Annexin A2 regulates phagocytosis of photoreceptor outer segments in the mouse retina
Open accessAbstract
The daily phagocytosis of shed photoreceptor outer segments by pigment epithelial cells is critical for the maintenance of the retina. In a subtractive polymerase chain reaction analysis, we found that functional differentiation of human ARPE19 retinal pigment epithelial (RPE) cells is accompanied by up-regulation of annexin (anx) A2, a major Src substrate and regulator of membrane-cytoskeleton dynamics. Here, we show that anx A2 is recruited to the nascent phagocytic cup in vitro and in vivo and that it fully dissociates once the phagosome is internalized. In ARPE19 cells depleted of anx A2 by using small interfering RNA and in ANX A2(-/-) mice the phagocytosis of outer segments was impaired, and in ANX A2(-/-) mice there was an accumulation of phagocytosed outer segments in the RPE apical processes, indicative of retarded phagosome transport. We show that anx A2 is tyrosine phosphorylated at the onset of phagocytosis and that the synchronized activation of focal adhesion kinase and c-Src is abnormal in ANX A2(-/-) mice. These findings reveal that anx A2 is involved in the circadian regulation of outer segment phagocytosis, and they provide new insight into the protein machinery that regulates phagocytic function in RPE cells.
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ANXA2 is a membrane-associated protein that regulates actin dynamics and binds signaling intermediates, serving as a direct or indirect linker between the phagosome membrane and actin cytoskeleton.
“Annexin A2 (ANXA2) is a membrane-associated protein that regulates actin dynamics and binds signaling intermediates such as Ca2+, cholesterol-rich membranes, and phosphoinositides, serving as a direct or indirect linker between the phagosome membrane and actin cytoskeleton (Turowski et al., 2004; Law et al., 2009).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Law et al., 2009
Anxa2−/− mice show phagosome accumulation in the apical microvilli, an observation not noted in wild type mice, strongly suggesting delayed phagosome ingestion in the absence of ANXA2.
“Similarly, Anxa2−/− mice show phagosome accumulation in the apical microvilli (Law et al., 2009), an observation not noted in wild type mice, strongly suggesting delayed phagosome ingestion in the absence of ANXA2.”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Law et al., 2009
ANXA2 localizes to the phagocytic cup and the early phagosome but dissociates from fully ingested phagosomes, mirroring the association kinetics of actin.
“Consistent with its function, ANXA2 localizes to the phagocytic cup and the early phagosome but dissociates from fully ingested phagosomes (in vivo and in vitro) (Law et al., 2009), mirroring the association kinetics of actin.”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Law et al., 2009
The monoclonal antibody 1D4 primarily detects phagosomes in the apical, but not basal RPE, indicative of early phagosomes.
“For example, the monoclonal antibody, 1D4, whose epitope corresponds to the C-terminus of rod opsin (Molday and MacKenzie, 1983), primarily detects phagosomes in the apical, but not basal RPE, indicative of early phagosomes (Law et al., 2009; Esteve-Rudd et al., 2014; Wavre-Shapton et al., 2014).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Law et al., 2009
Cites
The Retinal Pigment Epithelium in Visual Function
Strauss, O. (2005) · Physiological Reviews · doi:10.1152/physrev.00021.2004 · Cited by 2,828 · see citing works
Integrin-regulated FAK–Src signaling in normal and cancer cells
Mitra, S. K., & Schlaepfer, D. D. (2006) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2006.08.011 · Cited by 1,591 · see citing works
Annexins: linking Ca2+ signalling to membrane dynamics
Gerke, V., Creutz, C. E., & Moss, S. E. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1661 · Cited by 1,412 · see citing works
Drusen proteome analysis: an approach to the etiology of age-related macular degeneration
Crabb, J. W., Miyagi, M., Gu, X., Shadrach, K., West, K. A., Sakaguchi, H., Kamei, M., Hasan, A., Yan, L., Rayborn, M. E., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.222551899 · Cited by 1,208 · see citing works
Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat
D'Cruz, P. M. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.4.645 · Cited by 869 · see citing works
Slot, J. W., Geuze, H. J., Gigengack, S., Lienhard, G. E., & James, D. E. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.1.123 · Cited by 862 · see citing works
Phagocytosis and the actin cytoskeleton
May, R. C., & Machesky, L. M. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.6.1061 · Cited by 715 · see citing works
Localized Biphasic Changes in Phosphatidylinositol-4,5-Bisphosphate at Sites of Phagocytosis
Botelho, R. J., Teruel, M., Dierckman, R., Anderson, R., Wells, A., York, J. D., Meyer, T., & Grinstein, S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.7.1353 · Cited by 539 · cited 2× · see citing works
“It has been proposed that phosphatidylinositol 4,5bisphosphate (PtdIns4,5P2) at the site of formation of the phagocytic cup and its subsequent hydrolysis as the cup closes are the key signaling events regulating the cycle of actin polymerization and depolymerization (Botelho et al., 2000; Scott et al., 2005).”
