EBI2-mediated bridging channel positioning supports splenic dendritic cell homeostasis and particulate antigen capture

eLife

Volumn 2013, Issue 2, 2013, Pages

  Yi, Tangsheng ^a,b   Cyster, Jason G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7ALPHA HYDROXYCHOLESTEROL; CASPASE 3; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR4; EBI2 PROTEIN; G PROTEIN COUPLED RECEPTOR; GLYCOPROTEIN P 15095; OXYSTEROL; UNCLASSIFIED DRUG; ANTIGEN; GPR183 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN BINDING; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SELECTION; CELL TRANSFER; CHEMOTAXIS; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; GENETIC TRANSFECTION; HELPER CELL; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; VIRAL GENE DELIVERY SYSTEM; ANIMAL; CYTOLOGY; GENETICS; IMMUNOLOGY; PHYSIOLOGY; SPLEEN;

ANIMALS; ANTIGENS; DENDRITIC CELLS; HOMEOSTASIS; MICE; RECEPTORS, G-PROTEIN-COUPLED; SPLEEN;

EID: 84879033554     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00757     Document Type: Article

References (53)

1. Ansel KM, Ngo VN, Hyman PL, Luther SA, Förster R, Sedgwick JD, et al. 2000. A chemokine driven positive feedback loop organizes lymphoid follicles. Nature 406:309-14. doi: 10.1038/35018581.
2. Balazs M, Martin F, Zhou T, Kearney J. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17:341-52. doi: 10.1016/S1074-7613(02)00389-8.
3. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392:245-52. doi: 10.1038/32588.
4. Bauman DR, Bitmansour AD, McDonald JG, Thompson BM, Liang G, Russell DW. 2009. 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc Natl Acad Sci USA 106:16764-9. doi: 10.1073/pnas.0909142106.
5. Bromley SK, Mempel TR, Luster AD. 2008. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat Immunol 9:970-80. doi: 10.1038/ni.f.213.
6. Caton ML, Smith-Raska MR, Reizis B. 2007. Notch-RBP-J signaling controls the homeostasis of CD8-dendritic cells in the spleen. J Exp Med 204:1653-64. doi: 10.1084/jem.20062648.
7. Chappell CP, Draves KE, Giltiay NV, Clark EA. 2012. Extrafollicular B cell activation by marginal zone dendritic cells drives T cell-dependent antibody responses. J Exp Med 209:1825-40. doi: 10.1084/jem.20120774.
8. Chen M, Huang L, Wang J. 2007. Deficiency of Bim in dendritic cells contributes to overactivation of lymphocytes and autoimmunity. Blood 109:4360-7. doi: 10.1182/blood-2006-11-056424.
9. Cyster JG. 2005. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu Rev Immunol 23:127-59. doi: 10.1146/annurev.immunol.23.021704.115628.
10. De Becker G, Moulin V, Pajak B, Bruck C, Francotte M, Thiriart C, et al. 2000. The adjuvant monophosphoryl lipid A increases the function of antigen-presenting cells. Int Immunol 12:807-15. doi: 10.1093/intimm/12.6.807.
11. De Trez C, Pajak B, Brait M, Glaichenhaus N, Urbain J, Moser M, et al. 2005. TLR4 and Toll-IL-1 receptor domain-containing adapter-inducing IFN-beta, but not MyD88, regulate Escherichia coli-induced dendritic cell maturation and apoptosis in vivo. J Immunol 175:839-46.
12. De Trez C, Schneider K, Potter K, Droin N, Fulton J, Norris PS, et al. 2008. The inhibitory HVEM-BTLA pathway counter regulates lymphotoxin receptor signaling to achieve homeostasis of dendritic cells. J Immunol 180:238-48.
13. Dudziak D, Kamphorst AO, Heidkamp GF, Buchholz VR, Trumpfheller C, Yamazaki S, et al. 2007. Differential antigen processing by dendritic cell subsets in vivo. Science 315:107-11. doi: 10.1126/science.1136080.
14. Fukaya T, Murakami R, Takagi H, Sato K, Sato Y, Otsuka H, et al. 2012. Conditional ablation of CD205+ conventional dendritic cells impacts the regulation of T-cell immunity and homeostasis in vivo. Proc Natl Acad Sci USA 109:11288-93. doi: 10.1073/pnas.1202208109.
