In vivo-activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines

Journal of Experimental Medicine

Volumn 190, Issue 8, 1999, Pages 1123-1134

  Ansel, K Mark ^a   McHeyzer Williams, Louise J ^b   Ngo, Vu N ^a   McHeyzer Williams, Michael G ^b   Cyster, Jason G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Chemokine; CXCR5; ELC; Follicle; T lymphocyte

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5;

ANIMAL CELL; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; CELL COMPARTMENTALIZATION; CELL MIGRATION; GERMINAL CENTER; IMMUNE RESPONSE; IN SITU HYBRIDIZATION; LYMPHOCYTE COUNT; LYMPHOID TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RECEPTOR UPREGULATION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, CD8; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CHEMOKINES, CC; CHEMOKINES, CXC; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GERMINAL CENTER; IN SITU HYBRIDIZATION, FLUORESCENCE; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED MRL LPR; RECEPTORS, CHEMOKINE; RECEPTORS, CYTOKINE; SPLEEN; UP-REGULATION;

EID: 0032701695     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.8.1123     Document Type: Article

References (63)

1. MacLennan, I.C.M. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139.
2. Kelsoe, G. 1996. The germinal center: a crucible for lymphocyte selection. Semin. Immunol. 8:179-184.
3. Cyster, J.G. 1997. Signaling thresholds and interclonal competition in preimmune B-cell selection. Immunol. Rev. 156: 87-101.
4. Van den Eertwegh, A.J.M., R.J. Noelle, M. Roy, D.M. Shepherd, A. Aruffo, J.A. Ledbetter, W.J.A. Boersma, and E. Claassen. 1993. In vivo CD40-gp39 interactions are essential for thymus-dependent humoral immunity. I. In vivo expression of CD40 ligand, cytokines, and antibody production delineates sites of cognate T-B cell interactions. J. Exp. Med. 178:1555-1565.
5. Toellner, K.M., A. Gulbranson-Judge, D.R. Taylor, D.M. Sze, and I.C. MacLennan. 1996. Immunoglobulin switch transcript production in vivo related to the site and time of antigen-specific B cell activation. J. Exp. Med. 183:2303-2312.
6. Garside, P., E. Ingulli, R.R. Merica, J.G. Johnson, R.J. Noelle, and M.K. Jenkins. 1998. Visualization of specific B and T lymphocyte interactions in the lymph node. Science. 281: 96-99.
7. Fuller, K.A., O. Kanagawa, and M.H. Nahm. 1993. T cells within germinal centers are specific for the immunizing antigen. J. Immunol. 151:4505-4512.
8. + memory T cells contains preformed CD40 ligand that is rapidly but transiently expressed on their surface after activation through the T cell receptor complex. J. Exp. Med. 181:1293-1301.
9. Gulbranson-Judge, A., and I. MacLennan. 1996. Sequential antigen-specific growth of T cells in the T zones and follicles in response to pigeon cytochrome c. Eur. J. Immunol. 26: 1830-1837.
10. Zheng, B., S. Han, and G. Kelsoe. 1996. T helper cells in murine germinal centers are antigen-specific emigrants that downregulate Thy-1. J. Exp. Med. 184:1083-1091.
11. Luther, S.A., A. Gulbranson-Judge, H. Acha-Orbea, and I.C. MacLennan. 1997. Viral superantigen drives extrafollicular and follicular B cell differentiation leading to virus-specific antibody production. J. Exp. Med. 185:551-562.
12. Hutloff, A., A.M. Dittrich, K.C. Beier, B. Eljaschewitsch, R. Kraft, I. Anagnostopoulos, and R.A. Kroczek. 1999. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature. 397:263-266.
