Advertisement

A Multidisciplinary Approach to RNA Localisation

Chapter
Part of the Biophysics for the Life Sciences book series (BIOPHYS, volume 1)

Abstract

Intracellular mRNA transport and localised translation are important mechanisms that together target proteins to their site of function. In a number of model developmental systems mRNA localisation has been shown to play a key role in setting up embryonic axes. Furthermore, in the nervous system RNA localisation is thought to play a central role in synaptic plasticity, memory and learning. Important advances in our understanding of the mechanism of localisation have come from using genetic and biochemical approaches, leading to the identification of both the cis-acting RNA signals and trans-acting protein factors responsible for localising the RNAs. More recently, new and emerging biochemical methods, novel computer algorithms and advanced microscopy methods are leading to important insights into the underlying basis of localisation specificity. These multidisciplinary approaches include identification of the binding preferences of trans-acting factors by cross-linking and immunoprecipitation and NMR-based approaches as well as the computational prediction of RNA secondary and tertiary structure combined with the use of super-resolution microscopy methods. Moreover, molecular modelling and computer simulations have the potential to uncover the binding modes and dynamics of RNA transport particles and the basis for the selection of their specific intracellular destinations.

Keywords

Root Mean Square Deviation mRNA Localisation Drosophila Oocyte Ash1 mRNA 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

This work was supported by a Wellcome Trust Senior Research Fellowship (Grant number 081858) to ID for RSH and ID. GB is supported through a Wellcome Trust Strategic Award (091911).

References

  1. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Rout MP, Sali A (2007a) Determining the architectures of macromolecular assemblies. Nature 450(7170):683–694. doi: nature06404[pii]10.1038/nature06404PubMedGoogle Scholar
  2. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP (2007b) The molecular architecture of the nuclear pore complex. Nature 450(7170):695–701. doi:nature06405[pii]10.1038/nature06405PubMedGoogle Scholar
  3. Antonioli AH, Cochrane JC, Lipchock SV, Strobel SA (2010) Plasticity of the RNA kink turn structural motif. RNA 16(4):762–768. doi:rna.1883810[pii]10.1261/rna.1883810PubMedGoogle Scholar
  4. Bassell GJ, Zhang H, Byrd AL, Femino AM, Singer RH, Taneja KL, Lifshitz LM, Herman IM, Kosik KS (1998) Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J Neurosci 18(1):251–265PubMedGoogle Scholar
  5. Bauman JG, Wiegant J, Borst P, van Duijn P (1980) A new method for fluorescence microscopical localization of specific DNA sequences by in situ hybridization of fluorochromelabelled RNA. Exp Cell Res 128(2):485–490PubMedGoogle Scholar
  6. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2(4):437–445PubMedGoogle Scholar
  7. Beuth B, Garcia-Mayoral MF, Taylor IA, Ramos A (2007) Scaffold-independent analysis of RNA-protein interactions: the Nova-1 KH3-RNA complex. J Am Chem Soc 129(33):10205–10210. doi: 10.1021/ja072365q PubMedGoogle Scholar
  8. Blanchette M, Green RE, MacArthur S, Brooks AN, Brenner SE, Eisen MB, Rio DC (2009) Genome-wide analysis of alternative pre-mRNA splicing and RNA-binding specificities of the Drosophila hnRNP A/B family members. Mol Cell 33(4):438–449. doi:S1097-2765(09)00066-5[pii]10.1016/j.molcel.2009.01.022PubMedGoogle Scholar
