N-ethylmaleimide-sensitive factor attachment protein α (αSNAP) regulates matrix adhesion and integrin processing in human epithelial cells

Journal of Biological Chemistry

Volumn 289, Issue 4, 2014, Pages 2424-2439

  Naydenov, Nayden G ^a   Feygin, Alex ^a   Wang, Lifu ^b   Ivanov, Andrei I ^a,c  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Virginia Institute of Molecular Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DETACHMENT; CELL-MATRIX ADHESION; FOCAL ADHESIONS; HUMAN EPITHELIAL CELLS; MEMBRANE FUSION; NORMAL CONDITION; OVER-EXPRESSION; VESICLE TRAFFICKING;

CELL ADHESION; CELL MEMBRANES;

PROTEINS;

BETA1 INTEGRIN; CELL PROTEIN; N ETHYLMALEIMIDE SENSITIVE FACTOR; N ETHYLMALEIMIDE SENSITIVE FACTOR ATTACHMENT PROTEIN ALPHA; PROTEIN FA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FOCAL ADHESION; GOLGI COMPLEX; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY MECHANISM; SENSITIVITY ANALYSIS;

CELL ADHESION; CELL MIGRATION; CELL MOTILITY; SNARE PROTEINS; TRAFFICKING;

ANIMALS; ANTIGENS, CD29; CATTLE; CELL ADHESION; CELL LINE; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FOCAL ADHESION KINASE 1; GENE KNOCKDOWN TECHNIQUES; GOLGI APPARATUS; HUMANS; PAXILLIN; PHOSPHORYLATION; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS;

EID: 84893114457     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498691     Document Type: Article

References (87)

