ACKR4 on stromal cells scavenges CCL19 to enable CCR7-dependent trafficking of APCs from inflamed skin to lymph nodes
Abstract
Dermal dendritic cells and epidermal Langerhans cells are APCs that migrate from skin to draining lymph nodes (LN) to drive peripheral tolerance and adaptive immunity. Their migration requires the chemokine receptor CCR7, which directs egress from the skin via dermal lymphatic vessels and extravasation into the LN parenchyma from lymph in the subcapsular sinus. CCR7 is activated by two chemokines: CCL19 and CCL21. CCL21 alone is sufficient for the migration of APCs from skin to LN. CCL19 and CCL21 also bind atypical chemokine receptor (ACKR) 4. ACKR4-mediated CCL21 scavenging by lymphatic endothelial cells lining the subcapsular sinus ceiling stabilizes interfollicular CCL21 gradients that direct lymph-borne CCR7(+)APCs into the parenchyma of mouse LN. In this study, we show that ACKR4 also aids APC egress from mouse skin under steady-state and inflammatory conditions. ACKR4 plays a particularly prominent role during cutaneous inflammation when it facilitates Langerhans cell egress from skin and enables the accumulation of dermal dendritic cells in skin-draining LN. Stromal cells in mouse skin, predominantly keratinocytes and a subset of dermal lymphatic endothelial cells, express ACKR4 and are capable of ACKR4-dependent chemokine scavenging in situ. ACKR4-mediated scavenging of dermal-derived CCL19, rather than CCL21, is critical during inflammation, because the aberrant trafficking of skin-derived APCs inAckr4-deficient mice is completely rescued by genetic deletion ofCcl19…
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The impaired DC migration in ACKR4-deficient mice can be rescued by codisruption of the gene encoding CCL19.
“Curiously, the impaired migration can be rescued by codisruption of the gene that encodes the CCL19 chemokine that is normally produced by DCs themselves and fibroblasts and which also binds CCR7 (105).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [105]
Gradients of CCL21 are maintained by the ACKR4 scavenger receptor expressed by stromal cells in the interstitium.
“Gradients of CCL21 are maintained by the ACKR4 scavenger receptor that is expressed by stromal cells in the interstitium (104, 105).”
From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [105]
Cites
Förster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner‐Müller, I., Wolf, E., & Lipp, M. (1999) · Cell · doi:10.1016/s0092-8674(00)80059-8 · Cited by 2,348 · see citing works
CCR7 and its ligands: balancing immunity and tolerance
Förster, R., Davalos-Misslitz, A. C., & Rot, A. (2008) · Nature Reviews Immunology · doi:10.1038/nri2297 · Cited by 1,410 · see citing works
CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions
Ohl, L., Mohaupt, M., Czeloth, N., Hintzen, G., Kiafard, Z., Zwirner, J., Blankenstein, T., Henning, G., & Förster, R. (2004) · Immunity · doi:10.1016/j.immuni.2004.06.014 · Cited by 1,086 · see citing works
Gunn, M. D., Kyuwa, S., Tam‐Amersdorfer, C., Kakiuchi, T., Matsuzawa, A., Williams, L. T., & Nakano, H. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.3.451 · Cited by 1,019 · see citing works
Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells
Link, A., Vogt, T. K., Favre, S., Britschgi, M. R., Acha‐Orbea, H., Hinz, B., Cyster, J. G., & Luther, S. A. (2007) · Nature Immunology · doi:10.1038/ni1513 · Cited by 934 · see citing works
Origin, homeostasis and function of Langerhans cells and other langerin-expressing dendritic cells
Merad, M., Ginhoux, F., & Collin, M. (2008) · Nature Reviews Immunology · doi:10.1038/nri2455 · Cited by 850 · see citing works
