Annexin A2 Regulates β1 Integrin Internalization and Intestinal Epithelial Cell Migration
Open accessAbstract
The gastrointestinal epithelium functions as an important barrier that separates luminal contents from the underlying tissue compartment and is vital in maintaining mucosal homeostasis. Mucosal wounds in inflammatory disorders compromise the critical epithelial barrier. In response to injury, intestinal epithelial cells (IECs) rapidly migrate to reseal wounds. We have previously observed that a membrane-associated, actin binding protein, annexin A2 (AnxA2), is up-regulated in migrating IECs and plays an important role in promoting wound closure. To identify the mechanisms by which AnxA2 promotes IEC movement and wound closure, we used a loss of function approach. AnxA2-specific shRNA was utilized to generate IECs with stable down-regulation of AnxA2. Loss of AnxA2 inhibited IEC migration while promoting enhanced cell-matrix adhesion. These functional effects were associated with increased levels of β1 integrin protein, which is reported to play an important role in mediating the cell-matrix adhesive properties of epithelial cells. Because cell migration requires dynamic turnover of integrin-based adhesions, we tested whether AnxA2 modulates internalization of cell surface β1 integrin required for forward cell movement. Indeed, pulse-chase biotinylation experiments in IECs lacking AnxA2 demonstrated a significant increase in cell surface β1 integrin that was accompanied by decreased β1 integrin internalization and degradation. These findings support an important role of AnxA2 in controlling dynamics of β1 integrin at the cell surface that in turn is required for the active turnover of cell-matrix associations, cell migration, and wound closure. Background: Intestinal epithelial wound closure requires dynamic regulation/turnover of cell-matrix adhesions. Results: Down-regulation of annexin A2 increases cell-matrix adhesion and delays β1 integrin internalization from the plasma membrane. Conclusion: Annexin A2 promotes wound closure by regulating internalization of β1 integrin in migrating epithelial cells. Significance: This study identifies a novel role of annexin A2 in regulating β1 integrin internalization required for intestinal epithelial cell migration.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ANXA2 has previously been shown to regulate cell migration in other disease settings including carcinogenesis.
“ANXA2, which we have identified as a key marker in both human and mouse migratory hepatocytes, has been previously shown to regulate cell migration in other disease settings including carcinogenesis21–23”
From Multimodal decoding of human liver regeneration (2024) · cites this paper as [21]
Cites
1 retracted
Uittenbogaard, A., Everson, W. V., Matveev, S. V., & Smart, E. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109278200 · Cited by 115 · see citing works
RetractedAnalysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Burridge, K., Turner, C. E., & Romer, L. H. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.4.893 · Cited by 1,310 · see citing works
Organizing cell renewal in the intestine: stem cells, signals and combinatorial control
Crosnier, C., Stamataki, D., & Lewis, J. H. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1840 · Cited by 756 · see citing works
A Modular Design for the Clathrin- and Actin-Mediated Endocytosis Machinery
Kaksonen, M., Toret, C. P., & Drubin, D. G. (2005) · Cell · doi:10.1016/j.cell.2005.09.024 · Cited by 726 · see citing works
Annexins – unique membrane binding proteins with diverse functions
Rescher, U., & Gerke, V. (2004) · Journal of Cell Science · doi:10.1242/jcs.01245 · Cited by 595 · see citing works
Restoration of Barrier Function in Injured Intestinal Mucosa
Blikslager, A. T., Moeser, A. J., Gookin, J. L., Jones, S. L., & Odle, J. (2007) · Physiological Reviews · doi:10.1152/physrev.00012.2006 · Cited by 573 · see citing works
Gerke, V., & Weber, K. (1984) · The EMBO Journal · doi:10.1002/j.1460-2075.1984.tb01789.x · Cited by 550 · see citing works
Integrins: masters and slaves of endocytic transport
Caswell, P. T., Vadrevu, S., & Norman, J. C. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2799 · Cited by 527 · see citing works
Lamaze, C., Dujeancourt-Henry, A., Baba, T., Lo, C. G., Benmerah, A., & Dautry‐Varsat, A. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00212-x · Cited by 525 · see citing works
Roberts, M. S., Barry, S. T., Woods, A. J., van der Sluijs, P., & Norman, J. C. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00442-0 · Cited by 348 · see citing works
A simplified method for the preparation of detergent-free lipid rafts
MacDonald, J. L., & PIKE, L. J. (2005) · Journal of Lipid Research · doi:10.1194/jlr.d400041-jlr200 · Cited by 339 · see citing works
Mechanisms of integrin activation and trafficking
Margadant, C., Monsuur, H. N., Norman, J. C., & Sonnenberg, A. (2011) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2011.08.005 · Cited by 304 · see citing works
Blackwood, R. A., & Ernst, J. (1990) · Biochemical Journal · doi:10.1042/bj2660195 · Cited by 292 · 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
Annexins in Cell Membrane Dynamics
Babiychuk, E. B., & Draeger, A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.5.1113 · Cited by 266 · see citing works
Glenney, J. R. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38382-5 · Cited by 265 · see citing works
Endocytosis and recycling of the fibronectin receptor in CHO cells.