  9. Blichenberg A, Rehbein M, Muller R, Garner CC, Richter D, Kindler S (2001) Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca2+/calmodulin-dependent protein kinase II. Eur J Neurosci 13(10):1881–1888. doi:ejn1565[pii]PubMedGoogle Scholar
  10. Bobola N, Jansen RP, Shin TH, Nasmyth K (1996) Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84(5):699–709. doi:S0092-8674(00)81048-X[pii] PubMedGoogle Scholar
  11. Brion P, Westhof E (1997) Hierarchy and dynamics of RNA folding. Annu Rev Biophys Biomol Struct 26:113–137. doi: 10.1146/annurev.biophys.26.1.113 PubMedGoogle Scholar
  12. Bullock SL (2007) Translocation of mRNAs by molecular motors: think complex? Semin Cell Dev Biol 18(2):194–201. doi:S1084-9521(07)00026-2[pii]10.1016/j.semcdb.2007.01.004PubMedGoogle Scholar
  13. Bullock SL, Ish-Horowicz D (2001) Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis. Nature 414(6864):611–616. doi: 10.1038/414611a PubMedGoogle Scholar
  14. Bullock SL, Zicha D, Ish-Horowicz D (2003) The Drosophila hairy RNA localization signal modulates the kinetics of cytoplasmic mRNA transport. EMBO J 22(10):2484–2494. doi: 10.1093/emboj/cdg230 PubMedGoogle Scholar
  15. Bullock SL, Ringel I, Ish-Horowicz D, Lukavsky PJ (2010) A′-form RNA helices are required for cytoplasmic mRNA transport in Drosophila. Nat Struct Mol Biol 17(6):703–709. doi:nsmb.1813[pii]10.1038/nsmb.1813 PubMedGoogle Scholar
  16. Bycroft M, Grunert S, Murzin AG, Proctor M, St Johnston D (1995) NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5. EMBO J 14(14):3563–3571PubMedGoogle Scholar
  17. Caceres L, Nilson LA (2005) Production of gurken in the nurse cells is sufficient for axis determination in the Drosophila oocyte. Development 132(10):2345–2353PubMedGoogle Scholar
  18. Carson MB, Langlois R, Lu H (2010) NAPS: a residue-level nucleic acid-binding prediction server. Nucleic Acids Res 38(suppl):W431–W435. doi:gkq361[pii]10.1093/nar/gkq361PubMedGoogle Scholar
  19. Chao JA, Patskovsky Y, Patel V, Levy M, Almo SC, Singer RH (2010) ZBP1 recognition of beta-actin zipcode induces RNA looping. Genes Dev 24(2):148–158. doi:24/2/148[pii]10.1101/gad.1862910PubMedGoogle Scholar
  20. Chartrand P, Meng XH, Singer RH, Long RM (1999) Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo. Curr Biol 9(6):333–336PubMedGoogle Scholar
  21. Clark A, Meignin C, Davis I (2007) A dynein-dependent shortcut rapidly delivers axis determination transcripts into the Drosophila oocyte. Development 134(10):1955–1965PubMedGoogle Scholar
  22. Clouse KN, Ferguson SB, Schupbach T (2008) Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Dev Biol 313(2):713–724. doi:S0012-1606(07)01537-0[pii]10.1016/j.ydbio.2007.11.008PubMedGoogle Scholar
  23. Cohen RS, Zhang S, Dollar GL (2005) The positional, structural, and sequence requirements of the Drosophila TLS RNA localization element. RNA 11(7):1017–1029PubMedGoogle Scholar
  24. Condeelis J, Singer RH (2005) How and why does beta-actin mRNA target? Biol Cell 97(1):97–110. doi: BC20040063[pii]10.1042/BC20040063PubMedGoogle Scholar
  25. Cristofanilli M, Iacoangeli A, Muslimov IA, Tiedge H (2006) Neuronal BC1 RNA: microtubule-dependent dendritic delivery. J Mol Biol 356(5):1118–1123. doi:S0022-2836(05)01539-1[pii]10.1016/j.jmb.2005.11.090PubMedGoogle Scholar
  26. Cruz JA, Westhof E (2011) Sequence-based identification of 3D structural modules in RNA with RMDetect. Nat Methods 8(6):513–521. doi:nmeth.1603[pii]10.1038/nmeth.1603PubMedGoogle Scholar
