Skin dendritic cells induce follicular helper T cells and protective humoral immune responses

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 5, 2015, Pages 1387-1397.e7

  Yao, Chen ^a   Zurawski, Sandra M ^c   Jarrett, Elizabeth S ^a   Chicoine, Brian ^a   Crabtree, Juliet ^b   Peterson, Erik J ^b   Zurawski, Gerard ^c   Kaplan, Daniel H ^a   Igyártó, Botond Z ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

protective humoral immune responses; skin dendritic cells; Steady state conditions; T follicular helper cells

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON RECEPTOR; CD103 ANTIGEN; CD38 ANTIGEN; CD45 ANTIGEN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; THY 1 ANTIGEN; ALPHA E INTEGRINS; ALPHA INTEGRIN; BLR1 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CXCR5; INFLUENZA VACCINE; INTERFERON RECEPTOR; LEUKOCYTE ANTIGEN; PROTEIN BCL 6; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CD4+ T LYMPHOCYTE; DENDRITIC CELL; GERMINAL CENTER; HUMORAL IMMUNITY; LANGERHANS CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; TFH CELL; VIRUS LOAD; ANIMAL; C57BL MOUSE; FEMALE; GENETICS; HELPER CELL; IMMUNIZATION; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD; ANTIGENS, VIRAL; B-LYMPHOCYTES; DENDRITIC CELLS; FEMALE; IMMUNITY, HUMORAL; IMMUNIZATION; INFLUENZA VACCINES; INTEGRIN ALPHA CHAINS; INTERLEUKIN-6; LANGERHANS CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS C-BCL-6; RECEPTORS, CXCR5; RECEPTORS, INTERFERON; SKIN; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84928958293     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.04.001     Document Type: Article

References (39)