Bretscher, M. S. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03514.x · Cited by 228 · see citing works
The Mechanochemistry of Endocytosis
Liu, J., Sun, Y., Drubin, D. G., & Oster, G. F. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000204 · Cited by 222 · see citing works
Harder, T., Kellner, R., Parton, R. G., & Gruenberg, J. E. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.3.533 · Cited by 209 · see citing works
Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells
Mayran, N., Parton, R. G., & Gruenberg, J. E. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg321 · Cited by 207 · 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
Mandell, K. J., Babbin, B. A., Nusrat, A., & Parkos, C. A. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m412650200 · Cited by 198 · see citing works
Self-citationSarafian, T., Pradel, L., Henry, J., Aunis, D., & Bader, M. F. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.6.1135 · Cited by 196 · see citing works
Huckaba, T. M., Gay, A. C., Pantalena, L. F., Yang, H., & Pon, L. A. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200404173 · Cited by 181 · see citing works
Severson, E. A., Lee, W. Y., Capaldo, C., Nusrat, A., & Parkos, C. A. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-10-1014 · Cited by 175 · see citing works
Self-citationAnnexin 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
Upla, P., Marjomäki, V., Kankaanpää, P., Ivaska, J., Hyypiä, T., van der Goot, F. G., & Heino, J. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-08-0588 · Cited by 168 · see citing works
Bafilomycin A1 Treatment Retards Transferrin Receptor Recycling More than Bulk Membrane Recycling
Presley, J. F., Mayor, S., McGraw, T. E., Dunn, K. W., & Maxfield, F. R. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.21.13929 · Cited by 167 · see citing works
PKCϵ controls the traffic of β1 integrins in motile cells
Ivaska, J., Whelan, R. D. H., Watson, R., & Parker, P. J. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf371 · Cited by 156 · 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
Annexin II Is a Novel Player in Insulin Signal Transduction
Biener, Y., Feinstein, R., Mayak, M., Kaburagi, Y., Kadowaki, T., & Zick, Y. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.46.29489 · Cited by 136 · see citing works
Morphology and electrophysiology of guinea pig gastric mucosal repair in vitro
Rutten, M. J., & Ito, S. (1983) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1983.244.2.g171 · Cited by 129 · see citing works
MMP7 Shedding of Syndecan-1 Facilitates Re-Epithelialization by Affecting α2β1 Integrin Activation
Chen, P., Abacherli, L. E., Nadler, S. T., Wang, Y., Li, Q., & Parks, W. C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006565 · Cited by 117 · see citing works
Zobiack, N., Rescher, U., Ludwig, C., Zeuschner, D., & Gerke, V. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-06-0387 · Cited by 117 · see citing works
Bellis, S. L., Perrotta, J. A., Curtis, M. S., & Turner, C. E. (1997) · Biochemical Journal · doi:10.1042/bj3250375 · Cited by 116 · see citing works
Regulation of Integrin β1 Recycling to Lipid Rafts by Rab1a to Promote Cell Migration
Wang, C., Yoo, Y., Fan, H., Kim, E., Guan, K., & Guan, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.141440 · Cited by 100 · see citing works
Lotz, M. M., Nusrat, A., Madara, J., Ezzell, R. M., Wewer, U. M., & Mercurio, A. M. (1997) · Europe PMC (PubMed Central) · Cited by 96 · see citing works
Self-citationBabbin, B. A., Parkos, C. A., Mandell, K. J., Winfree, L. M., Laur, O., Ivanov, A. I., & Nusrat, A. (2007) · The American Journal of Pathology · doi:10.2353/ajpath.2007.060647 · Cited by 89 · see citing works
