 15-lipoxygenase mRNA is inhibited by a protein that binds to a repeated sequence in the 3' untranslated region. EMBO J. 1994; 13(6):1476-81. PMC: 394967. DOI: 10.1002/j.1460-2075.1994.tb06402.x. View

20.

Binder R, Horowitz J, Basilion J, Koeller D, Klausner R, Harford J . Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3' UTR and does not involve poly(A) tail shortening. EMBO J. 1994; 13(8):1969-80. PMC: 395039. DOI: 10.1002/j.1460-2075.1994.tb06466.x. View