#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Opposing roles for Egalitarian and Staufen in transport, anchoring and localization of oskar mRNA in the Drosophila oocyte


Autoři: Sabine Mohr aff001;  Andrew Kenny aff001;  Simon T. Y. Lam aff002;  Miles B. Morgan aff001;  Craig A. Smibert aff002;  Howard D. Lipshitz aff002;  Paul M. Macdonald aff001
Působiště autorů: Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, United States of America aff001;  Department of Molecular Genetics, University of Toronto, Toronto, Canada aff002;  Department of Biochemistry, University of Toronto, Toronto, Canada aff003
Vyšlo v časopise: Opposing roles for Egalitarian and Staufen in transport, anchoring and localization of oskar mRNA in the Drosophila oocyte. PLoS Genet 17(4): e1009500. doi:10.1371/journal.pgen.1009500
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009500

Souhrn

Localization of oskar mRNA includes two distinct phases: transport from nurse cells to the oocyte, a process typically accompanied by cortical anchoring in the oocyte, followed by posterior localization within the oocyte. Signals within the oskar 3’ UTR directing transport are individually weak, a feature previously hypothesized to facilitate exchange between the different localization machineries. We show that alteration of the SL2a stem-loop structure containing the oskar transport and anchoring signal (TAS) removes an inhibitory effect such that in vitro binding by the RNA transport factor, Egalitarian, is elevated as is in vivo transport from the nurse cells into the oocyte. Cortical anchoring within the oocyte is also enhanced, interfering with posterior localization. We also show that mutation of Staufen recognized structures (SRSs), predicted binding sites for Staufen, disrupts posterior localization of oskar mRNA just as in staufen mutants. Two SRSs in SL2a, one overlapping the Egalitarian binding site, are inferred to mediate Staufen-dependent inhibition of TAS anchoring activity, thereby promoting posterior localization. The other three SRSs in the oskar 3’ UTR are also required for posterior localization, including two located distant from any known transport signal. Staufen, thus, plays multiple roles in localization of oskar mRNA.

Klíčová slova:

3' UTR – Eggs – Embryos – Luciferase – Oocytes – Oogenesis – RNA transport – Transport inhibition assay


Zdroje

1. Lipshitz HD, Smibert CA. Mechanisms of RNA localization and translational regulation. Curr Opin Genet Dev. 2000; 10:476–488. doi: 10.1016/s0959-437x(00)00116-7 10980424

2. St Johnston D. Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol. 2005; 6:363–375. doi: 10.1038/nrm1643 15852043

3. Lehmann R. Germ Plasm Biogenesis-An Oskar-Centric Perspective. Curr Top Dev Biol. 2016; 116:679–707. doi: 10.1016/bs.ctdb.2015.11.024 26970648

4. Ephrussi A, Lehmann R. Induction of germ cell formation by oskar. Nature. 1992; 358:387–392. doi: 10.1038/358387a0 1641021

5. Smith JL, Wilson JE, Macdonald PM. Overexpression of oskar Directs Ectopic Activation of nanos and Presumptive Pole Cell Formation in Drosophila Embryos. Cell. 1992; 70:849–859. doi: 10.1016/0092-8674(92)90318-7 1516136

6. Jenny A, Hachet O, Závorszky P et al. A translation-independent role of oskar RNA in early Drosophila oogenesis. Development. 2006; 133:2827–2833. doi: 10.1242/dev.02456 16835436

7. Kanke M, Jambor H, Reich J et al. oskar RNA plays multiple noncoding roles to support oogenesis and maintain integrity of the germline/soma distinction. RNA. 2015; 21:1096–1109. doi: 10.1261/rna.048298.114 25862242

8. Kim-Ha J, Webster PJ, Smith JL, Macdonald PM. Multiple RNA regulatory elements mediate distinct steps in localization of oskar mRNA. Development. 1993; 119:169–178. 8275853

9. Kim J, Lee J, Lee S, Lee B, Kim-Ha J. Phylogenetic comparison of oskar mRNA localization signals. Biochem Biophys Res Commun. 2014; 444:98–103. doi: 10.1016/j.bbrc.2014.01.021 24440702

