1932

Abstract

The continuous migration of immune cells between lymphoid and nonlymphoid organs is a key feature of the immune system, facilitating the distribution of effector cells within nearly all compartments of the body. Furthermore, reaching their correct position within primary, secondary, or tertiary lymphoid organs is a prerequisite to ensure immune cells’ unimpaired differentiation, maturation, and selection, as well as their activation or functional silencing. The superfamilies of chemokines and chemokine receptors are of major importance in guiding immune cells to and within lymphoid and nonlymphoid tissues. In this review we focus on the role of the chemokine system in the migration dynamics of immune cells within lymphoid organs at the steady state and on how these dynamics are affected by infectious and inflammatory processes.

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2016-05-20
2024-06-19
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Literature Cited

  1. van de Pavert SA, Mebius RE. 1.  2010. New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10:664–74 [Google Scholar]
  2. Kufareva I, Salanga CL, Handel TM. 2.  2015. Chemokine and chemokine receptor structure and interactions: implications for therapeutic strategies. Immunol. Cell Biol. 93:372–83 [Google Scholar]
  3. Zlotnik A, Yoshie O. 3.  2012. The chemokine superfamily revisited. Immunity 36:705–16 [Google Scholar]
  4. Flad HD, Brandt E. 4.  2010. Platelet-derived chemokines: pathophysiology and therapeutic aspects. Cell Mol. Life Sci. 67:2363–86 [Google Scholar]
  5. Nomiyama H, Osada N, Yoshie O. 5.  2010. The evolution of mammalian chemokine genes. Cytokine Growth Factor Rev. 21:253–62 [Google Scholar]
  6. Bachelerie F, Ben-Baruch A, Burkhardt AM, Combadiere C, Farber JM. 6.  et al. 2014. International Union of Pharmacology. LXXXIX. Update on the extended family of chemokine receptors and introducing a new nomenclature for atypical chemokine receptors. Pharmacol. Rev. 66:1–79 [Google Scholar]
  7. Lefkowitz RJ, Shenoy SK. 7.  2005. Transduction of receptor signals by β-arrestins. Science 308:512–17 [Google Scholar]
  8. Nibbs RJ, Graham GJ. 8.  2013. Immune regulation by atypical chemokine receptors. Nat. Rev. Immunol. 13:815–29 [Google Scholar]
  9. Bachelerie F, Graham GJ, Locati M, Mantovani A, Murphy PM. 9.  et al. 2014. New nomenclature for atypical chemokine receptors. Nat. Immunol. 15:207–8 [Google Scholar]
  10. Girard JP, Moussion C, Forster R. 10.  2012. HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat. Rev. Immunol. 12:762–73 [Google Scholar]
  11. Schumann K, Lammermann T, Bruckner M, Legler DF, Polleux J. 11.  et al. 2010. Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 32:703–13 [Google Scholar]
  12. Klein L, Kyewski B, Allen PM, Hogquist KA. 12.  2014. Positive and negative selection of the T cell repertoire: what thymocytes see (and don't see). Nat. Rev. Immunol. 14:377–91 [Google Scholar]
  13. Blackburn CC, Manley NR. 13.  2004. Developing a new paradigm for thymus organogenesis. Nat. Rev. Immunol. 4:278–89 [Google Scholar]
  14. Douagi I, Vieira P, Cumano A. 14.  2002. Lymphocyte commitment during embryonic development, in the mouse. Semin. Immunol. 14:361–69 [Google Scholar]
  15. Gunn MD, Kyuwa S, Tam C, Kakiuchi T, Matsuzawa A. 15.  et al. 1999. Mice lacking expression of secondary lymphoid organ chemokine have defects in lymphocyte homing and dendritic cell localization. J. Exp. Med. 189:451–60 [Google Scholar]
  16. Liu C, Ueno T, Kuse S, Saito F, Nitta T. 16.  et al. 2005. The role of CCL21 in recruitment of T-precursor cells to fetal thymi. Blood 105:31–39 [Google Scholar]
  17. Bleul CC, Boehm T. 17.  2000. Chemokines define distinct microenvironments in the developing thymus. Eur. J. Immunol. 30:3371–79 [Google Scholar]
  18. Liu C, Saito F, Liu Z, Lei Y, Uehara S. 18.  et al. 2006. Coordination between CCR7- and CCR9-mediated chemokine signals in prevascular fetal thymus colonization. Blood 108:2531–39 [Google Scholar]
  19. Janas ML, Varano G, Gudmundsson K, Noda M, Nagasawa T, Turner M. 19.  2010. Thymic development beyond β-selection requires phosphatidylinositol 3-kinase activation by CXCR4. J. Exp. Med. 207:247–61 [Google Scholar]
  20. Plotkin J, Prockop SE, Lepique A, Petrie HT. 20.  2003. Critical role for CXCR4 signaling in progenitor localization and T cell differentiation in the postnatal thymus. J. Immunol. 171:4521–27 [Google Scholar]
  21. Calderon L, Boehm T. 21.  2011. Three chemokine receptors cooperatively regulate homing of hematopoietic progenitors to the embryonic mouse thymus. PNAS 108:7517–22 [Google Scholar]
  22. Jenkinson WE, Rossi SW, Parnell SM, Agace WW, Takahama Y. 22.  et al. 2007. Chemokine receptor expression defines heterogeneity in the earliest thymic migrants. Eur. J. Immunol. 37:2090–96 [Google Scholar]
  23. Schwarz BA, Sambandam A, Maillard I, Harman BC, Love PE, Bhandoola A. 23.  2007. Selective thymus settling regulated by cytokine and chemokine receptors. J. Immunol. 178:2008–17 [Google Scholar]
  24. Svensson M, Marsal J, Uronen-Hansson H, Cheng M, Jenkinson W. 24.  et al. 2008. Involvement of CCR9 at multiple stages of adult T lymphopoiesis. J. Leukoc. Biol. 83:156–64 [Google Scholar]
  25. Krueger A, Willenzon S, Lyszkiewicz M, Kremmer E, Forster R. 25.  2010. CC chemokine receptor 7 and 9 double-deficient hematopoietic progenitors are severely impaired in seeding the adult thymus. Blood 115:1906–12 [Google Scholar]
  26. Trampont PC, Tosello-Trampont AC, Shen Y, Duley AK, Sutherland AE. 26.  et al. 2010. CXCR4 acts as a costimulator during thymic β-selection. Nat. Immunol. 11:162–70 [Google Scholar]
  27. Zlotoff DA, Sambandam A, Logan TD, Bell JJ, Schwarz BA, Bhandoola A. 27.  2010. CCR7 and CCR9 together recruit hematopoietic progenitors to the adult thymus. Blood 115:1897–905 [Google Scholar]
  28. Lind EF, Prockop SE, Porritt HE, Petrie HT. 28.  2001. Mapping precursor movement through the postnatal thymus reveals specific microenvironments supporting defined stages of early lymphoid development. J. Exp. Med. 194:127–34 [Google Scholar]
