The Kinase Akt1 Controls Macrophage Response to Lipopolysaccharide by Regulating MicroRNAs

Immunity

Volumn 31, Issue 2, 2009, Pages 220-231

  Androulidaki, Ariadne ^a   Iliopoulos, Dimitrios ^b   Arranz, Alicia ^a   Doxaki, Christina ^a   Schworer, Steffen ^c   Zacharioudaki, Vassiliki ^a   Margioris, Andrew N ^a   Tsichlis, Philip N ^c   Tsatsanis, Christos ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ENDOTOXIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MICRORNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROSTAGLANDIN E2; PROTEIN KINASE B; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL CULTURE; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVATION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE REPRESSION; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSFECTION; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INFECTION RESISTANCE; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; IMMUNE TOLERANCE; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; PROTO-ONCOGENE PROTEINS C-AKT; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTOR 4;

EID: 68649091506     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.06.024     Document Type: Article

References (45)

1. Arranz A., Androulidaki A., Zacharioudaki V., Martinez C., Margioris A.N., Gomariz R.P., and Tsatsanis C. Vasoactive intestinal peptide suppresses toll-like receptor 4 expression in macrophages via Akt1 reducing their responsiveness to lipopolysaccharide. Mol. Immunol. 45 (2008) 2970-2980
2. Baltimore D., Boldin M.P., O'Connell R.M., Rao D.S., and Taganov K.D. MicroRNAs: New regulators of immune cell development and function. Nat. Immunol. 9 (2008) 839-845
3. Bommhardt U., Chang K.C., Swanson P.E., Wagner T.H., Tinsley K.W., Karl I.E., and Hotchkiss R.S. Akt decreases lymphocyte apoptosis and improves survival in sepsis. J. Immunol. 172 (2004) 7583-7591
4. Ceppi M., Pereira P.M., Dunand-Sauthier I., Barras E., Reith W., Santos M.A., and Pierre P. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc. Natl. Acad. Sci. USA 106 (2009) 2735-2740
5. Chen A., Luo M., Yuan G., Yu J., Deng T., Zhang L., Zhou Y., Mitchelson K., and Cheng J. Complementary analysis of microRNA and mRNA expression during phorbol 12-myristate 13-acetate (TPA)-induced differentiation of HL-60 cells. Biotechnol. Lett. 30 (2008) 2045-2052
6. Chen X.M., Splinter P.L., O'Hara S.P., and LaRusso N.F. A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J. Biol. Chem. 282 (2007) 28929-28938
7. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw III E.B., Kaestner K.H., Bartolomei M.S., Shulman G.I., and Birnbaum M.J. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292 (2001) 1728-1731
8. Chong M.M., Rasmussen J.P., Rudensky A.Y., and Littman D.R. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205 (2008) 2005-2017
9. Cobb B.S., Hertweck A., Smith J., O'Connor E., Graf D., Cook T., Smale S.T., Sakaguchi S., Livesey F.J., Fisher A.G., and Merkenschlager M. A role for Dicer in immune regulation. J. Exp. Med. 203 (2006) 2519-2527
10. Dumitru C.D., Ceci J.D., Tsatsanis C., Kontoyiannis D., Stamatakis K., Lin J.H., Patriotis C., Jenkins N.A., Copeland N.G., Kollias G., and Tsichlis P.N. TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway. Cell 103 (2000) 1071-1083
11. Easton R.M., Cho H., Roovers K., Shineman D.W., Mizrahi M., Forman M.S., Lee V.M., Szabolcs M., de Jong R., Oltersdorf T., et al. Role for Akt3/protein kinase Bgamma in attainment of normal brain size. Mol. Cell. Biol. 25 (2005) 1869-1878
12. Fernandez-Hernando C., Ackah E., Yu J., Suarez Y., Murata T., Iwakiri Y., Prendergast J., Miao R.Q., Birnbaum M.J., and Sessa W.C. Loss of akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab. 6 (2007) 446-457
