Regulation of intracellular membrane trafficking and cell dynamics by syntaxin-6

Bioscience Reports

Volumn 32, Issue 4, 2012, Pages 383-391

  Jung, Jae Joon ^a   Inamdar, Shivangi M ^a   Tiwari, Ajit ^a   Choudhury, Amit ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PROTEIN VAMP7; PROTEIN VAMP8; SNARE PROTEIN; SOLUBLE N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN; SYNAPTOBREVIN 1; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN I; SYNTAXIN; SYNTAXIN 6; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ALZHEIMER DISEASE; ANGIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE PERMEABILITY; CYSTIC FIBROSIS; EPITHELIUM CELL; EXOCYTOSIS; HUMAN; IMMUNOCOMPETENT CELL; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; NERVE CELL; NONHUMAN; PARATHYROID GLAND; PARKINSON DISEASE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVIEW; STRUCTURE ACTIVITY RELATION; TAUOPATHY;

ANIMALS; ENDOCYTOSIS; ENDOTHELIAL CELLS; HUMANS; INTRACELLULAR MEMBRANES; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SECRETORY VESICLES; SNARE PROTEINS;

MAMMALIA;

EID: 84863705415     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120006     Document Type: Review

References (89)

1. Hong, W. (2005) SNAREs and traffic. Biochim. Biophys. Acta 1744, 120-144
2. Jahn, R. and Scheller, R. H. (2006) SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643 (Pubitemid 44268209)
3. Ungermann, C. and Langosch, D. (2005) Functions of SNAREs in intracellular membrane fusion and lipid bilayer mixing. J. Cell Sci. 118, 3819-3828 (Pubitemid 41410266)
4. Gonzalo, S. and Linder, M. E. (1998) SNAP-25 palmitoylation and plasma membrane targeting require a functional secretory pathway. Mol. Biol. Cell 9, 585-597 (Pubitemid 28125618)
5. Lacy,P. (2005) The role of Rho GTPases and SNAREs in mediator release from granulocytes. Pharmacol. Ther. 107, 358-376
6. Logan, M. R., Odemuyiwa, S. O. and Moqbel, R. (2003) Understanding exocytosis in immune and inflammatory cells: the molecular basis of mediator secretion. J. Allergy Clin. Immunol. 111, 923-932 (Pubitemid 36570847)
7. Wang, Y. and Tang, B. L. (2006) SNAREs in neurons-beyond synaptic vesicle exocytosis. Mol. Membr. Biol. 23, 377-384 (Pubitemid 44630021)
8. Hou, J. C., Min, L. and Pessin, J. E. (2009) Insulin granule biogenesis, trafficking and exocytosis. Vitam. Horm. 80, 473-506
9. Jewell, J. L., Oh, E. and Thurmond, D. C. (2010) Exocytosis mechanisms underlying insulin release and glucose uptake: conserved roles for Munc18c and syntaxin 4. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R517-R531
10. Benado, A., Nasagi-Atiya, Y. and Sagi-Eisenberg, R. (2009) Protein trafficking in immune cells. Immunobiology 214, 507-525
11. Stow, J. L., Manderson, A. P. and Murray, R. Z. (2006) SNAREing immunity: the role of SNAREs in the immune system. Nat. Rev. Immunol. 6, 919-929 (Pubitemid 44851734)
12. Reales, E., Mora-Lopez, F., Rivas, V., Garcia-Poley, A., Brieva, J. A. and Campos-Caro, A. (2005) Identification of soluble N-ethylmaleimide-sensitive factor attachment protein receptor exocytotic machinery in human plasma cells: SNAP-23 is essential for antibody secretion. J. Immunol. 175, 6686-6693 (Pubitemid 41598912)
13. Chen, D., Bernstein, A. M., Lemons, P. P. and Whiteheart, S. W. (2000) Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 in dense core granule release. Blood 95, 921-929 (Pubitemid 30062714)
14. Chen, D., Lemons, P. P., Schraw, T. and Whiteheart, S. W. (2000) Molecular mechanisms of platelet exocytosis: role of SNAP-23 and syntaxin 2 and 4 in lysosome release. Blood 96, 1782-1788 (Pubitemid 30661062)
15. Feng, D., Crane, K., Rozenvayn, N., Dvorak, A. M. and Flaumenhaft, R. (2002) Subcellular distribution of 3 functional platelet SNARE proteins: human cellubrevin, SNAP-23, and syntaxin 2. Blood 99, 4006-4014 (Pubitemid 35332041)
