Cross talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion

Molecular Biology of the Cell

Volumn 14, Issue 10, 2003, Pages 4207-4220

  Alberts, Philipp ^a   Rudge, Rachel ^a   Hinners, Ina ^b   Muzerelle, Aude ^c   Martinez Arca, Sonia ^a   Irinopoulou, Theano ^a   Marthiens, Véronique ^a   Tooze, Sharon ^b   Rathjen, Fritz ^d   Gaspar, Patricia ^c   Galli, Thierry ^a  

^a INSERM   (France)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; L1 PROTEIN; N ETHYLMALEIMIDE; NERVE CELL ADHESION MOLECULE; SYNAPTOBREVIN; TETANUS NEUROTOXIN INSENSITIVE VESICLE ASSOCIATED MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MEMBRANE; CELL STRAIN; GENE SILENCING; HIPPOCAMPUS; MEMBRANE TRANSPORT; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; CADHERINS; CELL COMPARTMENTATION; CELL MEMBRANE; CELLS, CULTURED; CYTOPLASMIC GRANULES; EMBRYO; MEMBRANE PROTEINS; MICE; MICROSCOPY, VIDEO; NEURAL CELL ADHESION MOLECULE L1; NEURITES; NEURONS; PC12 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; R-SNARE PROTEINS; RATS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SNARE PROTEINS; SUBCELLULAR FRACTIONS; VESICULAR TRANSPORT PROTEINS;

ANIMALIA;

EID: 10744223512     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-03-0147     Document Type: Article

References (53)

