Moving to the suburbs: T-cell positioning within lymph nodes during activation and memory

Immunology and Cell Biology

Volumn 93, Issue 4, 2015, Pages 330-336

  Groom, Joanna R ^a,b  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CHEMOKINE; VACCINE;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOARCHITECTURE; EFFECTOR CELL; IMMUNE RESPONSE; LYMPH NODE; LYMPH NODE CELL; LYMPHOCYTE FUNCTION; MEMORY T LYMPHOCYTE; NONHUMAN; REVIEW; T LYMPHOCYTE ACTIVATION; ANIMAL; ANTIGEN PRESENTATION; CELL MOTION; DENDRITIC CELL; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; CELL MOVEMENT; DENDRITIC CELLS; HUMANS; IMMUNOLOGIC MEMORY; LYMPH NODES; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTES; VACCINES;

EID: 84928213781     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2015.29     Document Type: Review

References (86)

1. von Andrian UH, Mackay CR. T-cell function and migration. Two sides of the same coin. N Engl J Med 2000; 343: 1020-1034.
2. Förster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 2008; 8: 362-371.
3. von Andrian UH, Mempel TR. Homing and cellular traffic in lymph nodes. Nat Rev Immunol 2003; 3 pp 867-878.
4. Belz GT, Nutt SL. Transcriptional programming of the dendritic cell network. Nat Rev Immunol 2012; 12: 101-113.
5. Griffith JW, Sokol CL, Luster AD. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu Rev Immunol 2014; 32: 659-702.
6. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K, Bölter J et al. Afferent lymphderived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat Immunol 2011; 12: 879-887.
7. Wendland M, Willenzon S, Kocks J, Davalos-Misslitz AC, Hammerschmidt SI, Schumann K et al. Lymph node T cell homeostasis relies on steady state homing of dendritic cells. Immunity 2011; 35: 945-957.
8. Asperti-Boursin F, Real E, Bismuth G, Trautmann A, Donnadieu E. CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinaseindependent manner. J Exp Med 2007; 204: 1167-1179.
9. Bakocevi? N, Worbs T, Davalos-Misslitz A, Förster R. T cell-dendritic cell interaction dynamics during the induction of respiratory tolerance and immunity. J Immunol 2010; 184: 1317-1327.
10. Okada T, Cyster JG. CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J Immunol 2007; 178: 2973-2978.
11. Worbs T, Mempel TR, Bölter J, von Andrian UH, Förster R. CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J Exp Med 2007; 204: 489-495.
12. Bousso P, Robey E. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 2003; 4: 579-585.
13. Henrickson SE, Mempel TR, Mazo IB, Liu B, Artyomov MN, Zheng H et al. T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol 2008; 9: 282-291.
14. Mempel TR, Henrickson SE, von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004; 427: 154-159.
15. Miller MJ, Safrina O, Parker I, Cahalan MD. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J Exp Med 2004; 200: 847-856.
16. Kastenmüller W, Torabi-Parizi P, Subramanian N, Lämmermann T, Germain RN. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 2012; 150: 1235-1248.
17. Sung JH, Zhang H, Moseman EA, Alvarez D, Iannacone M, Henrickson SE et al. Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell 2012; 150: 1249-1263.
18. Woodruff MC, Heesters BA, Herndon CN, Groom JR, Thomas PG, Luster AD et al. Transnodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine. J Exp Med 2014; 211: 1611-1621.
19. Gerner MY, Kastenmüller W, Ifrim I, Kabat J, Germain RN. Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity 2012; 37: 364-376.
20. Shulman Z, Gitlin AD, Targ S, Jankovic M, Pasqual G, Nussenzweig MC et al. T follicular helper cell dynamics in germinal centers. Science 2013; 341: 673-677.
21. Groom JR, Richmond J, Murooka TT, Sorensen EW, Sung JH, Bankert K et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 2012; 37: 1091-1103.
