Dynactin regulates bidirectional transport of dense-core vesicles in the axon and dendrites of cultured hippocampal neurons

Neuroscience

Volumn 162, Issue 4, 2009, Pages 1001-1010

  Kwinter, D M ^a   Lo, K ^a   Mafi, P ^a   Silverman, M A ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

dense core vesicle; dynactin; live cell imaging; neuronal culture; p150Glued; p50

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DYNACTIN; NEUROPEPTIDE Y; PROTEIN P50; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; DENDRITE; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MICROSCOPY; MICROTUBULE; NERVE CELL CULTURE; NERVE FIBER; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; TRANSGENE;

ANIMALS; AXONS; BIOLOGICAL TRANSPORT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; DENDRITES; EMBRYO, MAMMALIAN; HIPPOCAMPUS; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDE Y; PROTEIN STRUCTURE, TERTIARY; RATS; SECRETORY VESICLES; TISSUE PLASMINOGEN ACTIVATOR;

EID: 67949110970     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.05.038     Document Type: Article

References (55)

1. Abney J.R., Meliza C.D., Cutler B., Kingma M., Lochner J.E., and Scalettar B.A. Real-time imaging of the dynamics of secretory granules in growth cones. Biophys J 77 (1999) 2887-2895
2. Ahmad F.J., He Y., Myers K.A., Hasaka T.P., Francis F., Black M.M., and Baas P.W. Effects of dynactin disruption and dynein depletion on axonal microtubules. Traffic 7 (2006) 524-537
3. Barkus R.V., Klyachko O., Horiuchi D., Dickson B.J., and Saxton W.M. Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol Biol Cell 19 (2008) 274-283
4. Berezuk M.A., and Schroer T.A. Dynactin enhances the processivity of kinesin-2. Traffic 8 (2007) 124-129
5. Berg H.C. Random walks in biology (1993), Princeton University Press, Princeton, NJ
6. Burkhardt J.K., Echeverri C.J., Nilsson T., and Vallee R.B. Overexpression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J Cell Biol 139 (1997) 469-484
7. Cohen S., and Greenberg M.E. Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 24 (2008) 183-209
8. Colin E., Zala D., Liot G., Rangone H., Borrell-Pages M., Li X.J., Saudou F., and Humbert S. Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons. EMBO J 27 (2008) 2124-2134
9. Craig A.M., and Banker G. Neuronal polarity. Annu Rev Neurosci 17 (1994) 267-310
10. Deacon S.W., Serpinskaya A.S., Vaughan P.S., Lopez Fanarraga M., Vernos I., Vaughan K.T., and Gelfand V.I. Dynactin is required for bidirectional organelle transport. J Cell Biol 160 (2003) 297-301
11. de Jong E.K., Vinet J., Stanulovic V.S., Meijer M., Wesseling E., Sjollema K., Boddeke H.W., and Biber K. Expression, transport, and axonal sorting of neuronal CCL21 in large dense-core vesicles. FASEB J 22 (2008) 4136-4145
12. de Wit J., Toonen R.F., Verhaagen J., and Verhage M. Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites. Traffic 7 (2006) 1060-1077
13. Dillman III J.F., Dabney L.P., Karki S., Paschal B.M., Holzbaur E.L., and Pfister K.K. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J Neurosci 16 (1996) 6742-6752
14. Dixit R., Levy J.R., Tokito M., Ligon L.A., and Holzbaur E.L. Regulation of dynactin through the differential expression of p150glued isoforms. J Biol Chem 283 (2008) 33611-33619
15. Dixit R., Ross J.L., Goldman Y.E., and Holzbaur E.L. Differential regulation of dynein and kinesin motor proteins by tau. Science 319 (2008) 1086-1089
16. Dompierre J.P., Godin J.D., Charrin B.C., Cordelieres F.P., King S.J., Humbert S., and Saudou F. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27 (2007) 3571-3583