BackgroundFinnemann, S. C., Bonilha, V. L., Marmorstein, A. D., & Rodriguez-Boulan, E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.12932 · Cited by 382 · see citing works
Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo
Qi, L., Jacovina, A. T., Deora, A. B., Febbraio, M., Simantov, R., Silverstein, R. L., Hempstead, B. L., Mark, W. H., & Hajjar, K. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci19684 · Cited by 381 · see citing works
Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking αvβ5 integrin
Nandrot, E. F., Kim, Y., Brodie, S. E., Huang, X., Sheppard, D., & Finnemann, S. C. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20041447 · Cited by 319 · see citing works
Peripherin. A rim-specific membrane protein of rod outer segment discs.
Molday, R. S., Hicks, D. R., & Molday, L. L. (1987) · PubMed · Cited by 305 · see citing works
Annexin II is a major component of fusogenic endosomal vesicles.
Emans, N., Gorvel, J., Walter, C., Gerke, V., Kellner, R., Griffiths, G. W., & Gruenberg, J. E. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.120.6.1357 · Cited by 269 · see citing works
Phosphatidylinositol-4,5- bis phosphate hydrolysis directs actin remodeling during phagocytosis
Scott, C. C., Dobson, W., Botelho, R. J., Coady-Osberg, N., Chavrier, P., Knecht, D. A., Heath, C. M., Stahl, P. D., & Grinstein, S. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200412162 · Cited by 252 · see citing works
Gibbs, D., Kitamoto, J., & Williams, D. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1130432100 · Cited by 250 · see citing works
Feng, W., Yasumura, D., Matthes, M. T., LaVail, M. M., & Vollrath, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m107876200 · Cited by 244 · see citing works
Essential role for MFG-E8 as ligand for αvβ5 integrin in diurnal retinal phagocytosis
Nandrot, E. F., Anand, M., Almeida, D., Atabai, K., Sheppard, D., & Finnemann, S. C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704756104 · Cited by 241 · see citing works
Deora, A. B., Kreitzer, G. E., Jacovina, A. T., & Hajjar, K. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408078200 · Cited by 233 · see citing works
Defective ingestion of rod outer segments by cultured dystrophic rat pigment epithelial cells.
Chaitin, M. H., & Hall, M. O. (1983) · PubMed · Cited by 215 · see citing works
Focal adhesion kinase signaling promotes phagocytosis of integrin‐bound photoreceptors
Finnemann, S. C. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg416 · Cited by 208 · see citing works
Regulation of actin dynamics by annexin 2
Hayes, M., Shao, D., Bailly, M., & Moss, S. E. (2006) · EMBO Journal · doi:10.1038/sj.emboj.7601078 · Cited by 205 · see citing works
Annexin A2-Dependent Polymerization of Actin Mediates Endosome Biogenesis
Morel, É., Parton, R. G., & Grüenberg, J. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.01.007 · Cited by 174 · see citing works
Rescher, U., Ruhe, D., Ludwig, C., Zobiack, N., & Gerke, V. (2004) · Journal of Cell Science · doi:10.1242/jcs.01208 · Cited by 169 · see citing works
The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex.
