Annexin A2 regulates phagocytosis of photoreceptor outer segments in the mouse retina

Molecular Biology of the Cell

Volumn 20, Issue 17, 2009, Pages 3896-3904

  Law, Ah Lai ^a   Ling, Qi ^b   Hajjar, Katherine A ^b   Futter, Clare E ^a   Greenwood, John ^a   Adamson, Peter ^a   Wavre Shapton, Silène T ^a   Moss, Stephen E ^a   Hayes, Matthew J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOCORTIN 2; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHAGOSOME; PHOTORECEPTOR; PIGMENT CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SWINE;

ANIMALS; ANNEXIN A2; CELLS, CULTURED; CIRCADIAN RHYTHM; HUMANS; MICE; MICE, KNOCKOUT; PHAGOCYTOSIS; PHAGOSOMES; PROTEIN-TYROSINE KINASES; RETINA; RNA, SMALL INTERFERING; ROD CELL OUTER SEGMENT; SIGNAL TRANSDUCTION; SWINE;

MUS;

EID: 70349331570     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-12-1204     Document Type: Article

References (43)

1. Abram, C. L., and Lowell, C. A. (2008). The diverse functions of Src family kinases in macrophages. Front. Biosci. 13, 4426-4450.
2. Alge, C. S., Suppmann, S., Priglinger, S. G., Neubauer, A. S., May, C. A., Hauck, S., Welge-Lussen, U., Ueffing, M., and Kampik, A. (2003). Comparative proteome analysis of native differentiated and cultured dedifferentiated human RPE cells. Invest. Ophthalmol. Vis. Sci. 44, 3629-3641.
3. Bellagamba, C., Hubaishy, I., Bjorge, J. D., Fitzpatrick, S. L., Fujita, D. J., and Waisman, D. M. (1997). Tyrosine phosphorylation of annexin II tetramer is stimulated by membrane binding. J. Biol. Chem. 272, 3195-3199.
4. Bonilha, V. L., Bhattacharya, S. K., West, K. A., Sun, J., Crabb, J. W., Rayborn, M. E., and Hollyfield, J. G. (2004). Proteomic characterization of isolated retinal pigment epithelium microvilli. Mol. Cell Proteomics 3, 1119-1127. (Pubitemid 40012104)
5. Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., and Grinstein, S. (2000). Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151, 1353-1368. (Pubitemid 32047586)
6. Chaitin, M. H., and Hall, M. O. (1983). Defective ingestion of rod outer segments by cultured dystrophic rat pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 24, 812-820.
7. Crabb, J. W., et al. (2002). Drusen proteome analysis: an approach to the etiology of age-related macular degeneration. Proc. Natl. Acad. Sci. USA 99, 14682-14687.
8. D'Cruz, P. M., Yasumura, D., Weir, J., Matthes, M. T., Abderrahim, H., LaVail, M. M., and Vollrath, D. (2000). Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum. Mol. Genet. 9, 645-651.
9. de Graauw, M., Tijdens, I., Smeets, M. B., Hensbergen, P. J., Deelder, A. M., and van de Water, B. (2008). Annexin A2 phosphorylation mediates cell scattering and branching morphogenesis via cofilin activation. Mol. Cell Biol. 28, 1029-1040.
10. Deora, A. B., Kreitzer, G., Jacovina, A. T., and Hajjar, K. A. (2004). An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J. Biol. Chem. 279, 43411-43418.
11. Diakonova, M., Gerke, V., Ernst, J., Liautard, J. P., van der Vusse, G., and Griffiths, G. (1997). Localization of five annexins in J774 macrophages and on isolated phagosomes. J. Cell Sci. 110, 1199-1213. (Pubitemid 27254395)
12. 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)
13. Feng, W., Yasumura, D., Matthes, M. T., LaVail, M. M., and Vollrath, D. (2002). Mertk triggers uptake of photoreceptor outer segments during phagocytosis by cultured retinal pigment epithelial cells. J. Biol. Chem. 277, 17016-17022.
14. Finnemann, S. C. (2003). Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J. 22, 4143-4154.
15. Finnemann, S. C., Bonilha, V. L., Marmorstein, A. D., and Rodriguez-Boulan, E. (1997). Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc. Natl. Acad. Sci. USA 94, 12932-12937.
16. Futter, C. E., Ramalho, J. S., Jaissle, G. B., Seeliger, M. W., and Seabra, M. C. (2004). The role of Rab27a in the regulation of melanosome distribution within retinal pigment epithelial cells. Mol. Biol. Cell 15, 2264-2275.
17. Gerke, V., Creutz, C. E., and Moss, S. E. (2005). Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449-461.
18. Gibbs, D., Kitamoto, J., and Williams, D. S. (2003). Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc. Natl. Acad. Sci. USA 100, 6481-6486.
19. Harder, T., and Gerke, V. (1993). The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. J. Cell Biol. 123, 1119-1132.
