Oxysterol Gradient Generation by Lymphoid Stromal Cells Guides Activated B Cell Movement during Humoral Responses

Immunity

Volumn 37, Issue 3, 2012, Pages 535-548

  Yi, Tangsheng ^a   Wang, Xiaoming ^a   Kelly, Lisa M ^a   An, Jinping ^a   Xu, Ying ^a   Sailer, Andreas W ^b   Gustafsson, Jan Ake ^c   Russell, David W ^d   Cyster, Jason G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NOVARTIS PHARMA AG   (Switzerland)

^c University of Houston   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7ALPHA,25 DIHYDROXYCHOLESTEROL; CH25H ENZYME; CHOLESTEROL DERIVATIVE; CYTOCHROME P450; CYTOCHROME P450 7B1; HSD3B7 ENZYME; OXYGENASE; OXYSTEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL MOTILITY; CONTROLLED STUDY; DENDRITIC CELL; HUMORAL IMMUNITY; LYMPHOID CELL; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; T LYMPHOCYTE;

3-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; B-LYMPHOCYTES; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HEK293 CELLS; HUMANS; HYDROXYCHOLESTEROLS; IMMUNITY, HUMORAL; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, G-PROTEIN-COUPLED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEROID HYDROXYLASES; STROMAL CELLS;

EID: 84866518376     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.06.015     Document Type: Article

References (38)