16. Polgar, J., Chung, S. H. and Reed, G. L. (2002) Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 100, 1081-1083 (Pubitemid 34832645)
17. Brumell, J. H., Volchuk, A., Sengelov, H., Borregaard, N., Cieutat, A. M., Bainton, D. F., Grinstein, S. and Klip, A. (1995) Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments. J. Immunol. 155, 5750-5759
18. Martin-Martin, B., Nabokina, S. M., Blasi, J., Lazo, P. A. and Mollinedo, F. (2000) Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis. Blood 96, 2574-2583
19. Mollinedo, F., Calafat, J., Janssen, H., Martin-Martin, B., Canchado, J., Nabokina, S. M. and Gajate, C. (2006) Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils. J. Immunol. 177, 2831-2841 (Pubitemid 44277798)
20. Mollinedo, F., Martin-Martin, B., Calafat, J., Nabokina, S. M. and Lazo, P. A. (2003) Role of vesicle-associated membrane protein-2, through Q-soluble N-ethylmaleimide-sensitive factor attachment protein receptor/R-soluble N-ethylmaleimide-sensitive factor attachment protein receptor interaction, in the exocytosis of specific and tertiary granules of human neutrophils. J. Immunol. 170, 1034-1042 (Pubitemid 36070559)
21. Logan, M. R., Lacy, P., Odemuyiwa, S. O., Steward, M., Davoine, F., Kita, H. and Moqbel, R. (2006) A critical role for vesicle-associated membrane protein-7 in exocytosis from human eosinophils and neutrophils. Allergy 61, 777-784 (Pubitemid 43801414)
22. Xie, L. X., Calafat, J., Janssen, H., de la Iglesia-Vicente, J. and Mollinedo, F. (2010) Intracellular location of syntaxin 7 in human neutrophils. Immunol. Lett. 129, 72-77
23. Hoffmann, H. J., Bjerke, T., Karawajczyk, M., Dahl, R., Knepper, M. A. and Nielsen, S. (2001) SNARE proteins are critical for regulated exocytosis of ECP from human eosinophils. Biochem. Biophys. Res. Commun. 282, 194-199 (Pubitemid 32924364)
24. Logan, M. R., Lacy, P., Bablitz, B. and Moqbel, R. (2002) Expression of eosinophil target SNAREs as potential cognate receptors for vesicle-associated membrane protein-2 in exocytosis. J. Allergy Clin. Immunol. 109, 299-306 (Pubitemid 34158298)
25. Frank, S. P., Thon, K. P., Bischoff, S. C. and Lorentz, A. (2011) SNAP-23 and syntaxin-3 are required for chemokine release by mature human mast cells. Mol. Immunol. 49, 353-358
26. Sander, L. E., Frank, S. P., Bolat, S., Blank, U., Galli, T., Bigalke, H., Bischoff, S. C. and Lorentz, A. (2008) Vesicle associated membrane protein (VAMP)-7 and VAMP-8, but not VAMP-2 or VAMP-3, are required for activation-induced degranulation of mature human mast cells. Eur. J. Immunol. 38, 855-863
27. Nagai, Y., Tadokoro, S., Sakiyama, H. and Hirashima, N. (2011) Effects of synaptotagmin 2 on membrane fusion between liposomes that contain SNAREs involved in exocytosis in mast cells. Biochim. Biophys. Acta 1808, 2435-2439
28. Tadokoro, S., Nakanishi, M. and Hirashima, N. (2010) Complexin II regulates degranulation in RBL-2H3 cells by interacting with SNARE complex containing syntaxin-3. Cell Immunol. 261, 51-56
29. Veale, K. J., Offenhauser, C., Lei, N., Stanley, A. C., Stow, J. L. and Murray, R. Z. (2011) VAMP3 regulates podosome organisation in macrophages and together with Stx4/SNAP23 mediates adhesion, cell spreading and persistent migration. Exp. Cell Res. 317, 1817-1829
30. Offenhauser, C., Lei, N., Roy, S., Collins, B. M., Stow, J. L. and Murray, R. Z. (2011) Syntaxin 11 binds Vti1b and regulates late endosome to lysosome fusion in macrophages. Traffic 12, 762-773
31. 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 (Pubitemid 27073745)
32. Kimura, K., Mizoguchi, A. and Ide, C. (2003) Regulation of growth cone extension by SNARE proteins. J. Histochem. Cytochem. 51, 429-433 (Pubitemid 36418039)