  29. Misslitz A, Bernhardt G, Forster R. 29.  2006. Trafficking on serpentines: molecular insight on how maturating T cells find their winding paths in the thymus. Immunol. Rev. 209:115–28 [Google Scholar]
  30. Misslitz A, Pabst O, Hintzen G, Ohl L, Kremmer E. 30.  et al. 2004. Thymic T cell development and progenitor localization depend on CCR7. J. Exp. Med. 200:481–91 [Google Scholar]
  31. Benz C, Heinzel K, Bleul CC. 31.  2004. Homing of immature thymocytes to the subcapsular microenvironment within the thymus is not an absolute requirement for T cell development. Eur. J. Immunol. 34:3652–63 [Google Scholar]
  32. Ueno T, Saito F, Gray DH, Kuse S, Hieshima K. 32.  et al. 2004. CCR7 signals are essential for cortex-medulla migration of developing thymocytes. J. Exp. Med. 200:493–505 [Google Scholar]
  33. Davalos-Misslitz AC, Rieckenberg J, Willenzon S, Worbs T, Kremmer E. 33.  et al. 2007. Generalized multi-organ autoimmunity in CCR7-deficient mice. Eur. J. Immunol. 37:613–22 [Google Scholar]
  34. Kurobe H, Liu C, Ueno T, Saito F, Ohigashi I. 34.  et al. 2006. CCR7-dependent cortex-to-medulla migration of positively selected thymocytes is essential for establishing central tolerance. Immunity 24:165–77 [Google Scholar]
  35. Ehrlich LI, Oh DY, Weissman IL, Lewis RS. 35.  2009. Differential contribution of chemotaxis and substrate restriction to segregation of immature and mature thymocytes. Immunity 31:986–98 [Google Scholar]
  36. Davalos-Misslitz AC, Worbs T, Willenzon S, Bernhardt G, Forster R. 36.  2007. Impaired responsiveness to T-cell receptor stimulation and defective negative selection of thymocytes in CCR7-deficient mice. Blood 110:4351–59 [Google Scholar]
  37. Hu Z, Lancaster JN, Sasiponganan C, Ehrlich LI. 37.  2015. CCR4 promotes medullary entry and thymocyte-dendritic cell interactions required for central tolerance. J. Exp. Med. 212:1947–65 [Google Scholar]
  38. Lucas B, White AJ, Ulvmar MH, Nibbs RJ, Sitnik KM. 38.  et al. 2015. CCRL1/ACKR4 is expressed in key thymic microenvironments but is dispensable for T lymphopoiesis at steady state in adult mice. Eur. J. Immunol. 45:574–83 [Google Scholar]
  39. Heinzel K, Benz C, Bleul CC. 39.  2007. A silent chemokine receptor regulates steady-state leukocyte homing in vivo. PNAS 104:8421–26 [Google Scholar]
  40. Bunting MD, Comerford I, Seach N, Hammett MV, Asquith DL. 40.  et al. 2013. CCX-CKR deficiency alters thymic stroma impairing thymocyte development and promoting autoimmunity. Blood 121:118–28 [Google Scholar]
  41. Reinhardt A, Ravens S, Fleige H, Haas JD, Oberdorfer L. 41.  et al. 2014. CCR7-mediated migration in the thymus controls γΔ T-cell development. Eur. J. Immunol. 44:1320–29 [Google Scholar]
  42. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD. 42.  et al. 2010. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466:829–34 [Google Scholar]
  43. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC. 43.  1997. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185:111–20 [Google Scholar]
  44. Sugiyama T, Kohara H, Noda M, Nagasawa T. 44.  2006. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25:977–88 [Google Scholar]
  45. Christopher MJ, Rao M, Liu F, Woloszynek JR, Link DC. 45.  2011. Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J. Exp. Med. 208:251–60 [Google Scholar]
  46. DiPersio JF, Stadtmauer EA, Nademanee A, Micallef IN, Stiff PJ. 46.  et al. 2009. Plerixafor and G-CSF versus placebo and G-CSF to mobilize hematopoietic stem cells for autologous stem cell transplantation in patients with multiple myeloma. Blood 113:5720–26 [Google Scholar]
  47. Griffith JW, Sokol CL, Luster AD. 47.  2014. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32:659–702 [Google Scholar]
  48. Randall TD, Carragher DM, Rangel-Moreno J. 48.  2008. Development of secondary lymphoid organs. Annu. Rev. Immunol. 26:627–50 [Google Scholar]
  49. van de Pavert SA, Mebius RE. 49.  2014. Development of secondary lymphoid organs in relation to lymphatic vasculature. Adv. Anat. Embryol. Cell Biol. 214:81–91 [Google Scholar]
  50. Onder L, Danuser R, Scandella E, Firner S, Chai Q. 50.  et al. 2013. Endothelial cell–specific lymphotoxin-β receptor signaling is critical for lymph node and high endothelial venule formation. J. Exp. Med. 210:465–73 [Google Scholar]
  51. Forster R, Mattis AE, Kremmer E, Wolf E, Brem G, Lipp M. 51.  1996. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87:1037–47 [Google Scholar]
  52. Ansel KM, Ngo VN, Hyman PL, Luther SA, Forster R. 52.  et al. 2000. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406:309–14 [Google Scholar]
  53. Gunn MD, Ngo VN, Ansel KM, Ekland EH, Cyster JG, Williams LT. 53.  1998. A B-cell–homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 391:799–803 [Google Scholar]
  54. Victora GD, Nussenzweig MC. 54.  2012. Germinal centers. Annu. Rev. Immunol. 30:429–57 [Google Scholar]
  55. Forster R, Pabst O, Bernhardt G. 55.  2008. Homeostatic chemokines in development, plasticity, and functional organization of the intestinal immune system. Semin. Immunol. 20:171–80 [Google Scholar]
  56. Brown FD, Turley SJ. 56.  2015. Fibroblastic reticular cells: organization and regulation of the T lymphocyte life cycle. J. Immunol. 194:1389–94 [Google Scholar]
  57. Malhotra D, Fletcher AL, Astarita J, Lukacs-Kornek V, Tayalia P. 57.  et al. 2012. Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat. Immunol. 13:499–510 [Google Scholar]
  58. Tomei AA, Siegert S, Britschgi MR, Luther SA, Swartz MA. 58.  2009. Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J. Immunol. 183:4273–83 [Google Scholar]
  59. Wendland M, Willenzon S, Kocks J, Davalos-Misslitz AC, Hammerschmidt SI. 59.  et al. 2011. Lymph node T cell homeostasis relies on steady state homing of dendritic cells. Immunity 35:945–57 [Google Scholar]
  60. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. 60.  2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7:678–89 [Google Scholar]
  61. Nourshargh S, Hordijk PL, Sixt M. 61.  2010. Breaching multiple barriers: leukocyte motility through venular walls and the interstitium. Nat. Rev. Mol. Cell Biol. 11:366–78 [Google Scholar]
