Endocytosis and Recycling of Immune Complexes by Follicular Dendritic Cells Enhances B Cell Antigen Binding and Activation

Immunity

Volumn 38, Issue 6, 2013, Pages 1164-1175

  Heesters, BalthasarA ^a,c   Chatterjee, Priyadarshini ^a   Kim, Young A ^a   Gonzalez, SantiagoF ^a   Kuligowski, MichaelP ^a   Kirchhausen, Tomas ^a,b   Carroll, MichaelC ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT COMPONENT C3D RECEPTOR;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL SURFACE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FLOW CYTOMETRY; FOLLICULAR DENDRITIC CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ACTINS; ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS; B-LYMPHOCYTES; CELLS, CULTURED; DENDRITIC CELLS, FOLLICULAR; ENDOCYTOSIS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; PROTEIN BINDING; RECEPTORS, COMPLEMENT 3B; RECEPTORS, COMPLEMENT 3D;

EID: 84879606860     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.02.023     Document Type: Article

References (43)

1. Alimzhanov M.B., Kuprash D.V., Kosco-Vilbois M.H., Luz A., Turetskaya R.L., Tarakhovsky A., Rajewsky K., Nedospasov S.A., Pfeffer K. Abnormal development of secondary lymphoid tissues in lymphotoxin beta-deficient mice. Proc. Natl. Acad. Sci. USA 1997, 94:9302-9307.
2. 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.
3. Bergtold A., Desai D.D., Gavhane A., Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 2005, 23:503-514.
4. Boulant S., Kural C., Zeeh J.C., Ubelmann F., Kirchhausen T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13:1124-1131.
5. Burton G.F., Kosco M.H., Szakal A.K., Tew J.G. Iccosomes and the secondary antibody response. Immunology 1991, 73:271-276.
6. Casella J.F., Flanagan M.D., Lin S. Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 1981, 293:302-305.
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. El Shikh M.E., El Sayed R., Szakal A.K., Tew J.G. Follicular dendritic cell (FDC)-FcgammaRIIB engagement via immune complexes induces the activated FDC phenotype associated with secondary follicle development. Eur. J. Immunol. 2006, 36:2715-2724.
9. Endres R., Alimzhanov M.B., Plitz T., Fütterer A., Kosco-Vilbois M.H., Nedospasov S.A., Rajewsky K., Pfeffer K. Mature follicular dendritic cell networks depend on expression of lymphotoxin beta receptor by radioresistant stromal cells and of lymphotoxin beta and tumor necrosis factor by B cells. J.Exp. Med. 1999, 189:159-168.
10. Fang Y., Xu C., Fu Y.X., Holers V.M., Molina H. Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J.Immunol. 1998, 160:5273-5279.
11. Fischer M.B., Goerg S., Shen L., Prodeus A.P., Goodnow C.C., Kelsoe G., Carroll M.C. Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science 1998, 280:582-585.
12. Fu Y.X., Molina H., Matsumoto M., Huang G., Min J., Chaplin D.D. Lymphotoxin-alpha (LTalpha) supports development of splenic follicular structure that is required for IgG responses. J.Exp. Med. 1997, 185:2111-2120.
13. Garin A., Meyer-Hermann M., Contie M., Figge M.T., Buatois V., Gunzer M., Toellner K.M., Elson G., Kosco-Vilbois M.H. Toll-like receptor 4 signaling by follicular dendritic cells is pivotal for germinal center onset and affinity maturation. Immunity 2010, 33:84-95.
14. Gommerman J.L., Mackay F., Donskoy E., Meier W., Martin P., Browning J.L. Manipulation of lymphoid microenvironments in nonhuman primates by an inhibitor of the lymphotoxin pathway. J.Clin. Invest. 2002, 110:1359-1369.
15. 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.
16. Gonzalez S.F., Lukacs-Kornek V., Kuligowski M.P., Pitcher L.A., Degn S.E., Kim Y.A., Cloninger M.J., Martinez-Pomares L., Gordon S., Turley S.J., Carroll M.C. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 2010, 11:427-434.
17. Hanna M.G., Szakal A.K. Localization of 125I-labeled antigen in germinal centers of mouse spleen: histologic and ultrastructural autoradiographic studies of the secondary immune reaction. J.Immunol. 1968, 101:949-962.
18. Kelsoe G. Life and death in germinal centers (redux). Immunity 1996, 4:107-111.
19. Kinoshita T., Fujita T., Tsunoda R. Expression of Complement Receptors CR1 and CR2 on Murine Follicular Dendritic Cells and B Lymphocytes 1991, Volume 2. Elsevier, Amsterdam.
