TGF-β inhibits the activation and functions of NK cells by repressing the mTOR pathway

Science Signaling

Volumn 9, Issue 415, 2016, Pages

  Viel, Sébastien ^a,b,c,d,e   Marçais, Antoine ^a,b,c,d   Guimaraes, Fernando Souza Fonseca ^f,g   Loftus, Roisin ^h   Rabilloud, Jessica ^a,b,c,d   Grau, Morgan ^a,b,c,d   Degouve, Sophie ^a,b,c,d   Djebali, Sophia ^a,b,c,d   Sanlaville, Amélien ⁱ   Charrier, Emily ^a,b,c,d,e   Bienvenu, Jacques ^a,b,c,d,e   Marie, Julien C ^i,j   Caux, Christophe ⁱ   Marvel, Jacqueline ^a,b,c,d   Town, Liam ^f   Huntington, Nicholas D ^k   Bartholin, Laurent ⁱ   Finlay, David ^h   Smyth, Mark J ^f,g   Walzer, Thierry ^a,b,c,d  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ LYON 1   (France)

^d CNRS   (France)

^e CENTRE HOSPITALIER LYON SUD   (France)

^f QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h TRINITY COLLEGE DUBLIN   (Ireland)

ⁱ CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^j GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^k UNIVERSITY OF MELBOURNE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 15; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; IL15 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE REPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; ANIMAL; CELLULAR IMMUNITY; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; IMMUNITY, CELLULAR; INTERLEUKIN-15; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NEOPLASMS, EXPERIMENTAL; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84959134520     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aad1884     Document Type: Article

References (51)