10. Jambor H, Mueller S, Bullock SL, Ephrussi A. A stem-loop structure directs oskar mRNA to microtubule minus ends. RNA. 2014; 20:429–439. doi: 10.1261/rna.041566.113 24572808

11. Ryu YH, Kenny A, Gim Y, Snee M, Macdonald PM. Multiple cis-acting signals, some weak by necessity, collectively direct robust transport of oskar mRNA to the oocyte. J Cell Sci. 2017; 130:3060–3071. doi: 10.1242/jcs.202069 28760927

12. Serano TL, Cohen RS. A small predicted stem-loop structure mediates oocyte localization of Drosophila K10 mRNA. Development. 1995; 121:3809–3818. 8582290

13. Bullock SL, Ish-Horowicz D. Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature. 2001; 414:611–616. doi: 10.1038/414611a 11740552

14. Dienstbier M, Boehl F, Li X, Bullock SL. Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motor. Genes Dev. 2009; 23:1546–1558. doi: 10.1101/gad.531009 19515976

15. Sanghavi P, Laxani S, Li X, Bullock SL, Gonsalvez GB. Dynein Associates with oskar mRNPs and Is Required For Their Efficient Net Plus-End Localization in Drosophila Oocytes. PLoS One. 2013;8:e80605. doi: 10.1371/journal.pone.0080605 24244700

16. Kim-Ha J, Smith JL, Macdonald PM. oskar mRNA Is Localized to the Posterior Pole of the Drosophila Oocyte. Cell. 1991; 66:23–35. doi: 10.1016/0092-8674(91)90136-m 2070416

17. Ephrussi A, Dickinson LK, Lehmann R. oskar Organizes the Germ Plasm and Directs Localization of the Posterior Determinant nanos. Cell. 1991; 66:37–50. doi: 10.1016/0092-8674(91)90137-n 2070417

18. Micklem DR, Adams J, Grunert S, St Johnston D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 2000; 19:1366–1377. doi: 10.1093/emboj/19.6.1366 10716936

19. Laver JD, Li X, Ancevicius K et al. Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity. Nucleic Acids Res. 2013; 41:9438–9460. doi: 10.1093/nar/gkt702 23945942

20. Cheong C, Varani G, Tinoco I Jr. Solution structure of an unusually stable RNA hairpin, 5’GGAC(UUCG)GUCC. Nature. 1990; 346:680–682. doi: 10.1038/346680a0 1696688

21. Uhlenbeck OC. Tetraloops and RNA folding. Nature. 1990; 346:613–614. doi: 10.1038/346613a0 1696683

22. Srisawat C, Engelke DR. Streptavidin aptamers: Affinity tags for the study of RNAs and ribonucleoproteins. RNA. 2001; 7:632–641. doi: 10.1017/s135583820100245x 11345441

23. Leppek K, Stoecklin G. An optimized streptavidin-binding RNA aptamer for purification of ribonucleoprotein complexes identifies novel ARE-binding proteins. Nucleic Acids Res. 2014;42:e13. doi: 10.1093/nar/gkt956 24157833

24. Liu Y, Salter HK, Holding AN et al. Bicaudal-D uses a parallel, homodimeric coiled coil with heterotypic registry to coordinate recruitment of cargos to dynein. Genes Dev. 2013; 27:1233–1246. doi: 10.1101/gad.212381.112 23723415

25. St Johnston D, Beuchle D, Nüsslein-Volhard C. staufen, a Gene Required to Localize Maternal RNAs in the Drosophila Egg. Cell. 1991; 66:51–63. doi: 10.1016/0092-8674(91)90138-o 1712672

26. Sanghavi P, Liu G, Veeranan-Karmegam R, Navarro C, Gonsalvez GB. Multiple Roles for Egalitarian in Polarization of the Drosophila Egg Chamber. Genetics. 2016; 203:415–432. doi: 10.1534/genetics.115.184622 27017624

27. Hoogenraad CC, Akhmanova A, Howell SA et al. Mammalian Golgi-associated Bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J. 2001; 20:4041–4054. doi: 10.1093/emboj/20.15.4041 11483508

28. Hoogenraad CC, Wulf P, Schiefermeier N et al. Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO J. 2003; 22:6004–6015. doi: 10.1093/emboj/cdg592 14609947

