A neuron-specific cytoplasmic dynein isoform preferentially transports TrkB signaling endosomes

Journal of Cell Biology

Volumn 181, Issue 6, 2008, Pages 1027-1039

  Ha, Junghoon ^a   Lo, Kevin W H ^a   Myers, Kenneth R ^a   Carr, Tiffany M ^a   Humsi, Michael K ^a   Rasoul, Bareza A ^a   Segal, Rosalind A ^b   Pfister, K Kevin ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYTOPLASM PROTEIN; DYNEIN ADENOSINE TRIPHOSPHATASE; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; UBIQUITIN;

ANIMAL CELL; ANTIBODY AFFINITY; ARTICLE; BRAIN; CELL MEMBRANE; CELL ORGANELLE; CELL SPECIFICITY; CELL STRAIN; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE; HIPPOCAMPUS; INTRACELLULAR TRANSPORT; NERVE CELL CULTURE; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN VARIANT; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CYTOPLASM; DYNEIN ATPASE; ENDOSOMES; GREEN FLUORESCENT PROTEINS; KINETICS; MICROTUBULES; NERVE GROWTH FACTORS; NEURITES; NEURONS; ORGAN SPECIFICITY; PC12 CELLS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RATS; RECEPTOR, TRKA; RECEPTOR, TRKB; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 45349098064     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200803150     Document Type: Article

References (51)

