Blood, Sphingosine-1-Phosphate and Lymphocyte Migration Dynamics in the Spleen

Chapter

Abstract

The spleen, the largest secondary lymphoid organ, has long been known to play important roles in immunity against blood-borne invaders. Yet how cells migrate within the spleen to ensure fast and effective responses is only now coming to light. Chemokines and oxysterols guide lymphocytes from sites of release at terminal arterioles into the lymphocyte-rich white pulp. Sphingosine-1-phosphate (S1P) and S1P-receptor-1 (S1PR1) promote lymphocyte egress from white to red pulp and back to circulation. Intravital two-photon microscopy has shown that marginal zone (MZ) B cells that are enriched between white and red pulps undergo continual oscillatory migration between the MZ and follicles, ferrying antigens. Cycles of G-protein-coupled receptor kinase-2 (GRK2) mediated S1PR1 desensitization and resensitization underlie this remarkable behavior. The findings discussed in this review have implications for understanding how splenic antibody and T-cell responses are mounted, how the immunosuppressant drug FTY720 (fingolimod) affects the spleen, and how cell shuttling behaviors contribute to immunity.

References

  1. Allen CD, Okada T, Tang HL, Cyster JG (2007) Imaging of germinal center selection events during affinity maturation. Science 315:528–531PubMedGoogle Scholar
  2. Allende ML, Tuymetova G, Lee BG, Bonifacino E, Wu YP, Proia RL (2010) S1P1 receptor directs the release of immature B cells from bone marrow into blood. J Exp Med 207:1113–1124PubMedCentralPubMedGoogle Scholar
  3. Alon R, Feigelson SW (2009) Chemokine signaling to lymphocyte integrins under shear flow. Microcirculation 16:3–16PubMedGoogle Scholar
  4. Aoshi T, Zinselmeyer BH, Konjufca V, Lynch JN, Zhang X, Koide Y, Miller MJ (2008) Bacterial entry to the splenic white pulp initiates antigen presentation to CD8 + T cells. Immunity 29:476–486PubMedGoogle Scholar
  5. Arnon TI, Horton RM, Grigorova IL, and Cyster JG (2013) Visualization of splenic marginal zone B-cell shuttling and follicular B-cell egress. Nature 493:684–688Google Scholar
  6. Arnon TI, Xu Y, Lo C, Pham T, An J, Coughlin S, Dorn GW, Cyster JG (2011) GRK2-dependent S1PR1 desensitization is required for lymphocytes to overcome their attraction to blood. Science 333:1898–1903PubMedCentralPubMedGoogle Scholar
  7. Bajenoff M, Glaichenhaus N, Germain RN (2008) Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol 181:3947–3954PubMedCentralPubMedGoogle Scholar
  8. Bankovich AJ, Shiow LR, Cyster JG (2010) CD69 suppresses sphingosine-1-phosophate receptor-1 function through interaction with membrane helix 4. J Biol Chem 285:22328–22337Google Scholar
  9. Barral P, Sanchez-Nino MD, van Rooijen N, Cerundolo V, Batista FD (2012) The location of splenic NKT cells favours their rapid activation by blood-borne antigen. EMBO J 31:2378–2390PubMedCentralPubMedGoogle Scholar
  10. Basu S, Ray A, Dittel BN (2011) Cannabinoid receptor 2 is critical for the homing and retention of marginal zone B lineage cells and for efficient T-independent immune responses. J Immunol 187:5720–5732PubMedCentralPubMedGoogle Scholar
  11. Boscacci RT, Pfeiffer F, Gollmer K, Sevilla AI, Martin AM, Soriano SF, Natale D, Henrickson S, von Andrian UH, Fukui Y, Mellado M, Deutsch U, Engelhardt B, Stein JV (2010) Comprehensive analysis of lymph node stroma-expressed Ig superfamily members reveals redundant and nonredundant roles for ICAM-1, ICAM-2, and VCAM-1 in lymphocyte homing. Blood 116:915–925PubMedCentralPubMedGoogle Scholar
