Interactome of two diverse RNA granules links mRNA localization to translational repression in neurons

Cell Reports

Volumn 5, Issue 6, 2013, Pages 1749-1762

  Fritzsche, Renate ^a   Karra, Daniela ^a,b,e   Bennett, Keiryn L ^c   Ang, Foongyee ^a,d   Heraud Farlow, Jacki E ^a,f   Tolino, Marco ^a   Doyle, Michael ^a   Bauer, Karl E ^a,d   Thomas, Sabine ^a,b,d   Planyavsky, Melanie ^c   Arn, Eric ^a,b   Bakosova, Anetta ^a   Jungwirth, Kerstin ^a,b   Hörmann, Alexandra ^a,g   Palfi, Zsofia ^a   Sandholzer, Julia ^a   Schwarz, Martina ^a,h   Macchi, Paolo ^a,b,i   Colinge, Jacques ^c   Superti Furga, Giulio ^c   Kiebler, Michael A ^a,b,d   more..

^a Medical University of Vienna   (Austria)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d UNIVERSITY OF MUNICH   (Germany)

^e PAUL EHRLICH INSTITUT   (Germany)

^f UNIVERSITY OF VIENNA   (Austria)

^g BOEHRINGER INGELHEIM RCV GMBH AND CO KG   (Austria)

^h GMI   (Austria)

ⁱ UNIVERSITY OF TRENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; MESSENGER RNA; PROTEIN CAMKII ALPHA; PROTEIN SERINE THREONINE KINASE; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EMBRYO; GENE CONTROL; GENE LOCATION; GENE REPRESSION; GENETIC HETEROGENEITY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RAT; RNA TRANSLATION; RNA TRANSPORT; TRANSLATION INITIATION;

RATTUS;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYTOSKELETAL PROTEINS; DENDRITES; HIPPOCAMPUS; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RATS; RIBONUCLEOPROTEINS; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84890976937     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.11.023     Document Type: Article

References (59)

