Diurnal, localized exposure of phosphatidylserine by rod outer segment tips in wild-type but not Itgb5 −/− or Mfge8 −/− mouse retina
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In the mammalian retina, life-long renewal of light-sensitive photoreceptor outer segments (POS) involves circadian shedding of distal rod POS tips and their subsequent phagocytosis by the adjacent retinal pigment epithelium (RPE) every morning after light onset. Molecular mechanisms that promote or synchronize POS tip shedding have thus far remained unknown. Here we examined plasma membrane asymmetry of living POS by quantifying surface exposure of the membrane phospholipid phosphatidylserine (PS) using antibodies, annexin V, and pSIVA (polarity-sensitive indicator of viability and apoptosis), an annexin-based biosensor with switchable states of fluorescence. We found that isolated POS particles possess externalized PS, whose blockade or removal reduces their binding and engulfment by RPE in culture. Imaging of live photoreceptors in freshly dissected mouse retina detected PS externalization restricted to POS tips with discrete boundaries. In wild-type mice, frequency of rod tips exposing PS and length of tips with exposed PS peak shortly after light onset. In contrast, PS-marked POS tips do not vary in mice lacking the diurnal phagocytic rhythm of the RPE due to loss of either the phagocytosis receptor αvβ5 integrin, expressed by the RPE but not by photoreceptors, or its extracellular ligand milk fat globule-EGF factor 8 (MFG-E8). These data identify a molecular distinction, localized PS exposure, that is specific to the surface of rod POS tips. Enhanced PS exposure preceding rod shedding and phagocytosis suggests that surface PS promotes these processes. Moreover, our results demonstrate that the diurnal rhythm of PS demarcation of POS tips is not intrinsic to rod photoreceptors but requires activities of the RPE as well.
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The tips of OSs contain PS exposed to the extracellular space, especially at light onset.
“the tips of OSs were found to contain PS exposed to the extracellular space, especially at light onset, using the PS-specific dye, pSIVA, a “polarity-sensitive indicator of viability and apoptosis” (Ruggiero et al., 2012)”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Ruggiero et al., 2012
Determination of the size of the phagocytic cup and the size of the ensuing phagosome likely involves an interaction between the pseudopodia and regulated features of the OS, such as PS exposure or the presence of open OS disks.
“Similarly, determination of the size of the phagocytic cup, and the size of the ensuing phagosome is likely to involve an interaction between the pseudopodia and regulated features of the OS, such as PS exposure (see section 3.4 (Ruggiero et al., 2012);) or the presence of open OS disks (Matsumoto and Besharse, 1985).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Ruggiero et al., 2012
External PS localization at the tips of OSs is stimulated only in the presence of the RPE, since it requires the RPE integrin αvβ5 and its extracellular ligand MFGE8.
“The external PS localization at the tips of OSs, mentioned above, is stimulated only in the presence of the RPE, since it requires the RPE integrin, αvβ5, and its extracellular ligand, MFGE8 (Ruggiero et al., 2012).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Ruggiero et al., 2012
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Cites
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321 · see citing works
Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., & Green, D. R. (1995) · The Journal of experimental medicine · doi:10.1084/jem.182.5.1545 · Cited by 2,824 · see citing works
Albert, M. L., Pearce, S. F. A., Francisco, L. M., Sauter, B., Roy, P., Silverstein, R. L., & Bhardwaj, N. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.7.1359 · Cited by 1,234 · see citing works
The renewal of photoreceptor cell outer segments
Young, R. W. (1967) · The Journal of Cell Biology · doi:10.1083/jcb.33.1.61 · Cited by 1,184 · see citing works
