Abstract
The precise restriction of proteins to specific domains within a cell plays an important role in early development and differentiation. An efficient way to localize and concentrate proteins is by localization of mRNA in a translationally repressed state, followed by activation of translation when the mRNA reaches its destination. A central issue is how localized mRNAs are derepressed. In this study we demonstrate that, when oskar mRNA reaches the posterior pole of the Drosophila oocyte, its translation is derepressed by an active process that requires a specific element in the 5′ region of the mRNA. We demonstrate that this novel type of element is a translational derepressor element, whose functional interaction with the previously identified repressor region in the oskar 3′ UTR is required for activation of oskar mRNA translation at the posterior pole. The derepressor element only functions at the posterior pole, suggesting that a locally restricted interaction betweentrans-acting factors and the derepressor element may be the link between mRNA localization and translational activation. We also show specific interaction of two proteins with the oskar mRNA 5′ region; one of these also recognizes the 3′ repressor element. We discuss the possible involvement of these factors as well as known genes in the process of localization-dependent translation.
References
57
Referenced
116
10.1083/jcb.123.2.431
/ J. Cell Biol. / Transport and localization of exogenous myelin basic protein mRNA microinjected into oligodendrocytes. by Ainger (1993)- Ausubel, F., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds. 1987–1998. Current protocols in molecular biology. Wiley & Sons, New York, NY..
10.1002/j.1460-2075.1988.tb03004.x
/ EMBO J. / The role of localization of bicoid RNA in organizing the anterior pattern of the Drosophila embryo. by Berleth (1988)10.1093/genetics/135.2.489
/ Genetics / Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: Characterization of male-sterile mutants generated by single P element mutagenesis. by Castrillon (1993)10.1016/S0960-9822(00)00068-3
/ Curr. Biol. / Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. by Clark (1994)10.1016/S0896-6273(00)80248-2
/ Neuron / Molecular characterization of the dendritic growth cone: Regulated mRNA transport and local protein synthesis. by Crino (1996)10.1101/gad.10.20.2610
/ Genes & Dev. / The Nanos gradient in Drosophila embryos is generated by translation regulation. by Dahanukar (1996)10.1016/0092-8674(88)90182-1
/ Cell / A gradient of bicoid protein in Drosophila embryos. by Driever (1988)10.1038/358387a0
/ Nature / Induction of germ cell formation by oskar. by Ephrussi (1992)10.1016/0092-8674(91)90137-N
/ Cell / oskar organizes the germ plasm and directs localization of the posterior determinant nanos. by Ephrussi (1991)- Ferrandon D. (1994) “Mise en place de la polarité antéro-postérieure de la Drosophile au cours de l’ovogénèse: Étude de la localisation de l’ARNm du morphogène bicoid au pôle antérieur de l’embryon.” Ph.D. thesis (Université Louis Pasteur Strasbourg, Strasbourg, France).
10.1038/324120a0
/ Nature / Organization of the anterior pattern in the Drosophila embryo by the maternal gene bicoid. by Frohnhöfer (1986)10.1016/0092-8674(92)90358-J
/ Cell / Localization of nanos RNA controls embryonic polarity. by Gavis (1992)10.1038/369315a0
/ Nature / Translational regulation of nanos by RNA localization. (1994)10.1242/dev.122.9.2791
/ Development / A conserved 90 nucleotide element mediates translational repression of nanos RNA. by Gavis (1996)10.1006/dbio.1996.9996
/ Dev. Biol. / Identification of cis-acting sequences that control nanos RNA localization. by Gavis (1996)10.1016/0092-8674(88)90216-4
/ Cell / A protein component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. by Hay (1988)- Jacobson A. (1996) Poly (A) metabolism and translation: The closed loop model. in Translational control, eds Hershey W.B. Mathews M. Sonenberg N. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 451–480.
10.1242/dev.119.1.169
/ Development / Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. by Kim-Ha (1993)10.1016/0092-8674(95)90393-3
/ Cell / Translational regulation of oskar mRNA by bruno, an ovarian RNA-binding protein, is essential. by Kim-Ha (1995){'key': '2021111418534167000_12.11.1652.21', 'first-page': '6547', 'article-title': 'Binding of a phosphoprotein to the 3′ untranslated region of the mouse protamine 2 mRNA temporally represses its translation.', 'volume': '13', 'author': 'Kwon', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'}
/ Mol. Cell. Biol. / Binding of a phosphoprotein to the 3′ untranslated region of the mouse protamine 2 mRNA temporally represses its translation. by Kwon (1993)10.1038/335611a0
/ Nature / The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. by Lasko (1988){'key': '2021111418534167000_12.11.1652.23', 'first-page': '5331', 'article-title': 'A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation.', 'volume': '13', 'author': 'Leathers', 'year': '1993', 'journal-title': 'Mol. Cell. Biol.'}
/ Mol. Cell. Biol. / A phylogenetically conserved sequence within viral 3′ untranslated RNA pseudoknots regulates translation. by Leathers (1993)10.1016/0092-8674(86)90375-2
/ Cell / Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. by Lehmann (1986)10.1242/dev.112.3.679
/ Development / The maternal gene nanos has a central role in posterior pattern formation of the Drosophila embryo. (1991)10.1242/dev.120.5.1201
/ Development / Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. by Liang (1994)10.1242/dev.122.2.579
/ Development / Mutations that perturb poly(A)-dependent maternal mRNA activation block the initiation of development. by Lieberfarb (1996)10.1016/S0959-437X(96)80060-8
/ Curr. Opin. Genet. Dev. / Translational regulation of maternal mRNAs. by Macdonald (1996)10.1038/336595a0
/ Nature / Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. by Macdonald (1988)10.1242/dev.121.11.3723
/ Development / Translational control of oskar generates Short OSK, the isoform that induces pole plasm assembly. by Markussen (1995)10.1101/SQB.1997.062.01.004
/ Cold Spring Harbor Symp. Quant. Biol. / Efficient translation and phosphorylation of Oskar require Oskar protein and the RNA helicase Vasa. by Markussen (1997)10.1006/dbio.1995.8048
/ Dev. Biol. / mRNA localisation during development. by Micklem (1995)10.1146/annurev.cellbio.12.1.441
/ Ann. Rev. Cell. Dev. Biol. / Transport vesicle docking: SNAREs and associates. by Pfeffer (1996)- Richter J. (1996) Dynamics of poly (A) addition and removal during development. in Translational control, eds Hershey W.B. Mathews M. Sonenberg N. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 481–503.
