Trans-nodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine

Journal of Experimental Medicine

Volumn 211, Issue 8, 2014, Pages 1611-1621

  Woodruff, Matthew C ^a,b   Heesters, Balthasar A ^b,c   Herndon, Caroline N ^b   Groom, Joanna R ^d   Thomas, Paul G ^e   Luster, Andrew D ^a,f   Turley, Shannon J ^a,g   Carroll, Michael C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INFLUENZA VACCINE; VIRUS ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; GERMINAL CENTER; INFLUENZA VACCINATION; LYMPH NODE; LYMPH NODE RESIDENT DENDRITIC CELL; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIRUS IMMUNITY;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, VIRAL; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CHEMOKINES; CLUSTER ANALYSIS; DENDRITIC CELLS; IMMUNITY; IMMUNOLOGIC MEMORY; INFLUENZA VACCINES; LYMPH; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, CXCR3; SPECIES SPECIFICITY; VACCINATION;

EID: 84905111574     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20132327     Document Type: Article

References (43)

1. Acton, S.E., J.L. Astarita, D. Malhotra, V. Lukacs-Kornek, B. Franz, P.R. Hess, Z. Jakus, M. Kuligowski, A.L. Fletcher, K.G. Elpek, et al. 2012. Podoplaninrich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity. 37:276-289. http://dx.doi .org/10.1016/j.immuni.2012.05.022.
2. Allan, R.S., J. Waithman, S. Bedoui, C.M. Jones, J.A. Villadangos, Y. Zhan, A.M. Lew, K. Shortman, W.R. Heath, and F.R. Carbone. 2006. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity. 25:153-162. http://dx.doi.org/10.1016/j.immuni.2006.04.017.
3. 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.
4. Alvarez, D., E.H. Vollmann, and U.H. von Andrian. 2008. Mechanisms and consequences of dendritic cell migration. Immunity. 29:325-342. http://dx.doi.org/10.1016/j.immuni.2008.08.006.
5. Arnason, J., and D. Avigan. 2012. Evolution of cellular immunotherapy: from allogeneic transplant to dendritic cell vaccination as treatment for multiple myeloma. Immunotherapy. 4:1043-1051. http://dx.doi.org/10.2217/imt.12.118.
6. Austyn, J.M. 1996. New insights into the mobilization and phagocytic activity of dendritic cells. J. Exp. Med. 183:1287-1292. http://dx.doi.org/10 .1084/jem.183.4.1287.
7. Braun, A., T. Worbs, G.L. Moschovakis, S. Halle, K. Hoffmann, J. Bölter, A. Münk, and R. Förster. 2011. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat. Immunol. 12:879-887. http://dx.doi.org/10.1038/ni.2085.
8. Carpenter, A.E., T.R. Jones, M.R. Lamprecht, C. Clarke, I.H. Kang, O. Friman, D.A. Guertin, J.H. Chang, R.A. Lindquist, J. Moffat, et al. 2006. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7:R100. http://dx.doi.org/10.1186/gb-2006-7-10-r100.
9. Carrasco, Y.R., and F.D. Batista. 2007. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity. 27:160-171. http://dx.doi .org/10.1016/j.immuni.2007.06.007.
10. Ertürk, A., C.P. Mauch, F. Hellal, F. Förstner, T. Keck, K. Becker, N. Jährling, H. Steffens, M. Richter, M. Hübener, et al. 2012. Three-dimensional imaging of the unsectioned adult spinal cord to assess axon regeneration and glial responses after injury. Nat. Med. 18:166-171. http://dx.doi.org/10.1038/nm.2600.
11. Gerner, M.Y., W. Kastenmuller, I. Ifrim, J. Kabat, and R.N. Germain. 2012. Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity. 37:364-376. http://dx.doi.org/10.1016/j.immuni.2012.07.011.
12. Gonzalez, S.F., 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, and M.C. Carroll. 2010. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 11:427-434. http://dx.doi.org/10.1038/ni.1856.
13. Gray, E.E., and J.G. Cyster. 2012. Lymph node macrophages. J. Innate Immun. 4:424-436. http://dx.doi.org/10.1159/000337007.
14. Grigorova, I.L., M. Panteleev, and J.G. Cyster. 2010. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. USA. 107:20447-20452. http://dx.doi.org/10.1073/pnas.1009968107.
15. + T helper 1 cell differentiation. Immunity. 37:1091-1103. http://dx.doi.org/10.1016/j.immuni.2012.08.016.
16. + T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9:155-165. http://dx.doi.org/10.1038/ni1557.
17. Hill, M., M. Segovia, and M.C. Cuturi. 2011. What is the role of antigenprocessing mechanisms in autologous tolerogenic dendritic cell therapy in organ transplantation? Immunotherapy. 3:12-14. http://dx.doi.org/10 .2217/imt.11.40.
18. 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 cellmediated immunity. Immunity. 19:47-57. http://dx.doi.org/10.1016/S1074-7613(03)00175-4.
19. Jones, T.R., I.H. Kang, D.B. Wheeler, R.A. Lindquist, A. Papallo, D.M. Sabatini, P. Golland, and A.E. Carpenter. 2008. CellProfiler Analyst: data exploration and analysis software for complex image-based screens. BMC Bioinformatics. 9:482. http://dx.doi.org/10.1186/1471-2105-9-482.