Self-citationAnnexin II Is Required for Apical Transport in Polarized Epithelial Cells
Jacob, R., Heine, M., Eikemeyer, J., Frerker, N., Zimmer, K., Rescher, U., Gerke, V., & Naim, H. Y. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.c300503200 · Cited by 84 · see citing works
Annexin A2 regulates phagocytosis of photoreceptor outer segments in the mouse retina
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. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-12-1204 · Cited by 75 · see citing works
Dukes, J. D., Fish, L. P., Richardson, J. D., Blaikley, E., Burns, S., Caunt, C. J., Chalmers, A. D., & Whitley, P. R. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-04-0343 · Cited by 66 · see citing works
Lipid rafts mediate internalization of β1-integrin in migrating intestinal epithelial cells
Vassilieva, E. V., Gerner-Smidt, K., Ivanov, A. I., & Nusrat, A. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00082.2008 · Cited by 59 · see citing works
Self-citationRaub, T. J., & Kuentzel, S. L. (1989) · Experimental Cell Research · doi:10.1016/0014-4827(89)90340-6 · Cited by 54 · see citing works
Ali, S. M., & Burgoyne, R. D. (1990) · Cellular Signalling · doi:10.1016/0898-6568(90)90054-e · Cited by 46 · see citing works
Hayashi, H., Naoi, S., Nakagawa, T., Nishikawa, T., Fukuda, H., Imajoh‐Ohmi, S., Kondo, A., Kubo, K., Yabuki, T., Hattori, A., et al. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.337931 · Cited by 40 · see citing works
Harrist, A. V., Ryzhova, E. V., Harvey, T. S., & González‐Scarano, F. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005020 · Cited by 38 · see citing works
The N-terminal Domain of Annexin 2 Serves as a Secondary Binding Site during Membrane Bridging
Zibouche, M., Vincent, M., Illien, F., Gallay, J., & Ayala‐Sanmartín, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801000200 · Cited by 32 · see citing works
Protein kinase C-dependent phosphorylation of annexins I and II in mesangial cells
Oudinet, J., Russo‐Marie, F., Cavadore, J. C., & Rothhut, B. (1993) · Biochemical Journal · doi:10.1042/bj2920063 · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Wound repair: role of immune–epithelial interactions
Leoni, G., Neumann, P.-A., Sumagin, R., Denning, T. L., & Nusrat, A. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.63 · Cited by 310 · see citing works
Self-citationAli, M. R. K., Ali, H. R. K., Rankin, C. R., & El‐Sayed, M. A. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.06.017 · Cited by 197 · see citing works
Self-citationSTAT3-EMT axis in tumors: Modulation of cancer metastasis, stemness and therapy response
Sadrkhanloo, M., Entezari, M., Orouei, S., Ghollasi, M., Fathi, N., Rezaei, S., Hejazi, E. S., Kakavand, A., Saebfar, H., Hashemi, M., et al. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106311 · Cited by 188 · see citing works
Xuan, Y., Huang, B., Tian, H. S., Li, S., Duan, Y. M., Wang, X., Zhu, Z. X., Cai, W. H., Zhu, Y. T., Wei, T. M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108182 · Cited by 164 · see citing works
Uchihara, T., Miyake, K., Yonemura, A., Komohara, Y., Itoyama, R., Koiwa, M., Yasuda, T., Arima, K., Harada, K., Eto, K., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-3803 · Cited by 159 · see citing works
Multimodal decoding of human liver regeneration
Matchett, K. P., Wilson-Kanamori, J. R., Portman, J. R., Kapourani, C. A., Fercoq, F., May, S., Zajdel, E., Beltran, M., Sutherland, E. F., Mackey, J. B. G., et al. (2024) · Nature · doi:10.1038/s41586-024-07376-2 · Cited by 140 · see citing works
“ANXA2, which we have identified as a key marker in both human and mouse migratory hepatocytes, has previously been shown to regulate cell migration in other disease settings including carcinogenesis 16-18 .”