29. Splinter D, Razafsky DS, Schlager MA et al. BICD2, dynactin, and LIS1 cooperate in regulating dynein recruitment to cellular structures. Mol Biol Cell. 2012; 23:4226–4241. doi: 10.1091/mbc.E12-03-0210 22956769

30. Bullock SL, Ringel I, Ish-Horowicz D, Lukavsky PJ. A’-form RNA helices are required for cytoplasmic mRNA transport in Drosophila. Nat Struct Mol Biol. 2010;17:703–709. doi: 10.1038/nsmb.1813 20473315

31. Yadav DK, Zigáčková D, Zlobina M et al. Staufen1 reads out structure and sequence features in ARF1 dsRNA for target recognition. Nucleic Acids Res. 2020; 48:2091–2106. doi: 10.1093/nar/gkz1163 31875226

32. Roegiers F, Jan YN. Staufen: a common component of mRNA transport in oocytes and neurons. Trends Cell Biol. 2000; 10:220–224. doi: 10.1016/s0962-8924(00)01767-0 10802537

33. Park E, Maquat LE. Staufen-mediated mRNA decay. Wiley Interdiscip Rev RNA. 2013; 4:423–435. doi: 10.1002/wrna.1168 23681777

34. Ren Z, Veksler-Lublinsky I, Morrissey D, Ambros V. Staufen Negatively Modulates MicroRNA Activity in Caenorhabditis elegans. G3 (Bethesda). 2016; 6:1227–1237. doi: 10.1534/g3.116.027300 26921297

35. Dugré-Brisson S, Elvira G, Boulay K, Chatel-Chaix L, Mouland AJ, DesGroseillers L. Interaction of Staufen1 with the 5’ end of mRNA facilitates translation of these RNAs. Nucleic Acids Res. 2005; 33:4797–4812. doi: 10.1093/nar/gki794 16126845

36. Reveal B, Yan N, Snee MJ, Pai C-I, Gim Y, Macdonald PM. BREs Mediate Both Repression and Activation of oskar mRNA Translation and Act In trans. Dev Cell. 2010; 18:496–502. doi: 10.1016/j.devcel.2009.12.021 20230756

37. Larkin A, Marygold SJ, Antonazzo G et al. FlyBase: updates to the Drosophila melanogaster knowledge base. Nucleic Acids Res. 2021;49: D899–D907. doi: 10.1093/nar/gkaa1026 33219682

38. Kim G, Pai C-I, Sato K, Person MD, Nakamura A, Macdonald PM. Region-Specific Activation of oskar mRNA Translation by Inhibition of Bruno-Mediated Repression. PLoS Genet. 2015;11:e1004992. doi: 10.1371/journal.pgen.1004992 25723530

39. Martin SG, St Johnston D. A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature. 2003; 421:379–384. doi: 10.1038/nature01296 12540903

40. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3:1101–1108. doi: 10.1038/nprot.2008.73 18546601

41. Abbaszadeh EK, Gavis ER. Fixed and live visualization of RNAs in Drosophila oocytes and embryos. Methods. 2016; 98:34–41. doi: 10.1016/j.ymeth.2016.01.018 26827935

42. Ryu YH, Macdonald PM. RNA sequences required for the noncoding function of oskar RNA also mediate regulation of Oskar protein expression by Bicoid Stability Factor. Dev Biol. 2015; 407:211–223. doi: 10.1016/j.ydbio.2015.09.014 26433064

43. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003; 31:3406–3415. doi: 10.1093/nar/gkg595 12824337

44. Mohan RD, Dialynas G, Weake VM et al. Loss of Drosophila Ataxin-7, a SAGA subunit, reduces H2B ubiquitination and leads to neural and retinal degeneration. Genes Dev. 2014; 28:259–272. doi: 10.1101/gad.225151.113 24493646


Článek vyšel v časopise

PLOS Genetics


2021 Číslo 4
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 3/2024 (znalostní test z časopisu)
nový kurz

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Aktuální možnosti diagnostiky a léčby litiáz
Autoři: MUDr. Tomáš Ürge, PhD.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#