Retention of Ag-specific memory CD4+ T cells in the draining lymph node indicates lymphoid tissue resident memory populations

European Journal of Immunology

Volumn 47, Issue 5, 2017, Pages 860-871

  Marriott, Clare L ^a   Dutton, Emma E ^a   Tomura, Michio ^b   Withers, David R ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b OSAKA OHTANI UNIVERSITY   (Japan)

Author keywords

Cell trafficking; Lymph nodes; Memory CD4+ T cells; Memory cells

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL POPULATION; CONTROLLED STUDY; EX VIVO STUDY; FLOW CYTOMETRY; LYMPH NODE; LYMPHOCYTE MIGRATION; LYMPHOCYTE RECIRCULATION; LYMPHOID TISSUE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANATOMY AND HISTOLOGY; ANIMAL; CELL MOTION; CYTOLOGY; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; IMMUNIZATION; IMMUNOLOGIC MEMORY; LYMPH NODES; LYMPHOID TISSUE; MICE; T-LYMPHOCYTE SUBSETS;

EID: 85017465124     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201646681     Document Type: Article

References (29)

1. Sprent, J. and Surh, C. D., T-cell memory. Annu. Rev. Immunol. 2002. 20: 551–579.
2. Sallusto, F., Lenig, D., Forster, R., Lipp, M. and Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999. 401: 708–712.
3. Pepper, M., Pagan, A. J., Igyarto, B. Z., Taylor, J. J. and Jenkins, M. K., Opposing signals from the Bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011. 35: 583–595.
4. Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R. and Carbone, F. R., Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 2009. 10: 524–530.
5. Masopust, D., Choo, D., Vezys, V., Wherry, E. J., Duraiswamy, J., Akondy, R., Wang, J. et al., Dynamic T-cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 2010. 207: 553–564.
6. Teijaro, J. R., Turner, D., Pham, Q., Wherry, E. J., Lefrancois, L. and Farber, D. L., Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol. 2011. 187: 5510–5514.
7. Schenkel, J. M. and Masopust, D., Tissue-resident memory T cells. Immunity 2014. 41: 886–897.
8. Vander Lugt, B., Tubo, N. J., Nizza, S. T., Boes, M., Malissen, B., Fuhlbrigge, R. C., Kupper, T. S. et al., CCR7 plays no appreciable role in trafficking of central memory CD4 T cells to lymph nodes. J. Immunol. 2013. 191: 3119–3127.
9. Mohammed, R. N., Watson, H. A., Vigar, M., Ohme, J., Thomson, A., Humphreys, I. R. and Ager, A., L-selectin is essential for delivery of activated CD8(+) T cells to virus-infected organs for protective immunity. Cell Rep. 2016. 14: 760–771.
10. Tomura, M., Yoshida, N., Tanaka, J., Karasawa, S., Miwa, Y., Miyawaki, A. and Kanagawa, O., Monitoring cellular movement in vivo with photoconvertible fluorescence protein “Kaede” transgenic mice. Proc. Natl. Acad. Sci. USA. 2008. 105: 10871–10876.
11. Bromley, S. K., Yan, S., Tomura, M., Kanagawa, O. and Luster, A. D., Recirculating memory T cells are a unique subset of CD4+ T cells with a distinct phenotype and migratory pattern. J. Immunol. 2013. 190: 970-976.
12. Ugur, M., Schulz, O., Menon, M. B., Krueger, A. and Pabst, O., Resident CD4+ T cells accumulate in lymphoid organs after prolonged Ag exposure. Nat. Commun. 2014. 5: 4821.
13. 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 2007. 27: 203–213.
14. Moon, J. J., Chu, H. H., Hataye, J., Pagan, A. J., Pepper, M., McLachlan, J. B., Zell, T. et al., Tracking epitope-specific T cells. Nat. Protocol. 2009. 4: 565–581.
15. Pepper, M., Linehan, J. L., Pagan, A. J., Zell, T., Dileepan, T., Cleary, P. P. and Jenkins, M. K., Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 2010. 11: 83–89.
16. Luther, S. A., Serre, K., Cunningham, A. F., Khan, M., Acha-Orbea, H., MacLennan, I. C. and Toellner, K. M., Recirculating CD4 memory T cells mount rapid secondary responses without major contributions from follicular CD4 effectors and B cells. Eur. J. Immunol. 2007. 37: 1476–1484.
17. Cucak, H., Yrlid, U., Reizis, B., Kalinke, U. and Johansson-Lindbom, B., Type I interferon signaling in dendritic cells stimulates the development of lymph-node-resident T follicular helper cells. Immunity 2009. 31: 491–501.
18. Shulman, Z., Gitlin, A. D., Targ, S., Jankovic, M., Pasqual, G., Nussenzweig, M. C. and Victora, G. D., T follicular helper cell dynamics in germinal centers. Science 2013. 341: 673–677.
19. Berg, E. L., Robinson, M. K., Warnock, R. A. and Butcher, E. C., The human peripheral lymph node vascular addressin is a ligand for LECAM-1, the peripheral lymph node homing receptor. J. Cell Biol. 1991. 114: 343–349.
20. Bradley, L. M., Watson, S. R. and Swain, S. L., Entry of naive CD4 T cells into peripheral lymph nodes requires L-selectin. J. Exp. Med. 1994. 180: 2401–2406.
21. Bradley, L. M., Atkins, G. G. and Swain, S. L., Long-term CD4+ memory T cells from the spleen lack MEL-14, the lymph node homing receptor. J. Immunol. 1992. 148: 324–331.
22. Williams, M. B. and Butcher, E. C., Homing of naive and memory T lymphocyte subsets to Peyer's patches, lymph nodes, and spleen. J. Immunol. 1997. 159: 1746–1752.
23. Mizuno, H., Mal, T. K., Tong, K. I., Ando, R., Furuta, T., Ikura, M. and Miyawaki, A., Photo-induced peptide cleavage in the green-to-red conversion of a fluorescent protein. Mol. Cell 2003. 12: 1051–1058.
24. Hutchison, S., Benson, R. A., Gibson, V. B., Pollock, A. H., Garside, P. and Brewer, J. M., Ag depot is not required for alum adjuvanticity. FASEB J. 2012. 26: 1272–1279.
25. Mackay, L. K., Braun, A., Macleod, B. L., Collins, N., Tebartz, C., Bedoui, S., Carbone, F. R. and Gebhardt, T., Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T-cell retention. J. Immunol. 2015. 194: 2059–2063.
26. Fazilleau, N., Eisenbraun, M. D., Malherbe, L., Ebright, J. N., Pogue-Caley, R. R., McHeyzer-Williams, L. J. and McHeyzer-Williams, M. G., Lymphoid reservoirs of Ag-specific memory T helper cells. Nat. Immunol. 2007. 8: 753–761.
27. Guo, L., Huang, Y., Chen, X., Hu-Li, J., Urban, J. F., Jr. and Paul, W. E., Innate immunological function of TH2 cells in vivo. Nat. Immunol. 2015. 16: 1051–1059.
28. Marriott, C. L., Mackley, E. C., Ferreira, C., Veldhoen, M., Yagita, H. and Withers, D. R., OX40 controls effector CD4+ T-cell expansion, not follicular T helper cell generation in acute Listeria infection. Eur. J. Immunol. 2014. 44: 2437–2447.
29. Marriott, C. L., Carlesso, G., Herbst, R. and Withers, D. R., ICOS is required for the generation of both central and effector CD4(+) memory T-cell populations following acute bacterial infection. Eur. J. Immunol. 2015. 45: 1706–1715.