Migratory CD11b+ conventional dendritic cells induce T follicular helper cell–dependent antibody responses

Science Immunology

Volumn 2, Issue 18, 2017, Pages

  Krishnaswamy, Jayendra Kumar ^a,b   Gowthaman, Uthaman ^a   Zhang, Biyan ^a   Mattsson, Johan ^b   Szeponik, Louis ^c   Liu, Dong ^a   Wu, Renee ^a,d   White, Theresa ^a   Calabro, Samuele ^a,e   Xu, Lan ^a   Collet, Magalie A ^f   Yurieva, Marina ^f   Alsén, Samuel ^c   Fogelstrand, Per ^g   Walter, Anne ^h   Heath, William R ^h   Mueller, Scott N ^h   Yrlid, Ulf ^c   Williams, Adam ^f,i   Eisenbarth, Stephanie C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ASTRAZENECA R AND D   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Roche Innovation Center Zurich   (Switzerland)

^f JACKSON LABORATORY   (United States)

^g UNIVERSITY OF GOTHENBURG   (Sweden)

^h UNIVERSITY OF MELBOURNE   (Australia)

ⁱ UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD11B ANTIGEN; REPRESSOR PROTEIN; SNFT PROTEIN, MOUSE;

ANIMAL; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DEFICIENCY; DENDRITIC CELL; FEMALE; HELPER CELL; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CD11B ANTIGEN; CELL PROLIFERATION; DENDRITIC CELLS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; REPRESSOR PROTEINS; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 85043728143     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aam9169     Document Type: Article

References (55)