  12. Breart B, Ramos-Perez WD, Mendoza A, Salous AK, Gobert M, Huang Y, Adams RH, Lafaille JJ, Escalante-Alcalde D, Morris AJ, Schwab SR (2011) Lipid phosphate phosphatase 3 enables efficient thymic egress. J Exp Med 208:1267–1278PubMedCentralPubMedGoogle Scholar
  13. Brown MJ, Nijhara R, Hallam JA, Gignac M, Yamada KM, Erlandsen SL, Delon J, Kruhlak M, Shaw S (2003) Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 102:3890–3899PubMedGoogle Scholar
  14. Busillo JM, Armando S, Sengupta R, Meucci O, Bouvier M, Benovic JL (2010) Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J Biol Chem 285:7805–7817PubMedCentralPubMedGoogle Scholar
  15. Cahalan MD, Parker I (2008) Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu Rev Immunol 26:585–626PubMedCentralPubMedGoogle Scholar
  16. Cambier JC, Lehmann KR (1989) Ia-mediated signal transduction leads to proliferation of primed B lymphocytes. J Exp Med 170:877–886PubMedGoogle Scholar
  17. Christoffersen C, Obinata H, Kumaraswamy SB, Galvani S, Ahnstrom J, Sevvana M, Egerer-Sieber C, Muller YA, Hla T, Nielsen LB, Dahlback B (2011) Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. Proc Natl Acad Sci USA 108:9613–9618PubMedCentralPubMedGoogle Scholar
  18. Chun J, Brinkmann V (2011) A mechanistically novel, first oral therapy for multiple sclerosis: the development of fingolimod (FTY720, Gilenya). Discov Med 12:213–228PubMedCentralPubMedGoogle Scholar
  19. Cinamon G, Matloubian M, Lesneski MJ, Xu Y, Low C, Lu T, Proia RL, Cyster JG (2004) Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat Immunol 5:713–720PubMedGoogle Scholar
  20. Cinamon G, Zachariah M, Lam O, Cyster JG (2008) Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol 9:54–62PubMedCentralPubMedGoogle Scholar
  21. Cyster JG (2005) Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol 23:127–159PubMedGoogle Scholar
  22. Cyster JG, Goodnow CC (1995) Pertussis toxin inhibits migration of B and T lymphocytes into splenic white pulp cords. J Exp Med 182:581–586PubMedGoogle Scholar
  23. Cyster JG, Schwab SR (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 30:69–94PubMedGoogle Scholar
  24. de Paz JL, Moseman EA, Noti C, Polito L, von Andrian UH, Seeberger PH (2007) Profiling heparin-chemokine interactions using synthetic tools. ACS Chem Biol 2:735–744PubMedCentralPubMedGoogle Scholar
  25. Diaz GA (2005) CXCR4 mutations in WHIM syndrome: a misguided immune system? Immunol Rev 203:235–243PubMedGoogle Scholar
  26. Fehon RG, McClatchey AI, Bretscher A (2010) Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 11:276–287PubMedCentralPubMedGoogle Scholar
  27. Ferguson AR, Youd ME, Corley RB (2004) Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int Immunol 16:1411–1422PubMedGoogle Scholar
  28. Ford WL (1969) The kinetics of lymphocyte recirculation within the rat spleen. Cell Tissue Kinet 2:171–191Google Scholar
  29. Förster R, Emrich T, Kremmer E, Lipp M (1994) Expression of the G-protein-coupled receptor BLR1 defines mature, recirculating B cells and a subset of T-helper memory cells. Blood 84:830–840PubMedGoogle Scholar
  30. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner-Muller I, Wolf E, Lipp M (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23–33PubMedGoogle Scholar
