Torsin Mediates Primary Envelopment of Large Ribonucleoprotein Granules at the Nuclear Envelope

Cell Reports

Volumn 3, Issue 4, 2013, Pages 988-995

  Jokhi, Vahbiz ^a   Ashley, James ^a   Nunnari, John ^a   Noma, Akiko ^b   Ito, Naoto ^c   Wakabayashi Ito, Noriko ^c   Moore, MelissaJ ^b   Budnik, Vivian ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; LARGE RIBONUCLEOPROTEIN; MESSENGER RNA; MUTANT PROTEIN; RIBONUCLEOPROTEIN; SYNAPTIC PROTEIN; TORSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL BUDDING; CELL GRANULE; CELL NUCLEUS MEMBRANE; CELLULAR PARAMETERS; CONTROLLED STUDY; DROSOPHILA; DYSTONIA; GENE EXPRESSION; NEUROTRANSMISSION; NONHUMAN; NUCLEAR BLEBBING; PERINUCLEAR SPACE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SYNTHESIS; SYNAPTIC BOUTON;

ANIMALS; CELL NUCLEUS; CELLS, CULTURED; DROSOPHILA; DYSTONIA; HUMANS; MOLECULAR CHAPERONES; MUTATION; NUCLEAR ENVELOPE; RIBONUCLEOPROTEINS;

HERPES;

EID: 84876955658     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.03.015     Document Type: Article

References (29)

1. Ashley J., Packard M., Ataman B., Budnik V. Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J.Neurosci. 2005, 25:5943-5955.
2. Ataman B., Ashley J., Gorczyca D., Gorczyca M., Mathew D., Wichmann C., Sigrist S.J., Budnik V. Nuclear trafficking of Drosophila Frizzled-2 during synapse development requires the PDZ protein dGRIP. Proc. Natl. Acad. Sci. USA 2006, 103:7841-7846.
3. Ataman B., Ashley J., Gorczyca M., Ramachandran P., Fouquet W., Sigrist S.J., Budnik V. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron 2008, 57:705-718.
4. Barco A., Lopez de Armentia M., Alarcon J.M. Synapse-specific stabilization of plasticity processes: the synaptic tagging and capture hypothesis revisited 10 years later. Neurosci. Biobehav. Rev. 2008, 32:831-851.
5. Breakefield X.O., Blood A.J., Li Y., Hallett M., Hanson P.I., Standaert D.G. The pathophysiological basis of dystonias. Nat. Rev. Neurosci. 2008, 9:222-234.
6. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 1996, 17:627-640.
7. Goodchild R.E., Kim C.E., Dauer W.T. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 2005, 48:923-932.
8. Grabham P.W., Goldberg D.J. Nerve growth factor stimulates the accumulation of beta1 integrin at the tips of filopodia in the growth cones of sympathetic neurons. J.Neurosci. 1997, 17:5455-5465.
9. Grünwald D., Singer R.H., Rout M. Nuclear export dynamics of RNA-protein complexes. Nature 2011, 475:333-341.
10. Iyer L.M., Leipe D.D., Koonin E.V., Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J.Struct. Biol. 2004, 146:11-31.
11. Kim C.E., Perez A., Perkins G., Ellisman M.H., Dauer W.T. A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc. Natl. Acad. Sci. USA 2010, 107:9861-9866.
12. Köhler A., Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 2007, 8:761-773.
13. Koles K., Nunnari J., Korkut C., Barria R., Brewer C., Li Y., Leszyk J., Zhang B., Budnik V. Mechanism of evenness interrupted (Evi)-exosome release at synaptic boutons. J.Biol. Chem. 2012, 287:16820-16834.
14. Maric M., Shao J., Ryan R.J., Wong C.S., Gonzalez-Alegre P., Roller R.J. A functional role for TorsinA in herpes simplex virus 1 nuclear egress. J.Virol. 2011, 85:9667-9679.
15. Mathew D., Ataman B., Chen J., Zhang Y., Cumberledge S., Budnik V. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 2005, 310:1344-1347.
16. Mettenleiter T.C., Klupp B.G., Granzow H. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 2006, 9:423-429.
17. Naismith T.V., Heuser J.E., Breakefield X.O., Hanson P.I. TorsinA in the nuclear envelope. Proc. Natl. Acad. Sci. USA 2004, 101:7612-7617.
18. Neuwald A.F., Aravind L., Spouge J.L., Koonin E.V. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res. 1999, 9:27-43.
19. Ozelius L.J., Hewett J.W., Page C.E., Bressman S.B., Kramer P.L., Shalish C., de Leon D., Brin M.F., Raymond D., Corey D.P., et al. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat. Genet. 1997, 17:40-48.
20. Packard M., Koo E.S., Gorczyca M., Sharpe J., Cumberledge S., Budnik V. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 2002, 111:319-330.
21. Ramachandran P., Barria R., Ashley J., Budnik V. A critical step for postsynaptic F-actin organization: regulation of Baz/Par-3 localization by aPKC and PTEN. Dev. Neurobiol. 2009, 69:583-602.
22. Richter J.D. Think globally, translate locally: what mitotic spindles and neuronal synapses have in common. Proc. Natl. Acad. Sci. USA 2001, 98:7069-7071.
23. Ruiz-Canada C., Ashley J., Moeckel-Cole S., Drier E., Yin J., Budnik V. New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 2004, 42:567-580.
24. Shu X., Lev-Ram V., Deerinck T.J., Qi Y., Ramko E.B., Davidson M.W., Jin Y., Ellisman M.H., Tsien R.Y. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol. 2011, 9:e1001041.
25. Speese S.D., Ashley J., Jokhi V., Nunnari J., Barria R., Li Y., Ataman B., Koon A., Chang Y.-T., Li Q., et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012, 149:832-846.
26. Tanabe L.M., Kim C.E., Alagem N., Dauer W.T. Primary dystonia: molecules and mechanisms. Nat. Rev. Neurol. 2009, 5:598-609.
27. Wakabayashi-Ito N., Doherty O.M., Moriyama H., Breakefield X.O., Gusella J.F., O'Donnell J.M., Ito N. Dtorsin, the Drosophila ortholog of the early-onset dystonia TOR1A (DYT1), plays a novel role in dopamine metabolism. PLoS ONE 2011, 6:e26183.
28. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982, 1:945-951.
29. Wiersma-Meems R., Van Minnen J., Syed N.I. Synapse formation and plasticity: the roles of local protein synthesis. Neuroscientist 2005, 11:228-237.