1. Bryant, D. M., and Mostov, K. E. (2008) From cells to organs. Building polarized tissue. Nat. Rev. Mol. Cell Biol. 9, 887-901
2. Schock, F., and Perrimon, N. (2002) Molecular mechanisms of epithelial morphogenesis. Annu. Rev. Cell Dev. Biol. 18, 463-493
3. Heath, J. P. (1996) Epithelial cell migration in the intestine. Cell Biol. Int 20, 139-146
4. Radtke, F., and Clevers, H. (2005) Self-renewal and cancer of the gut. Two sides of a coin. Science 307, 1904-1909
5. Condeelis, J., Singer, R. H., and Segall, J. E. (2005) The great escape. When cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21, 695-718
6. Mammen, J. M., and Matthews, J. B. (2003) Mucosal repair in the gastrointestinal tract. Crit. Care Med. 31, S532-537
7. Huttenlocher, A., and Horwitz, A. R. (2011) Integrins in cell migration. Cold Spring Harbor Perspect. Biol. 3, a005074
8. Sheppard, D. (1996) Epithelial integrins. Bioessays 18, 655-660
9. Wehrle-Haller, B. (2012) Structure and function of focal adhesions. Curr. Opin. Cell Biol. 24, 116-124
10. Wolfenson, H., Lavelin, I., and Geiger, B. (2013) Dynamic regulation of the structure and functions of integrin adhesions. Dev. Cell 24, 447-458
11. Zebda, N., Dubrovskyi, O., and Birukov, K. G. (2012) Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc. Res. 83, 71-81
12. Zhao, X., and Guan, J.-L. (2011) Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv. Drug Deliv. Rev. 63, 610-615
13. Kaverina, I., Krylyshkina, O., and Small, J. V. (2002) Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 34, 746-761
14. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T., and Horwitz, A. R. (2003) Cell migration. Integrating signals from front to back. Science 302, 1704-1709
15. Margadant, C., Monsuur, H. N., Norman, J. C., and Sonnenberg, A. (2011) Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614
16. Valdembri, D., and Serini, G. (2012) Regulation of adhesion site dynamics by integrin traffic. Curr. Opin. Cell Biol. 24, 582-591
17. Bonifacino, J. S., and Glick, B. S. (2004) The mechanisms of vesicle budding and fusion. Cell 116, 153-166
18. Zerial, M., and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117
19. Hong, W. (2005) SNAREs and traffic. Biochim Biophys Acta 1744, 120-144
20. Malsam, J., Kreye, S., and Söllner, T. H. (2008) Membrane fusion. SNAREs and regulation. Cell Mol. Life Sci. 65, 2814-2832
21. Day, P., Riggs, K. A., Hasan, N., Corbin, D., Humphrey, D., and Hu, C. (2011) Syntaxins 3 and 4 mediate vesicular trafficking of α5β1 and α3β1 integrins and cancer cell migration. Int. J. Oncol. 39, 863-871
22. Skalski, M., Yi, Q., Kean, M. J., Myers, D. W., Williams, K. C., Burtnik, A., and Coppolino, M. G. (2010) Lamellipodium extension and membrane ruffling require different SNARE-mediated trafficking pathways. BMC Cell Biol. 11, 62
23. Luftman, K., Hasan, N., Day, P., Hardee, D., and Hu, C. (2009) Silencing of VAMP3 inhibits cell migration and integrin-mediated adhesion. Biochem. Biophys. Res. Commun. 380, 65-70
24. Riggs, K. A., Hasan, N., Humphrey, D., Raleigh, C., Nevitt, C., Corbin, D., and Hu, C. (2012) Regulation of integrin endocytic recycling and chemotactic cell migration by syntaxin 6 and VAMP3 interaction. J. Cell Sci. 125, 3827-3839
25. 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 α5β1 integrin recycling. J. Biol. Chem. 286, 36749-36761
26. 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
27. Burgoyne, R. D., and Morgan, A. (1998) Analysis of regulated exocytosis in adrenal chromaffin cells. Insights into NSF/SNAP/SNARE function. Bioessays 20, 328-335
28. Whiteheart, S. W., Schraw, T., and Matveeva, E. A. (2001)N-Ethylmaleimide sensitive factor (NSF) structure and function. Int. Rev. Cytol. 207, 71-112
29. Andreeva, A. V., Kutuzov, M. A., and Voyno-Yasenetskaya, T. A. (2006) A ubiquitous membrane fusion protein αSNAP. A potential therapeutic target for cancer, diabetes and neurological disorders? Expert Opin. Ther. Targets 10, 723-733