  62. von Andrian UH, Mempel TR. 62.  2003. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3:867–78 [Google Scholar]
  63. Miyasaka M, Tanaka T. 63.  2004. Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat. Rev. Immunol. 4:360–70 [Google Scholar]
  64. Warnock RA, Askari S, Butcher EC, von Andrian UH. 64.  1998. Molecular mechanisms of lymphocyte homing to peripheral lymph nodes. J. Exp. Med. 187:205–16 [Google Scholar]
  65. Campbell JJ, Bowman EP, Murphy K, Youngman KR, Siani MA. 65.  et al. 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. 141:1053–59 [Google Scholar]
  66. Gunn MD, Tangemann K, Tam C, Cyster JG, Rosen SD, Williams LT. 66.  1998. A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. PNAS 95:258–63 [Google Scholar]
  67. Stein JV, Rot A, Luo Y, Narasimhaswamy M, Nakano H. 67.  et al. 2000. The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function–associated antigen 1–mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J. Exp. Med. 191:61–76 [Google Scholar]
  68. Baekkevold ES, Yamanaka T, Palframan RT, Carlsen HS, Reinholt FP. 68.  et al. 2001. The CCR7 ligand ELC (CCL19) is transcytosed in high endothelial venules and mediates T cell recruitment. J. Exp. Med. 193:1105–12 [Google Scholar]
  69. Pachynski RK, Wu SW, Gunn MD, Erle DJ. 69.  1998. Secondary lymphoid-tissue chemokine (SLC) stimulates integrin α4β7–mediated adhesion of lymphocytes to mucosal addressin cell adhesion molecule-1 (MAdCAM-1) under flow. J. Immunol. 161:952–56 [Google Scholar]
  70. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I. 70.  et al. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23–33 [Google Scholar]
  71. Warnock RA, Campbell JJ, Dorf ME, Matsuzawa A, McEvoy LM, Butcher EC. 71.  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 [Google Scholar]
  72. Luther SA, Tang HL, Hyman PL, Farr AG, Cyster JG. 72.  2000. Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. PNAS 97:12694–99 [Google Scholar]
  73. Okada T, Ngo VN, Ekland EH, Forster R, Lipp M. 73.  et al. 2002. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 196:65–75 [Google Scholar]
  74. Bai Z, Hayasaka H, Kobayashi M, Li W, Guo Z. 74.  et al. 2009. CXC chemokine ligand 12 promotes CCR7-dependent naive T cell trafficking to lymph nodes and Peyer's patches. J. Immunol. 182:1287–95 [Google Scholar]
  75. Ebisuno Y, Tanaka T, Kanemitsu N, Kanda H, Yamaguchi K. 75.  et al. 2003. Cutting edge: The B cell chemokine CXC chemokine ligand 13/B lymphocyte chemoattractant is expressed in the high endothelial venules of lymph nodes and Peyer's patches and affects B cell trafficking across high endothelial venules. J. Immunol. 171:1642–46 [Google Scholar]
  76. Kanemitsu N, Ebisuno Y, Tanaka T, Otani K, Hayasaka H. 76.  et al. 2005. CXCL13 is an arrest chemokine for B cells in high endothelial venules. Blood 106:2613–18 [Google Scholar]
  77. Bromley SK, Mempel TR, Luster AD. 77.  2008. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat. Immunol. 9:970–80 [Google Scholar]
  78. Scimone ML, Felbinger TW, Mazo IB, Stein JV, von Andrian UH, Weninger W. 78.  2004. CXCL12 mediates CCR7-independent homing of central memory cells, but not naive T cells, in peripheral lymph nodes. J. Exp. Med. 199:1113–20 [Google Scholar]
  79. Phillips R, Ager A. 79.  2002. Activation of pertussis toxin–sensitive CXCL12 (SDF-1) receptors mediates transendothelial migration of T lymphocytes across lymph node high endothelial cells. Eur. J. Immunol. 32:837–47 [Google Scholar]
  80. Knowlden S, Georas SN. 80.  2014. The autotaxin-LPA axis emerges as a novel regulator of lymphocyte homing and inflammation. J. Immunol. 192:851–57 [Google Scholar]
  81. Bai Z, Cai L, Umemoto E, Takeda A, Tohya K. 81.  et al. 2013. Constitutive lymphocyte transmigration across the basal lamina of high endothelial venules is regulated by the autotaxin/lysophosphatidic acid axis. J. Immunol. 190:2036–48 [Google Scholar]
  82. Lee M, Kiefel H, LaJevic MD, Macauley MS, Kawashima H. 82.  et al. 2014. Transcriptional programs of lymphoid tissue capillary and high endothelium reveal control mechanisms for lymphocyte homing. Nat. Immunol. 15:982–95 [Google Scholar]
  83. Yang BG, Tanaka T, Jang MH, Bai Z, Hayasaka H, Miyasaka M. 83.  2007. Binding of lymphoid chemokines to collagen IV that accumulates in the basal lamina of high endothelial venules: its implications in lymphocyte trafficking. J. Immunol. 179:4376–82 [Google Scholar]
  84. Tsuboi K, Hirakawa J, Seki E, Imai Y, Yamaguchi Y. 84.  et al. 2013. Role of high endothelial venule–expressed heparan sulfate in chemokine presentation and lymphocyte homing. J. Immunol. 191:448–55 [Google Scholar]
  85. Nagakubo D, Murai T, Tanaka T, Usui T, Matsumoto M. 85.  et al. 2003. A high endothelial venule secretory protein, mac25/angiomodulin, interacts with multiple high endothelial venule–associated molecules including chemokines. J. Immunol. 171:553–61 [Google Scholar]
  86. Carlsen HS, Haraldsen G, Brandtzaeg P, Baekkevold ES. 86.  2005. Disparate lymphoid chemokine expression in mice and men: no evidence of CCL21 synthesis by human high endothelial venules. Blood 106:444–46 [Google Scholar]
  87. Shulman Z, Cohen SJ, Roediger B, Kalchenko V, Jain R. 87.  et al. 2012. Transendothelial migration of lymphocytes mediated by intraendothelial vesicle stores rather than by extracellular chemokine depots. Nat. Immunol. 13:67–76 [Google Scholar]
  88. Kashiwazaki M, Tanaka T, Kanda H, Ebisuno Y, Izawa D. 88.  et al. 2003. A high endothelial venule–expressing promiscuous chemokine receptor DARC can bind inflammatory, but not lymphoid, chemokines and is dispensable for lymphocyte homing under physiological conditions. Int. Immunol. 15:1219–27 [Google Scholar]
  89. Comerford I, Nibbs RJ, Litchfield W, Bunting M, Harata-Lee Y. 89.  et al. 2010. The atypical chemokine receptor CCX-CKR scavenges homeostatic chemokines in circulation and tissues and suppresses Th17 responses. Blood 116:4130–40 [Google Scholar]
