Lymphotoxin-Dependent B Cell-FRC Crosstalk Promotes De Novo Follicle Formation and Antibody Production following Intestinal Helminth Infection

Cell Reports

Volumn 15, Issue 7, 2016, Pages 1527-1541

  Dubey, Lalit Kumar ^a   Lebon, Luc ^a   Mosconi, Ilaria ^a   Yang, Chen Ying ^c   Scandella, Elke ^b   Ludewig, Burkhard ^b   Luther, Sanjiv A ^c   Harris, Nicola L ^a  

^a EPFL   (Switzerland)

^b CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 4 RECEPTOR ALPHA; LYMPHOTOXIN ALPHA BETA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; LYMPHOTOXIN; LYMPHOTOXIN BETA RECEPTOR;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FIBROBLASTIC RETICULUM CELL; GERMINAL CENTER; HELMINTHIASIS; INFLAMMATION; INTESTINE LYMPHATIC TISSUE; LYMPH FOLLICLE; LYMPHADENOPATHY; LYMPHATIC DRAINAGE; MALE; MESENTERY LYMPH NODE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RETICULUM CELL; SIGNAL TRANSDUCTION; STROMA CELL; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; FIBROBLAST; HELIGMOSOMOIDES POLYGYRUS; IMMUNOLOGY; INTESTINE INFECTION; LYMPH NODE; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CELL PROLIFERATION; CHEMOKINE CCL19; FIBROBLASTS; HELMINTHIASIS; INTERLEUKIN-4 RECEPTOR ALPHA SUBUNIT; INTESTINAL DISEASES, PARASITIC; LYMPH NODES; LYMPHOTOXIN BETA RECEPTOR; LYMPHOTOXIN-ALPHA; MICE, INBRED C57BL; NEMATOSPIROIDES DUBIUS; SIGNAL TRANSDUCTION; STROMAL CELLS; T-LYMPHOCYTES;

EID: 84964951647     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.04.023     Document Type: Article

References (44)