Bachelerie, F., Ben‐Baruch, A., Burkhardt, A. M., Combadière, C., Farber, J. M., Graham, G. J., Horuk, R., Sparre‐Ulrich, A. H., Locati, M., Luster, A. D., et al. (2013) · Pharmacological Reviews · doi:10.1124/pr.113.007724 · Cited by 846 · see citing works
Self-citationInterstitial dendritic cell guidance by haptotactic chemokine gradients
Weber, M., Hauschild, R., Schwarz, J., Moussion, C., de Vries, I., Legler, D. F., Luther, S. A., Bollenbach, T., & Sixt, M. (2013) · Science · doi:10.1126/science.1228456 · Cited by 555 · see citing works
Tomura, M., Yoshida, N., Tanaka, J., Karasawa, S., Miwa, Y., Miyawaki, A., & Kanagawa, O. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802278105 · Cited by 414 · see citing works
Immune regulation by atypical chemokine receptors
Nibbs, R. J. B., & Graham, G. J. (2013) · Nature reviews. Immunology · doi:10.1038/nri3544 · Cited by 409 · see citing works
Self-citationInhibition of CXCR2 profoundly suppresses inflammation-driven and spontaneous tumorigenesis
Jamieson, T., Clarke, M., Steele, C. W., Samuel, M. S., Neumann, J., Jung, A., Huels, D., Olson, M. F., Das, S., Nibbs, R. J. B., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci61067 · Cited by 391 · see citing works
Self-citationBraun, A., Worbs, T., Moschovakis, G. L., Halle, S., Hoffmann, K., Bölter, J., Münk, A., & Förster, R. (2011) · Nature Immunology · doi:10.1038/ni.2085 · Cited by 337 · see citing works
Kohout, T. A., Nicholas, S., Perry, S. J., Reinhart, G. J., Junger, S., & Struthers, R. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402125200 · Cited by 333 · see citing works
Schumann, K., Lämmermann, T., Bruckner, M., Legler, D. F., Polleux, J., Spatz, J. P., Schuler, G., Förster, R., Lutz, M. B., Sorokin, L. M., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.04.017 · Cited by 324 · see citing works
Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules
Moussion, C., & Girard, J. (2011) · Nature · doi:10.1038/nature10540 · Cited by 312 · see citing works
Intestinal dendritic cells increase T cell expression of α4β7 integrin
Stagg, A. J., Kamm, M. A., & Knight, S. C. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200205)32:5 · Cited by 306 · see citing works
Self-citationThe chemokine receptor D6 limits the inflammatory response in vivo
Jamieson, T. J., Cook, D. N., Nibbs, R. J. B., Rot, A., Nixon, C., McLean, P., Alcamı́, A., Lira, S. A., Wiekowski, M., & Graham, G. J. (2005) · Nature Immunology · doi:10.1038/ni1182 · Cited by 302 · see citing works
Self-citationPreformed portals facilitate dendritic cell entry into afferent lymphatic vessels
Pflicke, H., & Sixt, M. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20091739 · Cited by 301 · see citing works
The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes
Ulvmar, M. H., Werth, K., Braun, A., Kelay, P., Hub, E., Eller, K., Chan, L., Lucas, B., Novitzky-Basso, I., Nakamura, K., et al. (2014) · Nature Immunology · doi:10.1038/ni.2889 · Cited by 290 · see citing works
Self-citationTal, O., Lim, H. Y., Gurevich, I., Milo, I., Shipony, Z., Ng, L. G., Angeli, V., & Shakhar, G. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20102392 · Cited by 269 · see citing works
CXCL12-CXCR4 Engagement Is Required for Migration of Cutaneous Dendritic Cells
Kabashima, K., Shiraishi, N., Sugita, K., Mori, T., Onoue, A., Kobayashi, M., Sakabe, J., Yoshiki, R., Tamamura, H., Fujii, N., et al. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.070225 · Cited by 268 · see citing works
The β-Chemokine Receptor D6 Is Expressed by Lymphatic Endothelium and a Subset of Vascular Tumors
Nibbs, R. J. B., Kriehuber, E., Ponath, P. D., Parent, D., Qin, S., Campbell, J. D., Henderson, A., Kerjaschki, D., Maurer, D., Graham, G. J., et al. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64035-7 · Cited by 268 · see citing works
