The Transcription Factor NFAT Exhibits Signal Memory during Serial T Cell Interactions with Antigen-Presenting Cells

Immunity

Volumn 38, Issue 2, 2013, Pages 237-249

  Marangoni, Francesco ^a,b   Murooka, Thomas T ^a,b   Manzo, Teresa ^a,c   Kim, Edward Y ^a,b   Carrizosa, Esteban ^a,b   Elpek, Natalie M ^a   Mempel, Thorsten R ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; TRANSCRIPTION FACTOR NFAT;

ANTIGEN PRESENTING CELL; ARTICLE; CELL INTERACTION; CELL NUCLEUS; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; MULTIPHOTON MICROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; ANTIGEN-PRESENTING CELLS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MOVEMENT; CELL NUCLEUS; CYTOSOL; EARLY GROWTH RESPONSE PROTEIN 2; GENE EXPRESSION REGULATION; HUMANS; IMMUNE TOLERANCE; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LYMPH NODES; MICE; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; NFATC TRANSCRIPTION FACTORS; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR CELLS, CULTURED;

EID: 84874273811     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.09.012     Document Type: Article

References (50)

1. Aramburu J., Yaffe M.B., López-Rodríguez C., Cantley L.C., Hogan P.G., Rao A. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science 1999, 285:2129-2133.
2. 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.
3. Boissonnas A., Fetler L., Zeelenberg I.S., Hugues S., Amigorena S. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 2007, 204:345-356.
4. Bromley S.K., Peterson D.A., Gunn M.D., Dustin M.L. Cutting edge: hierarchy of chemokine receptor and TCR signals regulating T cell migration and proliferation. J. Immunol. 2000, 165:15-19.
5. Celli S., Garcia Z., Bousso P. CD4 T cells integrate signals delivered during successive DC encounters in vivo. J. Exp. Med. 2005, 202:1271-1278.
6. Chen L., Ashe S., Brady W.A., Hellström I., Hellström K.E., Ledbetter J.A., McGowan P., Linsley P.S. Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4. Cell 1992, 71:1093-1102.
7. Clark C.E., Hasan M., Bousso P. A role for the immediate early gene product c-fos in imprinting T cells with short-term memory for signal summation. PLoS ONE 2011, 6:e18916.
8. Collins S., Lutz M.A., Zarek P.E., Anders R.A., Kersh G.J., Powell J.D. Opposing regulation of T cell function by Egr-1/NAB2 and Egr-2/Egr-3. Eur. J. Immunol. 2008, 38:528-536.
9. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
10. Das J., Ho M., Zikherman J., Govern C., Yang M., Weiss A., Chakraborty A.K., Roose J.P. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 2009, 136:337-351.
11. Dolmetsch R.E., Lewis R.S., Goodnow C.C., Healy J.I. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 1997, 386:855-858.
12. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., Roche P.C., Lu J., Zhu G., Tamada K., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 2002, 8:793-800.
13. Dustin M.L., Bromley S.K., Kan Z., Peterson D.A., Unanue E.R. Antigen receptor engagement delivers a stop signal to migrating T lymphocytes. Proc. Natl. Acad. Sci. USA 1997, 94:3909-3913.
14. Faroudi M., Zaru R., Paulet P., Müller S., Valitutti S. Cutting edge: T lymphocyte activation by repeated immunological synapse formation and intermittent signaling. J. Immunol. 2003, 171:1128-1132.
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 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 2009, 10:1185-1192.
16. Frey A.B., Monu N. Signaling defects in anti-tumor T cells. Immunol. Rev. 2008, 222:192-205.
17. Fukumura D., Xavier R., Sugiura T., Chen Y., Park E.C., Lu N., Selig M., Nielsen G., Taksir T., Jain R.K., Seed B. Tumor induction of VEGF promoter activity in stromal cells. Cell 1998, 94:715-725.
18. Germain R.N., Bajénoff M., Castellino F., Chieppa M., Egen J.G., Huang A.Y., Ishii M., Koo L.Y., Qi H. Making friends in out-of-the-way places: how cells of the immune system get together and how they conduct their business as revealed by intravital imaging. Immunol. Rev. 2008, 221:163-181.
19. Gunzer M., Weishaupt C., Hillmer A., Basoglu Y., Friedl P., Dittmar K.E., Kolanus W., Varga G., Grabbe S. A spectrum of biophysical interaction modes between T cells and different antigen-presenting cells during priming in 3-D collagen and in vivo. Blood 2004, 104:2801-2809.
20. Henrickson S.E., Mempel T.R., Mazo I.B., Liu B., Artyomov M.N., Zheng H., Peixoto A., Flynn M.P., Senman B., Junt T., 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.
21. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003, 17:2205-2232.
22. Kiani A., Rao A., Aramburu J. Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity 2000, 12:359-372.