Harder, T., & Gerke, V. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.5.1119 · Cited by 160 · see citing works
Tyrosine phosphorylation of annexin A2 regulates Rho-mediated actin rearrangement and cell adhesion
Rescher, U., Ludwig, C., Konietzko, V., Kharitonenkov, A., & Gerke, V. (2008) · Journal of Cell Science · doi:10.1242/jcs.028415 · Cited by 149 · see citing works
Localization of five annexins in J774 macrophages and on isolated phagosomes
Diakonova, M., Gerke, V., Ernst, J., Liautard, J., Vusse, G. J., & Griffiths, G. W. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.10.1199 · Cited by 132 · see citing works
de Graauw, M., Tijdens, I. B., Smeets, M. B., Hensbergen, P. J., Deelder, A. M., & van de Water, B. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01247-07 · Cited by 116 · see citing works
Hayes, M. J., Merrifield, C. J., Shao, D., Ayala‐Sanmartín, J., D’Souza‐Schorey, C., Levine, T. P., Proust, J., Curran, J., Bailly, M., & Moss, S. E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313025200 · Cited by 111 · see citing works
Futter, C. E., Ramalho, J. S., Jaissle, G. B., Seeliger, M. W., & Seabra, M. C. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-10-0772 · Cited by 110 · see citing works
Self-citationJost, M., Zeuschner, D., Seemann, J., Weber, K. K., & Gerken, V. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.2.221 · Cited by 107 · see citing works
Morel, É., & Grüenberg, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806499200 · Cited by 106 · see citing works
Annexin 2 has an essential role in actin-based macropinocytic rocketing
Merrifield, C. J., Rescher, U., Almers, W., Proust, J., Gerke, V., Sechi, A. S., & Moss, S. E. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00321-9 · Cited by 100 · see citing works
Comparative Proteome Analysis of Native Differentiated and Cultured Dedifferentiated Human RPE Cells
Alge, C. S., Suppmann, S., Priglinger, S. G., Neubauer, A. S., May, C. A., Hauck, S. M., Welge‐Lüßen, U., Ueffing, M., & Kampik, A. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-1225 · Cited by 92 · see citing works
The diverse functions of Src family kinases in macrophages
Clare, L. A. (2008) · Frontiers in bioscience · doi:10.2741/3015 · Cited by 70 · see citing works
Hayes, M., Shao, D., Grieve, A., Levine, T. P., Bailly, M., & Moss, S. (2008) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2008.10.007 · Cited by 61 · see citing works
Protein Database, Human Retinal Pigment Epithelium
West, K. A., Yan, L., Shadrach, K. G., Jian, S., Hasan, A., Miyagi, M., Crabb, J. S., Hollyfield, J. G., Marmorstein, A. D., & Crabb, J. W. (2003) · Molecular & Cellular Proteomics · doi:10.1074/mcp.d200001-mcp200 · Cited by 60 · see citing works
Proteomic Characterization of Isolated Retinal Pigment Epithelium Microvilli
Bonilha, V. L., Bhattacharya, S. K., West, K. A., Jian, S., Crabb, J. W., Rayborn, M. E., & Hollyfield, J. G. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m400106-mcp200 · Cited by 56 · see citing works
Age-related changes in the transcriptional profile of mouse RPE/choroid
Ida, H., Boylan, S. A., Weigel, A. L., & Hjelmeland, L. M. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00126.2003 · Cited by 51 · see citing works
Hayes, M. J., Longbottom, R. E., EVANS, M. A., & Moss, S. E. (2007) · Springer eBooks · doi:10.1007/978-1-4020-6191-2_1 · Cited by 51 · see citing works
Annexin 2 Has a Dual Role as Regulator and Effector of v-Src in Cell Transformation
Hayes, M. J., & Moss, S. E. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m807043200 · Cited by 48 · see citing works
