DOI: 10.1084/jem.189.3.451. Mice Lacking Expression of Secondary Lymphoid Organ Chemokine Have Defects in Lymphocyte Homing and Dendritic Cell Localization

Mice Lacking Expression of Secondary Lymphoid Organ Chemokine Have Defects in Lymphocyte Homing and Dendritic Cell Localization

10.1084/jem.189.3.451

Crossref journal-article

Rockefeller University Press

The Journal of Experimental Medicine (291)

Abstract

Secondary lymphoid organ chemokine (SLC) is expressed in high endothelial venules and in T cell zones of spleen and lymph nodes (LNs) and strongly attracts naive T cells. In mice homozygous for the paucity of lymph node T cell (plt) mutation, naive T cells fail to home to LNs or the lymphoid regions of spleen. Here we demonstrate that expression of SLC is undetectable in plt mice. In addition to the defect in T cell homing, we demonstrate that dendritic cells (DCs) fail to accumulate in spleen and LN T cell zones of plt mice. DC migration to LNs after contact sensitization is also substantially reduced. The physiologic significance of these abnormalities in plt mice is indicated by a markedly increased sensitivity to infection with murine hepatitis virus. The plt mutation maps to the SLC locus; however, the sequence of SLC introns and exons in plt mice is normal. These findings suggest that the abnormalities in plt mice are due to a genetic defect in the expression of SLC and that SLC mediates the entry of naive T cells and antigen-stimulated DCs into the T cell zones of secondary lymphoid organs.

Bibliography

Gunn, M. D., Kyuwa, S., Tam, C., Kakiuchi, T., Matsuzawa, A., Williams, L. T., & Nakano, H. (1999). Mice Lacking Expression of Secondary Lymphoid Organ Chemokine Have Defects in Lymphocyte Homing and Dendritic Cell Localization. The Journal of Experimental Medicine, 189(3), 451â460.

Authors 7

Michael D. Gunn (first)
Shigeru Kyuwa (additional)
Carmen Tam (additional)
Terutaka Kakiuchi (additional)
Akio Matsuzawa (additional)
Lewis T. Williams (additional)
Hideki Nakano (additional)

