Annexin A2 regulates β1 integrin internalization and intestinal epithelial cell migration

Journal of Biological Chemistry

Volumn 288, Issue 21, 2013, Pages 15229-15239

  Rankin, Carl R ^a   Hilgarth, Roland S ^a   Leoni, Giovanna ^a   Kwon, Mike ^a   Den Beste, Kyle A ^a   Parkos, Charles A ^a   Nusrat, Asma ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN-BINDING PROTEINS; ADHESIVE PROPERTIES; CELL-MATRIX ADHESION; EPITHELIAL BARRIER; EPITHELIAL CELLS; FUNCTION APPROACHES; INFLAMMATORY DISORDERS; INTESTINAL EPITHELIAL CELLS;

ADHESION; ANTIBIOTICS; BIOMATERIALS; CELL MEMBRANES; CYTOLOGY; TISSUE; TISSUE HOMEOSTASIS;

PROTEINS;

BETA1 INTEGRIN; LIPOCORTIN 2; SHORT HAIRPIN RNA;

ARTICLE; BIOTINYLATION; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; INTERNALIZATION; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REGULATORY MECHANISM;

Β1 INTEGRIN; ANNEXIN 2; ANNEXIN A2; CELL MIGRATION; ENDOCYTOSIS; INTEGRIN; INTESTINAL EPITHELIUM; WOUND HEALING;

ANNEXIN A2; ANTIGENS, CD29; CACO-2 CELLS; CELL ADHESION; CELL MOVEMENT; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; INTESTINAL MUCOSA; PROTEIN TRANSPORT; PROTEOLYSIS; WOUND HEALING;

EID: 84878225314     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.440909     Document Type: Article

References (50)