  27. Czaplinski K, Kocher T, Schelder M, Segref A, Wilm M, Mattaj IW (2005) Identification of 40LoVe, a Xenopus hnRNP D family protein involved in localizing a TGF-beta-related mRNA during oogenesis. Dev Cell 8(4):505–515. doi: S1534-5807(05)00016-X[pii]10.1016/j.devcel.2005.01.012PubMedGoogle Scholar
  28. Das R, Baker D (2007) Automated de novo prediction of native-like RNA tertiary structures. Proc Natl Acad Sci U S A 104(37):14664–14669. doi:0703836104[pii]10.1073/pnas.0703836104PubMedGoogle Scholar
  29. Delanoue R, Herpers B, Soetaert J, Davis I, Rabouille C (2007) Drosophila Squid/hnRNP helps dynein switch from a gurken mRNA transport motor to an ultrastructural static anchor in sponge bodies. Dev Cell 13(4):523–538. doi: S1534-5807(07)00344-9[pii]10.1016/j.devcel.2007.08.022 PubMedGoogle Scholar
  30. Dienstbier M, Boehl F, Li X, Bullock SL (2009) Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motor. Genes Dev 23(13):1546–1558. doi: gad.531009[pii]10.1101/gad.531009 PubMedGoogle Scholar
  31. Do CB, Woods DA, Batzoglou S (2006) CONTRAfold: RNA secondary structure prediction without physics-based models. Bioinformatics 22(14):e90–e98. doi: 22/14/e90[pii]10.1093/bioinformatics/btl246 PubMedGoogle Scholar
  32. Dreyfuss G, Kim VN, Kataoka N (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3(3):195–205. doi: 10.1038/nrm760nrm760[pii] PubMedGoogle Scholar
  33. Forrest KM, Gavis ER (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13(14):1159–1168. doi: S0960982203004512[pii] PubMedGoogle Scholar
  34. Garcia-Mayoral MF, Diaz-Moreno I, Hollingworth D, Ramos A (2008) The sequence selectivity of KSRP explains its flexibility in the recognition of the RNA targets. Nucleic Acids Res 36(16):5290–5296. doi: gkn509[pii]10.1093/nar/gkn509 PubMedGoogle Scholar
  35. Geisler R, Rauch GJ, Geiger-Rudolph S, Albrecht A, van Bebber F, Berger A, Busch-Nentwich E, Dahm R, Dekens MP, Dooley C, Elli AF, Gehring I, Geiger H, Geisler M, Glaser S, Holley S, Huber M, Kerr A, Kirn A, Knirsch M, Konantz M, Kuchler AM, Maderspacher F, Neuhauss SC, Nicolson T, Ober EA, Praeg E, Ray R, Rentzsch B, Rick JM, Rief E, Schauerte HE, Schepp CP, Schonberger U, Schonthaler HB, Seiler C, Sidi S, Sollner C, Wehner A, Weiler C, Nusslein-Volhard C (2007) Large-scale mapping of mutations affecting zebrafish development. BMC Genomics 8:11. doi: 1471-2164-8-11[pii]10.1186/1471-2164-8-11 PubMedGoogle Scholar
  36. Gonzalez I, Buonomo SB, Nasmyth K, von Ahsen U (1999) ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation. Curr Biol 9(6):337–340PubMedGoogle Scholar
  37. Goodrich JS, Clouse KN, Schupbach T (2004) Hrb27C, Sqd and Otu cooperatively regulate gurken RNA localization and mediate nurse cell chromosome dispersion in Drosophila oogenesis. Development 131(9):1949–1958. doi: 10.1242/dev.01078dev.01078[pii] PubMedGoogle Scholar
  38. Hafner M, Landthaler M, Ascano M, Khorshid M, Burger L, Zavolan M, Tuschl T, Hausser J, Berninger P, Rothballer A, Jungkamp A-C, Munschauer M, Ulrich A, Wardle GS, Dewell S (2010) PAR-CliP—a method to identify transcriptome-wide the binding sites of RNA binding proteins. J Vis Exp 41:e2034Google Scholar
  39. Hajdin CE, Ding F, Dokholyan NV, Weeks KM (2010) On the significance of an RNA tertiary structure prediction. RNA 16(7):1340–1349. doi: rna.1837410[pii]10.1261/rna.1837410 PubMedGoogle Scholar
  40. Hamilton RS, Davis I (2007) RNA localization signals: deciphering the message with bioinformatics. Semin Cell Dev Biol 18(2):178–185PubMedGoogle Scholar
  41. Hamilton RS, Davis I (2011) Identifying and searching for conserved RNA localisation signals. Methods Mol Biol 714:447–466. doi: 10.1007/978-1-61779-005-8_27 PubMedGoogle Scholar