References 53 Referenced 813

10.4049/jimmunol.157.2.495 / J Immunol / Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic by Gretz (1996)
10.1146/annurev.immunol.15.1.675 / Annu Rev Immunol / Human chemokines: an update by Baggiolini (1997)
10.1038/33340 / Nature / Chemokines and leukocyte traffic by Baggiolini (1998)
10.1002/jlb.62.5.634 / J Leukocyte Biol / Novel lymphocyte-specific CC chemokines and their receptors by Yoshie (1997)
10.1016/S0960-9822(06)00105-9 / Curr Biol / Lymphocyte homing: the scent of a follicle by Goodnow (1997)
10.1016/S0092-8674(00)81798-5 / Cell / A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen by Forster (1996)
10.1038/35876 / Nature / A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1 by Gunn (1998)
10.1084/jem.187.4.655 / J Exp Med / B cell–attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5 by Legler (1998)
10.3109/08830189009056624 / Int Rev Immunol / Interstitial dendritic cells by Hart (1990)
10.1146/annurev.iy.09.040191.001415 / Annu Rev Immunol / The dendritic cell system and its role in immunogenicity by Steinman (1991)
10.1038/32588 / Nature / Dendritic cells and the control of immunity by Banchereau (1998)
10.1084/jem.167.2.632 / J Exp Med / Migration patterns of dendritic cells in the mouse. Traffic from the blood, and T cell–dependent and –independent entry to lymphoid tissues by Kupiec-Weglinski (1988)
10.1084/jem.167.2.646 / J Exp Med / Migration patterns of dendritic cells in the mouse. Homing to T cell–dependent areas of spleen, and binding within marginal zone by Austyn (1988)
10.1084/jem.166.6.1654 / J Exp Med / Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies by Macatonia (1987)
10.1016/0008-8749(85)90266-7 / Cell Immunol / The role of dendritic cells in the initiation of immune responses to contact sensitizers. I. In vivo exposure to antigen by Knight (1985)
10.1146/annurev.ph.57.030195.004143 / Annu Rev Physiol / Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration by Springer (1995)
10.1126/science.272.5258.60 / Science / Lymphocyte homing and homeostasis by Butcher (1996)
10.1007/BF02002614 / Experientia / Compartments, domains and migration pathways of lymphoid cells in the splenic pulp by van Ewijk (1985)
10.1074/jbc.272.31.19518 / J Biol Chem / Molecular cloning of a novel human CC chemokine secondary lymphoid-tissue chemokine that is a potent chemoattractant for lymphocytes and mapped to chromosome 9p13 by Nagira (1997)
10.4049/jimmunol.159.4.1589 / J Immunol / Identification and characterization of a novel beta chemokine containing six conserved cysteines by Hedrick (1997)
10.4049/jimmunol.159.6.2554 / J Immunol / Isolation and characterization of Exodus-2, a novel C-C chemokine with a unique 37 amino acid carboxyl-terminal extension by Hromas (1997)
10.4049/jimmunol.159.11.5671 / J Immunol / Identification of a new mouse beta-chemokine, thymus-derived chemotactic agent 4, with activity on T lymphocytes and mesangial cells by Tanabe (1997)
10.1073/pnas.95.1.258 / Proc Natl Acad Sci USA / A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes by Gunn (1998)
10.1083/jcb.141.4.1053 / J Cell Biol / 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3beta receptor CCR7 by Campbell (1998)
10.1126/science.279.5349.381 / Science / Chemokines and the arrest of lymphocytes rolling under flow conditions by Campbell (1998)
10.4049/jimmunol.161.2.952 / J Immunol / Secondary lymphoid-tissue chemokine (SLC) stimulates integrin α4β7-mediated adhesion of lymphocytes to mucosal addressin cell adhesion molecule-1 (MadCAM-1) under flow by Pachynski (1998)
10.4049/jimmunol.161.11.6330 / J Immunol / A high endothelial cell-derived chemokine induces rapid, efficient, and subset-selective arrest of rolling T lymphocytes on a reconstituted endothelial substrate by Tangemann (1998)
10.1002/eji.1830270132 / Eur J Immunol / Genetic defect in T lymphocyte-specific homing into peripheral lymph nodes by Nakano (1997)
10.1182/blood.V91.8.2886.2886_2886_2895 / Blood / A novel mutant gene involved in T-lymphocyte-specific homing into peripheral lymphoid organs on mouse chromosome 4 by Nakano (1998)
10.4049/jimmunol.160.5.2166 / J Immunol / Heterogeneity of mouse spleen dendritic cells: in vivo phagocytic activity, expression of macrophage markers, and subpopulation turnover by Leenen (1998)