15. Gatto D, Paus D, Basten A, Mackay CR, Brink R. 2009. Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity 31:259-69. doi: 10.1016/j.immuni.2009.06.016.
16. Gatto D, Wood K, Caminschi I, Murphy-Durland D, Schofield P, Christ D, et al. 2013. The chemotactic receptor EBI2 regulates the homeostasis, localization and immunological function of splenic dendritic cells. Nat Immunol 14:446-53. doi: 10.1038/ni.2555.
17. Hagnerud S, Manna PP, Cella M, Stenberg A, Frazier WA, Colonna M, et al. 2006. Deficit of CD47 results in a defect of marginal zone dendritic cells, blunted immune response to particulate antigen and impairment of skin dendritic cell migration. J Immunol 176:5772-8.
18. Hannedouche S, Zhang J, Yi T, Shen W, Nguyen D, Pereira JP, et al. 2011. Oxysterols direct immune cell migration via EBI2. Nature 475:524-7. doi: 10.1038/nature10280.
19. Hashimoto D, Miller J, Merad M. 2011. Dendritic cell and macrophage heterogeneity in vivo. Immunity 35:323-35. doi: 10.1016/j.immuni.2011.09.007.
20. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, et al. 2008. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322:1097-100. doi: 10.1126/science.1164206.
21. Jego G, Pascual V, Palucka AK, Banchereau J. 2005. Dendritic cells control B cell growth and differentiation. Curr Dir Autoimmun 8:124-39. doi: 10.1159/000082101.
22. Kabashima K, Banks TA, Ansel KM, Lu TT, Ware CF, Cyster JG. 2005. Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity 22:439-50. doi: 10.1016/j.immuni.2005.02.007.
23. Kamath AT, Henri S, Battye F, Tough DF, Shortman K. 2002. Developmental kinetics and lifespan of dendritic cells in mouse lymphoid organs. Blood 100:1734-41.
24. Lee SK, Rigby RJ, Zotos D, Tsai LM, Kawamoto S, Marshall JL, et al. 2011. B cell priming for extrafollicular antibody responses requires Bcl-6 expression by T cells. J Exp Med 208:1377-88. doi: 10.1084/jem.20102065.
25. Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT, Ng D, et al. 2011. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 35:780-91. doi: 10.1016/j.immuni.2011.08.013.
26. Liu C, Yang XV, Wu J, Kuei C, Mani NS, Zhang L, et al. 2011. Oxysterols direct B-cell migration through EBI2. Nature 475:519-23. doi: 10.1038/nature10226.
27. Liu K, Waskow C, Liu X, Yao K, Hoh J, Nussenzweig M. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 8:578-83. doi: 10.1038/ni1462.
28. MacPherson G, Kushnir N, Wykes M. 1999. Dendritic cells, B cells and the regulation of antibody synthesis. Immunol Rev 172:325-34. doi: 10.1111/j.1600-065X.1999.tb01376.x.
29. Mebius RE, Kraal G. 2005. Structure and function of the spleen. Nat Rev Immunol 5:606-16. doi: 10.1038/nri1669.
30. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, et al. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 13:888-99. doi: 10.1038/ni.2370.
31. Mitchell J. 1973. Lymphocyte circulation in the spleen: marginal zone bridging channels and their possible role in cell traffic. Immunology 24:93-107.
32. Naik SH, Metcalf D, van Nieuwenhuijze A, Wicks I, Wu L, O'Keeffe M, et al. 2006. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 7:663-71. doi: 10.1038/ni1340.
33. Ngo VN, Cornall RJ, Cyster JG. 2001. Splenic T zone development is B cell dependent. J Exp Med 194:1649-60. doi: 10.1084/jem.194.11.1649.
34. Nolte MA, Belien JA, Schadee-Eestermans I, Jansen W, Unger WW, van Rooijen N, et al. 2003. A conduit system distributes chemokines and small blood-borne molecules through the splenic white pulp. J Exp Med 198:505-12. doi: 10.1084/jem.20021801.