Calcium-dependent phospholipid scrambling by TMEM16F
Suzuki, J., Umeda, M., Sims, P. J., & Nagata, S. (2010) · Nature · doi:10.1038/nature09583 · Cited by 982 · see citing works
Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis
Savill, J., Dransfield, I., Hogg, N., & Haslett, C. (1990) · Nature · doi:10.1038/343170a0 · Cited by 846 · see citing works
Rod outer segment disk shedding in rat retina: relationship to cyclic lighting
LaVail, M. M. (1976) · Science · doi:10.1126/science.982063 · Cited by 689 · see citing works
Finnemann, 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
Phosphatidylserine recognition by phagocytes: a view to a kill
Wu, Y., Tibrewal, N., & Birge, R. B. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.02.003 · Cited by 341 · 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
Self-citationPeripherin. 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
van den Eijnde, S. M., van den Hoff, M. J. B., Reutelingsperger, C. P. M., van Heerde, W. L., Henfling, M. E. R., Vermeij‐Keers, C., Schütte, B., Borgers, M. J., & Ramaekers, F. C. S. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.20.3631 · Cited by 289 · see citing works
PARTICIPATION OF THE RETINAL PIGMENT EPITHELIUM IN THE ROD OUTER SEGMENT RENEWAL PROCESS
Young, R. W., & Bok, D. (1969) · Journal of Cell Biology · doi:10.1083/jcb.42.2.392 · Cited by 271 · 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
Self-citationAnti-rhodopsin monoclonal antibodies of defined specificity: Characterization and application
Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H., & Hargrave, P. A. (1991) · Vision Research · doi:10.1016/0042-6989(91)90069-h · Cited by 224 · see citing works
Normal Development, Wound Healing, and Adenovirus Susceptibility in β5-Deficient Mice
Huang, X., Griffiths, M., Wu, J., Farese, R. V., & Sheppard, D. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.3.755-759.2000 · Cited by 215 · see citing works
Krahling, S., Callahan, M. K., Williamson, P., & Schlegel, R. (1999) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400473 · Cited by 211 · 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
Coleman, J. A., Kwok, M. C. M., & Molday, R. S. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.047415 · Cited by 181 · see citing works
Wong, K., Valdez, P. A., Tan, C., Yeh, S. H., Hongo, J.-A., & Ouyang, W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910929107 · Cited by 167 · see citing works
Macrophage and Retinal Pigment Epithelium Phagocytosis
Finnemann, S. C., & Rodriguez-Boulan, E. J. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.6.861 · Cited by 144 · see citing works
Physiological roles and diseases of tmem16/anoctamin proteins: are they all chloride channels?
Duran, C., & Hartzell, H. C. (2011) · Acta Pharmacologica Sinica · doi:10.1038/aps.2011.48 · Cited by 133 · see citing works
Mfge8 Is Critical for Mammary Gland Remodeling during Involution
Atabai, K., Fernandez, R. J., Huang, X., Ueki, I. F., Kline, A., Li, Y., Sadatmansoori, S., Smith-Steinhart, C., Zhu, W., Pytela, R., et al. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-02-0128 · Cited by 107 · see citing works
Kim, Y., Chen, J., Langen, R., & Chan, J. R. (2010) · Nature Protocols · doi:10.1038/nprot.2010.101 · Cited by 61 · see citing works
Light and temperature modulated staining of the rod outer segment distal tips with Lucifer yellow.
Matsumoto, B., & Besharse, J. C. (1985) · PubMed · Cited by 48 · see citing works
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Klionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Self-citationGetting to the Outer Leaflet: Physiology of Phosphatidylserine Exposure at the Plasma Membrane
Bevers, E. M., & Williamson, P. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00020.2015 · Cited by 444 · see citing works
How macrophages deal with death
Lemke, G. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0167-y · Cited by 437 · see citing works
The cell biology of the retinal pigment epithelium
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