1. Advani, R.J., Yang, B., Prekeris, R., Lee, K.C., Klumperman, J., and Scheller, R.H. (1999). VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146, 765-775.
2. Berditchevski, F. (2001). Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 114, 4143-4151.
3. Bogdanovic, A., Bennett, N., Kieffer, S., Louwagie, M., Morio, T., Garin, J., Satre, M., and Bruckert, F. (2002). Syntaxin 7, Syntaxin 8, Vti1 and VAMP7 form an active SNARE complex for early macropinocytic compartment fusion in Dictyostelium discoideum. Biochem J. 368, 29-39.
4. Borgonovo, B., Cocucci, E., Racchetti, G., Podini, P., Bachi, A., and Meldolesi, J. (2002). Regulated exocytosis: a novel, widely expressed system. Nat. Cell Biol. 4, 955-962.
5. Brummendorf, T., Kenwrick, S., and Rathjen, F.G. (1998). Neural cell recognition molecule L 1, from cell biology to human hereditary brain malformations. Curr. Opin. Neurobiol. 8, 87-97.
6. Chang, S., and De Camilli, P. (2001). Glutamate regulates actin-based motility in axonal filopodia. Nat. Neurosci. 4, 787-793.
7. Chen, D., Minger, S.L., Honer, W.G., and Whiteheart, S.W. (1999). Organization of the secretory machinery in the rodent brain: distribution of the t-SNAREs, SNAP-25 and SNAP-23. Brain Res. 831, 11-24.
8. Chilcote, T.J., Galli, T., Mundigl, O., Edelmann, L., McPherson, P.S., Takei, K., and De Camilli, P. (1995). Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC12 cells. J. Cell Biol. 129, 219-231.
9. Coco, S., Raposo, G., Martinez, S., Fontaine, J.J., Takamori, S., Zahraoui, A., Jahn, R., Matteoli, M., Louvard, D., and Galli, T. (1999). Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: evidence for a novel membrane compartment. J. Neurosci. 19, 9803-9812.
10. Dahme, M., Bartsch, U., Martini, R., Anliker, B., Schachner, M., and Mantei, N. (1997). Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17, 346-349.
11. Davis, J.Q., and Bennett, V. (1994). Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J. Biol. Chem. 269, 27163-27166.
12. De Angelis, E., MacFarlane, J., Du, J.S., Yeo, G., Hicks, R., Rathjen, F.G., Kenwrick, S., and Brummendorf, T. (1999). Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities. EMBO J. 18, 4744-4753.
13. Dickson, T.C., Mintz, C.D., Benson, D.L., and Salton, S.R. (2002). Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J. Cell Biol. 157, 1105-1112.
14. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
15. Filippini, F., Rossi, V., Galli, T., Budillon, A., D'Urso, M., and D'Esposito, M. (2001). Longins: a new evolutionary conserved VAMP family sharing a novel SNARE domain. Trends Biochem. Sci. 26, 407-409.
16. Futerman, A.H., and Banker, G.A. (1996). The economics of neurite outgrowth-the addition of new membrane to growing axons. Trends Neurosci. 19, 144-149.
17. Galli, T., and Haucke, V. (2001). Cycling of synaptic vesicles: how far? How fast! Sci STKE 2001, RE1. Available at http://stke.sciencemag.org/. Accessed September 11, 2003.
18. Galli, T., Zahraoui, A., Vaidyanathan, V.V., Raposo, G., Tian, J.M., Karin, M., Niemann, H., and Louvard, D. (1998). A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol. Biol. Cell 9, 1437-1448.
19. Grosse, G., Grosse, J., Tapp, R., Kuchinke, J., Gorsleben, M., Fetter, I., HohneZell, B., Gratzl, M., and Bergmann, M. (1999). SNAP-25 requirement for dendritic growth of hippocampal neurons. J. Neurosci. Res. 56, 539-546.
20. Harlow, E., and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
21. Ignelzi, M.A., Jr., Miller, D.R., Soriano, P., and Maness, P.F. (1994). Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12, 873-884.
22. Kamiguchi, H., and Lemmon, V. (2000a). IgCAMs: bidirectional signals underlying neurite growth. Curr. Opin. Cell Biol. 12, 598-605.
23. Kamiguchi, H., and Lemmon, V. (2000b). Recycling of the cell adhesion molecule L1 in axonal growth cones. J. Neurosci. 20, 3676-3686.
24. Kamiguchi, H., Long, K.E., Pendergast, M., Schaefer, A.W., Rapoport, I., Kirchhausen, T., and Lemmon, V. (1998). The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J. Neurosci. 18, 5311-5321.
25. Kamiguchi, H., and Yoshihara, F. (2001). The role of endocytic l1 trafficking in polarized adhesion and migration of nerve growth cones. J. Neurosci. 21, 9194-9203.
26. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
27. Lambert, M., Padilla, F., and Mege, R.M. (2000). Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: contribution of both outside-in and inside-out signals. J. Cell Sci. 113, 2207-2219.
28. Le, T.L., Yap, A.S., and Stow, J.L. (1999). Recycling of E-cadherin: a potential mechanism for regulating cadherin dynamics. J. Cell Biol. 146, 219-232.