  31. Fukuhara S, Simmons S, Kawamura S, Inoue A, Orba Y, Tokudome T, Sunden Y, Arai Y, Moriwaki K, Ishida J, Uemura A, Kiyonari H, Abe T, Fukamizu A, Hirashima M, Sawa H, Aoki J, Ishii M, Mochizuki N (2012) The sphingosine-1-phosphate transporter Spns2 expressed on endothelial cells regulates lymphocyte trafficking in mice. J Clin Invest 122:1416–1426PubMedCentralPubMedGoogle Scholar
  32. Gaengel K, Niaudet C, Hagikura K, Siemsen BL, Muhl L, Hofmann JJ, Ebarasi L, Nystrom S, Rymo S, Chen LL, Pang MF, Jin Y, Raschperger E, Roswall P, Schulte D, Benedito R, Larsson J, Hellstrom M, Fuxe J, Uhlen P, Adams R, Jakobsson L, Majumdar A, Vestweber D, Uv A, Betsholtz C (2012) The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR2. Dev Cell 23:587–599PubMedGoogle Scholar
  33. Gatto D, Wood K, Brink R (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 187:4621–4628PubMedGoogle Scholar
  34. Gonzalez-Cabrera PJ, Hla T, Rosen H (2007) Mapping pathways downstream of sphingosine 1-phosphate subtype 1 by differential chemical perturbation and proteomics. J Biol Chem 282:7254–7264PubMedGoogle Scholar
  35. Gowans JL, Knight EJ (1964) The route of re-circulation of lymphocytes in the rat. Proc Royal Soc Lon Biol 159:257–282Google Scholar
  36. Gray D, Kumararatne DS, Lortan J, Khan M, MacLennan IC (1984) Relation of intra-splenic migration of marginal zone B cells to antigen localization on follicular dendritic cells. Immunology 52:659–669PubMedCentralPubMedGoogle Scholar
  37. Grayson MH, Hotchkiss RS, Karl IE, Holtzman MJ, Chaplin DD (2003) Intravital microscopy comparing T lymphocyte trafficking to the spleen and the mesenteric lymph node. Am J Physiol Heart Circ Physiol 284:H2213–2226PubMedGoogle Scholar
  38. Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci USA 107:20447–20452PubMedCentralPubMedGoogle Scholar
  39. Grigorova IL, Schwab SR, Phan TG, Pham TH, Okada T, Cyster JG (2009) Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat Immunol 10:58–65PubMedCentralPubMedGoogle Scholar
  40. Guinamard R, Okigaki M, Schlessinger J, Ravetch JV (2000) Absence of marginal zone B cells in Pyk-2 deficient mice define their role in the humoral response. Nat Immunol 1:31–36PubMedGoogle Scholar
  41. Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D, Pereira JP, Guerini D, Baumgarten BU, Roggo S, Wen B, Knochenmuss R, Noel S, Gessier F, Kelly LM, Vanek M, Laurent S, Preuss I, Miault C, Christen I, Karuna R, Li W, Koo DI, Suply T, Schmedt C, Peters EC, Falchetto R, Katopodis A, Spanka C, Roy MO, Detheux M, Chen YA, Schultz PG, Cho CY, Seuwen K, Cyster JG, Sailer AW (2011) Oxysterols direct immune cell migration via EBI2. Nature 475:524–527PubMedGoogle Scholar
  42. Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A, Suzuki G, Zou YR, Littman DR, Cyster JG (2001) A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med 194:45–56PubMedCentralPubMedGoogle Scholar
  43. Hauser AE, Shlomchik MJ, Haberman AM (2007) In vivo imaging studies shed light on germinal-centre development. Nat Rev Immunol 7:499–504PubMedGoogle Scholar
  44. Ito K, Anada Y, Tani M, Ikeda M, Sano T, Kihara A, Igarashi Y (2007) Lack of sphingosine 1-phosphate-degrading enzymes in erythrocytes. Biochem Biophys Res Commun 357:212–217PubMedGoogle Scholar
  45. Jacob J, Kassir R, Kelsoe G (1991) In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. I. The architecture and dynamics of responding cell populations. J Exp Med 173:1165–1175PubMedGoogle Scholar
  46. Kabashima K, Haynes NM, Xu Y, Nutt SL, Allende ML, Proia RL, Cyster JG (2006) Plasma cell S1P1 expression determines secondary lymphoid organ retention versus bone marrow tropism. J Exp Med 203:2683–2690PubMedCentralPubMedGoogle Scholar