1. Bauman D.R., Bitmansour A.D., McDonald J.G., Thompson B.M., Liang G., Russell D.W. 25-Hydroxycholesterol secreted by macrophages in response to Toll-like receptor activation suppresses immunoglobulin A production. Proc. Natl. Acad. Sci. USA 2009, 106:16764-16769.
2. Benned-Jensen T., Smethurst C., Holst P.J., Page K.R., Sauls H., Sivertsen B., Schwartz T.W., Blanchard A., Jepras R., Rosenkilde M.M. Ligand modulation of the Epstein-Barr virus-induced seven-transmembrane receptor EBI2: identification of a potent and efficacious inverse agonist. J. Biol. Chem. 2011, 286:29292-29302.
3. Bensinger S.J., Bradley M.N., Joseph S.B., Zelcer N., Janssen E.M., Hausner M.A., Shih R., Parks J.S., Edwards P.A., Jamieson B.D., Tontonoz P. LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 2008, 134:97-111.
4. Chan T.D., Gatto D., Wood K., Camidge T., Basten A., Brink R. Antigen affinity controls rapid T-dependent antibody production by driving the expansion rather than the differentiation or extrafollicular migration of early plasmablasts. J. Immunol. 2009, 183:3139-3149.
5. Coffey F., Alabyev B., Manser T. Initial clonal expansion of germinal center B cells takes place at the perimeter of follicles. Immunity 2009, 30:599-609.
6. Cyster J.G. B cell follicles and antigen encounters of the third kind. Nat. Immunol. 2010, 11:989-996.
7. Cyster J.G., Ansel K.M., Reif K., Ekland E.H., Hyman P.L., Tang H.L., Luther S.A., Ngo V.N. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 2000, 176:181-193.
8. Diczfalusy U., Olofsson K.E., Carlsson A.M., Gong M., Golenbock D.T., Rooyackers O., Fläring U., Björkbacka H. Marked upregulation of cholesterol 25-hydroxylase expression by lipopolysaccharide. J. Lipid Res. 2009, 50:2258-2264.
9. Gatto D., Paus D., Basten A., Mackay C.R., Brink R. Guidance of B cells by the orphan G protein-coupled receptor EBI2 shapes humoral immune responses. Immunity 2009, 31:259-269.
10. Gatto D., Wood K., Brink R. 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. 2011, 187:4621-4628.
11. Hannedouche S., Zhang J., Yi T., Shen W., Nguyen D., Pereira J.P., Guerini D., Baumgarten B.U., Roggo S., Wen B., et al. Oxysterols direct immune cell migration via EBI2. Nature 2011, 475:524-527.
12. Kalaany N.Y., Mangelsdorf D.J. LXRS and FXR: the yin and yang of cholesterol and fat metabolism. Annu. Rev. Physiol. 2006, 68:159-191.
13. Katakai T., Suto H., Sugai M., Gonda H., Togawa A., Suematsu S., Ebisuno Y., Katagiri K., Kinashi T., Shimizu A. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol. 2008, 181:6189-6200.
14. Kelly L.M., Pereira J.P., Yi T., Xu Y., Cyster J.G. EBI2 guides serial movements of activated B cells and ligand activity is detectable in lymphoid and nonlymphoid tissues. J. Immunol. 2011, 187:3026-3032.
15. Kerfoot S.M., Yaari G., Patel J.R., Johnson K.L., Gonzalez D.G., Kleinstein S.H., Haberman A.M. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011, 34:947-960.
16. Kitano M., Moriyama S., Ando Y., Hikida M., Mori Y., Kurosaki T., Okada T. Bcl6 protein expression shapes pre-germinal center B cell dynamics and follicular helper T cell heterogeneity. Immunity 2011, 34:961-972.
17. Li-Hawkins J., Lund E.G., Turley S.D., Russell D.W. Disruption of the oxysterol 7alpha-hydroxylase gene in mice. J. Biol. Chem. 2000, 275:16536-16542.
18. Link A., Vogt T.K., Favre S., Britschgi M.R., Acha-Orbea H., Hinz B., Cyster J.G., Luther S.A. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 2007, 8:1255-1265.
19. Liu C., Yang X.V., Wu J., Kuei C., Mani N.S., Zhang L., Yu J., Sutton S.W., Qin N., Banie H., et al. Oxysterols direct B-cell migration through EBI2. Nature 2011, 475:519-523.
20. Lund E.G., Kerr T.A., Sakai J., Li W.P., Russell D.W. cDNA cloning of mouse and human cholesterol 25-hydroxylases, polytopic membrane proteins that synthesize a potent oxysterol regulator of lipid metabolism. J. Biol. Chem. 1998, 273:34316-34327.
21. Miyake Y., Asano K., Kaise H., Uemura M., Nakayama M., Tanaka M. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell-associated antigens. J. Clin. Invest. 2007, 117:2268-2278.
22. Muppidi J.R., Arnon T.I., Bronevetsky Y., Veerapen N., Tanaka M., Besra G.S., Cyster J.G. Cannabinoid receptor 2 positions and retains marginal zone B cells within the splenic marginal zone. J. Exp. Med. 2011, 208:1941-1948.
23. Okada T., Miller M.J., Parker I., Krummel M.F., Neighbors M., Hartley S.B., O'Garra A., Cahalan M.D., Cyster J.G. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005, 3:e150.
24. Omoto Y., Lathe R., Warner M., Gustafsson J.A. Early onset of puberty and early ovarian failure in CYP7B1 knockout mice. Proc. Natl. Acad. Sci. USA 2005, 102:2814-2819.
25. Park K., Scott A.L. Cholesterol 25-hydroxylase production by dendritic cells and macrophages is regulated by type I interferons. J. Leukoc. Biol. 2010, 88:1081-1087.
26. Paus D., Phan T.G., Chan T.D., Gardam S., Basten A., Brink R. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 2006, 203:1081-1091.
27. Pereira J.P., Kelly L.M., Xu Y., Cyster J.G. EBI2 mediates B cell segregation between the outer and centre follicle. Nature 2009, 460:1122-1126.
28. Phan T.G., Green J.A., Gray E.E., Xu Y., Cyster J.G. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 2009, 10:786-793.
29. Reif K., Ekland E.H., Ohl L., Nakano H., Lipp M., Förster R., Cyster J.G. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature 2002, 416:94-99.
30. Rose K., Allan A., Gauldie S., Stapleton G., Dobbie L., Dott K., Martin C., Wang L., Hedlund E., Seckl J.R., et al. 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. 2001, 276:23937-23944.
31. Russell D.W. The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 2003, 72:137-174.
32. Schwarz M., Wright A.C., Davis D.L., Nazer H., Björkhem I., Russell D.W. The bile acid synthetic gene 3beta-hydroxy-Delta(5)-C(27)-steroid oxidoreductase is mutated in progressive intrahepatic cholestasis. J. Clin. Invest. 2000, 106:1175-1184.
33. Shea H.C., Head D.D., Setchell K.D., Russell D.W. Analysis of HSD3B7 knockout mice reveals that a 3alpha-hydroxyl stereochemistry is required for bile acid function. Proc. Natl. Acad. Sci. USA 2007, 104:11526-11533.
34. Steinman R.M., Pack M., Inaba K. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 1997, 156:25-37.
35. Stiles A.R., McDonald J.G., Bauman D.R., Russell D.W. CYP7B1: one cytochrome P450, two human genetic diseases, and multiple physiological functions. J. Biol. Chem. 2009, 284:28485-28489.
36. Villablanca E.J., Raccosta L., Zhou D., Fontana R., Maggioni D., Negro A., Sanvito F., Ponzoni M., Valentinis B., Bregni M., et al. Tumor-mediated liver X receptor-alpha activation inhibits CC chemokine receptor-7 expression on dendritic cells and dampens antitumor responses. Nat. Med. 2010, 16:98-105.
37. Wang X., Cho B., Suzuki K., Xu Y., Green J.A., An J., Cyster J.G. Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J. Exp. Med. 2011, 208:2497-2510.
38. Zou T., Garifulin O., Berland R., Boyartchuk V.L. Listeria monocytogenes infection induces prosurvival metabolic signaling in macrophages. Infect. Immun. 2011, 79:1526-1535.