The Xenopus ELAV Protein ElrB Represses Vg1 MRNA Translation During Oogenesis

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2005 Oct 4

PMID 16199879

Citations 22

Authors

Lucy J Colegrove-Otero

Agathe Devaux

Nancy Standart

Affiliations

Soon will be listed here.

Abstract

Xenopus laevis Vg1 mRNA undergoes both localization and translational control during oogenesis. We previously characterized a 250-nucleotide AU-rich element, the Vg1 translation element (VTE), in the 3'-untranslated region (UTR) of this mRNA that is responsible for the translational repression. UV-cross-linking and immunoprecipitation experiments, described here, revealed that the known AU-rich element binding proteins, ElrA and ElrB, and TIA-1 and TIAR interact with the VTE. The levels of these proteins during oogenesis are most consistent with a possible role for ElrB in the translational control of Vg1 mRNA, and ElrB, in contrast to TIA-1 and TIAR, is present in large RNP complexes. Immunodepletion of TIA-1 and TIAR from Xenopus translation extract confirmed that these proteins are not involved in the translational repression. Mutagenesis of a potential ElrB binding site destroyed the ability of the VTE to bind ElrB and also abolished translational repression. Moreover, multiple copies of the consensus motif both bind ElrB and support translational control. Therefore, there is a direct correlation between ElrB binding and translational repression by the Vg1 3'-UTR. In agreement with the reporter data, injection of a monoclonal antibody against ElrB into Xenopus oocytes resulted in the production of Vg1 protein, arguing for a role for the ELAV proteins in the translational repression of Vg1 mRNA during early oogenesis.

Citing Articles

RNA binding proteins are potential novel biomarkers of egg quality in yellow catfish.

Ren F, Zhou Q, Meng Y, Guo W, Tang Q, Mei J BMC Genomics. 2023; 24(1):121.

PMID: 36927412 PMC: 10018890. DOI: 10.1186/s12864-023-09220-9.

T-Cell Intracellular Antigen 1-Like Protein in Physiology and Pathology.

Velasco B, Izquierdo J Int J Mol Sci. 2022; 23(14).

PMID: 35887183 PMC: 9318959. DOI: 10.3390/ijms23147836.

L-bodies are RNA-protein condensates driving RNA localization in oocytes.

Neil C, Jeschonek S, Cabral S, OConnell L, Powrie E, Otis J Mol Biol Cell. 2021; 32(22):ar37.

PMID: 34613784 PMC: 8694076. DOI: 10.1091/mbc.E21-03-0146-T.

Organizing the oocyte: RNA localization meets phase separation.

Cabral S, Mowry K Curr Top Dev Biol. 2020; 140:87-118.

PMID: 32591084 PMC: 7323867. DOI: 10.1016/bs.ctdb.2020.02.007.

Translational activation of maternally derived mRNAs in oocytes and early embryos and the role of embryonic poly(A) binding protein (EPAB).

Esencan E, Kallen A, Zhang M, Seli E Biol Reprod. 2019; 100(5):1147-1157.

PMID: 30806655 PMC: 8127035. DOI: 10.1093/biolre/ioz034.

References

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

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

Gao F, Carson C, Levine T, Keene J . Selection of a subset of mRNAs from combinatorial 3' untranslated region libraries using neuronal RNA-binding protein Hel-N1. Proc Natl Acad Sci U S A. 1994; 91(23):11207-11. PMC: 45196. DOI: 10.1073/pnas.91.23.11207. View

Kim-Ha J, Kerr K, Macdonald P . Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. Cell. 1995; 81(3):403-12. DOI: 10.1016/0092-8674(95)90393-3. View

Good P . A conserved family of elav-like genes in vertebrates. Proc Natl Acad Sci U S A. 1995; 92(10):4557-61. PMC: 41983. DOI: 10.1073/pnas.92.10.4557. View

Chen C, Shyu A . AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci. 1995; 20(11):465-70. DOI: 10.1016/s0968-0004(00)89102-1. View

Hake L, Richter J . CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 1996; 15(10):2582-92. PMC: 450191. View

Gavis E, Lunsford L, Bergsten S, Lehmann R . A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development. 1996; 122(9):2791-800. DOI: 10.1242/dev.122.9.2791. View

Mowry K . Complex formation between stage-specific oocyte factors and a Xenopus mRNA localization element. Proc Natl Acad Sci U S A. 1996; 93(25):14608-13. PMC: 26181. DOI: 10.1073/pnas.93.25.14608. View

10.

Jain R, Andrews L, McGowan K, Pekala P, Keene J . Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol Cell Biol. 1997; 17(2):954-62. PMC: 231821. DOI: 10.1128/MCB.17.2.954. View

11.

Ladomery M, Wade E, Sommerville J . Xp54, the Xenopus homologue of human RNA helicase p54, is an integral component of stored mRNP particles in oocytes. Nucleic Acids Res. 1997; 25(5):965-73. PMC: 146530. DOI: 10.1093/nar/25.5.965. View

12.

Antic D, Keene J . Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am J Hum Genet. 1997; 61(2):273-8. PMC: 1715898. DOI: 10.1086/514866. View

13.

Hyatt B, Yost H . The left-right coordinator: the role of Vg1 in organizing left-right axis formation. Cell. 1998; 93(1):37-46. DOI: 10.1016/s0092-8674(00)81144-7. View

14.

Fan X, Steitz J . Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 1998; 17(12):3448-60. PMC: 1170681. DOI: 10.1093/emboj/17.12.3448. View

15.

Peng S, Chen C, Xu N, Shyu A . RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 1998; 17(12):3461-70. PMC: 1170682. DOI: 10.1093/emboj/17.12.3461. View

16.

Atasoy U, Watson J, Patel D, Keene J . ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J Cell Sci. 1998; 111 ( Pt 21):3145-56. DOI: 10.1242/jcs.111.21.3145. View

17.

Voeltz G, Steitz J . AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol Cell Biol. 1998; 18(12):7537-45. PMC: 109334. DOI: 10.1128/MCB.18.12.7537. View

18.

Gueydan C, Droogmans L, Chalon P, Huez G, Caput D, Kruys V . Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor alpha mRNA. J Biol Chem. 1999; 274(4):2322-6. DOI: 10.1074/jbc.274.4.2322. View

19.

Walker J, Minshall N, Hake L, Richter J, Standart N . The clam 3' UTR masking element-binding protein p82 is a member of the CPEB family. RNA. 1999; 5(1):14-26. PMC: 1369736. DOI: 10.1017/s1355838299981219. View

20.

Minshall N, Walker J, Dale M, Standart N . Dual roles of p82, the clam CPEB homolog, in cytoplasmic polyadenylation and translational masking. RNA. 1999; 5(1):27-38. PMC: 1369737. DOI: 10.1017/s1355838299981220. View