Turowski, P., Adamson, P., Sathia, J., Zhang, J. J., Moss, S. E., Aylward, G. W., Hayes, M. J., Kanuga, N., & Greenwood, J. (2004) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.03-0943 · Cited by 47 · see citing works
Tyrosine Phosphorylation of Annexin II Tetramer Is Stimulated by Membrane Binding
Bellagamba, C., Hubaishy, I., Bjorge, J. D., Fitzpatrick, S. L., Fujita, D. J., & Waisman, D. M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.6.3195 · Cited by 37 · see citing works
Altered Rhythm of Photoreceptor Outer Segment Phagocytosis in β5 Integrin Knockout Mice
Nandrot, E. F., & Finnemann, S. C. (2007) · Springer eBooks · doi:10.1007/0-387-32442-9_18 · Cited by 16 · see citing works
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Sparrrow, J. R., Hicks, D., & Hamel, C. (2010) · Current Molecular Medicine · doi:10.2174/156652410793937813 · Cited by 625 · see citing works
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Lakkaraju, A., Umapathy, A., Tan, L. X., Daniele, L., Philp, N. J., Boesze-Battaglia, K., & Williams, D. S. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100846 · Cited by 422 · see citing works
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Mazzoni, F., Safa, H., & Finnemann, S. C. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.01.010 · Cited by 221 · see citing works
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Grindheim, A. K., Saraste, J., & Vedeler, A. (2017) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2017.08.024 · Cited by 145 · see citing works
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Dallacasagrande, V., & Hajjar, K. A. (2020) · Cells · doi:10.3390/cells9061499 · Cited by 128 · see citing works
A nnexin A 2 complexes with S 100 proteins: structure, function and pharmacological manipulation
Liu, Y., Myrvang, H. K., & Dekker, L. V. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12978 · Cited by 124 · see citing works
Grieve, A. G., Moss, S. E., & Hayes, M. J. (2012) · International Journal of Cell Biology · doi:10.1155/2012/852430 · Cited by 122 · see citing works
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Streubel-Gallasch, L., Giusti, V., Sandre, M., Tessari, I., Plotegher, N., Giusto, E., Masato, A., Iovino, L., Battisti, I., Arrigoni, G., et al. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02327-8 · Cited by 123 · see citing works
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McConnell, R. E., Benesh, A. E., Mao, S., Tabb, D. L., & Tyska, M. J. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00005.2011 · Cited by 103 · see citing works
He, S., Li, X., Li, R., Fang, L., Sun, L., Wang, Y., & Wu, M. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005743 · Cited by 93 · see citing works
Zhang, S., Yu, M., Guo, Q., Li, R., Li, G., Tan, S., Li, X., Wei, Y., & Wu, M. (2015) · Scientific Reports · doi:10.1038/srep15859 · Cited by 85 · see citing works
Crucial role of Anxa2 in cancer progression: highlights on its novel regulatory mechanism
Wang, T., Wang, Z., Niu, R., & Wang, L. (2019) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2019.0228 · Cited by 81 · see citing works
Shah, N., Ishii, M., Brandon, C. S., Ablonczy, Z., Cai, J., Liu, Y., Chou, C. J., & Rohrer, B. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.04.016 · Cited by 77 · see citing works
Liu, Y., Wang, Z., Jiang, M., Dai, L., Zhang, W., Wu, D., & Ruan, C. (2010) · Leukemia Research · doi:10.1016/j.leukres.2010.11.008 · Cited by 71 · see citing works
Keeling, E., Lotery, A. J., Tumbarello, D. A., & Ratnayaka, J. A. (2018) · Cells · doi:10.3390/cells7020016 · Cited by 68 · see citing works