  47. Kelly LM, Pereira JP, Yi T, Xu Y, Cyster JG (2011) EBI2 guides serial movements of activated B cells and ligand activity is detectable in lymphoid and nonlymphoid tissues. J Immunol 187:3026–3032PubMedCentralPubMedGoogle Scholar
  48. Khanna KM, McNamara JT, Lefrancois L (2007) In situ imaging of the endogenous CD8 T cell response to infection. Science 318:116–120PubMedCentralPubMedGoogle Scholar
  49. Knisely MH (1936) Spleen studies. I. Microscopic observations of the circulatory system of living unstimulated mammalian spleens. Anat Rec 65:23–50Google Scholar
  50. Kraal G, Mebius R (2006) New insights into the cell biology of the marginal zone of the spleen. Int Rev Cytol 250:175–215PubMedGoogle Scholar
  51. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, Keller M, Forster R, Critchley DR, Fassler R, Sixt M (2008) Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453:51–55PubMedGoogle Scholar
  52. Leuschner F, Panizzi P, Chico-Calero I, Lee WW, Ueno T, Cortez-Retamozo V, Waterman P, Gorbatov R, Marinelli B, Iwamoto Y, Chudnovskiy A, Figueiredo JL, Sosnovik DE, Pittet MJ, Swirski FK, Weissleder R, Nahrendorf M (2010) Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction. Circ Res 107:1364–1373PubMedCentralPubMedGoogle Scholar
  53. Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8:1255–1265PubMedGoogle Scholar
  54. Liu C, Yang XV, Wu J, Kuei C, Mani NS, Zhang L, Yu J, Sutton SW, Qin N, Banie H, Karlsson L, Sun S, Lovenberg TW (2011) Oxysterols direct B-cell migration through EBI2. Nature 475:519–523PubMedGoogle Scholar
  55. Liu CH, Thangada S, Lee MJ, Van Brocklyn JR, Spiegel S, Hla T (1999) Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol Biol Cell 10:1179–1190PubMedCentralPubMedGoogle Scholar
  56. Lo CG, Lu TT, Cyster JG (2003) Integrin-dependence of lymphocyte entry into the splenic white pulp. J Exp Med 197:353–361PubMedCentralPubMedGoogle Scholar
  57. Lo CG, Xu Y, Proia RL, Cyster JG (2005) Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit. J Exp Med 201:291–301PubMedCentralPubMedGoogle Scholar
  58. Lu TT, Cyster JG (2002) Integrin-mediated long-term B cell retention in the splenic marginal zone. Science 297:409–412PubMedGoogle Scholar
  59. Luo ZJ, Tanaka T, Kimura F, Miyasaka M (1999) Analysis of the mode of action of a novel immunosuppressant FTY720 in mice. Immunopharmacology 41:199–207PubMedGoogle Scholar
  60. MacDonald IC, Ragan DM, Schmidt EE, Groom AC (1987) Kinetics of red blood cell passage through interendothelial slits into venous sinuses in rat spleen, analyzed by in vivo microscopy. Microvasc Res 33:118–134PubMedGoogle Scholar
  61. MacLennan ICM, Gray D, Kumararatne DS, Bazin H (1982) The lymphocytes of splenic marginal zones: a distinct B-cell lineage. Immunol Today 3:305–307Google Scholar
  62. Mandala S, Hajdu R, Bergstrom J, Quackenbush E, Xie J, Milligan J, Thornton R, Shei GJ, Card D, Keohane C, Rosenbach M, Hale J, Lynch CL, Rupprecht K, Parsons W, Rosen H (2002) Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296:346–349PubMedGoogle Scholar
  63. Manevich-son E, Grabovsky V, Feigelson SW, Cinamon G, Gore Y, Goverse G, Monkley SJ, Margalit R, Melamed D, Mebius RE, Critchley DR, Shachar I, Alon R (2010) Talin1 is required for integrin-dependent B lymphocyte homing to lymph nodes and the bone marrow but not for follicular B-cell maturation in the spleen. Blood 116:5907–5918PubMedGoogle Scholar
