Migratory and Lymphoid-Resident Dendritic Cells Cooperate to Efficiently Prime Naive CD4 T cells

Immunity

Volumn 29, Issue 5, 2008, Pages 795-806

  Allenspach, Eric J ^a   Lemos, Maria P ^a   Porrett, Paige M ^a   Turka, Laurence A ^a   Laufer, Terri M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CELLIMMUNO

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; IMMUNIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL MOVEMENT; DENDRITIC CELLS; GENE KNOCKDOWN TECHNIQUES; LYMPH NODES; MICE; MICE, INBRED C57BL; OVALBUMIN;

EID: 55349084353     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.08.013     Document Type: Article

References (50)

1. Allan R.S., Smith C.M., Belz G.T., van Lint A.L., Wakim L.M., Heath W.R., and Carbone F.R. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 301 (2003) 1925-1928
2. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., Lew A.M., Shortman K., Heath W.R., and Carbone F.R. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity 25 (2006) 153-162
3. Bajenoff M., Egen J.G., Koo L.Y., Laugier J.P., Brau F., Glaichenhaus N., and Germain R.N. Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25 (2006) 989-1001
4. Bajenoff M., Granjeaud S., and Guerder S. 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 (2003) 715-724
5. Bogunovic M., Ginhoux F., Wagers A., Loubeau M., Isola L.M., Lubrano L., Najfeld V., Phelps R.G., Grosskreutz C., Scigliano E., et al. Identification of a radio-resistant and cycling dermal dendritic cell population in mice and men. J. Exp. Med. 203 (2006) 2627-2638
6. Boonstra A., Asselin-Paturel C., Gilliet M., Crain C., Trinchieri G., Liu Y.J., and O'Garra A. Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: Dependency on antigen dose and differential toll-like receptor ligation. J. Exp. Med. 197 (2003) 101-109
7. Bursch L.S., Wang L., Igyarto B., Kissenpfennig A., Malissen B., Kaplan D.H., and Hogquist K.A. Identification of a novel population of Langerin+ dendritic cells. J. Exp. Med. 204 (2007) 3147-3156
8. Bynoe M.S., Evans J.T., Viret C., and Janeway Jr. C.A. Epicutaneous immunization with autoantigenic peptides induces T suppressor cells that prevent experimental allergic encephalomyelitis. Immunity 19 (2003) 317-328
9. Cahill R.N., Frost H., and Trnka Z. The effects of antigen on the migration of recirculating lymphocytes through single lymph nodes. J. Exp. Med. 143 (1976) 870-888
10. Catron D.M., Rusch L.K., Hataye J., Itano A.A., and Jenkins M.K. CD4+ T cells that enter the draining lymph nodes after antigen injection participate in the primary response and become central-memory cells. J. Exp. Med. 203 (2006) 1045-1054
11. Forster R., Schubel A., Breitfeld D., Kremmer E., Renner-Muller I., Wolf E., and Lipp M. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99 (1999) 23-33
12. Garg S., Oran A., Wajchman J., Sasaki S., Maris C.H., Kapp J.A., and Jacob J. Genetic tagging shows increased frequency and longevity of antigen-presenting, skin-derived dendritic cells in vivo. Nat. Immunol. 4 (2003) 907-912
13. Ginhoux F., Collin M.P., Bogunovic M., Abel M., Leboeuf M., Helft J., Ochando J., Kissenpfennig A., Malissen B., Grisotto M., et al. Blood-derived dermal langerin+ dendritic cells survey the skin in the steady state. J. Exp. Med. 204 (2007) 3133-3146
14. Grusby M.J., Johnson R.S., Papaioannou V.E., and Glimcher L.H. Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice. Science 253 (1991) 1417-1420
15. Hickman H.D., Takeda K., Skon C.N., Murray F.R., Hensley S.E., Loomis J., Barber G.N., Bennink J.R., and Yewdell J.W. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9 (2008) 155-165
16. Itano A.A., McSorley S.J., Reinhardt R.L., Ehst B.D., Ingulli E., Rudensky A.Y., and Jenkins M.K. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 19 (2003) 47-57
17. Kissenpfennig A., Henri S., Dubois B., Laplace-Builhe C., Perrin P., Romani N., Tripp C.H., Douillard P., Leserman L., Kaiserlian D., et al. Dynamics and function of Langerhans cells in vivo: Dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22 (2005) 643-654
18. Kleindienst P., and Brocker T. Endogenous dendritic cells are required for amplification of T cell responses induced by dendritic cell vaccines in vivo. J. Immunol. 170 (2003) 2817-2823
19. Lemos M.P., Fan L., Lo D., and Laufer T.M. CD8alpha+ and CD11b+ dendritic cell-restricted MHC class II controls Th1 CD4+ T cell immunity. J. Immunol. 171 (2003) 5077-5084
20. Mach N., Gillessen S., Wilson S.B., Sheehan C., Mihm M., and Dranoff G. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 60 (2000) 3239-3246
21. Marta M., Andersson A., Isaksson M., Kampe O., and Lobell A. Unexpected regulatory roles of TLR4 and TLR9 in experimental autoimmune encephalomyelitis. Eur. J. Immunol. 38 (2008) 565-575
22. Matloubian M., Lo C.G., Cinamon G., Lesneski M.J., Xu Y., Brinkmann V., Allende M.L., Proia R.L., and Cyster J.G. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427 (2004) 355-360
23. McGill J., Van Rooijen N., and Legge K.L. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med. 205 (2008) 1635-1646