Parinot, C., Rieu, Q., Chatagnon, J., Finnemann, S. C., & Nandrot, E. F. (2014) · Journal of Visualized Experiments · doi:10.3791/52100 · Cited by 66 · see citing works
Wavre-Shapton, S. T., Meschede, I. P., Seabra, M. C., & Futter, C. E. (2014) · Journal of Cell Science · doi:10.1242/jcs.154757 · Cited by 60 · see citing works
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Rankin, C. R., Hilgarth, R. S., Leoni, G., Kwon, M., Den Beste, K. A., Parkos, C. A., & Nusrat, A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.440909 · Cited by 55 · see citing works
Somarajan, S. R., Al-Asadi, F., Ramasamy, K., Pandranki, L., Baseman, J. B., & Kannan, T. R. (2014) · mBio · doi:10.1128/mbio.01497-14 · Cited by 54 · see citing works
Myrvang, H. K., Guo, X., Li, C., & Dekker, L. V. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.08.012 · Cited by 53 · see citing works
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Yin, J., Brocher, J., Linder, B., Hirmer, A., Sundaramurthi, H., Fischer, U., & Winkler, C. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9511 · Cited by 51 · see citing works
Lieffrig, S. A., Gyimesi, G., Mao, Y., & Finnemann, S. C. (2023) · Immunological Reviews · doi:10.1111/imr.13264 · Cited by 47 · see citing works
Stukes, S. A., Coelho, C., Rivera, J., Jedlicka, A., Hajjar, K. A., & Casadevall, A. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1501855 · Cited by 44 · see citing works
Fang, Y., Lin, C., Wang, C., Anderson, R., & Lin, Y. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.23026 · Cited by 43 · see citing works
Bulloj, A., Duan, W., & Finnemann, S. C. (2013) · Experimental Eye Research · doi:10.1016/j.exer.2013.05.002 · Cited by 39 · see citing works
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Lei, Y., Wang, K., Li, X., Li, Y., Feng, X., Zhou, J., Zhang, Z., Huang, C., & Zhang, T. (2019) · Clinical Science · doi:10.1042/cs20180687 · Cited by 33 · see citing works
Annexin A5 regulates surface αvβ5 integrin for retinal clearance phagocytosis
Chen, Y., Munoz, L. E., Mallavarapu, M., i, M. H., & Finnemann, S. C. (2019) · Journal of Cell Science · doi:10.1242/jcs.232439 · Cited by 33 · see citing works
Regulation of the rhythmic diversity of daily photoreceptor outer segment phagocytosis in vivo
Moran, A. L., Fehilly, J. D., Jones, D. F., Collery, R. F., & Kennedy, B. N. (2022) · The FASEB Journal · doi:10.1096/fj.202200990rr · Cited by 27 · see citing works
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Vargas, J. A., & Finnemann, S. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073661 · Cited by 25 · see citing works
Zhang, H., Lu, D., Zhang, Y., Zhao, G., Raheem, A., Chen, Y., Chen, X., Hu, C., Chen, H., Yang, L., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.974006 · Cited by 23 · see citing works
In vivo and in vitro monitoring of phagosome maturation in retinal pigment epithelium cells
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The Formation and Renewal of Photoreceptor Outer Segments
Jingjin, X., Zhao, C., & Kang, Y. (2024) · Cells · doi:10.3390/cells13161357 · Cited by 21 · see citing works
Shelby, S. J., Feathers, K. L., Ganios, A. M., Jia, L., Miller, J. M. L., & Thompson, D. A. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.08.006 · Cited by 22 · see citing works
Su, Z., Chang, Q., Drelich, A. K., Shelite, T. R., Judy, B. M., Liu, Y., Xiao, J., Zhou, C., He, X., Jin, Y., et al. (2020) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007960 · Cited by 18 · see citing works