  42. Hamilton RS, Hartswood E, Vendra G, Jones C, Van De Bor V, Finnegan D, Davis I (2009) A bioinformatics search pipeline, RNA2DSearch, identifies RNA localization elements in Drosophila retrotransposons. RNA 15(2):200–207. doi:15/2/200[pii]10.1261/rna.1264109 PubMedGoogle Scholar
  43. Hamilton RS, Parton RM, Oliveira RA, Vendra G, Ball G, Nasmyth K, Davis I (2010) ParticleStats: open source software for the analysis of particle motility and cytoskeletal polarity. Nucleic Acids Res 38(Web Server issue):W641–646. doi:gkq542[pii]10.1093/nar/gkq542 Google Scholar
  44. Herpers B, Rabouille C (2004) mRNA localization and ER-based protein sorting mechanisms dictate the use of transitional endoplasmic reticulum-golgi units involved in gurken transport in Drosophila oocytes. Mol Biol Cell 15(12):5306–5317. doi: 10.1091/mbc.E04-05-0398E04-05-0398[pii] PubMedGoogle Scholar
  45. Herpers B, Xanthakis D, Rabouille C (2010) ISH-IEM: a sensitive method to detect endogenous mRNAs at the ultrastructural level. Nat Protoc 5(4):678–687. doi: nprot.2010.12[pii]10.1038/nprot.2010.12 PubMedGoogle Scholar
  46. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31(13):3429–3431PubMedGoogle Scholar
  47. Jacquemont S, Hagerman RJ, Hagerman PJ, Leehey MA (2007) Fragile-X syndrome and fragile X-associated tremor/ataxia syndrome: two faces of FMR1. Lancet Neurol 6(1):45–55. doi: S1474-4422(06)70676-7[pii]10.1016/S1474-4422(06)70676-7 PubMedGoogle Scholar
  48. Jaramillo AM, Weil TT, Goodhouse J, Gavis ER, Schupbach T (2008) The dynamics of fluorescently labeled endogenous gurken mRNA in Drosophila. J Cell Sci 121(Pt 6):887–894. doi: jcs.019091[pii]10.1242/jcs.019091 PubMedGoogle Scholar
  49. Jeffery WR, Wilson LJ (1983) Localization of messenger RNA in the cortex of Chaetopterus eggs and early embryos. J Embryol Exp Morphol 75:225–239PubMedGoogle Scholar
  50. Jonikas MA, Radmer RJ, Altman RB (2009a) Knowledge-based instantiation of full atomic detail into coarse-grain RNA 3D structural models. Bioinformatics 25(24):3259–3266. doi: btp576[pii]10.1093/bioinformatics/btp576 PubMedGoogle Scholar
  51. Jonikas MA, Radmer RJ, Laederach A, Das R, Pearlman S, Herschlag D, Altman RB (2009b) Coarse-grained modeling of large RNA molecules with knowledge-based potentials and structural filters. RNA 15(2):189–199. doi: 15/2/189[pii]10.1261/rna.1270809 PubMedGoogle Scholar
  52. Katsimitsoulia Z, Taylor WR (2010) A hierarchic collision detection algorithm for simple Brownian dynamics. Comput Biol Chem 34(2):71–79. doi: S1476-9271(10)00002-2[pii]10.1016/j.compbiolchem.2010.01.001 PubMedGoogle Scholar
  53. Kazan H, Ray D, Chan ET, Hughes TR, Morris Q (2010) RNAcontext: a new method for learning the sequence and structure binding preferences of RNA-binding proteins. PLoS Comput Biol 6:e1000832. doi: 10.1371/journal.pcbi.1000832 PubMedGoogle Scholar
  54. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M (2011) A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 8(7):559–564. doi: nmeth.1608[pii]10.1038/nmeth.1608 PubMedGoogle Scholar
  55. Kislauskis EH, Zhu X, Singer RH (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J Cell Biol 127(2):441–451PubMedGoogle Scholar
  56. Kobayashi H, Yamamoto S, Maruo T, Murakami F (2005) Identification of a cis-acting element required for dendritic targeting of activity-regulated cytoskeleton-associated protein mRNA. Eur J Neurosci 22(12):2977–2984. doi: EJN4508[pii]10.1111/j.1460-9568.2005.04508.x PubMedGoogle Scholar