1. R. T. Kenney, S. A. Frech, L. R. Muenz, C. P. Villar, G. M. Glenn, Dose sparing with intradermal injection of influenza vaccine. N. Engl. J. Med. 351, 2295–2301 (2004).
2. S. Crotty, T follicular helper cell differentiation, function, and roles in disease. Immunity 41, 529–542 (2014).
3. C. G. Vinuesa, M. A. Linterman, D. Yu, I. C. M. MacLennan, Follicular helper T cells. Annu. Rev. Immunol. 34, 335–368 (2016).
4. M. W. Dahlgren, T. Gustafsson-Hedberg, M. Livingston, H. Cucak, S. Alsén, U. Yrlid, B. Johansson-Lindbom, T follicular helper, but not Th1, cell differentiation in the absence of conventional dendritic cells. J. Immunol. 194, 5187–5199 (2015).
5. R. Goenka, L. G. Barnett, J. S. Silver, P. J. O’Neill, C. A. Hunter, M. P. Cancro, T. M. Laufer, Cutting edge: Dendritic cell-restricted antigen presentation initiates the follicular helper T cell program but cannot complete ultimate effector differentiation. J. Immunol. 187, 1091–1095 (2011).
6. A. Ballesteros-Tato, T. D. Randall, Priming of T follicular helper cells by dendritic cells. Immunol. Cell Biol. 92, 22–27 (2014).
7. V. Durai, K. M. Murphy, Functions of murine dendritic cells. Immunity 45, 719–736 (2016).
8. S. Calabro, A. Gallman, U. Gowthaman, D. Liu, P. Chen, J. Liu, J. K. Krishnaswamy, M. S. L. Nascimento, L. Xu, S. R. Patel, A. Williams, C. A. Tormey, E. A. Hod, S. L. Spitalnik, J. C. Zimring, J. E. Hendrickson, S. R. Stowell, S. C. Eisenbarth, Bridging channel dendritic cells induce immunity to transfused red blood cells. J. Exp. Med. 213, 887–896 (2016).
9. J. Li, E. Lu, T. Yi, J. G. Cyster, EBI2 augments Tfh cell fate by promoting interaction with IL-2-quenching dendritic cells. Nature 533, 110–114 (2016).
10. M. H. Lahoud, F. Ahmet, S. Kitsoulis, S. S. Wan, D. Vremec, C.-N. Lee, B. Phipson, W. Shi, G. K. Smyth, A. M. Lew, Y. Kato, S. N. Mueller, G. M. Davey, W. R. Heath, K. Shortman, I. Caminschi, Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J. Immunol. 187, 842–850 (2011).
11. − dendritic cells induce antigen-specific T follicular helper cells generating efficient humoral immune responses. Cell Rep. 11, 1929–1940 (2015).
12. C. Yao, S. M. Zurawski, E. S. Jarrett, B. Chicoine, J. Crabtree, E. J. Peterson, G. Zurawski, D. H. Kaplan, B. Z. Igyártó, Skin dendritic cells induce follicular helper T cells and protective humoral immune responses. J. Allergy Clin. Immunol. 136, 1387–1397.e7 (2015).
13. M. Y. Gerner, P. Torabi-Parizi, R. N. Germain, Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. Immunity 42, 172–185 (2015).
14. + dendritic cells suppress T follicular helper cells and antibody responses to protein antigens. Elife 5, e17979 (2016).
15. M. C. Woodruff, B. A. Heesters, C. N. Herndon, J. R. Groom, P. G. Thomas, A. D. Luster, S. J. Turley, M. C. Carroll, Trans-nodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine. J. Exp. Med. 211, 1611–1621 (2014).
16. N. Anandasabapathy, R. Feder, S. Mollah, S.-W. Tse, M. P. Longhi, S. Mehandru, I. Matos, C. Cheong, D. Ruane, L. Brane, A. Teixeira, J. Dobrin, O. Mizenina, C. G. Park, M. Meredith, B. E. Clausen, M. C. Nussenzweig, R. M. Steinman, Classical Flt3L-dependent dendritic cells control immunity to protein vaccine. J. Exp. Med. 211, 1875–1891 (2014).
17. A. A. Itano, S. J. McSorley, R. L. Reinhardt, B. D. Ehst, E. Ingulli, A. Y. Rudensky, M. K. Jenkins, Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19, 47–57 (2003).
18. C. Levin, O. Bonduelle, C. Nuttens, C. Primard, B. Verrier, A. Boissonnas, B. Combadière, Critical role for skin-derived migratory DCs and Langerhans cells in TFH and GC responses after intradermal immunization. J. Invest. Dermatol. 137, 1905–1913 (2017).
19. L. Ohl, M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, R. Förster, CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21, 279–288 (2004).
20. H. Tang, W. Cao, S. P. Kasturi, R. Ravindran, H. I. Nakaya, K. Kundu, N. Murthy, T. B. Kepler, B. Malissen, B. Pulendran, The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11, 608–617 (2010).