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Letelier, J., Bovolenta, P., & Martínez‐Morales, J. R. (2017) · Journal of Neurogenetics · doi:10.1080/01677063.2017.1395876 · Cited by 18 · see citing works
Chiang, C.-K., Tworak, A., Kevany, B. M., Xu, B., Mayne, J., Ning, Z., Figeys, D., & Palczewski, K. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.812677 · Cited by 17 · see citing works
Luo, M., Almeida, D., Dallacasagrande, V., Hedhli, N., Patel, M. M., D’Amico, D. J., Kiss, S., & Hajjar, K. A. (2024) · Nature Communications · doi:10.1038/s41467-024-52675-x · Cited by 16 · see citing works
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Khoh‐Reiter, S., Sokolowski, S. A., Jessen, B. A., Evans, M. G., Dalvie, D., & Lu, S. (2015) · Toxicological Sciences · doi:10.1093/toxsci/kfv059 · Cited by 15 · see citing works
Yeh, H., & Klesius, P. H. (2010) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2010.02.013 · Cited by 15 · see citing works
Carter, S. P., Moran, A. L., Matallanas, D., McManus, G., Blacque, O. E., & Kennedy, B. N. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00136 · Cited by 14 · see citing works
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Nandrot, E. F. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3209-8_10 · Cited by 13 · see citing works
Bennis, A., ten Brink, J. B., Moerland, P. D., Heine, V. M., & Bergen, A. A. B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182983 · Cited by 11 · see citing works
Campbell, L. J., West, M. C., & Jensen, A. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-32336-y · Cited by 11 · see citing works
β -actin is essential for structural integrity and physiological function of the retinaPreprint
Vedula, P., Fina, M. E., Bell, B. A., Nikonov, S. S., Kashina, A. S., & Dong, D. W. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.27.534392 · Cited by 11 · see citing works
Annexins as potential targets in ocular diseases
da Silva, R. A., Roda, V. M. D. P., Ferreira, L. P. D. S., Oliani, S. M., Girol, A. P., & Gil, C. D. (2022) · Drug Discovery Today · doi:10.1016/j.drudis.2022.103367 · Cited by 10 · see citing works
Rhythmicity of the Retinal Pigment Epithelium
Ruggiero, L., & Finnemann, S. C. (2013) · Springer eBooks · doi:10.1007/978-1-4614-9613-7_6 · Cited by 9 · see citing works
Receptor role of the annexin A2 in the mesothelial endocytosis of crocidolite fibers
Yamashita, K., Nagai, H., & Toyokuni, S. (2015) · Laboratory Investigation · doi:10.1038/labinvest.2015.28 · Cited by 9 · see citing works
Shao, A., Lopez, A. J., Chen, J., Tham, A., Javier, S., Alonso, A. Q., Frick, S., Levine, E. M., Lloyd, K. C. K., Leonard, B. C., et al. (2022) · Disease Models & Mechanisms · doi:10.1242/dmm.049343 · Cited by 7 · see citing works
Aareskjold, E., Grindheim, A. K., Hollås, H., Goris, M., Lillehaug, J. R., & Vedeler, A. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.05.028 · Cited by 7 · see citing works
Regulation of C3 Activation by the Alternative Complement Pathway in the Mouse Retina
Williams, J. A. E., Stampoulis, D., Gunter, C. E., Greenwood, J., Adamson, P., & Moss, S. E. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161898 · Cited by 7 · see citing works
Cheng, S.-Y., Malachi, A., Cipi, J., Ma, S., Brush, R. S., Agbaga, M., & Punzo, C. (2021) · Biomolecules · doi:10.3390/biom11060871 · Cited by 7 · see citing works
Müller, C., & Finnemann, S. C. (2020) · Springer eBooks · doi:10.1007/978-3-030-28384-1_3 · Cited by 6 · see citing works
Xiao, S., Ouyang, Q., Feng, Y., Lu, X., Han, Y., Ren, H., Huang, Q., Zhao, J., Xiao, C., & Yang, M. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.105591 · Cited by 5 · see citing works
On Your Marks… Get Bound… Internalize!
