B cell homeostasis and follicle confines are governed by fibroblastic reticular cells

Nature Immunology

Volumn 15, Issue 10, 2014, Pages 973-981

  Cremasco, Viviana ^a   Woodruff, Matthew C ^b,c   Onder, Lucas ^d   Cupovic, Jovana ^d   Nieves Bonilla, Janice M ^a   Schildberg, Frank A ^a   Chang, Jonathan ^a,c   Cremasco, Floriana ^a,e   Harvey, Christopher J ^a   Wucherpfennig, Kai ^a   Ludewig, Burkhard ^d   Carroll, Michael C ^b,c   Turley, Shannon J ^a,c,f  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^e UNIVERSITY OF MILAN   (Italy)

^f GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; PHOTOPROTEIN; TNFSF13B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FIBROBLAST; HOMEOSTASIS; HUMORAL IMMUNITY; LYMPHOCYTE SUBPOPULATION; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; RETICULUM CELL; T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CELL SURVIVAL; CONFOCAL MICROSCOPY; DENDRITIC CELL; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; LYMPH NODE; MALE; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; DENDRITIC CELLS; FIBROBLASTS; FLOW CYTOMETRY; HOMEOSTASIS; IMMUNITY, HUMORAL; LUMINESCENT PROTEINS; LYMPH NODES; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; T-LYMPHOCYTES;

EID: 84922014960     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2965     Document Type: Article

References (44)