Differential TAM receptor–ligand–phospholipid interactions delimit differential TAM bioactivities
Lew, E. D., Oh, J., Burrola, P., Lax, I., Zagórska, A., Través, P. G., Schlessinger, J., & Lemke, G. (2014) · eLife · doi:10.7554/elife.03385 · Cited by 271 · see citing works
Structural and functional consequences of reversible lipid asymmetry in living membranes
Doktorova, M., Symons, J. L., & Levental, I. (2020) · Nature Chemical Biology · doi:10.1038/s41589-020-00688-0 · Cited by 232 · see citing works
Understanding photoreceptor outer segment phagocytosis: use and utility of RPE cells in culture
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
Protein sorting, targeting and trafficking in photoreceptor cells
Pearring, J. N., Salinas, R. Y., Baker, S. A., & Arshavsky, V. Y. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.03.002 · Cited by 207 · see citing works
Circadian organization of the mammalian retina: From gene regulation to physiology and diseases
McMahon, D. G., Iuvone, P. M., & Tosini, G. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.12.001 · Cited by 195 · see citing works
Retina Metabolism and Metabolism in the Pigmented Epithelium: A Busy Intersection
Hurley, J. B. (2021) · Annual Review of Vision Science · doi:10.1146/annurev-vision-100419-115156 · Cited by 196 · see citing works
Molecular basis for photoreceptor outer segment architecture
Goldberg, A. F. X., Moritz, O. L., & Williams, D. S. (2016) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2016.05.003 · Cited by 180 · see citing works
Lipid somersaults: Uncovering the mechanisms of protein-mediated lipid flipping
Pomorski, T. G., & Menon, A. K. (2016) · Progress in Lipid Research · doi:10.1016/j.plipres.2016.08.003 · Cited by 165 · see citing works
Anoctamins/TMEM16 Proteins: Chloride Channels Flirting with Lipids and Extracellular Vesicles
Whitlock, J. M., & Hartzell, H. C. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034031 · Cited by 165 · see citing works
Regulation of phagocytosis by Rho GTPases
Mao, Y., & Finnemann, S. C. (2015) · Small GTPases · doi:10.4161/21541248.2014.989785 · Cited by 163 · see citing works
Tissue-specific differentiation of colonic macrophages requires TGFβ receptor-mediated signaling
Schridde, A., Bain, C. C., Mayer, J. U., Montgomery, J. P., Pollet, É., Denecke, B., Milling, S. W. F., Jenkins, S. J., Dalod, M., Henri, S., et al. (2017) · Mucosal Immunology · doi:10.1038/mi.2016.142 · Cited by 158 · see citing works
Mammalian P4-ATPases and ABC transporters and their role in phospholipid transport
Coleman, J. A., Quazi, F., & Molday, R. S. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2012.10.006 · Cited by 154 · see citing works
Phagocytosis by the Retinal Pigment Epithelium: Recognition, Resolution, Recycling
Kwon, W., & Freeman, S. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604205 · Cited by 157 · see citing works
Segawa, K., Kurata, S., & Nagata, S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.690727 · Cited by 130 · see citing works
Valapala, M., Wilson, C., Hose, S., Bhutto, I. A., Grebe, R., Dong, A., Greenbaum, S., Gu, L., Sengupta, S., Cano, M., et al. (2014) · Autophagy · doi:10.4161/auto.27292 · Cited by 144 · see citing works
Phosphatidylserine Is the Signal for TAM Receptors and Their Ligands
Lemke, G. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.06.004 · Cited by 129 · see citing works
Rueda‐Carrasco, J., Sokolova, D., Lee, S., Childs, T., Jurčáková, N., Crowley, G., Schepper, S. D., Ge, J. Z., Lachica, J., Toomey, C. E., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022113246 · Cited by 120 · see citing works
Phosphatidylserine Externalization Results from and Causes Neurite Degeneration in Drosophila
Sapar, M. L., Ji, H., Wang, B., Poe, A. R., Dubey, K., Ren, X., Ni, J., & Han, C. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.095 · Cited by 107 · see citing works
Microglial MERTK eliminates phosphatidylserine‐displaying inhibitory post‐synapses
Park, J., Choi, Y., Jung, E., Lee, S., Sohn, J., & Chung, W. (2021) · The EMBO Journal · doi:10.15252/embj.2020107121 · Cited by 114 · see citing works