  90. Gretz JE, Norbury CC, Anderson AO, Proudfoot AE, Shaw S. 90.  2000. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192:1425–40 [Google Scholar]
  91. Palframan RT, Jung S, Cheng G, Weninger W, Luo Y. 91.  et al. 2001. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 194:1361–73 [Google Scholar]
  92. Janatpour MJ, Hudak S, Sathe M, Sedgwick JD, McEvoy LM. 92.  2001. Tumor necrosis factor–dependent segmental control of MIG expression by high endothelial venules in inflamed lymph nodes regulates monocyte recruitment. J. Exp. Med. 194:1375–84 [Google Scholar]
  93. Gorlino CV, Ranocchia RP, Harman MF, Garcia IA, Crespo MI. 93.  et al. 2014. Neutrophils exhibit differential requirements for homing molecules in their lymphatic and blood trafficking into draining lymph nodes. J. Immunol. 193:1966–74 [Google Scholar]
  94. Brackett CM, Muhitch JB, Evans SS, Gollnick SO. 94.  2013. IL-17 promotes neutrophil entry into tumor-draining lymph nodes following induction of sterile inflammation. J. Immunol. 191:4348–57 [Google Scholar]
  95. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H. 95.  et al. 1999. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat. Med. 5:919–23 [Google Scholar]
  96. Seth S, Oberdorfer L, Hyde R, Hoff K, Thies V. 96.  et al. 2011. CCR7 essentially contributes to the homing of plasmacytoid dendritic cells to lymph nodes under steady-state as well as inflammatory conditions. J. Immunol. 186:3364–72 [Google Scholar]
  97. Matsutani T, Tanaka T, Tohya K, Otani K, Jang MH. 97.  et al. 2007. Plasmacytoid dendritic cells employ multiple cell adhesion molecules sequentially to interact with high endothelial venule cells—molecular basis of their trafficking to lymph nodes. Int. Immunol. 19:1031–37 [Google Scholar]
  98. Yoneyama H, Matsuno K, Zhang Y, Nishiwaki T, Kitabatake M. 98.  et al. 2004. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int. Immunol. 16:915–28 [Google Scholar]
  99. Mueller SN, Hosiawa-Meagher KA, Konieczny BT, Sullivan BM, Bachmann MF. 99.  et al. 2007. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 317:670–74 [Google Scholar]
  100. Auffray C, Sieweke MH, Geissmann F. 100.  2009. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 27:669–92 [Google Scholar]
  101. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K. 101.  et al. 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. 12:879–87 [Google Scholar]
  102. Ulvmar MH, Werth K, Braun A, Kelay P, Hub E. 102.  et al. 2014. The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes. Nat. Immunol. 15:623–30 [Google Scholar]
  103. Abadie V, Badell E, Douillard P, Ensergueix D, Leenen PJ. 103.  et al. 2005. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106:1843–50 [Google Scholar]
  104. Maletto BA, Ropolo AS, Alignani DO, Liscovsky MV, Ranocchia RP. 104.  et al. 2006. Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood 108:3094–102 [Google Scholar]
  105. Chtanova T, Schaeffer M, Han SJ, van Dooren GG, Nollmann M. 105.  et al. 2008. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29:487–96 [Google Scholar]
  106. Hampton HR, Bailey J, Tomura M, Brink R, Chtanova T. 106.  2015. Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes. Nat. Commun. 6:7139 [Google Scholar]
  107. Beauvillain C, Cunin P, Doni A, Scotet M, Jaillon S. 107.  et al. 2010. CCR7 is involved in the migration of neutrophils to lymph nodes. Blood 117:1196–204 [Google Scholar]
  108. Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F. 108.  et al. 2006. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25:989–1001 [Google Scholar]
  109. Park C, Hwang IY, Sinha RK, Kamenyeva O, Davis MD, Kehrl JH. 109.  2012. Lymph node B lymphocyte trafficking is constrained by anatomy and highly dependent upon chemoattractant desensitization. Blood 119:978–89 [Google Scholar]
  110. Choe K, Hwang Y, Seo H, Kim P. 110.  2013. In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes. J. Biomed. Opt. 18:036005 [Google Scholar]
  111. Mempel TR, Junt T, von Andrian UH. 111.  2006. Rulers over randomness: Stroma cells guide lymphocyte migration in lymph nodes. Immunity 25:867–69 [Google Scholar]
  112. Cahalan MD, Parker I. 112.  2008. Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu. Rev. Immunol. 26:585–626 [Google Scholar]
  113. Bajenoff M, Granjeaud S, Guerder S. 113.  2003. The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J. Exp. Med. 198:715–24 [Google Scholar]
  114. Worbs T, Mempel TR, Bolter J, von Andrian UH, Forster R. 114.  2007. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J. Exp. Med. 204:489–95 [Google Scholar]
  115. Asperti-Boursin F, Real E, Bismuth G, Trautmann A, Donnadieu E. 115.  2007. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase–independent manner. J. Exp. Med. 204:1167–79 [Google Scholar]
  116. Coelho FM, Natale D, Soriano SF, Hons M, Swoger J. 116.  et al. 2013. Naive B-cell trafficking is shaped by local chemokine availability and LFA-1–independent stromal interactions. Blood 121:4101–9 [Google Scholar]
  117. Shi GX, Harrison K, Wilson GL, Moratz C, Kehrl JH. 117.  2002. RGS13 regulates germinal center B lymphocytes responsiveness to CXC chemokine ligand (CXCL)12 and CXCL13. J. Immunol. 169:2507–15 [Google Scholar]
  118. Estes JD, Thacker TC, Hampton DL, Kell SA, Keele BF. 118.  et al. 2004. Follicular dendritic cell regulation of CXCR4-mediated germinal center CD4 T cell migration. J. Immunol. 173:6169–78 [Google Scholar]
  119. Moratz C, Hayman JR, Gu H, Kehrl JH. 119.  2004. Abnormal B-cell responses to chemokines, disturbed plasma cell localization, and distorted immune tissue architecture in Rgs1/− mice. Mol. Cell. Biol. 24:5767–75 [Google Scholar]
  120. Mempel TR, Henrickson SE, von Andrian UH. 120.  2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154–59 [Google Scholar]
  121. Miller MJ, Safrina O, Parker I, Cahalan MD. 121.  2004. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 200:847–56 [Google Scholar]
  122. Woodruff MC, Heesters BA, Herndon CN, Groom JR, Thomas PG. 122.  et al. 2014. Trans-nodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine. J. Exp. Med. 211:1611–21 [Google Scholar]
