Tuning of Antigen Sensitivity by T Cell Receptor-Dependent Negative Feedback Controls T Cell Effector Function in Inflamed Tissues

Immunity

Volumn 40, Issue 2, 2014, Pages 235-247

  Honda, Tetsuya ^a   Egen, Jackson G ^a,c   Lämmermann, Tim ^a   Kastenmüller, Wolfgang ^a   Torabi Parizi, Parizad ^a,b   Germain, Ronald N ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS; CELL MOVEMENT; FEEDBACK, PHYSIOLOGICAL; FLOW CYTOMETRY; INFLAMMATION; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; SKIN; T-LYMPHOCYTES;

EID: 84894082425     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.11.017     Document Type: Article

References (54)

1. Ariotti S., Beltman J.B., Chodaczek G., Hoekstra M.E., van Beek A.E., Gomez-Eerland R., Ritsma L., van Rheenen J., Marée A.F., Zal T., et al. Tissue-resident memory CD8+ Tcells continuously patrol skin epithelia to quickly recognize local antigen. Proc. Natl. Acad. Sci. USA 2012, 109:19739-19744.
2. Azar G.A., Lemaître F., Robey E.A., Bousso P. Subcellular dynamics of Tcell immunological synapses and kinapses in lymph nodes. Proc. Natl. Acad. Sci. USA 2010, 107:3675-3680.
3. Barnden M.J., Allison J., Heath W.R., Carbone F.R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998, 76:34-40.
4. Bartholomäus I., Kawakami N., Odoardi F., Schläger C., Miljkovic D., Ellwart J.W., Klinkert W.E., Flügel-Koch C., Issekutz T.B., Wekerle H., Flügel A. Effector Tcell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 2009, 462:94-98.
5. Beattie L., Peltan A., Maroof A., Kirby A., Brown N., Coles M., Smith D.F., Kaye P.M. Dynamic imaging of experimental Leishmania donovani-induced hepatic granulomas detects Kupffer cell-restricted antigen presentation to antigen-specific CD8 Tcells. PLoS Pathog. 2010, 6:e1000805.
6. Bhakta N.R., Oh D.Y., Lewis R.S. Calcium oscillations regulate thymocyte motility during positive selection in the three-dimensional thymic environment. Nat. Immunol. 2005, 6:143-151.
7. Bousso P., Robey E. Dynamics of CD8+ Tcell priming by dendritic cells in intact lymph nodes. Nat. Immunol. 2003, 4:579-585.
8. Campbell D.J., Butcher E.C. Rapid acquisition of tissue-specific homing phenotypes by CD4(+) Tcells activated in cutaneous or mucosal lymphoid tissues. J.Exp. Med. 2002, 195:135-141.
9. Chodaczek G., Papanna V., Zal M.A., Zal T. Body-barrier surveillance by epidermal γδ TCRs. Nat. Immunol. 2012, 13:272-282.
10. Downey J., Smith A., Schneider H., Hogg N., Rudd C.E. TCR/CD3 mediated stop-signal is decoupled in T-cells from Ctla4 deficient mice. Immunol. Lett. 2008, 115:70-72.
11. Dustin M.L. Stop and go traffic to tune Tcell responses. Immunity 2004, 21:305-314.
12. Egen J.G., Allison J.P. Cytotoxic T lymphocyte antigen-4 accumulation in the immunological synapse is regulated by TCR signal strength. Immunity 2002, 16:23-35.
13. Egen J.G., Rothfuchs A.G., Feng C.G., Winter N., Sher A., Germain R.N. Macrophage and Tcell dynamics during the development and disintegration of mycobacterial granulomas. Immunity 2008, 28:271-284.
14. Egen J.G., Rothfuchs A.G., Feng C.G., Horwitz M.A., Sher A., Germain R.N. Intravital imaging reveals limited antigen presentation and Tcell effector function in mycobacterial granulomas. Immunity 2011, 34:807-819.
15. Fife B.T., Pauken K.E., Eagar T.N., Obu T., Wu J., Tang Q., Azuma M., Krummel M.F., Bluestone J.A. Interactions between PD-1 andPD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 2009, 10:1185-1192.
16. Filipe-Santos O., Pescher P., Breart B., Lippuner C., Aebischer T., Glaichenhaus N., Späth G.F., Bousso P. A dynamic map of antigen recognition by CD4 Tcells at the site of Leishmania major infection. Cell Host Microbe 2009, 6:23-33.