22. Ulvmar MH, Werth K, Braun A, Kelay P, Hub E, Eller K et al. The atypical chemokine receptor CCRL1 shapes functional CCL21 gradients in lymph nodes. Nat Immunol 2014; 15: 623-630.
23. Weber M, Hauschild R, Schwarz J, Moussion C, de Vries I, Legler DF et al. Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 2013; 339: 328-332.
24. Weber M, Sixt M. Live cell imaging of chemotactic dendritic cell migration in explanted mouse ear preparations. Methods Mol Biol 2013; 1013: 215-226.
25. Katakai T, Hara T, Sugai M, Gonda H, Shimizu A. Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med 2004; 200: 783-795.
26. Chang JE, Turley SJ. Stromal infrastructure of the lymph node and coordination of immunity. Trends Immunol 2015; 36: 30-39.
27. Cremasco V, Woodruff MC, Onder L, Cupovic J, Nieves-Bonilla JM, Schildberg FA et al. B cell homeostasis and follicle confines are governed by fibroblastic reticular cells. Nat Immunol 2014; 15: 973-981.
28. Förster R, Mattis AE, Kremmer E, Wolf E, Brem G, Lipp M. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 1996; 87: 1037-1047.
29. Gunn MD, Ngo VN, Ansel KM, Ekland EH, Cyster JG, Williams LT. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 1998; 391: 799-803.
30. Katakai T, Hara T, Lee J-H, Gonda H, Sugai M, Shimizu A. A novel reticular stromal structure in lymph node cortex: an immuno-platform for interactions among dendritic cells, T cells and B cells. Int Immunol 2004; 16: 1133-1142.
31. Grigorova IL, Schwab SR, Phan TG, Pham THM, Okada T, Cyster JG. Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat Immunol 2009; 10: 58-65.
32. Pham THM, Okada T, Matloubian M, Lo CG, Cyster JG. S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 2008; 28: 122-133.
33. Cahalan MD, Parker I. Choreography of cell motility and interaction dynamics imaged by two-photon microscopy in lymphoid organs. Annu Rev Immunol 2008; 26: 585-626.
34. Mori S, Nakano H, Aritomi K, Wang CR, Gunn MD, Kakiuchi T. Mice lacking expression of the chemokines CCL21-ser and CCL19 (plt mice) demonstrate delayed but enhanced T cell immune responses. J Exp Med 2001; 193: 207-218.
35. Hickman HD, Takeda K, Skon CN, Murray FR, Hensley SE, Loomis J et al. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat Immunol 2008; 9: 155-165.
36. Chtanova T, Han S-J, Schaeffer M, van Dooren GG, Herzmark P, Striepen B et al. Dynamics of T cell, antigen-presenting cell, and pathogen interactions during recall responses in the lymph node. Immunity 2009; 31: 342-355.
37. Castellino F, Huang AY, Altan-Bonnet G, Stoll S, Scheinecker C, Germain RN. Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell-dendritic cell interaction. Nature 2006; 440: 890-895.
38. Hugues S, Scholer A, Boissonnas A, Nussbaum A, Combadière C, Amigorena S et al. Dynamic imaging of chemokine-dependent CD8+ T cell help for CD8+ T cell responses. Nat Immunol 2007; 8: 921-930.
39. Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U et al. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 2010; 11: 313-320.
40. Kastenmüller W, Brandes M, Wang Z, Herz J, Egen JG, Germain RN. Peripheral prepositioning and local CXCL9 chemokine-mediated guidance orchestrate rapid memory CD8+ T cell responses in the lymph node. Immunity 2013; 38: 502-513.
41. Gerner MY, Torabi-Parizi P, Germain RN. Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. Immunity 2015; 42: 172-185.
42. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annu Rev Immunol 2010; 28: 445-489.
43. Kerfoot SM, Yaari G, Patel JR, Johnson KL, Gonzalez DG, Kleinstein SH et al. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011; 34: 947-960.