35. Pereira JP, Kelly LM, Xu Y, Cyster JG. 2009. EBI2 mediates B cell segregation between the outer and centre follicle. Nature 460:1122-6. doi: 10.1038/nature08226.
36. Pooley JL, Heath WR, Shortman K. 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.
37. Qi H, Egen JG, Huang AY, Germain RN. 2006. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 312:1672-6. doi: 10.1126/science.1125703.
38. Reif K, Ekland EH, Ohl L, Nakano H, Lipp M, Forster R, et al. 2002. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 416:94-9. doi: 10.1038/416094a.
39. Rose K, Allan A, Gauldie S, Stapleton G, Dobbie L, Dott K, et al. 2001. Neurosteroid hydroxylase CYP7B: vivid reporter activity in dentate gyrus of gene-targeted mice and abolition of a widespread pathway of steroid and oxysterol hydroxylation. J Biol Chem 276:23937-44. doi: 10.1074/jbc.M011564200.
40. Russell DW. 2003. The enzymes, regulation, and genetics of bile acid synthesis. Annu Rev Biochem 72:137-74. doi: 10.1146/annurev.biochem.72.121801.161712.
41. Saito Y, Iwamura H, Kaneko T, Ohnishi H, Murata Y, Okazawa H, et al. 2010. Regulation by SIRPalpha of dendritic cell homeostasis in lymphoid tissues. Blood 116:3517-25. doi: 10.1182/blood-2010-03-277244.
42. Satpathy AT, Wu X, Albring JC, Murphy KM. 2012. Re(de)fining the dendritic cell lineage. Nat Immunol 13:1145-54. doi: 10.1038/ni.2467.
43. Seul HJ, Ahn YR, Song HM, Ha YJ, Lee JR. 2012. Over-expression of a RhoA-specific guanine nucleotide exchange factor, p190RhoGEF, in mouse dendritic cells negatively regulates cellular responses to bacterial lipopolysaccharide. Mol Cells 34:159-64. doi: 10.1007/s10059-012-0055-9.
44. Shea HC, Head DD, Setchell KD, Russell DW. 2007. Analysis of HSD3B7 knockout mice reveals that a 3alpha-hydroxyl stereochemistry is required for bile acid function. Proc Natl Acad Sci USA 104:11526-33. doi: 10.1073/pnas.0705089104.
45. Shortman K, Liu YJ. 2002. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2:151-61. doi: 10.1038/nri746.
46. Stanley AC, de Labastida Rivera F, Haque A, Sheel M, Zhou Y, Amante FH, et al. 2011. Critical roles for LIGHT and its receptors in generating T cell-mediated immunity during Leishmania donovani infection. PLoS Pathog 7:e1002279. doi: 10.1371/journal.ppat.1002279.
47. Steinman RM, Pack M, Inaba K. 1997. Dendritic cells in the T-cell areas of lymphoid organs. Immunol Rev 156:25-37. doi: 10.1111/j.1600-065X.1997.tb00956.x.
48. Tamura T, Tailor P, Yamaoka K, Kong HJ, Tsujimura H, O'Shea JJ, Singh H, et al. 2005. IFN regulatory factor-4 and-8 govern dendritic cell subset development and their functional diversity. J Immunol 174:2573-81.
49. Van VQ, Lesage S, Bouguermouh S, Gautier P, Rubio M, Levesque M, et al. 2006. Expression of the self-marker CD47 on dendritic cells governs their trafficking to secondary lymphoid organs. EMBO J 25:5560-8. doi: 10.1038/sj.emboj.7601415.
50. Vinuesa CG, Cyster JG. 2011. How T cells earn the follicular rite of passage. Immunity 35:671-80. doi: 10.1016/j.immuni.2011.11.001.
51. Wang YG, Kim KD, Wang J, Yu P, Fu YX. 2005. Stimulating lymphotoxin beta receptor on the dendritic cells is critical for their homeostasis and expansion. J Immunol 175:6997-7002.
52. Witmer MD, Steinman RM. 1984. The anatomy of peripheral lymphoid organs with emphasis on accessory cells: light-microscopic immunocytochemical studies of mouse spleen, lymph node, and Peyer's patch. Am J Anat 170:465-81. doi: 10.1002/(ISSN)1553-0795.
53. Yi T, Wang X, Kelly LM, An J, Xu Y, Sailer AW, et al. 2012. Oxysterol gradient generation by lymphoid stromal cells guides activated B cell movement during humoral responses. Immunity 37:535-48. doi: 10.1016/j.immuni.2012.06.015.