33. Tafoya, L. C., Shuttleworth, C. W., Yanagawa, Y., Obata, K. and Wilson, M. C. (2008) The role of the t-SNARE SNAP-25 in action potential-dependent calcium signaling and expression in GABAergic and glutamatergic neurons. BMC Neurosci. 9, 105
34. Sorensen, J. B. (2004) Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch. 448, 347-362
35. Nagy, G., Kim, J. H., Pang, Z. P., Matti, U., Rettig, J., Sudhof, T. C. and Sorensen, J. B. (2006) Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26, 632-643 (Pubitemid 43237128)
36. Herrick, D. Z., Sterbling, S., Rasch, K. A., Hinderliter, A. and Cafiso, D. S. (2006) Position of synaptotagmin I at the membrane interface: cooperative interactions of tandem C2 domains. Biochemistry 45, 9668-9674 (Pubitemid 44257414)
37. Hui, E., Bai, J. and Chapman, E. R. (2006) Ca2+-triggered simultaneous membrane penetration of the tandem C2-domains of synaptotagmin I. Biophys. J. 91, 1767-1777 (Pubitemid 44352441)
38. Markin, V. S. and Albanesi, J. P. (2002) Membrane fusion: stalk model revisited. Biophys. J. 82, 693-712 (Pubitemid 34111211)
39. Fernandez-Chacon, R., Konigstorfer, A., Gerber, S. H., Garcia, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C. and Sudhof, T. C. (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49 (Pubitemid 32225830)
40. Rhee, J. S., Li, L. Y., Shin, O. H., Rah, J. C., Rizo, J., Sudhof, T. C. and Rosenmund, C. (2005) Augmenting neurotransmitter release by enhancing the apparent Ca2+ affinity of synaptotagmin 1. Proc. Natl. Acad. Sci. U.S.A. 102, 18664-18669 (Pubitemid 43011283)
41. Pang, Z. P., Shin, O. H., Meyer, A. C., Rosenmund, C. and Sudhof, T. C. (2006) A gain-of-function mutation in synaptotagmin-1 reveals a critical role of Ca2+-dependent soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex binding in synaptic exocytosis. J. Neurosci. 26, 12556-12565 (Pubitemid 44864520)
42. Sudhof, T. C. and Rothman, J. E. (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477
43. Feldmann, A., Winterstein, C., White, R., Trotter, J. and Kramer-Albers, E. M. (2009) Comprehensive analysis of expression, subcellular localization, and cognate pairing of SNARE proteins in oligodendrocytes. J. Neurosci. Res. 87, 1760-1772
44. Steiner, P., Alberi, S., Kulangara, K., Yersin, A., Sarria, J. C., Regulier, E., Kasas, S., Dietler, G., Muller, D., Catsicas, S. and Hirling, H. (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J. 24, 2873-2884 (Pubitemid 43079891)
45. Barakauskas, V. E., Beasley, C. L., Barr, A. M., Ypsilanti, A. R., Li, H. Y., Thornton, A. E., Wong, H., Rosokilja, G., Mann, J. J., Mancevski, B. et al. (2010) A novel mechanism and treatment target for presynaptic abnormalities in specific striatal regions in schizophrenia. Neuropsychopharmacology 35, 1226-1238
46. Chana, G., Lucero, G., Salaria, S., Lozach, J., Du, P., Woelk, C. and Everall, I. (2009) Upregulation of NRG-1 and VAMP-1 in human brain aggregates exposed to clozapine. Schizophr. Res. 113, 273-276
47. Gray, L. J., Dean, B., Kronsbein, H. C., Robinson, P. J. and Scarr, E. (2010) Region and diagnosis-specific changes in synaptic proteins in schizophrenia and bipolar I disorder. Psychiatry Res. 178, 374-380
48. Honer, W. G., Falkai, P., Bayer, T. A., Xie, J., Hu, L., Li, H. Y., Arango, V., Mann, J. J., Dwork, A. J. and Trimble, W. S. (2002) Abnormalities of SNARE mechanism proteins in anterior frontal cortex in severe mental illness. Cereb. Cortex 12, 349-356 (Pubitemid 34226059)
49. Vetrivel, K. S., Cheng, H., Lin, W., Sakurai, T., Li, T., Nukina, N., Wong, P. C., Xu, H. and Thinakaran, G. (2004) Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 279, 44945-44954 (Pubitemid 39430908)
50. Curtis, L., Datta, P., Liu, X., Bogdanova, N., Heidelberger, R. and Janz, R. (2010) Syntaxin 3B is essential for the exocytosis of synaptic vesicles in ribbon synapses of the retina. Neuroscience 166, 832-841