Self-citationLymph node homing of T cells and dendritic cells via afferent lymphatics
Förster, R., Braun, A., & Worbs, T. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.02.007 · Cited by 226 · see citing works
Nakano, H., & Gunn, M. D. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.1.361 · Cited by 212 · see citing works
Gosling, J., Dairaghi, D. J., Wang, Y., Hanley, M. R., Talbot, D., Miao, Z., & Schall, T. J. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.6.2851 · Cited by 209 · see citing works
Weber, M., Blair, E., Simpson, C. V., O'Hara, M., Blackburn, P. E., Rot, A., Graham, G. J., & Nibbs, R. J. B. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0634 · Cited by 188 · see citing works
Self-citationProfiling Heparin–Chemokine Interactions Using Synthetic Tools
de Paz, J. L., Moseman, E. A., Noti, C., Polito, L., von Andrian, U. H., & Seeberger, P. H. (2007) · ACS Chemical Biology · doi:10.1021/cb700159m · Cited by 165 · see citing works
The chemokine receptor CCX‐CKR mediates effective scavenging of CCL19 in vitro
Comerford, I., Milasta, S., Morrow, V. A., Milligan, G., & Nibbs, R. J. B. (2006) · European Journal of Immunology · doi:10.1002/eji.200535716 · Cited by 151 · see citing works
Self-citationThe atypical chemokine receptor D6 suppresses the development of chemically induced skin tumors
Nibbs, R. J. B., Gilchrist, D. S., King, V., Ferra, A., Forrow, S., Hunter, K. D., & Graham, G. J. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30068 · Cited by 148 · see citing works
Self-citationChemokines Have Diverse Abilities to Form Solid Phase Gradients
Patel, D. D., Koopmann, W., Imai, T., Whichard, L. P., Yoshie, O., & Krangel, M. S. (2001) · Clinical Immunology · doi:10.1006/clim.2000.4997 · Cited by 142 · see citing works
CXCL12 is essential for migration of activated Langerhans cells from epidermis to dermis
Ouwehand, K., Santegoets, S. J. A. M., Bruynzeel, D. P., Scheper, R. J., de Gruijl, T. D., & Gibbs, S. (2008) · European Journal of Immunology · doi:10.1002/eji.200838384 · Cited by 136 · see citing works
Lymph Node T Cell Homeostasis Relies on Steady State Homing of Dendritic Cells
Wendland, M., Willenzon, S., Kocks, J. R., Davalos‐Misslitz, A. C. M., Hammerschmidt, S. I., Schumann, K., Kremmer, E., Sixt, M., Hoffmeyer, A., Pabst, O., et al. (2011) · Immunity · doi:10.1016/j.immuni.2011.10.017 · Cited by 119 · see citing works
A silent chemokine receptor regulates steady-state leukocyte homing in vivo
Heinzel, K., Benz, C., & Bleul, C. C. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608274104 · Cited by 107 · see citing works
CCL21 is sufficient to mediate DC migration, maturation and function in the absence of CCL19
Britschgi, M. R., Favre, S., & Luther, S. A. (2010) · European Journal of Immunology · doi:10.1002/eji.200939921 · Cited by 89 · see citing works
Comerford, I., Nibbs, R. J. B., Litchfield, W., Bunting, M. D., Harata‐Lee, Y., Haylock‐Jacobs, S., Forrow, S., Körner, H., & McColl, S. R. (2010) · Blood · doi:10.1182/blood-2010-01-264390 · Cited by 85 · see citing works
Self-citationHansell, C. A. H., Schiering, C., Kinstrie, R., Ford, L. B., Bordon, Y., McInnes, I. B., Goodyear, C. S., & Nibbs, R. J. B. (2011) · Blood · doi:10.1182/blood-2010-11-317115 · Cited by 81 · see citing works
Self-citationAn analysis of the function and expression of D6 on lymphatic endothelial cells
McKimmie, C. S., Singh, M. D., Hewit, K. D., López‐Franco, Ó., Brocq, M. L. L., Rose‐John, S., Lee, K. M., Baker, A. H., Wheat, R. L., Blackbourn, D. J., et al. (2013) · Blood · doi:10.1182/blood-2012-04-425314 · Cited by 80 · see citing works
Self-citationHigh IL-13 production by human neonatal T cells: neonate immune system regulator?