10.1242/dev.121.9.2737
/ Development / Localization of oskar RNA regulates oskar translation and requires Oskar protein. by Rongo (1995)10.1126/science.7801127
/ Science / Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. by Sallés (1994)10.1093/genetics/129.4.1119
/ Genetics / Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. by Schüpbach (1991)10.1242/dev.121.9.3013
/ Development / Gratuitous mRNA localization in the Drosophila oocyte. by Serano (1995)10.1016/S0959-437X(96)80083-9
/ Curr. Opin. Genet. Dev. / Mechanisms of translational control in early development. by Seydoux (1996)10.1101/gad.10.20.2600
/ Genes & Dev. / Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. by Smibert (1996)10.1016/0092-8674(92)90318-7
/ Cell / Overexpression of oskar directs ectopic action of nanos and presumptive pole cell formation in Drosophila embryos. by Smith (1992)10.1126/science.6289435
/ Science / Transposition of cloned P elements into Drosophila germ line chromosomes. by Spradling (1982)10.1016/0300-9084(94)90189-9
/ Biochimie / Regulation of translation by specific protein/mRNA interactions. by Standart (1994)10.1016/0092-8674(95)90324-0
/ Cell / The intracellular localization of messenger RNAs. by St Johnston (1995)10.1016/0092-8674(91)90138-O
/ Cell / Staufen, a gene required to localize maternal RNAs in the Drosophila egg. by St Johnston (1991)10.1073/pnas.89.22.10979
/ Proc. Natl. Acad. Sci. / A conserved double-stranded RNA-binding domain. by St Johnston (1992)10.1016/S0896-6273(01)80041-6
/ Neuron / mRNA localization in neurons: A multipurpose mechanism? by Steward (1997)10.1074/jbc.271.24.14316
/ J. Biol. Chem. / Isolation and characterization of the 102-kilodalton RNA-binding protein that binds to the 5′ and 3′ translational enhancers of tobacco mosaic virus RNA. by Tanguay (1996)10.1002/j.1460-2075.1996.tb01108.x
/ EMBO J. / Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. by Tarun (1996)10.1146/annurev.cellbio.12.1.27
/ Ann. Rev. Cell. Dev. Biol. / Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. by Teasdale (1996)10.1242/dev.125.9.1723
/ Development / Oocyte polarity depends on regulation of gurken by Vasa. by Tomancak (1998)10.1006/dbio.1996.0024
/ Dev. Biol. / Unmasking mRNA in clam oocytes: Role of phosphorylation of a 3′ UTR masking element-binding protein at fertilization. by Walker (1996)10.1016/0092-8674(91)90110-K
/ Cell / Nanos is the localized posterior determinant in Drosophila. by Wang (1991)10.1038/369400a0
/ Nature / Implications for bcd mRNA localization from spatial distribution of exu protein in Drosophila oogenesis. by Wang (1994)10.1101/gad.11.19.2510
/ Genes & Dev. / Translational repressor Bruno plays multiple roles in development and is widely conserved. by Webster (1997)- Wickens M. Kimble J. Strickland S. (1996) Translational control of developmental decisions. in Translational control, eds Hershey W.B. Mathews M. Sonenberg N. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY), pp 411–450.
10.1242/dev.122.5.1631
/ Development / aubergine enhances oskar translation in the Drosophila ovary. by Wilson (1996)
Dates
Type | When |
---|---|
Created | 17 years, 6 months ago (Feb. 20, 2008, 5:52 p.m.) |
Deposited | 3 years, 9 months ago (Nov. 14, 2021, 10:15 p.m.) |
Indexed | 1 month, 1 week ago (July 14, 2025, 11:18 p.m.) |
Issued | 27 years, 2 months ago (June 1, 1998) |
Published | 27 years, 2 months ago (June 1, 1998) |
Published Online | 27 years, 2 months ago (June 1, 1998) |
Published Print | 27 years, 2 months ago (June 1, 1998) |
@article{Gunkel_1998, title={Localization-dependent translation requires a functional interaction between the 5′ and 3′ ends ofoskar mRNA}, volume={12}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.12.11.1652}, DOI={10.1101/gad.12.11.1652}, number={11}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Gunkel, Niki and Yano, Tamaki and Markussen, Finn-Hugo and Olsen, Lisbeth C. and Ephrussi, Anne}, year={1998}, month=jun, pages={1652–1664} }