29. Lemmon, V., Farr, K.L., and Lagenaur, C. (1989). L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2, 1597-1603.
30. Liljelund, P., Ghosh, P., and van den Pol, A.N. (1994). Expression of the neural axon adhesion molecule L1 in the developing and adult rat brain. J. Biol. Chem. 269, 32886-32895.
31. Martinez-Arca, S., Rudge, R.E., Vacca, M., Camonis, J., Daviet, L., Formstecher, E., Hamburger, A., Filippini, F., D'Esposito, M., and Galli, T. (2003b). A novel dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Nat. Acad. Sci. USA. 100, 9011-9016.
32. Martinez-Arca, S., Alberts, P., Zahraoui, A., Louvard, D., and Galli, T. (2000). Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 149, 889-899.
33. Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouille, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D., and Galli, T. (2001). A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838.
34. Martinez-Arca, S., Proux-Gillardeaux, V., Alberts, P., Louvard, D., and Galli, T. (2003a). Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J. Cell Sci. 116, 2805-2816.
35. Mechtersheimer, S., Gutwein, P., Agmon-Levin, N., Stoeck, A., Oleszewski, M., Riedle, S., Fogel, M., Lemmon, V., and Altevogt, P. (2001). Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J. Cell Biol. 155, 661-673.
36. Muzerelle, A., Alberts, P., Martinez Arca, S., Jeannequin, O., Lafaye, P., Mazié, J.-C., Galli, T., and Gaspar, P. (2003). Identification of a presynaptic membrane compartment containing tetanus neurotoxin-insensitive vesicle associated membrane protein in the rat brain. Neuroscience. (in press).
37. Osen-Sand, A., Catsicas, M., Staple, J.K., Jones, K.A., Ayala, G., Knowles, J., Grenningloh, G., and Catsicas, S. (1993). Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo. Nature 364, 445-448.
38. Osen-Sand, A., Staple, J.K., Naldi, E., Schiavo, G., Rossetto, O., Petitpierre, S., Malgaroli, A., Montecucco, C., and Catsicas, S. (1996). Common and distinct fusion proteins in axonal growth and transmitter release. J. Comp. Neurol. 367, 222-234.
39. Prochiantz, A. (1995). Neuronal polarity: giving neurons heads and tails. Neuron 15, 743-746.
40. Rathjen, F.G., and Rutishauser, U. (1984). Comparison of two cell surface molecules involved in neural cell adhesion. EMBO J. 3, 461-465.
41. Rousselet, A., Autillo-Touati, A., Araud, D., and Prochiantz, A. (1990). In vitro regulation of neuronal morphogenesis and polarity by astrocyte-derived factors. Dev. Biol. 137, 33-45.
42. Schaefer, A.W., Kamei, Y., Kamiguchi, H., Wong, E.V., Rapoport, I., Kirchhausen, T., Beach, C.M., Landreth, G., Lemmon, S.K., and Lemmon, V. (2002). L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J. Cell Biol. 157, 1223-1232.
43. Schaefer, A.W., Kamiguchi, H., Wong, E.V., Beach, C.M., Landreth, G., and Lemmon, V. (1999). Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization. J. Biol. Chem. 274, 37965-37973.
44. Schagger, H., and von Jagow, G. (1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368-379.
45. Schmid, R.S., Pruitt, W.M., and Maness, P.F. (2000). A MAP kinase-signaling pathway mediates neurite outgrowth on L1 and requires Src-dependent endocytosis. J. Neurosci. 20, 4177-4188.
46. Schoch, S., Deak, F., Konigstorfer, A., Mozhayeva, M., Sara, Y., Sudhof, T.C., and Kavalali, E.T. (2001). SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294, 1117-1122.
47. Silletti, S., Mei, F., Sheppard, D., and Montgomery, A.M. (2000). Plasmin-sensitive dibasic sequences in the third fibronectin-like domain of L1-cell adhesion molecule (CAM) facilitate homomultimerization and concomitant integrin recruitment. J. Cell Biol. 149, 1485-1502.
48. Sytnyk, V., Leshchynska, I., Delling, M., Dityateva, G., Dityatev, A., and Schachner, M. (2002). Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts. J. Cell Biol. 159, 649-661.
49. Verhage, M., et al. (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869.
50. Wade, N., Bryant, N.J., Connolly, L.M., Simpson, R.J., Luzio, J.P., Piper, R.C., and James, D.E. (2001). Syntaxin 7 complexes with mouse Vps10p tail interactor 1b, Syntaxin 6, vesicle-associated membrane protein (VAMP)8, and VAMP7 in B16 melanoma cells. J. Biol. Chem. 276, 19820-19827.
51. Washbourne, P., et al. (2002). Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5, 19-26.
52. Yang, B., Gonzalez, L., Prekeris, R., Steegmaier, M., Advani, R.J., and Scheller, R.H. (1999). SNARE interactions are not selective - Implications for membrane fusion specificity. J. Biol. Chem. 274, 5649-5653.
53. Yip, P.M., and Siu, C.H. (2001). PC12 cells utilize the homophilic binding site of L1 for cell-cell adhesion but L1-alphavbeta3 interaction for neurite outgrowth. J. Neurochem. 76, 1552-1564.