Clathrin adaptor AP1B controls adenovirus infectivity of epithelial cells
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Adenoviruses invading the organism via normal digestive or respiratory routes require the Coxsackie-adenovirus receptor (CAR) to infect the epithelial barrier cells. Because CAR is a component of tight junctions and the basolateral membrane and is normally excluded from the apical membrane, most epithelia are resistant to adenoviruses. However, we discovered that a specialized epithelium, the retinal pigment epithelium (RPE), anomalously expressed CAR at the apical surface and was highly susceptible to adenovirus infection. These properties of RPE cells correlated with the absence of the epithelial-specific clathrin adaptor AP1B. Furthermore, knockdown of this basolateral sorting adaptor in adenovirus-resistant MDCK cells promoted apical localization of CAR and increased dramatically Adenovirus infectivity. Targeting assays showed that AP1B is required for accurate basolateral recycling of CAR after internalization. AP1B knock down MDCK cells missorted CAR from recycling endosomes to the apical surface. In summary, we have characterized the cellular machinery responsible for normal sorting of an adenovirus receptor and illustrated how tissue-specific variations in such machinery result in drastic changes in tissue-susceptibility to adenoviruses.
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Apical localization of CAR makes the RPE highly susceptible to adenovirus infection.
“Apical localization of CAR makes the RPE highly susceptible to adenovirus infection (Diaz et al., 2009).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Diaz et al., 2009
Common recycling endosomes mediate transcytosis of the transferrin receptor and CAR from the basolateral to the apical surface in the RPE.
“Common recycling endosomes are responsible for mediating transcytosis of the transferrin receptor and the Coxsackie-adenovirus receptor (CAR) from the basolateral to the apical surface in the RPE (Diaz et al., 2009; Perez Bay et al., 2013; Perez Bay et al., 2014)”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Diaz et al., 2009
Cites
Isolation of a Common Receptor for Coxsackie B Viruses and Adenoviruses 2 and 5
Bergelson, J. M., Cunningham, J. A., Droguett, G., Kurt‐Jones, E. A., Krithivas, A., Hong, J. S., Horwitz, M. S., Crowell, R. L., & Finberg, R. W. (1997) · Science · doi:10.1126/science.275.5304.1320 · Cited by 3,102 · see citing works
Mendelsohn, C. L., Wimmer, E., & Racaniello, V. R. (1989) · Cell · doi:10.1016/0092-8674(89)90690-9 · Cited by 1,116 · see citing works
Geraghty, R. J., Krummenacher, C., Cohen, G. H., Eisenberg, R. J., & Spear, P. G. (1998) · Science · doi:10.1126/science.280.5369.1618 · Cited by 907 · see citing works
Disruption of the Epithelial Apical-Junctional Complex by Helicobacter pylori CagA
Amieva, M. R., Vogelmann, R., Covacci, A., Tompkins, L. S., Nelson, W. J., & Falkow, S. (2003) · Science · doi:10.1126/science.1081919 · Cited by 739 · see citing works
The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction
Cohen, C. J., Shieh, J. T. C., Pickles, R. J., Okegawa, T., Hsieh, J., & Bergelson, J. M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261452898 · Cited by 702 · see citing works
Organization of vesicular trafficking in epithelia
Rodriguez-Boulan, E., Kreitzer, G., & Müsch, A. (2005) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1593 · Cited by 644 · see citing works
Self-citationJunction Adhesion Molecule Is a Receptor for Reovirus
Barton, E. S., Forrest, J. C., Connolly, J. L., Chappell, J. D., Liu, Y., Schnell, F. J., Nusrat, A., Parkos, C. A., & Dermody, T. S. (2001) · Cell · doi:10.1016/s0092-8674(01)00231-8 · Cited by 627 · see citing works
Coyne, C. B., & Bergelson, J. M. (2006) · Cell · doi:10.1016/j.cell.2005.10.035 · Cited by 547 · see citing works
A Novel Clathrin Adaptor Complex Mediates Basolateral Targeting in Polarized Epithelial Cells
Fölsch, H., Ohno, H., Bonifacino, J. S., & Mellman, I. (1999) · Cell · doi:10.1016/s0092-8674(00)81650-5 · Cited by 515 · see citing works
New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity
