Calsyntenin-1 docks vesicular cargo to Kinesin-1

Molecular Biology of the Cell

Volumn 17, Issue 8, 2006, Pages 3651-3663

  Konecna, Anetta ^a   Frischknecht, Renato ^a,b   Kinter, Jochen ^a   Ludwig, Alexander ^a   Steuble, Martin ^a   Meskenaite, Virginia ^a   Indermühle, Martin ^a   Engel, Marianne ^a   Cen, Chuan ^a   Mateos, José Maria ^a   Streit, Peter ^a   Sonderegger, Peter ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALSYNTENIN 1; DOCKING PROTEIN; KINESIN; KINESIN 1; MOLECULAR MOTOR; MUTANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; CELL ORGANELLE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; IN VITRO STUDY; INTRACELLULAR TRANSPORT; LIGHT CHAIN; MEMBRANE VESICLE; MICROTUBULE; MOUSE; NERVE CELL CULTURE; NERVE FIBER TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; SEQUENCE ANALYSIS; TETRATRICOPEPTIDE REPEAT;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; CONSERVED SEQUENCE; CYTOPLASMIC VESICLES; GROWTH CONES; HELA CELLS; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33746645123     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-02-0112     Document Type: Article

References (65)

1. Allen, R. D., Meruzals, J., Tasaki, I., Brady, S. T., and Gilbert, S. P. (1982). Fast axonal transport in squid giant axon. Science 218, 1127-1129.
2. Araki, Y., Tomita, S., Yamaguchi, H., Miyagi, N., Sumioka, A., Kirino, Y., and Suzuki, T. (2003). Novel cadherin-related membrane proteins, Alcadeins, enhance the X11-like protein-mediated stabilization of amyloid beta-protein precursor metabolism. J. Biol. Chem. 278, 49448-49458.
3. Ashkin, A., Schutze, K., Dziedzic, J. M., Euteneuer, U., and Schliwa, M. (1990). Force generation of organelle transport measured in vivo by an infrared laser trap. Nature 348, 346-348.
4. Banker, G. A. (1980). Trophic interactions between astroglial cells and hippocampal neurons in culture. Science 209, 809-810.
5. Blatch, G. L., and Lassie, M. (1999). The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21, 932-939.
6. Block, S. M., Goldstein, L. S., and Schnapp, B. J. (1990). Bead movement by single kinesin molecules studied with optical tweezers. Nature 348, 348-352.
7. Bowman, A. B., Kamal, A., Ritchings, B. W., Philp, A. V., McGrail, M., Gindhart, J. G., and Goldstein, L. S. (2000). Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103, 583-594.
8. Bradke, F., and Dotti, C. G. (2000). Establishment of neuronal polarity: lessons from cultured hippocampal neurons. Curr. Opin. Neurobiol. 10, 574-581.
9. Brady, S. T. (1985). A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317, 73-75.
10. Das, A. K., Cohen, P. W., and Barford, D. (1998). The structure of the tetratricopeptide repeats of protein phosphatase 5, implications for TPR-mediated protein-protein interactions. EMBO J. 17, 1192-1199.
11. Deacon, S. W., Serpinskaya, A. S., Vaughan, P. S., Lopez Fanarraga, M., Vernos, I., Vaughan, K. T., and Gelfand, V. I. (2003). Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160, 297-301.
12. Diefenbach, R. J., Diefenbach, E., Douglas, M. W., and Cunningham, A. L. (2002). The heavy chain of conventional kinesin interacts with the SNARE proteins SNAP25 and SNAP23. Biochemistry 41, 14906-14915.
13. Grafstein, B., and Forman, D. S. (1980). Intracellular transport in neurons. Physiol. Rev. 60, 1167-1283.
14. Gross, S. P., Welte, M. A., Block, S. M., and Wieschaus, E. F. (2002). Coordination of opposite-polarity microtubule motors. J. Cell Biol. 156, 715-724.
15. Hill, D. B., Plaza, M. J., Bonin, K., and Holzwarth, G. (2004). Fast vesicle transport in PC12 neurites: velocities and forces. Eur. Biophys. J. 33, 623-632.
16. Hintsch, G., Zurlinden, A., Meskenaite, V., Steuble, M., Fink-Widmer, K., Kinter, J., and Sonderegger, P. (2002). The calsyntenins-a family of postsynaptic membrane proteins with distinct neuronal expression patterns. Mol. Cell Neurosci. 21, 393-409.
17. Hirokawa, N. (1998). Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279, 519-526.
