Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5

Nature Immunology

Volumn 5, Issue 9, 2004, Pages 943-952

  Allen, Christopher D C ^a   Ansel, K Mark ^a,c   Low, Caroline ^a   Lesley, Robin ^a   Tamamura, Hirokazu ^b   Fujii, Nobutaka ^b   Cyster, Jason G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; LIGAND; STROMAL CELL DERIVED FACTOR 1; ALPHA CHEMOKINE; BLR1 PROTEIN, MOUSE; CHEMOKINE RECEPTOR; CXCL13 PROTEIN, MOUSE; CYTOKINE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BLAST CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENETIC SELECTION; GERMINAL CENTER; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOMATIC HYPERMUTATION; WILD TYPE; ANIMAL; ANTIGEN PRESENTATION; CYTOLOGY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MICRODISSECTION; NEUTROPHIL CHEMOTAXIS; RADIATION CHIMERA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; ANTIGEN PRESENTATION; B-LYMPHOCYTES; CHEMOKINES, CXC; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; GERMINAL CENTER; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; MICRODISSECTION; RADIATION CHIMERA; RATS; RECEPTORS, CHEMOKINE; RECEPTORS, CXCR4; RECEPTORS, CYTOKINE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 4644219817     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni1100     Document Type: Article

References (48)

