Syntaxin 1C, a soluble form of syntaxin, attenuates membrane recycling by destabilizing microtubules

Journal of Cell Science

Volumn 125, Issue 4, 2012, Pages 817-830

  Nakayama, Takahiro ^a   Kamiguchi, Hiroyuki ^b   Akagawa, Kimio ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Glucose transporter; Microtubule stability; Recycling; Syntaxin; Vesicle motility

Indexed keywords

ALPHA TUBULIN; GLUCOSE TRANSPORTER 1; SYNTAXIN 1; SYNTAXIN 1C; TUBULIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DYNAMICS; ENDOCYTOSIS; GLUCOSE TRANSPORT; MEMBRANE; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CELL MEMBRANE; CYTOPLASMIC VESICLES; ENDOCYTOSIS; GLUCOSE TRANSPORTER TYPE 1; MICROTUBULES; PROTEIN STABILITY; RATS; SOLUBILITY; SYNTAXIN 1; TUBULIN;

EID: 84861207997     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.081943     Document Type: Article

References (47)

1. Bennett, M. K., Calakos, N. and Scheller, R. H. (1992). Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-259.
2. Brumback, A. C., Lieber, J. L., Angleson, J. K. and Betz, W. J. (2004). Using FM1-43 to study neuropeptide granule dynamics and exocytosis. Methods 33, 287-294.
3. Bunker, J. M., Wilson, L., Jordan, M. A. and Feinstein, S. C. (2004). Modulation of microtubule dynamics by tau in living cells: implications for development and neurodegeneration. Mol. Biol. Cell 15, 2720-2728.
4. Bunker, J. M., Kamath, K., Wilson, L., Jordan, M. A. and Feinstein, S. C. (2006). FTDP-17 mutations compromise the ability of tau to regulate microtubule dynamics in cells. J. Biol. Chem. 281, 11856-11863.
5. Bunn, R. C., Jensen, M. A. and Reed, B. C. (1999). Protein interactions with the glucose transporter binding protein GLUT1CBP that provide a link between GLUT1 and the cytoskeleton. Mol. Biol. Cell 10, 819-832.
6. Cai, Q., Pan, P. Y. and Sheng, Z. H. (2007). Syntabulin-kinesin-1 family member 5B-mediated axonal transport contributes to activity-dependent presynaptic assembly. J. Neurosci. 27, 7284-7296.
7. Desai, A. and Mitchison, T. J. (1997). Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13, 83-117.
8. Dransfeld, O., Rakatzi, I., Sasson, S., Gruzman, A., Schmitt, M., Haussinger, D. and Eckel, J. (2001). Eicosanoids participate in the regulation of cardiac glucose transport by contribution to a rearrangement of actin cytoskeletal elements. Biochem. J. 359, 47-54.
9. Fujiwara, T., Yamamori, T., Yamaguchi, K. and Akagawa, K. (1997). Interaction of HPC-1/syntaxin 1A with the cytoskeletal protein, tubulin. Biochem. Biophys. Res. Commun. 231, 352-355.
10. Howard, J. and Hyman, A. A. (2009). Growth, fluctuation and switching at microtubule plus ends. Nat. Rev. Mol. Cell Biol. 10, 569-574.
11. Ibaraki, K., Horikawa, H. P., Morita, T., Mori, H., Sakimura, K., Mishina, M., Saisu, H. and Abe, T. (1995). Identification of four different forms of syntaxin 3. Biochem. Biophys. Res. Commun. 211, 997-1005.
12. Inoue, A., Obata, K. and Akagawa, K. (1992). Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J. Biol. Chem. 267, 10613-10619.
13. Itoh, T., Fujiwara, T., Shibuya, T., Akagawa, K. and Hotani, H. (1999). Inhibition of microtubule assembly by HPC-1/syntaxin 1A, an exocytosis relating protein. Cell Struct. Funct. 24, 359-364.
14. Jagadish, M. N., Tellam, J. T., Macaulay, S. L., Gough, K. H., James, D. E. and Ward, C. W. (1997). Novel isoform of syntaxin 1 is expressed in mammalian cells. Biochem. J. 321, 151-156.