1. Amrute-Nayak M., Bullock S.L. Single-molecule assays reveal that RNA localization signals regulate dynein-dynactin copy number on individual transcript cargoes. Nat. Cell Biol. 2012, 14:416-423.
2. Anderson P., Kedersha N. RNA granules. J.Cell Biol. 2006, 172:803-808.
3. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 2008, 33:141-150.
4. Andersen C.B., Ballut L., Johansen J.S., Chamieh H., Nielsen K.H., Oliveira C.L., Pedersen J.S., Séraphin B., Le Hir H., Andersen G.R. Structure of the exon junction core complex with a trapped DEAD-box ATPase bound to RNA. Science 2006, 313:1968-1972.
5. Ashraf S.I., McLoon A.L., Sclarsic S.M., Kunes S. Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 2006, 124:191-205.
6. Ballut L., Marchadier B., Baguet A., Tomasetto C., Séraphin B., Le Hir H. The exon junction core complex is locked onto RNA by inhibition ofeIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 2005, 12:861-869.
7. Banerjee S., Neveu P., Kosik K.S. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 2009, 64:871-884.
8. Batish M., van den Bogaard P., Kramer F.R., Tyagi S. Neuronal mRNAs travel singly into dendrites. Proc. Natl. Acad. Sci. USA 2012, 109:4645-4650.
9. Bono F., Ebert J., Lorentzen E., Conti E. The crystal structure of the exon junction complex reveals how it maintains a stable grip on mRNA. Cell 2006, 126:713-725.
10. Brendel C., Rehbein M., Kreienkamp H.J., Buck F., Richter D., Kindler S. Characterization of Staufen 1 ribonucleoprotein complexes. Biochem. J. 2004, 384:239-246.
11. Chazal P.E., Daguenet E., Wendling C., Ulryck N., Tomasetto C., Sargueil B., Le Hir H. EJC core component MLN51 interacts with eIF3 and activates translation. Proc. Natl. Acad. Sci. USA 2013, 110:5903-5908.
12. Chiu Y.L., Witkowska H.E., Hall S.C., Santiago M., Soros V.B., Esnault C., Heidmann T., Greene W.C. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc. Natl. Acad. Sci. USA 2006, 103:15588-15593.
13. Costa-Mattioli M., Sossin W.S., Klann E., Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61:10-26.
14. di Penta A., Mercaldo V., Florenzano F., Munck S., Ciotti M.T., Zalfa F., Mercanti D., Molinari M., Bagni C., Achsel T. Dendritic LSm1/CBP80-mRNPs mark the early steps of transport commitment and translational control. J.Cell Biol. 2009, 184:423-435.
15. Doyle M., Kiebler M.A. Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J. 2011, 30:3540-3552.
16. Dubnau J., Chiang A.S., Grady L., Barditch J., Gossweiler S., McNeil J., Smith P., Buldoc F., Scott R., Certa U., et al. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 2003, 13:286-296.
17. Duchaîne T.F., Hemraj I., Furic L., Deitinghoff A., Kiebler M.A., DesGroseillers L. Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. J.Cell Sci. 2002, 115:3285-3295.
18. Elvira G., Wasiak S., Blandford V., Tong X.K., Serrano A., Fan X., del Rayo Sánchez-Carbente M., Servant F., Bell A.W., Boismenu D., et al. Characterization of an RNA granule from developing brain. Mol. Cell. Proteomics 2006, 5:635-651.
19. Giorgi C., Yeo G.W., Stone M.E., Katz D.B., Burge C., Turrigiano G., Moore M.J. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 2007, 130:179-191.
20. Goetze B., Tuebing F., Xie Y., Dorostkar M.M., Thomas S., Pehl U., Boehm S., Macchi P., Kiebler M.A. The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J.Cell Biol. 2006, 172:221-231.
21. Harlow E., Lane D. Antibodies: A Laboratory Manual 1988, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
22. Heraud-Farlow J.E., Sharangdhar T., Li X., Pfeifer P., Tauber S., Orozco D., Hörmann A., Thomas S., Bakosova A., Farlow A.R., et al. Staufen2 regulates neuronal target mRNAs. Cell Rep. 2013, 5:1511-1518. this issue.
23. Holt C.E., Bullock S.L. Subcellular mRNA localization in animal cells and why it matters. Science 2009, 326:1212-1216.
24. Hüttelmaier S., Zenklusen D., Lederer M., Dictenberg J., Lorenz M., Meng X., Bassell G.J., Condeelis J., Singer R.H. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 2005, 438:512-515.
25. Hwang J., Sato H., Tang Y., Matsuda D., Maquat L.E. UPF1 association with the cap-binding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol. Cell 2010, 39:396-409.
26. Jankowsky E. RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 2011, 36:19-29.
27. Jønson L., Vikesaa J., Krogh A., Nielsen L.K., Hansen Tv., Borup R., Johnsen A.H., Christiansen J., Nielsen F.C. Molecular composition of IMP1 ribonucleoprotein granules. Mol. Cell. Proteomics 2007, 6:798-811.
28. Kanai Y., Dohmae N., Hirokawa N. Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 2004, 43:513-525.
29. Kiebler M.A., Bassell G.J. Neuronal RNA granules: movers and makers. Neuron 2006, 51:685-690.
30. Kiebler M.A., López-García J.C., Leopold P.L. Purification and characterization of rat hippocampal CA3-dendritic spines associated with mossy fiber terminals. FEBS Lett. 1999, 445:80-86.
