Murine dendritic cell rapamycin-resistant and rictor-independent mTOR controls IL-10, B7-H1, and regulatory T-cell induction

Blood

Volumn 121, Issue 18, 2013, Pages 3619-3630

  Rosborough, Brian R ^a   Raïch Regué, Dàlia ^a   Matta, Benjamin M ^a   Lee, Keunwook ^b   Gan, Boyi ^c   DePinho, Ronald A ^c   Hackstein, Holger ^d   Boothby, Mark ^b   Turnquist, Heth R ^a,e   Thomson, Angus W ^a,e  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^d UNIVERSITY HOSPITAL GIESSEN   (Germany)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; PROGRAMMED DEATH 1 LIGAND 1; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; CARRIER PROTEIN; MTOR PROTEIN, MOUSE; RAPAMYCIN; RICTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; ENZYME INHIBITION; INFLAMMATORY DISEASE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT;

ANIMALS; ANTIGENS, CD274; CARRIER PROTEINS; CELLS, CULTURED; DENDRITIC CELLS; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; SIROLIMUS; T-LYMPHOCYTES, REGULATORY; TOR SERINE-THREONINE KINASES;

MLCS; MLOWN;

EID: 84879316492     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-448290     Document Type: Article

References (50)

1. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol. 2003;21:685-711. (Pubitemid 37174545)
2. Morelli AE, Thomson AW. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol. 2007;7(8):610-621. (Pubitemid 47123548)
3. Freeman GJ, Long AJ, Iwai Y, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 2000;192(7):1027-1034.
4. Latchman YE, Liang SC, Wu Y, et al. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci USA. 2004;101(29):10691-10696. (Pubitemid 38955804)
5. Sharpe AH, Wherry EJ, Ahmed R, Freeman GJ. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol. 2007;8(3):239-245. (Pubitemid 46745373)
6. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med. 1999;5(12):1365-1369.
7. Francisco LM, Salinas VH, Brown KE, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 2009;206(13):3015-3029.
8. Thomson AW, Turnquist HR, Raimondi G. Immunoregulatory functions of mTOR inhibition. Nat Rev Immunol. 2009;9(5):324-337.
9. Powell JD, Delgoffe GM. The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity. 2010;33(3):301-311.
10. Jacinto E, Loewith R, Schmidt A, et al. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol. 2004;6(11):1122-1128. (Pubitemid 39468014)
11. Sarbassov DD, Ali SM, Kim D-H, et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol. 2004;14(14):1296-1302. (Pubitemid 38991819)
12. Guertin DA, Sabatini DM. The pharmacology of mTOR inhibition. Sci Signal. 2009;2(67):pe24.
13. Thoreen CC, Kang SA, Chang JW, et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem. 2009;284(12):8023-8032.
14. Feldman ME, Apsel B, Uotila A, et al. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 2009;7(2):e38.
15. Taner T, Hackstein H, Wang Z, Morelli AE, Thomson AW. Rapamycin-treated, alloantigen-pulsed host dendritic cells induce ag-specific T cell regulation and prolong graft survival. Am J Transplant. 2005;5(2):228-236. (Pubitemid 40179509)
16. Turnquist HR, Sumpter TL, Tsung A, et al. IL-1beta-driven ST2L expression promotes maturation resistance in rapamycin-conditioned dendritic cells. J Immunol. 2008;181(1):62-72.
17. Weichhart T, Costantino G, Poglitsch M, et al. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity. 2008;29(4):565-577.
18. Schmitz F, Heit A, Dreher S, et al. Mammalian target of rapamycin (mTOR) orchestrates the defense program of innate immune cells. Eur J Immunol. 2008;38(11):2981-2992.
19. Turnquist HR, Cardinal J, Macedo C, et al. mTOR and GSK-3 shape the CD4+ T-cell stimulatory and differentiation capacity of myeloid DCs after exposure to LPS. Blood. 2010;115(23):4758-4769.
20. Haidinger M, Poglitsch M, Geyeregger R, et al. A versatile role of mammalian target of rapamycin in human dendritic cell function and differentiation. J Immunol. 2010;185(7):3919-3931.
21. Wang H, Brown J, Gu Z, et al. Convergence of the mammalian target of rapamycin complex 1- and glycogen synthase kinase 3-β-signaling pathways regulates the innate inflammatory response. J Immunol. 2011;186(9):5217-5226.
22. Lee K, Gudapati P, Dragovic S, et al. Mammalian target of rapamycin protein complex 2 regulates differentiation of Th1 and Th2 cell subsets via distinct signaling pathways. Immunity. 2010;32(6):743-753.
23. Delgoffe GM, Pollizzi KN, Waickman AT, et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol. 2011;12(4):295-303.
24. Yu K, Shi C, Toral-Barza L, et al. Beyond rapalog therapy: preclinical pharmacology and antitumor activity of WYE-125132, an ATP-competitive and specific inhibitor of mTORC1 and mTORC2. Cancer Res. 2010;70(2):621-631.