51. Safieddine, S. and Wenthold, R. J. (1999) SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle- and synaptic membrane-associated proteins. Eur. J. Neurosci. 11, 803-812 (Pubitemid 29106041)
52. Lu, M., Forsberg, L., Hoog, A., Juhlin, C. C., Vukojevic, V., Larsson, C., Conigrave, A. D., Delbridge, L. W., Gill, A., Bark, C. et al. (2008) Heterogeneous expression of SNARE proteins SNAP-23, SNAP-25, Syntaxin1 and VAMP in human parathyroid tissue. Mol. Cell. Endocrinol. 287, 72-80
53. Wang, Z. and Thurmond, D. C. (2009) Mechanisms of biphasic insulin-granule exocytosis-roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 122, 893-903
54. Ostenson, C. G., Gaisano, H., Sheu, L., Tibell, A. and Bartfai, T. (2006) Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes 55, 435-440 (Pubitemid 43343274)
55. Chat, S., Layani, S., Mahaut, C., Henry, C., Chanat, E. and Truchet, S. (2011) Characterisation of the potential SNARE proteins relevant to milk product release by mouse mammary epithelial cells. Eur. J. Cell Biol. 90, 401-413
56. Bock, J. B., Lin, R. C. and Scheller, R. H. (1996) A new syntaxin family member implicated in targeting of intracellular transport vesicles. J. Biol. Chem. 271, 17961-17965 (Pubitemid 26250779)
57. Watson, R. T. and Pessin, J. E. (2000) Functional cooperation of two independent targeting domains in syntaxin 6 is required for its efficient localization in the trans-Golgi network of 3T3L1 adipocytes. J. Biol. Chem. 275, 1261-1268 (Pubitemid 30051179)
58. Bock, J. B., Klumperman, J., Davanger, S. and Scheller, R. H. (1997) Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell 8, 1261-1271 (Pubitemid 27310473)
59. Burkhardt, P., Hattendorf, D. A., Weis, W. I. and Fasshauer, D. (2008) Munc18a controls SNARE assembly through its interaction with the syntaxin N-peptide. EMBO J. 27, 923-933 (Pubitemid 351508147)
60. Dulubova, I., Yamaguchi, T., Gao, Y., Min, S. W., Huryeva, I., Sudhof, T. C. and Rizo, J. (2002) How Tlg2p/syntaxin 16 'snares' Vps45. EMBO J. 21, 3620-3631 (Pubitemid 34787036)
61. Choudhury, A., Marks, D. L., Proctor, K. M., Gould, G. W. and Pagano, R. E. (2006) Regulation of caveolar endocytosis by syntaxin 6-dependent delivery of membrane components to the cell surface. Nat. Cell Biol. 8, 317-328
62. Parton, R. G. and Simons, K. (2007) The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8, 185-194
63. Sharma, D. K., Brown, J. C., Choudhury, A., Peterson, T. E., Holicky, E., Marks, D. L., Simari, R., Parton, R. G. and Pagano, R. E. (2004) Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. Mol. Biol. Cell 15, 3114-3122 (Pubitemid 38850109)
64. Simonsen, A., Gaullier, J. M., D'Arrigo, A. and Stenmark, H. (1999) The Rab5 effector EEA1 interacts directly with syntaxin-6. J. Biol. Chem. 274, 28857-28860
65. Urano, Y., Watanabe, H., Murphy, S. R., Shibuya, Y., Geng, Y., Peden, A. A., Chang, C. C. and Chang, T. Y. (2008) Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc. Natl. Acad. Sci. U.S.A. 105, 16513-16518
66. Wendler, F., Page, L., Urbe, S. and Tooze, S. A. (2001) Homotypic fusion of immature secretory granules during maturation requires syntaxin 6. Mol. Biol. Cell 12, 1699-1709 (Pubitemid 33049723)
67. Ahras, M., Otto, G. P. and Tooze, S. A. (2006) Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J. Cell Biol. 173, 241-251
68. Zwilling, D., Cypionka, A., Pohl, W. H., Fasshauer, D., Walla, P. J., Wahl, M. C. and Jahn, R. (2007) Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies. EMBO J. 26, 9-18 (Pubitemid 46094695)
69. Tiwari, A., Jung, J. J., Inamdar, S. M., Brown, C. O., Goel, A. and Choudhury, A. (2011) Endothelial cell migration on fibronectin is regulated by syntaxin 6-mediated {alpha}5{beta}1 integrin recycling. J. Biol. Chem. 286, 36749-36761