1. Mueller, S.N. & Germain, R.N. Stromal cell contributions to the homeostasis and functionality of the immune system. Nat. Rev. Immunol. 9, 618-629 (2009).
2. Turley, S.J., Fletcher, A.L. & Elpek, K.G. The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat. Rev. Immunol. 10, 813-825 (2010).
3. Gretz, J.E., Norbury, C.C., Anderson, A.O., Proudfoot, A.E. & Shaw, S. 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, 1425-1440 (2000).
4. Roozendaal, R. et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 30, 264-276 (2009).
5. Sixt, M. et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 22, 19-29 (2005).
6. Acton, S.E. et al. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 37, 276-289 (2012).
7. Astarita, J.L., Acton, S.E. & Turley, S.J. Podoplanin: emerging functions in development, the immune system, and cancer. Front. Immunol. 3, 283 (2012).
8. Malhotra, D. et al. Transcriptional profling of stroma from infamed and resting lymph nodes defnes immunological hallmarks. Nat. Immunol. 13, 499-510 (2012).
9. Link, A. et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8, 1255-1265 (2007).
10. Khan, O. et al. Regulation of T cell priming by lymphoid stroma. PLoS ONE 6, e26138 (2011).
11. Lukacs-Kornek, V. et al. Regulated release of nitric oxide by nonhematopoietic stroma controls expansion of the activated T cell pool in lymph nodes. Nat. Immunol. 12, 1096-1104 (2011).
12. Siegert, S. et al. Fibroblastic reticular cells from lymph nodes attenuate T cell expansion by producing nitric oxide. PLoS ONE 6, e27618 (2011).
13. Cyster, J.G. B cell follicles and antigen encounters of the third kind. Nat. Immunol. 11, 989-996 (2010).
14. Cyster, J.G. et al. Follicular stromal cells and lymphocyte homing to follicles. Immunol. Rev. 176, 181-193 (2000).
15. Roozendaal, R. & Carroll, M.C. Complement receptors CD21 and CD35 in humoral immunity. Immunol. Rev. 219, 157-166 (2007).
16. Tew, J.G., Kosco, M.H., Burton, G.F. & Szakal, A.K. Follicular dendritic cells as accessory cells. Immunol. Rev. 117, 185-211 (1990).
17. Wang, X. et al. Follicular dendritic cells help establish follicle identity and promote B cell retention in germinal centers. J. Exp. Med. 208, 2497-2510 (2011).
18. Katakai, T. et al. Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J. Immunol. 181, 6189-6200 (2008).
19. Chai, Q. et al. Maturation of lymph node fbroblastic reticular cells from myofbroblastic precursors is critical for antiviral immunity. Immunity 38, 1013-1024 (2013).
20. Katakai, T. Marginal reticular cells: a stromal subset directly descended from the lymphoid tissue organizer. Front. Immunol. 3, 200 (2012).
21. Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419-426 (2005).
22. Fletcher, A.L. et al. Reproducible isolation of lymph node stromal cells reveals site-dependent differences in fbroblastic reticular cells. Front. Immunol. 2, 35 (2011).
23. Cervantes-Barragan, L. et al. Dendritic cell-specifc antigen delivery by coronavirus vaccine vectors induces long-lasting protective antiviral and antitumor immunity. mBio 1, 4 (2010).
24. Cupovic, J. Low Avidity CD8+ T cells In Viral Infection from Neuroinfammation to Adoptive T Cell Therapy. PhD thesis, Eidgenössische Technische Hochschule Zürich (2014).
25. Gonzalez, S.F. et al. Capture of infuenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 11, 427-434 (2010).
26. Chyou, S. et al. Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J. Immunol. 181, 3887-3896 (2008).
27. Okada, T. et al. Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J. Exp. Med. 196, 65-75 (2002).
28. Mackay, F. & Browning, J.L. BAFF: a fundamental survival factor for B cells. Nat. Rev. Immunol. 2, 465-475 (2002).
29. Mackay, F. et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190, 1697-1710 (1999).
30. Gorelik, L. et al. Normal B cell homeostasis requires B cell activation factor production by radiation-resistant cells. J. Exp. Med. 198, 937-945 (2003).
31. Garin, A. et al. Toll-like receptor 4 signaling by follicular dendritic cells is pivotal for germinal center onset and affnity maturation. Immunity 33, 84-95 (2010).
32. Gonzalez, S.F. et al. Traffcking of B cell antigen in lymph nodes. Annu. Rev. Immunol. 29, 215-233 (2011).
33. Bajénoff, M. & Germain, R.N. B-cell follicle development remodels the conduit system and allows soluble antigen delivery to follicular dendritic cells. Blood 114, 4989-4997 (2009).
34. Alimzhanov, M.B. et al. Abnormal development of secondary lymphoid tissues in lymphotoxin beta-defcient mice. Proc. Natl. Acad. Sci. USA 94, 9302-9307 (1997).
35. + follicular dendritic cells but dissipate prematurely. J. Immunol. 191, 4521-4530 (2013).
36. Browning, J.L. et al. Lymphotoxin-β receptor signaling is required for the homeostatic control of HEV differentiation and function. Immunity 23, 539-550 (2005).
37. Koni, P.A. et al. Distinct roles in lymphoid organogenesis for lymphotoxins α and β revealed in lymphotoxin β-defcient mice. Immunity 6, 491-500 (1997).
38. Mebius, R.E. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3, 292-303 (2003).
39. Jarjour, M. et al. Fate mapping reveals origin and dynamics of lymph node follicular dendritic cells. J. Exp. Med. 211, 1109-1122 (2014).
40. Yang, C.Y. et al. Trapping of naive lymphocytes triggers rapid growth and remodeling of the fbroblast network in reactive murine lymph nodes. Proc. Natl. Acad. Sci. USA 111, E109-E118 (2014).
41. Junt, T., Scandella, E. & Ludewig, B. Form follows function: lymphoid tissue microarchitecture in antimicrobial immune defence. Nat. Rev. Immunol. 8, 764-775 (2008).
42. Koning, J.J. & Mebius, R.E. Interdependence of stromal and immune cells for lymph node function. Trends Immunol. 33, 264-270 (2012).
43. Malhotra, D., Fletcher, A.L. & Turley, S.J. Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol. Rev. 251, 160-176 (2013).
44. Scandella, E. et al. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 9, 667-675 (2008).