17. Gunawardena S., and Goldstein L.S. Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch Neurol 62 (2005) 46-51
18. Ha J., Lo K.W., Myers K.R., Carr T.M., Humsi M.K., Rasoul B.A., Segal R.A., and Pfister K.K. A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes. J Cell Biol 181 (2008) 1027-1039
19. Haghnia M., Cavalli V., Shah S.B., Schimmelpfeng K., Brusch R., Yang G., Herrera C., Pilling A., and Goldstein L.S. Dynactin is required for coordinated bidirectional motility, but not for dynein membrane attachment. Mol Biol Cell 18 (2007) 2081-2089
20. Haubensak W., Narz F., Heumann R., and Lessmann V. BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons. J Cell Sci 111 Pt 11 (1998) 1483-1493
21. Horton A.C., Racz B., Monson E.E., Lin A.L., Weinberg R.J., and Ehlers M.D. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48 (2005) 757-771
22. Johansson M., Rocha N., Zwart W., Jordens I., Janssen L., Kuijl C., Olkkonen V.M., and Neefjes J. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor {beta}lll spectrin. J Cell Biol 176 (2007) 459-471
23. Kaech S., and Banker G. Culturing hippocampal neurons. Nat Protoc 1 (2006) 2406-2415
24. King S.J., and Schroer T.A. Dynactin increases the processivity of the cytoplasmic dynein motor. Nat Cell Biol 2 (2000) 20-24
25. Laird F.M., Farah M.H., Ackerley S., Hoke A., Maragakis N., Rothstein J.D., Griffin J., Price D.L., Martin L.J., and Wong P.C. Motor neuron disease occurring in a mutant dynactin mouse model is characterized by defects in vesicular trafficking. J Neurosci 28 (2008) 1997-2005
26. Lawrence C.J., Dawe R.K., Christie K.R., Cleveland D.W., Dawson S.C., Endow S.A., Goldstein L.S., Goodson H.V., Hirokawa N., Howard J., et al. A standardized kinesin nomenclature. J Cell Biol 167 (2004) 19-22
27. Ligon L.A., Tokito M., Finklestein J.M., Grossman F.E., and Holzbaur E.L. A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J Biol Chem 279 (2004) 19201-19208
28. Lippincott-Schwartz J., Roberts T.H., and Hirschberg K. Secretory protein trafficking and organelle dynamics in living cells. Annu Rev Cell Dev Biol 16 (2000) 557-589
29. Lochner J.E., Spangler E., Chavarha M., Jacobs C., McAllister K., Schuttner L.C., and Scalettar B.A. Efficient copackaging and cotransport yields postsynaptic colocalization of neuromodulators associated with synaptic plasticity. Dev Neurobiol 68 (2008) 1243-1256
30. Maier K.C., Godfrey J.E., Echeverri C.J., Cheong F.K., and Schroer T.A. Dynamitin mutagenesis reveals protein-protein interactions important for dynactin structure. Traffic 9 (2008) 481-491
31. Mallik R., Carter B.C., Lex S.A., King S.J., and Gross S.P. Cytoplasmic dynein functions as a gear in response to load. Nature 427 (2004) 649-652
32. Muresan V., Stankewich M.C., Steffen W., Morrow J.S., Holzbaur E.L., and Schnapp B.J. Dynactin-dependent, dynein-driven vesicle transport in the absence of membrane proteins: a role for spectrin and acidic phospholipids. Mol Cell 7 (2001) 173-183
33. Nakata T., and Hirokawa N. Microtubules provide directional cues for polarized axonal transport through interaction with kinesin motor head. J Cell Biol 162 (2003) 1045-1055
34. Overly C.C., Rieff H.I., and Hollenbeck P.J. Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons. J Cell Sci 109 5 (1996) 971-980
35. Park J.J., Cawley N.X., and Loh Y.P. A bi-directional carboxypeptidase E-driven transport mechanism controls BDNF vesicle homeostasis in hippocampal neurons. Mol Cell Neurosci 39 (2008) 63-73
36. Pfister K.K., Fisher E.M., Gibbons I.R., Hays T.S., Holzbaur E.L., McIntosh J.R., Porter M.E., Schroer T.A., Vaughan K.T., Witman G.B., King S.M., and Vallee R.B. Cytoplasmic dynein nomenclature. J Cell Biol 171 (2005) 411-413