  123. Ngo VN, Tang HL, Cyster JG. 123.  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. 188:181–91 [Google Scholar]
  124. Sallusto F, Palermo B, Lenig D, Miettinen M, Matikainen S. 124.  et al. 1999. Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur. J. Immunol. 29:1617–25 [Google Scholar]
  125. Friedman RS, Jacobelli J, Krummel MF. 125.  2006. Surface-bound chemokines capture and prime T cells for synapse formation. Nat. Immunol. 7:1101–8 [Google Scholar]
  126. Zhao X, Sato A, Dela Cruz CS, Linehan M, Luegering A. 126.  et al. 2003. CCL9 is secreted by the follicle-associated epithelium and recruits dome region Peyer's patch CD11b+ dendritic cells. J. Immunol. 171:2797–803 [Google Scholar]
  127. Iwasaki A, Kelsall BL. 127.  2000. Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J. Exp. Med. 191:1381–94 [Google Scholar]
  128. Hase K, Murakami T, Takatsu H, Shimaoka T, Iimura M. 128.  et al. 2006. The membrane-bound chemokine CXCL16 expressed on follicle-associated epithelium and M cells mediates lympho-epithelial interaction in GALT. J. Immunol. 176:43–51 [Google Scholar]
  129. Tang HL, Cyster JG. 129.  1999. Chemokine up-regulation and activated T cell attraction by maturing dendritic cells. Science 284:819–22 [Google Scholar]
  130. Yoneyama H, Narumi S, Zhang Y, Murai M, Baggiolini M. 130.  et al. 2002. Pivotal role of dendritic cell–derived CXCL10 in the retention of T helper cell 1 lymphocytes in secondary lymph nodes. J. Exp. Med. 195:1257–66 [Google Scholar]
  131. Alferink J, Lieberam I, Reindl W, Behrens A, Weiss S. 131.  et al. 2003. Compartmentalized production of CCL17 in vivo: strong inducibility in peripheral dendritic cells contrasts selective absence from the spleen. J. Exp. Med. 197:585–99 [Google Scholar]
  132. Leon B, Ballesteros-Tato A, Browning JL, Dunn R, Randall TD, Lund FE. 132.  2012. Regulation of TH2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13:681–90 [Google Scholar]
  133. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. 133.  2006. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 440:890–95 [Google Scholar]
  134. Hugues S, Scholer A, Boissonnas A, Nussbaum A, Combadiere C. 134.  et al. 2007. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat. Immunol. 8:921–30 [Google Scholar]
  135. Hickman HD, Li L, Reynoso GV, Rubin EJ, Skon CN. 135.  et al. 2011. Chemokines control naive CD8+ T cell selection of optimal lymph node antigen presenting cells. J. Exp. Med. 208:2511–24 [Google Scholar]
  136. Kastenmuller W, Brandes M, Wang Z, Herz J, Egen JG, Germain RN. 136.  2013. Peripheral prepositioning and local CXCL9 chemokine-mediated guidance orchestrate rapid memory CD8+ T cell responses in the lymph node. Immunity 38:502–13 [Google Scholar]
  137. Henry CJ, Ornelles DA, Mitchell LM, Brzoza-Lewis KL, Hiltbold EM. 137.  2008. IL-12 produced by dendritic cells augments CD8+ T cell activation through the production of the chemokines CCL1 and CCL17. J. Immunol. 181:8576–84 [Google Scholar]
  138. Gerard A, Khan O, Beemiller P, Oswald E, Hu J. 138.  et al. 2013. Secondary T cell–T cell synaptic interactions drive the differentiation of protective CD8+ T cells. Nat. Immunol. 14:356–63 [Google Scholar]
  139. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH. 139.  et al. 2012. CXCR3 chemokine receptor–ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 37:1091–103 [Google Scholar]
  140. Langenkamp A, Nagata K, Murphy K, Wu L, Lanzavecchia A, Sallusto F. 140.  2003. Kinetics and expression patterns of chemokine receptors in human CD4+ T lymphocytes primed by myeloid or plasmacytoid dendritic cells. Eur. J. Immunol. 33:474–82 [Google Scholar]
  141. Kohlmeier JE, Reiley WW, Perona-Wright G, Freeman ML, Yager EJ. 141.  et al. 2011. Inflammatory chemokine receptors regulate CD8+ T cell contraction and memory generation following infection. J. Exp. Med. 208:1621–34 [Google Scholar]
  142. Castellino F, Germain RN. 142.  2007. Chemokine-guided CD4+ T cell help enhances generation of IL-6RαhighIL-7Rαhigh prememory CD8+ T cells. J. Immunol. 178:778–87 [Google Scholar]
  143. Baekkevold ES, Wurbel MA, Kivisakk P, Wain CM, Power CA. 143.  et al. 2005. A role for CCR4 in development of mature circulating cutaneous T helper memory cell populations. J. Exp. Med. 201:1045–51 [Google Scholar]
  144. Sung JH, Zhang H, Moseman EA, Alvarez D, Iannacone M. 144.  et al. 2012. Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell 150:1249–63 [Google Scholar]
  145. Reif K, Ekland EH, Ohl L, Nakano H, Lipp M. 145.  et al. 2002. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 416:94–99 [Google Scholar]
  146. Okada T, Miller MJ, Parker I, Krummel MF, Neighbors M. 146.  et al. 2005. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLOS Biol. 3:e150 [Google Scholar]
  147. Ansel KM, McHeyzer-Williams LJ, Ngo VN, McHeyzer-Williams MG, Cyster JG. 147.  1999. In vivo–activated CD4 T cells upregulate CXC chemokine receptor 5 and reprogram their response to lymphoid chemokines. J. Exp. Med. 190:1123–34 [Google Scholar]
  148. Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F. 148.  et al. 2000. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 192:1545–52 [Google Scholar]
  149. Schaerli P, Willimann K, Lang AB, Lipp M, Loetscher P, Moser B. 149.  2000. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192:1553–62 [Google Scholar]
  150. Kim CH, Rott LS, Clark-Lewis I, Campbell DJ, Wu L, Butcher EC. 150.  2001. Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center–localized subset of CXCR5+ T cells. J. Exp. Med. 193:1373–81 [Google Scholar]
  151. Allen CD, Okada T, Tang HL, Cyster JG. 151.  2007. Imaging of germinal center selection events during affinity maturation. Science 315:528–31 [Google Scholar]
  152. Hauser AE, Junt T, Mempel TR, Sneddon MW, Kleinstein SH. 152.  et al. 2007. Definition of germinal-center B cell migration in vivo reveals predominant intrazonal circulation patterns. Immunity 26:655–67 [Google Scholar]
  153. Schwickert TA, Lindquist RL, Shakhar G, Livshits G, Skokos D. 153.  et al. 2007. In vivo imaging of germinal centres reveals a dynamic open structure. Nature 446:83–87 [Google Scholar]
