Classical Flt3L-dependent dendritic cells control immunity to protein vaccine

Journal of Experimental Medicine

Volumn 211, Issue 9, 2014, Pages 1875-1891

  Anandasabapathy, Niroshana ^a,c   Feder, Rachel ^a   Mollah, Shamim ^a   Tse, Sze Wah ^c   Longhi, Maria Paula ^a   Mehandru, Saurabh ^a   Matos, Ines ^a   Cheong, Cheolho ^a   Ruane, Darren ^a   Brane, Lucas ^a   Teixeira, Angela ^a   Dobrin, Joseph ^a   Mizenina, Olga ^a   Park, Chae Gyu ^a   Meredith, Matthew ^a   Clausen, Björn E ^b   Nussenzweig, Michel C ^a   Steinman, Ralph M ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; FMS LIKE TYROSINE KINASE 3 LIGAND; INTERLEUKIN 15; LANGERIN; LIGAND; UNCLASSIFIED DRUG; VACCINE;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MIGRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; GENE DELETION; GENE EXPRESSION; HUMORAL IMMUNITY; LAMINA PROPRIA; LANGERHANS CELL; LYMPHOCYTE DIFFERENTIATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VACCINATION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, SURFACE; DENDRITIC CELLS; FEMALE; GENE EXPRESSION; HUMANS; IMMUNITY, HUMORAL; INJECTIONS, INTRADERMAL; INJECTIONS, SUBCUTANEOUS; INTERFERON-GAMMA; LECTINS, C-TYPE; LIGANDS; MALE; MANNOSE-BINDING LECTINS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; PROTEINS; T-LYMPHOCYTE SUBSETS; TRANSCRIPTION FACTORS; VACCINES;

EID: 84906568561     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131397     Document Type: Article

References (71)

1. Ahmed, R., and R.S. Akondy. 2011. Insights into human CD8(+) T-cell memory using the yellow fever and smallpox vaccines. Immunol. Cell Biol. 89:340-345. http://dx.doi.org/10.1038/icb.2010.155
2. Allenspach, E.J., M.P. Lemos, P.M. Porrett, L.A. Turka, and T.M. Laufer. 2008. Migratory and lymphoid-resident dendritic cells cooperate to efficiently prime naive CD4 T cells. Immunity. 29:795-806. http://dx.doi.org/10.1016/j.immuni.2008.08.013
3. Bajénoff, M., S. Granjeaud, and S. Guerder. 2003. The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J. Exp. Med. 198:715-724. http://dx.doi.org/10.1084/jem.20030167
4. Bedoui, S., S. Prato, J. Mintern, T. Gebhardt, Y. Zhan, A.M. Lew, W.R. Heath, J.A. Villadangos, and E. Segura. 2009a. Characterization of an immediate splenic precursor of CD8+ dendritic cells capable of inducing antiviral T cell responses. J. Immunol. 182:4200-4207. http://dx.doi.org/10.4049/jimmunol.0802286
5. Bedoui, S., P.G. Whitney, J. Waithman, L. Eidsmo, L. Wakim, I. Caminschi, R.S. Allan, M. Wojtasiak, K. Shortman, F.R. Carbone, et al. 2009b. Crosspresentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 10:488-495. http://dx.doi.org/10.1038/ni.1724
6. Bennett, C.L., E. van Rijn, S. Jung, K. Inaba, R.M. Steinman, M.L. Kapsenberg, and B.E. Clausen. 2005. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169:569-576. http://dx.doi.org/10.1083/jcb.200501071
7. Boulland, M.L., J. Marquet, V. Molinier-Frenkel, P. Möler, C. Guiter, F. Lasoudris, C. Copie-Bergman, M. Baia, P. Gaulard, K. Leroy, and F. Castellano. 2007. Human IL4I1 is a secreted L-phenylalanine oxidase expressed by mature dendritic cells that inhibits T-lymphocyte proliferation. Blood. 110:220-227. http://dx.doi.org/10.1182/blood-2006-07-036210
8. Bozzacco, L., C. Trumpfheller, Y. Huang, M.P. Longhi, I. Shimeliovich, J.D. Schauer, C.G. Park, and R.M. Steinman. 2010. HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur. J. Immunol. 40:36-46. http://dx.doi.org/10.1002/eji.200939748
9. Brasel, K., H.J. McKenna, P.J. Morrissey, K. Charrier, A.E. Morris, C.C. Lee, D.E. Williams, and S.D. Lyman. 1996. Hematologic effects of flt3 ligand in vivo in mice. Blood. 88:2004-2012.