37. Pilling A.D., Horiuchi D., Lively C.M., and Saxton W.M. Kinesin-1 and dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 17 (2006) 2057-2068
38. Puls I., Jonnakuty C., LaMonte B.H., Holzbaur E.L., Tokito M., Mann E., Floeter M.K., Bidus K., Drayna D., Oh S.J., Brown Jr. R.H., Ludlow C.L., and Fischbeck K.H. Mutant dynactin in motor neuron disease. Nat Genet 33 (2003) 455-456
39. Quintyne N.J., Gill S.R., Eckley D.M., Crego C.L., Compton D.A., and Schroer T.A. Dynactin is required for microtubule anchoring at centrosomes. J Cell Biol 147 (1999) 321-334
40. Ross J.L., Ali M.Y., and Warshaw D.M. Cargo transport: molecular motors navigate a complex cytoskeleton. Curr Opin Cell Biol 20 (2008) 41-47
41. Samson A.L., and Medcalf R.L. Tissue-type plasminogen activator: a multifaceted modulator of neurotransmission and synaptic plasticity. Neuron 50 (2006) 673-678
42. Schroer T.A. Dynactin. Annu Rev Cell Dev Biol 20 (2004) 759-779
43. Seitz A., Kojima H., Oiwa K., Mandelkow E.M., Song Y.H., and Mandelkow E. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J 21 (2002) 4896-4905
44. Setou M., Nakagawa T., Seog D.H., and Hirokawa N. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288 (2000) 1796-1802
45. Shakiryanova D., Tully A., and Levitan E.S. Activity-dependent synaptic capture of transiting peptidergic vesicles. Nat Neurosci 9 (2006) 896-900
46. Silverman M.A., Johnson S., Gurkins D., Farmer M., Lochner J.E., Rosa P., and Scalettar B.A. Mechanisms of transport and exocytosis of dense-core granules containing tissue plasminogen activator in developing hippocampal neurons. J Neurosci 25 (2005) 3095-3106
47. Silverman M.A., Peck R., Glover G., He C., Carlin C., and Banker G. Motifs that mediate dendritic targeting in hippocampal neurons: a comparison with basolateral targeting signals. Mol Cell Neurosci 29 (2005) 173-180
48. Strom A.L., Shi P., Zhang F., Gal J., Kilty R., Hayward L.J., and Zhu H. Interaction of amyotrophic lateral sclerosis (ALS)-related mutant copper-zinc superoxide dismutase with the dynein-dynactin complex contributes to inclusion formation. J Biol Chem 283 (2008) 22795-22805
49. Toba S., Watanabe T.M., Yamaguchi-Okimoto L., Toyoshima Y.Y., and Higuchi H. Overlapping hand-over-hand mechanism of single molecular motility of cytoplasmic dynein. Proc Natl Acad Sci U S A 103 (2006) 5741-5745
50. Tokito M.K., Howland D.S., Lee V.M., and Holzbaur E.L. Functionally distinct isoforms of dynactin are expressed in human neurons. Mol Biol Cell 7 (1996) 1167-1180
51. Varadi A., Tsuboi T., Johnson-Cadwell L.I., Allan V.J., and Rutter G.A. Kinesin I and cytoplasmic dynein orchestrate glucose-stimulated insulin-containing vesicle movements in clonal MIN6 beta-cells. Biochem Biophys Res Commun 311 (2003) 272-282
52. Wang Y., Jerdeva G., Yarber F.A., da Costa S.R., Xie J., Qian L., Rose C.M., Mazurek C., Kasahara N., Mircheff A.K., and Hamm-Alvarez S.F. Cytoplasmic dynein participates in apically targeted stimulated secretory traffic in primary rabbit lacrimal acinar epithelial cells. J Cell Sci 116 (2003) 2051-2065
53. Waterman-Storer C.M., Karki S.B., Kuznetsov S.A., Tabb J.S., Weiss D.G., Langford G.M., and Holzbaur E.L. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci U S A 94 (1997) 12180-12185
54. Welte M.A. Bidirectional transport along microtubules. Curr Biol 14 (2004) R525-R537
55. Zahn T.R., Angleson J.K., MacMorris M.A., Domke E., Hutton J.F., Schwartz C., and Hutton J.C. Dense core vesicle dynamics in Caenorhabditis elegans neurons and the role of kinesin UNC-104. Traffic 5 (2004) 544-559