Transcription factor foxo1 is a negative regulator of natural killer cell maturation and function

Immunity

Volumn 42, Issue 3, 2015, Pages 457-470

  Deng, Youcai ^a,b,c   Kerdiles, Yann ^d   Chu, Jianhong ^c   Yuan, Shunzong ^c,e   Wang, Youwei ^c   Chen, Xilin ^c,e   Mao, Hsiaoyin ^c   Zhang, Lingling ^c   Zhang, Jianying ^f   Hughes, Tiffany ^c   Deng, Yafei ^b   Zhang, Qi ^b   Wang, Fangjie ^b   Zou, Xianghong ^c   Liu, Chang Gong ^g   Freud, Aharon G ^c   Li, Xiaohui ^b   Caligiuri, Michael A ^a,c   Vivier, Eric ^d,h   Yu, Jianhua ^a,c  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c OHIO STATE UNIVERSITY   (United States)

^d CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^e BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^f OHIO STATE UNIVERSITY   (United States)

^g UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^h ASSISTANCE PUBLIQUE HÔPITAUX DE MARSEILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; L SELECTIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR T BET; FOXO1 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL HOMING; CELL MATURATION; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; LYMPH NODE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; UPREGULATION; ANIMAL; CANCER TRANSPLANTATION; EXPERIMENTAL MELANOMA; GENE EXPRESSION REGULATION; GENETICS; HETEROZYGOTE; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; LUNG TUMOR; LYMPHOCYTE DEPLETION; PATHOLOGY; SECONDARY; SIGNAL TRANSDUCTION; SKIN TUMOR;

ANIMALS; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROZYGOTE; KILLER CELLS, NATURAL; L-SELECTIN; LUNG; LUNG NEOPLASMS; LYMPH NODES; LYMPHOCYTE DEPLETION; MELANOMA, EXPERIMENTAL; MICE; MICE, KNOCKOUT; NEOPLASM TRANSPLANTATION; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; T-BOX DOMAIN PROTEINS;

EID: 84925036069     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.02.006     Document Type: Article

References (48)