10. Brenchley, J.M., and D.C. Douek. 2008. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 1:23-30. http://dx.doi.org/10.1038/mi.2007.1
11. Butte, M.J., M.E. Keir, T.B. Phamduy, A.H. Sharpe, and G.J. Freeman. 2007. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 27:111-122. http://dx.doi.org/10.1016/j.immuni.2007.05.016
12. Castillo, E.F., S.W. Stonier, L. Frasca, and K.S. Schluns. 2009. Dendritic cells support the in vivo development and maintenance of NK cells via IL-15 trans-presentation. J. Immunol. 183:4948-4956. http://dx.doi.org/10.4049/jimmunol.0900719
13. Chang, L.Y., Y.C. Lin, C.W. Kang, C.Y. Hsu, Y.Y. Chu, C.T. Huang, Y.J. Day, T.C. Chen, C.T. Yeh, and C.Y. Lin. 2012. The indispensable role of CCR5 for in vivo suppressor function of tumor-derived CD103+ effector/memory regulatory T cells. J. Immunol. 189:567-574. http://dx.doi.org/10.4049/jimmunol.1200266
14. Cheong, C., J. Idoyaga, Y. Do, M. Pack, S.H. Park, H. Lee, Y.S. Kang, J.H. Choi, J.Y. Kim, A. Bonito, et al. 2007. Production of monoclonal antibodies that recognize the extracellular domain of mouse langerin/CD207. J. Immunol. Methods. 324:48-62. http://dx.doi.org/10.1016/j.jim.2007.05.001
15. Cheong, C., I. Matos, J.H. Choi, D.B. Dandamudi, E. Shrestha, M.P. Longhi, K.L. Jeffrey, R.M. Anthony, C. Kluger, G. Nchinda, et al. 2010. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell. 143:416-429. http://dx.doi.org/10.1016/j.cell.2010.09.039
16. Choi, J.H., C. Cheong, D.B. Dandamudi, C.G. Park, A. Rodriguez, S. Mehandru, K. Velinzon, I.H. Jung, J.Y. Yoo, G.T. Oh, and R.M. Steinman. 2011. Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity. 35:819-831.
17. Condamine, T., L. Le Texier, D. Howie, A. Lavault, M. Hill, F. Halary, S. Cobbold, H. Waldmann, M.C. Cuturi, and E. Chiffoleau. 2010. Tmem176B and Tmem176A are associated with the immature state of dendritic cells. J. Leukoc. Biol. 88:507-515. http://dx.doi.org/10.1189/jlb.1109738
18. Dorner, B.G., M.B. Dorner, X. Zhou, C. Opitz, A. Mora, S. Güttler, A. Hutloff, H.W. Mages, K. Ranke, M. Schaefer, et al. 2009. Selective expression of the chemokine receptor XCR1 on cross-presenting dendritic cells determines cooperation with CD8+ T cells. Immunity. 31:823-833. http://dx.doi.org/10.1016/j.immuni.2009.08.027
19. Duthie, M.S., H.P. Windish, C.B. Fox, and S.G. Reed. 2011. Use of defined TLR ligands as adjuvants within human vaccines. Immunol. Rev. 239:178-196. http://dx.doi.org/10.1111/j.1600-065X.2010.00978.x
20. Eidenschenk, C., K. Crozat, P. Krebs, R. Arens, D. Popkin, C.N. Arnold, A.L. Blasius, C.A. Benedict, E.M. Moresco, Y. Xia, and B. Beutler. 2010. Flt3 permits survival during infection by rendering dendritic cells competent to activate NK cells. Proc. Natl. Acad. Sci. USA. 107:9759-9764. http://dx.doi.org/10.1073/pnas.1005186107
21. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell. 99:23-33. http://dx.doi.org/10.1016/S0092-8674(00)80059-8
22. Ginhoux, F., K. Liu, J. Helft, M. Bogunovic, M. Greter, D. Hashimoto, J. Price, N. Yin, J. Bromberg, S.A. Lira, et al. 2009. The origin and development of nonlymphoid tissue CD103+ DCs. J. Exp. Med. 206:3115-3130. http://dx.doi.org/10.1084/jem.20091756
23. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R.A. Flavell, M.S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA. 103:8459-8464. http://dx.doi.org/10.1073/pnas.0603082103
24. Guermonprez, P., J. Helft, C. Claser, S. Deroubaix, H. Karanje, A. Gazumyan, G. Darasse-Jeze, S.B. Telerman, G. Breton, H.A. Schreiber, et al. 2013. Inflammatory Flt3l is essential to mobilize dendritic cells and for T cell responses during Plasmodium infection. Nat. Med. 19:730-738.