13. Kearney, E.R., K.A. Pape, D.Y. Loh, and M.K. Jenkins. 1994. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1:327-339.
14. Zheng, B., S. Han, Q. Zhu, R. Goldsby, and G. Kelsoe. 1996. Alternative pathways for the selection of antigen-specific peripheral T cells. Nature. 384:263-266.
15. Hedrick, S.M., I. Engel, D.L. McElligott, P.J. Fink, M.L. Hsu, D. Hansburg, and L.A. Matis. 1988. Selection of amino acid sequences in the beta chain of the T cell antigen receptor. Science. 239:1541-1544.
16. McHeyzer-Williams, M.G., and M.M. Davis. 1995. Antigen-specific development of primary and memory T cells in vivo. Science. 268:106-111.
17. McHeyzer-Williams, L.J., J.F. Panus, J.A. Mikszta, and M.G. McHeyzer-Williams. 1999. Evolution of antigen-specific T cell receptors in vivo: preimmune and antigen-driven selection of preferred complementarity-determining region 3 (CDR3) motifs. J. Exp. Med. 189:1823-1838.
18. Gunn, M.D., V.N. Ngo, K.M. Ansel, E.H. Ekland, J.G. Cyster, and L.T. Williams. 1998. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature. 391:799-803.
19. Legler, D.F., M. Loetscher, R.S. Roos, I. Clark-Lewis, M. Baggiolini, and B. Moser. 1998. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J. Exp. Med. 187:655-660.
20. Forster, R., T. Emrich, E. Kremmer, and M. Lipp. 1994. Expression of the G-protein-coupled receptor BLR1 defines mature, recirculating B cells and a subset of T-helper memory cells. Blood. 84:830-840.
21. Forster, R., A.E. Mattis, E. Kremmer, E. Wolf, G. Brem, and M. Lipp. 1996. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell. 87:1037-1047.
22. Gunn, M.D., K. Tangemann, C. Tam, J.G. Cyster, S.D. Rosen, and L.T. Williams. 1998. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc. Natl. Acad. Sci. USA. 95:258-263.
23. Ngo, V.N., H.L. Tang, and J.G. Cyster. 1998. 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. J. Exp. Med. 188:181-191.
24. Tanabe, S., Z. Lu, Y. Luo, E.J. Quackenbush, M.A. Berman, L.A. Collins-Racie, S. Mi, C. Reilly, D. Lo, K.A. Jacobs, and M.E. Dorf. 1997. Identification of a new mouse beta-chemokine, thymus-derived chemotactic agent 4, with activity on T lymphocytes and mesangial cells. J. Immunol. 159:5671-5679.
25. Yoshida, R., M. Nagira, M. Kitaura, N. Imagawa, T. Imai, and O. Yoshie. 1998. Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7. J. Biol. Chem. 273:7118-7122.
26. Campbell, J.J., E.P. Bowman, K. Murphy, K.R. Youngman, M.A. Siani, D.A. Thompson, L. Wu, A. Zlotnik, and E.C. Butcher. 1998. 6-C-kine (SLC), a lymphocyte adhesion-triggering chemokine expressed by high endothelium, is an agonist for the MIP-3β receptor CCR7. J. Cell Biol. 141:1053-1059.
27. Kim, C.H., L.M. Pelus, J.R. White, E. Applebaum, K. Johanson, and H.E. Broxmeyer. 1998. CK beta-11/macrophage inflammatory protein-3 beta/EBI1-ligand chemokine is an efficacious chemoattractant for T and B cells. J. Immunol. 160:2418-2424.
28. Nagira, M., T. Imai, R. Yoshida, S. Takagi, M. Iwasaki, M. Baba, Y. Tabira, J. Akagi, H. Nomiyama, and O. Yoshie. 1998. A lymphocyte-specific CC chemokine, secondary lymphoid tissue chemokine (SLC), is a highly efficient chemoattractant for B cells and activated T cells. Eur. J. Immunol. 28:1516-1523.
29. Willimann, K., D.F. Legler, M. Loetscher, R.S. Roos, M.B. Delgado, I. Clark-Lewis, M. Baggiolini, and B. Moser. 1998. The chemokine SLC is expressed in T cell areas of lymph nodes and mucosal lymphoid tissues and attracts activated T cells via CCR7. Eur. J. Immunol. 28:2025-2034.