Ribeiro-do-Couto, L. M., Boeije, L. C. M., Kroon, J., Hooibrink, B., Breur-Vriesendorp, B. S., Aarden, L. A., & Boog, C. J. P. (2001) · European Journal of Immunology · doi:10.1002/1521-4141(200111)31:11 · Cited by 80 · see citing works
Hirose, J., Kawashima, H., Willis, M. S., Springer, T. A., Hasegawa, H., Yoshie, O., & Miyasaka, M. (2002) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(02)00232-5 · Cited by 61 · see citing works
Characterization of Conventional and Atypical Receptors for the Chemokine CCL2 on Mouse Leukocytes
Ford, L. B., Cerovic, V., Milling, S. W. F., Graham, G. J., Hansell, C. A. H., & Nibbs, R. J. B. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303236 · Cited by 43 · see citing works
Self-citationCCX-CKR deficiency alters thymic stroma impairing thymocyte development and promoting autoimmunity
Bunting, M. D., Comerford, I., Seach, N., Hammett, M. V., Asquith, D. L., Körner, H., Boyd, R. L., Nibbs, R. J. B., & McColl, S. R. (2012) · Blood · doi:10.1182/blood-2012-06-434886 · Cited by 43 · see citing works
Self-citationRibeiro, A. R., Meireles, C., Rodrigues, P. M., & Alves, N. L. (2014) · European Journal of Immunology · doi:10.1002/eji.201444585 · Cited by 37 · see citing works
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Self-citationChemokines and the immune response to cancer
Ozga, A. J., Chow, M. T., & Luster, A. D. (2021) · Immunity · doi:10.1016/j.immuni.2021.01.012 · Cited by 846 · see citing works
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Wu, B., Zhang, B., Li, B., Wu, H., & Jiang, M. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-01979-x · Cited by 751 · see citing works
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Mempel, T. R., Lill, J. K., & Altenburger, L. M. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00635-w · Cited by 306 · see citing works
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Tiberio, L., Prete, A. D., Schioppa, T., Sozio, F., Bosisio, D., & Sozzani, S. (2018) · Cellular and Molecular Immunology · doi:10.1038/s41423-018-0005-3 · Cited by 257 · see citing works
Vu, R., Jin, S., Sun, P., Haensel, D., Nguyen, Q., Dragan, M., Kessenbrock, K., Nie, Q. H., & Dai, X. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111155 · Cited by 149 · see citing works
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Salem, A., Alamir, M. B., Mroueh, R., Basheer, H. A., & Afarinkia, K. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188499 · Cited by 123 · see citing works
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Jackson, D. G. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00471 · Cited by 120 · see citing works
New Insights of CCR7 Signaling in Dendritic Cell Migration and Inflammatory Diseases
Hong, W., Yang, B., He, Q., Wang, J., & Weng, Q. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.841687 · Cited by 102 · see citing works
Schwarz, J., Bierbaum, V., Merrin, J., Frank, T., Hauschild, R., Bollenbach, T., Tay, S., Sixt, M., & Mehling, M. (2016) · Scientific Reports · doi:10.1038/srep36440 · Cited by 80 · see citing works
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Bastow, C. R., Bunting, M. D., Kara, E. E., McKenzie, D. R., Caon, A., Devi, S., Tolley, L., Mueller, S. N., Frazer, I. H., Harvey, N., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025763118 · Cited by 47 · see citing works
Thomson, C. A., van de Pavert, S. A., Stakenborg, M., Labeeuw, E., Matteoli, G., Mowat, A. M., & Nibbs, R. J. B. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1700967 · Cited by 46 · see citing works
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Friess, M. C., Kritikos, I., Schineis, P., Medina-Sanchez, J. D., Gkountidi, A., Vallone, A., Sigmund, E. C., Schwitter, C., Vranova, M., Matti, C., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110334 · Cited by 38 · see citing works
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Wangmo, D., Premsrirut, P. K., Yuan, C., Morris, W. S., Zhao, X., & Subramanian, S. (2021) · Cancers · doi:10.3390/cancers13195021 · Cited by 21 · see citing works
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Zhao, L., Shireman, J. M., Probelsky, S. M., Rigg, B., Wang, X., Huff, W. X., Kwon, J. H., & Dey, M. (2024) · Cancers · doi:10.3390/cancers16203459 · Cited by 11 · see citing works
Generating a Tolerogenic Cell Therapy Knowledge Graph from Literature
Lamúrias, A., Ferreira, J. D., Clarke, L. A., & Couto, F. M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01656 · Cited by 11 · see citing works
Evaluation of Atypical Chemokine Receptor Expression in T Cell Subsets
Pacheco, M. O., Rocha, F. A., Aloia, T. P. A., & Marti, L. C. (2022) · Cells · doi:10.3390/cells11244099 · Cited by 8 · see citing works
Lokhande, L., Nilsson, D., Rodrigues, J. D. M., Hassan, M., Olsson, L. M., Pyl, P. T., Vasquez, L. J., Porwit‐MacDonald, A., Gerdtsson, A. S., Jerkeman, M., et al. (2024) · Cancers · doi:10.3390/cancers16132289 · Cited by 7 · see citing works
Canonical and atypical chemokine receptors in the neutrophil life cycle.
