Gene Deregulation and Chronic Activation in Natural Killer Cells Deficient in the Transcription Factor ETS1

Immunity

Volumn 36, Issue 6, 2012, Pages 921-932

  Ramirez, Kevin ^a   Chandler, Katherine J ^b   Spaulding, Christina ^a   Zandi, Sasan ^c   Sigvardsson, Mikael ^c   Graves, Barbara J ^b   Kee, Barbara L ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBITOR OF DIFFERENTIATION 2; LY49D PROTEIN; LY49H PROTEIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS1; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; GENE EXPRESSION; GENETIC ASSOCIATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE EXPRESSION REGULATION; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INTERLEUKIN-15; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; PROTO-ONCOGENE PROTEIN C-ETS-1; RADIATION CHIMERA; RECEPTORS, NATURAL KILLER CELL; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84862985534     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.04.006     Document Type: Article

References (58)

1. Aliahmad P., de la Torre B., Kaye J. Shared dependence on the DNA-binding factor TOX for the development of lymphoid tissue-inducer cell and NK cell lineages. Nat. Immunol. 2010, 11:945-952.
2. Bailey T.L., Boden M., Buske F.A., Frith M., Grant C.E., Clementi L., Ren J., Li W.W., Noble W.S. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009, 37(Web Server issue):W202-W208.
3. Barao I., Alvarez M., Ames E., Orr M.T., Stefanski H.E., Blazar B.R., Lanier L.L., Anderson S.K., Redelman D., Murphy W.J. Mouse Ly49G2+ NK cells dominate early responses during both immune reconstitution and activation independently of MHC. Blood 2011, 117:7032-7041.
4. Barton K., Muthusamy N., Fischer C., Ting C.N., Walunas T.L., Lanier L.L., Leiden J.M. The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 1998, 9:555-563.
5. Boos M.D., Yokota Y., Eberl G., Kee B.L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 2007, 204:1119-1130.
6. Caraux A., Lu Q., Fernandez N., Riou S., Di Santo J.P., Raulet D.H., Lemke G., Roth C. Natural killer cell differentiation driven by Tyro3 receptor tyrosine kinases. Nat. Immunol. 2006, 7:747-754.
7. Carotta S., Pang S.H., Nutt S.L., Belz G.T. Identification of the earliest NK-cell precursor in the mouse BM. Blood 2011, 117:5449-5452.
8. Chiossone L., Chaix J., Fuseri N., Roth C., Vivier E., Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009, 113:5488-5496.
9. Clements J.L., John S.A., Garrett-Sinha L.A. Impaired generation of CD8+ thymocytes in Ets-1-deficient mice. J. Immunol. 2006, 177:905-912.
10. Cowley D.O., Graves B.J. Phosphorylation represses Ets-1 DNA binding by reinforcing autoinhibition. Genes Dev. 2000, 14:366-376.
11. Dias S., Månsson R., Gurbuxani S., Sigvardsson M., Kee B.L. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008, 29:217-227.
12. Elpek K.G., Rubinstein M.P., Bellemare-Pelletier A., Goldrath A.W., Turley S.J. Mature natural killer cells with phenotypic and functional alterations accumulate upon sustained stimulation with IL-15/IL-15Ralpha complexes. Proc. Natl. Acad. Sci. USA 2010, 107:21647-21652.
13. Eyquem S., Chemin K., Fasseu M., Bories J.C. The Ets-1 transcription factor is required for complete pre-T cell receptor function and allelic exclusion at the T cell receptor beta locus. Proc. Natl. Acad. Sci. USA 2004, 101:15712-15717.
14. Eyquem S., Chemin K., Fasseu M., Chopin M., Sigaux F., Cumano A., Bories J.C. The development of early and mature B cells is impaired in mice deficient for the Ets-1 transcription factor. Eur. J. Immunol. 2004, 34:3187-3196.
15. Fathman J.W., Bhattacharya D., Inlay M.A., Seita J., Karsunky H., Weissman I.L. Identification of the earliest natural killer cell-committed progenitor in murine bone marrow. Blood 2011, 118:5439-5447.
16. Fehniger T.A., Suzuki K., Ponnappan A., VanDeusen J.B., Cooper M.A., Florea S.M., Freud A.G., Robinson M.L., Durbin J., Caligiuri M.A. Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8+ T cells. J. Exp. Med. 2001, 193:219-231.
17. Fitzsimmons D., Lukin K., Lutz R., Garvie C.W., Wolberger C., Hagman J. Highly cooperative recruitment of Ets-1 and release of autoinhibition by Pax5. J. Mol. Biol. 2009, 392:452-464.
18. Fraser K.P., Gays F., Robinson J.H., van Beneden K., Leclercq G., Vance R.E., Raulet D.H., Brooks C.G. NK cells developing in vitro from fetal mouse progenitors express at least one member of the Ly49 family that is acquired in a time-dependent and stochastic manner independently of CD94 and NKG2. Eur. J. Immunol. 2002, 32:868-878.
19. Gascoyne D.M., Long E., Veiga-Fernandes H., de Boer J., Williams O., Seddon B., Coles M., Kioussis D., Brady H.J. The basic leucine zipper transcription factor E4BP4 is essential for natural killer cell development. Nat. Immunol. 2009, 10:1118-1124.
20. Gaston K., Fried M. CpG methylation has differential effects on the binding of YY1 and ETS proteins to the bi-directional promoter of the Surf-1 and Surf-2 genes. Nucleic Acids Res. 1995, 23:901-909.
21. Gordon S.M., Chaix J., Rupp L.J., Wu J., Madera S., Sun J.C., Lindsten T., Reiner S.L. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 2012, 36:55-67.
22. Grenningloh R., Kang B.Y., Ho I.C. Ets-1, a functional cofactor of T-bet, is essential for Th1 inflammatory responses. J. Exp. Med. 2005, 201:615-626.
23. Grenningloh R., Tai T.S., Frahm N., Hongo T.C., Chicoine A.T., Brander C., Kaufmann D.E., Ho I.C. Ets-1 maintains IL-7 receptor expression in peripheral T cells. J. Immunol. 2011, 186:969-976.
24. Held W., Kunz B., Lowin-Kropf B., van de Wetering M., Clevers H. Clonal acquisition of the Ly49A NK cell receptor is dependent on the trans-acting factor TCF-1. Immunity 1999, 11:433-442.
25. Higuchi T., Bartel F.O., Masuya M., Deguchi T., Henderson K.W., Li R., Muise-Helmericks R.C., Kern M.J., Watson D.K., Spyropoulos D.D. Thymomegaly, microsplenia, and defective homeostatic proliferation of peripheral lymphocytes in p51-Ets1 isoform-specific null mice. Mol. Cell. Biol. 2007, 27:3353-3366.
26. Hollenhorst P.C., Shah A.A., Hopkins C., Graves B.J. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 2007, 21:1882-1894.
27. Hollenhorst P.C., Chandler K.J., Poulsen R.L., Johnson W.E., Speck N.A., Graves B.J. DNA specificity determinants associate with distinct transcription factor functions. PLoS Genet. 2009, 5:e1000778.
28. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
29. Intlekofer A.M., Takemoto N., Wherry E.J., Longworth S.A., Northrup J.T., Palanivel V.R., Mullen A.C., Gasink C.R., Kaech S.M., Miller J.D., et al. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 2005, 6:1236-1244.
30. John S.A., Clements J.L., Russell L.M., Garrett-Sinha L.A. Ets-1 regulates plasma cell differentiation by interfering with the activity of the transcription factor Blimp-1. J. Biol. Chem. 2008, 283:951-962.
31. Joncker N.T., Raulet D.H. Regulation of NK cell responsiveness to achieve self-tolerance and maximal responses to diseased target cells. Immunol. Rev. 2008, 224:85-97.
32. Joncker N.T., Fernandez N.C., Treiner E., Vivier E., Raulet D.H. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J. Immunol. 2009, 182:4572-4580.
33. Kallies A., Carotta S., Huntington N.D., Bernard N.J., Tarlinton D.M., Smyth M.J., Nutt S.L. A role for Blimp1 in the transcriptional network controlling natural killer cell maturation. Blood 2011, 117:1869-1879.
34. Kamizono S., Duncan G.S., Seidel M.G., Morimoto A., Hamada K., Grosveld G., Akashi K., Lind E.F., Haight J.P., Ohashi P.S., et al. Nfil3/E4bp4 is required for the development and maturation of NK cells in vivo. J. Exp. Med. 2009, 206:2977-2986.
35. Karlhofer F.M., Orihuela M.M., Yokoyama W.M. Ly-49-independent natural killer (NK) cell specificity revealed by NK cell clones derived from p53-deficient mice. J. Exp. Med. 1995, 181:1785-1795.
36. Kee B.L., Murre C. Induction of early B cell factor (EBF) and multiple B lineage genes by the basic helix-loop-helix transcription factor E12. J. Exp. Med. 1998, 188:699-713.
