Kinesin transports RNA: Isolation and characterization of an RNA-transporting granule

Neuron

Volumn 43, Issue 4, 2004, Pages 513-525

  Kanai, Yoshimitsu ^a   Dohmae, Naoshi ^b   Hirokawa, Nobutaka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; ISOPROTEIN; KINESIN; PROTEIN; PROTEIN ALY; PROTEIN CGI 99; PROTEIN DDX1; PROTEIN DDX3; PROTEIN EF 1ALPHA; PROTEIN FMRP; PROTEIN HNRNP U; PROTEIN HSPC117; PROTEIN NONO; PROTEIN PSF; PROTEIN PUR ALPHA; PROTEIN PUR BETA; PROTEIN STAUFEN; PROTEIN SYNCRIP; PROTEIN TLS; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; EMBRYO; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA ANALYSIS; RNA ISOLATION; RNA TRANSPORT; SECRETORY GRANULE;

ANIMALS; CELLS, CULTURED; CYTOPLASMIC GRANULES; HIPPOCAMPUS; KINESIN; MICE; NEURONS; PROTEIN BINDING; RNA TRANSPORT;

EID: 4143088149     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.07.022     Document Type: Article

References (77)

1. Ainger K., Avossa D., Diana A.S., Barry C., Barbarese E., Carson J.H. Transport and localization elements in myelin basic protein mRNA. J. Cell Biol. 138:1997;1077-1087
2. Barbarese E., Koppel D.E., Deutscher M.P., Smith C.L., Ainger K., Morgan F., Carson J.H. Protein translation components are colocalized in granules in oligodendrocytes. J. Cell Sci. 108:1995;2781-2790
3. Bardoni B., Schenck A., Mandel J.L. The Fragile X mental retardation protein. Brain Res. Bull. 56:2001;375-382
4. Bassell G.J., Singer R.H. Neuronal RNA localization and the cytoskeleton. Results Probl. Cell Differ. 34:2001;41-56
5. Bassell G.J., Zhang H., Byrd A.L., Femino A.M., Singer R.H., Taneja K.L., Lifshitz L.M., Herman I.M., Kosik K.S. Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18:1998;251-265
6. Blichenberg A., Schwanke B., Rehbein M., Garner C.C., Richter D., Kindler S. Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci. 19:1999;8818-8829
7. 2+/calmodulin-dependent protein kinase II. Eur. J. Neurosci. 13:2001;1881-1888
8. Brady S.T. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature. 317:1985;73-75
9. Breitwieser W., Markussen F.H., Horstmann H., Ephrussi A. Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev. 10:1996;2179-2188
10. Brendza R.P., Serbus L.R., Duffy J.B., Saxton W.M. A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science. 289:2000;2120-2122
11. Bruhn L., Munnerlyn A., Grosschedl R. ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRalpha enhancer function. Genes Dev. 11:1997;640-653
12. 2+/calmodulin- dependent protein kinase in developing rat brain. J. Neurosci. 10:1990;1788-1798
13. Carson J.H., Worboys K., Ainger K., Barbarese E. Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin. Cell Motil. Cytoskeleton. 38:1997;318-328
14. Carson J.H., Cui H., Barbarese E. The balance of power in RNA trafficking. Curr. Opin. Neurobiol. 11:2001;558-563
15. Casadio A., Martin K.C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C.H., Kandel E.R. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell. 99:1999;221-237
16. Chanas-Sacre G., Mazy-Servais C., Wattiez R., Pirard S., Rogister B., Patton J.G., Belachew S., Malgrange B., Moonen G., Leprince P. Identification of PSF, the polypyrimidine tract-binding protein-associated splicing factor, as a developmentally regulated neuronal protein. J. Neurosci. Res. 57:1999;62-73
17. Ephrussi A., Dickinson L.K., Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell. 66:1991;37-50
18. Ferrandon D., Elphick L., Nusslein-Volhard C., St Johnston D. Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell. 79:1994;1221-1232
19. Fukaya M., Watanabe M. Improved immunohistochemical detection of postsynaptically located PSD-95/SAP90 protein family by protease section pretreatment. a study in the adult mouse brain J. Comp. Neurol. 426:2000;572-586
20. Gallia G.L., Darbinian N., Johnson E.M., Khalili K. Self-association of Puralpha is mediated by RNA. J. Cell. Biochem. 74:1999;334-348
21. Gardiol A., Racca C., Triller A. RNA transport and local protein synthesis in the dendritic compartment. Results Probl. Cell Differ. 34:2001;105-128
22. Garner C.C., Tucker R.P., Matus A. Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature. 336:1988;674-677
23. Godbout R., Squire J. Amplification of a DEAD box protein gene in retinoblastoma cell lines. Proc. Natl. Acad. Sci. USA. 90:1993;7578-7582
24. Goslin K., Asmussen H., Banker G. Rat hippocampal neurons in low-density culture. Banker G., Goslin K. Culturing Nerve Cells. 1998;339-370 MIT press, Cambridge, MA