20. Hayes, M. J., Longbottom, R. E., Evans, M. A., and Moss, S. E. (2007). Annexinopathies. Subcell. Biochem. 45, 1-28.
21. Hayes, M. J., Merrifield, C. J., Shao, D., Ayala-Sanmartin, J., Schorey, C. D., Levine, T. P., Proust, J., Curran, J., Bailly, M., and Moss, S. E. (2004). Annexin 2 binding to phosphatidylinositol 4,5-bisphosphate on endocytic vesicles is regulated by the stress response pathway. J. Biol. Chem. 279, 14157-14164.
22. Hayes, M. J., Shao, D., Bailly, M., and Moss, S. E. (2006). Regulation of actin dynamics by annexin A2. EMBO J. 25, 1816-1826.
23. Hayes, M. J., Shao, D. M., Grieve, A., Levine, T., Bailly, M., and Moss, S. E. (2009). Annexin A2 at the interface between F-actin and membranes enriched in phosphatidylinositol 4,5,-bisphosphate. Biochim. Biophys. Acta 1793, 1086-1095.
24. Hayes, M. J., and Moss, S. E. (2009). Annexin 2 has a dual role as regulator and effector of v-Src in cell transformation. J. Biol. Chem. 284, 10202-10210.
25. Ida, H., Boylan, S. A., Weigel, A. L., and Hjelmeland, L. M. (2003). Age-related changes in the transcriptional profile of mouse RPE/choroid. Physiol. Genomics 15, 258-262.
26. Jost, M., Zeuschner, D., Seemann, J., Weber, K., and Gerke, V. (1997). Identification and characterization of a novel type of annexin-membrane interaction: Ca2+ is not required for the association of annexin II with early endosomes. J. Cell Sci. 110, 221-228. (Pubitemid 27075866)
27. Ling, Q., Jacovina, A. T., Deora, A., Febbraio, M., Simantov, R., Silverstein, R. L., Hempstead, B., Mark, W. H., and Hajjar, K. A. (2004). Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J. Clin. Invest. 113, 38-48.
28. May, R. C., and Machesky, L. M. (2001). Phagocytosis and the actin cytoskeleton. J. Cell Sci. 114, 1061-1077.
29. Merrifield, C. J., Rescher, U., Almers, W., Proust, J., Gerke, V., Sechi, A. S., and Moss, S. E. (2001). Annexin A2 has an essential role in actin-based macropinocytic rocketing. Curr. Biol. 11, 1136-1141.
30. Mitra, S. K., and Schlaepfer, D. D. (2006). Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523.
31. Molday, R. S., Hicks, D., and Molday, L. (1987). Peripherin. A rim-specific membrane protein of rod outer segment discs. Invest. Ophthalmol. Vis. Sci. 28, 50-61.
32. Morel, E., Parton, R. G., and Gruenberg, J. (2009). Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev. Cell 16, 445-457.
33. Morel, E., and Gruenberg, J. (2009). Annexin A2 binding to endosomes and functions in endosomal transport are regulated by tyrosine 23 phosphorylation. J. Biol. Chem. 284, 1604-1611.
34. Nandrot, E. F., Anand, M., Almeida, D., Atabai, K., Sheppard, D., and Finnemann, S. C. (2007). Essential role for MFG-E8 as ligand for avb5 integrin in diurnal retinal phagocytosis. Proc. Natl. Acad. Sci. USA 104, 12005-12010.
35. Nandrot, E. F., and Finnemann, S. C. (2006). Altered rhythm of photoreceptor outer segment phagocytosis in beta5 integrin knockout mice. Adv. Exp. Med. Biol. 572, 119-123.
36. Nandrot, E. F., Kim, Y., Brodie, S. E., Huang, X., Sheppard, D., and Finnemann, S. C. (2004). Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J. Exp. Med. 200, 1539-1545.
37. 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.
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. Scott, C. C., Dobson, W., Botelho, R. J., Coady-Osberg, N., Chavrier, P., Knecht, D. A., Heath, C., Stahl, P., and Grinstein, S. (2005). Phosphatidylinositol-4,5-bisphosphate hydrolysis directs actin remodeling during phagocytosis. J. Cell Biol. 169, 139-149. (Pubitemid 40562921)
40. Slot, J. W., Geuze, H. J., Gigengack, S., Lienhard, G. E., and James, D. E. (1991). Immuno-localization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J. Cell Biol. 113, 123-135. (Pubitemid 21909679)
41. Strauss, O. (2005). The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881.
42. Turowski, P., Adamson, P., Sathia, J., Zhang, J. J., Moss, S. E., Aylward, G. W., Hayes, M. J., Kanuga, N., and Greenwood, J. (2004). Basement membrane-dependent modification of phenotype and gene expression in human retinal pigment epithelial ARPE-19 cells. Invest. Ophthalmol. Vis. Sci. 45, 2786-2794.
43. West, K. A., Yan, L., Shadrach, K., Sun, J., Hasan, A., Miyagi, M., Crabb, J. S., Hollyfield, J. G., Marmorstein, A. D., and Crabb, J. W. (2003). Protein database, human retinal pigment epithelium. Mol. Cell Proteomics 2, 37-49.