1. Allan D.S., Rybalov B., Awong G., Zúñiga-Pflücker J.C., Kopcow H.D., Carlyle J.R., Strominger J.L. TGF-β affects development and differentiation of human natural killer cell subsets. Eur. J. Immunol. 2010, 40:2289-2295.
2. Amin R.H., Schlissel M.S. Foxo1 directly regulates the transcription of recombination-activating genes during B cell development. Nat. Immunol. 2008, 9:613-622.
3. Araya N., Sato T., Ando H., Tomaru U., Yoshida M., Coler-Reilly A., Yagishita N., Yamauchi J., Hasegawa A., Kannagi M., et al. HTLV-1 induces a Th1-like state in CD4+CCR4+ Tcells. J.Clin. Invest. 2014, 124:3431-3442.
4. Bouquet F., Pal A., Pilones K.A., Demaria S., Hann B., Akhurst R.J., Babb J.S., Lonning S.M., DeWyngaert J.K., Formenti S.C., Barcellos-Hoff M.H. TGFβ1 inhibition increases the radiosensitivity of breast cancer cells invitro and promotes tumor control by radiation invivo. Clin. Cancer Res. 2011, 17:6754-6765.
5. Calnan D.R., Brunet A. The FoxO code. Oncogene 2008, 27:2276-2288.
6. 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.
7. Chow K.T., Timblin G.A., McWhirter S.M., Schlissel M.S. MK5 activates Rag transcription via Foxo1 in developing B cells. J.Exp. Med. 2013, 210:1621-1634.
8. Colucci F., Caligiuri M.A., Di Santo J.P. What does it take to make a natural killer?. Nat. Rev. Immunol. 2003, 3:413-425.
9. Deng Y., Chu J., Ren Y., Fan Z., Ji X., Mundy-Bosse B., Yuan S., Hughes T., Zhang J., Cheema B., et al. The natural product phyllanthusmin Cenhances IFN-γ production by human NK cells through upregulation of TLR-mediated NF-κB signaling. J.Immunol. 2014, 193:2994-3002.
10. Di Santo J.P. Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 2006, 24:257-286.
11. Dong X.C., Copps K.D., Guo S., Li Y., Kollipara R., DePinho R.A., White M.F. Inactivation of hepatic Foxo1 by insulin signaling is required for adaptive nutrient homeostasis and endocrine growth regulation. Cell Metab. 2008, 8:65-76.
12. Freud A.G., Becknell B., Roychowdhury S., Mao H.C., Ferketich A.K., Nuovo G.J., Hughes T.L., Marburger T.B., Sung J., Baiocchi R.A., et al. A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 2005, 22:295-304.
13. 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.
14. Hayakawa Y., Smyth M.J. CD27 dissects mature NK cells into twosubsets with distinct responsiveness and migratory capacity. J.Immunol. 2006, 176:1517-1524.
15. Hedrick S.M., Hess Michelini R., Doedens A.L., Goldrath A.W., Stone E.L. FOXO transcription factors throughout Tcell biology. Nat. Rev. Immunol. 2012, 12:649-661.
16. Hess Michelini R., Doedens A.L., Goldrath A.W., Hedrick S.M. Differentiation of CD8 memory Tcells depends on Foxo1. J.Exp. Med. 2013, 210:1189-1200.
17. Hesslein D.G., Lanier L.L. Transcriptional control of natural killer cell development and function. Adv. Immunol. 2011, 109:45-85.
18. Huntington N.D., Tabarias H., Fairfax K., Brady J., Hayakawa Y., Degli-Esposti M.A., Smyth M.J., Tarlinton D.M., Nutt S.L. NK cell maturation and peripheral homeostasis is associated with KLRG1 up-regulation. J.Immunol. 2007, 178:4764-4770.
19. Huntington N.D., Nutt S.L., Carotta S. Regulation of murine natural killer cell commitment. Front. Immunol. 2013, 4:14.
20. Kerdiles Y.M., Beisner D.R., Tinoco R., Dejean A.S., Castrillon D.H., DePinho R.A., Hedrick S.M. Foxo1 links homing and survival of naive Tcells by regulating L-selectin, CCR7 and interleukin 7 receptor. Nat. Immunol. 2009, 10:176-184.
21. Kim S., Iizuka K., Kang H.S., Dokun A., French A.R., Greco S., Yokoyama W.M. Invivo developmental stages in murine natural killer cell maturation. Nat. Immunol. 2002, 3:523-528.
22. Kim M.V., Ouyang W., Liao W., Zhang M.Q., Li M.O. The transcription factor Foxo1 controls central-memory CD8+ Tcell responses to infection. Immunity 2013, 39:286-297.
23. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. 2005, 23:225-274.
24. Li H., Liang J., Castrillon D.H., DePinho R.A., Olson E.N., Liu Z.P. FoxO4 regulates tumor necrosis factor alpha-directed smooth muscle cell migration by activating matrix metalloproteinase 9 gene transcription. Mol.Cell. Biol. 2007, 27:2676-2686.
25. Liu J., Liao S., Diop-Frimpong B., Chen W., Goel S., Naxerova K., Ancukiewicz M., Boucher Y., Jain R.K., Xu L. TGF-β blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma. Proc. Natl. Acad. Sci. USA 2012, 109:16618-16623.
26. Luevano M., Madrigal A., Saudemont A. Transcription factors involved in the regulation of natural killer cell development and function: an update. Front. Immunol. 2012, 3:319.