20. Junt, T., E.A. Moseman, M. Iannacone, S. Massberg, P.A. Lang, M. Boes, K. Fink, S.E. Henrickson, D.M. Shayakhmetov, N.C. Di Paolo, et al. 2007. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature. 450:110-114. http://dx.doi.org/10.1038/nature06287.
21. Kastenmüller, W., M. Brandes, Z. Wang, J. Herz, J.G. Egen, and R.N. Germain. 2013. Peripheral prepositioning and local CXCL9 chemokine-mediated guidance orchestrate rapid memory CD8+ T cell responses in the lymph node. Immunity. 38:502-513. http://dx.doi.org/10.1016/j.immuni.2012.11.012.
22. 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.
23. Lämmermann, T., B.L. Bader, S.J. Monkley, T. Worbs, R. Wedlich-Söldner, K. Hirsch, M. Keller, R. Förster, D.R. Critchley, R. Fässler, and M. Sixt. 2008. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature. 453:51-55. http://dx.doi.org/10.1038/nature06887.
24. Larsen, C.P., R.M. Steinman, M. Witmer-Pack, D.F. Hankins, P.J. Morris, and J.M. Austyn. 1990. Migration and maturation of Langerhans cells in skin transplants and explants. J. Exp. Med. 172:1483-1493. http://dx.doi.org/10.1084/jem.172.5.1483.
25. + dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13:681-690. http://dx.doi.org/10.1038/ni.2309.
26. Lindquist, R.L., G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M.L. Dustin, and M.C. Nussenzweig. 2004. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5:1243-1250. http://dx.doi.org/10.1038/ni1139.
27. Liu, H., K.D. Moynihan, Y. Zheng, G.L. Szeto, A.V. Li, B. Huang, D.S. Van Egeren, C. Park, and D.J. Irvine. 2014. Structure-based programming of lymph-node targeting in molecular vaccines. Nature. 507:519-522. http://dx.doi.org/10.1038/nature12978.
28. Llanos, C., L.J. Carreño, and A.M. Kalergis. 2011. Contribution of dendritic cell/T cell interactions to triggering and maintaining autoimmunity. Biol. Res. 44:53-61. http://dx.doi.org/10.4067/S0716-97602011000100007.
29. Moodycliffe, A.M., I. Kimber, and M. Norval. 1994. Role of tumour necrosis factor-alpha in ultraviolet B light-induced dendritic cell migration and suppression of contact hypersensitivity. Immunology. 81:79-84.
30. Phan, T.G., I. Grigorova, T. Okada, and J.G. Cyster. 2007. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8:992-1000. http://dx.doi.org/10.1038/ni1494.
31. Poudrier, J., J. Chagnon-Choquet, and M. Roger. 2012. Influence of dendritic cells on B-cell responses during HIV infection. Clin. Dev. Immunol. 2012:592187. http://dx.doi.org/10.1155/2012/592187.
32. Qi, H., J.G. Egen, A.Y.C. Huang, and R.N. Germain. 2006. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science. 312:1672-1676. http://dx.doi.org/10.1126/science.1125703.
33. Randolph, G.J., V. Angeli, and M.A. Swartz. 2005. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol. 5:617-628. http://dx.doi.org/10.1038/nri1670.
34. Rescigno, M., C. Winzler, D. Delia, C. Mutini, M. Lutz, and P. Ricciardi-Castagnoli. 1997. Dendritic cell maturation is required for initiation of the immune response. J. Leukoc. Biol. 61:415-421.
35. Roozendaal, R., T.R. Mempel, L.A. Pitcher, S.F. Gonzalez, A. Verschoor, R.E. Mebius, U.H. von Andrian, and M.C. Carroll. 2009. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity. 30:264-276. http://dx.doi.org/10.1016/j.immuni.2008.12.014.
36. Steinman, R.M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271-296. http://dx.doi.org/10.1146/annurev.iy.09.040191.001415.
37. Steinman, R.M., M. Pack, and K. Inaba. 1997. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 156:25-37. http://dx.doi.org/10.1111/j.1600-065X.1997.tb00956.x.
38. Sung, J.H., H. Zhang, E.A. Moseman, D. Alvarez, M. Iannacone, S.E. Henrickson, J.C. de la Torre, J.R. Groom, A.D. Luster, and U.H. von Andrian. 2012. Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell. 150:1249-1263. http://dx.doi.org/10.1016/j.cell.2012.08.015.
39. Szakal, A.K., K.L. Holmes, and J.G. Tew. 1983. Transport of immune complexes from the subcapsular sinus to lymph node follicles on the surface of nonphagocytic cells, including cells with dendritic morphology. J. Immunol. 131:1714-1727.
40. Szretter, K.J., A.L. Balish, and J.M. Katz. 2006. Influenza: propagation, quantification, and storage. Curr. Protoc. Microbiol. Chapter 15:Unit 15G.1.
41. Tal, O., H.Y. Lim, I. Gurevich, I. Milo, Z. Shipony, L.G. Ng, V. Angeli, and G. Shakhar. 2011. DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J. Exp. Med. 208:2141-2153. http://dx.doi.org/10.1084/jem.20102392.
42. Thomas, P.G., S.A. Brown, W. Yue, J. So, R.J. Webby, and P.C. Doherty. 2006. An unexpected antibody response to an engineered influenza virus modifies CD8+ T cell responses. Proc. Natl. Acad. Sci. USA. 103:2764-2769. http://dx.doi.org/10.1073/pnas.0511185103.
43. Yen, J.-H., T. Khayrullina, and D. Ganea. 2008. PGE2-induced metalloproteinase-9 is essential for dendritic cell migration. Blood. 111:260-270. http://dx.doi .org/10.1182/blood-2007-05-090613.