18. Hirokawa, N., Pfister, K. K., Yorifuji, H., Wagner, M. C., Brady, S. T., and Bloom, G. S. (1989). Submolecular domains of bovine brain kinesin identified by electron microscopy and mAb decoration. Cell 56, 867-878.
19. Hirokawa, N., Sato-Yoshitake, R., Yoshida, T., and Kawashima, T. (1990). Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo. J. Cell Biol. 111, 1027-1037.
20. Hirokawa, N., and Takemura, R. (2005). Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 6, 201-214.
21. Howard, J., Hudspeth, A. J., and Vale, R. D. (1989). Movement of microtubules by single kinesin molecules. Nature 342, 154-158.
22. Hunt, A. J., Gittes, F., and Howard, J. (1994). The force exerted by a single kinesin molecule against a viscous load. Biophys. J. 67, 766-781.
23. Igarashi, M., Tagaya, M., and Komiya, Y. (1997). The soluble N-ethylmaleimide-sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J. Neurosci. 17, 1460-1470.
24. Inomata, H., Nakamura, Y., Hayakawa, A., Takata, H., Suzuki, T., Miyazawa, K., and Kitamura, N. (2003). A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1. J. Biol. Chem. 278, 22946-22955.
25. Jan, Y. N., and Jan, L. Y. (2001). Dendrites. Genes Dev. 15, 2627-2641.
26. Kaether, C., Skehel, P., and Dotti, C. G. (2000). Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol. Biol. Cell 11, 1213-1224.
27. Kamal, A., Almenar-Queralt, A., LeBlanc, J. P., Roberts, E. A., and Goldstein, L. S. (2001). Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414, 643-648.
28. Kamal, A., Stokin, G. B., Yang, Z., Xia, C. H., and Goldstein, L. S. (2000). Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28, 449-459.
29. Kanai, Y., Okada, Y., Tanaka, Y., Harada, A., Terada, S., and Hirokawa, N. (2000). KIF5C, a novel neuronal kinesin enriched in motor neurons. J. Neurosci. 20, 6374-6384.
30. Klumpp, S., and Lipowsky, R. (2005). Cooperative cargo transport by several molecular motors. Proc. Natl. Acad. Sci. USA 102, 17284-17289.
31. Kreitzer, G., Marmorstein, A., Okamoto, P., Vallee, R., and Rodriguez-Boulan, E. (2000). Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat. Cell Biol. 2, 125-127.
32. Kural, C., Kim, H., Syed, S., Goshima, G., Gelfand, V. I., and Selvin, P. R. (2005). Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement? Science 308, 1469-1472.
33. Lazarov, O. et al. (2005). Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J. Neurosci. 25, 2386-2395.
34. Ligon, L. A., Tokito, M., Finklestein, J. M., Grossman, F. E., and Holzbaur, E. L. (2004). A direct interaction between cytoplasmic dynein and kinesin I may coordinate motor activity. J. Biol. Chem. 279, 19201-19208.
35. Lindsey, J. D., and Ellisman, M. H. (1985). The neuronal endomembrane system. I. Direct links between rough endoplasmic reticulum and the cis element of the Golgi apparatus. J. Neurosci. 5, 3111-3123.
36. Lipowsky, R., Klumpp, S., and Nieuwenhuizen, T. M. (2001). Random walks of cytoskeletal motors in open and closed compartments. Phys. Rev. Lett. 87, 108101.
37. Lohse, K., Helmke, S. M., Wood, M. R., Quiroga, S., de la Houssaye, B. A., Miller, V. E., Negre-Aminou, P., and Pfenninger, K. H. (1996). Axonal origin and purity of growth cones isolated from fetal rat brain. Brain Res. Dev. Brain Res. 96, 83-96.
38. Martinez-Arca, S., et al. (2001). A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838.
39. Matsuda, S., Matsuda, Y., and D'Adamio, L. (2003). Amyloid beta protein precursor (AbetaPP), but not AbetaPP-like protein 2, is bridged to the kinesin light chain by the scaffold protein JNK-interacting protein 1. J. Biol. Chem. 278, 38601-38606.
40. Miller, K. E., DeProto, J., Kaufmann, N., Patel, B. N., Duckworth, A., and Van Vactor, D. (2005). Direct observation demonstrates that Liprin-alpha is required for trafficking of synaptic vesicles. Curr. Biol. 15, 684-689.
41. Miller, R. H., and Lasek, R. J. (1985). Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm. J. Cell Biol. 101, 2181-2193.