1. Rutten, M. J., and Ito, S. (1983) Morphology and electrophysiology of guinea pig gastric mucosal repair in vitro. Am. J. Physiol. 244, G171-182 (Pubitemid 13194889)
2. Crosnier, C., Stamataki, D., and Lewis, J. (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet. 7, 349-359
3. Blikslager, A. T., Moeser, A. J., Gookin, J. L., Jones, S. L., and Odle, J. (2007) Restoration of barrier function in injured intestinal mucosa. Physiol. Rev. 87, 545-564 (Pubitemid 47084680)
4. Caswell, P. T., Vadrevu, S., and Norman, J. C. (2009) Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10, 843-853
5. 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
6. Bretscher, M. S. (1989) Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8, 1341-1348
7. Raub, T. J., and Kuentzel, S. L. (1989) Kinetic and morphological evidence for endocytosis of mammalian cell integrin receptors by using an anti-fibronectin receptor beta subunit monoclonal antibody. Exp. Cell Res. 184, 407-426 (Pubitemid 19259724)
8. Lotz, M. M., Nusrat, A., Madara, J. L., Ezzell, R., Wewer, U. M., and Mercurio, A. M. (1997) Intestinal epithelial restitution. Involvement of specific laminin isoforms and integrin laminin receptors in wound closure of a transformed model epithelium. Am. J. Pathol. 150, 747-760 (Pubitemid 27073801)
9. Mandell, K. J., Babbin, B. A., Nusrat, A., and Parkos, C. A. (2005) Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on beta1 integrins and Rap1 activity. J. Biol. Chem. 280, 11665-11674 (Pubitemid 40418481)
10. Chen, P., Abacherli, L. E., Nadler, S. T., Wang, Y., Li, Q., and Parks, W. C. (2009) MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting α(2)β(1) integrin activation. PloS one 4, e6565
11. Vassilieva, E. V., Gerner-Smidt, K., Ivanov, A. I., and Nusrat, A. (2008) Lipid rafts mediate internalization ofβ1-integrin in migrating intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 295, G965-976
12. Wang, C., Yoo, Y., Fan, H., Kim, E., Guan, K. L., and Guan, J. L. (2010) Regulation of Integrin beta 1 recycling to lipid rafts by Rab1a to promote cell migration. J. Biol. Chem. 285, 29398-29405
13. Babbin, B. A., Parkos, C. A., Mandell, K. J., Winfree, L. M., Laur, O., Ivanov, A. I., and Nusrat, A. (2007) Annexin 2 regulates intestinal epithelial cell spreading and wound closure through Rho-related signaling. Am. J. Pathol. 170, 951-966 (Pubitemid 47339364)
14. 2+ binding by the 36-kDa tyrosine kinase substrate (calpactin) and its 33-kDa core. J. Biol. Chem. 261, 7247-7252
15. Harder, T., Kellner, R., Parton, R. G., and Gruenberg, J. (1997) Specific release of membrane-bound annexin II and cortical cytoskeletal elements by sequestration of membrane cholesterol. Mol. Biol. Cell 8, 533-545 (Pubitemid 27171300)
16. 2+-regulated association of lipid microdomains. J. Cell Biol. 150, 1113-1124
17. Uittenbogaard, A., Everson, W. V., Matveev, S. V., and Smart, E. J. (2002) Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J. Biol. Chem. 277, 4925-4931 (Pubitemid 34968530)
18. Jacob, R., Heine, M., Eikemeyer, J., Frerker, N., Zimmer, K. P., Rescher, U., Gerke, V., and Naim, H. Y. (2004) Annexin II is required for apical transport in polarized epithelial cells. J. Biol. Chem. 279, 3680-3684 (Pubitemid 38140610)
19. Rescher, U., Ruhe, D., Ludwig, C., Zobiack, N., and Gerke, V. (2004) Annexin 2 is a phosphatidylinositol (4,5)-bisphosphate binding protein recruited to actin assembly sites at cellular membranes. J. Cell Sci. 117, 3473-3480 (Pubitemid 39206387)
20. Harrist, A. V., Ryzhova, E. V., Harvey, T., and González-Scarano, F. (2009) Anx2 interacts with HIV-1 Gag at phosphatidylinositol (4,5) bisphosphate-containing lipid rafts and increases viral production in 293T cells. PloS One 4, e5020
21. Gerke, V., and Weber, K. (1984) Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J. 3, 227-233
22. Hayes, M. J., Shao, D., Bailly, M., and Moss, S. E. (2006) Regulation of actin dynamics by annexin 2. EMBO J. 25, 1816-1826
23. Ali, S. M., and Burgoyne, R. D. (1990) The stimulatory effect of calpactin (annexin II) on calcium-dependent exocytosis in chromaffin cells: requirement for both the N-terminal and core domains of p36 and ATP. Cell. Signal. 2, 265-276
24. Blackwood, R. A., and Ernst, J. D. (1990) Characterization of Ca2(+)-dependent phospholipid binding, vesicle aggregation and membrane fusion by annexins. Biochem. J. 266, 195-200 (Pubitemid 20069039)
25. Sarafian, T., Pradel, L. A., Henry, J. P., Aunis, D., and Bader, M. F. (1991) The participation of annexin II (calpactin I) in calcium-evoked exocytosis requires protein kinase C. J. Cell Biol. 114, 1135-1147 (Pubitemid 21909874)
26. Emans, N., Gorvel, J. P., Walter, C., Gerke, V., Kellner, R., Griffiths, G., and Gruenberg, J. (1993) Annexin II is a major component of fusogenic endosomal vesicles. J. Cell Biol. 120, 1357-1369 (Pubitemid 23081683)