30. Zhao, C., Smith, E. C., and Whiteheart, S. W. (2012) Requirements for the catalytic cycle of the N-ethylmaleimide-sensitive factor (NSF). Biochim. Biophys. Acta 1823, 159-171
31. Morrell, C. N., Matsushita, K., and Lowenstein, C. J. (2005) A novel inhibitor of N-ethylmaleimide-sensitive factor decreases leukocyte trafficking and peritonitis. J. Pharmacol. Exp. Ther. 314, 155-161
32. Skalski, M., and Coppolino, M. G. (2005) SNARE-mediated trafficking of α5β1 integrin is required for spreading in CHO cells. Biochem. Biophys. Res. Commun. 335, 1199-1210
33. Skalski, M., Sharma, N., Williams, K., Kruspe, A., and Coppolino, M. G. (2011) SNARE-mediated membrane traffic is required for focal adhesion kinase signaling and Src-regulated focal adhesion turnover. Biochim. Biophys. Acta 1813, 148-158
34. Naydenov, N. G., Brown, B., Harris, G., Dohn, M. R., Morales, V. M., Baranwal, S., Reynolds, A. B., and Ivanov, A. I. (2012) A membrane fusion protein αSNAP is a novel regulator of epithelial apical junctions. PLoS One 7, e34320
35. Naydenov, N. G., Harris, G., Brown, B., Schaefer, K. L., Das, S. K., Fisher, P. B., and Ivanov, A. I. (2012) Loss of soluble N-ethylmaleimide-sensitive factor attachment protein alpha (αSNAP) induces epithelial cell apoptosis via down-regulation of Bcl-2 expression and disruption of the Golgi. J. Biol. Chem. 287, 5928-5941
36. Naydenov, N. G., Harris, G., Morales, V., and Ivanov, A. I. (2012) Loss of a membrane trafficking protein αSNAP induces non-canonical autophagy in human epithelia. Cell Cycle 11, 4613-4625
37. Wang, L., and Brautigan, D. L. (2013)α-SNAP inhibits AMPK signaling to reduce mitochondrial biogenesis and dephosphorylates Thr-172 in AMPKα in vitro. Nat. Commun. 4, 1559
38. Le Bivic, A., Real, F. X., and Rodriguez-Boulan, E. (1989) Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line. Proc. Natl. Acad. Sci. U.S.A. 86, 9313-9317
39. Naydenov, N. G., Hopkins, A. M., and Ivanov, A. I. (2009) c-Jun N-terminal kinase mediates disassembly of apical junctions in model intestinal epithelia. Cell Cycle 8, 2110-2121
40. Ivanov, A. I., Bachar, M., Babbin, B. A., Adelstein, R. S., Nusrat, A., and Parkos, C. A. (2007) A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS One 2, e658
41. Wu, Z.-Z., Chow, K.-P. N., Kuo, T.-C., Chang, Y.-S., and Chao, C. C. K. (2011) Latent membrane protein 1 of Epstein-Barr virus sensitizes cancer cells to cisplatin by enhancing NF-κB p50 homodimer formation and down-regulating NAPA expression. Biochem. Pharmacol. 82, 1860-1872
42. Naydenov, N. G., and Ivanov, A. I. (2010) Adducins regulate remodeling of apical junctions in human epithelial cells. Mol. Biol. Cell 21, 3506-3517
43. Babbin, B. A., Koch, S., Bachar, M., Conti, M.-A., Parkos, C. A., Adelstein, R. S., Nusrat, A., and Ivanov, A. I. (2009) Non-muscle myosin IIA differentially regulates intestinal epithelial cell restitution and matrix invasion. Am. J. Pathol. 174, 436-448
44. Rankin, C. R., Hilgarth, R. S., Leoni, G., Kwon, M., Den Beste, K. A., Parkos, C. A., and Nusrat, A. (2013) Annexin A2 regulates β1 integrin internalization and intestinal epithelial cell migration. J. Biol. Chem. 288, 15229-15239
45. Akiyama, S. K., and Yamada, K. M. (1987) Biosynthesis and acquisition of biological activity of the fibronectin receptor. J. Biol. Chem. 262, 17536-17542
46. Wu, Z.-Z., and Chao, C. C. (2010) Knockdown of NAPA using shorthairpin RNA sensitizes cancer cells to cisplatin. Implications to overcome chemoresistance. Biochem. Pharmacol. 80, 827-837
47. Barnard, R. J., Morgan, A., and Burgoyne, R. D. (1997) Stimulation of NSF ATPase activity by alpha-SNAP is required for SNARE complex disassembly and exocytosis. J. Cell Biol. 139, 875-883
48. Jackson, C. L. (2000) Brefeldin A revealing the fundamental principles governing membrane dynamics and protein transport. Subcell. Biochem. 34, 233-272
49. Sáenz, J. B., Sun, W. J., Chang, J. W., Li, J., Bursulaya, B., Gray, N. S., and Haslam, D. B. (2009) Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat. Chem. Biol. 5, 157-165