42. Morfini, G., Szebenyi, G., Richards, B., and Brady, S. T. (2001a). Regulation of kinesin: implications for neuronal development. Dev. Neurosci. 23, 364-376.
43. Morfini, G., Tsai, M. Y., Szebenyi, G., and Brady, S. T. (2001b). Approaches to study interactions between kinesin motors and membranes. Methods Mol. Biol. 164, 147-162.
44. Muresan, V., Godek, C. P., Reese, T. S., and Schnapp, B. J. (1996). Plus-end motors override minus-end motors during transport of squid axon vesicles on microtubules. J. Cell Biol. 135, 383-397.
45. Nakata, T., Terada, S., and Hirokawa, N. (1998). Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons. J. Cell Biol. 140, 659-674.
46. Patel, S. D., Chen, C. P., Bahna, F., Honig, B., and Shapiro, L. (2003). Cadherin-mediated cell-cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13, 690-698.
47. Pfenninger, K. H., Ellis, L., Johnson, M. P., Friedman, L. B., and Somlo, S. (1983). Nerve growth cones isolated from fetal rat brain: subcellular fractionation and characterization. Cell 35, 573-584.
48. Rahman, A., Friedman, D. S., and Goldstein, L. S. (1998). Two kinesin light chain genes in mice. Identification and characterization of the encoded proteins. J. Biol. Chem. 273, 15395-15403.
49. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U., and Moarefi, I. (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199-210.
50. Scott, E. K., and Luo, L. (2001). How do dendrites take their shape? Nat. Neurosci. 4, 359-365.
51. Setou, M., Seog, D. H., Tanaka, Y., Kanai, Y., Takei, Y., Kawagishi, M., and Hirokawa, N. (2002). Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417, 83-87.
52. Shin, H., et al. (2003). Association of the kinesin motor KIF1A with the multimodular protein liprin-alpha. J. Biol. Chem. 278, 11393-11401.
53. Stockinger, W., Brandes, C., Fasching, D., Hermann, M., Gotthardt, M., Herz, J., Schneider, W. J., and Nimpf, J. (2000). The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2. J. Biol. Chem. 275, 25625-25632.
54. Terlecky, S. R., Nuttley, W. M., McCollum, D., Sock, E., and Subramani, S. (1995). The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO J. 14, 3627-3634.
55. Tsai, M. Y., Morfini, G., Szebenyi, G., and Brady, S. T. (2000). Release of kinesin from vesicles by hsc70 and regulation of fast axonal transport. Mol. Biol. Cell 11, 2161-2173.
56. Tsukita, S., and Ishikawa, H. (1980). The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J. Cell Biol. 84, 513-530.
57. Vale, R. D., Reese, T. S., and Sheetz, M. P. (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50.
58. Verhey, K. J., Lizotte, D. L., Abramson, T., Barenboim, L., Schnapp, B. J., and Rapoport, T. A. (1998). Light chain-dependent regulation of Kinesin's interaction with microtubules. J. Cell Biol. 143, 1053-1066.
59. Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A., and Margolis, B. (2001). Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970.
60. Vignali, G., Lizier, C., Sprocati, M. T., Sirtori, C., Battaglia, G., and Navone, F. (1997). Expression of neuronal kinesin heavy chain is developmentally regulated in the central nervous system of the rat. J. Neurochem. 69, 1840-1849.
61. Vogt, L., et al. (1996). Continuous renewal of the axonal pathway sensor apparatus by insertion of new sensor molecules into the growth cone membrane. Curr. Biol. 6, 1153-1158.
62. Vogt, L., Schrimpf, S. P., Meskenaite, V., Frischknecht, R., Kinter, J., Leone, D. P., Ziegler, U., and Sonderegger, P. (2001). Calsyntenin-1, a proteolytically processed postsynaptic membrane protein with a cytoplasmic calcium-binding domain. Mol. Cell Neurosci. 17, 151-166.
63. Ward, B. M., and Moss, B. (2004). Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J. Virol. 78, 2486-2493.
64. Welte, M. A. (2004). Bidirectional transport along microtubules. Curr. Biol. 14, R525-537.
65. Xia, C., Rahman, A., Yang, Z., and Goldstein, L. S. (1998). Chromosomal localization reveals three kinesin heavy chain genes in mouse. Genomics 52, 209-213.