BackgroundAnnexin A2 in Inflammation and Host Defense
Dallacasagrande, V., & Hajjar, K. A. (2020) · Cells · doi:10.3390/cells9061499 · Cited by 128 · see citing works
Rocha, M. R., Barcellos‐de‐Souza, P., Squiavinato, A. C. M. S., Fernandes, P. V., de Oliveira, I. M., Boroni, M., & Morgado‐Díaz, J. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-29703-0 · Cited by 87 · see citing works
Annexin A2 in Fibrinolysis, Inflammation and Fibrosis
Lim, H. I., & Hajjar, K. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136836 · Cited by 67 · see citing works
Zhang, F., Zhang, H., Wang, Z., Yu, M., Tian, R., Ji, W., Yang, Y., & Niu, R. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.11.003 · Cited by 67 · see citing works
Dynamic reciprocity: the role of annexin A2 in tissue integrity
Hitchcock, J. K., Katz, A. A., & Schäfer, G. (2014) · Journal of Cell Communication and Signaling · doi:10.1007/s12079-014-0231-0 · Cited by 57 · see citing works
Galectin-3 Regulates Desmoglein-2 and Intestinal Epithelial Intercellular Adhesion
Jiang, K., Rankin, C. R., Nava, P., Sumagin, R., Kamekura, R., Stowell, S. R., Feng, M., Parkos, C. A., & Nusrat, A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.538538 · Cited by 55 · see citing works
Self-citationIntracellular targeting of annexin A2 inhibits tumor cell adhesion, migration, and in vivo grafting
Staquicini, D. I., Rangel, R., Guzman‐Rojas, L., Staquicini, F. I., Dobroff, A. S., Tarleton, C. A., Ozbun, M. A., Kolonin, M. G., Gelovani, J. G., Marchiò, S., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-03470-w · Cited by 55 · see citing works
Epithelial CD47 is critical for mucosal repair in the murine intestine in vivo
Reed, M., Luissint, A., Azcutia, V., Fan, S., O’Leary, M. N., Quirós, M., Brazil, J. C., Nusrat, A., & Parkos, C. A. (2019) · Nature Communications · doi:10.1038/s41467-019-12968-y · Cited by 54 · see citing works
Self-citationHang, Q., Isaji, T., Hou, S., Wang, Y., Fukuda, T., & Gu, J. (2017) · Molecular and Cellular Biology · doi:10.1128/mcb.00558-16 · Cited by 53 · see citing works
Intestinal Transcriptome Analysis Reveals Soy Derivative-Linked Changes in Atlantic Salmon
Kiron, V., Park, Y., Siriyappagouder, P., Dahle, D., Vasanth, G. K., Dias, J. P., Fernandes, J. M. O., Sørensen, M., & Verlhac-Trichet, V. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.596514 · Cited by 53 · see citing works
O’Boyle, N., & Boyd, A. (2014) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00114 · Cited by 45 · see citing works
Flemming, S., Luissint, A., Kusters, D. H. M., Raya‐Sandino, A., Fan, S., Zhou, D. W., Hasegawa, M., García‐Hernández, V., Garcı́a, A. J., Parkos, C. A., et al. (2020) · Molecular Biology of the Cell · doi:10.1091/mbc.e19-12-0692 · Cited by 43 · see citing works
Self-citationAnnexin A2 Regulates TRPA1-Dependent Nociception
Avenali, L., Narayanan, P., Rouwette, T., Cervellini, I., Sereda, M. W., Gómez‐Varela, D., & Schmidt, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1801-14.2014 · Cited by 41 · see citing works
Patterson, A. M., & Watson, A. J. M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00841 · Cited by 39 · see citing works
Role of Corneal Stromal Cells on Epithelial Cell Function during Wound Healing
Kowtharapu, B. S., Murín, R., Jünemann, A., & Stachs, O. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020464 · Cited by 34 · see citing works
Kummerlowe, C., Mwakamui, S., Hughes, T. K., Mulugeta, N., Mudenda, V. C., Besa, E. C., Zyambo, K., Shay, J. E. S., Fleming, I., Vukovic, M., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abi8633 · Cited by 33 · see citing works
Glia Maturation Factor-γ Regulates Monocyte Migration through Modulation of β1-Integrin
Aerbajinai, W., Liu, L., Zhu, J., Kumkhaek, C., Chin, K., & Rodgers, G. P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.674200 · Cited by 30 · see citing works