Circadian Clock Regulation on Lipid Metabolism and Metabolic Diseases
Pan, X., Mota, S., & Zhang, B. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-6082-8_5 · Cited by 115 · see citing works
Bestrophinopathy: An RPE-photoreceptor interface disease
Guziewicz, K. E., Sinha, D., Gómez, N. M., Zorych, K., Dutrow, E. V., Dhingra, A., Mullins, R. F., Stone, E. M., Gamm, D. M., Boesze‐Battaglia, K., et al. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.01.005 · Cited by 109 · see citing works
Dynamic lipid turnover in photoreceptors and retinal pigment epithelium throughout life
Lewandowski, D., Sander, C. L., Tworak, A., Gao, F., Xu, Q., & Skowronska‐Krawczyk, D. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.101037 · Cited by 104 · see citing works
Photoreceptor disc shedding in the living human eye
Kocaoglu, O. P., Liu, Z., Zhang, F., Kurokawa, K., Jonnal, R. S., & Miller, D. T. (2016) · Biomedical Optics Express · doi:10.1364/boe.7.004554 · Cited by 97 · see citing works
Ocular Clocks: Adapting Mechanisms for Eye Functions and Health
Felder‐Schmittbuhl, M., Buhr, E. D., Dkhissi‐Benyahya, O., Hicks, D., Peirson, S. N., Ribelayga, C., Sandu, C., Spessert, R., & Tosini, G. (2018) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-24957 · Cited by 89 · see citing works
The Retina and Other Light-sensitive Ocular Clocks
Besharse, J. C., & McMahon, D. G. (2016) · Journal of Biological Rhythms · doi:10.1177/0748730416642657 · Cited by 90 · see citing works
Metabolic Deregulation of the Blood-Outer Retinal Barrier in Retinitis Pigmentosa
Wang, W., Kini, T. A., Wang, Y., Liu, T., Chen, Y., Vukmanic, E. V., Emery, D., Liu, Y., Lu, X., Jin, L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.06.093 · Cited by 86 · see citing works
Phosphatidylserine Exposure Controls Viral Innate Immune Responses by Microglia
Tufail, Y., Cook, D., Fourgeaud, L., Powers, C. J., Merten, K., Clark, C. L., Hoffman, E. A., Ngo, A., Sekiguchi, K. J., O’Shea, C. C., et al. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.021 · Cited by 81 · see citing works
The “Phagocytic Synapse” and Clearance of Apoptotic Cells
Barth, N. D., Marwick, J. A., Vendrell, M., Rossi, A. G., & Dransfield, I. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01708 · Cited by 78 · see citing works
Law, A.-L., Parinot, C., Chatagnon, J., Gravez, B., Sahel, J., Bhattacharya, S. S., & Nandrot, E. F. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.628297 · Cited by 78 · see citing works
Farkas, M. H., Lew, D., Sousa, M. E., Bujakowska, K. M., Chatagnon, J., Bhattacharya, S. S., Pierce, E. A., & Nandrot, E. F. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2014.06.026 · Cited by 79 · see citing works
Katschke, K. J., Xi, H., Cox, C., Truong, T., Malato, Y., Lee, W. P., McKenzie, B. S., Arceo, R., Tao, J., Rangell, L. K., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-25557-8 · Cited by 77 · see citing works
Muniz-Feliciano, L., Doggett, T. A., Zhou, Z., & Ferguson, T. A. (2017) · Autophagy · doi:10.1080/15548627.2017.1380124 · Cited by 73 · see citing works
Circadian regulation in the retina: From molecules to network
Ko, G. Y. ‐. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14185 · Cited by 73 · see citing works
Selective drug delivery to the retinal cells: Biological barriers and avenues.
Ramsay, E., Lajunen, T., Bhattacharya, M., Reinisalo, M., Rilla, K., Kidron, H., Terasaki, T., & Urtti, A. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.07.028 · Cited by 67 · see citing works
Coleman, J. A., Zhu, X., Djajadi, H. R., Molday, L. L., Smith, R. S., Libby, R. T., John, S. W. M., & Molday, R. S. (2014) · Journal of Cell Science · doi:10.1242/jcs.145052 · Cited by 70 · 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
Single-cell RNA sequencing in vision research: Insights into human retinal health and disease
Voigt, A. P., Mullin, N. K., Stone, E. M., Tucker, B. A., Scheetz, T. E., & Mullins, R. F. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100934 · Cited by 64 · see citing works