25. Haniffa, M., A. Shin, V. Bigley, N. McGovern, P. Teo, P. See, P.S. Wasan, X.N. Wang, F. Malinarich, B. Malleret, et al. 2012. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+ nonlymphoid dendritic cells. Immunity. 37:60-73. http://dx.doi.org/10.1016/j.immuni.2012.04.012
26. Henri, S., M. Guilliams, L.F. Poulin, S. Tamoutounour, L. Ardouin, M. Dalod, and B. Malissen. 2010a. Disentangling the complexity of the skin dendritic cell network. Immunol. Cell Biol. 88:366-375. http://dx.doi.org/10.1038/icb.2010.34
27. Henri, S., L.F. Poulin, S. Tamoutounour, L. Ardouin, M. Guilliams, B. de Bovis, E. Devilard, C. Viret, H. Azukizawa, A. Kissenpfennig, and B. Malissen. 2010b. CD207+ CD103+ dermal dendritic cells cross-present keratinocytederived antigens irrespective of the presence of Langerhans cells. J. Exp. Med. 207:189-206. http://dx.doi.org/10.1084/jem.20091964
28. Itano, A.A., S.J. McSorley, R.L. Reinhardt, B.D. Ehst, E. Ingulli, A.Y. Rudensky, and M.K. Jenkins. 2003. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity. 19:47-57. http://dx.doi.org/10.1016/S1074-7613(03)00175-4
29. Jelinek, I., J.N. Leonard, G.E. Price, K.N. Brown, A. Meyer-Manlapat, P.K. Goldsmith, Y. Wang, D. Venzon, S.L. Epstein, and D.M. Segal. 2011. TLR3-specific double-stranded RNA oligonucleotide adjuvants induce dendritic cell cross-presentation, CTL responses, and antiviral protection. J. Immunol. 186:2422-2429. http://dx.doi.org/10.4049/jimmunol.1002845
30. Kastenmüller, K., U. Wille-Reece, R.W. Lindsay, L.R. Trager, P.A. Darrah, B.J. Flynn, M.R. Becker, M.C. Udey, B.E. Clausen, B.Z. Igyarto, et al. 2011. Protective T cell immunity in mice following protein-TLR7/8 agonist-conjugate immunization requires aggregation, type I IFN, and multiple DC subsets. J. Clin. Invest. 121:1782-1796. http://dx.doi.org/10.1172/JCI45416
31. Kissenpfennig, A., S. Henri, B. Dubois, C. Laplace-Builhé P. Perrin, N. Romani, C.H. Tripp, P. Douillard, L. Leserman, D. Kaiserlian, et al. 2005. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity. 22:643-654. http://dx.doi.org/10.1016/j.immuni.2005.04.004
32. Langley, K.E., L.G. Bennett, J. Wypych, S.A. Yancik, X.D. Liu, K.R. Westcott, D.G. Chang, K.A. Smith, and K.M. Zsebo. 1993. Soluble stem cell factor in human serum. Blood. 81:656-660.