Su, Y., & Besner, G. E. (2014) · Journal of Surgical Research · doi:10.1016/j.jss.2014.02.055 · Cited by 29 · see citing works
Song, Y., Wang, F., Xia, J., Zhang, Q., He, K., Wang, L., Zhu, M., Liu, J., Liu, L., & Liu, J. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.10.042 · Cited by 26 · see citing works
Bydoun, M., & Waisman, D. M. (2014) · Future Oncology · doi:10.2217/fon.14.163 · Cited by 23 · see citing works
Naydenov, N. G., Feygin, A., Wang, L., & Ivanov, A. I. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.498691 · Cited by 22 · see citing works
Soroosh, A., Fang, K., Hoffman, J. M., Law, I. K. M., Videlock, E. J., Lokhandwala, Z. A., Zhao, J. J., Hamidi, S., Padua, D. M., Frey, M. R., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04463-4 · Cited by 18 · see citing works
Self-citationUtilization of Nannochloropsis oceanica in plant-based feeds by Atlantic salmon (Salmo salar)
Liu, C., Palihawadana, A. M., Nadanasabesan, N., Vasanth, G. K., Vatsos, I. N., Dias, J. P., Valente, L. M. P., Micallef, G., Sørensen, M., & Kiron, V. (2022) · Aquaculture · doi:10.1016/j.aquaculture.2022.738651 · Cited by 18 · see citing works
Nguyen, D. N., Jiang, P., Jacobsen, S., Sangild, P. T., Bendixen, E., & Chatterton, D. E. W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117608 · Cited by 18 · see citing works
iTRAQ-Based Quantitative Proteomic Analysis of the Initiation of Head Regeneration in Planarians
Geng, X., Wang, G., Qin, Y., Zang, X., Li, P., Geng, Z., Xue, D., Dong, Z., Ma, K.-X., Chen, G., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132045 · Cited by 18 · see citing works
Clinical and prognostic role of annexin A2 in adamantinomatous craniopharyngioma
Wang, Y., Deng, J., Guo, G. F., Tong, A., Peng, X., Chen, H., Xu, J., Liu, Y., You, C., & Zhou, L. (2016) · Journal of Neuro-Oncology · doi:10.1007/s11060-016-2273-z · Cited by 16 · see citing works
Ying, Y.-T., Ren, W., Tan, X., Yang, J., Liu, R., & Du, A. (2021) · Microorganisms · doi:10.3390/microorganisms9102090 · Cited by 15 · see citing works
Komalasari, N. L. G. Y., Tomonobu, N., Kinoshita, R., Chen, Y., Sakaguchi, Y. M., Gohara, Y., Jiang, F., Yamamoto, K.-I., Murata, H., Ruma, I. M. W., et al. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1142907 · Cited by 15 · see citing works
Tedesco, L., Rossi, F., Ruocco, C., Ragni, M., Carruba, M. O., Valerio, A., & Nisoli, E. (2022) · Experimental Eye Research · doi:10.1016/j.exer.2022.109060 · Cited by 14 · see citing works
Fernández, M. P., García, M., Martin‐Almedina, S., & Morgan, R. O. (2016) · Biological Chemistry · doi:10.1515/hsz-2016-0273 · Cited by 12 · see citing works
Nordvi, M. F., Løvmo, S. D., Whatmore, P., Sundh, H., Sigholt, T., & Olsen, R. E. (2022) · Aquaculture · doi:10.1016/j.aquaculture.2022.738920 · Cited by 11 · see citing works
Ziegler, A. L., Caldwell, M. L., Erwin, S. J., Hellstrom, E. A., Sheridan, A. E., Touvron, M. S., Pridgen, T. A., Magness, S. T., Odle, J., Landeghem, L. V., et al. (2023) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00216.2022 · Cited by 11 · see citing works
Yang, Y., Zhao, X., Huang, D., Wang, J., Qi, Y., Jiang, L., Zhao, H., & Cheng, G. (2019) · Animal Production Science · doi:10.1071/an18242 · Cited by 10 · see citing works
Swain, S. D., Grifka‐Walk, H. M., Gripentrog, J. M., Lehmann, M. M., Deuling, B., Jenkins, B., Liss, H., Blaseg, N. A., Bimczok, D., & Kominsky, D. J. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00071.2019 · Cited by 9 · see citing works
Chen, J., Li, J., Ran, L., Yang, J., & Xie, Y. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-07177-9 · Cited by 8 · see citing works
Latour, Y. L., Allaman, M. M., Barry, D. P., Smith, T. M., Williams, K. J., McNamara, K. M., Jacobse, J., Goettel, J. A., Delgado, A. G., Piazuelo, M. B., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2192623 · Cited by 8 · see citing works