1. Arevalo, J.C., D.B. Pereira, H. Yano, K.K. Teng, and M.V. Chao. 2006. Identification of a switch in neurotrophin signaling by selective tyrosine phosphorylation. J. Biol. Chem. 281:1001-1007.
2. Bhattacharyya, A., F.L. Watson, S.L. Pomeroy, Y.Z. Zhang, C.D. Stiles, and R.A. Segal. 2002. High-resolution imaging demonstrates dynein-based vesicular transport of activated Trk receptors. J. Neurobiol. 51:302-312.
3. Bronfman, F.C., M. Tcherpakov, T.M. Jovin, and M. Fainzilber. 2003. Ligand-induced internalization of the p75 neurotrophin receptor: a slow route to the signaling endosome. J. Neurosci. 23:3209-3220.
4. Campbell, R.E., O. Tour, A.E. Palmer, P.A. Steinbach, G.S. Baird, D.A. Zacharias, and R.Y. Tsien. 2002. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. USA. 99:7877-7882.
5. Caviston, J.P., J.L. Ross, S.M. Antony, M. Tokito, and E.L. Holzbaur. 2007. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc. Natl. Acad. Sci. USA. 104:10045-10050.
6. Delcroix, J.D., J.S. Valletta, C. Wu, S.J. Hunt, A.S. Kowal, and W.C. Mobley. 2003. NGF signaling in sensory neurons: evidence that early endosomes carry NGF retrograde signals. Neuron. 39:69-84.
7. Dillman, J.F. III, and K.K. Pfister. 1994. Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. J. Cell Biol. 127:1671-1681.
8. Dillman, J.F. III, L.P. Dabney, S. Karki, B.M. Paschal, E.L. Holzbaur, and K.K. Pfister. 1996. Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J. Neurosci. 16:6742-6752.
9. Ding, L., A. Spencer, K. Morita, and M. Han. 2005. The developmental timing regulator AIN-1 interacts with miRISCs and may target the argonaute protein ALG-1 to cytoplasmic P bodies in C. elegans. Mol. Cell. 19:437-447.
10. Goslin, K., H. Asmussen, and G. Banker. 1998. Rat hippocampal neurons in low-density culture. In Culturing nerve cells. G. Banker and K. Goslin, editors. The MIT Press, Cambridge, MA. 339-370.
11. Grimes, M.L., J. Zhou, E.C. Beattie, E.C. Yuen, D.E. Hall, J.S. Valletta, K.S. Topp, J.H. LaVail, N.W. Bunnett, and W.C. Mobley. 1996. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 16:7950-7964.
12. Habermann, A., T.A. Schroer, G. Griffiths, and J.K. Burkhardt. 2001. Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J. Cell Sci. 114:229-240.
13. Heerssen, H.M., M.F. Pazyra, and R.A. Segal. 2004. Dynein motors transport activated Trks to promote survival of target-dependent neurons. Nat. Neurosci. 7:596-604.
14. Huang, E.J., and L.F. Reichardt. 2003. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72:609-642.
15. Jullien, J., V. Guili, E.A. Derrington, J.L. Darlix, L.F. Reichardt, and B.B. Rudkin. 2003. Trafficking of TrkA-green fluorescent protein chimerae during nerve growth factor-induced differentiation. J. Biol. Chem. 278:8706-8716.
16. Karki, S., and E.L. Holzbaur. 1995. Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270:28806-28811.
17. Kieran, D., M. Hafezparast, S. Bohnert, J.R. Dick, J. Martin, G. Schiavo, E.M. Fisher, and L. Greensmith. 2005. A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J. Cell Biol. 169:561-567.
18. Lee, M.K., L.I. Rebhun, and A. Frankfurter. 1990a. Posttranslational modification of class III beta-tubulin. Proc. Natl. Acad. Sci. USA. 87:7195-7199.
19. Lee, M.K., J.B. Tuttle, L.I. Rebhun, D.W. Cleveland, and A. Frankfurter. 1990b. The expression and posttranslational modification of a neuronspecific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton. 17:118-132.
20. Levy, J.R., and E.L. Holzbaur. 2006. Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int. J. Dev. Neurosci. 24:103-111.
21. Ligon, L.A., M. Tokito, J.M. Finklestein, F.E. Grossman, and E.L. Holzbaur. 2004. A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J. Biol. Chem. 279:19201-19208.
22. Lindsay, R.M., S.J. Wiegand, C.A. Altar, and P.S. DiStefano. 1 994. Neurotrophic factors: from molecule to man. Trends Neurosci. 17:182-190.
23. Lo, K.W., H.M. Kan, and K.K. Pfister. 2006. Identification of a novel region of the cytoplasmic Dynein intermediate chain important for dimerization in the absence of the light chains. J. Biol. Chem. 281:9552-9559.
24. Lo, K.W., J.M. Kogoy, and K.K. Pfister. 2007a. The DYNLT3 light chain directly links cytoplasmic dynein to a spindle checkpoint protein, Bub3. J. Biol. Chem. 282:11205-11212.
25. Lo, K.W., J.M. Kogoy, B.A. Rasoul, S.M. King, and K.K. Pfister. 2007b. Interaction of the DYNLT (TCTEX1/RP3) light chains and the intermediate chains reveals novel intersubunit regulation during assembly of the dynein complex. J. Biol. Chem. 282:36871-36878.
26. Myers, K.R., K.W. Lo, R.J. Lye, J.M. Kogoy, V. Soura, M. Hafezparast, and K.K. Pfister. 2007. Intermediate chain subunit as a probe for cytoplasmic dynein function: Biochemical analyses and live cell imaging in PC12 cells. J. Neurosci. Res. 85:2640-2647.
