Dissecting T Cell Contraction In Vivo Using a Genetically Encoded Reporter of Apoptosis

Cell Reports

Volumn 2, Issue 5, 2012, Pages 1438-1447

  Garrod, Kym R ^a,b   Moreau, Hélène D ^a,b,c   Garcia, Zacarias ^a,b   Lemaître, Fabrice ^a,b   Bouvier, Isabelle ^a,d   Albert, Matthew L ^a,d   Bousso, Philippe ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3;

ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; CELL DEATH; CELL MOTILITY; CELLULAR IMMUNITY; EFFECTOR CELL; ENZYME ACTIVITY; GENETIC CODE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; MEMORY; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; APOPTOSIS; CASPASE 3; CD8-POSITIVE T-LYMPHOCYTES; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENES, REPORTER; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 84870474671     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.10.015     Document Type: Article

References (47)

1. Alam A., Cohen L.Y., Aouad S., Sékaly R.P. Early activation of caspases during T lymphocyte stimulation results in selective substrate cleavage in nonapoptotic cells. J. Exp. Med. 1999, 190:1879-1890.
2. Badovinac V.P., Harty J.T. CD8(+) T-cell homeostasis after infection: setting the 'curve'. Microbes Infect. 2002, 4:441-447.
3. Badovinac V.P., Harty J.T. Programming, demarcating, and manipulating CD8+ T-cell memory. Immunol. Rev. 2006, 211:67-80.
4. Badovinac V.P., Tvinnereim A.R., Harty J.T. Regulation of antigen-specific CD8+ T cell homeostasis by perforin and interferon-gamma. Science 2000, 290:1354-1358.
5. Badovinac V.P., Porter B.B., Harty J.T. Programmed contraction of CD8(+) T cells after infection. Nat. Immunol. 2002, 3:619-626.
6. Badovinac V.P., Porter B.B., Harty J.T. CD8+ T cell contraction is controlled by early inflammation. Nat. Immunol. 2004, 5:809-817.
7. Bahl K., Hüebner A., Davis R.J., Welsh R.M. Analysis of apoptosis of memory T cells and dendritic cells during the early stages of viral infection or exposure to toll-like receptor agonists. J. Virol. 2010, 84:4866-4877.
8. Bevan M.J., Fink P.J. The CD8 response on autopilot. Nat. Immunol. 2001, 2:381-382.
9. Blair D.A., Turner D.L., Bose T.O., Pham Q.M., Bouchard K.R., Williams K.J., McAleer J.P., Cauley L.S., Vella A.T., Lefrançois L. Duration of antigen availability influences the expansion and memory differentiation of T cells. J. Immunol. 2011, 187:2310-2321.
10. Breart B., Lemaître F., Celli S., Bousso P. Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J. Clin. Invest. 2008, 118:1390-1397.
11. D'Cruz L.M., Rubinstein M.P., Goldrath A.W. Surviving the crash: transitioning from effector to memory CD8+ T cell. Semin. Immunol. 2009, 21:92-98.
12. Dahl A.M., Klein C., Andres P.G., London C.A., Lodge M.P., Mulligan R.C., Abbas A.K. Expression of bcl-X(L) restores cell survival, but not proliferation off effector differentiation, in CD28-deficient T lymphocytes. J. Exp. Med. 2000, 191:2031-2038.
13. Elmore S. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 2007, 35:495-516.
14. Harbertson J., Biederman E., Bennett K.E., Kondrack R.M., Bradley L.M. Withdrawal of stimulation may initiate the transition of effector to memory CD4 cells. J. Immunol. 2002, 168:1095-1102.
15. Harty J.T., Badovinac V.P. Shaping and reshaping CD8+ T-cell memory. Nat. Rev. Immunol. 2008, 8:107-119.
16. Hovav A.H., Panas M.W., Rahman S., Sircar P., Gillard G., Cayabyab M.J., Letvin N.L. Duration of antigen expression in vivo following DNA immunization modifies the magnitude, contraction, and secondary responses of CD8+ T lymphocytes. J. Immunol. 2007, 179:6725-6733.
17. Huang L., Soldevila G., Leeker M., Flavell R., Crispe I.N. The liver eliminates T cells undergoing antigen-triggered apoptosis in vivo. Immunity 1994, 1:741-749.
18. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., Gapin L., Kaech S.M. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007, 27:281-295.
19. Jusforgues-Saklani H., Uhl M., Blachère N., Lemaître F., Lantz O., Bousso P., Braun D., Moon J.J., Albert M.L. Antigen persistence is required for dendritic cell licensing and CD8+ T cell cross-priming. J. Immunol. 2008, 181:3067-3076.
20. Kaech S.M., Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells. Nat. Immunol. 2001, 2:415-422.