27. Rescher, U., and Gerke, V. (2004) Annexins-unique membrane binding proteins with diverse functions. J. Cell Sci. 117, 2631-2639 (Pubitemid 38997247)
28. Morel, E., Parton, R. G., and Gruenberg, J. (2009) Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16, 445-457
29. Law, A. L., Ling, Q., Hajjar, K. A., Futter, C. E., Greenwood, J., Adamson, P., Wavre-Shapton, S. T., Moss, S. E., and Hayes, M. J. (2009) Annexin A2 regulates phagocytosis of photoreceptor outer segments in the mouse retina. Mol. Biol. Cell 20, 3896-3904
30. Severson, E. A., Lee, W. Y., Capaldo, C. T., Nusrat, A., and Parkos, C. A. (2009) Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate β1 integrin levels, and enhance cell migration. Mol. Biol. Cell 20, 1916-1925
31. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔCT) Method. Methods 25, 402-408 (Pubitemid 34164012)
32. Macdonald, J. L., and Pike, L. J. (2005) A simplified method for the preparation of detergent-free lipid rafts. J. Lipid Res. 46, 1061-1067
33. Roberts, M., Barry, S., Woods, A., van der Sluijs, P., and Norman, J. (2001) PDGF-regulated rab4-dependent recycling of αvβ3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr. Biol. 11, 1392-1402 (Pubitemid 32863188)
34. Dukes, J. D., Fish, L., Richardson, J. D., Blaikley, E., Burns, S., Caunt, C. J., Chalmers, A. D., and Whitley, P. (2011) Functional ESCRT machinery is required for constitutive recycling of claudin-1 and maintenance of polarity in vertebrate epithelial cells. Mol. Biol. Cell 22, 3192-3205
35. Burridge, K., Turner, C. E., and Romer, L. H. (1992) Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903
36. Bellis, S. L., Perrotta, J. A., Curtis, M. S., and Turner, C. E. (1997) Adhesion of fibroblasts to fibronectin stimulates both serine and tyrosine phosphorylation of paxillin. Biochem. J. 325, 375-381 (Pubitemid 27338716)
37. Presley, J. F., Mayor, S., McGraw, T. E., Dunn, K. W., and Maxfield, F. R. (1997) Bafilomycin A1 treatment retards transferrin receptor recycling more than bulk membrane recycling. J. Biol. Chem. 272, 13929 -13936
38. Rescher, U., Ludwig, C., Konietzko, V., Kharitonenkov, A., and Gerke, V. (2008) Tyrosine phosphorylation of annexin A2 regulates Rho-mediated actin rearrangement and cell adhesion. J. Cell Sci. 121, 2177-2185
39. Hayashi, H., Naoi, S., Nakagawa, T., Nishikawa, T., Fukuda, H., Imajoh-Ohmi, S., Kondo, A., Kubo, K., Yabuki, T., Hattori, A., Hirouchi, M., and Sugiyama, Y. (2012) Sorting nexin 27 interacts with multidrug resistance-associated protein 4 (MRP4) and mediates internalization of MRP4. J. Biol. Chem. 287, 15054-15065
40. Lamaze, C., Dujeancourt, A., Baba, T., Lo, C. G., Benmerah, A., and Dautry-Varsat, A. (2001) Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol. Cell 7, 661-671 (Pubitemid 32706357)
41. Mayran, N., Parton, R. G., and Gruenberg, J. (2003) Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 22, 3242-3253 (Pubitemid 36834855)
42. Zibouche, M., Vincent, M., Illien, F., Gallay, J., and Ayala-Sanmartin, J. (2008) The N-terminal domain of annexin 2 serves as a secondary binding site during membrane bridging. J. Biol. Chem. 283, 22121-22127
43. Zobiack, N., Rescher, U., Ludwig, C., Zeuschner, D., and Gerke, V. (2003) The annexin 2/S100A10 complex controls the distribution of transferrin receptor-containing recycling endosomes. Mol. Biol. Cell 14, 4896-4908 (Pubitemid 37484805)
44. Biener, Y., Feinstein, R., Mayak, M., Kaburagi, Y., Kadowaki, T., and Zick, Y. (1996) Annexin II is a novel player in insulin signal transduction. Possible association between annexin II phosphorylation and insulin receptor internalization. J. Biol. Chem. 271, 29489-29496 (Pubitemid 26382670)
45. Huckaba, T. M., Gay, A. C., Pantalena, L. F., Yang, H. C., and Pon, L. A. (2004) Live cell imaging of the assembly, disassembly, and actin cable-dependent movement of endosomes and actin patches in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 167, 519-530 (Pubitemid 39489059)
46. Kaksonen, M., Toret, C. P., and Drubin, D. G. (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305-320 (Pubitemid 41457219)
47. Liu, J., Sun, Y., Drubin, D. G., and Oster, G. F. (2009) The mechanochemistry of endocytosis. PLoS Biol. 7, e1000204
48. Upla, P., Marjomäki, V., Kankaanpää, P., Ivaska, J., Hyypiä, T., Van Der Goot, F. G., and Heino, J. (2004) Clustering induces a lateral redistribution of α2β1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 15, 625-636 (Pubitemid 38146479)
49. Oudinet, J. P., Russo-Marie, F., Cavadore, J. C., and Rothhut, B. (1993) Protein kinase C-dependent phosphorylation of annexins I and II in mesangial cells. Biochem. J. 292, 63-68 (Pubitemid 23158962)
50. Ivaska, J., Whelan, R. D., Watson, R., and Parker, P. J. (2002) PKCε controls the traffic of β1 integrins in motile cells. EMBO J. 21, 3608-3619 (Pubitemid 34787035)