20. Kosco M.H., Monfalcone A.P., Szakal A.K., Tew J.G. Germinal center B cells present antigen obtained invivo to Tcells invitro and stimulate mixed lymphocyte reactions. Adv. Exp. Med. Biol. 1988, 237:883-888.
21. Kranich J., Krautler N.J., Heinen E., Polymenidou M., Bridel C., Schildknecht A., Huber C., Kosco-Vilbois M.H., Zinkernagel R., Miele G., Aguzzi A. Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J.Exp. Med. 2008, 205:1293-1302.
22. Krautler N.J., Kana V., Kranich J., Tian Y., Perera D., Lemm D., Schwarz P., Armulik A., Browning J.L., Tallquist M., et al. Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell 2012, 150:194-206.
23. Lam K.P., Rajewsky K. B cell antigen receptor specificity and surface density together determine B-1 versus B-2 cell development. J.Exp. Med. 1999, 190:471-477.
24. MacLennan I.C. Germinal centers. Annu. Rev. Immunol. 1994, 12:117-139.
25. Mandel T.E., Phipps R.P., Abbot A., Tew J.G. The follicular dendritic cell: long term antigen retention during immunity. Immunol. Rev. 1980, 53:29-59.
26. Matsumoto M., Lo S.F., Carruthers C.J.L., Min J., Mariathasan S., Huang G., Plas D.R., Martin S.M., Geha R.S., Nahm M.H., Chaplin D.D. Affinity maturation without germinal centres in lymphotoxin-alpha-deficient mice. Nature 1996, 382:462-466.
27. May J.A., Ratan H., Glenn J.R., Lösche W., Spangenberg P., Heptinstall S. GPIIb-IIIa antagonists cause rapid disaggregation of platelets pre-treated with cytochalasin D. Evidence that the stability of platelet aggregates depends on normal cytoskeletal assembly. Platelets 1998, 9:227-232.
28. Nimmerjahn F., Ravetch J.V. Fcgamma receptors: old friends and new family members. Immunity 2006, 24:19-28.
29. Nossal G.J., Abbot A., Mitchell J., Lummus Z. Antigens in immunity. XV. Ultrastructural features of antigen capture in primary and secondary lymphoid follicles. J.Exp. Med. 1968, 127:277-290.
30. Pasparakis M., Alexopoulou L., Episkopou V., Kollias G. Immune and inflammatory responses in TNF alpha-deficient mice: a critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, and in the maturation of the humoral immune response. J.Exp. Med. 1996, 184:1397-1411.
31. Phan T.G., Grigorova I., Okada T., Cyster J.G. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 2007, 8:992-1000.
32. 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.
33. Qi H., Egen J.G., Huang A.Y., Germain R.N. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science 2006, 312:1672-1676.
34. Qin D., Wu J., Vora K.A., Ravetch J.V., Szakal A.K., Manser T., Tew J.G. Fc gamma receptor IIB on follicular dendritic cells regulates the B cell recall response. J.Immunol. 2000, 164:6268-6275.
35. Roozendaal R., Carroll M.C. Complement receptors CD21 and CD35 in humoral immunity. Immunol. Rev. 2007, 219:157-166.
36. 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.
37. Shokat K.M., Goodnow C.C. Antigen-induced B-cell death and elimination during germinal-centre immune responses. Nature 1995, 375:334-338.
38. Suzuki K., Grigorova I., Phan T.G., Kelly L.M., Cyster J.G. Visualizing B cell capture of cognate antigen from follicular dendritic cells. J.Exp. Med. 2009, 206:1485-1493.
39. Szakal A.K., Kosco M.H., Tew J.G. A novel invivo follicular dendritic cell-dependent iccosome-mediated mechanism for delivery of antigen to antigen-processing cells. J.Immunol. 1988, 140:341-353.
40. Taylor P.R., Pickering M.C., Kosco-Vilbois M.H., Walport M.J., Botto M., Gordon S., Martinez-Pomares L. The follicular dendritic cell restricted epitope, FDC-M2, is complement C4; localization of immune complexes in mouse tissues. Eur. J. Immunol. 2002, 32:1888-1896.
41. Tew J.G., Kosco M.H., Burton G.F., Szakal A.K. Follicular dendritic cells as accessory cells. Immunol. Rev. 1990, 117:185-211.
42. 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.
43. Wu Y., El Shikh M.E., El Sayed R.M., Best A.M., Szakal A.K., Tew J.G. IL-6 produced by immune complex-activated follicular dendritic cells promotes germinal center reactions, IgG responses and somatic hypermutation. Int. Immunol. 2009, 21:745-756.