  154. Allen CD, Okada T, Cyster JG. 154.  2007. Germinal-center organization and cellular dynamics. Immunity 27:190–202 [Google Scholar]
  155. Allen CD, Ansel KM, Low C, Lesley R, Tamamura H. 155.  et al. 2004. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat. Immunol. 5:943–52 [Google Scholar]
  156. Wang X, Cho B, Suzuki K, Xu Y, Green JA. 156.  et al. 2011. Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J. Exp. Med. 208:2497–510 [Google Scholar]
  157. Lo CG, Xu Y, Proia RL, Cyster JG. 157.  2005. Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J. Exp. Med. 201:291–301 [Google Scholar]
  158. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG. 158.  2008. S1P1 receptor signaling overrides retention mediated by Gαi-coupled receptors to promote T cell egress. Immunity 28:122–33 [Google Scholar]
  159. Schmidt TH, Bannard O, Gray EE, Cyster JG. 159.  2013. CXCR4 promotes B cell egress from Peyer's patches. J. Exp. Med. 210:1099–107 [Google Scholar]
  160. Schulz O, Ugur M, Friedrichsen M, Radulovic K, Niess JH. 160.  et al. 2014. Hypertrophy of infected Peyer's patches arises from global, interferon-receptor, and CD69-independent shutdown of lymphocyte egress. Mucosal Immunol. 7:892–904 [Google Scholar]
  161. Shiow LR, Rosen DB, Brdicková N, Xu Y, An J. 161.  et al. 2006. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:7083540–44 [Google Scholar]
  162. Schwab SR, Cyster JG. 162.  2007. Finding a way out: lymphocyte egress from lymphoid organs. Nat. Immunol. 8:121295–301 [Google Scholar]
  163. Cyster JG, Schwab SR. 163.  2012. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 30:69–94 [Google Scholar]
  164. Kraal G, Schornagel K, Streeter PR, Holzmann B, Butcher EC. 164.  1995. Expression of the mucosal vascular addressin, MAdCAM-1, on sinus-lining cells in the spleen. Am. J. Pathol. 147:763–71 [Google Scholar]
  165. Katakai T, Suto H, Sugai M, Gonda H, Togawa A. 165.  et al. 2008. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol. 181:6189–200 [Google Scholar]
  166. Lo CG, Lu TT, Cyster JG. 166.  2003. Integrin-dependence of lymphocyte entry into the splenic white pulp. J. Exp. Med. 197:353–61 [Google Scholar]
  167. Steiniger B, Barth P, Hellinger A. 167.  2001. The perifollicular and marginal zones of the human splenic white pulp: Do fibroblasts guide lymphocyte immigration?. Am. J. Pathol. 159:501–12 [Google Scholar]
  168. Gatto D, Wood K, Brink R. 168.  2011. EBI2 operates independently of but in cooperation with CXCR5 and CCR7 to direct B cell migration and organization in follicles and the germinal center. J. Immunol. 187:4621–28 [Google Scholar]
  169. Pereira JP, Kelly LM, Xu Y, Cyster JG. 169.  2009. EBI2 mediates B cell segregation between the outer and centre follicle. Nature 460:1122–26 [Google Scholar]
  170. Nolte MA, Hamann A, Kraal G, Mebius RE. 170.  2002. The strict regulation of lymphocyte migration to splenic white pulp does not involve common homing receptors. Immunology 106:299–307 [Google Scholar]
  171. Grayson MH, Hotchkiss RS, Karl IE, Holtzman MJ, Chaplin DD. 171.  2003. Intravital microscopy comparing T lymphocyte trafficking to the spleen and the mesenteric lymph node. Am. J. Physiol. Heart Circ. Physiol. 284:H2213–26 [Google Scholar]
  172. Nolte MA, Belien JA, Schadee-Eestermans I, Jansen W, Unger WW. 172.  et al. 2003. A conduit system distributes chemokines and small blood-borne molecules through the splenic white pulp. J. Exp. Med. 198:505–12 [Google Scholar]
  173. Bajenoff M, Glaichenhaus N, Germain RN. 173.  2008. Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J. Immunol. 181:3947–54 [Google Scholar]
  174. Umemoto E, Otani K, Ikeno T, Verjan Garcia N, Hayasaka H. 174.  et al. 2012. Constitutive plasmacytoid dendritic cell migration to the splenic white pulp is cooperatively regulated by CCR7- and CXCR4-mediated signaling. J. Immunol. 189:191–99 [Google Scholar]
  175. Yi T, Wang X, Kelly LM, An J, Xu Y. 175.  et al. 2012. Oxysterol gradient generation by lymphoid stromal cells guides activated B cell movement during humoral responses. Immunity 37:535–48 [Google Scholar]
  176. Liu C, Yang XV, Wu J, Kuei C, Mani NS. 176.  et al. 2011. Oxysterols direct B-cell migration through EBI2. Nature 475:519–23 [Google Scholar]
  177. Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D. 177.  et al. 2011. Oxysterols direct immune cell migration via EBI2. Nature 475:524–27 [Google Scholar]
  178. Ngo VN, Korner H, Gunn MD, Schmidt KN, Riminton DS. 178.  et al. 1999. Lymphotoxin α/β and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J. Exp. Med. 189:403–12 [Google Scholar]
  179. Matsumoto M, Mariathasan S, Nahm MH, Baranyay F, Peschon JJ, Chaplin DD. 179.  1996. Role of lymphotoxin and the type I TNF receptor in the formation of germinal centers. Science 271:1289–91 [Google Scholar]
  180. Mebius RE, van Tuijl S, Weissman IL, Randall TD. 180.  1998. Transfer of primitive stem/progenitor bone marrow cells from LTα−/− donors to wild-type hosts: implications for the generation of architectural events in lymphoid B cell domains. J. Immunol. 161:3836–43 [Google Scholar]
  181. Endres R, Alimzhanov MB, Plitz T, Futterer A, Kosco-Vilbois MH. 181.  et al. 1999. Mature follicular dendritic cell networks depend on expression of lymphotoxin β receptor by radioresistant stromal cells and of lymphotoxin β and tumor necrosis factor by B cells. J. Exp. Med. 189:159–68 [Google Scholar]
  182. Ngo VN, Cornall RJ, Cyster JG. 182.  2001. Splenic T zone development is B cell dependent. J. Exp. Med. 194:1649–60 [Google Scholar]
  183. Zhao L, Liu L, Gao J, Yang Y, Hu C. 183.  et al. 2014. T lymphocytes maintain structure and function of fibroblastic reticular cells via lymphotoxin (LT)-B. BMC Immunol. 15:33 [Google Scholar]
  184. Lu TT, Cyster JG. 184.  2002. Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 297:409–12 [Google Scholar]
  185. Cinamon G, Zachariah MA, Lam OM, Foss FW Jr, Cyster JG. 185.  2008. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9:54–62 [Google Scholar]