25. Rosborough BR, Castellaneta A, Natarajan S, Thomson AW, Turnquist HR. Histone deacetylase inhibition facilitates GM-CSF-mediated expansion of myeloid-derived suppressor cells in vitro and in vivo. J Leukoc Biol. 2012;91(5):701-709.
26. Chresta CM, Davies BR, Hickson I, et al. AZD8055 is a potent, selective, and orally bioavailable ATP-competitive mammalian target of rapamycin kinase inhibitor with in vitro and in vivo antitumor activity. Cancer Res. 2010;70(1):288-298.
27. Turnquist HR, Raimondi G, Zahorchak AF, Fischer RT, Wang Z, Thomson AW. Rapamycin-conditioned dendritic cells are poor stimulators of allogeneic CD4+ T cells, but enrich for antigen-specific Foxp3+ T regulatory cells and promote organ transplant tolerance. J Immunol. 2007;178(11):7018-7031. (Pubitemid 46847428)
28. Lee S-J, Jang B-C, Lee S-W, et al. Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-gamma-induced upregulation of B7-H1 (CD274). FEBS Lett. 2006;580(3):755-762. (Pubitemid 43152293)
29. Marzec M, Zhang Q, Goradia A, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci USA. 2008;105(52):20852-20857.
30. Wölfle SJ, Strebovsky J, Bartz H, et al. PD-L1 expression on tolerogenic APCs is controlled by STAT-3. Eur J Immunol. 2011;41(2):413-424.
31. Coffer PJ, Burgering BMT. Forkhead-box transcription factors and their role in the immune system. Nat Rev Immunol. 2004;4(11):889-899. (Pubitemid 39490764)
32. Dejean AS, Beisner DR, Ch'en IL, et al. Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat Immunol. 2009;10(5):504-513.
33. Watkins SK, Zhu Z, Riboldi E, et al. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J Clin Invest. 2011;121(4):1361-1372.
34. Gan B, Lim C, Chu G, et al. FoxOs enforce a progression checkpoint to constrain mTORC1-activated renal tumorigenesis. Cancer Cell. 2010;18(5):472-484.
35. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol. 2007;7(6):454-465. (Pubitemid 46834848)
36. Nakagawa R, Naka T, Tsutsui H, et al. SOCS-1 participates in negative regulation of LPS responses. Immunity. 2002;17(5):677-687. (Pubitemid 35351512)
37. Seki Y-i, Hayashi K, Matsumoto A, et al. Expression of the suppressor of cytokine signaling-5 (SOCS5) negatively regulates IL-4-dependent STAT6 activation and Th2 differentiation. Proc Natl Acad Sci USA. 2002;99(20):13003- 13008.
38. Lang R, Pauleau A-L, Parganas E, et al. SOCS3 regulates the plasticity of gp130 signaling. Nat Immunol. 2003;4(6):546-550. (Pubitemid 36701337)
39. Parham C, Chirica M, Timans J, et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol. 2002;168(11):5699-5708. (Pubitemid 34556153)
40. Brender C, Tannahill GM, Jenkins BJ, et al. Suppressor of cytokine signaling 3 regulates CD8 T-cell proliferation by inhibition of interleukins 6 and 27. Blood. 2007;110(7):2528-2536. (Pubitemid 47523175)
41. Hackstein H, Taner T, Zahorchak AF, et al. Rapamycin inhibits IL-4-induced dendritic cell maturation in vitro and dendritic cell mobilization and function in vivo. Blood. 2003;101(11):4457-4463. (Pubitemid 36857814)
42. Ganesh BB, Bhattacharya P, Gopisetty A, Sheng J, Vasu C, Prabhakar BS. IL-1β promotes TGF-β1 and IL-2 dependent Foxp3 expression in regulatory T cells. PLoS ONE. 2011;6(7):e21949.
43. Salmond RJ, Zamoyska R. The influence of mTOR on T helper cell differentiation and dendritic cell function. Eur J Immunol. 2011;41(8):2137- 2141.
44. Sarbassov DD, Ali SM, Sengupta S, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell. 2006;22(2):159-168.
45. Ohtani M, Nagai S, Kondo S, et al. Mammalian target of rapamycin and glycogen synthase kinase 3 differentially regulate lipopolysaccharide-induced interleukin-12 production in dendritic cells. Blood. 2008;112(3):635-643.
46. Brown J, Wang H, Suttles J, Graves DT, Martin M. Mammalian target of rapamycin complex 2 (mTORC2) negatively regulates Toll-like receptor 4-mediated inflammatory response via FoxO1. J Biol Chem. 2011;286(52):44295-44305.
47. Ohtani M, Hoshii T, Fujii H, Koyasu S, Hirao A, Matsuda S. Cutting edge: mTORC1 in intestinal CD11c+ CD11b+ dendritic cells regulates intestinal homeostasis by promoting IL-10 production. J Immunol. 2012;188(10):4736-4740.
48. Delgoffe GM, Kole TP, Zheng Y, et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity. 2009;30(6):832-844.
49. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8(8):793-800.
50. Chhajed PN, Dickenmann M, Bubendorf L, Mayr M, Steiger J, Tamm M. Patterns of pulmonary complications associated with sirolimus. Respiration. 2006;73(3):367-374. (Pubitemid 43725797)