30. Yoshida, R., M. Nagira, T. Imai, M. Baba, S. Takagi, Y. Tabira, J. Akagi, H. Nomiyama, and O. Yoshie. 1998. EBI1-ligand chemokine (ELC) attracts a broad spectrum of lymphocytes: activated T cells strongly up-regulate CCR7 and efficiently migrate toward ELC. Int. Immunol. 10:901-910.
31. Gunn, M.D., S. Kyuwa, C. Tam, T. Kakiuchi, A. Matsuzawa, L.T. Williams, and H. Nakano. 1999. Mice lacking expression of secondary lymphoid-organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189:451-460.
32. 1o thymocytes in vivo. Science. 250:1720-1723.
33. Lamarche, N., N. Tapon, L. Stowers, P.D. Burbelo, P. Aspenstrom, T. Bridges, J. Chant, and A. Hall. 1996. Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65pak and the JNK/SAPK MAP kinase cascade. Cell. 87:519-529.
34. Pape, K.A., A. Khoruts, A. Mondino, and M.K. Jenkins. 1997. Inflammatory cytokines enhance the in vivo clonal expansion and differentiation of antigen-activated CD4+ T cells. J. Immunol. 159:591-598.
35. Schmidt, K.N., C.W. Hsu, C.T. Griffin, C.C. Goodnow, and J.G. Cyster. 1998. Spontaneous follicular exclusion of SHP1-deficient B cells is conditional on the presence of competitor wild-type B cells. J. Exp. Med. 187:929-937.
36. Cyster, J.G., V.N. Ngo, E.H. Ekland, M.D. Gunn, J.D. Sedgwick, and K.M. Ansel. 1999. Chemokines and B-cell homing to follicles. Curr. Top. Microbiol. Immunol. 246:87-92.
37. Kraal, G., and M. Janse. 1986. Marginal metallophilic cells of the mouse spleen identified by a monoclonal antibody. Immunology. 58:665-669.
38. Peacock, J.W., and F.R. Jink. 1999. TCR activation inhibits chemotaxis toward stromal cell-derived factor-1: evidence for reciprocal regulation between CXCR4 and the TCR. J. Immunol. 162:215-223.
39. Lieberum, B., and K.U. Hartmann. 1988. Successive changes of the cellular composition in lymphoid organs of MRL-Mp/lpr-lpr mice during the development of lymphoproliferative disease as investigated in cryosections. Clin. Immunol. Immunopathol. 46:421-131.
40. Usui, T., H. Yoshioka, K. Ko, M.E. Sung, N. Nagata, T. Okamoto, G. Ohshio, T. Kita, and M. Inada. 1996. Age associated changes in the distribution of lpr gene-induced B220-positive T cells in lymphoid organs of MRL/Mp-lpr/lpr mice using dual exposure microphotographs of double immunofluorescence staining. Biotech. Histochem. 71:182-189.
41. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
42. Ohshima, Y., Y. Tanaka, H. Tozawa, Y. Takahashi, C. Maliszewski, and G. Delespesse. 1997. Expression and function of OX40 ligand on human dendritic cells. J. Immunol. 159: 3838-3848.
43. Flynn, S., K.M. Toellner, C. Raykundalia, M. Goodall, and P. Lane. 1998. CD4 T cell cytokine differentiation: the B cell activation molecule, OX40 ligand, instructs CD4 T cells to express interleukin 4 and upregulates expression of the chemokine receptor, Blr-1. J. Exp. Med. 188:297-304.
44. Brocker, T., A. Gulbranson-Judge, S. Flynn, M. Riedinger, C. Raykundalia, and P. Lane. 1999. CD4 T cell traffic control: in vivo evidence that ligation of OX40 on CD4 T cells by OX40-ligand expressed on dendritic cells leads to the accumulation of CD4 T cells in B cell follicles. Eur. J. Immunol. 29:1610-1616.
45. Nakano, H., T. Tamura, T. Yoshimoto, H. Yagita, M. Miyasaka, E.C. Butcher, H. Nariuchi, T. Kakiuchi, and A. Matsuzawa. 1997. Genetic defect in T lymphocyte-specific homing into peripheral lymph nodes. Eur. J. Immunol. 27:215-221.