44. Haynes NM, Allen CD, Lesley R, Ansel KM, Killeen N, Cyster JG. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J Immunol 2007; 179: 5099-5108.
45. Xu H, Li X, Liu D, Li J, Zhang X, Chen X et al. Follicular T-helper cell recruitment governed by bystander B cells and ICOS-driven motility. Nature 2013; 496: 523-527.
46. León B, Ballesteros-Tato A, Browning JL, Dunn R, Randall TD, Lund FE. Regulation of T (H)2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat Immunol 2012; 13: 681-690.
47. Shulman Z, Gitlin AD, Weinstein JS, Lainez B, Esplugues E, Flavell RA et al. Dynamic signaling by T follicular helper cells during germinal center B cell selection. Science 2014; 345: 1058-1062.
48. Moriyama S, Takahashi N, Green JA, Hori S, Kubo M, Cyster JG et al. Sphingosine-1-phosphate receptor 2 is critical for follicular helper T cell retention in germinal centers. J Exp Med 2014; 211: 1297-1305.
49. Groom JR, Luster AD. CXCR3 in T cell function. Exp Cell Res 2011; 317: 620-631.
50. Groom JR, Luster AD. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 2011; 89: 207-215.
51. Gonzalez SF, Lukacs-Kornek V, Kuligowski MP, Pitcher LA, Degn SE, Kim Y-A et al. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat Immunol 2010; 11: 427-434.
52. Nakayamada S, Kanno Y, Takahashi H, Jankovic D, Lu KT, Johnson TA et al. Early Th1 cell differentiation is marked by a Tfh cell-like transition. Immunity 2011; 35: 919-931.
53. Blair DA, Turner DL, Bose TO, Pham Q-M, Bouchard KR, Williams KJ et al. Duration of antigen availability influences the expansion and memory differentiation of T cells. J Immunol 2011; 187: 2310-2321.
54. Zehn D, Lee SY, Bevan MJ. Complete but curtailed T-cell response to very low-affinity antigen. Nature 2009; 459: 211-214.
55. Hu JK, Kagari T, Clingan JM, Matloubian M. Expression of chemokine receptor CXCR3 on T cells affects the balance between effector and memory CD8 T-cell generation. Proc Natl Acad Sci USA 2011; 108: E118-E127.
56. Kohlmeier JE, Reiley WW, Perona-Wright G, Freeman ML, Yager EJ, Connor LM et al. Inflammatory chemokine receptors regulate CD8(+) T cell contraction and memory generation following infection. J Exp Med 2011; 208: 1621-1634.
57. Kurachi M, Kurachi J, Suenaga F, Tsukui T, Abe J, Ueha S et al. Chemokine receptor CXCR3 facilitates CD8(+) T cell differentiation into short-lived effector cells leading to memory degeneration. J Exp Med 2011; 208: 1605-1620.
58. Masopust D, Schenkel JM. The integration of T cell migration, differentiation and function. Nat Rev Immunol 2013; 13: 309-320.
59. Sallusto F, Lenig D, Förster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999; 401: 708-712.
60. Kastenmüller W, Kastenmüller K, Kurts C, Seder RA. Dendritic cell-targeted vaccines-hope or hype? Nat Rev Immunol 2014; 14: 705-711.
61. Mueller SN, Gebhardt T, Carbone FR, Heath WR. Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 2013; 31: 137-161.
62. Cinamon G, Matloubian M, Lesneski MJ, Xu Y, Low C, Lu T et al. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat Immunol 2004; 5: 713-720.
63. Cyster JG, Schwab SR. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 2012; 30: 69-94.
64. Baekkevold ES, Wurbel M-A, Kivisäkk P, Wain CM, Power CA, Haraldsen G et al. A role for CCR4 in development of mature circulating cutaneous T helper memory cell populations. J Exp Med 2005; 201: 1045-1051.