Yeaman, C. A., Grindstaff, K. K., & Nelson, W. J. (1999) · Physiological Reviews · doi:10.1152/physrev.1999.79.1.73 · Cited by 515 · see citing works
Multicolour imaging of post-Golgi sorting and trafficking in live cells
Keller, P., Toomre, D. K., Díaz, E., White, J., & Simons, K. (2001) · Nature Cell Biology · doi:10.1038/35055042 · Cited by 423 · see citing works
Coat proteins: shaping membrane transport
Bonifacino, J. S., & Lippincott‐Schwartz, J. (2003) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1099 · Cited by 420 · see citing works
Walters, R. W., Grunst, T., Bergelson, J. M., Finberg, R. W., Welsh, M. J., & Zabner, J. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.15.10219 · Cited by 372 · see citing works
Adenovirus Type 11 Uses CD46 as a Cellular Receptor
Segerman, A., Atkinson, J. P., Marttila, M., Dennerquist, V., Wadell, G., & Arnberg, N. (2003) · Journal of Virology · doi:10.1128/jvi.77.17.9183-9191.2003 · Cited by 358 · see citing works
Polarized epithelial membrane traffic: conservation and plasticity
Mostov, K. E., Su, T., & ter Beest, M. (2003) · Nature Cell Biology · doi:10.1038/ncb0403-287 · Cited by 296 · see citing works
ROLE OF TIGHT JUNCTIONS IN ESTABLISHING AND MAINTAINING CELL POLARITY
Cereijido, M., Valdés, J., Shoshani, L., & Contreras, R. G. (1998) · Annual Review of Physiology · doi:10.1146/annurev.physiol.60.1.161 · Cited by 257 · see citing works
μ1B, a novel adaptor medium chain expressed in polarized epithelial cells1
Ohno, H., Tomemori, T., Nakatsu, F., Okazaki, Y., Aguilar, R. C., Foelsch, H., Mellman, I., Saito, T., Shirasawa, T., & Bonifacino, J. S. (1999) · FEBS Letters · doi:10.1016/s0014-5793(99)00432-9 · Cited by 248 · see citing works
Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein
Kreitzer, G. E., Marmorstein, A. D., Okamoto, P. M., Vallee, R. B., & Rodriguez-Boulan, E. J. (2000) · Nature Cell Biology · doi:10.1038/35000081 · Cited by 242 · see citing works
Self-citationAdenovirus vector-mediated in vivo gene transfer into adult murine retina.
Bennett, J., Wilson, J. M., Sun, D., Forbes, B. J., & Maguire, A. (1994) · PubMed · Cited by 238 · see citing works
Clathrin is a key regulator of basolateral polarity
Deborde, S., Perret, E., Gravotta, D., Deora, A. A., Salvarezza, S. B., Schreiner, R. P., & Rodriguez-Boulan, E. J. (2008) · Nature · doi:10.1038/nature06828 · Cited by 213 · see citing works
Self-citationLewis, M. L., Culbertson, W. W., Post, M. J. D., Miller, D., Kokame, G. T., & Dix, R. D. (1989) · Ophthalmology · doi:10.1016/s0161-6420(89)32823-5 · Cited by 209 · see citing works
The epithelial-specific adaptor AP1B mediates post-endocytic recycling to the basolateral membrane
Gan, Y., McGraw, T. E., & Rodriguez-Boulan, E. J. (2002) · Nature Cell Biology · doi:10.1038/ncb827 · Cited by 195 · see citing works
Self-citationAP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells
Gravotta, D., Deora, A. A., Perret, E., Oyanadel, C., Soza, A., Schreiner, R. P., González, A., & Rodriguez-Boulan, E. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610700104 · Cited by 149 · see citing works
Self-citationGLUT4 is internalized by a cholesterol‐dependent nystatin‐sensitive mechanism inhibited by insulin
Blot, V., & McGraw, T. E. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601462 · Cited by 115 · see citing works
Cancino, J., Torrealba, C., Soza, A., Yuseff, M.-I., Gravotta, D., Henklein, P., Rodriguez-Boulan, E. J., & González, A. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-06-0563 · Cited by 94 · see citing works
Self-citationStonebraker, J. R., Wagner, D., Lefensty, R. W., Burns, K. A., Gendler, S. J., Bergelson, J. M., Boucher, R. C., O’Neal, W. K., & Pickles, R. J. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13755-13768.2004 · Cited by 82 · see citing works
Cohen, C. J., Gaetz, J., Ohman, T., & Bergelson, J. M. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009531200 · Cited by 73 · see citing works
Breaking into the epithelial apical–junctional complex — news from pathogen hackers
Vogelmann, R., Amieva, M. R., Falkow, S., & Nelson, W. J. (2003) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2003.12.002 · Cited by 67 · see citing works