46. Campbell, J.J., J. Hedrick, A. Zlotnik, M.A. Siani, D.A. Thompson, and E.C. Butcher. 1998. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science. 279:381-384.
47. Zipfel, P.F., J. Balke, S.G. Irving, K. Kelly, and U. Siebenlist. 1989. Mitogenic activation of human T cells induces two closely related genes which share structural similarities with a new family of secreted factors. J. Immunol. 142:1582-1590.
48. Krzysiek, R., E.A. Lefevre, W. Zou, A. Foussat, J. Bernard, A. Portier, P. Galanaud, and Y. Richard. 1999. Antigen receptor engagement selectively induces macrophage inflammatory protein-1α (MIP-1α) and MIP-1β chemokine production in human B cells. J. Immunol. 162:4455-4463.
49. Schaniel, C., E. Pardali, F. Sallusto, M. Speletas, C. Ruedl, T. Shimizu, T. Seidl, J. Andersson, F. Melchers, A.G. Rolink, and P. Sideras. 1998. Activated murine B lymphocytes and dendritic cells produce a novel CC chemokine which acts selectively on activated T cells. J. Exp. Med. 188: 451-463.
50. Loetscher, P., M. Seitz, M. Baggiolini, and B. Moser. 1996. Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J. Exp. Med. 184:569-577.
51. Sallusto, F., D. Lenig, C.R. Mackay, and A. Lanzavecchia. 1998. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J. Exp. Med. 187:875-883.
52. Bonecchi, R., G. Bianchi, P.P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P.A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187:129-134.
53. Tang, H.L., and J.G. Cyster. 1999. Chemokine upregulation and activated T cell attraction by maturing dendritic cells. Science. 284:819-822.
54. Steinberg, M.S. 1963. Reconstitution of tissues by dissociated cells. Science. 141:401-408.
55. Nose, A., A. Nagafuchi, and M. Takeichi. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell. 54:993-1001.
56. Xu, Q., G. Mellitzer, V. Robinson, and D.G. Wilkinson. 1999. In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature. 399: 267-271.
57. Neumann, B., A. Luz, K. Pfeffer, and B. Holzmann. 1996. Defective Peyer's patch organogenesis in mice lacking the 55-kD receptor for tumor necrosis factor. J. Exp. Med. 184: 259-264.
58. Pasparakis, M., L. Alexopoulou, V. Episkopou, and G. Kollias. 1996. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J. Exp. Med. 184:1397-1411.
59. Korner, H., M. Cook, D.S. Riminton, F.A. Lemckert, R.M. Hoek, B. Ledermann, F. Kontgen, B. Fazekas de St. Groth, and J.D. Sedgwick. 1997. Distinct roles for lymphotoxin-alpha and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur. J. Immunol. 27:2600-2609.
60. Fu, Y.X., G. Huang, M. Matsumoto, H. Molina, and D.D. Chaplin. 1997. Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc. Natl. Acad. Sci. USA. 94:5739-5743.
61. Forster, R., G. Schweigard, S. Johann, T. Emrich, E. Kremmer, C. Nerl, and M. Lipp. 1997. Abnormal expression of the B-cell homing chemokine receptor BLR1 during the progression of acquired immunodeficiency syndrome. Blood. 90:520-525.
62. Homann, D., A. Tishon, D.P. Berger, W.O. Weigle, M.G. von Herrath, and M.B.A. Oldstone. 1998. Evidence for an underlying CD4 helper and CD8 T-cell defect in B-cell deficient mice: failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from μMT/μMT mice. J. Virol. 72:9208-9216.
63. Westermann, J., U. Geismar, A. Sponholz, U. Bode, S.M. Sparshott, and E.B. Bell. 1997. CD4+ T cells of both the naive and the memory phenotype enter rat lymph nodes and Peyer's patches via high endothelial venules: within the tissue their migratory behavior differs. Eur. J. Immunol. 27:3174-3181.