21. Kaech S.M., Wherry E.J., Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2002, 2:251-262.
22. Krammer P.H., Arnold R., Lavrik I.N. Life and death in peripheral T cells. Nat. Rev. Immunol. 2007, 7:532-542.
23. Malherbe L., Hausl C., Teyton L., McHeyzer-Williams M.G. Clonal selection of helper T cells is determined by an affinity threshold with no further skewing of TCR binding properties. Immunity 2004, 21:669-679.
24. Marrack P., Kappler J. Control of T cell viability. Annu. Rev. Immunol. 2004, 22:765-787.
25. Marrack P., Scott-Browne J., MacLeod M.K. Terminating the immune response. Immunol. Rev. 2010, 236:5-10.
26. McComb S., Mulligan R., Sad S. Caspase-3 is transiently activated without cell death during early antigen driven expansion of CD8(+) T cells in vivo. PLoS ONE 2010, 5:e15328.
27. McKinstry K.K., Golech S., Lee W.H., Huston G., Weng N.P., Swain S.L. Rapid default transition of CD4 T cell effectors to functional memory cells. J. Exp. Med. 2007, 204:2199-2211.
28. McKinstry K.K., Strutt T.M., Swain S.L. Regulation of CD4+ T-cell contraction during pathogen challenge. Immunol. Rev. 2010, 236:110-124.
29. Mercado R., Vijh S., Allen S.E., Kerksiek K., Pilip I.M., Pamer E.G. Early programming of T cell populations responding to bacterial infection. J. Immunol. 2000, 165:6833-6839.
30. Moreau H.D., Lemaître F., Terriac E., Azar G.A., Piel M., Lennon-Dumenil A.M., Bousso P. Dynamic in situ cytometry uncovers T cell receptor signaling during immunological synapses and kinapses in vivo. Immunity 2012, 37:351-363.
31. Murakami K., Liadis N., Sarmiento J., Elford A.R., Woo M., Nguyen L.T., Mak T.W., Ohashi P.S. Caspase 3 is not essential for the induction of anergy or multiple pathways of CD8+ T-cell death. Eur. J. Immunol. 2010, 40:3372-3377.
32. Nussbaum A.K., Whitton J.L. The contraction phase of virus-specific CD8+ T cells is unaffected by a pan-caspase inhibitor. J. Immunol. 2004, 173:6611-6618.
33. Pear W.S., Miller J.P., Xu L., Pui J.C., Soffer B., Quackenbush R.C., Pendergast A.M., Bronson R., Aster J.C., Scott M.L., Baltimore D. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 1998, 92:3780-3792.
34. Prlic M., Hernandez-Hoyos G., Bevan M.J. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J. Exp. Med. 2006, 203:2135-2143.
35. Puga I., Rao A., Macian F. Targeted cleavage of signaling proteins by caspase 3 inhibits T cell receptor signaling in anergic T cells. Immunity 2008, 29:193-204.
36. Rubinstein M.P., Lind N.A., Purton J.F., Filippou P., Best J.A., McGhee P.A., Surh C.D., Goldrath A.W. IL-7 and IL-15 differentially regulate CD8+ T-cell subsets during contraction of the immune response. Blood 2008, 112:3704-3712.
37. Sallusto F., Lanzavecchia A., Araki K., Ahmed R. From vaccines to memory and back. Immunity 2010, 33:451-463.
38. Sanjabi S., Mosaheb M.M., Flavell R.A. Opposing effects of TGF-beta and IL-15 cytokines control the number of short-lived effector CD8+ T cells. Immunity 2009, 31:131-144.
39. Schluns K.S., Lefrançois L. Cytokine control of memory T-cell development and survival. Nat. Rev. Immunol. 2003, 3:269-279.
40. Sprent J., Tough D.F. T cell death and memory. Science 2001, 293:245-248.
41. Surh C.D., Sprent J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 1994, 372:100-103.
42. Tyas L., Brophy V.A., Pope A., Rivett A.J., Tavaré J.M. Rapid caspase-3 activation during apoptosis revealed using fluorescence-resonance energy transfer. EMBO Rep. 2000, 1:266-270.
43. van Stipdonk M.J., Lemmens E.E., Schoenberger S.P. Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol. 2001, 2:423-429.
44. Wang X.Z., Stepp S.E., Brehm M.A., Chen H.D., Selin L.K., Welsh R.M. Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 2003, 18:631-642.
45. Wensveen F.M., van Gisbergen K.P., Derks I.A., Gerlach C., Schumacher T.N., van Lier R.A., Eldering E. Apoptosis threshold set by Noxa and Mcl-1 after T cell activation regulates competitive selection of high-affinity clones. Immunity 2010, 32:754-765.
46. Williams M.A., Bevan M.J. Effector and memory CTL differentiation. Annu. Rev. Immunol. 2007, 25:171-192.
47. Zehn D., Lee S.Y., Bevan M.J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 2009, 458:211-214.