15. Jahn, R. and Sudhof, T. C. (1999). Membrane fusion and exocytosis. Annu. Rev. Biochem. 68, 863-911.
16. Jerdeva, G. V., Wu, K., Yarber, F. A., Rhodes, C. J., Kalman, D., Schechter, J. E. and Hamm-Alvarez, S. F. (2005). Actin and non-muscle myosin II facilitate apical exocytosis of tear proteins in rabbit lacrimal acinar epithelial cells. J. Cell Sci. 118, 4797-4812.
17. Jourdain, L., Curmi, P., Sobel, A., Pantaloni, D. and Carlier, M. F. (1997). Stathmin: a tubulin-sequestering protein which forms a ternary T2S complex with two tubulin molecules. Biochemistry 36, 10817-10821.
18. 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.
19. Kinet, S., Swainson, L., Lavanya, M., Mongellaz, C., Montel-Hagen, A., Craveiro, M., Manel, N., Battini, J. L., Sitbon, M. and Taylor, N. (2007). Isolated receptor binding domains of HTLV-1 and HTLV-2 envelopes bind Glut-1 on activated CD4+ and CD8+ T cells. Retrovirology 4,31.
20. Lewis, S. A., Wang, D. H. and Cowan, N. J. (1988). Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242, 936-939.
21. Manneville, J. B., Etienne-Manneville, S., Skehel, P., Carter, T., Ogden, D. and Ferenczi, M. (2003). Interaction of the actin cytoskeleton with microtubules regulates secretory organelle movement near the plasma membrane in human endothelial cells. J. Cell Sci. 116, 3927-3938.
22. Marchant, J. S., Subramanian, V. S., Parker, I. and Said, H. M. (2002). Intracellular trafficking and membrane targeting mechanisms of the human reduced folate carrier in Mammalian epithelial cells. J. Biol. Chem. 277, 33325-33333.
23. Martin-Verdeaux, S., Pombo, I., Iannascoli, B., Roa, M., Varin-Blank, N., Rivera, J. and Blank, U. (2003). Evidence of a role for Munc18-2 and microtubules in mast cell granule exocytosis. J. Cell Sci. 116, 325-334.
24. Mueckler, M., Caruso, C., Baldwin, S. A., Panico, M., Blench, I., Morris, H. R., Allard, W. J., Lienhard, G. E. and Lodish, H. F. (1985). Sequence and structure of a human glucose transporter. Science 229, 941-945.
25. Nakayama, T., Fujiwara, T., Miyazawa, A., Asakawa, S., Shimizu, N., Shimizu, Y., Mikoshiba, K. and Akagawa, K. (1997). Mapping of the human HPC-1/syntaxin 1A gene (STX1A) to chromosome 7 band q11.2. Genomics 42, 173-176.
26. Nakayama, T., Matsuoka, R., Kimura, M., Hirota, H., Mikoshiba, K., Shimizu, Y., Shimizu, N. and Akagawa, K. (1998). Hemizygous deletion of the HPC-1/syntaxin 1A gene (STX1A) in patients with Williams syndrome. Cytogenet. Cell Genet. 82, 49-51.
27. Nakayama, T., Mikoshiba, K., Yamamori, T. and Akagawa, K. (2003). Expression of syntaxin 1C, an alternative splice variant of HPC-1/syntaxin 1A, is enhanced by phorbol-ester stimulation in astroglioma: participation of the PKC signaling pathway. FEBS Lett. 536, 209-214.
28. Nakayama, T., Mikoshiba, K., Yamamori, T. and Akagawa, K. (2004). Activation of syntaxin 1C, an alternative splice variant of HPC-1/syntaxin 1A, by phorbol 12-myristate 13-acetate (PMA) suppresses glucose transport into astroglioma cells via the glucose transporter-1 (GLUT-1). J. Biol. Chem. 279, 23728-23739.
29. Olson, A. L. and Pessin, J. E. (1996). Structure, function, and regulation of the mammalian facilitative glucose transporter gene family. Annu. Rev. Nutr. 16, 235-256.
