CXCR4 promotes B cell egress from peyer's patches

Journal of Experimental Medicine

Volumn 210, Issue 6, 2013, Pages 1099-1107

  Schmidt, Timothy H ^a   Bannard, Oliver ^a   Gray, Elizabeth E ^a   Cyster, Jason G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; KIKGR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL ADHESION; CELL AGGREGATION; CELLULAR DISTRIBUTION; CHIMERA; CONTROLLED STUDY; ENDOTHELIUM CELL; HALF LIFE TIME; INTESTINE LYMPHATIC TISSUE; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WILD TYPE;

ANIMALS; B-LYMPHOCYTES; CHEMOKINE CXCL12; CHEMOKINE CXCL13; ENDOTHELIAL CELLS; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; PEYER'S PATCHES; RECEPTORS, CXCR4; RECEPTORS, CXCR5;

EID: 84880669087     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20122574     Document Type: Article

References (43)

1. Allen, C.D.C., K.M. Ansel, C. Low, R. Lesley, H. Tamamura, N. Fujii, and J.G. Cyster. 2004. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5:943-952. http://dx.doi.org/10.1038/ni1100
2. Ara, T., K. Tokoyoda, T. Sugiyama, T. Egawa, K. Kawabata, and T. Nagasawa. 2003. Long-term hematopoietic stem cells require stromal cell-derived factor-1 for colonizing bone marrow during ontogeny. Immunity. 19: 257-267. http://dx.doi.org/10.1016/S1074-7613(03)00201-2
3. Azzali, G. 2003. Structure, lymphatic vascularization and lymphocyte migration in mucosa-associated lymphoid tissue. Immunol. Rev. 195:178-189. http://dx.doi.org/10.1034/j.1600-065X.2003.00072.x
4. Azzali, G., and M.L. Arcari. 2000. Ultrastructural and three dimensional aspects of the lymphatic vessels of the absorbing peripheral lymphatic apparatus in Peyer's patches of the rabbit. Anat. Rec. 258:71-79. http://dx.doi.org/10.1002/(SICI)1097-0185(20000101)258:1<71::AID-AR8>3.0.CO;2-N
5. Bargatze, R.F., M.A. Jutila, and E.C. Butcher. 1995. Distinct roles of L-selectin and integrins alpha 4 beta 7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: the multistep model confirmed and refined. Immunity. 3:99-108. http://dx.doi.org/10.1016/1074-7613(95)90162-0
6. Berlin, C., E.L. Berg, M.J. Briskin, D.P. Andrew, P.J. Kilshaw, B. Holzmann, I.L. Weissman, A. Hamann, and E.C. Butcher. 1993. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell. 74:185-195. http://dx.doi.org/10.1016/0092-8674(93)90305-A
7. Bleul, C.C., R.C. Fuhlbrigge, J.M. Casasnovas, A. Aiuti, and T.A. Springer. 1996. A highly efficacious lymphocyte chemoattractant, stromal cell- derived factor 1 (SDF-1). J. Exp. Med. 184:1101-1109. http://dx.doi.org/10.1084/jem.184.3.1101
8. Braun, A., T. Worbs, G.L. Moschovakis, S. Halle, K. Hoffmann, J. Bölter, A. Münk, and R. Förster. 2011. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat. Immunol. 12: 879-887. http://dx.doi.org/10.1038/ni.2085
9. Cornes, J.S. 1965. Number, size, and distribution of Peyer's patches in the human small intestine: Part I The development of Peyer's patches. Gut. 6:225-229. http://dx.doi.org/10.1136/gut.6.3.225
10. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663. http://dx.doi.org/10.1146/annurev-immunol-031210-101400
11. Förster, 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. http://dx.doi.org/10.1016/S0092-8674(00)81798-5
12. Gohda, M., J. Kunisawa, F. Miura, Y. Kagiyama, Y. Kurashima, M. Higuchi, I. Ishikawa, I. Ogahara, and H. Kiyono. 2008. Sphingosine 1-phosphate regulates the egress of IgA plasmablasts from Peyer's patches for intestinal IgA responses. J. Immunol. 180:5335-5343.