  57. Kondo J, Westhof E (2011) Classification of pseudo pairs between nucleotide bases and amino acids by analysis of nucleotide-protein complexes. Nucleic Acids Res 39:8628–8637. doi: gkr452[pii]10.1093/nar/gkr452 PubMedGoogle Scholar
  58. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J (2010) iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 17(7):909–915. doi:nsmb.1838[pii]10.1038/nsmb.1838 PubMedGoogle Scholar
  59. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM (2007) Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131(1):174–187. doi: S0092-8674(07)01022-7[pii]10.1016/j.cell.2007.08.003 PubMedGoogle Scholar
  60. Leontis NB, Westhof E (2001) Geometric nomenclature and classification of RNA base pairs. RNA 7(4):499–512PubMedGoogle Scholar
  61. Leontis NB, Westhof E (2002) The annotation of RNA motifs. Comp Funct Genomics 3(6):518–524. doi: 10.1002/cfg.213 PubMedGoogle Scholar
  62. Lerman YV, Kennedy SD, Shankar N, Parisien M, Major F, Turner DH (2011) NMR structure of a 4 x 4 nucleotide RNA internal loop from an R2 retrotransposon: identification of a three purine-purine sheared pair motif and comparison to MC-SYM predictions. RNA 17:1664–1677. doi: rna.2641911[pii]10.1261/rna.2641911 PubMedGoogle Scholar
  63. Levsky JM, Singer RH (2003) Fluorescence in situ hybridization: past, present and future. J Cell Sci 116(pt 14):2833–2838. doi: 10.1242/jcs.00633116/14/2833[pii] PubMedGoogle Scholar
  64. Levsky JM, Shenoy SM, Pezo RC, Singer RH (2002) Single-cell gene expression profiling. Science 297(5582):836–840. doi: 10.1126/science.1072241297/5582/836[pii] PubMedGoogle Scholar
  65. Li X, Quon G, Lipshitz HD, Morris Q (2010) Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA 16(6):1096–1107. doi: rna.2017210[pii]10.1261/rna.2017210 PubMedGoogle Scholar
  66. Lunde BM, Moore C, Varani G (2007) RNA-binding proteins: modular design for efficient function. Nat Rev Mol Cell Biol 8(6):479–490. doi: nrm2178[pii]10.1038/nrm2178 PubMedGoogle Scholar
  67. Luschnig S, Moussian B, Krauss J, Desjeux I, Perkovic J, Nusslein-Volhard C (2004) An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics 167(1):325–342. doi:167/1/325[pii] PubMedGoogle Scholar
  68. Macdonald PM, Kerr K (1998) Mutational analysis of an RNA recognition element that mediates localization of bicoid mRNA. Mol Cell Biol 18(7):3788–3795PubMedGoogle Scholar
  69. Maquat LE, Kiledjian M (2008) RNA turnover in eukaryotes: analysis of specialized and quality control RNA decay pathways. Preface. Methods Enzymol 449:xvii–xviii. doi: S0076-6879(08)02422-1[pii]10.1016/S0076-6879(08)02422-1 Google Scholar
  70. Masquida B, Beckert B, Jossinet F (2010) Exploring RNA structure by integrative molecular modelling. N Biotechnol 27(3):170–183. doi: S1871-6784(10)00394-8[pii]10.1016/j.nbt.2010.02.022 PubMedGoogle Scholar
  71. Mathews DH, Moss WN, Turner DH (2010) Folding and finding RNA secondary structure. Cold Spring Harb Perspect Biol 2(12):a003665. doi: cshperspect.a003665[pii]10.1101/cshperspect.a003665 PubMedGoogle Scholar
  72. Meignin C, Davis I (2008) UAP56 RNA helicase is required for axis specification and cytoplasmic mRNA localization in Drosophila. Dev Biol 315(1):89–98. doi: S0012-1606(07)01574-6[pii]10.1016/j.ydbio.2007.12.004 PubMedGoogle Scholar
  73. Mowry KL, Melton DA (1992) Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes. Science 255(5047):991–994PubMedGoogle Scholar
  74. Murakami Y, Spriggs RV, Nakamura H, Jones S (2010) PiRaNhA: a server for the computational prediction of RNA-binding residues in protein sequences. Nucleic Acids Res 38(suppl):W412–W416. doi: gkq474[pii]10.1093/nar/gkq474 PubMedGoogle Scholar