33. Lasoudris, F., C. Cousin, A. Prevost-Blondel, N. Martin-Garcia, I. Abd-Alsamad, N. Ortonne, J.P. Farcet, F. Castellano, and V. Molinier-Frenkel. 2011. IL4I1: an inhibitor of the CD8+ antitumor T-cell response in vivo. Eur. J. Immunol. 41:1629-1638. http://dx.doi.org/10.1002/eji.201041119
34. Liu, K., C. Waskow, X. Liu, K. Yao, J. Hoh, and M. Nussenzweig. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat. Immunol. 8:578-583. http://dx.doi.org/10.1038/ni1462
35. Liu, K., G.D. Victora, T.A. Schwickert, P. Guermonprez, M.M. Meredith, K. Yao, F.F. Chu, G.J. Randolph, A.Y. Rudensky, and M. Nussenzweig. 2009. In vivo analysis of dendritic cell development and homeostasis. Science. 324:392-397.
36. Longhi, M.P., C. Trumpfheller, J. Idoyaga, M. Caskey, I. Matos, C. Kluger, A.M. Salazar, M. Colonna, and R.M. Steinman. 2009. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J. Exp. Med. 206:1589-1602. http://dx.doi.org/10.1084/jem.20090247
37. Louvet, C., E. Chiffoleau, M. Heslan, L. Tesson, J.M. Heslan, R. Brion, G. Bériou, C. Guillonneau, J. Khalife, I. Anegon, and M.C. Cuturi. 2005. Identification of a new member of the CD20/FcepsilonRIbeta family overexpressed in tolerated allografts. Am. J. Transplant. 5:2143-2153. http://dx.doi.org/10.1111/j.1600-6143.2005.01007.x
38. Lyman, S.D., and H.J. McKenna. 2003. Flt3 ligand. In The Cytokine Handbook. A. Thomson, editor. Academic Press. pp. 989-1010. http://dx.doi.org/10.1016/B978-012689663-3/50046-6
39. Maraskovsky, E., K. Brasel, M. Teepe, E.R. Roux, S.D. Lyman, K. Shortman, and H.J. McKenna. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184:1953-1962. http://dx.doi.org/10.1084/jem.184.5.1953
40. Martín-Fontecha, A., S. Sebastiani, U.E. Höpken, M. Uguccioni, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2003. Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming. J. Exp. Med. 198:615-621. http://dx.doi.org/10.1084/jem.20030448
41. Martín-Fontecha, A., D. Baumjohann, G. Guarda, A. Reboldi, M. Hons, A. Lanzavecchia, and F. Sallusto. 2008. CD40L+ CD4+ memory T cells migrate in a CD62P-dependent fashion into reactive lymph nodes and license dendritic cells for T cell priming. J. Exp. Med. 205:2561-2574. http://dx.doi.org/10.1084/jem.20081212
42. Menning, A., U.E. Höpken, K. Siegmund, M. Lipp, A. Hamann, and J. Huehn. 2007. Distinctive role of CCR7 in migration and functional activity of naive- and effector/memory-like Treg subsets. Eur. J. Immunol. 37:1575-1583. http://dx.doi.org/10.1002/eji.200737201
43. Meredith, M.M., K. Liu, G. Darrasse-Jeze, A.O. Kamphorst, H.A. Schreiber, P. Guermonprez, J. Idoyaga, C. Cheong, K.H. Yao, R.E. Niec, and M.C. Nussenzweig. 2012. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 209:1153-1165. http://dx.doi.org/10.1084/jem.20112675
44. Miller, J.C., B.D. Brown, T. Shay, E.L. Gautier, V. Jojic, A. Cohain, G. Pandey, M. Leboeuf, K.G. Elpek, J. Helft, et al. Immunological Genome Consortium. 2012. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol. 13:888-899. http://dx.doi.org/10.1038/ni.2370