TAM receptors in phagocytosis: Beyond the mere internalization of particles
Burstyn-Cohen, T., & Fresia, R. (2023) · Immunological Reviews · doi:10.1111/imr.13267 · Cited by 54 · see citing works
Rethinking Phagocytes: Clues from the Retina and Testes
Penberthy, K. K., Lysiak, J. J., & Ravichandran, K. S. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.01.004 · Cited by 57 · see citing works
Bhoi, J. D., Goel, M., Ribelayga, C., & Mangel, S. C. (2022) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2022.101119 · Cited by 51 · see citing works
Si, Z., Zheng, Y., & Zhao, J. (2023) · Biomolecules · doi:10.3390/biom13060901 · Cited by 55 · see citing works
Zhou, T., Souzeau, E., Sharma, S., Landers, J. A., Mills, R. A., Goldberg, I., Healey, P. R., Graham, S. L., Hewitt, A. W., Mackey, D. A., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172427 · Cited by 50 · see citing works
Ying, G., Boldt, K., Ueffing, M., Gerstner, C. D., Frederick, J. M., & Baehr, W. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005484 · Cited by 48 · 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
Photoreceptor phagocytosis is mediated by phosphoinositide signaling
Mustafi, D., Kevany, B. M., Genoud, C., Bai, X., & Palczewski, K. (2013) · The FASEB Journal · doi:10.1096/fj.13-237537 · Cited by 44 · see citing works
Diurnal rodents as pertinent animal models of human retinal physiology and pathology
Verra, D. M., Sajdak, B. S., Merriman, D. K., & Hicks, D. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.100776 · Cited by 45 · see citing works
qPTM: an updated database for PTM dynamics in human, mouse, rat and yeast
Yu, K., Wang, Y., Zheng, Y., Liu, Z., Zhang, Q., Wang, S., Zhao, Q., Zhang, X.-L., Li, X., Xu, R., et al. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac820 · Cited by 47 · see citing works
Dopamine 2 Receptor Activation Entrains Circadian Clocks in Mouse Retinal Pigment Epithelium
Baba, K., DeBruyne, J. P., & Tosini, G. (2017) · Scientific Reports · doi:10.1038/s41598-017-05394-x · Cited by 44 · see citing works
Laurent, V., Sengupta, A., Sánchez‐Bretaño, A., Hicks, D., & Tosini, G. (2017) · Experimental Eye Research · doi:10.1016/j.exer.2017.09.007 · Cited by 44 · see citing works
Developing Initial Conditions for Simulations of Asymmetric Membranes: A Practical Recommendation.
Park, S., Im, W., & Pastor, R. (2021) · Biophysical Journal · doi:10.1016/j.bpj.2021.10.009 · Cited by 33 · see citing works
Phospholipid scrambling by rhodopsin
Ernst, O. P., & Menon, A. K. (2015) · Photochemical & Photobiological Sciences · doi:10.1039/c5pp00195a · Cited by 41 · see citing works
Cao, J., Murat, C., An, W., Yao, X., Lee, J., Santulli-Marotto, S., Harris, I. R., & Inana, G. (2015) · Stem Cells · doi:10.1002/stem.2239 · Cited by 41 · 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
Redistribution of the glycocalyx exposes phagocytic determinants on apoptotic cells
Le, T., Ferling, I., Qiu, L., Nabaile, C., Assunção, L., Roskelley, C. D., Grinstein, S., & Freeman, S. A. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.01.020 · Cited by 36 · see citing works
Sinha, T., Naash, M. I., & Al‐Ubaidi, M. R. (2020) · iScience · doi:10.1016/j.isci.2020.101004 · Cited by 38 · see citing works
Shedding of ciliary vesicles at a glance
Naharros, I. O., & Nachury, M. V. (2022) · Journal of Cell Science · doi:10.1242/jcs.246553 · Cited by 37 · see citing works
Tam, B. M., Noorwez, S. M., Kaushal, S., Kono, M., & Moritz, O. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1655-14.2014 · Cited by 37 · see citing works
Kif17 phosphorylation regulates photoreceptor outer segment turnover
Lewis, T. R., Kundinger, S. R., Link, B. A., Insinna, C., & Besharse, J. C. (2018) · BMC Cell Biology · doi:10.1186/s12860-018-0177-9 · Cited by 35 · see citing works
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Li, C., Wang, Y., Xing, Y., Han, J., Zhang, Y., Zhang, A., Hu, J., Hua, Y., & Bai, Y. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.953534 · Cited by 36 · see citing works