1. E. Vivier, E. Tomasello, M. Baratin, T. Walzer, S. Ugolini, Functions of natural killer cells. Nat. Immunol. 9, 503-510 (2008).
2. C. Daussy, F. Faure, K. Mayol, S. Viel, G. Gasteiger, E. Charrier, J. Bienvenu, T. Henry, E. Debien, U. A. Hasan, J. Marvel, K. Yoh, S. Takahashi, I. Prinz, S. de Bernard, L. Buffat, T. Walzer, T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J. Exp. Med. 211, 563-577 (2014).
3. H. Peng, X. Jiang, Y. Chen, D. K. Sojka, H. Wei, X. Gao, R. Sun, W. M. Yokoyama, Z. Tian, Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J. Clin. Invest. 123, 1444-1456 (2013).
4. A. Marçais, S. Viel, M. Grau, T. Henry, J. Marvel, T. Walzer, Regulation of mouse NK cell development and function by cytokines. Front. Immunol. 4, 450 (2013).
5. Y. Hayakawa, M. J. Smyth, CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 176, 1517-1524 (2006).
6. L. Chiossone, J. Chaix, N. Fuseri, C. Roth, E. Vivier, T. Walzer, Maturation of mouse NK cells is a 4-stage developmental program. Blood 113, 5488-5496 (2009).
7. T. Walzer, L. Chiossone, J. Chaix, A. Calver, C. Carozzo, L. Garrigue-Antar, Y. Jacques, M. Baratin, E. Tomasello, E. Vivier, Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol. 8, 1337-1344 (2007).
8. M. Lucas, W. Schachterle, K. Oberle, P. Aichele, A. Diefenbach, Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26, 503-517 (2007).
9. A. Marçais, J. Cherfils-Vicini, C. Viant, S. Degouve, S. Viel, A. Fenis, J. Rabilloud, K. Mayol, A. Tavares, J. Bienvenu, Y.-G. Gangloff, E. Gilson, E. Vivier, T. Walzer, The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat. Immunol. 15, 749-757 (2014).
10. X. Xu, L. Ye, K. Araki, R. Ahmed, mTOR, linking metabolism and immunity. Semin. Immunol. 24, 429-435 (2012).
11. A. W. Thomson, H. R. Turnquist, G. Raimondi, Immunoregulatory functions of mTOR inhibition. Nat. Rev. Immunol. 9, 324-337 (2009).
12. M. A. Travis, D. Sheppard, TGF-b activation and function in immunity. Annu. Rev. Immunol. 32, 51-82 (2014).
13. R. Derynck, Y. E. Zhang, Smad-dependent and Smad-independent pathways in TGF-b family signalling. Nature 425, 577-584 (2003).
14. M. O. Li, Y. Y. Wan, S. Sanjabi, A.-K. L. Robertson, R. A. Flavell, Transforming growth factor-b regulation of immune responses. Annu. Rev. Immunol. 24, 99-146 (2006).
15. F. Ghiringhelli, C. Ménard, M. Terme, C. Flament, J. Taieb, N. Chaput, P. E. Puig, S. Novault, B. Escudier, E. Vivier, A. Lecesne, C. Robert, J.-Y. Blay, J. Bernard, S. Caillat-Zucman, A. Freitas, T. Tursz, O. Wagner-Ballon, C. Capron, W. Vainchencker, F. Martin, L. Zitvogel, CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-b-dependent manner. J. Exp. Med. 202, 1075-1085 (2005).
16. M. J. Smyth, M. W. L. Teng, J. Swann, K. Kyparissoudis, D. I. Godfrey, Y. Hayakawa, CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer. J. Immunol. 176, 1582-1587 (2006).
17. J. R. Ortaldo, A. T. Mason, J. J.O'Shea, M. J. Smyth, L. A. Falk, I. C. Kennedy, D. L. Longo, F. W. Ruscetti, Mechanistic studies of transforming growth factor-beta inhibition of IL-2- dependent activation of CD3- large granular lymphocyte functions. Regulation of IL-2R beta (p75) signal transduction. J. Immunol. 146, 3791-3798 (1991).
18. A. M. Malygin, S. Meri, T. Timonen, Regulation of natural killer cell activity by transforming growth factor-b and prostaglandin E2. Scand. J. Immunol. 37, 71-76 (1993).
19. Y. Laouar, F. S. Sutterwala, L. Gorelik, R. A. Flavell, Transforming growth factor-b controls T helper type 1 cell development through regulation of natural killer cell interferon-g. Nat. Immunol. 6, 600-607 (2005).
20. R. Castriconi, C. Cantoni, M. Della Chiesa, M. Vitale, E. Marcenaro, R. Conte, R. Biassoni, C. Bottino, L. Moretta, A. Moretta, Transforming growth factor b1 inhibits expression of NKp30 and NKG2D receptors: Consequences for the NK-mediated killing of dendritic cells. Proc. Natl. Acad. Sci. U.S.A. 100, 4120-4125 (2003).