Herpes simplex virus type 1 exhibits a tropism for basal entry in polarized epithelial cells
Schelhaas, M., Jansen, M. K., Haase, I., & Knebel-Mörsdorf, D. (2003) · Journal of General Virology · doi:10.1099/vir.0.19226-0 · Cited by 64 · see citing works
Marmorstein, A. D., Gan, Y., Bonilha, V. L., Finnemann, S. C., Csaky, K. G., & Rodriguez-Boulan, E. J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.3.697 · Cited by 60 · see citing works
Self-citationSaturation of, and competition for entry into, the apical secretory pathway
Marmorstein, A. D., Csaky, K. G., Baffi, J., Lam, L., Rahaal, F., & Rodriguez-Boulan, E. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3248 · Cited by 57 · see citing works
Self-citationPolarized biosynthetic traffic in renal epithelial cells: sorting, sorting, everywhere
Ellis, M. A., Potter, B. A., Cresawn, K. O., & Weisz, O. A. (2006) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00161.2006 · Cited by 49 · see citing works
Membrane Cofactor Protein (CD46) Is a Basolateral Protein That Is Not Endocytosed
Maisner, A., Zimmer, G., Liszewski, M. K., Lublin, D. M., Atkinson, J. P., & Herrler, G. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.33.20793 · Cited by 46 · see citing works
Influence of Fiber Detargeting on Adenovirus-Mediated Innate and Adaptive Immune Activation
Schoggins, J. W., Nociari, M., Philpott, N. J., & Falck-Pedersen, E. (2005) · Journal of Virology · doi:10.1128/jvi.79.18.11627-11637.2005 · Cited by 40 · see citing works
Self-citationMaisner, A., Liszewski, M. K., Atkinson, J. P., Schwartz‐Albiez, R., & Herrler, G. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.31.18853 · Cited by 40 · see citing works
Ohka, S., Ohno, H., Tohyama, K., & Nomoto, A. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5660 · Cited by 36 · see citing works
Deora, A. A., Diaz, F., Schreiner, R. P., & Rodriguez-Boulan, E. J. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00617.x · Cited by 31 · see citing works
Self-citationHerpes Virus Infection of RPE and MDCK Cells: Polarity of Infection
Topp, K. S., Rothman, A., & LaVail, J. H. (1997) · Experimental Eye Research · doi:10.1006/exer.1996.0209 · Cited by 23 · see citing works
Open Sesame! Coxsackieviruses Conspire to Trespass the Tight Junctional Gate
Diaz, F., & Rodriguez-Boulan, E. J. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.01.005 · Cited by 5 · see citing works
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Rodriguez-Boulan, E. J., & Macara, I. G. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3775 · Cited by 679 · see citing works
Self-citationProteomics of Primary Cilia by Proximity Labeling
Mick, D. U., Rodrigues, R. B., Leib, R. D., Adams, C. M., Chien, A. S., Gygi, S. P., & Nachury, M. V. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.10.015 · Cited by 409 · 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
Apical trafficking in epithelial cells: signals, clusters and motors
Weisz, O. A., & Rodriguez-Boulan, E. J. (2009) · Journal of Cell Science · doi:10.1242/jcs.032615 · Cited by 299 · see citing works
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Bonifacino, J. S. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201310021 · Cited by 247 · see citing works
Structural Basis for Recruitment and Activation of the AP-1 Clathrin Adaptor Complex by Arf1
Ren, X., Farı́as, G. G., Canagarajah, B. J., Bonifacino, J. S., & Hurley, J. H. (2013) · Cell · doi:10.1016/j.cell.2012.12.042 · Cited by 195 · see citing works
The Clathrin Adaptor AP-1A Mediates Basolateral Polarity
Gravotta, D., Carvajal-Gonzalez, J. M., Mattera, R., Deborde, S., Banfelder, J. R., Bonifacino, J. S., & Rodriguez-Boulan, E. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.02.004 · Cited by 148 · see citing works
Self-citationGetting active: protein sorting in endocytic recycling
Hsu, V. W., Bai, M., & Li, J. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3332 · Cited by 131 · see citing works
Farías, G. G., Cuitino, L., Guo, X., Ren, X., Jarnik, M., Mattera, R., & Bonifacino, J. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.007 · Cited by 122 · see citing works