37. Kim S., Iizuka K., Kang H.S., Dokun A., French A.R., Greco S., Yokoyama W.M. In vivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 2002, 3:523-528.
38. Lacorazza H.D., Miyazaki Y., Di Cristofano A., Deblasio A., Hedvat C., Zhang J., Cordon-Cardo C., Mao S., Pandolfi P.P., Nimer S.D. The ETS protein MEF plays a critical role in perforin gene expression and the development of natural killer and NK-T cells. Immunity 2002, 17:437-449.
39. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. 2005, 23:225-274.
40. Lee G.M., Pufall M.A., Meeker C.A., Kang H.S., Graves B.J., McIntosh L.P. The affinity of Ets-1 for DNA is modulated by phosphorylation through transient interactions of an unstructured region. J. Mol. Biol. 2008, 382:1014-1030.
41. Moisan J., Grenningloh R., Bettelli E., Oukka M., Ho I.C. Ets-1 is a negative regulator of Th17 differentiation. J. Exp. Med. 2007, 204:2825-2835.
42. Muthusamy N., Barton K., Leiden J.M. Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature 1995, 377:639-642.
43. Narni-Mancinelli E., Jaeger B.N., Bernat C., Fenis A., Kung S., De Gassart A., Mahmood S., Gut M., Heath S.C., Estellé J., et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012, 335:344-348.
44. Nishimori H., Sasaki Y., Yoshida K., Irifune H., Zembutsu H., Tanaka T., Aoyama T., Hosaka T., Kawaguchi S., Wada T., et al. The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 2002, 21:8302-8309.
45. Nutt S.L., Kee B.L. The transcriptional regulation of B cell lineage commitment. Immunity 2007, 26:715-725.
46. Pufall M.A., Lee G.M., Nelson M.L., Kang H.S., Velyvis A., Kay L.E., McIntosh L.P., Graves B.J. Variable control of Ets-1 DNA binding by multiple phosphates in an unstructured region. Science 2005, 309:142-145.
47. Rodewald H.R., Moingeon P., Lucich J.L., Dosiou C., Lopez P., Reinherz E.L. A population of early fetal thymocytes expressing Fc gamma RII/III contains precursors of T lymphocytes and natural killer cells. Cell 1992, 69:139-150.
48. Rosmaraki E.E., Douagi I., Roth C., Colucci F., Cumano A., Di Santo J.P. Identification of committed NK cell progenitors in adult murine bone marrow. Eur. J. Immunol. 2001, 31:1900-1909.
49. Russell L., Garrett-Sinha L.A. Transcription factor Ets-1 in cytokine and chemokine gene regulation. Cytokine 2010, 51:217-226.
50. Seth A., Papas T.S. The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene 1990, 5:1761-1767.
51. Stewart C.A., Walzer T., Robbins S.H., Malissen B., Vivier E., Prinz I. Germ-line and rearranged Tcrd transcription distinguish bona fide NK cells and NK-like gammadelta T cells. Eur. J. Immunol. 2007, 37:1442-1452.
52. Vivier E., Raulet D.H., Moretta A., Caligiuri M.A., Zitvogel L., Lanier L.L., Yokoyama W.M., Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44-49.
53. Vosshenrich C.A., Ranson T., Samson S.I., Corcuff E., Colucci F., Rosmaraki E.E., Di Santo J.P. Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J. Immunol. 2005, 174:1213-1221.
54. Wang D., John S.A., Clements J.L., Percy D.H., Barton K.P., Garrett-Sinha L.A. Ets-1 deficiency leads to altered B cell differentiation, hyperresponsiveness to TLR9 and autoimmune disease. Int. Immunol. 2005, 17:1179-1191.
55. Wei G.H., Badis G., Berger M.F., Kivioja T., Palin K., Enge M., Bonke M., Jolma A., Varjosalo M., Gehrke A.R., et al. Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 2010, 29:2147-2160.
56. Yokomori N., Kobayashi R., Moore R., Sueyoshi T., Negishi M. A DNA methylation site in the male-specific P450 (Cyp 2d-9) promoter and binding of the heteromeric transcription factor GABP. Mol. Cell. Biol. 1995, 15:5355-5362.
57. Yokota Y., Mansouri A., Mori S., Sugawara S., Adachi S., Nishikawa S., Gruss P. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 1999, 397:702-706.
58. Yokoyama W.M., Kim S. Licensing of natural killer cells by self-major histocompatibility complex class I. Immunol. Rev. 2006, 214:143-154.