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Storm, T., Burgoyne, T., & Futter, C. E. (2020) · Journal of Cell Science · doi:10.1242/jcs.238279 · Cited by 34 · see citing works
The fine‐tuning of cell membrane lipid bilayers accentuates their compositional complexity
Dingjan, T., & Futerman, A. H. (2021) · BioEssays · doi:10.1002/bies.202100021 · Cited by 35 · see citing works
Goyal, V., DeVera, C., Laurent, V., Sellers, J., Chrenek, M., Hicks, D., Baba, K., Iuvone, P., & Tosini, G. (2019) · bioRxiv · doi:10.1167/iovs.61.5.10 · Cited by 22 · see citing works
Yednock, T. A., Fong, D. S., & Lad, E. M. (2022) · International Journal of Retina and Vitreous · doi:10.1186/s40942-022-00431-y · Cited by 35 · see citing works
ABCF1 extrinsically regulates retinal pigment epithelial cell phagocytosis
Guo, F., Ding, Y., Caberoy, N. B., Alvarado, G., Wang, F., Chen, R., & Li, W. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-09-1343 · Cited by 32 · 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
Promoters and Antagonists of Phagocytosis: A Plastic and Tunable Response
Freeman, S. A., & Grinstein, S. (2021) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120219-055903 · Cited by 29 · see citing works
Context-dependent compensation among phosphatidylserine-recognition receptors
Penberthy, K. K., Rival, C., Shankman, L. S., Raymond, M. H., Zhang, J., Perry, J. S. A., Lee, C. S., Han, C. Z., Onengut-Gumuscu, S., Palczewski, K., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15191-1 · Cited by 30 · see citing works
The phototransduction machinery in the rod outer segment has a strong efficacy gradient
Mazzolini, M., Facchetti, G., Andolfi, L., Zaccaria, R. P., Tuccio, S., Treu, J., Altafini, C., Fabrizio, E. M. D., Lazzarino, M., Rapp, G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1423162112 · Cited by 30 · see citing works
Advanced Analysis of Photoreceptor Outer Segment Phagocytosis by RPE Cells in Culture
Mazzoni, F., Mao, Y., & Finnemann, S. C. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8669-9_7 · Cited by 29 · 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
Photoreceptor Inner and Outer Segments
Baker, S. A., & Kerov, V. (2013) · Current topics in membranes · doi:10.1016/b978-0-12-417027-8.00007-6 · Cited by 28 · see citing works
Circadian Regulation of Retinal Pigment Epithelium Function
Baba, K., Goyal, V., & Tosini, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052699 · Cited by 26 · see citing works
Safely removing cell debris with LC3‐associated phagocytosis
Fazeli, G., & Wehman, A. M. (2017) · Biology of the Cell · doi:10.1111/boc.201700028 · Cited by 27 · see citing works
Milićević, N., Mazzaro, N., de Bruin, I., Wils, E., ten Brink, J. B., ten Asbroek, A. L. M. A., Mendoza, J., Bergen, A. A. B., & Felder‐Schmittbuhl, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-48203-3 · Cited by 26 · see citing works
Probing Photoreceptor Outer Segment Phagocytosis by the RPE In Vivo: Models and Methodologies
Vargas, J. A., & Finnemann, S. C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073661 · Cited by 25 · see citing works
Umapathy, A., Torten, G., Paniagua, A. E., Chung, J., Tomlinson, M., Lim, C., & Williams, D. S. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1726-22.2023 · Cited by 24 · see citing works
Bulloj, A., Maminishkis, A., Mizui, M., & Finnemann, S. C. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0649-5 · Cited by 23 · see citing works
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
Tan, L. X., Germer, C. J., Thamban, T., Cunza, N. L., & Lakkaraju, A. (2023) · Current Biology · doi:10.1016/j.cub.2023.07.031 · Cited by 22 · see citing works
Ikarashi, R., Akechi, H., Kanda, Y., Ahmad, A., Takeuchi, K., Morioka, E., Sugiyama, T., Ebisawa, T., Ikeda, M., & Ikeda, M. (2017) · Scientific Reports · doi:10.1038/srep44175 · Cited by 22 · see citing works
Campbell, L. J., & Jensen, A. M. (2017) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.17-21958 · Cited by 21 · see citing works
Circadian analysis of the mouse retinal pigment epithelium transcriptome
DeVera, C., & Tosini, G. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.107988 · Cited by 20 · see citing works