70. Mills, I. G., Urbe, S. and Clague, M. J. (2001) Relationships between EEA1 binding partners and their role in endosome fusion. J. Cell. Sci. 114, 1959-1965 (Pubitemid 32530050)
71. Moore, E. R., Mead, D. J., Dooley, C. A., Sager, J. and Hackstadt, T. (2011) The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157, 830-838
72. Madan, R., Rastogi, R., Parashuraman, S. and Mukhopadhyay, A. (2012) Salmonella acquires lysosome-associated membrane protein 1 (LAMP1) on phagosomes from Golgi via SipC pProtein-mediated recruitment of host syntaxin 6. J. Biol. Chem. 287, 5574-5587
73. Nakamura, N., Fukuda, H., Kato, A. and Hirose, S. (2005) MARCH-II is a syntaxin-6-binding protein involved in endosomal trafficking. Mol. Biol. Cell 16, 1696-1710 (Pubitemid 40471941)
74. Otto, G. P., Razi, M., Morvan, J., Stenner, F. and Tooze, S. A. (2010) A novel syntaxin 6-interacting protein, SHIP164, regulates syntaxin 6-dependent sorting from early endosomes. Traffic 11, 688-705
75. Laufman, O., Hong, W. and Lev, S. (2011) The COG complex interacts directly with Syntaxin 6 and positively regulates endosome-to-TGN retrograde transport. J. Cell Biol. 194, 459-472
76. Klumperman, J., Kuliawat, R., Griffith, J. M., Geuze, H. J. and Arvan, P. (1998) Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J. Cell Biol. 141, 359-371 (Pubitemid 28237085)
77. Kuliawat, R., Kalinina, E., Bock, J., Fricker, L., McGraw, T. E., Kim, S. R., Zhong, J., Scheller, R. and Arvan, P. (2004) Syntaxin-6 SNARE involvement in secretory and endocytic pathways of cultured pancreatic beta-cells. Mol. Biol. Cell 15, 1690-1701 (Pubitemid 38401819)
78. 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 (Pubitemid 36871533)
79. Watson, R. T., Hou, J. C. and Pessin, J. E. (2008) Recycling of IRAP from the plasma membrane back to the insulin-responsive compartment requires the Q-SNARE syntaxin 6 but not the GGA clathrin adaptors. J. Cell Sci. 121, 1243-1251 (Pubitemid 351753508)
80. Yeh, T. Y., Sbodio, J. I., Tsun, Z. Y., Luo, B. and Chi, N. W. (2007) Insulin-stimulated exocytosis of GLUT4 is enhanced by IRAP and its partner tankyrase. Biochem. J. 402, 279-290 (Pubitemid 46383425)
81. Murray, R. Z., Wylie, F. G., Khromykh, T., Hume, D. A. and Stow, J. L. (2005) Syntaxin 6 and Vti1b form a novel SNARE complex, which is up-regulated in activated macrophages to facilitate exocytosis of tumor necrosis factor-alpha. J. Biol. Chem. 280, 10478-10483 (Pubitemid 40395906)
82. 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
83. Dejana, E., Tournier-Lasserve, E. and Weinstein, B. M. (2009) The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev. Cell 16, 209-221
84. Weis, S. M. and Cheresh, D. A. (2005) Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437, 497-504 (Pubitemid 41613541)
85. Manickam, V., Tiwari, A., Jung, J. J., Bhattacharya, R., Goel, A., Mukhopadhyay, D. and Choudhury, A. (2011) Regulation of vascular endothelial growth factor receptor 2 trafficking and angiogenesis by Golgi localized t-SNARE syntaxin 6. Blood 117, 1425-1435
86. Zhang, Y., Shu, L. and Chen, X. (2008) Syntaxin 6, a regulator of the protein trafficking machinery and a target of the p53 family, is required for cell adhesion and survival. J. Biol. Chem. 283, 30689-30698
87. Cheng, J., Cebotaru, V., Cebotaru, L. and Guggino, W. B. (2010) Syntaxin 6 and CAL mediate the degradation of the cystic fibrosis transmembrane conductance regulator. Mol. Biol. Cell 21, 1178-1187
88. Kabayama, H., Tokushige, N., Takeuchi, M. and Mikoshiba, K. (2008) Syntaxin 6 regulates nerve growth factor-dependent neurite outgrowth. Neurosci. Lett. 436, 340-344
89. Hoglinger, G. U., Melhem, N. M., Dickson, D. W., Sleiman, P. M., Wang, L. S., Klei, L., Rademakers, R., de Silva, R., Litvan, I., Riley, D. E. et al. (2011) Identification of common variants influencing risk of the tauopathy progressive supranuclear palsy. Nat. Genet. 43, 699-705