10.1084/jem.172.5.1483 / J Exp Med / Migration and maturation of Langerhans cells in skin transplants and explants by Larsen (1990)
10.1538/expanim.46.311 / Exp Anim / Replication of murine coronaviruses in mouse embryonic stem cell lines in vitro by Kyuwa (1997)
10.1128/jvi.70.6.4146-4149.1996 / J Virol / Maintenance of pluripotency in mouse embryonic stem cells persistently infected with murine coronavirus by Okumura (1996)
10.1006/cimm.1995.1110 / Cell Immunol / Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues by Witmer-Pack (1995)
{'key': '2023072508303853800_B35', 'first-page': '277', 'article-title': 'Systemic migration of dendritic cells during contact sensitization', 'volume': '71', 'author': 'Hill', 'year': '1990', 'journal-title': 'Immunology'} / Immunology / Systemic migration of dendritic cells during contact sensitization by Hill (1990)
10.1002/jlb.52.1.34 / J Leukocyte Biol / Two populations of splenic dendritic cells detected with M342, a new monoclonal to an intracellular antigen of interdigitating dendritic cells and some B lymphocytes by Agger (1992)
10.4049/jimmunol.159.2.565 / J Immunol / Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes by Vremec (1997)
10.1084/jem.184.4.1413 / J Exp Med / Regulation of dendritic cell numbers and maturation by lipopolysaccharide in vivo by De Smedt (1996)
10.1074/jbc.273.12.7118 / J Biol Chem / Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7 by Yoshida (1998)
10.4049/jimmunol.160.5.2418 / J Immunol / CK beta-11/macrophage inflammatory protein-3 beta/EBI1-ligand chemokine is an efficacious chemoattractant for T and B cells by Kim (1998)
10.1084/jem.188.1.181 / J Exp Med / Epstein-Barr virus–induced molecule 1 ligand chemokine is expressed by dendritic cells in lymphoid tissues and strongly attracts naive T cells and activated B cells by Ngo (1998)
10.4049/jimmunol.132.1.354 / J Immunol / Molecular mechanisms of lymphocyte extravasation. I. Studies of two selective inhibitors of lymphocyte recirculation by Spangrude (1984)
10.1084/jem.182.2.581 / J Exp Med / Pertussis toxin inhibits migration of B and T lymphocytes into splenic white pulp cords by Cyster (1995)
10.1038/42716 / Nature / A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells by Adema (1997)
10.1084/jem.184.6.2341 / J Exp Med / The route of antigen entry determines the requirement for L-selectin during immune responses by Catalina (1996)
10.1016/0008-8749(85)90267-9 / Cell Immunol / The role of dendritic cells in the initiation of immune responses to contact sensitizers. II. Studies in nude mice by Knight (1985)
10.4049/jimmunol.161.3.1083 / J Immunol / Differential regulation of chemokine receptors during dendritic cell maturation: a model for their trafficking properties by Sozzani (1998)
10.1084/jem.188.2.373 / J Exp Med / Selective recruitment of immature and mature dendritic cells by distinct chemokines expressed in different anatomic sites by Dieu (1998)
10.1002/(SICI)1521-4141(199809)28:09<2760::AID-IMMU2760>3.0.CO;2-N / Eur J Immunol / Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation by Sallusto (1988)
10.1084/jem.164.3.723 / J Exp Med / Cooperation between cytotoxic and helper T lymphocytes in protection against lethal Sendai virus infection. Protection by T cells is MHC-restricted and MHC-regulated; a model for MHC–disease associations by Kast (1986)
10.1126/science.7569902 / Science / Activation of dual T cell signaling pathways by the chemokine RANTES by Bacon (1995)
10.4049/jimmunol.156.6.2095 / J Immunol / Chemokines and T lymphocyte activation. I. Beta chemokines costimulate human T lymphocyte activation in vitro by Taub (1996)
10.1073/pnas.86.19.7470 / Proc Natl Acad Sci USA / Gamma delta beta-thalassemia due to a de novo mutation deleting the 5′ beta-globin gene activation-region hypersensitive sites by Driscoll (1989)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:49 p.m.)
Deposited	2 years, 1 month ago (July 25, 2023, 5:42 a.m.)
Indexed	1 hour, 17 minutes ago (Sept. 3, 2025, 3:32 a.m.)
Issued	26 years, 7 months ago (Feb. 1, 1999)
Published	26 years, 7 months ago (Feb. 1, 1999)
Published Online	26 years, 7 months ago (Feb. 1, 1999)
Published Print	26 years, 7 months ago (Feb. 1, 1999)