  75. Muslimov IA, Patel MV, Rose A, Tiedge H (2011) Spatial code recognition in neuronal RNA targeting: role of RNA-hnRNP A2 interactions. J Cell Biol 194:441–457. doi: jcb.201010027[pii]10.1083/jcb.201010027 PubMedGoogle Scholar
  76. Nakamura A, Sato K, Hanyu-Nakamura K (2004) Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev Cell 6(1):69–78. doi: S1534580703004003[pii] PubMedGoogle Scholar
  77. Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O (2011) Translation-independent localization of mRNA in E. coli. Science 331(6020):1081–1084. doi: 331/6020/1081[pii]10.1126/science.1195691 Google Scholar
  78. Norvell A, Kelley RL, Wehr K, Schupbach T (1999) Specific isoforms of squid, a Drosophila hnRNP, perform distinct roles in Gurken localization during oogenesis. Genes Dev 13(7):864–876PubMedGoogle Scholar
  79. Olivier C, Poirier G, Gendron P, Boisgontier A, Major F, Chartrand P (2005) Identification of a conserved RNA motif essential for She2p recognition and mRNA localization to the yeast bud. Mol Cell Biol 25(11):4752–4766PubMedGoogle Scholar
  80. Parisien M, Major F (2008) The MC-fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452(7183):51–55. doi: nature06684[pii]10.1038/nature06684 PubMedGoogle Scholar
  81. Parton RM, Hamilton RS, Ball G, Yang L, Cullen F, Lu W, Ohkura H et al (2011) A PAR-1-dependent orientation gradient of dynamic microtubules directs posterior cargo transport in the Drosophila oocyte. J Cell Biol, 194(1):121–135. doi:10.1083/jcb.201103160Google Scholar
  82. Rabani M, Kertesz M, Segal E (2008) Computational prediction of RNA structural motifs involved in posttranscriptional regulatory processes. Proc Natl Acad Sci U S A 105(39):14885–14890. doi: 0803169105[pii]10.1073/pnas.0803169105 PubMedGoogle Scholar
  83. Ramos A, Grunert S, Adams J, Micklem DR, Proctor MR, Freund S, Bycroft M, St Johnston D, Varani G (2000) RNA recognition by a Staufen double-stranded RNA-binding domain. EMBO J 19(5):997–1009. doi: 10.1093/emboj/19.5.997 PubMedGoogle Scholar
  84. Rom I, Faicevici A, Almog O, Neuman-Silberberg FS (2007) Drosophila Dynein light chain (DDLC1) binds to gurken mRNA and is required for its localization. Biochim Biophys Acta 1773(10):1526–1533. doi: S0167-4889(07)00119-X[pii]10.1016/j.bbamcr.2007.05.005 PubMedGoogle Scholar
  85. Rosbash M, Singer RH (1993) RNA travel: tracks from DNA to cytoplasm. Cell 75(3):399–401. doi: 0092-8674(93)90373-X[pii] PubMedGoogle Scholar
  86. Ross AF, Oleynikov Y, Kislauskis EH, Taneja KL, Singer RH (1997) Characterization of a beta-actin mRNA zipcode-binding protein. Mol Cell Biol 17(4):2158–2165PubMedGoogle Scholar
  87. Russel D, Lasker K, Phillips J, Schneidman-Duhovny D, Velazquez-Muriel JA, Sali A (2009) The structural dynamics of macromolecular processes. Curr Opin Cell Biol 21(1):97–108. doi: S0955-0674(09)00031-3[pii]10.1016/j.ceb.2009.01.022 PubMedGoogle Scholar
  88. Schroeder KT, McPhee SA, Ouellet J, Lilley DM (2010) A structural database for k-turn motifs in RNA. RNA 16(8):1463–1468. doi: rna.2207910[pii]10.1261/rna.2207910 PubMedGoogle Scholar
  89. Schupbach T, Wieschaus E (1989) Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121(1):101–117PubMedGoogle Scholar
  90. Serano TL, Cohen RS (1995) A small predicted stem-loop structure mediates oocyte localization of Drosophila K10 mRNA. Development 121(11):3809–3818PubMedGoogle Scholar
  91. St Johnston D (1995) The intracellular localization of messenger RNAs. Cell 81(2):161–170. doi: 0092-8674(95)90324-0[pii] PubMedGoogle Scholar