13. Flegel W.A., Baumstark M.W., Weinstock C., Berg A., and Northoff H. Prevention of endotoxin-induced monokine release by human low- and high-density lipoproteins and by apolipoprotein A-I. Infect. Immun. 61 (1993) 5140-5146
14. Freudenberg M.A., Bog-Hansen T.C., Back U., and Galanos C. Interaction of lipopolysaccharides with plasma high-density lipoprotein in rats. Infect. Immun. 28 (1980) 373-380
15. Fukao T., and Koyasu S. PI3K and negative regulation of TLR signaling. Trends Immunol. 24 (2003) 358-363
16. Fukao T., Tanabe M., Terauchi Y., Ota T., Matsuda S., Asano T., Kadowaki T., Takeuchi T., and Koyasu S. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3 (2002) 875-881
17. Guha M., and Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277 (2002) 32124-32132
18. Kinjyo I., Hanada T., Inagaki-Ohara K., Mori H., Aki D., Ohishi M., Yoshida H., Kubo M., and Yoshimura A. SOCS1/JAB is a negative regulator of LPS-induced macrophage activation. Immunity 17 (2002) 583-591
19. Kobayashi K., Hernandez L.D., Galan J.E., Janeway Jr. C.A., Medzhitov R., and Flavell R.A. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110 (2002) 191-202
20. Liston A., Lu L.F., O'Carroll D., Tarakhovsky A., and Rudensky A.Y. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J. Exp. Med. 205 (2008) 1993-2004
21. Lu L.F., Thai T.H., Calado D.P., Chaudhry A., Kubo M., Tanaka K., Loeb G.B., Lee H., Yoshimura A., Rajewsky K., and Rudensky A.Y. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30 (2009) 80-91
22. Luyendyk J.P., Schabbauer G.A., Tencati M., Holscher T., Pawlinski R., and Mackman N. Genetic analysis of the role of the PI3K-Akt pathway in lipopolysaccharide-induced cytokine and tissue factor gene expression in monocytes/macrophages. J. Immunol. 180 (2008) 4218-4226
23. Mao C., Tili E.G., Dose M., Haks M.C., Bear S.E., Maroulakou I., Horie K., Gaitanaris G.A., Fidanza V., Ludwig T., et al. Unequal contribution of Akt isoforms in the double-negative to double-positive thymocyte transition. J. Immunol. 178 (2007) 5443-5453
24. Maroulakou I.G., Oemler W., Naber S.P., and Tsichlis P.N. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice. Cancer Res. 67 (2007) 167-177
25. Martin M., Rehani K., Jope R.S., and Michalek S.M. Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6 (2005) 777-784
26. Maruyama K., Takada Y., Ray N., Kishimoto Y., Penninger J.M., Yasuda H., and Matsuo K. Receptor activator of NF-kappa B ligand and osteoprotegerin regulate proinflammatory cytokine production in mice. J. Immunol. 177 (2006) 3799-3805
27. Medvedev A.E., Kopydlowski K.M., and Vogel S.N. Inhibition of lipopolysaccharide-induced signal transduction in endotoxin-tolerized mouse macrophages: Dysregulation of cytokine, chemokine, and toll-like receptor 2 and 4 gene expression. J. Immunol. 164 (2000) 5564-5574
28. Nakagawa R., Naka T., Tsutsui H., Fujimoto M., Kimura A., Abe T., Seki E., Sato S., Takeuchi O., Takeda K., et al. SOCS-1 participates in negative regulation of LPS responses. Immunity 17 (2002) 677-687
29. Nomura F., Akashi S., Sakao Y., Sato S., Kawai T., Matsumoto M., Nakanishi K., Kimoto M., Miyake K., Takeda K., and Akira S. Cutting edge: Endotoxin tolerance in mouse peritoneal macrophages correlates with down-regulation of surface toll-like receptor 4 expression. J. Immunol. 164 (2000) 3476-3479
30. O'Connell R.M., Chaudhuri A.A., Rao D.S., and Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci. USA 106 (2009) 7113-7118
31. O'Connell R.M., Taganov K.D., Boldin M.P., Cheng G., and Baltimore D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104 (2007) 1604-1609
32. Roger T., Miconnet I., