The Transcription Factor NFAT Promotes Exhaustion of Activated CD8+ T Cells

Immunity

Volumn 42, Issue 2, 2015, Pages 265-278

  Martinez, Gustavo J ^a,d   Pereira, Renata M ^a   Äijö, Tarmo ^a,b   Kim, Edward Y ^c   Marangoni, Francesco ^c   Pipkin, Matthew E ^a,d   Togher, Susan ^a   Heissmeyer, Vigo ^e,f   Zhang, YiChen ^g   Crotty, Shane ^a   Lamperti, Edward D ^h   Ansel, K Mark ⁱ   Mempel, Thorsten R ^c   Lähdesmäki, Harri ^b   Hogan, Patrick G ^a   Rao, Anjana ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b AALTO UNIVERSITY   (Finland)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f UNIVERSITY OF MUNICH   (Germany)

^g ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

^h BOSTON CHILDREN S HOSPITAL   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT1; UNCLASSIFIED DRUG; LYMPHOCYTE ANTIGEN RECEPTOR; NFATC2 PROTEIN, MOUSE; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIUM COLONY; CD8+ T LYMPHOCYTE; CLONAL ANERGY; CONTROLLED STUDY; GENE EXPRESSION; LISTERIOSIS; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SECONDARY IMMUNE RESPONSE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE EXHAUSTION; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; NEOPLASM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CLONAL ANERGY; GENE EXPRESSION REGULATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; NEOPLASMS; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT PROTEINS; TRANSCRIPTION FACTOR AP-1;

EID: 84923026945     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.01.006     Document Type: Article

References (49)