31. Kim K.M., Cho H., Choi K., Kim J., Kim B.W., Ko Y.G., Jang S.K., Kim Y.K. A new MIF4G domain-containing protein, CTIF, directs nuclear cap-binding protein CBP80/20-dependent translation. Genes Dev. 2009, 23:2033-2045.
32. Köhrmann M., Luo M., Kaether C., DesGroseillers L., Dotti C.G., Kiebler M.A. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 1999, 10:2945-2953.
33. Konecna A., Heraud J.E., Schoderboeck L., Raposo A.A., Kiebler M.A. What are the roles of microRNAs at the mammalian synapse?. Neurosci. Lett. 2009, 466:63-68.
34. Krichevsky A.M., Kosik K.S. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 2001, 32:683-696.
35. Le Hir H., Séraphin B. EJCs at the heart of translational control. Cell 2008, 133:213-216.
36. Macchi P., Kroening S., Palacios I.M., Baldassa S., Grunewald B., Ambrosino C., Goetze B., Lupas A., St Johnston D., Kiebler M. Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner. J.Neurosci. 2003, 23:5778-5788.
37. Maher-Laporte M., Berthiaume F., Moreau M., Julien L.A., Lapointe G., Mourez M., DesGroseillers L. Molecular composition of staufen2-containing ribonucleoproteins in embryonic rat brain. PLoS ONE 2010, 5:e11350.
38. Mallardo M., Deitinghoff A., Müller J., Goetze B., Macchi P., Peters C., Kiebler M.A. Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain. Proc. Natl. Acad. Sci. USA 2003, 100:2100-2105.
39. Martin K.C., Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009, 136:719-730.
40. Martin S.G., Leclerc V., Smith-Litière K., St Johnston D. The identification of novel genes required for Drosophila anteroposterior axis formation in a germline clone screen using GFP-Staufen. Development 2003, 130:4201-4215.
41. Meister G., Landthaler M., Peters L., Chen P.Y., Urlaub H., Lührmann R., Tuschl T. Identification of novel argonaute-associated proteins. Curr. Biol. 2005, 15:2149-2155.
42. Mikl M., Vendra G., Kiebler M.A. Independent localization of MAP2, CaMKIIα and β-actin RNAs in low copy numbers. EMBO Rep. 2011, 12:1077-1084.
43. Palacios I.M., Gatfield D., St Johnston D., Izaurralde E. AneIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 2004, 427:753-757.
44. Rappsilber J., Ishihama Y., Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75:663-670.
45. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68:850-858.
46. Sisson T.H., Castor C.W. An improved method for immobilizing IgG antibodies on protein A-agarose. J.Immunol. Methods 1990, 127:215-220.
47. St Johnston D. Moving messages: the intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 2005, 6:363-375.
48. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127:49-58.
49. Tang S.J., Meulemans D., Vazquez L., Colaco N., Schuman E. A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 2001, 32:463-475.
50. Tiedge H., Brosius J. Translational machinery in dendrites of hippocampal neurons in culture. J.Neurosci. 1996, 16:7171-7181.
51. Tübing F., Vendra G., Mikl M., Macchi P., Thomas S., Kiebler M.A. Dendritically localized transcripts are sorted into distinct ribonucleoprotein particles that display fast directional motility along dendrites of hippocampal neurons. J.Neurosci. 2010, 30:4160-4170.
52. van Eeden F.J., Palacios I.M., Petronczki M., Weston M.J., St Johnston D. Barentsz is essential for the posterior localization of oskar mRNA and colocalizes with it to the posterior pole. J.Cell Biol. 2001, 154:511-523.
53. Vessey J.P., Vaccani A., Xie Y., Dahm R., Karra D., Kiebler M.A., Macchi P. Dendritic localization of the translational repressor Pumilio 2 and its contribution to dendritic stress granules. J.Neurosci. 2006, 26:6496-6508.
54. Vessey J.P., Schoderboeck L., Gingl E., Luzi E., Riefler J., Di Leva F., Karra D., Thomas S., Kiebler M.A., Macchi P. Mammalian Pumilio 2regulates dendrite morphogenesis and synaptic function. Proc. Natl. Acad. Sci. USA 2010, 107:3222-3227.
55. Vessey J.P., Amadei G., Burns S.E., Kiebler M.A., Kaplan D.R., Miller F.D. An asymmetrically localized Staufen2-dependent RNA complex regulates maintenance of mammalian neural stem cells. Cell Stem Cell 2012, 11:517-528.
56. Villacé P., Marión R.M., Ortín J. The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res. 2004, 32:2411-2420.
57. Wessel D., Flügge U.I. A method for the quantitative recovery ofprotein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 1984, 138:141-143.
58. Zeitelhofer M., Karra D., Macchi P., Tolino M., Thomas S., Schwarz M., Kiebler M., Dahm R. Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J.Neurosci. 2008, 28:7555-7562.
59. Zimyanin V.L., Belaya K., Pecreaux J., Gilchrist M.J., Clark A., Davis I., St Johnston D. Invivo imaging of oskar mRNA transport reveals the mechanism of posterior localization. Cell 2008, 134:843-853.