30. Pereira, S., Massacrier, A., Roll, P., Verine, A., Etienne-Grimaldi, M. C., Poitelon, Y., Robaglia-Schlupp, A., Jamali, S., Roeckel-Trevisiol, N., Royer, B. et al. (2008). Nuclear localization of a novel human syntaxin 1B isoform. Gene 423, 160-171.
31. Perera, H. K., Clarke, M., Morris, N. J., Hong, W., Chamberlain, L. H. and Gould, G. W. (2003). Syntaxin 6 regulates Glut4 trafficking in 3T3-L1 adipocytes. Mol. Biol. Cell 14, 2946-2958.
32. Pooley, R. D., Moynihan, K. L., Soukoulis, V., Reddy, S., Francis, R., Lo, C., Ma, L. J. and Bader, D. M. (2008). Murine CENPF interacts with syntaxin 4 in the regulation of vesicular transport. J. Cell Sci. 121, 3413-3421.
33. Quinones, B., Riento, K., Olkkonen, V. M., Hardy, S. and Bennett, M. K. (1999). Syntaxin 2 splice variants exhibit differential expression patterns, biochemical properties and subcellular localizations. J. Cell Sci. 112, 4291-4304.
34. Reddy, A., Caler, E. V. and Andrews, N. W. (2001). Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106, 157-169.
35. Reed, B. C., Cefalu, C., Bellaire, B. H., Cardelli, J. A., Louis, T., Salamon, J., Bloecher, M. A. and Bunn, R. C. (2005). GLUT1CBP(TIP2/GIPC1) interactions with GLUT1 and myosin VI: evidence supporting an adapter function for GLUT1CBP. Mol. Biol. Cell 16, 4183-4201.
36. Ringhoff, D. N. and Cassimeris, L. (2009). Stathmin regulates centrosomal nucleation of microtubules and tubulin dimer/polymer partitioning. Mol. Biol. Cell 20, 3451-3458.
37. Rothman, J. E. (1994). Mechanisms of intracellular protein transport. Nature 372,55-63.
38. Sahlen, G. E., Egevad, L., Ahlander, A., Norlen, B. J., Ronquist, G. and Nilsson, B. O. (2002). Ultrastructure of the secretion of prostasomes from benign and malignant epithelial cells in the prostate. Prostate 53, 192-199.
39. Simonsen, A., Bremnes, B., Ronning, E., Aasland, R. and Stenmark, H. (1998). Syntaxin-16, a putative Golgi t-SNARE. Eur. J. Cell Biol. 75, 223-231.
40. Singh, S. P., Gao, Y., Singh, L. D., Kunapuli, S. P. and Ravindra, R. (1998). Role of microtubules in glucose uptake by C6 glioma cells. Pharmacol. Toxicol. 83, 83-89.
41. Su, Q., Cai, Q., Gerwin, C., Smith, C. L. and Sheng, Z. H. (2004). Syntabulin is a microtubule-associated protein implicated in syntaxin transport in neurons. Nat. Cell Biol. 6, 941-953.
42. Szodorai, A., Kuan, Y. H., Hunzelmann, S., Engel, U., Sakane, A., Sasaki, T., Takai, Y., Kirsch, J., Muller, U., Beyreuther, K. et al. (2009). APP anterograde transport requires Rab3A GTPase activity for assembly of the transport vesicle. J. Neurosci. 29, 14534-14544.
43. Teng, F. Y., Wang, Y. and Tang, B. L. (2001). The syntaxins. Genome Biol. 2, REVIEWS3012.
44. Tojima, T., Akiyama, H., Itofusa, R., Li, Y., Katayama, H., Miyawaki, A. and Kamiguchi, H. (2007). Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat. Neurosci. 10, 58-66.
45. Tong, P., Khayat, Z. A., Huang, C., Patel, N., Ueyama, A. and Klip, A. (2001). Insulin-induced cortical actin remodeling promotes GLUT4 insertion at muscle cell membrane ruffles. J. Clin. Invest. 108, 371-381.
46. Wang, Q., Bilan, P. J., Tsakiridis, T., Hinek, A. and Klip, A. (1998). Actin filaments participate in the relocalization of phosphatidylinositol3-kinase to glucose transporter-containing compartments and in the stimulation of glucose uptake in 3T3-L1 adipocytes. Biochem. J. 331, 917-928.
47. Wittmann, T. and Waterman-Storer, C. M. (2001). Cell motility: can Rho GTPases and microtubules point the way? J. Cell Sci. 114, 3795-3803.