25. Gupta A.K., Drazba J.A., Banerjee A.K. Specific interaction of heterogeneous nuclear ribonucleoprotein particle U with the leader RNA sequence of vesicular stomatitis virus. J. Virol. 72:1998;8532-8540
26. Hirokawa N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 279:1998;519-526
27. Hirokawa N., Funakoshi T., Sato-Harada R., Kanai Y. Selective stabilization of tau in axons and microtubule-associated protein 2C in cell bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J. Cell Biol. 132:1996;667-679
28. Hoek K.S., Kidd G.J., Carson J.H., Smith R. hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA. Biochemistry. 37:1998;7021-7029
29. Huang J.D., Brady S.T., Richards B.W., Stenolen D., Resau J.H., Copeland N.G., Jenkins N.A. Direct interaction of microtubule- and actin-based transport motors. Nature. 397:1999;267-270
30. Huber K.M., Kayser M.S., Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science. 288:2000;1254-1257
31. Kanai Y., Hirokawa N. Sorting mechanisms of tau and MAP2 in neurons. suppressed axonal transit of MAP2 and locally regulated microtubule binding Neuron. 14:1995;421-432
32. Kanai Y., Takemura R., Oshima T., Mori H., Ihara Y., Yanagisawa M., Masaki T., Hirokawa N. Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109:1989;1173-1184
33. Kanai Y., Chen J., Hirokawa N. Microtubule bundling by tau proteins in vivo. analysis of functional domains EMBO J. 11:1992;3953-3961
34. Kanai Y., Okada Y., Tanaka Y., Harada A., Terada S., Hirokawa N. KIF5C, a novel neuronal kinesin enriched in motor neurons. J. Neurosci. 20:2000;6374-6384
35. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science. 273:1996;1402-1406
36. Kelm R.J. Jr., Elder P.K., Strauch A.R., Getz M.J. Sequence of cDNAs encoding components of vascular actin single-stranded DNA-binding factor 2 establish identity to Puralpha and Purbeta. J. Biol. Chem. 272:1997;26727-26733
37. Kiledjian M., Dreyfuss G. Primary structure and binding activity of the hnRNP U protein. binding RNA through RGG box EMBO J. 11:1992;2655-2664
38. Kindler S., Mohr E., Rehbein M., Richter D. Extrasomatic targeting of MAP2, vasopressin and oxytocin mRNAs in mammalian neurons. Results Probl. Cell Differ. 34:2001;83-104
39. Kislauskis E.H., Li Z., Singer R.H., Taneja K.L. Isoform-specific 3′-untranslated sequences sort alpha-cardiac and beta-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. J. Cell Biol. 123:1993;165-172
40. Krichevsky A.M., Kosik K.S. Neuronal RNA granules. a link between RNA localization and stimulation-dependent translation Neuron. 32:2001;683-696
41. Lai C.H., Chou C.Y., Ch'ang L.Y., Liu C.S., Lin W. Identification of novel human genes evolutionarily conserved in Caenorhabditis elegans by comparative proteomics. Genome Res. 10:2000;703-713
42. Li P., Yang X., Wasser M., Cai Y., Chia W. Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions. Cell. 90:1997;437-447
43. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., Kuhl D. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA. 92:1995;5734-5738
44. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., Worley P.F. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton- associated protein that is enriched in neuronal dendrites. Neuron. 14:1995;433-445
45. Macioce P., Gambara G., Bernassola M., Gaddini L., Torreri P., Macchia G., Ramoni C., Ceccarini M., Petrucci T.C. Beta-dystrobrevin interacts directly with kinesin heavy chain in brain. J. Cell Sci. 116:2003;4847-4856
46. Mallardo M., Deitinghoff A., Muller 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. 100:2003;2100-2105
47. Martin K.C., Casadio A., Zhu H., Yaping E., Rose J.C., Chen M., Bailey C.H., Kandel E.R. Synapse-specific, long-term facilitation of aplysia sensory to motor synapses. a function for local protein synthesis in memory storage Cell. 91:1997;927-938
48. Masaki T., Tanabe M., Nakamura K., Soejima M. Studies on a new proteolytic enzyme from A chromobacter lyticus M497-1. I. Purification and some enzymatic properties. Biochim. Biophys. Acta. 660:1981;44-50
49. Miki H., Setou M., Kaneshiro K., Hirokawa N. All kinesin superfamily protein, KIF, genes in mouse and human. Proc. Natl. Acad. Sci. USA. 98:2001;7004-7011
50. Mizutani A., Fukuda M., Ibata K., Shiraishi Y., Mikoshiba K. SYNCRIP, a cytoplasmic counterpart of heterogeneous nuclear ribonucleoprotein R, interacts with ubiquitous synaptotagmin isoforms. J. Biol. Chem. 275:2000;9823-9831
51. Mori Y., Imaizumi K., Katayama T., Yoneda T., Tohyama M. Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat. Neurosci. 3:2000;1079-1084