  64. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, Brinkmann V, Allende ML, Proia RL, Cyster JG (2004) Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427:355–360PubMedGoogle Scholar
  65. McCuskey RS, McCuskey PA (1985) In vivo and electron microscopic studies of the splenic microvasculature in mice. Experientia 41:179–187PubMedGoogle Scholar
  66. Mebius RE, Kraal G (2005) Structure and function of the spleen. Nat Rev Immunol 5:606–616PubMedGoogle Scholar
  67. Mendelson K, Zygmunt T, Torres-Vazquez J, Evans T, Hla T (2013) Sphingosine-1-Phosphate receptors S1pr1 and S1pr2 cooperatively regulate embryonic vascular development. J Biol Chem 288:2145–2156Google Scholar
  68. Mendoza A, Breart B, Ramos-Perez WD, Pitt LA, Gobert M, Sunkara M, Lafaille JJ, Morris AJ, Schwab SR (2012) The transporter spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Rep 2:1104–1110PubMedCentralPubMedGoogle Scholar
  69. Mitchell J (1973) Lymphocyte circulation in the spleen: Marginal zone bridging channels and their possible role in cell traffic. Immunology 24:93–107PubMedCentralPubMedGoogle Scholar
  70. Morris MA, Gibb DR, Picard F, Brinkmann V, Straume M, Ley K (2005) Transient T cell accumulation in lymph nodes and sustained lymphopenia in mice treated with FTY720. Eur J Immunol 35:3570–3580PubMedGoogle Scholar
  71. Muppidi JR, Arnon TI, Bronevetsky Y, Veerapen N, Tanaka M, Besra GS, Cyster JG (2011) Cannabinoid receptor 2 positions and retains marginal zone B cells within the splenic marginal zone. J Exp Med 208:1941–1948PubMedCentralPubMedGoogle Scholar
  72. Murata N, Sato K, Kon J, Tomura H, Yanagita M, Kuwabara A, Ui M, Okajima F (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352(Pt 3):809–815PubMedCentralPubMedGoogle Scholar
  73. Murooka TT, Deruaz M, Marangoni F, Vrbanac VD, Seung E, von Andrian UH, Tager AM, Luster AD, Mempel TR (2012) HIV-infected T cells are migratory vehicles for viral dissemination. Nature 490:283–287PubMedCentralPubMedGoogle Scholar
  74. Ngo VN, Tang HL, Cyster JG (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 188:181–191PubMedCentralPubMedGoogle Scholar
  75. Nieuwenhuis P, Ford WL (1976) Comparative migration of B- and T-lymphocytes in the rat spleen and lymph nodes. Cell Immunol 23:254–267PubMedGoogle Scholar
  76. Ohnishi K, Melchers F, Shimizu T (2005) Lymphocyte-expressed BILL-cadherin/cadherin-17 contributes to the development of B cells at two stages. Eur J Immunol 35:957–963PubMedGoogle Scholar
  77. Oo ML, Chang SH, Thangada S, Wu MT, Rezaul K, Blaho V, Hwang SI, Han DK, Hla T (2011) Engagement of S1P1-degradative mechanisms leads to vascular leak in mice. J Clin Invest 121:2290–2300PubMedCentralPubMedGoogle Scholar
  78. Oo ML, Thangada S, Wu MT, Liu CH, Macdonald TL, Lynch KR, Lin CY, Hla T (2007) Immunosuppressive and anti-angiogenic sphingosine 1-phosphate receptor-1 agonists induce ubiquitinylation and proteasomal degradation of the receptor. J Biol Chem 282:9082–9089PubMedGoogle Scholar
  79. Pappu R, Schwab SR, Cornelissen I, Pereira JP, Regard JB, Xu Y, Camerer E, Zheng YW, Huang Y, Cyster JG, Coughlin SR (2007) Promotion of lymphocyte egress into blood and lymph by distinct sources of sphingosine-1-phosphate. Science 316:295–298PubMedGoogle Scholar
  80. Park C, Hwang IY, Sinha RK, Kamenyeva O, Davis MD, Kehrl JH (2012) Lymph node B lymphocyte trafficking is constrained by anatomy and highly dependent upon chemoattractant desensitization. Blood 119:978–989PubMedCentralPubMedGoogle Scholar