24. Merad M., Manz M.G., Karsunky H., Wagers A., Peters W., Charo I., Weissman I.L., Cyster J.G., and Engleman E.G. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3 (2002) 1135-1141
25. Moon J.J., Chu H.H., Pepper M., McSorley S.J., Jameson S.C., Kedl R.M., and Jenkins M.K. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27 (2007) 203-213
26. Mount A.M., Smith C.M., Kupresanin F., Stoermer K., Heath W.R., and Belz G.T. Multiple dendritic cell populations activate CD4+ T cells after viral stimulation. PLoS ONE 3 (2008) e1691
27. Naik S.H., Sathe P., Park H.Y., Metcalf D., Proietto A.I., Dakic A., Carotta S., O'Keeffe M., Bahlo M., Papenfuss A., et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8 (2007) 1217-1226
28. Onai N., Obata-Onai A., Schmid M.A., Ohteki T., Jarrossay D., and Manz M.G. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 8 (2007) 1207-1216
29. Ortner U., Inaba K., Koch F., Heine M., Miwa M., Schuler G., and Romani N. An improved isolation method for murine migratory cutaneous dendritic cells. J. Immunol. Methods 193 (1996) 71-79
30. Poulin L.F., Henri S., de Bovis B., Devilard E., Kissenpfennig A., and Malissen B. The dermis contains langerin+ dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204 (2007) 3119-3131
31. Randolph G.J., Ochando J., and Partida-Sánchez S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 26 (2007) 293-316
32. Ravindran R., Rusch L., Itano A., Jenkins M.K., and McSorley S.J. CCR6-dependent recruitment of blood phagocytes is necessary for rapid CD4 T cell responses to local bacterial infection. Proc. Natl. Acad. Sci. USA 104 (2007) 12075-12080
33. Sakoda Y., Hashimoto D., Asakura S., Takeuchi K., Harada M., Tanimoto M., and Teshima T. Donor-derived thymic-dependent T cells cause chronic graft-versus-host disease. Blood 109 (2007) 1756-1764
34. Shiow L.R., Rosen D.B., Brdickova N., Xu Y., An J., Lanier L.L., Cyster J.G., and Matloubian M. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440 (2006) 540-544
35. Shklovskaya E., Roediger B., and Fazekas de St Groth B. Epidermal and dermal dendritic cells display differential activation and migratory behavior while sharing the ability to stimulate CD4+ T cell proliferation in vivo. J. Immunol. 181 (2008) 418-430
36. Shlomchik W.D., Couzens M.S., Tang C.B., McNiff J., Robert M.E., Liu J., Shlomchik M.J., and Emerson S.G. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285 (1999) 412-415
37. Sixt M., Kanazawa N., Selg M., Samson T., Roos G., Reinhardt D.P., Pabst R., Lutz M.B., and Sorokin L. 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 (2005) 19-29
38. Smith A.L., Wikstrom M.E., and Fazekas de St Groth B. Visualizing T cell competition for peptide/MHC complexes: A specific mechanism to minimize the effect of precursor frequency. Immunity 13 (2000) 783-794
39. Soderberg K.A., Payne G.W., Sato A., Medzhitov R., Segal S.S., and Iwasaki A. Innate control of adaptive immunity via remodeling of lymph node feed arteriole. Proc. Natl. Acad. Sci. USA 102 (2005) 16315-16320
40. Sprent J., Miller J.F., and Mitchell G.F. Antigen-induced selective recruitment of circulating lymphocytes. Cell. Immunol. 2 (1971) 171-181
41. Sprent J., and von Boehmer H. Helper function of T cells depleted of alloantigen-reactive lymphocytes by filtration through irradiated F1 hybrid recipients. I. Failure to collaborate with allogeneic B cells in a secondary response to sheep erythrocytes measured in vivo. J. Exp. Med. 144 (1976) 616-626
42. Stenger S., and Modlin R.L. Control of Mycobacterium tuberculosis through mammalian Toll-like receptors. Curr. Opin. Immunol. 14 (2002) 452-457
43. Stoitzner P., Green L.K., Jung J.Y., Price K.M., Tripp C.H., Malissen B., Kissenpfennig A., Hermans I.F., and Ronchese F. Tumor immunotherapy by epicutaneous immunization requires langerhans cells. J. Immunol. 180 (2008) 1991-1998
44. Tacken P.J., de Vries I.J., Torensma R., and Figdor C.G. Dendritic-cell immunotherapy: From ex vivo loading to in vivo targeting. Nat. Rev. Immunol. 7 (2007) 790-802
45. Van V.Q., Lesage S., Bouguermouh S., Gautier P., Rubio M., Levesque M., Nguyen S., Galibert L., and Sarfati M. Expression of the self-marker CD47 on dendritic cells governs their trafficking to secondary lymphoid organs. EMBO J. 25 (2006) 5560-5568
46. Villadangos J.A., and Heath W.R. Life cycle, migration and antigen presenting functions of spleen and lymph node dendritic cells: Limitations of the Langerhans cells paradigm. Semin. Immunol. 17 (2005) 262-272
47. Vremec D., Pooley J., Hochrein H., Wu L., and Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164 (2000) 2978-2986
48. Vremec D., and Shortman K. Dendritic cell subtypes in mouse lymphoid organs: Cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J. Immunol. 159 (1997) 565-573
49. Wang L., Bursch L.S., Kissenpfennig A., Malissen B., Jameson S.C., and Hogquist K.A. Langerin expressing cells promote skin immune responses under defined conditions. J. Immunol. 180 (2008) 4722-4727
50. Zhao X., Deak E., Soderberg K., Linehan M., Spezzano D., Zhu J., Knipe D.M., and Iwasaki A. Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2. J. Exp. Med. 197 (2003) 153-162