23. Klein L., Khazaie K., von Boehmer H. In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc. Natl. Acad. Sci. USA 2003, 100:8886-8891.
24. Kupfer A., Mosmann T.R., Kupfer H. Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. USA 1991, 88:775-779.
25. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 2005, 5:472-484.
26. Macián F., López-Rodríguez C., Rao A. Partners in transcription: NFAT and AP-1. Oncogene 2001, 20:2476-2489.
27. 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.
28. Mempel T.R., Pittet M.J., Khazaie K., Weninger W., Weissleder R., von Boehmer H., von Andrian U.H. Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 2006, 25:129-141.
29. Miller M.J., Safrina O., Parker I., Cahalan M.D. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 2004, 200:847-856.
30. Mrass P., Takano H., Ng L.G., Daxini S., Lasaro M.O., Iparraguirre A., Cavanagh L.L., von Andrian U.H., Ertl H.C., Haydon P.G., Weninger W. Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J. Exp. Med. 2006, 203:2749-2761.
31. Müller M.R., Rao A. NFAT, immunity and cancer: a transcription factor comes of age. Nat. Rev. Immunol. 2010, 10:645-656.
32. Negulescu P.A., Krasieva T.B., Khan A., Kerschbaum H.H., Cahalan M.D. Polarity of T cell shape, motility, and sensitivity to antigen. Immunity 1996, 4:421-430.
33. Nishikawa H., Sakaguchi S. Regulatory T cells in tumor immunity. Int. J. Cancer 2010, 127:759-767.
34. Okada T., Miller M.J., Parker I., Krummel M.F., Neighbors M., Hartley S.B., O'Garra A., Cahalan M.D., Cyster J.G. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 2005, 3:e150.
35. Pittet M.J., Mempel T.R. Regulation of T-cell migration and effector functions: insights from in vivo imaging studies. Immunol. Rev. 2008, 221:107-129.
36. Podtschaske M., Benary U., Zwinger S., Höfer T., Radbruch A., Baumgrass R. Digital NFATc2 activation per cell transforms graded T cell receptor activation into an all-or-none IL-2 expression. PLoS ONE 2007, 2:e935.
37. Pulecio J., Petrovic J., Prete F., Chiaruttini G., Lennon-Dumenil A.M., Desdouets C., Gasman S., Burrone O.R., Benvenuti F. Cdc42-mediated MTOC polarization in dendritic cells controls targeted delivery of cytokines at the immune synapse. J. Exp. Med. 2010, 207:2719-2732.
38. Qureshi O.S., Zheng Y., Nakamura K., Attridge K., Manzotti C., Schmidt E.M., Baker J., Jeffery L.E., Kaur S., Briggs Z., et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011, 332:600-603.
39. Revy P., Sospedra M., Barbour B., Trautmann A. Functional antigen-independent synapses formed between T cells and dendritic cells. Nat. Immunol. 2001, 2:925-931.
40. Scholer A., Hugues S., Boissonnas A., Fetler L., Amigorena S. Intercellular adhesion molecule-1-dependent stable interactions between T cells and dendritic cells determine CD8+ T cell memory. Immunity 2008, 28:258-270.
41. Skokos D., Shakhar G., Varma R., Waite J.C., Cameron T.O., Lindquist R.L., Schwickert T., Nussenzweig M.C., Dustin M.L. Peptide-MHC potency governs dynamic interactions between T cells and dendritic cells in lymph nodes. Nat. Immunol. 2007, 8:835-844.
42. Slifka M.K., Rodriguez F., Whitton J.L. Rapid on/off cycling of cytokine production by virus-specific CD8+ T cells. Nature 1999, 401:76-79.
43. Soto-Nieves N., Puga I., Abe B.T., Bandyopadhyay S., Baine I., Rao A., Macian F. Transcriptional complexes formed by NFAT dimers regulate the induction of T cell tolerance. J. Exp. Med. 2009, 206:867-876.
44. Spiotto M.T., Yu P., Rowley D.A., Nishimura M.I., Meredith S.C., Gajewski T.F., Fu Y.X., Schreiber H. Increasing tumor antigen expression overcomes " ignorance" to solid tumors via crosspresentation by bone marrow-derived stromal cells. Immunity 2002, 17:737-747.
45. Srinivasan M., Frauwirth K.A. Reciprocal NFAT1 and NFAT2 nuclear localization in CD8+ anergic T cells is regulated by suboptimal calcium signaling. J. Immunol. 2007, 179:3734-3741.
46. Stinchcombe J.C., Bossi G., Booth S., Griffiths G.M. The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 2001, 15:751-761.
47. Tadokoro C.E., Shakhar G., Shen S., Ding Y., Lino A.C., Maraver A., Lafaille J.J., Dustin M.L. Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 2006, 203:505-511.
48. Tang Q., Adams J.Y., Tooley A.J., Bi M., Fife B.T., Serra P., Santamaria P., Locksley R.M., Krummel M.F., Bluestone J.A. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 2006, 7:83-92.
49. Tomida T., Hirose K., Takizawa A., Shibasaki F., Iino M. NFAT functions as a working memory of Ca2+ signals in decoding Ca2+ oscillation. EMBO J. 2003, 22:3825-3832.
50. Wei S.H., Safrina O., Yu Y., Garrod K.R., Cahalan M.D., Parker I. Ca2+ signals in CD4+ T cells during early contacts with antigen-bearing dendritic cells in lymph node. J. Immunol. 2007, 179:1586-1594.