  186. Arnon TI, Horton RM, Grigorova IL, Cyster JG. 186.  2013. Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature 493:684–88 [Google Scholar]
  187. Cinamon G, Matloubian M, Lesneski MJ, Xu Y, Low C. 187.  et al. 2004. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5:713–20 [Google Scholar]
  188. Vora KA, Nichols E, Porter G, Cui Y, Keohane CA. 188.  et al. 2005. Sphingosine 1-phosphate receptor agonist FTY720-phosphate causes marginal zone B cell displacement. J. Leukoc. Biol. 78:471–80 [Google Scholar]
  189. Wang H, Beaty N, Chen S, Qi CF, Masiuk M. 189.  et al. 2012. The CXCR7 chemokine receptor promotes B-cell retention in the splenic marginal zone and serves as a sink for CXCL12. Blood 119:465–68 [Google Scholar]
  190. Luker KE, Steele JM, Mihalko LA, Ray P, Luker GD. 190.  2010. Constitutive and chemokine-dependent internalization and recycling of CXCR7 in breast cancer cells to degrade chemokine ligands. Oncogene 29:4599–610 [Google Scholar]
  191. Aoshi T, Zinselmeyer BH, Konjufca V, Lynch JN, Zhang X. 191.  et al. 2008. Bacterial entry to the splenic white pulp initiates antigen presentation to CD8+ T cells. Immunity 29:476–86 [Google Scholar]
  192. Czeloth N, Schippers A, Wagner N, Muller W, Kuster B. 192.  et al. 2007. Sphingosine-1 phosphate signaling regulates positioning of dendritic cells within the spleen. J. Immunol. 179:5855–63 [Google Scholar]
  193. Rathinasamy A, Czeloth N, Pabst O, Forster R, Bernhardt G. 193.  2010. The origin and maturity of dendritic cells determine the pattern of sphingosine 1-phosphate receptors expressed and required for efficient migration. J. Immunol. 185:4072–81 [Google Scholar]
  194. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. 194.  2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164:2978–86 [Google Scholar]
  195. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C. 195.  et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315:107–11 [Google Scholar]
  196. Gatto D, Wood K, Caminschi I, Murphy-Durland D, Schofield P. 196.  et al. 2013. The chemotactic receptor EBI2 regulates the homeostasis, localization and immunological function of splenic dendritic cells. Nat. Immunol. 14:446–53 [Google Scholar]
  197. Yi T, Cyster JG. 197.  2013. EBI2-mediated bridging channel positioning supports splenic dendritic cell homeostasis and particulate antigen capture. eLife 2:e00757 [Google Scholar]
  198. Pooley JL, Heath WR, Shortman K. 198.  2001. Cutting edge: Intravenous soluble antigen is presented to CD4 T cells by CD8 dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166:5327–30 [Google Scholar]
  199. Chappell CP, Draves KE, Giltiay NV, Clark EA. 199.  2012. Extrafollicular B cell activation by marginal zone dendritic cells drives T cell–dependent antibody responses. J. Exp. Med. 209:1825–40 [Google Scholar]
  200. Yu P, Wang Y, Chin RK, Martinez-Pomares L, Gordon S. 200.  et al. 2002. B cells control the migration of a subset of dendritic cells into B cell follicles via CXC chemokine ligand 13 in a lymphotoxin-dependent fashion. J. Immunol. 168:5117–23 [Google Scholar]
  201. Balazs M, Martin F, Zhou T, Kearney J. 201.  2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17:341–52 [Google Scholar]
  202. Pape KA, Kouskoff V, Nemazee D, Tang HL, Cyster JG. 202.  et al. 2003. Visualization of the genesis and fate of isotype-switched B cells during a primary immune response. J. Exp. Med. 197:1677–87 [Google Scholar]
  203. Gatto D, Paus D, Basten A, Mackay CR, Brink R. 203.  2009. Guidance of B cells by the orphan G protein–coupled receptor EBI2 shapes humoral immune responses. Immunity 31:259–69 [Google Scholar]
  204. Kurachi M, Kurachi J, Suenaga F, Tsukui T, Abe J. 204.  et al. 2011. Chemokine receptor CXCR3 facilitates CD8+ T cell differentiation into short-lived effector cells leading to memory degeneration. J. Exp. Med. 208:1605–20 [Google Scholar]
  205. Hu JK, Kagari T, Clingan JM, Matloubian M. 205.  2011. Expression of chemokine receptor CXCR3 on T cells affects the balance between effector and memory CD8 T-cell generation. PNAS 108:E118–27 [Google Scholar]
  206. Ato M, Stager S, Engwerda CR, Kaye PM. 206.  2002. Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat. Immunol. 3:1185–91 [Google Scholar]
  207. Scandella E, Bolinger B, Lattmann E, Miller S, Favre S. 207.  et al. 2008. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue–inducer cells with stroma of the T cell zone. Nat. Immunol. 9:667–75 [Google Scholar]
  208. Khanna KM, McNamara JT, Lefrancois L. 208.  2007. In situ imaging of the endogenous CD8 T cell response to infection. Science 318:116–20 [Google Scholar]
  209. Shimizu K, Morikawa S, Kitahara S, Ezaki T. 209.  2009. Local lymphogenic migration pathway in normal mouse spleen. Cell Tissue Res. 338:423–32 [Google Scholar]
  210. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y. 210.  et al. 2004. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427:355–60 [Google Scholar]
  211. Sze DM, Toellner KM, Garcia de Vinuesa C, Taylor DR, MacLennan IC. 211.  2000. Intrinsic constraint on plasmablast growth and extrinsic limits of plasma cell survival. J. Exp. Med. 192:813–21 [Google Scholar]
  212. Ellyard JI, Avery DT, Mackay CR, Tangye SG. 212.  2005. Contribution of stromal cells to the migration, function and retention of plasma cells in human spleen: potential roles of CXCL12, IL-6 and CD54. Eur. J. Immunol. 35:699–708 [Google Scholar]
  213. Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A. 213.  et al. 2001. A coordinated change in chemokine responsiveness guides plasma cell movements. J. Exp. Med. 194:45–56 [Google Scholar]
  214. Kabashima K, Haynes NM, Xu Y, Nutt SL, Allende ML. 214.  et al. 2006. Plasma cell S1P1 expression determines secondary lymphoid organ retention versus bone marrow tropism. J. Exp. Med. 203:2683–90 [Google Scholar]
  215. Unsoeld H, Voehringer D, Krautwald S, Pircher H. 215.  2004. Constitutive expression of CCR7 directs effector CD8 T cells into the splenic white pulp and impairs functional activity. J. Immunol. 173:3013–19 [Google Scholar]