Funders 0

None

BibTeX

@article{Gunn_1999, title={Mice Lacking Expression of Secondary Lymphoid Organ Chemokine Have Defects in Lymphocyte Homing and Dendritic Cell Localization}, volume={189}, ISSN={1540-9538}, url={http://dx.doi.org/10.1084/jem.189.3.451}, DOI={10.1084/jem.189.3.451}, number={3}, journal={The Journal of Experimental Medicine}, publisher={Rockefeller University Press}, author={Gunn, Michael D. and Kyuwa, Shigeru and Tam, Carmen and Kakiuchi, Terutaka and Matsuzawa, Akio and Williams, Lewis T. and Nakano, Hideki}, year={1999}, month=feb, pages={451–460} }

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      "first-page": "495",
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      "article-title": "Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic",
      "volume": "157",
      "author": "Gretz",
      "year": "1996",
      "journal-title": "J Immunol"
    },
    {
      "key": "2023072508303853800_B2",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1146/annurev.immunol.15.1.675",
      "article-title": "Human chemokines: an update",
      "volume": "15",
      "author": "Baggiolini",
      "year": "1997",
      "journal-title": "Annu Rev Immunol"
    },
    {
      "key": "2023072508303853800_B3",
      "doi-asserted-by": "crossref",
      "first-page": "565",
      "DOI": "10.1038/33340",
      "article-title": "Chemokines and leukocyte traffic",
      "volume": "392",
      "author": "Baggiolini",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "2023072508303853800_B4",
      "doi-asserted-by": "crossref",
      "first-page": "634",
      "DOI": "10.1002/jlb.62.5.634",
      "article-title": "Novel lymphocyte-specific CC chemokines and their receptors",
      "volume": "62",
      "author": "Yoshie",
      "year": "1997",
      "journal-title": "J Leukocyte Biol"
    },
    {
      "key": "2023072508303853800_B5",
      "doi-asserted-by": "crossref",
      "first-page": "R219",
      "DOI": "10.1016/S0960-9822(06)00105-9",
      "article-title": "Lymphocyte homing: the scent of a follicle",
      "volume": "7",
      "author": "Goodnow",
      "year": "1997",
      "journal-title": "Curr Biol"
    },
    {
      "key": "2023072508303853800_B6",
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      "first-page": "1",
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      "author": "Forster",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2023072508303853800_B7",
      "doi-asserted-by": "crossref",
      "first-page": "799",
      "DOI": "10.1038/35876",
      "article-title": "A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1",
      "volume": "391",
      "author": "Gunn",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "2023072508303853800_B8",
      "doi-asserted-by": "crossref",
      "first-page": "655",
      "DOI": "10.1084/jem.187.4.655",
      "article-title": "B cell\u2013attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5",
      "volume": "187",
      "author": "Legler",
      "year": "1998",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072508303853800_B9",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.3109/08830189009056624",
      "article-title": "Interstitial dendritic cells",
      "volume": "6",
      "author": "Hart",
      "year": "1990",
      "journal-title": "Int Rev Immunol"
    },
    {
      "key": "2023072508303853800_B10",
      "doi-asserted-by": "crossref",
      "first-page": "271",
      "DOI": "10.1146/annurev.iy.09.040191.001415",
      "article-title": "The dendritic cell system and its role in immunogenicity",
      "volume": "9",
      "author": "Steinman",
      "year": "1991",
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    },
    {
      "key": "2023072508303853800_B11",
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      "first-page": "245",
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      "first-page": "632",
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      "author": "Kupiec-Weglinski",
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      "author": "Springer",
      "year": "1995",
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      "first-page": "199",
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      "volume": "41",
      "author": "van Ewijk",
      "year": "1985",
      "journal-title": "Experientia"
    },
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      "first-page": "19518",
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      "article-title": "Molecular cloning of a novel human CC chemokine secondary lymphoid-tissue chemokine that is a potent chemoattractant for lymphocytes and mapped to chromosome 9p13",
      "volume": "272",
      "author": "Nagira",
      "year": "1997",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "2023072508303853800_B20",
      "doi-asserted-by": "crossref",
      "first-page": "1589",
      "DOI": "10.4049/jimmunol.159.4.1589",
      "article-title": "Identification and characterization of a novel beta chemokine containing six conserved cysteines",
      "volume": "159",
      "author": "Hedrick",
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      "volume": "95",
      "author": "Gunn",
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      "volume": "141",
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      "first-page": "381",
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      "volume": "27",
      "author": "Nakano",
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      "first-page": "1483",
      "DOI": "10.1084/jem.172.5.1483",
      "article-title": "Migration and maturation of Langerhans cells in skin transplants and explants",
      "volume": "172",
      "author": "Larsen",
      "year": "1990",
      "journal-title": "J Exp Med"
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      "first-page": "311",
      "DOI": "10.1538/expanim.46.311",
      "article-title": "Replication of murine coronaviruses in mouse embryonic stem cell lines in vitro",
      "volume": "46",
      "author": "Kyuwa",
      "year": "1997",
      "journal-title": "Exp Anim"
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      "first-page": "4146",
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      "volume": "70",
      "author": "Okumura",
      "year": "1996",
      "journal-title": "J Virol"
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      "key": "2023072508303853800_B34",
      "doi-asserted-by": "crossref",
      "first-page": "157",
      "DOI": "10.1006/cimm.1995.1110",
      "article-title": "Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues",
      "volume": "163",
      "author": "Witmer-Pack",
      "year": "1995",
      "journal-title": "Cell Immunol"
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    {
      "key": "2023072508303853800_B35",
      "first-page": "277",
      "article-title": "Systemic migration of dendritic cells during contact sensitization",
      "volume": "71",
      "author": "Hill",
      "year": "1990",
      "journal-title": "Immunology"
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      "key": "2023072508303853800_B36",
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      "first-page": "34",
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      "article-title": "Two populations of splenic dendritic cells detected with M342, a new monoclonal to an intracellular antigen of interdigitating dendritic cells and some B lymphocytes",
      "volume": "52",
      "author": "Agger",
      "year": "1992",
      "journal-title": "J Leukocyte Biol"
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      "key": "2023072508303853800_B37",
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      "first-page": "565",
      "DOI": "10.4049/jimmunol.159.2.565",
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      "volume": "159",
      "author": "Vremec",
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      "journal-title": "J Immunol"
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      "first-page": "1413",
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      "volume": "184",
      "author": "De Smedt",
      "year": "1996",
      "journal-title": "J Exp Med"
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      "first-page": "7118",
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      "article-title": "Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7",
      "volume": "273",
      "author": "Yoshida",
      "year": "1998",
      "journal-title": "J Biol Chem"
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      "key": "2023072508303853800_B40",
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      "volume": "160",
      "author": "Kim",
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      "volume": "188",
      "author": "Ngo",
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      "article-title": "Molecular mechanisms of lymphocyte extravasation. I. Studies of two selective inhibitors of lymphocyte recirculation",
      "volume": "132",
      "author": "Spangrude",
      "year": "1984",
      "journal-title": "J Immunol"
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      "first-page": "581",
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      "volume": "182",
      "author": "Cyster",
      "year": "1995",
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      "first-page": "713",
      "DOI": "10.1038/42716",
      "article-title": "A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells",
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      "author": "Adema",
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      "journal-title": "Nature"
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      "author": "Catalina",
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      "DOI": "10.1016/0008-8749(85)90267-9",
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      "volume": "94",
      "author": "Knight",
      "year": "1985",
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      "author": "Sozzani",
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      "author": "Dieu",
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      "article-title": "Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation",
      "volume": "28",
      "author": "Sallusto",
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      "volume": "164",
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      "volume": "156",
      "author": "Taub",
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      "volume": "86",
      "author": "Driscoll",
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