1. Acton S.E., Farrugia A.J., Astarita J.L., Mourão-Sá D., Jenkins R.P., Nye E., Hooper S., van Blijswijk J., Rogers N.C., Snelgrove K.J., et al. Dendritic cells control fibroblastic reticular network tension and lymph node expansion. Nature 2014, 514:498-502.
2. Anthony R.M., Urban J.F., Alem F., Hamed H.A., Rozo C.T., Boucher J.-L., Van Rooijen N., Gause W.C. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 2006, 12:955-960.
3. Astarita J.L., Cremasco V., Fu J., Darnell M.C., Peck J.R., Nieves-Bonilla J.M., Song K., Kondo Y., Woodruff M.C., Gogineni A., et al. The CLEC-2-podoplanin axis controls the contractility of fibroblastic reticular cells and lymph node microarchitecture. Nat. Immunol. 2015, 16:75-84.
4. Bajénoff M., Germain R.N. B-cell follicle development remodels the conduit system and allows soluble antigen delivery to follicular dendritic cells. Blood 2009, 114:4989-4997.
5. Bethony J., Brooker S., Albonico M., Geiger S.M., Loukas A., Diemert D., Hotez P.J. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006, 367:1521-1532.
6. Chai Q., Onder L., Scandella E., Gil-Cruz C., Perez-Shibayama C., Cupovic J., Danuser R., Sparwasser T., Luther S.A., Thiel V., et al. Maturation of lymph node fibroblastic reticular cells from myofibroblastic precursors is critical for antiviral immunity. Immunity 2013, 38:1013-1024.
7. Cremasco V., Woodruff M.C., Onder L., Cupovic J., Nieves-Bonilla J.M., Schildberg F.A., Chang J., Cremasco F., Harvey C.J., Wucherpfennig K., et al. B cell homeostasis and follicle confines are governed by fibroblastic reticular cells. Nat. Immunol. 2014, 15:973-981.
8. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., Schopf L., Urban J.F. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 2004, 201:139-155.
9. Fletcher A.L., Lukacs-Kornek V., Reynoso E.D., Pinner S.E., Bellemare-Pelletier A., Curry M.S., Collier A.-R., Boyd R.L., Turley S.J. Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J. Exp. Med. 2010, 207:689-697.
10. Fletcher A.L., Malhotra D., Acton S.E., Lukacs-Kornek V., Bellemare-Pelletier A., Curry M., Armant M., Turley S.J. Reproducible isolation of lymph node stromal cells reveals site-dependent differences in fibroblastic reticular cells. Front. Immunol. 2011, 2:35.
11. Gonzalez M., Mackay F., Browning J.L., Kosco-Vilbois M.H., Noelle R.J. The sequential role of lymphotoxin and B cells in the development of splenic follicles. J. Exp. Med. 1998, 187:997-1007.
12. Grainger J.R., Smith K.A., Hewitson J.P., McSorley H.J., Harcus Y., Filbey K.J., Finney C.A.M., Greenwood E.J.D., Knox D.P., Wilson M.S., et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J. Exp. Med. 2010, 207:2331-2341.
13. Harris N.L. Advances in helminth immunology: optimism for future vaccine design?. Trends Parasitol. 2011, 27:288-293.
14. Heesters B.A., Myers R.C., Carroll M.C. Follicular dendritic cells: dynamic antigen libraries. Nat. Rev. Immunol. 2014, 14:495-504.
15. Hewitson J.P., Ivens A.C., Harcus Y., Filbey K.J., McSorley H.J., Murray J., Bridgett S., Ashford D., Dowle A.A., Maizels R.M. Secretion of protective antigens by tissue-stage nematode larvae revealed by proteomic analysis and vaccination-induced sterile immunity. PLoS Pathog. 2013, 9:e1003492.
16. Jarjour M., Jorquera A., Mondor I., Wienert S., Narang P., Coles M.C., Klauschen F., Bajénoff M. Fate mapping reveals origin and dynamics of lymph node follicular dendritic cells. J. Exp. Med. 2014, 211:1109-1122.
17. Katakai T., Hara T., Lee J.-H., Gonda H., Sugai M., Shimizu A. A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells and B cells. Int. Immunol. 2004, 16:1133-1142.
18. 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.
19. Ke M.-T., Fujimoto S., Imai T. SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction. Nat. Neurosci. 2013, 16:1154-1161.
20. King I.L., Mohrs M. IL-4-producing CD4+ T cells in reactive lymph nodes during helminth infection are T follicular helper cells. J. Exp. Med. 2009, 206:1001-1007.
21. Kumar V., Scandella E., Danuser R., Onder L., Nitschké M., Fukui Y., Halin C., Ludewig B., Stein J.V. Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin-dependent pathway. Blood 2010, 115:4725-4733.
22. León B., Ballesteros-Tato A., Browning J.L., Dunn R., Randall T.D., Lund F.E. Regulation of T(H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 2012, 13:681-690.
23. 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.
24. Lu T.T., Browning J.L. Role of the lymphotoxin/LIGHT system in the development and maintenance of reticular networks and vasculature in lymphoid tissues. Front. Immunol. 2014, 5:47.
25. Luther S.A., Bidgol A., Hargreaves D.C., Schmidt A., Xu Y., Paniyadi J., Matloubian M., Cyster J.G. Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J. Immunol. 2002, 169:424-433.
26. Massacand J.C., Stettler R.C., Meier R., Humphreys N.E., Grencis R.K., Marsland B.J., Harris N.L. Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function. Proc. Natl. Acad. Sci. USA 2009, 106:13968-13973.
27. McCoy K.D., Stoel M., Stettler R., Merky P., Fink K., Senn B.M., Schaer C., Massacand J., Odermatt B., Oettgen H.C., et al. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 2008, 4:362-373.
28. Mionnet C., Mondor I., Jorquera A., Loosveld M., Maurizio J., Arcangeli M.-L., Ruddle N.H., Nowak J., Aurrand-Lions M., Luche H., Bajénoff M. Identification of a new stromal cell type involved in the regulation of inflamed B cell follicles. PLoS Biol. 2013, 11:e1001672.
29. Mohrs M., Shinkai K., Mohrs K., Locksley R.M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 2001, 15:303-311.
30. Morimoto M., Morimoto M., Whitmire J., Xiao S., Anthony R.M., Mirakami H., Star R.A., Urban J.F., Gause W.C. Peripheral CD4 T cells rapidly accumulate at the host: parasite interface during an inflammatory Th2 memory response. J. Immunol. 2004, 172:2424-2430.
31. Mosconi I., Dubey L.K., Volpe B., Esser-von Bieren J., Zaiss M.M., Lebon L., Massacand J.C., Harris N.L. Parasite proximity drives the expansion of regulatory T cells in Peyer's patches following intestinal helminth infection. Infect. Immun. 2015, 83:3657-3665.
32. Mueller S.N., Germain R.N. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 2009, 9:618-629.
33. Mulu A., Anagaw B., Gelaw A., Ota F., Kassu A., Yifru S. Effect of deworming on Th2 immune response during HIV-helminths co-infection. J. Transl. Med. 2015, 13:236.
34. Roozendaal R., Mebius R.E. Stromal cell-immune cell interactions. Annu. Rev. Immunol. 2011, 29:23-43.
35. Roozendaal R., Mempel T.R., Pitcher L.A., Gonzalez S.F., Verschoor A., Mebius R.E., von Andrian U.H., Carroll M.C. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009, 30:264-276.
36. Salgame P., Yap G.S., Gause W.C. Effect of helminth-induced immunity on infections with microbial pathogens. Nat. Immunol. 2013, 14:1118-1126.
37. Schneider K., Potter K.G., Ware C.F. Lymphotoxin and LIGHT signaling pathways and target genes. Immunol. Rev. 2004, 202:49-66.
38. Siegert S., Luther S.A. Positive and negative regulation of T cell responses by fibroblastic reticular cells within paracortical regions of lymph nodes. Front. Immunol. 2012, 3:285.
39. Sixt M., Kanazawa N., Selg M., Samson T., Roos G., Reinhardt D.P., Pabst R., Lutz M.B., Sorokin L. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005, 22:19-29.
40. Urban J.F., Noben-Trauth N., Donaldson D.D., Madden K.B., Morris S.C., Collins M., Finkelman F.D. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 1998, 8:255-264.
41. 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.
42. Wojciechowski W., Harris D.P., Sprague F., Mousseau B., Makris M., Kusser K., Honjo T., Mohrs K., Mohrs M., Randall T., Lund F.E. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 2009, 30:421-433.
43. Yang C.-Y., Vogt T.K., Favre S., Scarpellino L., Huang H.-Y., Tacchini-Cottier F., Luther S.A. Trapping of naive lymphocytes triggers rapid growth and remodeling of the fibroblast network in reactive murine lymph nodes. Proc. Natl. Acad. Sci. USA 2014, 111:E109-E118.
44. Zeng M., Smith A.J., Wietgrefe S.W., Southern P.J., Schacker T.W., Reilly C.S., Estes J.D., Burton G.F., Silvestri G., Lifson J.D., et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J. Clin. Invest. 2011, 121:998-1008.