  216. Schenkel JM, Fraser KA, Masopust D. 216.  2014. Cutting edge: Resident memory CD8 T cells occupy frontline niches in secondary lymphoid organs. J. Immunol. 192:2961–64 [Google Scholar]
  217. Bajenoff M, Narni-Mancinelli E, Brau F, Lauvau G. 217.  2010. Visualizing early splenic memory CD8+ T cells reactivation against intracellular bacteria in the mouse. PLOS ONE 5:e11524 [Google Scholar]
  218. Fleige H, Ravens S, Moschovakis GL, Bolter J, Willenzon S. 218.  et al. 2014. IL-17–induced CXCL12 recruits B cells and induces follicle formation in BALT in the absence of differentiated FDCs. J. Exp. Med. 211:643–51 [Google Scholar]
  219. Neyt K, Perros F, GeurtsvanKessel CH, Hammad H, Lambrecht BN. 219.  2012. Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol. 33:297–305 [Google Scholar]
  220. Aloisi F, Pujol-Borrell R. 220.  2006. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6:205–17 [Google Scholar]
  221. Drayton DL, Liao S, Mounzer RH, Ruddle NH. 221.  2006. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7:344–53 [Google Scholar]
  222. Marinkovic T, Garin A, Yokota Y, Fu YX, Ruddle NH. 222.  et al. 2006. Interaction of mature CD3+CD4+ T cells with dendritic cells triggers the development of tertiary lymphoid structures in the thyroid. J. Clin. Investig. 116:2622–32 [Google Scholar]
  223. Rangel-Moreno J, Moyron-Quiroz JE, Hartson L, Kusser K, Randall TD. 223.  2007. Pulmonary expression of CXC chemokine ligand 13, CC chemokine ligand 19, and CC chemokine ligand 21 is essential for local immunity to influenza. PNAS 104:10577–82 [Google Scholar]
  224. Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y. 224.  et al. 2002. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J. Immunol. 169:424–33 [Google Scholar]
  225. Rangel-Moreno J, Carragher DM, de la Luz Garcia-Hernandez M, Hwang JY, Kusser K. 225.  et al. 2011. The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat. Immunol. 12:639–46 [Google Scholar]
  226. Peters A, Pitcher LA, Sullivan JM, Mitsdoerffer M, Acton SE. 226.  et al. 2011. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity 35:986–96 [Google Scholar]
  227. GeurtsvanKessel CH, Willart MA, Bergen IM, van Rijt LS, Muskens F. 227.  et al. 2009. Dendritic cells are crucial for maintenance of tertiary lymphoid structures in the lung of influenza virus–infected mice. J. Exp. Med. 206:2339–49 [Google Scholar]
  228. Halle S, Dujardin HC, Bakocevic N, Fleige H, Danzer H. 228.  et al. 2009. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J. Exp. Med. 206:2593–601 [Google Scholar]
  229. Muniz LR, Pacer ME, Lira SA, Furtado GC. 229.  2011. A critical role for dendritic cells in the formation of lymphatic vessels within tertiary lymphoid structures. J. Immunol. 187:828–34 [Google Scholar]
  230. Kocks JR, Davalos-Misslitz AC, Hintzen G, Ohl L, Forster R. 230.  2007. Regulatory T cells interfere with the development of bronchus-associated lymphoid tissue. J. Exp. Med. 204:723–34 [Google Scholar]
  231. Winter S, Loddenkemper C, Aebischer A, Rabel K, Hoffmann K. 231.  et al. 2010. The chemokine receptor CXCR5 is pivotal for ectopic mucosa-associated lymphoid tissue neogenesis in chronic Helicobacter pylori–induced inflammation. J. Mol. Med. 88:1169–80 [Google Scholar]
  232. Wengner AM, Hopken UE, Petrow PK, Hartmann S, Schurigt U. 232.  et al. 2007. CXCR5- and CCR7-dependent lymphoid neogenesis in a murine model of chronic antigen-induced arthritis. Arthritis Rheum. 56:3271–83 [Google Scholar]
  233. Barone F, Bombardieri M, Manzo A, Blades MC, Morgan PR. 233.  et al. 2005. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome. Arthritis Rheum. 52:1773–84 [Google Scholar]
  234. Shiao YM, Lee CC, Hsu YH, Huang SF, Lin CY. 234.  et al. 2010. Ectopic and high CXCL13 chemokine expression in myasthenia gravis with thymic lymphoid hyperplasia. J. Neuroimmunol. 221:101–6 [Google Scholar]
  235. Schmutz C, Hulme A, Burman A, Salmon M, Ashton B. 235.  et al. 2005. Chemokine receptors in the rheumatoid synovium: upregulation of CXCR5. Arthritis Res. Ther. 7:R217–29 [Google Scholar]
  236. Takemura S, Braun A, Crowson C, Kurtin PJ, Cofield RH. 236.  et al. 2001. Lymphoid neogenesis in rheumatoid synovitis. J. Immunol. 167:1072–80 [Google Scholar]
  237. Carlsen HS, Baekkevold ES, Morton HC, Haraldsen G, Brandtzaeg P. 237.  2004. Monocyte-like and mature macrophages produce CXCL13 (B cell–attracting chemokine 1) in inflammatory lesions with lymphoid neogenesis. Blood 104:3021–27 [Google Scholar]
  238. Buckley CD, Amft N, Bradfield PF, Pilling D, Ross E. 238.  et al. 2000. Persistent induction of the chemokine receptor CXCR4 by TGF-β1 on synovial T cells contributes to their accumulation within the rheumatoid synovium. J. Immunol. 165:3423–29 [Google Scholar]
  239. Finch DK, Ettinger R, Karnell JL, Herbst R, Sleeman MA. 239.  2013. Effects of CXCL13 inhibition on lymphoid follicles in models of autoimmune disease. Eur. J. Clin. Investig. 43:501–9 [Google Scholar]
  240. Zheng B, Ozen Z, Zhang X, De Silva S, Marinova E. 240.  et al. 2005. CXCL13 neutralization reduces the severity of collagen-induced arthritis. Arthritis Rheum. 52:620–26 [Google Scholar]
  241. Kramer JM, Klimatcheva E, Rothstein TL. 241.  2013. CXCL13 is elevated in Sjögren's syndrome in mice and humans and is implicated in disease pathogenesis. J. Leukoc. Biol. 94:1079–89 [Google Scholar]
  242. Bagaeva LV, Rao P, Powers JM, Segal BM. 242.  2006. CXC chemokine ligand 13 plays a role in experimental autoimmune encephalomyelitis. J. Immunol. 176:7676–85 [Google Scholar]
  243. Horuk R. 243.  2009. Chemokine receptor antagonists: overcoming developmental hurdles. Nat. Rev. Drug Discov. 8:23–33 [Google Scholar]
  244. Pease J, Horuk R. 244.  2012. Chemokine receptor antagonists. J. Med. Chem. 55:9363–92 [Google Scholar]
  245. Cyster JG. 245.  1999. Chemokines and cell migration in secondary lymphoid organs. Science 286:2098–102 [Google Scholar]
  246. Steiniger BS. 246.  2015. Human spleen microanatomy: why mice do not suffice. Immunology 145:334–46 [Google Scholar]
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