1. Röhlich, K. Beitrag zur Cytologie der Keimzentren der Lymphknoten. Z. Mikrosk. Anat. Forsch. 20, 287-297 (1930).
2. MacLennan, I.C. Germinal centers. Annu. Rev. Immunol. 12, 117-139 (1994).
3. Kelsoe, G. Life and death in germinal centers (redux). Immunity 4, 107-111 (1996).
4. McHeyzer-Williams, M.G. & Ahmed, R. B cell memory and the long-lived plasma cell. Curr. Opin. Immunol. 11, 172-179 (1999).
5. Berek, C., Berger, A. & Apel, M. Maturation of the immune response in germinal centers. Cell 67, 1121-1129 (1991).
6. Liu, Y.J., Zhang, J., Lane, P.J., Chan, E.Y. & MacLennan, I.C. Sites of specific B cell activation in primary and secondary responses to T cell-dependent and T cell-independent antigens. Eur. J. Immunol. 21, 2951-2962 (1991).
7. Koburg, E. in Germinal Centers in Immune Responses. (eds. Cottier, H., Odartchenko, N, Schindler, R. & Congdon, C.C.) 177-182 (Springer-Verlag, New York, University of Bern, Switzerland; 1966).
8. Koopman, G. et al. Adhesion of human B cells to follicular dendritic cells involves both the lymphocyte function-associated antigen 1/intercellular adhesion molecule 1 and very late antigen 4/vascular cell adhesion molecule 1 pathways. J. Exp. Med. 173, 1297-1304 (1991).
9. Freedman, A.S. et al. Adhesion of human B cells to germinal centers in vitro involves VLA-4 and INCAM-110. Science 249, 1030-1033 (1990).
10. Voigt, I. et al. CXCR5-deficient mice develop functional germinal centers in the splenic T cell zone. Eur. J. Immunol. 30, 560-567 (2000).
11. Ansel, K.M. et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406, 309-314 (2000).
12. Forster, R. et al. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen, Cell 87, 1037-1047 (1996).
13. Roy, M.P., Kim, C.H, & Butcher, E.C. Cytokine control of memory B cell homing machinery. J. Immunol. 169, 1676-1682 (2002).
14. Bowman, E.P. et al. Developmental switches in chemokine response profiles during B cell differentiation and maturation. J. Exp. Med. 191, 1303-1318 (2000).
15. Bleul, C.C., Schultze, J.L. & Springer, T.A. B lymphocyte chemotaxis regulated in association with microanatomic localization, differentiation state, and B cell receptor engagement. J. Exp. Med. 187, 753-762 (1998).
16. Forster, R. et al. Intracellular and surface expression of the HIV-1 coreceptor CXCR4/fusin on various leukocyte subsets: rapid internalization and recycling upon activation. J. Immunol. 160, 1522-1531 (1998).
17. Casamayor-Palleja, M., Mondiere, P., Verschelde, C., Bella, C. & Defrance, T. BCR ligation reprograms B cells for migration to the T zone and B-cell follicle sequentially. Blood 99, 1913-1921 (2002).
18. Estes, J.D. et al. Follicular dendritic cell-mediated up-regulation of CXCR4 expression on CD4 T cells and HIV pathogenesis. J. Immunol. 169, 2313-2322 (2002).
19. Corcione, A. et al. Stromal cell-derived factor-1 as a chemoattractant for follicular center lymphoma B cells. J. Natl. Cancer Inst. 92, 628-635 (2000).
20. Shinall, S.M., Gonzalez-Fernandez, M., Noelle, R.J. & Waldschmidt, T.J. Identification of murine germinal center B cell subsets defined by the expression of surface isotypes and differentiation antigens. J. Immunol. 164, 5729-5738 (2000).
21. Maeda, K. et al. Murine follicular dendritic cells and low affinity Fc receptors for IgE (FcERII). J. Immunol. 148, 2340-2347 (1992).
22. Cyster, J.G. et al. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 176, 181-193 (2000).
23. + cells limit germinal centre formation? Immunology 69, 487-489 (1990).
24. Tamamura, H. et al. Enhancement of the T140-based pharmacophores leads to the development of more potent and bio-stable CXCR4 antagonists. Org. Biomol. Chem. 1, 3663-3669 (2003).
25. Strasser, A. et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl. Acad. Sci. USA 88, 8661-8665 (1991).
26. Second, E.A., Edington, J.M. & Thorbecke, G.J. The Eμ-bcl-2 transgene enhances antigen-induced germinal center formation in both BALB/c and SJL mice but causes age-dependent germinal center hyperplasia only in the lymphoma-prone SJL strain, Am. J. Pathol. 147, 422-433 (1995).
27. Smith, K.G. et al. Bcl-2 transgene expression inhibits apoptosis in the germinal center and reveals differences in the selection of memory B cells and bone marrow antibody-forming cells. J. Exp. Med. 191, 475-484 (2000).
28. Hargreaves, D.C. et al. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194, 45-56 (2001).
29. Okada, T. et al. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 196, 65-75 (2002).
30. Krug, A. et al. IFN-producing cells respond to CXCR3 ligands in the presence of CXCL12 and secrete inflammatory chemokines upon activation. J. Immunol. 169, 6079-6083 (2002).
31. Casamayor-Palleja, M. et al. Expression of macrophage inflammatory protein-3alpha, stromal cell-derived factor-1, and B-cell-attracting chemokine-1 identifies the tonsil crypt as an attractive site for B cells. Blood 97, 3992-3994 (2001).
32. Amara, A. et al. Stromal cell-derived factor-1alpha associates with heparan sulfates through the first β-strand of the chemokine. J. Biol. Chem. 274, 23916-23925 (1999).
33. Nieuwenhuis, P. & Opstelten, D. Functional anatomy of germinal centers. Am. J. Anat. 170, 421-435 (1984).
34. Wehrli, N. et al. Changing responsiveness to chemokines allows medullary plasma-blasts to leave lymph nodes. Eur. J. Immunol. 31, 609-616 (2001).
35. Guinamard, R. et al. B cell antigen receptor engagement inhibits stromal cell-derived factor (SDF)-1α chemotaxis and promotes protein kinase C (PKC)-induced internalization of CXCR4. J. Exp. Med. 189, 1461-1466 (1999).
36. Marchese, A. & Benovic, J.L. Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. J. Biol. Chem. 276, 45509-45512 (2001).
37. Balogh, P., Aydar, Y., Tew, J.G. & Szakal, A.K. Appearance and phenotype of murine follicular dendritic cells expressing VCAM-1. Anat. Rec. 268, 160-168 (2002).
38. Egawa, T. et al. The earliest stages of B cell development require a chemokine stromal cell-derived factor/pre-B cell growth-stimulating factor. Immunity 15, 323-334 (2001).
39. Ma, Q. et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. USA 95, 9448-9453 (1998).
40. Zou, Y.R., Kottmann, A.H., Kuroda, M., Taniuchi, I. & Littman, D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599 (1998).
41. Ara, T. et al. A role of CXC chemokine ligand 12/stromal cell-derived factor-1/pre-B cell growth stimulating factor and its receptor CXCR4 in fetal and adult T cell development in vivo. J. Immunol. 170, 4649-4655 (2003).
42. Plotkin, J., Prockop, S.E., Lepique, A. & Petrie, H.T. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. J. Immunol. 171, 4521-4527 (2003).
43. Martin, C. et al. Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583-593 (2003).
44. Bleul, C.C., Fuhlbrigge, R.C., Casasnovas, J.M., Aiuti, A. & Springer, T.A. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J. Exp. Med. 184, 1101-1109 (1996).
45. Hernandez, P.A. et al. Mutations in the chemokine receptor gene CXCR4 are associated with WHIM syndrome, a combined immunodeficiency disease. Nat. Genet. 34, 70-74 (2003).
46. Luther, S.A., Gulbranson-Judge, A., Acha-Orbea, H. & MacLennan, I.C. Viral super-antigen drives extrafollicular and follicular B cell differentiation leading to virus-specific antibody production. J. Exp. Med. 185, 551-562 (1997).
47. Ngo, V.N., Tang, H.L. & Cyster, J.G. 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 (1998).
48. Cinamon, G. et al. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5, 713-720 (2004).