17. Gattinoni L., Lugli E., Ji Y., Pos Z., Paulos C.M., Quigley M.F., Almeida J.R., Gostick E., Yu Z., Carpenito C., et al. A human memory Tcell subset with stem cell-like properties. Nat. Med. 2011, 17:1290-1297.
18. Gebhardt T., Whitney P.G., Zaid A., Mackay L.K., Brooks A.G., Heath W.R., Carbone F.R., Mueller S.N. Different patterns of peripheral migration by memory CD4+ and CD8+ Tcells. Nature 2011, 477:216-219.
19. Germain R.N., Robey E.A., Cahalan M.D. A decade of imaging cellular motility and interaction dynamics in the immune system. Science 2012, 336:1676-1681.
20. Grossman Z., Paul W.E. Adaptive cellular interactions in the immune system: the tunable activation threshold and the significance of subthreshold responses. Proc. Natl. Acad. Sci. USA 1992, 89:10365-10369.
21. Hafalla J.C., Claser C., Couper K.N., Grau G.E., Renia L., de Souza J.B., Riley E.M. The CTLA-4 and PD-1/PD-L1 inhibitory pathways independently regulate host resistance to Plasmodium-induced acute immune pathology. PLoS Pathog. 2012, 8:e1002504.
22. Islam S.A., Luster A.D. T cell homing to epithelial barriers in allergic disease. Nat. Med. 2012, 18:705-715.
23. Kawakami N., Nägerl U.V., Odoardi F., Bonhoeffer T., Wekerle H., Flügel A. Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J.Exp. Med. 2005, 201:1805-1814.
24. Kearney E.R., Pape K.A., Loh D.Y., Jenkins M.K. Visualization ofpeptide-specific Tcell immunity and peripheral tolerance induction invivo. Immunity 1994, 1:327-339.
25. Kim J.V., Kang S.S., Dustin M.L., McGavern D.B. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acuteviral meningitis. Nature 2009, 457:191-195.
26. Lindquist R.L., Shakhar G., Dudziak D., Wardemann H., Eisenreich T., Dustin M.L., Nussenzweig M.C. Visualizing dendritic cell networks invivo. Nat. Immunol. 2004, 5:1243-1250.
27. Linsley P.S., Bradshaw J., Greene J., Peach R., Bennett K.L., Mittler R.S. Intracellular trafficking of CTLA-4 and focal localization towards sites of TCR engagement. Immunity 1996, 4:535-543.
28. Masters B.R., So P.T., Buehler C., Barry N., Sutin J.D., Mantulin W.W., Gratton E. Mitigating thermal mechanical damage potential during two-photon dermal imaging. J.Biomed. Opt. 2004, 9:1265-1270.
29. Matheu M.P., Beeton C., Garcia A., Chi V., Rangaraju S., Safrina O., Monaghan K., Uemura M.I., Li D., Pal S., et al. Imaging of effector memory Tcells during a delayed-type hypersensitivity reaction and suppression by Kv1.3 channel block. Immunity 2008, 29:602-614.
30. Mempel T.R., Henrickson S.E., Von Andrian U.H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 2004, 427:154-159.
31. Miller M.J., Wei S.H., Parker I., Cahalan M.D. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 2002, 296:1869-1873.
32. Mora J.R., Bono M.R., Manjunath N., Weninger W., Cavanagh L.L., Rosemblatt M., Von Andrian U.H. Selective imprinting of gut-homing Tcells by Peyer's patch dendritic cells. Nature 2003, 424:88-93.
33. Müller A.J., Filipe-Santos O., Eberl G., Aebischer T., Späth G.F., Bousso P. CD4+ Tcells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity 2012, 37:147-157.
34. Negulescu P.A., Krasieva T.B., Khan A., Kerschbaum H.H., Cahalan M.D. Polarity of Tcell shape, motility, and sensitivity to antigen. Immunity 1996, 4:421-430.
35. Reinhardt R.L., Bullard D.C., Weaver C.T., Jenkins M.K. Preferential accumulation of antigen-specific effector CD4 Tcells at an antigen injection site involves CD62E-dependent migration but not local proliferation. J.Exp. Med. 2003, 197:751-762.