Donato, R. D., Bonecchi, R., & Albano, F. (2023) · Cytokine · doi:10.1016/j.cyto.2023.156297 · Cited by 7 · see citing works
Disruption of placental ACKR3 impairs growth and hematopoietic development of offspring
Fukuoka, A., Wilson, G. J., Pitmon, E., Foley, L. K., Johnsson, H. J., Pingen, M., & Graham, G. J. (2024) · Development · doi:10.1242/dev.202333 · Cited by 5 · see citing works
Self-citationRedder, E., Kirschnick, N., Fang, S., Kuhlmann, M. T., González‐Loyola, A., Wyss, T., Stehling, M., Adams, R. H., Petrova, T. V., Alitalo, K. K., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.11.548304 · Cited by 5 · see citing works
CD112 Supports Lymphatic Migration of Human Dermal Dendritic Cells
Jahromi, N. H., Gkountidi, A., Collado‐Díaz, V., Blatter, K., Bauer, A., Zambounis, L., Medina-Sanchez, J. D., Russo, E., Runge, P., Restivo, G., et al. (2024) · Cells · doi:10.3390/cells13050424 · Cited by 4 · see citing works
Lymphangiogenesis orchestrating tumor microenvironment: Face changing in immunotherapy
Zhang, J.-Y., Li, H., Zhang, M.-J., & Sun, Z. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189278 · Cited by 3 · see citing works
COVID-19 vaccine type controls stromal reprogramming in draining lymph nodes
Fair-Mäkelä, R., Thorén, P., Näsiaho, J., Sundqvist, P., Piiroinen, I., Kähäri, L., Julkunen, I., Ivaska, J., Hub, E., Rot, A., et al. (2025) · Science Immunology · doi:10.1126/sciimmunol.adr6787 · Cited by 4 · see citing works
Choi, K.-M., Hwang, S. D., Joo, M.-S., Hwang, J. Y., Kwon, M., Jeong, J.-M., Seo, J. S., Jee, B.-Y., & Park, C. (2019) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2019.07.004 · Cited by 3 · see citing works
Gerken, O. J., Catone, N., & Legler, D. F. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01961-8 · Cited by 2 · see citing works
Naser, I. H., Hamza, A. A., Alhili, A., Faisal, A. N., Ali, M. S., Kadhim, N. A., Suliman, M., Alshahrani, M. Y., & Alawadi, A. H. (2024) · Cell Biochemistry and Function · doi:10.1002/cbf.4009 · Cited by 2 · see citing works
Development of specific anti-mouse atypical chemokine receptor 4 monoclonal antibodies
Hirose, M., Suzuki, H., Ubukata, R., Tanaka, T., Kaneko, M. K., & Kato, Y. (2024) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2024.101824 · Cited by 2 · see citing works
Development of a human antibody that exhibits antagonistic activity toward CC chemokine receptor 7
Jang, M.-S., Ismail, N. S. B., & Yu, Y. G. (2022) · Antibody Therapeutics · doi:10.1093/abt/tbac016 · Cited by 1 · see citing works
Redder, E., Kirschnick, N., Fang, S., Kuhlmann, M. T., González‐Loyola, A., Wyss, T., Stehling, M., Adams, R. H., Petrova, T. V., Alitalo, K. K., et al. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4523131 · Cited by 1 · see citing works
Liu, M., Chen, S., Xu, Y., Kong, Y., Deng, Y., Li, F., & Tao, Z. (2019) · International Archives of Allergy and Immunology · doi:10.1159/000504476
Disruption of maternal ACKR3 has profound effects on embryos and offspringPreprint
Fukuoka, A., Wilson, G. J., Pitmon, E., Foley, L. K., Johnsson, H. J., Pingen, M., & Graham, G. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.15.545186