21. J.-C. Lee, K.-M. Lee, D.-W. Kim, D. S. Heo, Elevated TGF-b1 secretion and downmodulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J. Immunol. 172, 7335-7340 (2004).
22. A. L. Ruiz, S. M. Soudja, C. Deceneux, G. Lauvau, J. C. Marie, NK1.1+ CD8+ T cells escape TGF-b control and contribute to early microbial pathogen response. Nat. Commun. 5, 5150 (2014).
23. J. Yu, M. Wei, B. Becknell, R. Trotta, S. Liu, Z. Boyd, M. S. Jaung, B. W. Blaser, J. Sun, D. M. Benson Jr., H. Mao, A. Yokohama, D. Bhatt, L. Shen, R. Davuluri, M. Weinstein, G. Marcucci, M. A. Caligiuri, Pro- and antiinflammatory cytokine signaling: Reciprocal antagonism regulates interferon-gamma production by human natural killer cells. Immunity 24, 575-590 (2006).
24. J. P. Marcoe, J. R. Lim, K. L. Schaubert, N. Fodil-Cornu, M. Matka, A. L. McCubbrey, A. R. Farr, S. M. Vidal, Y. Laouar, TGF-b is responsible for NK cell immaturity during ontogeny and increased susceptibility to infection during mouse infancy. Nat. Immunol. 13, 843-850 (2012).
25. E. Narni-Mancinelli, J. Chaix, A. Fenis, Y. M. Kerdiles, N. Yessaad, A. Reynders, C. Gregoire, H. Luche, S. Ugolini, E. Tomasello, T. Walzer, E. Vivier, Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. U.S.A. 108, 18324-18329 (2011).
26. P. Levéen, M. Carlsén, A. Makowska, S. Oddsson, J. Larsson, M.-J. Goumans, C. M. Cilio, S. Karlsson, TGF-b type II receptor-deficient thymocytes develop normally but demonstrate increased CD8+ proliferation in vivo. Blood 106, 4234-4240 (2005).
27. D. D. Sarbassov, S. M. Ali, D.-H. Kim, D. A. Guertin, R. R. Latek, H. Erdjument-Bromage, P. Tempst, D. M. Sabatini, Rictor, a novel binding partner of mTOR, defines a rapamycininsensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302 (2004).
28. A. M. Intlekofer, N. Takemoto, E. J. Wherry, S.A. Longworth, J. T.Northrup, V. R. Palanivel, A. C. Mullen, C. R. Gasink, S. M. Kaech, J. D. Miller, L. Gapin, K. Ryan, A. P. Russ, T. Lindsten, J. S. Orange, A. W. Goldrath, R. Ahmed, S. L. Reiner, Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6, 1236-1244 (2005).
29. V. Risson, L. Mazelin, M. Roceri, H. Sanchez, V. Moncollin, C. Corneloup, H. Richard-Bulteau, A. Vignaud, D. Baas, A. Defour, D. Freyssenet, J.-F. Tanti, Y. Le-Marchand-Brustel, B. Ferrier, A. Conjard-Duplany, K. Romanino, S. Bauché, D. Hantaï, M. Mueller, S. C. Kozma, G. Thomas, M. A. Rüegg, A. Ferry, M. Pende, X. Bigard, N. Koulmann, L. Schaeffer, Y.-G. Gangloff, Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J. Cell Biol. 187, 859-874 (2009).
30. L. Bartholin, F. S. Cyprian, D. Vincent, C. N. Garcia, S. Martel, B. Horvat, C. Berthet, S. Goddard-Léon, I. Treilleux, R. Rimokh, J. C. Marie, Generation of mice with conditionally activated transforming growth factor beta signaling through the TbRI/ALK5 receptor. Genesis 46, 724-731 (2008).
31. S. Sauer, L. Bruno, A. Hertweck, D. Finlay, M. Leleu, M. Spivakov, Z. A. Knight, B. S. Cobb, D. Cantrell, E. O'Connor, K. M. Shokat, A. G. Fisher, M. Merkenschlager, T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. U.S.A. 105, 7797-7802 (2008).
32. H. D. Marshall, J. P. Ray, B. J. Laidlaw, N. Zhang, D. Gawande, M. M. Staron, J. Craft, S. M. Kaech, The transforming growth factor beta signaling pathway is critical for the formation of CD4 T follicular helper cells and isotype-switched antibody responses in the lung mucosa. Elife 4, e04851 (2015).
33. J.-S. Delisle, M. Giroux, G. Boucher, J.-R. Landry, M.-P. Hardy, S. Lemieux, R. G. Jones, B. T. Wilhelm, C. Perreault, The TGF-b-Smad3 pathway inhibits CD28-dependent cell growth and proliferation of CD4 T cells. Genes Immun. 14, 115-126 (2013).
34. H. Zeng, H. Chi, mTOR and lymphocyte metabolism. Curr. Opin. Immunol. 25, 347-355 (2013).
35. A. Marçais, T. Walzer, mTOR: A gate to NK cell maturation and activation. Cell Cycle 13, 3315-3316 (2014).
36. R. Trotta, J. Dal Col, J. Yu, D. Ciarlariello, B. Thomas, X. Zhang, J. Allard II, M. Wei, H. Mao, J. C. Byrd, D. Perrotti, M. A. Caligiuri, TGF-b utilizes SMAD3 to inhibit CD16- mediated IFN-g production and antibody-dependent cellular cytotoxicity in human NK cells. J. Immunol. 181, 3784-3792 (2008).
37. M. Barrios-Rodiles, K. R. Brown, B. Ozdamar, R. Bose, Z. Liu, R. S. Donovan, F. Shinjo, Y. Liu, J. Dembowy, I. W. Taylor, V. Luga, N. Przulj, M. Robinson, H. Suzuki, Y. Hayashizaki, I. Jurisica, J. L. Wrana, High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307, 1621-1625 (2005).
38. A. Weiss, L. Attisano, The TGFbeta superfamily signaling pathway. Wiley Interdiscip. Rev. Dev. Biol. 2, 47-63 (2013).
39. R. C. J. D'Souza, A. M. Knittle, N. Nagaraj, M. van Dinther, C. Choudhary, P. ten Dijke, M. Mann, K. Sharma, Time-resolved dissection of early phosphoproteome and ensuing proteome changes in response to TGF-b. Sci. Signal. 7, rs5 (2014).
40. T. Wang, B.-Y. Li, P. D. Danielson, P. C. Shah, S. Rockwell, R. J. Lechleider, J. Martin, T. Manganaro, P. K. Donahoe, The immunophilin FKBP12 functions as a common inhibitor of the TGFb family type I receptors. Cell 86, 435-444 (1996).
41. S. N. Sehgal, Sirolimus: Its discovery, biological properties, and mechanism of action. Transplant. Proc. 35, S7-S14 (2003).
42. V. L. Chiasson, D. Talreja, K. J. Young, P. Chatterjee, A. K. Banes-Berceli, B. M. Mitchell, Fk506 binding protein 12 deficiency in endothelial and hematopoietic cells decreases regulatory T cells and causes hypertension. Hypertension 57, 1167-1175 (2011).
43. D. S. Segundo, J. C. Ruiz, M. Izquierdo, G. Fernández-Fresnedo, C. Gómez-Alamillo, R. Merino, M. J. Benito, E. Cacho, E. Rodrigo, R. Palomar, M. López-Hoyos, M. Arias, Calcineurin inhibitors, but not rapamycin, reduce percentages of CD4+CD25+FOXP3+ regulatory T cells in renal transplant recipients. Transplantation 82, 550-557 (2006).
44. H. Ishigame, M. M. Mosaheb, S. Sanjabi, R. A. Flavell, Truncated form of TGF-bRII, but not its absence, induces memory CD8+ T cell expansion and lymphoproliferative disorder in mice. J. Immunol. 190, 6340-6350 (2013).
45. Y. Zhao, J. Hu, R. Li, J. Song, Y. Kang, S. Liu, D. Zhang, Enhanced NK cell adoptive antitumor effects against breast cancer in vitro via blockade of the transforming growth factor-b signaling pathway. OncoTargets Ther. 8, 1553-1559 (2015).
46. J.-S. Nam, M. Terabe, M. Mamura, M.-J. Kang, H. Chae, C. Stuelten, E. Kohn, B. Tang, H. Sabzevari, M. R. Anver, S. Lawrence, D. Danielpour, S. Lonning, J. A. Berzofsky, L. M. Wakefield, An anti-transforming growth factor b antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res. 68, 3835-3843 (2008).
47. T. Krneta, A. Gillgrass, M. Chew, A. A. Ashkar, The breast tumor microenvironment alters the phenotype and function of natural killer cells. Cell. Mol. Immunol., in press.
48. M. J. Townsend, A. S. Weinmann, J. L. Matsuda, R. Salomon, P. J. Farnham, C. A. Biron, L. Gapin, L. H. Glimcher, T-bet regulates the terminal maturation and homeostasis of NK and Va14i NKT cells. Immunity 20, 477-494 (2004).
49. F. Souza-Fonseca-Guimaraes, A. Young, D. Mittal, L. Martinet, C. Bruedigam, K. Takeda, C. E. Andoniou, M. A. Degli-Esposti, G. R. Hill, M. J. Smyth, NK cells require IL-28R for optimal in vivo activity. Proc. Natl. Acad. Sci. U.S.A. 112, E2376-E2384 (2015).
50. I. Le Mercier, D. Poujol, A. Sanlaville, V. Sisirak, M. Gobert, I. Durand, B. Dubois, I. Treilleux, J. Marvel, J. Vlach, J.-Y. Blay, N. Bendriss-Vermare, C. Caux, I. Puisieux, N. Goutagny, Tumor promotion by intratumoral plasmacytoid dendritic cells is reversed by TLR7 ligand treatment. Cancer Res. 73, 4629-4640 (2013).
51. R. P. Donnelly, R. M. Loftus, S. E. Keating, K. T. Liou, C. A. Biron, C. M. Gardiner, D. K. Finlay, mTORC1-dependent metabolic reprogramming is a prerequisite for NK cell effector function. J. Immunol. 193, 4477-4484 (2014).