36. Sadik C.D., Luster A.D. Lipid-cytokine-chemokine cascades orchestrate leukocyte recruitment in inflammation. J.Leukoc. Biol. 2012, 91:207-215.
37. Sancho D., Vicente-Manzanares M., Mittelbrunn M., Montoya M.C., Gordón-Alonso M., Serrador J.M., Sánchez-Madrid F. Regulation of microtubule-organizing center orientation and actomyosin cytoskeleton rearrangement during immune interactions. Immunol. Rev. 2002, 189:84-97.
38. Schaefer B.C., Schaefer M.L., Kappler J.W., Marrack P., Kedl R.M. Observation of antigen-dependent CD8+ T-cell/ dendritic cell interactions invivo. Cell. Immunol. 2001, 214:110-122.
39. Schaeffer M., Han S.J., Chtanova T., van Dooren G.G., Herzmark P., Chen Y., Roysam B., Striepen B., Robey E.A. Dynamic imaging of Tcell-parasite interactions in the brains of mice chronically infected with Toxoplasma gondii. J.Immunol. 2009, 182:6379-6393.
40. Schneider H., Downey J., Smith A., Zinselmeyer B.H., Rush C., Brewer J.M., Wei B., Hogg N., Garside P., Rudd C.E. Reversal of the TCR stop signal by CTLA-4. Science 2006, 313:1972-1975.
41. Schneider H., Smith X., Liu H., Bismuth G., Rudd C.E. CTLA-4 disrupts ZAP70 microcluster formation with reduced Tcell/APC dwell times and calcium mobilization. Eur. J. Immunol. 2008, 38:40-47.
42. Schreiber H.A., Hulseberg P.D., Lee J., Prechl J., Barta P., Szlavik N., Harding J.S., Fabry Z., Sandor M. Dendritic cells in chronic mycobacterial granulomas restrict local anti-bacterial Tcell response in a murine model. PLoS ONE 2010, 5:e11453.
43. Segel L.A., Bar-Or R.L. On the role of feedback in promoting conflicting goals of the adaptive immune system. J.Immunol. 1999, 163:1342-1349.
44. Stoll S., Delon J., Brotz T.M., Germain R.N. Dynamic imaging of Tcell-dendritic cell interactions in lymph nodes. Science 2002, 296:1873-1876.
45. + Tcells in immunity to viruses. Nat. Rev. Immunol. 2012, 12:136-148.
46. Utzny C., Coombs D., Müller S., Valitutti S. Analysis of peptide/MHC-induced TCR downregulation: deciphering the triggering kinetics. Cell Biochem. Biophys. 2006, 46:101-111.
47. Valitutti S., Coombs D., Dupré L. The space and time frames of Tcell activation at the immunological synapse. FEBS Lett. 2010, 584:4851-4857.
48. Vintersten K., Monetti C., Gertsenstein M., Zhang P., Laszlo L., Biechele S., Nagy A. Mouse in red: red fluorescent protein expression in mouse ES cells, embryos, and adult animals. Genesis 2004, 40:241-246.
49. Waite J.C., Leiner I., Lauer P., Rae C.S., Barbet G., Zheng H., Portnoy D.A., Pamer E.G., Dustin M.L. Dynamic imaging of the effector immune response to listeria infection invivo. PLoS Pathog. 2011, 7:e1001326.
50. Wilson E.H., Harris T.H., Mrass P., John B., Tait E.D., Wu G.F., Pepper M., Wherry E.J., Dzierzinski F., Roos D., et al. Behavior of parasite-specific effector CD8+ Tcells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 2009, 30:300-311.
51. Wolf A.J., Desvignes L., Linas B., Banaiee N., Tamura T., Takatsu K., Ernst J.D. Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs. J.Exp. Med. 2008, 205:105-115.
52. Yokosuka T., Takamatsu M., Kobayashi-Imanishi W., Hashimoto-Tane A., Azuma M., Saito T. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit Tcell receptor signaling by recruiting phosphatase SHP2. J.Exp. Med. 2012, 209:1201-1217.
53. *). Annu. Rev. Immunol. 2010, 28:445-489.
54. Zinselmeyer B.H., Heydari S., Sacristán C., Nayak D., Cammer M., Herz J., Cheng X., Davis S.J., Dustin M.L., McGavern D.B. PD-1 promotes immune exhaustion by inducing antiviral Tcell motility paralysis. J.Exp. Med. 2013, 210:757-774.