65. Hale JS, Youngblood B, Latner DR, Mohammed AUR, Ye L, Akondy RS et al. Distinct memory CD4+ T cells with commitment to T follicular helper-and T helper 1-cell lineages are generated after acute viral infection. Immunity 2013; 38: 805-817.
66. Sixt M, Kanazawa N, Selg M, Samson T, Roos G, Reinhardt DP et al. The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity 2005; 22: 19-29.
67. Chtanova T, Schaeffer M, Han S-J, van Dooren GG, Nollmann M, Herzmark P et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 2008; 29: 487-496.
68. Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007; 450: 110-114.
69. Phan TG, Grigorova I, Okada T, Cyster JG. Subcapsular encounter and complementdependent transport of immune complexes by lymph node B cells. Nat Immunol 2007; 8: 992-1000.
70. Gaya M, Castello A, Montaner B, Rogers N, Reis e Sousa C, Bruckbauer A et al. Host response. Inflammation-induced disruption of SCS macrophages impairs B cell responses to secondary infection. Science 2015; 347: 667-672.
71. Grigorova IL, Panteleev M, Cyster JG. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci USA 2010; 107: 20447-20452.
72. Belz GT, Bedoui S, Kupresanin F, Carbone FR, Heath WR. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat Immunol 2007; 8: 1060-1066.
73. Garcia Z, Lemaître F, van Rooijen N, Albert ML, Levy Y, Schwartz O et al. Subcapsular sinus macrophages promote NK cell accumulation and activation in response to lymphborne viral particles. Blood 2012; 120: 4744-4750.
74. Gray EE, Friend S, Suzuki K, Phan TG, Cyster JG. Subcapsular sinus macrophage fragmentation and CD169+ bleb acquisition by closely associated IL-17-committed innate-like lymphocytes. PLoS ONE 2012; 7: e38258.
75. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 2009; 10: 786-793.
76. Astarita JL, Cremasco V, Fu J, Darnell MC, Peck JR, Nieves-Bonilla JM et al. The CLEC-2-podoplanin axis controls the contractility of fibroblastic reticular cells and lymph node microarchitecture. Nat Immunol 2015; 16: 75-84.
77. Yoneyama H, Matsuno K, Toda E, Nishiwaki T, Matsuo N, Nakano A et al. Plasmacytoid DCs help lymph node DCs to induce anti-HSV CTLs. J Exp Med 2005; 202: 425-435.
78. Wiesel M, Crouse J, Bedenikovic G, Sutherland A, Joller N, Oxenius A. Type-I IFN drives the differentiation of short-lived effector CD8+ T cells in vivo. Eur J Immunol 2012; 42: 320-329.
79. Liu H, Moynihan KD, Zheng Y, Szeto GL, Li AV, Huang B et al. Structure-based programming of lymph-node targeting in molecular vaccines. Nature 2014; 507: 519-522.
80. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996; 274: 94-96.
81. Moon JJ, Chu HH, Pepper M, McSorley SJ, Jameson SC, Kedl RM et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 2007; 27: 203-213.
82. Pepper M, Jenkins MK. Origins of CD4(+) effector and central memory T cells. Nat Immunol 2011; 12: 467-471.
83. Tubo NJ, Pagán AJ, Taylor JJ, Nelson RW, Linehan JL, Ertelt JM et al. Single naive CD4 + T cells from a diverse repertoire produce different effector cell types during infection. Cell 2013; 153: 785-796.
84. Khanna KM, McNamara JT, Lefrançois L. In situ imaging of the endogenous CD8 T cell response to infection. Science 2007; 318: 116-120.
85. King IL, Amiel E, Tighe M, Mohrs K, Veerapen N, Besra G et al. The mechanism of splenic invariant NKT cell activation dictates localization in vivo. J Immunol 2013; 191: 572-582.
86. Becattini S, Latorre D, Mele F, Foglierini M, De Gregorio C, Cassotta A et al. Functional heterogeneity of human memory CD4+ T cell clones primed by pathogens or vaccines. Science 2015; 347: 400-406.