21. J. E. Gretz, C. C. Norbury, A. O. Anderson, A. E. I. Proudfoot, S. Shaw, 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).
22. S. F. Gonzalez, V. Lukacs-Kornek, M. P. Kuligowski, L. A. Pitcher, S. E. Degn, Y.-A. Kim, M. J. Cloninger, L. Martinez-Pomares, S. Gordon, S. J. Turley, M. C. Carroll, Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 11, 427–434 (2010).
23. I. L. Grigorova, M. Panteleev, J. G. Cyster, Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. U.S.A. 107, 20447–20452 (2010).
24. E. K. Deenick, A. Chan, C. S. Ma, D. Gatto, P. L. Schwartzberg, R. Brink, S. G. Tangye, Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33, 241–253 (2010).
25. M. Kool, V. Pétrilli, T. De Smedt, A. Rolaz, H. Hammad, M. van Nimwegen, I. M. Bergen, R. Castillo, B. N. Lambrecht, J. Tschopp, Cutting edge: Alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol. 181, 3755–3759 (2008).
26. K. L. Randall, T. Lambe, A. L. Johnson, B. Treanor, E. Kucharska, H. Domaschenz, B. Whittle, L. E. Tze, A. Enders, T. L. Crockford, T. Bouriez-Jones, D. Alston, J. G. Cyster, M. J. Lenardo, F. Mackay, E. K. Deenick, S. G. Tangye, T. D. Chan, T. Camidge, R. Brink, C. G. Vinuesa, F. D. Batista, R. J. Cornall, C. C. Goodnow, Dock8 mutations cripple B cell immunological synapses, germinal centers and long-lived antibody production. Nat. Immunol. 10, 1283–1291 (2009).
27. Q. Zhang, H. Jing, H. C. Su, Recent advances in DOCK8 immunodeficiency syndrome. J. Clin. Immunol. 36, 441–449 (2016).
28. Y. Harada, Y. Tanaka, M. Terasawa, M. Pieczyk, K. Habiro, T. Katakai, K. Hanawa-Suetsugu, M. Kukimoto-Niino, T. Nishizaki, M. Shirouzu, X. Duan, T. Uruno, A. Nishikimi, F. Sanematsu, S. Yokoyama, J. V. Stein, T. Kinashi, Y. Fukui, DOCK8 is a Cdc42 activator critical for interstitial dendritic cell migration during immune responses. Blood 119, 4451–4461 (2012).
29. J. K. Krishnaswamy, A. Singh, U. Gowthaman, R. Wu, P. Gorrepati, M. S. L. Nascimento, A. Gallman, D. Liu, A. M. Rhebergen, S. Calabro, L. Xu, P. Ranney, A. Srivastava, M. Ranson, J. D. Gorham, Z. McCaw, S. R. Kleeberger, L. X. Heinz, A. C. Müller, K. L. Bennett, G. Superti-Furga, J. Henao-Mejia, F. S. Sutterwala, A. Williams, R. A. Flavell, S. C. Eisenbarth, Coincidental loss of DOCK8 function in NLRP10-deficient and C3H/HeJ mice results in defective dendritic cell migration. Proc. Natl. Acad. Sci. U.S.A. 112, 3056–3061 (2015).
30. S. Calabro, D. Liu, A. Gallman, M. S. L. Nascimento, Z. Yu, T.-T. Zhang, P. Chen, B. Zhang, L. Xu, U. Gowthaman, J. K. Krishnaswamy, A. M. Haberman, A. Williams, S. C. Eisenbarth, Differential intrasplenic migration of dendritic cell subsets tailors adaptive immunity. Cell Rep. 16, 2472–2485 (2016).
31. + T cells are biased to a TH2 effector fate at the expense of TH1 and TH17 cells. J. Allergy Clin. Immunol. 139, 933–949 (2017).
32. E. Janssen, M. Tohme, M. Hedayat, M. Leick, S. Kumari, N. Ramesh, M. J. Massaad, S. Ullas, V. Azcutia, C. C. Goodnow, K. L. Randall, Q. Qiao, H. Wu, W. Al-Herz, D. Cox, J. Hartwig, D. J. Irvine, F. W. Luscinskas, R. S. Geha, A DOCK8-WIP-WASp complex links T cell receptors to the actin cytoskeleton. J. Clin. Invest. 126, 3837–3851 (2016).
33. D. Baumjohann, S. Preite, A. Reboldi, F. Ronchi, K. M. Ansel, A. Lanzavecchia, F. Sallusto, Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity 38, 596–605 (2013).
34. S. M. Kerfoot, G. Yaari, J. R. Patel, K. L. Johnson, D. G. Gonzalez, S. H. Kleinstein, A. M. Haberman, Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 34, 947–960 (2011).
35. B. Z. Igyártó, D. H. Kaplan, Antigen presentation by Langerhans cells. Curr. Opin. Immunol. 25, 115–119 (2013).
36. M. Tomura, A. Hata, S. Matsuoka, F. H. W. Shand, Y. Nakanishi, R. Ikebuchi, S. Ueha, H. Tsutsui, K. Inaba, K. Matsushima, A. Miyawaki, K. Kabashima, T. Watanabe, O. Kanagawa, Tracking and quantification of dendritic cell migration and antigen trafficking between the skin and lymph nodes. Sci. Rep. 4, 6030 (2014).