1. Merad, M., Sathe, P., Helft, J., Miller, J., Mortha, A., The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31 (2013), 563–604.
2. Steinman, R.M., Hawiger, D., Nussenzweig, M.C., Tolerogenic dendritic cells. Annu Rev Immunol 21 (2003), 685–711.
3. Igyártó B.Z., Haley, K., Ortner, D., Bobr, A., Gerami-Nejad, M., Edelson, B.T., et al. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35 (2011), 260–272.
4. Bedoui, S., Whitney, P.G., Waithman, J., Eidsmo, L., Wakim, L., Caminschi, I., et al. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol 10 (2009), 488–495.
5. Flacher, V., Tripp, C.H., Mairhofer, D.G., Steinman, R.M., Stoitzner, P., Idoyaga, J., et al. Murine Langerin+ dermal dendritic cells prime CD8+ T cells while Langerhans cells induce cross-tolerance. EMBO Mol Med 6 (2014), 1191–1204.
6. Henri, S., Poulin, L.F., Tamoutounour, S., Ardouin, L., Guilliams, M., de Bovis, B., et al. CD207+ CD103+ dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 207 (2010), 189–206.
7. Kaplan, D.H., In vivo function of Langerhans cells and dermal dendritic cells. Trends Immunol 31 (2010), 446–451.
8. Gomez de Agüero, M., Vocanson, M., Hacini-Rachinel, F., Taillardet, M., Sparwasser, T., Kissenpfennig, A., et al. Langerhans cells protect from allergic contact dermatitis in mice by tolerizing CD8(+) T cells and activating Foxp3(+) regulatory T cells. J Clin Invest 122 (2012), 1700–1711.
9. Shklovskaya, E., O'Sullivan, B.J., Ng, L.G., Roediger, B., Thomas, R., Weninger, W., et al. Langerhans cells are precommitted to immune tolerance induction. Proc Natl Acad Sci U S A 108 (2011), 18049–18054.
10. Kautz-Neu, K., Noordegraaf, M., Dinges, S., Bennett, C.L., John, D., Clausen, B.E., et al. Langerhans cells are negative regulators of the anti-Leishmania response. J Exp Med 208 (2011), 885–891.
11. Ouchi, T., Kubo, A., Yokouchi, M., Adachi, T., Kobayashi, T., Kitashima, D.Y., et al. Langerhans cell antigen capture through tight junctions confers preemptive immunity in experimental staphylococcal scalded skin syndrome. J Exp Med 208 (2011), 2607–2613.
12. Idoyaga, J., Fiorese, C., Zbytnuik, L., Lubkin, A., Miller, J., Malissen, B., et al. Specialized role of migratory dendritic cells in peripheral tolerance induction. J Clin Invest 123 (2013), 844–854.
13. Bonifaz, L., Bonnyay, D., Mahnke, K., Rivera, M., Nussenzweig, M.C., Steinman, R.M., Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 196 (2002), 1627–1638.
14. Moon, J.J., Chu, H.H., Pepper, M., McSorley, S.J., Jameson, S.C., Kedl, R.M., et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27 (2007), 203–213.
15. Bobr, A., Olvera-Gomez, I., Igyártó B.Z., Haley, K.M., Hogquist, K.A., Kaplan, D.H., Acute ablation of Langerhans cells enhances skin immune responses. J Immunol 185 (2010), 4724–4728.
16. Igyártó B.Z., Jenison, M.C., Dudda, J.C., Roers, A., Müller, W., Koni, P.A., et al. Langerhans cells suppress contact hypersensitivity responses via cognate CD4 interaction and langerhans cell-derived IL-10. J Immunol 183 (2009), 5085–5093.
17. Edelson, B.T., KC, W., Juang, R., Kohyama, M., Benoit, L.A., Klekotka, P.A., et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 207 (2010), 823–836.
18. Grubin, C.E., Kovats, S., deRoos, P., Rudensky, A.Y., Deficient positive selection of CD4 T cells in mice displaying altered repertoires of MHC class II-bound self-peptides. Immunity 7 (1997), 197–208.
19. Flamar, A.L., Zurawski, S., Scholz, F., Gayet, I., Ni, L., Li, X.H., et al. Noncovalent assembly of anti-dendritic cell antibodies and antigens for evoking immune responses in vitro and in vivo. J Immunol 189 (2012), 2645–2655.
20. Idoyaga, J., Cheong, C., Suda, K., Suda, N., Kim, J.Y., Lee, H., et al. Cutting edge: langerin/CD207 receptor on dendritic cells mediates efficient antigen presentation on MHC I and II products in vivo. J Immunol 180 (2008), 3647–3650.
21. Flacher, V., Tripp, C.H., Stoitzner, P., Haid, B., Ebner, S., Del Frari, B., et al. Epidermal Langerhans cells rapidly capture and present antigens from C-type lectin-targeting antibodies deposited in the dermis. J Invest Dermatol 130 (2010), 755–762.
22. Kaplan, D.H., Jenison, M.C., Saeland, S., Shlomchik, W.D., Shlomchik, M.J., Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23 (2005), 611–620.
23. Kaplan, D.H., Li, M.O., Jenison, M.C., Shlomchik, W.D., Flavell, R.A., Shlomchik, M.J., Autocrine/paracrine TGFbeta1 is required for the development of epidermal Langerhans cells. J Exp Med 204 (2007), 2545–2552.
24. Tubo, N.J., Pagán, A.J., Taylor, J.J., Nelson, R.W., Linehan, J.L., Ertelt, J.M., et al. Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection. Cell 153 (2013), 785–796.
25. Crotty, S., Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29 (2011), 621–663.
26. Tangye, S.G., Ma, C.S., Brink, R., Deenick, E.K., The good, the bad and the ugly—TFH cells in human health and disease. Nat Rev Immunol 13 (2013), 412–426.
27. Baumjohann, D., Preite, S., Reboldi, A., Ronchi, F., Ansel, K.M., Lanzavecchia, A., et al. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38 (2013), 596–605.
28. Deenick, E.K., Chan, A., Ma, C.S., Gatto, D., Schwartzberg, P.L., Brink, R., et al. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33 (2010), 241–253.
29. Ballesteros-Tato, A., Randall, T.D., Priming of T follicular helper cells by dendritic cells. Immunol Cell Biol 92 (2014), 22–27.
30. de Witte, L., Nabatov, A., Pion, M., Fluitsma, D., de Jong, M.A., de Gruijl, T., et al. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 13 (2007), 367–371.
31. Lahoud, M.H., Ahmet, F., Kitsoulis, S., Wan, S.S., Vremec, D., Lee, C.N., et al. Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J Immunol 187 (2011), 842–850.
32. Choi, Y.S., Yang, J.A., Crotty, S., Dynamic regulation of Bcl6 in follicular helper CD4 T (Tfh) cells. Curr Opin Immunol 25 (2013), 366–372.
33. Choi, Y.S., Kageyama, R., Eto, D., Escobar, T.C., Johnston, R.J., Monticelli, L., et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34 (2011), 932–946.
34. Cai, G., Nie, X., Zhang, W., Wu, B., Lin, J., Wang, H., et al. A regulatory role for IL-10 receptor signaling in development and B cell help of T follicular helper cells in mice. J Immunol 189 (2012), 1294–1302.
35. Goenka, R., Barnett, L.G., Silver, J.S., O'Neill, P.J., Hunter, C.A., Cancro, M.P., et al. Cutting edge: dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J Immunol 187 (2011), 1091–1095.
36. Ma, C.S., Deenick, E.K., Batten, M., Tangye, S.G., The origins, function, and regulation of T follicular helper cells. J Exp Med 209 (2012), 1241–1253.
37. Barnett, L.G., Simkins, H.M., Barnett, B.E., Korn, L.L., Johnson, A.L., Wherry, E.J., et al. B cell antigen presentation in the initiation of follicular helper T cell and germinal center differentiation. J Immunol 192 (2014), 3607–3617.
38. Nagao, K., Ginhoux, F., Leitner, W.W., Motegi, S., Bennett, C.L., Clausen, B.E., et al. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci U S A 106 (2009), 3312–3317.
39. Romani, N., Flacher, V., Tripp, C.H., Sparber, F., Ebner, S., Stoitzner, P., Targeting skin dendritic cells to improve intradermal vaccination. Curr Top Microbiol Immunol 351 (2012), 113–138.