TAM receptors: A phosphatidylserine receptor family and its implications in viral infections
Roy, S. G. (2020) · International review of cytology · doi:10.1016/bs.ircmb.2020.09.003 · Cited by 19 · see citing works
Differential day-night expression of tight junction components in murine retinal pigment epithelium
Louer, E., Günzel, D., Rosenthal, R., Carmone, C., Yi, G., Stunnenberg, H. G., den Hollander, A. I., & Deen, P. M. T. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.107985 · Cited by 19 · see citing works
Regulation of phospholipid dynamics in brain
Maruoka, M., & Suzuki, J. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.01.003 · Cited by 19 · see citing works
Lew, D., McGrath, M. J., & Finnemann, S. C. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.878260 · Cited by 18 · see citing works
Xu, P. A., Chen, Z., Ma, J., Shan, Y., Wang, Y., Xie, B., Zheng, D., Guo, F., Song, X., Gao, G., et al. (2023) · Human Genetics · doi:10.1007/s00439-023-02531-7 · 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
Mechanobiological implications of age-related remodelling in the outer retina
Piskova, T., Kozyrina, A. N., & Russo, J. D. (2023) · Biomaterials Advances · doi:10.1016/j.bioadv.2023.213343 · Cited by 17 · see citing works
Li, L., Rao, K. N., Zheng‐Le, Y., Hurd, T. W., Lillo, C., & Khanna, H. (2015) · Cytoskeleton · doi:10.1002/cm.21255 · Cited by 17 · see citing works
Rieu, Q., Bougoüin, A., Zagar, Y., Chatagnon, J., Hamieh, A., Enderlin, J., Huby, T., & Nandrot, E. F. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073445 · Cited by 16 · see citing works
Protein Sorting in Healthy and Diseased Photoreceptors
Imanishi, Y. (2019) · Annual Review of Vision Science · doi:10.1146/annurev-vision-091718-014843 · Cited by 16 · see citing works
Deletion of IFT20 exclusively in the RPE ablates primary cilia and leads to retinal degeneration
Kretschmer, V., Schneider, S., Matthiessen, P. A., Reichert, D., Hotaling, N. A., Glaßer, G., Lieberwirth, I., Bharti, K., Cegli, R. D., Conte, I., et al. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002402 · Cited by 15 · see citing works
Louer, E., Yi, G., Carmone, C., Robben, J., Stunnenberg, H. G., den Hollander, A. I., & Deen, P. M. T. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.5.49 · Cited by 15 · see citing works
Morra, G., Razavi, A. M., Menon, A., & Khelashvili, G. (2022) · Structure · doi:10.1016/j.str.2022.05.010 · Cited by 12 · see citing works
Neniškytė, U., Kuliešiūtė, U., Vadišiūtė, A., Jevdokimenko, K., Coletta, L., Deivasigamani, S., Pamedytytė, D., Daugelaviciene, N., Dabkevičienė, D., Perlas, E., et al. (2023) · The EMBO Journal · doi:10.15252/embj.2022111790 · Cited by 13 · see citing works
- Authors
- Ruggiero, L., Connor, M. P., Chen, J., Langen, R., & Finnemann, S. C.
- Affiliations
- Fordham University (US)
- Departments of bCell and Neurobiology and
- University of Southern California (US)
- Corresponding author
- Finnemann, Silvia C.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-05-07
- Volume
- 109
- Issue
- 21
- Pages
- 8145-8148
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3361434
- OpenAlex
- W2148756146
- Cited by
- 156
- References
- 26
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 8 · 2023: 14 · 2022: 16 · 2021: 11 · 2020: 17 · 2019: 6 · 2018: 11 · 2017: 15 · 2016: 9 · 2015: 10 · 2014: 13 · 2013: 6 · 2012: 1
- FWCI
- 3.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (EY-12155, R01EY013295, EY-13295, R01EY012155)
- National Institute of General Medical Sciences (R01GM063915, GM063915)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- phosphatidylserine exposure, diurnal cycle, alpha v beta 5 integrin, MFG-E8, membrane asymmetry, annexin V, circadian rhythm
- MeSH terms
- Animals, Antigens, Surface, Cell Membrane, Cells, Cultured, Circadian Rhythm, Light, Mice, Mutant Strains, Milk Proteins, Phagocytosis, Phosphatidylserines, Rod Cell Outer Segment, Apoptosis, Integrin beta Chains, Mice, Retinal Pigment Epithelium, Mice, 129 Strain
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