  81. Patel DD, Koopmann W, Imai T, Whichard LP, Yoshie O, Krangel MS (2001) Chemokines have diverse abilities to form solid phase gradients. Clin Immunol 99:43–52PubMedGoogle Scholar
  82. Penela P, Ribas C, Aymerich I, Mayor F Jr (2009) New roles of G protein-coupled receptor kinase 2 (GRK2) in cell migration. Cell Adh Migr 3:19–23PubMedCentralPubMedGoogle Scholar
  83. Pereira JP, An J, Xu Y, Huang Y, Cyster JG (2009a) Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat Immunol 10:403–411PubMedCentralPubMedGoogle Scholar
  84. Pereira JP, Kelly LM, Xu Y, Cyster JG (2009b) EBI2 mediates B cell segregation between the outer and centre follicle. Nature 460:1122–1126PubMedCentralPubMedGoogle Scholar
  85. Pham TH, Baluk P, Xu Y, Grigorova I, Bankovich AJ, Pappu R, Coughlin SR, McDonald DM, Schwab SR, Cyster JG (2010) Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J Exp Med 207:17–27PubMedCentralPubMedGoogle Scholar
  86. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG (2008) S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28:122–133PubMedCentralPubMedGoogle Scholar
  87. Phan TG, Grigorova I, Okada T, Cyster JG (2007) Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol 8:992–1000PubMedGoogle Scholar
  88. Reiter E, Lefkowitz RJ (2006) GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol Metab 17:159–165PubMedGoogle Scholar
  89. Rosen H, Sanna MG, Cahalan SM, Gonzalez-Cabrera PJ (2007) Tipping the gatekeeper: S1P regulation of endothelial barrier function. Trends Immunol 28:102–107PubMedGoogle Scholar
  90. Santos-Argumedo L, Kincade PW, Partida-Sanchez S, Parkhouse RM (1997) CD44-stimulated dendrite formation (‘spreading’) in activated B cells. Immunology 90:147–153PubMedCentralPubMedGoogle Scholar
  91. Schmidt EE, MacDonald IC, Groom AC (1985) Microcirculation in mouse spleen (nonsinusal) studied by means of corrosion casts. J Morphology 186:17–29Google Scholar
  92. Schmidt EE, MacDonald IC, Groom AC (1993) Comparative aspects of splenic microcirculatory pathways in mammals: the region bordering the white pulp. Scanning Microsc 7:613–628PubMedGoogle Scholar
  93. Schumann K, Lammermann T, Bruckner M, Legler DF, Polleux J, Spatz JP, Schuler G, Forster R, Lutz MB, Sorokin L, Sixt M (2010) Immobilized chemokine fields and soluble chemokine gradients cooperatively shape migration patterns of dendritic cells. Immunity 32:703–713PubMedGoogle Scholar
  94. Schwab SR, Pereira JP, Matloubian M, Xu Y, Huang Y, Cyster JG (2005) Lymphocyte sequestration through S1P lyase inhibition and disruption of S1P gradients. Science 309:1735–1739PubMedGoogle Scholar
  95. Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M (2006) CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544PubMedGoogle Scholar
  96. Shoham AB, Malkinson G, Krief S, Shwartz Y, Ely Y, Ferrara N, Yaniv K, Zelzer E (2012) S1P1 inhibits sprouting angiogenesis during vascular development. Development 139:3859–3869PubMedGoogle Scholar
  97. Sinha RK, Park C, Hwang IY, Davis MD, Kehrl JH (2009) B lymphocytes exit lymph nodes through cortical lymphatic sinusoids by a mechanism independent of sphingosine-1-phosphate-mediated chemotaxis. Immunity 30:434–446PubMedCentralPubMedGoogle Scholar
  98. Suzuki K, Grigorova I, Phan TG, Kelly L, Cyster JG (2009) Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 206:1485–1493PubMedCentralPubMedGoogle Scholar
  99. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ (2009) Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325:612–616PubMedCentralPubMedGoogle Scholar