52. Nakagawa T., Setou M., Seog D., Ogasawara K., Dohmae N., Takio K., Hirokawa N. A novel motor, KIF13A, transports mannose-6-phosphate receptor to plasma membrane through direct interaction with AP-1 complex. Cell. 103:2000;569-581
53. Nakamura A., Amikura R., Hanyu K., Kobayashi S. Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development. 128:2001;3233-3242
54. Nakata T., Hirokawa N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J. Cell Biol. 162:2003;1045-1055
55. Ohashi S., Koike K., Omori A., Ichinose S., Ohara S., Kobayashi S., Sato T.A., Anzai K. Identification of mRNA/protein (mRNP) complexes containing Puralpha, mStaufen, fragile X protein, and myosin Va and their association with rough endoplasmic reticulum equipped with a kinesin motor. J. Biol. Chem. 277:2002;37804-37810
56. Ong L.L., Lim A.P., Er C.P., Kuznetsov S.A., Yu H. Kinectin-kinesin binding domains and their effects on organelle motility. J. Biol. Chem. 275:2000;32854-32860
57. Ouyang Y., Rosenstein A., Kreiman G., Schuman E.M., Kennedy M.B. Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci. 19:1999;7823-7833
58. Raymond C.R., Thompson V.L., Tate W.P., Abraham W.C. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J. Neurosci. 20:2000;969-976
59. Rook M.S., Lu M., Kosik K.S. CaMKIIalpha 3′ untranslated region-directed mRNA translocation in living neurons. visualization by GFP linkage J. Neurosci. 20:2000;6385-6393
60. Setou M., Nakagawa T., Seog D.H., Hirokawa N. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science. 288:2000;1796-1802
61. Setou M., Seog D.H., Tanaka Y., Kanai Y., Takei Y., Kawagishi M., Hirokawa N. Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature. 417:2002;83-87
62. Shan J., Moran-Jones K., Munro T.P., Kidd G.J., Winzor D.J., Hoek K.S., Smith R. Binding of an RNA trafficking response element to heterogeneous nuclear ribonucleoproteins A1 and A2. J. Biol. Chem. 275:2000;38286-38295
63. Sowden J., Putt W., Morrison K., Beddington R., Edwards Y. The embryonic RNA helicase gene (ERH). a new member of the DEAD box family of RNA helicases Biochem. J. 308:1995;839-846
64. St Johnston D., Beuchle D., Nusslein-Volhard C. Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell. 66:1991;51-63
65. Steward O., Worley P. Localization of mRNAs at synaptic sites on dendrites. Results Probl. Cell Differ. 34:2001;1-26
66. Steward O., Bakker C.E., Willems P.J., Oostra B.A. No evidence for disruption of normal patterns of mRNA localization in dendrites or dendritic transport of recently synthesized mRNA in FMR1 knockout mice, a model for human fragile-X mental retardation syndrome. Neuroreport. 9:1998;477-481
67. 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. 32:2001;463-475
68. Vale R.D., Reese T.S., Sheetz M.P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 42:1985;39-50
69. Wallace C.S., Lyford G.L., Worley P.F., Steward O. Differential intracellular sorting of immediate early gene mRNAs depends on signals in the mRNA sequence. J. Neurosci. 18:1998;26-35
70. Widnell C.C., Tata J.R. A procedure for the isolation of enzymically active rat-liver nuclei. Biochem. J. 92:1964;313-317
71. Wilsch-Brauninger M., Schwarz H., Nusslein-Volhard C. A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J. Cell Biol. 139:1997;817-829
72. Wu L., Wells D., Tay J., Mendis D., Abbott M.A., Barnitt A., Quinlan E., Heynen A., Fallon J.R., Richter J.D. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron. 21:1998;1129-1139
73. Yamazaki H., Nakata T., Okada Y., Hirokawa N. KIF3a/b. a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport J. Cell Biol. 130:1995;1387-1399
74. Yang Y.S., Hanke J.H., Carayannopoulos L., Craft C.M., Capra J.D., Tucker P.W. NonO, a non-POU-domain-containing, octamer-binding protein, is the mammalian homolog of Drosophila nonAdiss. Mol. Cell. Biol. 13:1993;5593-5603
75. Yang L., Embree L.J., Tsai S., Hickstein D.D. Oncoprotein TLS interacts with serine-arginine proteins involved in RNA splicing. J. Biol. Chem. 273:1998;27761-27764
76. Zhang Q.H., Ye M., Wu X.Y., Ren S.X., Zhao M., Zhao C.J., Fu G., Shen Y., Fan H.Y., Lu G., et al. Cloning and functional analysis of cDNAs with open reading frames for 300 previously undefined genes expressed in CD34+ hematopoietic stem/progenitor cells. Genome Res. 10:2000;1546-1560
77. Zhang H.L., Eom T., Oleynikov Y., Shenoy S.M., Liebelt D.A., Dictenberg J.B., Singer R.H., Bassell G.J. Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron. 31:2001;261-275