50. Kawamoto, K., Yoshida, Y., Tamaki, H., Torii, S., Shinotsuka, C., Yamashina, S., and Nakayama, K. (2002) GBF1, a guanine nucleotide exchange factor for ADP-ribosylation factors, is localized to the cis-Golgi and involved in membrane association of the COPI coat. Traffic 3, 483-495
51. Niu, T.-K., Pfeifer, A. C., Lippincott-Schwartz, J., and Jackson, C. L. (2005) Dynamics of GBF1, a brefeldin A-sensitive Arf1 exchange factor at the Golgi. Mol. Biol. Cell 16, 1213-1222
52. Hotchin, N. A., and Watt, F. M. (1992) Transcriptional and post-translational regulation of β1 integrin expression during keratinocyte terminal differentiation. J. Biol. Chem. 267, 14852-14858
53. Veiga, S. S., Chammas, R., Cella, N., and Brentani, R. R. (1995) Glycosylation of β1 integrins in B16-F10 mouse melanoma cells as determinant of differential binding and acquisition of biological activity. Int. J. Cancer 61, 420-424
54. Chrispeels, M. J., Higgins, T. J., Craig, S., and Spencer, D. (1982) Role of the endoplasmic reticulum in the synthesis of reserve proteins and the kinetics of their transport to protein bodies in developing pea cotyledons. J. Cell Biol. 93, 5-14
55. Tulsiani, D. R., Harris, T. M., and Touster, O. (1982) Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of Golgi mannosidase II. J. Biol. Chem. 257, 7936-7939
56. Akiyama, S. K., Yamada, S. S., Chen, W. T., and Yamada, K. M. (1989) Analysis of fibronectin receptor function with monoclonal antibodies. Roles in cell adhesion, migration, matrix assembly, and cytoskeletal organization. J. Cell Biol. 109, 863-875
57. Tse, K. W., Dang-Lawson, M., Lee, R. L., Vong, D., Bulic, A., Buckbinder, L., and Gold, M. R. (2009) B cell receptor-induced phosphorylation of Pyk2 and focal adhesion kinase involves integrins and the Rap GTPases and is required for B cell spreading. J. Biol. Chem. 284, 22865-22877
58. Fletcher, S. J., and Rappoport, J. Z. (2009) The role of vesicle trafficking in epithelial cell motility. Biochem. Soc. Trans. 37, 1072-1076
59. Hendrix, A., Westbroek, W., Bracke, M., and De Wever, O. (2010) An ex(o)citing machinery for invasive tumor growth. Cancer Res. 70, 9533-9537
60. Jung, J.-J., Inamdar, S. M., Tiwari, A., and Choudhury, A. (2012) Regulation of intracellular membrane trafficking and cell dynamics by syntaxin-6. Biosci. Rep. 32, 383-391
61. Babcock, M., Macleod, G. T., Leither, J., and Pallanck, L. (2004) Genetic analysis of soluble N-ethylmaleimide-sensitive factor attachment protein function in Drosophila reveals positive and negative secretory roles. J. Neurosci. 24, 3964-3973
62. Chae, T. H., Kim, S., Marz, K. E., Hanson, P. I., and Walsh, C. A. (2004) The hyh mutation uncovers roles for αSnap in apical protein localization and control of neural cell fate. Nat. Genet. 36, 264-270
63. Hong, H.-K., Chakravarti, A., and Takahashi, J. S. (2004) The gene for soluble N-ethylmaleimide sensitive factor attachment protein α is mutated in hydrocephaly with hop gait (hyh) mice. Proc. Natl. Acad. Sci. U.S.A. 101, 1748-1753
64. Bátiz, L. F., Páez, P., Jiménez, A. J., Rodríguez, S., Wagner, C., Pérez-Fígares, J. M., and Rodríguez, E. M. (2006) Heterogeneous expression of hydrocephalic phenotype in the hyh mice carrying a point mutation in α-SNAP. Neurobiol. Dis. 23, 152-168
65. Ferland, R. J., Batiz, L. F., Neal, J., Lian, G., Bundock, E., Lu, J., Hsiao, Y.-C., Diamond, R., Mei, D., Banham, A. H., Brown, P. J., Vanderburg, C. R., Joseph, J., Hecht, J. L., Folkerth, R., Guerrini, R., Walsh, C. A., Rodriguez, E. M., and Sheen, V. L. (2009) Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum. Mol. Genet. 18, 497-516
66. Roales-Buján, R., Páez, P., Guerra, M., Rodríguez, S., Vío, K., Ho-Plagaro, A., García-Bonilla, M., Rodríguez-Pérez, L. M., Domínguez-Pinos, M. D., Rodríguez, E. M., Pérez-Fígares, J. M., and Jiménez, A. J. (2012) Astrocytes acquire morphological and functional characteristics of ependymal cells following disruption of ependyma in hydrocephalus. Acta Neuropathol. 124, 531-546
67. DiMilla, P. A., Stone, J. A., Quinn, J. A., Albelda, S. M., and Lauffenburger, D. A. (1993) Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122, 729-737