  100. Teijaro JR, Walsh KB, Cahalan S, Fremgen DM, Roberts E, Scott F, Martinborough E, Peach R, Oldstone MB, Rosen H (2011) Endothelial cells are central orchestrators of cytokine amplification during influenza virus infection. Cell 146:980–991PubMedCentralPubMedGoogle Scholar
  101. Thangada S, Khanna KM, Blaho VA, Oo ML, Im DS, Guo C, Lefrancois L, Hla T (2010) Cell-surface residence of sphingosine 1-phosphate receptor 1 on lymphocytes determines lymphocyte egress kinetics. J Exp Med 207:1475–1483PubMedCentralPubMedGoogle Scholar
  102. Tomura M, Itoh K, Kanagawa O (2010) Naive CD4 + T lymphocytes circulate through lymphoid organs to interact with endogenous antigens and upregulate their function. J Immunol 184:4646–4653PubMedGoogle Scholar
  103. Tomura M, Yoshida N, Tanaka J, Karasawa S, Miwa Y, Miyawaki A, Kanagawa O (2008) Monitoring cellular movement in vivo with photoconvertible fluorescence protein “Kaede” transgenic mice. Proc Natl Acad Sci USA 105:10871–10876PubMedCentralPubMedGoogle Scholar
  104. van Rooijen N (1973) Mechanism of follicular antigen trapping. Migration of antigen-antibody complexes from marginal zone towards follicle centres. Immunology 25:847–852PubMedCentralPubMedGoogle Scholar
  105. Veerman AJ, van Ewijk W (1975) White pulp compartments in the spleen of rats and mice. A light and electron microscopic study of lymphoid and non-lymphoid cell types in T- and B- areas. Cell Tissue Res 156:417–441PubMedGoogle Scholar
  106. Venkataraman K, Lee YM, Michaud J, Thangada S, Ai Y, Bonkovsky HL, Parikh NS, Habrukowich C, Hla T (2008) Vascular endothelium as a contributor of plasma sphingosine 1-phosphate. Circ Res 102:669–676PubMedCentralPubMedGoogle Scholar
  107. Vora KA, Nichols E, Porter G, Cui Y, Keohane CA, Hajdu R, Hale J, Neway W, Zaller D, Mandala S (2005) Sphingosine 1-phosphate receptor agonist FTY720-phosphate causes marginal zone B cell displacement. J Leukoc Biol 78:471–480PubMedGoogle Scholar
  108. Waite JC, Leiner I, Lauer P, Rae CS, Barbet G, Zheng H, Portnoy DA, Pamer EG, Dustin ML (2011) Dynamic imaging of the effector immune response to listeria infection in vivo. PLoS Pathog 7:e1001326PubMedCentralPubMedGoogle Scholar
  109. Watterson KR, Johnston E, Chalmers C, Pronin A, Cook SJ, Benovic JL, Palmer TM (2002) Dual regulation of EDG1/S1P(1) receptor phosphorylation and internalization by protein kinase C and G-protein-coupled receptor kinase 2. J Biol Chem 277:5767–5777PubMedGoogle Scholar
  110. Weill JC, Weller S, Reynaud CA (2009) Human marginal zone B cells. Annu Rev Immunol 27:267–285PubMedGoogle Scholar
  111. Woolf E, Grigorova I, Sagiv A, Grabovsky V, Feigelson SW, Shulman Z, Hartmann T, Sixt M, Cyster JG, Alon R (2007) Lymph node chemokines promote sustained T lymphocyte motility without triggering stable integrin adhesiveness in the absence of shear forces. Nat Immunol 8:1076–1085PubMedGoogle Scholar
  112. Yi T, Wang X, Kelly LM, An J, Xu Y, Sailer AW, Gustafsson JA, Russell DW, Cyster JG (2012) Oxysterol gradient generation by lymphoid stromal cells guides activated B cell movement during humoral responses. Immunity 37:535–548PubMedCentralPubMedGoogle Scholar

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© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Howard Hughes Medical Institute and Department of Microbiology and ImmunologyUniversity of California San FranciscoSan FranciscoUSA
  2. 2.The Kennedy Institute of RheumatologyUniversity of OxfordHeadington, OxfordUK

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