13. Green, J.A., K. Suzuki, B. Cho, L.D. Willison, D. Palmer, C.D.C. Allen, T.H. Schmidt, Y. Xu, R.L. Proia, S.R. Coughlin, and J.G. Cyster. 2011. The sphingosine 1-phosphate receptor S1P2 maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat. Immunol. 12:672-680. http://dx.doi.org/10.1038/ni.2047
14. Grigorova, I.L., S.R. Schwab, T.G. Phan, T.H.M. Pham, T. Okada, and J.G. Cyster. 2009. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat. Immunol. 10:58-65. http://dx.doi.org/10.1038/ni.1682
15. Grigorova, I.L., M. Panteleev, and J.G. Cyster. 2010. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. USA. 107:20447-20452. http://dx.doi.org/10.1073/pnas.1009968107
16. Hargreaves, D.C., P.L. Hyman, T.T. Lu, V.N. Ngo, A. Bidgol, G. Suzuki, Y.-R. Zou, D.R. Littman, and J.G. Cyster. 2001. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194:45-56. http://dx.doi.org/10.1084/jem.194.1.45
17. Hobeika, E., S. Thiemann, B. Storch, H. Jumaa, P.J. Nielsen, R. Pelanda, and M. Reth. 2006. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA. 103:13789-13794. http://dx.doi.org/10.1073/pnas.0605944103
18. Lo, C.G., T.T. Lu, and J.G. Cyster. 2003. Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 197:353-361. http://dx.doi.org/10.1084/jem.20021569
19. Macpherson, A.J., M.B. Geuking, and K.D. McCoy. 2005. Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria. Immunology. 115:153-162. http://dx.doi.org/10.1111/j.1365-2567.2005.02159.x
20. Matloubian, M., C.G. Lo, G. Cinamon, M.J. Lesneski, Y. Xu, V. Brinkmann, M.L. Allende, R.L. Proia, and J.G. Cyster. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 427:355-360. http://dx.doi.org/10.1038/nature02284
21. Miura, S., Y. Tsuzuki, D. Fukumura, H. Serizawa, M. Suematsu, I. Kurose, H. Imaeda, H. Kimura, H. Nagata, M. Tsuchiya, et al. 1995. Intravital demonstration of sequential migration process of lymphocyte subpopulations in rat Peyer's patches. Gastroenterology. 109:1113-1123. http://dx.doi.org/10.1016/0016-5085(95)90569-3
22. Nagasawa, T., S. Hirota, K. Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, and T. Kishimoto. 1996. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 382:635-638. http://dx.doi.org/10.1038/382635a0
23. Nakagawa, R., A. Togawa, T. Nagasawa, and S.-I. Nishikawa. 2013. Peyer's patch inducer cells play a leading role in the formation of B and T cell zone architecture. J. Immunol. 190:3309-3318. http://dx.doi.org/10.4049/jimmunol.1202766
24. Nie, Y., J. Waite, F. Brewer, M.-J. Sunshine, D.R. Littman, and Y.-R. Zou. 2004. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200:1145-1156. http://dx.doi.org/10.1084/jem.20041185
25. Nowotschin, S., and A.-K. Hadjantonakis. 2009. Use of KikGR a photoconvertible green-to-red fluorescent protein for cell labeling and lineage analysis in ES cells and mouse embryos. BMC Dev. Biol. 9:49. http://dx.doi.org/10.1186/1471-213X-9-49
26. Ohtani, O., and T. Murakami. 1990. Organization of the lymphatic vessels and their relationships to blood vessels in rabbit Peyer's patches. Arch. Histol. Cytol. 53:155-164. http://dx.doi.org/10.1679/aohc.53.Suppl_155
27. Okada, T., V.N. Ngo, E.H. Ekland, R. Förster, M. Lipp, D.R. Littman, and J.G. Cyster. 2002. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 196:65-75. http://dx.doi.org/10.1084/jem.20020201
28. Park, C., I.-Y. Hwang, R.K. Sinha, O. Kamenyeva, M.D. Davis, and J.H. Kehrl. 2012. Lymph node B lymphocyte trafficking is constrained by anatomy and highly dependent upon chemoattractant desensitization. Blood. 119:978-989. http://dx.doi.org/10.1182/blood-2011-06-364273