Kummerlowe, C., Wallach, T. E., Mwakamui, S., Hughes, T. K., Mulugeta, N., Mudenda, V. C., Besa, E. C., Zyambo, K., Fleming, I., Vukovic, M., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.11.439202 · Cited by 8 · see citing works
Gastrointestinal Mucosal Defense System
Kvietys, P. R., Yaqinuddin, A., & Al-Kattan, W. (2014) · Colloquium Series on Integrated Systems Physiology From Molecule to Function · doi:10.4199/c00119ed1v01y201409isp058 · Cited by 7 · see citing works
Wu, L.-Y., Zhai, M.-N., Bai, X.-Q., He, C., Guo, Y.-Y., Zhang, Y., Wang, J., Gao, Y.-T., Tu, Q., Liu, M., et al. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110343 · Cited by 6 · see citing works
Nudelman, A., Shenoy, A., Allouche‐Arnon, H., Fisler, M., Rosenhek‐Goldian, I., Dayan, L., Karam, P. A., Porat, Z., Solomonov, I., Regev‐Rudzki, N., et al. (2024) · Biomedicines · doi:10.3390/biomedicines12020434 · Cited by 4 · see citing works
Murshed, N. M. F., Shetty, P., Jayaswamy, P. K., Jacob, A. M., Al-Awadhi, S. S. A., & Laxminarayana, K. P. H. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1725965 · Cited by 4 · see citing works
CLDN5 as a novel modulator of podocyte adhesion to extracellular matrix via β1-integrin binding
Wang, C., Han, J., Fan, B., Shen, Y., An, Y., Kong, F., Ge, N., Zhang, X., Liu, H., Wang, M., et al. (2026) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2026.111163 · Cited by 3 · see citing works
Bijelić, D. D., Adžić, M., Perić, M., Reiss, G., Milosevic, M. M., Anđjus, P. R., & Jakovčevski, I. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.952208 · Cited by 3 · see citing works
Role of Annexin A2 isoform 2 on the aggregative growth of dermal papillae cells
Gu, J., Ma, Y., Yang, L., Wang, F., Cao, L., Zhai, J.-X., & Xia, R. (2018) · Bioscience Reports · doi:10.1042/bsr20180971 · Cited by 3 · see citing works
Molecular cloning and characterization of duck Annexin A2 and its effect on DTMUV replication
Xian, X., Shen, B., & Chen, Q. (2024) · Poultry Science · doi:10.1016/j.psj.2024.104005 · Cited by 1 · see citing works
Gómez-Buitrago, P.-A., González-Correa, C.-A., Osorio, M. S., Ocampo, G. T., Koolen, H. H. F., & Arruda, M. A. Z. (2020) · Brazilian Journal of Analytical Chemistry · doi:10.30744/brjac.2179-3425.ar-41-2019 · Cited by 1 · see citing works
Ziegler, A. L., Erwin, S. J., Caldwell, M. L., Touvron, M. S., Pridgen, T. A., Magness, S. T., Odle, J., Landeghem, L. V., & Blikslager, A. T. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.04.514575
Rose, E. C., Simon, J. M., Gomez-Martinez, I., Magness, S. T., Odle, J., Blikslager, A. T., & Ziegler, A. L. (2025) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00194.2024
- Authors
- Rankin, C. R., Hilgarth, R. S., Leoni, G., Kwon, M., Den Beste, K. A., Parkos, C. A., & Nusrat, A.
- Affiliations
- Emory University (US)
- Corresponding author
- Nusrat, Asma
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2013-05
- Volume
- 288
- Issue
- 21
- Pages
- 15229-15239
- ISSN
- 0021-9258 (ISSN-L)
- PMC
- PMC3663542
- OpenAlex
- W2003489386
- Cited by
- 55
- References
- 50
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 3 · 2022: 7 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 4 · 2015: 3 · 2014: 8 · 2013: 2
- FWCI
- 5.49
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK055679, R24DK064399, R01DK061379, R01DK072564, DK059888, R01DK059888, R01DK079392)
- Topics
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › S100 Proteins and Annexins
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- annexin A2, beta1 integrin, integrin internalization, intestinal epithelial cell migration, cell-matrix adhesion, epithelial barrier function, actin-binding proteins
- MeSH terms
- Cell Adhesion, Cell Movement, Epithelial Cells, Extracellular Matrix, Humans, Intestinal Mucosa, Wound Healing, Annexin A2, Caco-2 Cells, Integrin beta1, Protein Transport, Proteolysis
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