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Lehmann, G. L., Benedicto, I., Philp, N. J., & Rodriguez-Boulan, E. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.04.021 · Cited by 122 · see citing works
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Self-citationLütschg, V. A., Boucke, K., Hemmi, S., & Greber, U. F. (2011) · Nature Communications · doi:10.1038/ncomms1391 · Cited by 94 · see citing works
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González, A., & Rodriguez-Boulan, E. J. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.10.050 · Cited by 83 · see citing works
Self-citationRecycling endosomes in apical plasma membrane domain formation and epithelial cell polarity
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Guo, X., Mattera, R., Ren, X., Chen, Y., Retamal, C., González, A., & Bonifacino, J. S. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.10.006 · Cited by 71 · see citing works
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Self-citationThe Role of the Clathrin Adaptor AP-1: Polarized Sorting and Beyond
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Kotha, P. L. N., Sharma, P., Kolawole, A. O., Yan, R., Alghamri, M. S., Brockman, T. L., Gómez-Cambronero, J., & Excoffon, K. J. D. A. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1004696 · Cited by 65 · see citing works
The kinesin KIF16B mediates apical transcytosis of transferrin receptor in AP-1B-deficient epithelia
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Self-citationMechanism of polarized lysosome exocytosis in epithelial cells
Xu, J., Toops, K. A., Diaz, F., Carvajal-González, J. M., Gravotta, D., Mazzoni, F., Schreiner, R. P., Rodriguez-Boulan, E. J., & Lakkaraju, A. (2012) · Journal of Cell Science · doi:10.1242/jcs.109421 · Cited by 61 · see citing works
Self-citationCastorino, J. J., Deborde, S., Deora, A. A., Schreiner, R. P., Gallagher‐Colombo, S. M., Rodriguez-Boulan, E. J., & Philp, N. J. (2010) · Traffic · doi:10.1111/j.1600-0854.2010.01155.x · Cited by 55 · see citing works
Self-citationThe absence of a clathrin adapter confers unique polarity essential to proximal tubule function
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Self-citationSalinas, S., Zussy, C., Loustalot, F., Henaff, D., Menéndez, G., Morton, P. E., Parsons, M., Schiavo, G., & Kremer, E. J. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.518365 · Cited by 44 · see citing works
Caceres, P. S., Gravotta, D., Zager, P. J., Dephoure, N., & Rodriguez-Boulan, E. J. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821076116 · Cited by 43 · see citing works
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Gephart, J., Singh, B., Higginbotham, J. N., Franklin, J. L., González, A., Fölsch, H., & Coffey, R. J. (2011) · Traffic · doi:10.1111/j.1600-0854.2011.01282.x · Cited by 38 · see citing works
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Peng, S., Wang, S.-B., Singh, D., Zhao, P. Y., Davis, K., Chen, B., Adelman, R. A., & Rizzolo, L. J. (2016) · Experimental Eye Research · doi:10.1016/j.exer.2016.08.021 · Cited by 35 · see citing works
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Self-citationKoumarianou, P., Fernández-Méndez, C., Fajardo-Delgado, D., Mielu, L. M., Santisteban, P., & la Vieja, A. D. (2022) · Thyroid · doi:10.1089/thy.2022.0163 · Cited by 12 · see citing works
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Mimura, M., Masuda, A., Nishiumi, S., Kawakami, K., Fujishima, Y., Yoshie, T., Mizuno, S., Miki, I., Ohno, H., Hase, K., et al. (2011) · International Journal of Cancer · doi:10.1002/ijc.26131 · Cited by 12 · see citing works
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Hirata, Y., Funato, Y., & Miki, H. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.10.138 · Cited by 12 · see citing works
AP1S3 is required for hepatitis C virus infection by stabilizing E2 protein
Li, X. O., Niu, Y., Cheng, M., Chi, X., Liu, X., & Yang, W. Z. (2016) · Antiviral Research · doi:10.1016/j.antiviral.2016.04.006 · Cited by 9 · see citing works