68. Gupton, S. L., and Waterman-Storer, C. M. (2006) Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125, 1361-1374
69. Clary, D. O., Griff, I. C., and Rothman, J. E. (1990) SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 61, 709-721
70. Whiteheart, S. W., Brunner, M., Wilson, D. W., Wiedmann, M., and Rothman, J. E. (1992) Soluble N-ethylmaleimide-sensitive fusion attachment proteins (SNAPs) bind to a multi-SNAP receptor complex in Golgi membranes. J. Biol. Chem. 267, 12239-12243
71. Shen, X., Hong, M.-S., Moss, J., and Vaughan, M. (2007) BIG1, a brefeldin A-inhibited guanine nucleotide-exchange protein, is required for correct glycosylation and function of integrin β1. Proc. Natl. Acad. Sci. U.S.A. 104, 1230-1235
72. Zou, K., Hosono, T., Nakamura, T., Shiraishi, H., Maeda, T., Komano, H., Yanagisawa, K., and Michikawa, M. (2008) Novel role of presenilins in maturation and transport of integrin β1. Biochemistry 47, 3370-3378
73. Parvani, J. G., Galliher-Beckley, A. J., Schiemann, B. J., and Schiemann, W. P. (2013) Targeted inactivation of beta1 integrin induces β3 integrin switching, which drives breast cancer metastasis by TGF-β. Mol. Biol. Cell 24, 3449-3459
74. Chen, P.-W., and Kroog, G. S. (2010) Leupaxin is similar to paxillin in focal adhesion targeting and tyrosine phosphorylation but has distinct roles in cell adhesion and spreading. Cell Adh. Migr. 4, 527-540
75. Deakin, N. O., and Turner, C. E. (2011) Distinct roles for paxillin and Hic-5 in regulating breast cancer cell morphology, invasion, and metastasis. Mol. Biol. Cell 22, 327-341
76. Hervy, M., Hoffman, L., and Beckerle, M. C. (2006) From the membrane to the nucleus and back again. Bifunctional focal adhesion proteins. Curr. Opin. Cell Biol. 18, 524-532
77. Manabe, R., Kovalenko, M., Webb, D. J., and Horwitz, A. R. (2002) GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J. Cell Sci. 115, 1497-1510
78. Spiczka, K. S., and Yeaman, C. (2008) Ral-regulated interaction between Sec5 and paxillin targets Exocyst to focal complexes during cell migration. J. Cell Sci. 121, 2880-2891
79. Low, S. H., Chapin, S. J., Wimmer, C., Whiteheart, S. W., Kömüves, L. G., Mostov, K. E., and Weimbs, T. (1998) The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J. Cell Biol. 141, 1503-1513
80. Aoki, T., Kojima, M., Tani, K., and Tagaya, M. (2008) Sec22b-dependent assembly of endoplasmic reticulum Q-SNARE proteins. Biochem. J. 410, 93-100
81. Rabouille, C., Kondo, H., Newman, R., Hui, N., Freemont, P., and Warren, G. (1998) Syntaxin 5 is a common component of the NSF-and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell 92, 603-610
82. Jahn, R., and Scheller, R. H. (2006) SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643
83. Peter, F., Wong, S. H., Subramaniam, V. N., Tang, B. L., and Hong, W. (1998) α-SNAP but not α-SNAP is required for ER-Golgi transport after vesicle budding and the Rab1-requiring step but before the EGTA-sensitive step. J. Cell Sci. 111, 2625-2633
84. Nishiwaki, Y., Yoshizawa, A., Kojima, Y., Oguri, E., Nakamura, S., Suzuki, S., Yuasa-Kawada, J., Kinoshita-Kawada, M., Mochizuki, T., and Masai, I. (2013) The BH3-only SNARE BNip1 mediates photoreceptor apoptosis in response to vesicular fusion defects. Dev. Cell 25, 374-387
85. Grabowski, P., Schönfelder, J., Ahnert-Hilger, G., Foss, H.-D., Heine, B., Schindler, I., Stein, H., Berger, G., Zeitz, M., and Scherübl, H. (2002) Expression of neuroendocrine markers. A signature of human undifferentiated carcinoma of the colon and rectum. Virchows Arch. 441, 256-263
86. Weitzdoerfer, R., Dierssen, M., Fountoulakis, M., and Lubec, G. (2001) Fetal life in Down syndrome starts with normal neuronal density but impaired dendritic spines and synaptosomal structure. J. Neural Transm. Suppl. 61, 59-70
87. Morton, A. J., Faull, R. L., and Edwardson, J. M. (2001) Abnormalities in the synaptic vesicle fusion machinery in Huntington's disease. Brain Res. Bull. 56, 111-117