37. + pulmonary dendritic cells preferentially acquire and present apoptotic cell–associated antigen. J. Exp. Med. 208, 1789–1797 (2011).
38. + dendritic cells in human and mouse control mucosal IL-17 cytokine responses. Immunity 38, 970–983 (2013).
39. B.-C. Chiu, V. R. Stolberg, S. W. Chensue, Mononuclear phagocyte-derived IL-10 suppresses the innate IL-12/IFN- axis in lung-challenged aged mice. J. Immunol. 181, 3156–3166 (2008).
40. D. Baumjohann, T. Okada, K. M. Ansel, Cutting edge: Distinct waves of BCL6 expression during T follicular helper cell development. J. Immunol. 187, 2089–2092 (2011).
41. J. L. Cannons, H. Qi, K. T. Lu, M. Dutta, J. Gomez-Rodriguez, J. Cheng, E. K. Wakeland, R. N. Germain, P. L. Schwartzberg, Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32, 253–265 (2010).
42. A. C. Poholek, K. Hansen, S. G. Hernandez, D. Eto, A. Chandele, J. S. Weinstein, X. Dong, J. M. Odegard, S. M. Kaech, A. L. Dent, S. Crotty, J. Craft, In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 185, 313–326 (2010).
43. H. H. Jabara, D. R. Mcdonald, E. Janssen, M. J. Massaad, N. Ramesh, A. Borzutzky, I. Rauter, H. Benson, L. Schneider, S. Baxi, M. Recher, L. D. Notarangelo, R. Wakim, G. Dbaibo, M. Dasouki, W. Al-Herz, I. Barlan, S. Baris, N. Kutukculer, H. D. Ochs, A. Plebani, M. Kanariou, G. Lefranc, I. Reisli, K. A. Fitzgerald, D. Golenbock, J. Manis, S. Keles, R. Ceja, T. A. Chatila, R. S. Geha, DOCK8 functions as an adaptor that links TLR-MyD88 signaling to B cell activation. Nat. Immunol. 13, 612–620 (2012).
44. Y. Takahashi, P. R. Dutta, D. M. Cerasoli, G. Kelsoe, In situ studies of the primary immune response to (4-hydroxy-3-nitrophenyl)acetyl. V. Affinity maturation develops in two stages of clonal selection. J. Exp. Med. 187, 885–895 (1998).
45. K. Miyauchi, A. Sugimoto-Ishige, Y. Harada, Y. Adachi, Y. Usami, T. Kaji, K. Inoue, H. Hasegawa, T. Watanabe, A. Hijikata, S. Fukuyama, T. Maemura, M. Okada-Hatakeyama, O. Ohara, Y. Kawaoka, Y. Takahashi, T. Takemori, M. Kubo, Protective neutralizing influenza antibody response in the absence of T follicular helper cells. Nat. Immunol. 17, 1447–1458 (2016).
46. C. Jakubzick, J. Helft, T. J. Kaplan, G. J. Randolph, Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus particulate antigen. J. Immunol. Methods 337, 121–131 (2008).
47. + T cell responses to influenza A virus. Nat. Immunol. 14, 246–253 (2013).
48. J. P. Ray, M. M. Staron, J. A. Shyer, P.-C. Ho, H. D. Marshall, S. M. Gray, B. J. Laidlaw, K. Araki, R. Ahmed, S. M. Kaech, J. Craft, The interleukin-2-mTORc1 kinase axis defines the signaling, differentiation, and metabolism of T helper 1 and follicular B helper T cells. Immunity 43, 690–702 (2015).
49. E. Lu, E. V. Dang, J. G. McDonald, J. G. Cyster, Distinct oxysterol requirements for positioning naïve and activated dendritic cells in the spleen. Sci. Immunol. 2, eaal5237 (2017).
50. high germinal center-associated subpopulation. J. Immunol. 179, 5099–5108 (2007).
51. S. Kijani, U. Yrlid, M. Heyden, M. Levin, J. Borén, P. Fogelstrand, Filter-dense multicolor microscopy. PLOS ONE 10, e0119499 (2015).
52. T. Yi, J. Li, H. Chen, J. Wu, J. An, Y. Xu, Y. Hu, C. A. Lowell, J. G. Cyster, Splenic dendritic cells survey red blood cells for missing self-CD47 to trigger adaptive immune responses. Immunity 43, 764–775 (2015).
53. T. A. Waldmann, C. K. Goldman, R. J. Robb, J. M. Depper, W. J. Leonard, S. O. Sharrow, K. F. Bongiovanni, S. J. Korsmeyer, W. C. Greene, Expression of interleukin 2 receptors on activated human B cells. J. Exp. Med. 160, 1450–1466 (1984).
54. + dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13, 681–690 (2012).
55. T. Granot, T. Senda, D. J. Carpenter, N. Matsuoka, J. Weiner, C. L. Gordon, M. Miron, B. V. Kumar, A. Griesemer, S.-H. Ho, H. Lerner, J. J. C. Thome, T. Connors, B. Reizis, D. L. Farber, Dendritic cells display subset and tissue-specific maturation dynamics over human life. Immunity 46, 504–515 (2017).