45. Mollah, S.A., J.S. Dobrin, R.E. Feder, S.W. Tse, I.G. Matos, C. Cheong, R.M. Steinman, and N. Anandasabapathy. 2014. Flt3L dependence helps define an uncharacterized subset of murine cutaneous dendritic cells. J. Invest. Dermatol. 134:1265-1275. http://dx.doi.org/10.1038/jid.2013.515
46. Naik, S.H., A.I. Proietto, N.S. Wilson, A. Dakic, P. Schnorrer, M. Fuchsberger, M.H. Lahoud, M. O'Keeffe, Q.X. Shao, W.F. Chen, et al. 2005. Cutting edge: generation of splenic CD8+ and CD8-dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174:6592-6597. http://dx.doi.org/10.4049/jimmunol.174.11.6592
47. Noordegraaf, M., V. Flacher, P. Stoitzner, and B.E. Clausen. 2010. Functional redundancy of Langerhans cells and Langerin+ dermal dendritic cells in contact hypersensitivity. J. Invest. Dermatol. 130:2752-2759. http://dx.doi.org/10.1038/jid.2010.223
48. Ohl, L., M. Mohaupt, N. Czeloth, G. Hintzen, Z. Kiafard, J. Zwirner, T. Blankenstein, G. Henning, and R. Förter. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. 21:279-288. http://dx.doi.org/10.1016/j.immuni.2004.06.014
49. Ohnmacht, C., A. Pullner, S.B. King, I. Drexler, S. Meier, T. Brocker, and D. Voehringer. 2009. Constitutive ablation of dendritic cells breaks selftolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J. Exp. Med. 206:549-559. http://dx.doi.org/10.1084/jem.20082394
50. Pantel, A., C. Cheong, D. Dandamudi, E. Shrestha, S. Mehandru, L. Brane, D. Ruane, A. Teixeira, L. Bozzacco, R.M. Steinman, and M.P. Longhi. 2012. A new synthetic TLR4 agonist, GLA, allows dendritic cells targeted with antigen to elicit Th1 T-cell immunity in vivo. Eur. J. Immunol. 42:101-109. http://dx.doi.org/10.1002/eji.201141855
51. Pepper, M., J.L. Linehan, A.J. Pagán, T. Zell, T. Dileepan, P.P. Cleary, and M.K. Jenkins. 2010. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 11:83-89. http://dx.doi.org/10.1038/ni.1826
52. Petersen, S.H., E. Odintsova, T.A. Haigh, A.B. Rickinson, G.S. Taylor, and F. Berditchevski. 2011. The role of tetraspanin CD63 in antigen presentation via MHC class II. Eur. J. Immunol. 41:2556-2561. http://dx.doi.org/10.1002/eji.201141438
53. Posselt, G., H. Schwarz, A. Duschl, and J. Horejs-Hoeck. 2011. Suppressor of cytokine signaling 2 is a feedback inhibitor of TLR-induced activation in human monocyte-derived dendritic cells. J. Immunol. 187:2875-2884. http://dx.doi.org/10.4049/jimmunol.1003348
54. Romani, N., M. Thurnher, J. Idoyaga, R.M. Steinman, and V. Flacher. 2010. Targeting of antigens to skin dendritic cells: possibilities to enhance vaccine efficacy. Immunol. Cell Biol. 88:424-430. http://dx.doi.org/10.1038/icb.2010.39
55. Sallusto, F., and A. Lanzavecchia. 2009. Heterogeneity of CD4+ memory T cells: functional modules for tailored immunity. Eur. J. Immunol. 39: 2076-2082. http://dx.doi.org/10.1002/eji.200939722
56. Sallusto, F., D. Lenig, R. Förster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401:708-712. http://dx.doi.org/10.1038/44385
57. Sallusto, F., C.R. Mackay, and A. Lanzavecchia. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18:593-620. http://dx.doi.org/10.1146/annurev.immunol.18.1.593
58. Sathaliyawala, T., W.E. O'Gorman, M. Greter, M. Bogunovic, V. Konjufca, Z.E. Hou, G.P. Nolan, M.J. Miller, M. Merad, and B. Reizis. 2010. Mammalian target of rapamycin controls dendritic cell development downstream of Flt3 ligand signaling. Immunity. 33:597-606. http://dx.doi.org/10.1016/j.immuni.2010.09.012