27. O'Rourke, S.M., M.D. Dorfman, J.C. Carter, and B. Bowerman. 2007. Dynein modifiers in C. elegans: light chains suppress conditional heavy chain mutants. PLoS Genet. 3:e128.
28. Paschal, B.M., H.S. Shpetner, and R.B. Vallee. 1987. MAP 1C is a microtubuleactivated ATPase which translocates microtubules in vitro and has dyneinlike properties. J. Cell Biol. 105:1273-1282.
29. Paschal, B.M., A. Mikami, K.K. Pfister, and R.B. Vallee. 1992. Homology of the 74-kD cytoplasmic dynein subunit with a flagellar dynein polypeptide suggests an intracellular targeting function. J. Cell Biol. 118:1133-1143.
30. Pfister, K.K., M.W. Salata, J.F. Dillman III, E. Torre, and R.J. Lye. 1996a. Identification and developmental regulation of a neuron-specific subunit of cytoplasmic dynein. Mol. Biol. Cell. 7:331-343.
31. Pfister, K.K., M.W. Salata, J.F. Dillman III, K.T. Vaughan, R.B. Vallee, E. Torre, and R.J. Lye. 1996b. Differential expression and phosphorylation of the 74-kDa intermediate chains of cytoplasmic dynein in cultured neurons and glia. J. Biol. Chem. 271:1687-1694.
32. Pfister, K.K., E.M. Fisher, I.R. Gibbons, T.S. Hays, E.L. Holzbaur, J.R. McIntosh, M.E. Porter, T.A. Schroer, K.T. Vaughan, G.B. Witman, et al. 2005. Cytoplasmic dynein nomenclature. J. Cell Biol. 171:411-413.
33. Pfister, K.K., P.R. Shah, H. Hummerich, A. Russ, J. Cotton, A.A. Annuar, S.M. King, and E.M. Fisher. 2006. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet. 2:e1.
34. Reilein, A.R., A.S. Serpinskaya, R.L. Karcher, D.L. Dujardin, R.B. Vallee, and V.I. Gelfand. 2003. Differential regulation of dynein-driven melanosome movement. Biochem. Biophys. Res. Commun. 309:652-658.
35. Roy, S., M.J. Winton, M.M. Black, J.Q. Trojanowski, and V.M. Lee. 2007. Rapid and intermittent cotransport of slow component-b proteins. J. Neurosci. 27:3131-3138.
36. Salata, M.W., J.F. Dillman III, R.J. Lye, and K.K. Pfister. 2001. Growth factor regulation of cytoplasmic dynein intermediate chain subunit expression preceding neurite extension. J. Neurosci. Res. 65:408-416.
37. Sambrook, J., and D.W. Russell. 2001. Molecular Cloning. A Laboratory Manual. Third Edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 16.14-16.18.
38. Segal, R.A., A. Bhattacharyya, L.A. Rua, J.A. Alberta, R.M. Stephens, D.R. Kaplan, and C.D. Stiles. 1996. Differential utilization of Trk autophosphorylation sites. J. Biol. Chem. 271:20175-20181.
39. Steegmaier, M., J. Klumperman, D.L. Foletti, J.S. Yoo, and R.H. Scheller. 1999. Vesicle-associated membrane protein 4 is implicated in trans-Golgi network vesicle trafficking. Mol. Biol. Cell. 10:1957-1972.
40. Stepanova, T., J. Slemmer, C.C. Hoogenraad, G. Lansbergen, B. Dortland, C.I. De Zeeuw, F. Grosveld, G. van Cappellen, A. Akhmanova, and N. Galjart. 2003. Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23:2655-2664.
41. Susalka, S.J., and K.K. Pfister. 2000. Cytoplasmic dynein subunit heterogeneity: implications for axonal transport. J. Neurocytol. 29:819-829.
42. Tai, A.W., J.Z. Chuang, C. Bode, U. Wolfrum, and C.H. Sung. 1999. Rhodopsin's carboxy-terminal cytoplasmic tail acts as a membrane receptor for cytoplasmic dynein by binding to the dynein light chain Tctex-1. Cell. 97:877-887.
43. Tynan, S.H., A. Purohit, S.J. Doxsey, and R.B. Vallee. 2000. Light intermediate chain 1 defines a functional subfraction of cytoplasmic dynein which binds to pericentrin. J. Biol. Chem. 275:32763-32768.
44. Vallee, R.B., J.C. Williams, D. Varma, and L.E. Barnhart. 2004. Dynein: An ancient motor protein involved in multiple modes of transport. J. Neurobiol. 58:189-200.
45. Vaughan, K.T., and R.B. Vallee. 1995. Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131:1507-1516.
46. Watson, F.L., H.M. Heerssen, D.B. Moheban, M.Z. Lin, C.M. Sauvageot, A. Bhattacharyya, S.L. Pomeroy, and R.A. Segal. 1999. Rapid nuclear responses to target-derived neurotrophins require retrograde transport of ligand-receptor complex. J. Neurosci. 19:7889-7900.
47. Wiedenmann, B., and W.W. Franke. 1985. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 41:1017-1028.
48. Winckler, B., P. Forscher, and I. Mellman. 1999. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature. 397:698-701.
49. Yano, H., F.S. Lee, H. Kong, J. Chuang, J. Arevalo, P. Perez, C. Sung, and M.V. Chao. 2001. Association of Trk neurotrophin receptors with components of the cytoplasmic dynein motor. J. Neurosci. 21:RC125.
50. Ye, H., R. Kuruvilla, L.S. Zweifel, and D.D. Ginty. 2 003. E vidence in support of signaling endosome-based retrograde survival of sympathetic neurons. Neuron. 39:57-68.
51. Zhang, H., D.J. Webb, H. Asmussen, and A.F. Horwitz. 2003. Synapse formation is regulated by the signaling adaptor GIT1. J. Cell Biol. 161:131-142.