1. Agnellini P., Wolint P., Rehr M., Cahenzli J., Karrer U., Oxenius A. Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8+ Tcell functions during chronic viral infection. Proc. Natl. Acad. Sci. USA 2007, 104:4565-4570.
2. Anderson A.C., Lord G.M., Dardalhon V., Lee D.H., Sabatos-Peyton C.A., Glimcher L.H., Kuchroo V.K. T-bet, a Th1 transcription factor regulates the expression of Tim-3. Eur. J. Immunol. 2010, 40:859-866.
3. Bandukwala H.S., Wu Y., Feuerer M., Chen Y., Barboza B., Ghosh S., Stroud J.C., Benoist C., Mathis D., Rao A., Chen L. Structure of a domain-swapped FOXP3 dimer on DNA and its function in regulatory Tcells. Immunity 2011, 34:479-491.
4. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., Ahmed R. Restoring function in exhausted CD8 Tcells during chronic viral infection. Nature 2006, 439:682-687.
5. Bauer C.A., Kim E.Y., Marangoni F., Carrizosa E., Claudio N.M., Mempel T.R. Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction. J.Clin. Invest. 2014, 124:2425-2440.
6. Blackburn S.D., Shin H., Haining W.N., Zou T., Workman C.J., Polley A., Betts M.R., Freeman G.J., Vignali D.A., Wherry E.J. Coregulation of CD8+ Tcell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 2009, 10:29-37.
7. Chen L., Glover J.N., Hogan P.G., Rao A., Harrison S.C. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature 1998, 392:42-48.
8. Chuvpilo S., Jankevics E., Tyrsin D., Akimzhanov A., Moroz D., Jha M.K., Schulze-Luehrmann J., Santner-Nanan B., Feoktistova E., König T., et al. Autoregulation of NFATc1/A expression facilitates effector Tcells to escape from rapid apoptosis. Immunity 2002, 16:881-895.
9. Crabtree G.R., Olson E.N. NFAT signaling: choreographing the social lives of cells. Cell 2002, 109:S67-S79.
10. Doering T.A., Crawford A., Angelosanto J.M., Paley M.A., Ziegler C.G., Wherry E.J. Network analysis reveals centrally connected genes and pathways involved in CD8+ Tcell exhaustion versus memory. Immunity 2012, 37:1130-1144.
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. 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.
13. Fathman C.G., Lineberry N.B. Molecular mechanisms of CD4+ T-cell anergy. Nat. Rev. Immunol. 2007, 7:599-609.
14. Fehr T., Lucas C.L., Kurtz J., Onoe T., Zhao G., Hogan T., Vallot C., Rao A., Sykes M. A CD8 Tcell-intrinsic role for the calcineurin-NFAT pathway for tolerance induction invivo. Blood 2010, 115:1280-1287.
15. Giffin M.J., Stroud J.C., Bates D.L., von Koenig K.D., Hardin J., Chen L. Structure of NFAT1 bound as a dimer to the HIV-1 LTR kappa B element. Nat. Struct. Biol. 2003, 10:800-806.
16. Heissmeyer V., Macián F., Im S.H., Varma R., Feske S., Venuprasad K., Gu H., Liu Y.C., Dustin M.L., Rao A. Calcineurin imposes Tcell unresponsiveness through targeted proteolysis of signaling proteins. Nat. Immunol. 2004, 5:255-265.
17. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003, 17:2205-2232.
18. Jain J., Valge-Archer V.E., Rao A. Analysis of the AP-1 sites in the IL-2 promoter. J.Immunol. 1992, 148:1240-1250.
19. Jain J., McCaffrey P.G., Miner Z., Kerppola T.K., Lambert J.N., Verdine G.L., Curran T., Rao A. The T-cell transcription factor NFATp isa substrate for calcineurin and interacts with Fos and Jun. Nature 1993, 365:352-355.
20. Jain J., Burgeon E., Badalian T.M., Hogan P.G., Rao A. A similar DNA-binding motif in NFAT family proteins and the Rel homology region. J.Biol. Chem. 1995, 270:4138-4145.
21. Jin H.T., Anderson A.C., Tan W.G., West E.E., Ha S.J., Araki K., Freeman G.J., Kuchroo V.K., Ahmed R. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. USA 2010, 107:14733-14738.
22. Joshi R.P., Koretzky G.A. Diacylglycerol kinases: regulated controllers of Tcell activation, function, and development. Int. J. Mol. Sci. 2013, 14:6649-6673.
23. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 Tcells that give rise to long-lived memory cells. Nat. Immunol. 2003, 4:1191-1198.
24. Langmead B., Trapnell C., Pop M., Salzberg S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009, 10:R25.
25. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 2005, 5:472-484.
26. Macián F., García-Rodríguez C., Rao A. Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J. 2000, 19:4783-4795.
27. Macián F., García-Cózar F., Im S.H., Horton H.F., Byrne M.C., Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002, 109:719-731.
28. Marangoni F., Murooka T.T., Manzo T., Kim E.Y., Carrizosa E., Elpek N.M., Mempel T.R. The transcription factor NFAT exhibits signal memory during serial Tcell interactions with antigen-presenting cells. Immunity 2013, 38:237-249.
29. Mathieu M., Cotta-Grand N., Daudelin J.F., Thébault P., Labrecque N. Notch signaling regulates PD-1 expression during CD8(+) T-cell activation. Immunol. Cell Biol. 2013, 91:82-88.
30. Mueller D.L. Mechanisms maintaining peripheral tolerance. Nat. Immunol. 2010, 11:21-27.
31. Nurieva R.I., Liu X., Dong C. Molecular mechanisms of T-cell tolerance. Immunol. Rev. 2011, 241:133-144.
32. Oestreich K.J., Yoon H., Ahmed R., Boss J.M. NFATc1 regulates PD-1 expression upon Tcell activation. J.Immunol. 2008, 181:4832-4839.
33. Oh-Hora M., Yamashita M., Hogan P.G., Sharma S., Lamperti E., Chung W., Prakriya M., Feske S., Rao A. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in Tcell activation and tolerance. Nat. Immunol. 2008, 9:432-443.
34. Okamura H., Aramburu J., García-Rodríguez C., Viola J.P., Raghavan A., Tahiliani M., Zhang X., Qin J., Hogan P.G., Rao A. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol. Cell 2000, 6:539-550.
35. Okamura T., Fujio K., Shibuya M., Sumitomo S., Shoda H., Sakaguchi S., Yamamoto K. CD4+CD25-LAG3+ regulatory Tcells controlled by the transcription factor Egr-2. Proc. Natl. Acad. Sci. USA 2009, 106:13974-13979.
36. Pipkin M.E., Sacks J.A., Cruz-Guilloty F., Lichtenheld M.G., Bevan M.J., Rao A. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic Tcells. Immunity 2010, 32:79-90.
37. Rao A., Luo C., Hogan P.G. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 1997, 15:707-747.
38. Sakuishi K., Apetoh L., Sullivan J.M., Blazar B.R., Kuchroo V.K., Anderson A.C. Targeting Tim-3 and PD-1 pathways to reverse Tcell exhaustion and restore anti-tumor immunity. J.Exp. Med. 2010, 207:2187-2194.
39. Schietinger A., Greenberg P.D. Tolerance and exhaustion: defining mechanisms of Tcell dysfunction. Trends Immunol. 2014, 35:51-60.
40. 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 Tcell tolerance. J.Exp. Med. 2009, 206:867-876.
41. Srinivasan M., Frauwirth K.A. Reciprocal NFAT1 and NFAT2 nuclear localization in CD8+ anergic Tcells is regulated by suboptimal calcium signaling. J.Immunol. 2007, 179:3734-3741.
42. Stroud J.C., Lopez-Rodriguez C., Rao A., Chen L. Structure of a TonEBP-DNA complex reveals DNA encircled by a transcription factor. Nat. Struct. Biol. 2002, 9:90-94.
43. Terawaki S., Chikuma S., Shibayama S., Hayashi T., Yoshida T., Okazaki T., Honjo T. IFN-α directly promotes programmed cell death-1transcription and limits the duration of Tcell-mediated immunity. J.Immunol. 2011, 186:2772-2779.
44. Trapnell C., Pachter L., Salzberg S.L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
45. Wherry E.J. T cell exhaustion. Nat. Immunol. 2011, 12:492-499.
46. Wherry E.J., Ha S.J., Kaech S.M., Haining W.N., Sarkar S., Kalia V., Subramaniam S., Blattman J.N., Barber D.L., Ahmed R. Molecular signature of CD8+ Tcell exhaustion during chronic viral infection. Immunity 2007, 27:670-684.
47. Wu Y., Borde M., Heissmeyer V., Feuerer M., Lapan A.D., Stroud J.C., Bates D.L., Guo L., Han A., Ziegler S.F., et al. FOXP3 controls regulatory Tcell function through cooperation with NFAT. Cell 2006, 126:375-387.
48. Xanthoudakis S., Viola J.P., Shaw K.T., Luo C., Wallace J.D., Bozza P.T., Luk D.C., Curran T., Rao A. An enhanced immune response in mice lacking the transcription factor NFAT1. Science 1996, 272:892-895.
49. Yoon S.J., Lee M.J., Shin D.C., Kim J.S., Chwae Y.J., Kwon M.H., Kim K., Park S. Activation of mitogen activated protein kinase-Erk kinase (MEK) increases Tcell immunoglobulin mucin domain-3 (TIM-3) transcription in human T lymphocytes and a human mast cell line. Mol. Immunol. 2011, 48:1778-1783.