59. Sathe, P., J. Pooley, D. Vremec, J. Mintern, J.O. Jin, L. Wu, J.Y. Kwak, J.A. Villadangos, and K. Shortman. 2011. The acquisition of antigen crosspresentation function by newly formed dendritic cells. J. Immunol. 186:5184-5192. http://dx.doi.org/10.4049/jimmunol.1002683
60. Satpathy, A.T., W. Kc, J.C. Albring, B.T. Edelson, N.M. Kretzer, D. Bhattacharya, T.L. Murphy, and K.M. Murphy. 2012. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 209:1135-1152. http://dx.doi.org/10.1084/jem.20120030
61. Schulz, O., S.S. Diebold, M. Chen, T.I. Näslund, M.A. Nolte, L. Alexopoulou, Y.T. Azuma, R.A. Flavell, P. Liljeström, and C. Reis e Sousa. 2005. Tolllike receptor 3 promotes cross-priming to virus-infected cells. Nature. 433:887-892. http://dx.doi.org/10.1038/nature03326
62. Shadle, P.J., J.I. Allen, M.D. Geier, and K. Koths. 1989. Detection of endogenous macrophage colony-stimulating factor (M-CSF) in human blood. Exp. Hematol. 17:154-159.
63. Sixt, M., N. Kanazawa, M. Selg, T. Samson, G. Roos, D.P. Reinhardt, R. Pabst, M.B. Lutz, and L. Sorokin. 2005. 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. http://dx.doi.org/10.1016/j.immuni.2004.11.013
64. Steinman, R.M., D. Hawiger, and M.C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711. http://dx.doi.org/10.1146/annurev.immunol.21.120601.141040
65. Travis, M.A., B. Reizis, A.C. Melton, E. Masteller, Q. Tang, J.M. Proctor, Y. Wang, X. Bernstein, X. Huang, L.F. Reichardt, et al. 2007. Loss of integrin α(v)β8 on dendritic cells causes autoimmunity and colitis in mice. Nature. 449:361-365. http://dx.doi.org/10.1038/nature06110
66. Trumpfheller, C., M. Caskey, G. Nchinda, M.P. Longhi, O. Mizenina, Y. Huang, S.J. Schlesinger, M. Colonna, and R.M. Steinman. 2008. The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine. Proc. Natl. Acad. Sci. USA. 105:2574-2579. http://dx.doi.org/10.1073/pnas.0711976105
67. Urban, B.C., D.J. Ferguson, A. Pain, N. Willcox, M. Plebanski, J.M. Austyn, and D.J. Roberts. 1999. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature. 400:73-77. http://dx.doi.org/10.1038/21900
68. Urban, B.C., N. Willcox, and D.J. Roberts. 2001. A role for CD36 in the regulation of dendritic cell function. Proc. Natl. Acad. Sci. USA. 98:8750-8755. http://dx.doi.org/10.1073/pnas.151028698
69. Waskow, C., K. Liu, G. Darrasse-Jèze, P. Guermonprez, F. Ginhoux, M. Merad, T. Shengelia, K. Yao, and M. Nussenzweig. 2008. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9:676-683. http://dx.doi.org/10.1038/ni.1615
70. Zaft, T., A. Sapoznikov, R. Krauthgamer, D.R. Littman, and S. Jung. 2005. CD11chigh dendritic cell ablation impairs lymphopenia-driven proliferation of naive and memory CD8+ T cells. J. Immunol. 175:6428-6435. http://dx.doi.org/10.4049/jimmunol.175.10.6428
71. Zhang, J.G., P.E. Czabotar, A.N. Policheni, I. Caminschi, S.S. Wan, S. Kitsoulis, K.M. Tullett, A.Y. Robin, R. Brammananth, M.F. van Delft, et al. 2012. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity. 36:646-657. http://dx.doi.org/10.1016/j.immuni.2012.03.009