Self-citationNMR indicates the N-termini of PSGL1 and CCR7 bind competitively to the chemokine CCL21
Witt, R. N., Nickel, K. S., Binns, J. R., Gray, A. M., Hintz, A. M., Kofron, N. F., Steigleder, S. F., Peterson, F. C., & Veldkamp, C. T. (2023) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2023.101524
GPCR kinase 3 phosphorylates atypical chemokine receptor 4 independent of G proteinsPreprint
Lamme, T. D., Arroyo, I. B. S., Smit, M. J., & Schafer, C. T. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.09.698634
G protein–coupled receptor kinase 3 couples atypical chemokine receptor 4 independent of G proteins
Lamme, T. D., Arroyo, I. B. S., Smit, M. J., & Schafer, C. T. (2026) · Molecular Pharmacology · doi:10.1016/j.molpha.2026.100129
GPCR kinases shape ACKR4 functions via differential C-terminal phosphorylation
Gerken, O. J., Warmers, R., Hild, C., Kielkopf, N., Catone, N., Bruderer, R., & Legler, D. F. (2026) · Nature Communications · doi:10.1038/s41467-026-73074-4
Hirose, M., Tanaka, T., Yanaka, M., Nakamura, T., Kaneko, M. K., Suzuki, H., & Kato, Y. (2026) · Monoclonal Antibodies in Immunodiagnosis and Immunotherapy · doi:10.1177/21679436261461702
Lymphatic Endothelial Cells in Health and Disease
Tang, D., Wang, L., Liu, H., Zhong, J., Li, S., & Rao, X. (2026) · MedComm · doi:10.1002/mco2.70891
- Authors
- Bryce, S. A., Wilson, R. A. M., Tiplady, E. M., Asquith, D. L., Bromley, S. K., Luster, A. D., Graham, G. J., & Nibbs, R. J. B.
- Affiliations
- University of Glasgow (GB)
- Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, University of Glasgow , Glasgow G12 8TA ,
- Harvard University (US)
- Corresponding author
- Nibbs, Robert J B
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-04
- Volume
- 196
- Issue
- 8
- Pages
- 3341-3353
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2305178018
- Cited by
- 71
- References
- 42
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 13 · 2023: 8 · 2022: 7 · 2021: 11 · 2020: 5 · 2019: 8 · 2018: 8 · 2017: 3 · 2016: 1
- FWCI
- 3.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (submittedVersion)
- Funders
- Cancer Research Institute
- Cancer Research UK (C596A17196, C596/A18076)
- University of Glasgow
- Medical Research Council (MR/M019764/1)
- Biotechnology and Biological Sciences Research Council (1371671)
- Beatson Institute for Cancer Research
- Topics
- Health Sciences › Medicine › Oncology › Chemokine receptors and signaling
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- ACKR4, CCL19, CCL21, CCR7, Langerhans cells, dermal dendritic cells, skin-draining lymph nodes, chemokine scavenging, keratinocytes, skin inflammation, subcapsular sinus
- MeSH terms
- Animals, Cell Movement, Dendritic Cells, Inflammation, Lymph Nodes, Male, Mice, Inbred C57BL, Skin, Keratinocytes, Stromal Cells, Mice, Knockout, Protein Transport, Endothelial Cells, Mice, Receptors, CCR, Receptors, CCR7, Chemokine CCL19, Chemokine CCL21
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.
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