29. Pereira, J.P., J. An, Y. Xu, Y. Huang, and J.G. Cyster. 2009. Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat. Immunol. 10:403-411. http://dx.doi.org/10.1038/ni.1710
30. Pham, T.H.M., T. Okada, M. Matloubian, C.G. Lo, and J.G. Cyster. 2008. S1P1 receptor signaling overrides retention mediated by G α i-coupled receptors to promote T cell egress. Immunity. 28:122-133. http://dx.doi.org/10.1016/j.immuni.2007.11.017
31. Pham, T.H.M., P. Baluk, Y. Xu, I. Grigorova, A.J. Bankovich, R. Pappu, S.R. Coughlin, D.M. McDonald, S.R. Schwab, and J.G. Cyster. 2010. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207:17-27. http://dx.doi.org/10.1084/jem.20091619
32. Rasheed, A.-U., H.-P. Rahn, F. Sallusto, M. Lipp, and G. Müller. 2006. Follicular B helper T cell activity is confined to CXCR5(hi)ICOS(hi) CD4 T cells and is independent of CD57 expression. Eur. J. Immunol. 36:1892-1903. http://dx.doi.org/10.1002/eji.200636136
33. Shiow, L.R., D.B. Rosen, N. Brdicková, Y. Xu, J. An, L.L. Lanier, J.G. Cyster, and M. Matloubian. 2006. CD69 acts downstream of interferon- α/β to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature. 440:540-544. http://dx.doi.org/10.1038/nature04606
34. Sinha, R.K., C. Park, I.-Y. Hwang, M.D. Davis, and J.H. Kehrl. 2009. B lymphocytes exit lymph nodes through cortical lymphatic sinusoids by a mechanism independent of sphingosine-1-phosphate-mediated chemotaxis. Immunity. 30:434-446. http://dx.doi.org/10.1016/j.immuni.2008.12.018
35. Sobhon, P. 1971. The light and the electron microscopic studies of Peyer's patches in non germ-free adult mice. J. Morphol. 135:457-481. http://dx.doi.org/10.1002/jmor.1051350404
36. Sugiyama, T., H. Kohara, M. Noda, and T. Nagasawa. 2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 25:977-988. http://dx.doi.org/10.1016/j.immuni.2006.10.016
37. Tomura, M., N. Yoshida, J. Tanaka, S. Karasawa, Y. Miwa, A. Miyawaki, and O. Kanagawa. 2008. Monitoring cellular movement in vivo with photoconvertible fluorescence protein "Kaede" transgenic mice. Proc. Natl. Acad. Sci. USA. 105:10871-10876. http://dx.doi.org/10.1073/pnas.0802278105
38. Tomura, M., T. Honda, H. Tanizaki, A. Otsuka, G. Egawa, Y. Tokura, H. Waldmann, S. Hori, J.G. Cyster, T. Watanabe, et al. 2010. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J. Clin. Invest. 120:883-893. http://dx.doi.org/10.1172/JCI40926
39. Tsutsui, H., S. Karasawa, H. Shimizu, N. Nukina, and A. Miyawaki. 2005. Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep. 6:233-238. http://dx.doi.org/10.1038/sj.embor.7400361
40. von Andrian, U.H., and T.R. Mempel. 2003. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3:867-878. http://dx.doi.org/10.1038/nri1222
41. Warnock, R.A., J.J. Campbell, M.E. Dorf, A. Matsuzawa, L.M. McEvoy, and E.C. Butcher. 2000. The role of chemokines in the microenvironmental control of T versus B cell arrest in Peyer's patch high endothelial venules. J. Exp. Med. 191:77-88. http://dx.doi.org/10.1084/jem.191.1.77
42. Wei, S.H., H. Rosen, M.P. Matheu, M.G. Sanna, S.-K. Wang, E. Jo, C.-H. Wong, I. Parker, and M.D. Cahalan. 2005. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6:1228-1235. http://dx.doi.org/10.1038/ni1269
43. Zou, Y.R., A.H. Kottmann, M. Kuroda, I. Taniuchi, and D.R. Littman. 1998. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature. 393:595-599. http://dx.doi.org/10.1038/31269