Apodaca, G. L., & Gallo, L. I. (2013) · Colloquium Series on Building Blocks of the Cell Cell Structure and Function · doi:10.4199/c00077ed1v01y201303bbc002 · Cited by 9 · see citing works
Polar release of pathogenic Old World hantaviruses from renal tubular epithelial cells
Krautkrämer, E., Lehmann, M. J., Bollinger, V., & Zeier, M. (2012) · Virology Journal · doi:10.1186/1743-422x-9-299 · Cited by 7 · see citing works
Alghamri, M. S., Sharma, P., Williamson, T. L., Readler, J. M., Yan, R., Rider, S. D., Hostetler, H. A., Cool, D. R., Kolawole, A. O., & Excoffon, K. J. D. A. (2021) · Journal of Virology · doi:10.1128/jvi.00046-21 · Cited by 7 · see citing works
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Bay, A. E. P., Schreiner, R. P., & Rodriguez-Boulan, E. J. (2015) · Methods in cell biology · doi:10.1016/bs.mcb.2015.06.019 · Cited by 6 · see citing works
Self-citationPhilp, N. J., Shoshani, L., Cereijido, M., & Rodriguez-Boulan, E. J. (2011) · doi:10.1002/9781118015759.ch21 · Cited by 5 · see citing works
Self-citationZhang, Y., & Lui, W. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-77779-1_5 · Cited by 4 · see citing works
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Moresco, E. M. Y., & Brandl, K. (2013) · Tissue Barriers · doi:10.4161/tisb.23119 · Cited by 4 · see citing works
Niu, Y., Wang, M.-X., Liang, S., Zhou, F., & Miao, Y. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1971-7 · Cited by 2 · see citing works
CHARACTERIZATION OF ADAPTOR PROTEIN COMPLEX‐1 IN THE SILKWORM, Bombyx mori
Niu, Y., Cai, Z., Lu, Y., Wang, M., Liang, S., Zhou, F., & Miao, Y. (2012) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.21077
Identification of novel non-muscle myosin IIA (NMIIA) interacting partners
Patrícia, M., & Santos, F. (2013)
Protein Trafficking in Polarized Epithelial Cells
Zink, S., & Jacob, R. (2015) · Springer eBooks · doi:10.1007/978-3-319-14463-4_16
企業人材育成研究のフロンティア : 経営学修論の黎明(基調講演,第34回研究大会報告)
中原, 淳. (2013)
ECELBARGER, C. A. (2010) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.7236956.7485056
Coyne, C. B. (2011) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.12282956.14653194
Cellular Organization of the Retinal Pigment Epithelium
Burgoyne, T., & Futter, C. E. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-13820-1.00067-0
Guo, H., Yan, R., Han, X., & Yu, W. (2026) · Journal of Inflammation Research · doi:10.2147/jir.s612984
Valbuena, F. M., Lessard, M., Krahn, A. H., Pantazopoulou, A., Lee-Smith, C. F., Adarska, P., Bottanelli, F., & Glick, B. S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.10.21.760840
- Authors
- Diaz, F., Gravotta, D., Deora, A., Schreiner, R., Schoggins, J., Falck-Pedersen, E., & Rodriguez-Boulan, E.
- Affiliations
- Cornell University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-07-07
- Volume
- 106
- Issue
- 27
- Pages
- 11143-11148
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2708682
- OpenAlex
- W2076297345
- Cited by
- 73
- References
- 39
- Citations by year
- 2026: 2 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 5 · 2020: 2 · 2019: 2 · 2017: 1 · 2016: 4 · 2015: 10 · 2014: 9 · 2013: 9 · 2012: 11
- FWCI
- 3.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Research to Prevent Blindness
- Dyson Foundation
- National Eye Institute (EY08538, R01EY008538)
- National Institute of General Medical Sciences (GM-34107, R01GM034107)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Virus-based gene therapy research
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Keywords
- adenovirus infection, coxsackievirus and adenovirus receptor, retinal pigment epithelium, apical membrane localization, basolateral sorting, recycling endosomes, tight junctions, MDCK cells, receptor internalization
- MeSH terms
- Adenoviridae, Animals, Cell Line, Clathrin, Dogs, Endocytosis, Epithelial Cells, Humans, Receptors, Virus, Cell Polarity, Tight Junctions, Protein Transport, Adaptor Protein Complex beta Subunits, Retinal Pigment Epithelium, Gene Knockdown Techniques, Coxsackie and Adenovirus Receptor-Like Membrane Protein
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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