  92. St Johnston D (2005) Moving messages: the intracellular localization of mRNAs. Nat Rev Mol Cell Biol 6(5):363–375. doi: 10.1038/nrm1643 PubMedGoogle Scholar
  93. Stefl R, Oberstrass FC, Hood JL, Jourdan M, Zimmermann M, Skrisovska L, Maris C, Peng L, Hofr C, Emeson RB, Allain FH (2010) The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell 143(2):225–237. doi: S0092-8674(10)01074-3[pii]10.1016/j.cell.2010.09.026 PubMedGoogle Scholar
  94. Taylor WR, Katsimitsoulia Z (2010a) A coarse-grained molecular model for actin-myosin simulation. J Mol Graph Model 29(2):266–279. doi: S1093-3263(10)00084-7[pii]10.1016/j.jmgm.2010.06.004 PubMedGoogle Scholar
  95. Taylor WR, Katsimitsoulia Z (2010b) A soft collision detection algorithm for simple Brownian dynamics. Comput Biol Chem 34(1):1–10. doi: S1476-9271(09)00136-4[pii]10.1016/j.compbiolchem.2009.11.003 PubMedGoogle Scholar
  96. Tekotte H, Davis I (2002) Intracellular mRNA localization: motors move messages. Trends Genet 18(12):636–642. doi: 10.1016/S0168-9525(02)02819-6 PubMedGoogle Scholar
  97. Terribilini M, Lee JH, Yan C, Jernigan RL, Honavar V, Dobbs D (2006) Prediction of RNA binding sites in proteins from amino acid sequence. RNA 12(8):1450–1462. doi: rna.2197306[pii]10.1261/rna.2197306 PubMedGoogle Scholar
  98. Tiedge H (2006) K-turn motifs in spatial RNA coding. RNA Biol 3(4):133–139. doi: 3249[pii] PubMedGoogle Scholar
  99. Ule J, Jensen K, Mele A, Darnell RB (2005a) CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37(4):376–386. doi: S1046-2023(05)00178-7[pii]10.1016/j.ymeth.2005.07.018 PubMedGoogle Scholar
  100. Ule J, Ule A, Spencer J, Williams A, Hu JS, Cline M, Wang H, Clark T, Fraser C, Ruggiu M, Zeeberg BR, Kane D, Weinstein JN, Blume J, Darnell RB (2005b) Nova regulates brain-specific splicing to shape the synapse. Nat Genet 37(8):844–852. doi: ng1610[pii]10.1038/ng1610 PubMedGoogle Scholar
  101. Van De Bor V, Hartswood E, Jones C, Finnegan D, Davis I (2005) gurken and the I factor retrotransposon RNAs share common localization signals and machinery. Dev Cell 9(1):51–62Google Scholar
  102. Weil TT, Forrest KM, Gavis ER (2006) Localization of bicoid mRNA in late oocytes is maintained by continual active transport. Dev Cell 11(2):251–262. doi: S1534-5807(06)00262-0[pii]10.1016/j.devcel.2006.06.006 PubMedGoogle Scholar
  103. Wilkie GS, Davis I (2001) Drosophila wingless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105(2):209–219. doi: 10.1016/S0092-8674(01)00312-9 PubMedGoogle Scholar
  104. Williams KR, Konigsberg WH (1991) Identification of amino acid residues at interface of protein-nucleic acid complexes by photochemical cross-linking. Methods Enzymol 208:516–539PubMedGoogle Scholar
  105. Yisraeli JK, Sokol S, Melton DA (1990) 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 108(2):289–298PubMedGoogle Scholar
  106. Zimyanin VL, Belaya K, Pecreaux J, Gilchrist MJ, Clark A, Davis I, St Johnston D (2008) In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 134(5):843–853. doi: S0092-8674(08)00841-6[pii]10.1016/j.cell.2008.06.053 PubMedGoogle Scholar
  107. zu Siederdissen CH, Bernhart SH, Stadler PF, Hofacker IL (2011) A folding algorithm for extended RNA secondary structures. Bioinformatics 27(13):i129–i136. doi: btr220[pii]10.1093/bioinformatics/btr220 Google Scholar
  108. Zuker M (1994) Prediction of RNA secondary structure by energy minimization. Methods Mol Biol 25:267–294PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Department of BiochemistryUniversity of OxfordOxfordUK

Personalised recommendations