Law, A.-L., & Nandrot, E. F. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-0631-0_91 · Cited by 4 · see citing works
Retinal Pigment Epithelium Phagocytosis and Retinal Degenerative Diseases
Du, Y., & Xia, Y. (2025) · Aging and Disease · doi:10.14336/ad.2025.0542 · Cited by 3 · see citing works
Electroretinographic and Morphological Characterization of the Retina of Annexin A1 Knockout Mice
da Silva, R. A., Liber, A. M. P., Ferreira, L. P. D. S., Moreno-Carmona, F. M., dos Santos, D. D., Sant’Ana, M., Costa, M. F., Ventura, D. F., & Gil, C. D. (2025) · Neuroglia · doi:10.3390/neuroglia6020019 · Cited by 2 · see citing works
Paschou, C., Apokotou, O., Κόλλιας, Α., Charmpi, K., Dede, S., Samiotaki, M. K., Palese, F., Dimoula, K., Emmanouilidou, E., Taoufik, E., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.06.621638 · Cited by 2 · see citing works
Zhang, Q., Autterson, G. A., & Miller, J. M. L. (2023) · Journal of Visualized Experiments · doi:10.3791/65242 · Cited by 1 · see citing works
The role of cholesterol metabolism in predicting clinical outcome of patients with severe COVID-19Preprint
Usenko, T. S., Мирошникова, В. В., Bezrukova, A. I., Basharova, K. S., Ланда, С. Б., Korobova, Z. R., Liubimova, N. E., Vlasov, I. N., Nikolaev, M. A., Izyumchenko, A. D., et al. (2022) · medRxiv · doi:10.1101/2022.11.10.22282185 · Cited by 1 · see citing works
Phagocytosis of Retinal Rod and Cone Photoreceptors
Farnoodian, M., Kinter, J. B., Aghdam, S. Y., Zaitoun, I. S., Christine, M. S., Khoh‐Reiter, S., Sokolowski, S. A., Jessen, B. A., Evans, M. G., Dalvie, D., et al. (2015)
Shelby, S. J. (2012) · Deep Blue (University of Michigan)
Dietary Antioxidants, αvβ5 Integrin, and Ocular Protection
Sethna, S., & Finnemann, S. C. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-401717-7.00058-7
A systemically-delivered stem cell therapy for dry age related macular degeneration
Pay, S. L. (2017) · IUScholarWorks (Indiana University) · doi:10.7912/c2006q
Arap1 Loss Causes RPE Phagocytic Dysfunction and Subsequent Photoreceptor DeathPreprint
Shao, A., Lopez, A. J., Chen, J., Tham, A., Javier, S., Quiroz, A., Frick, S., Levine, E., Lloyd, K. C. K., Leonard, B., et al. (2021) · bioRxiv · doi:10.1101/2021.08.09.455745
Gupta, G. (2012) · Springer eBooks · doi:10.1007/978-3-7091-1065-2_21
Müller, C., & Finnemann, S. C. (2024) · Springer eBooks · doi:10.1007/978-3-031-35055-9_3
Breast cancer spheroids prefer activated macrophages as an accomplice: An in vitro studyPreprint
Teli, A., Iyer, R., Shanbhag, K., Gawarguru, R., Gayan, S., Shaikh, S., Tamhankar, A. S., Kamat, S. S., & Dey, T. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.24.614655
- Authors
- Law, A.-L., Ling, Q., Hajjar, K. A., Futter, C. E., Greenwood, J., Adamson, P., Wavre-Shapton, S. T., Moss, S. E., & Hayes, M. J.
- Affiliations
- University College London (GB)
- Department of Cell and Developmental Biology, Weill Cornell Medical College, New York, NY 10065
- Weill Cornell Medicine (US)
- *Department of Cell Biology, University College London Institute of Ophthalmology, University College London, London EC1V 9EL, United Kingdom; and
- ORCID
- Venue
- Molecular Biology of the Cell
- Published
- 2009-09
- Volume
- 20
- Issue
- 17
- Pages
- 3896-3904
- ISSN
- 1059-1524 (ISSN-L)
- 1939-4586
- PMC
- PMC2735488
- OpenAlex
- W2167429009
- Cited by
- 75
- References
- 43
- Citations by year
- 2025: 2 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 3 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 6 · 2014: 8 · 2013: 5 · 2012: 4
- FWCI
- 1.74
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Biology of the Cell (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust (GR072694MF)
- University College London
- National Institutes of Health
- Medical Research Council
- National Heart, Lung, and Blood Institute (R01HL042493, P01HL046403, HL-42493, R01HL067939, HL 67939, HL-46403)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- annexin A2, photoreceptor outer segment phagocytosis, retinal pigment epithelium, ARPE-19 cells, tyrosine phosphorylation, focal adhesion kinase, Src kinase, circadian regulation
- MeSH terms
- Animals, Cells, Cultured, Circadian Rhythm, Humans, Phagocytosis, Phagosomes, Protein-Tyrosine Kinases, Retina, Rod Cell Outer Segment, Swine, Signal Transduction, Annexin A2, Mice, Knockout, RNA, Small Interfering, Mice
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