27. Marcoe J.P., Lim J.R., Schaubert K.L., Fodil-Cornu N., Matka M., McCubbrey A.L., Farr A.R., Vidal S.M., Laouar Y. TGF-β is responsible for NK cell immaturity during ontogeny and increased susceptibility to infection during mouse infancy. Nat. Immunol. 2012, 13:843-850.
28. Martín-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A., Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 2004, 5:1260-1265.
29. Narni-Mancinelli E., Chaix J., Fenis A., Kerdiles Y.M., Yessaad N., Reynders A., Gregoire C., Luche H., Ugolini S., Tomasello E., et al. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 2011, 108:18324-18329.
30. Ouyang W., Liao W., Luo C.T., Yin N., Huse M., Kim M.V., Peng M., Chan P., Ma Q., Mo Y., et al. Novel Foxo1-dependent transcriptional programs control T(reg) cell function. Nature 2012, 491:554-559.
31. Ramirez K., Kee B.L. Transcriptional regulation of natural killer cell development. Curr. Opin. Immunol. 2010, 22:193-198.
32. Rao R.R., Li Q., Gubbels Bupp M.R., Shrikant P.A. Transcription factor Foxo1 represses T-bet-mediated effector functions and promotes memory CD8(+) Tcell differentiation. Immunity 2012, 36:374-387.
33. Soderquest K., Powell N., Luci C., van Rooijen N., Hidalgo A., Geissmann F., Walzer T., Lord G.M., Martín-Fontecha A. Monocytes control natural killer cell differentiation to effector phenotypes. Blood 2011, 117:4511-4518.
34. Staron M.M., Gray S.M., Marshall H.D., Parish I.A., Chen J.H., Perry C.J., Cui G., Li M.O., Kaech S.M. The transcription factor FoxO1 sustains expression of the inhibitory receptor PD-1 and survival of antiviral CD8(+) Tcells during chronic infection. Immunity 2014, 41:802-814.
35. Togher S., Larange A., Schoenberger S.P., Feau S. FoxO3 is a negative regulator of primary CD8(+) T-cell expansion but not of memory formation. Immunol. Cell Biol. 2015, 93:120-125.
36. Tong Q., He S., Xie F., Mochizuki K., Liu Y., Mochizuki I., Meng L., Sun H., Zhang Y., Guo Y., et al. Ezh2 regulates transcriptional and posttranslational expression of T-bet and promotes Th1 cell responses mediating aplastic anemia in mice. J.Immunol. 2014, 192:5012-5022.
37. Townsend M.J., Weinmann A.S., Matsuda J.L., Salomon R., Farnham P.J., Biron C.A., Gapin L., Glimcher L.H. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 2004, 20:477-494.
38. Trotta R., Parihar R., Yu J., Becknell B., Allard J., Wen J., Ding W., Mao H., Tridandapani S., Carson W.E., Caligiuri M.A. Differential expression of SHIP1 in CD56bright and CD56dim NK cells providesa molecular basis for distinct functional responses to monokine costimulation. Blood 2005, 105:3011-3018.
39. 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.
40. Vivier E., Ugolini S., Blaise D., Chabannon C., Brossay L. Targeting natural killer cells and natural killer Tcells in cancer. Nat. Rev. Immunol. 2012, 12:239-252.
41. Werneck M.B., Lugo-Villarino G., Hwang E.S., Cantor H., Glimcher L.H. T-bet plays a key role in NK-mediated control of melanoma metastatic disease. J.Immunol. 2008, 180:8004-8010.
42. Yokoyama W.M., Kim S., French A.R. The dynamic life of natural killer cells. Annu. Rev. Immunol. 2004, 22:405-429.
43. Yu J., Wei M., Becknell B., Trotta R., Liu S., Boyd Z., Jaung M.S., Blaser B.W., Sun J., Benson D.M., et al. Pro- and antiinflammatory cytokine signaling: reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity 2006, 24:575-590.
44. Yu J., Wei M., Boyd Z., Lehmann E.B., Trotta R., Mao H., Liu S., Becknell B., Jaung M.S., Jarjoura D., et al. Transcriptional control of human T-BET expression: the role of Sp1. Eur. J. Immunol. 2007, 37:2549-2561.
45. Yu J., Mao H.C., Wei M., Hughes T., Zhang J., Park I.K., Liu S., McClory S., Marcucci G., Trotta R., Caligiuri M.A. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood 2010, 115:274-281.
46. Yu J., Freud A.G., Caligiuri M.A. Location and cellular stages of natural killer cell development. Trends Immunol. 2013, 34:573-582.
47. Yun S., Lee S.H., Yoon S.R., Kim M.S., Piao Z.H., Myung P.K., Kim T.D., Jung H., Choi I. TOX regulates the differentiation of human natural killer cells from hematopoietic stem cells invitro. Immunol. Lett. 2011, 136:29-36.
48. Zwaagstra J.C., Sulea T., Baardsnes J., Lenferink A.E., Collins C., Cantin C., Paul-Roc B., Grothe S., Hossain S., Richer L.P., et al. Engineering and therapeutic application of single-chain bivalent TGF-β family traps. Mol. Cancer Ther. 2012, 11:1477-1487.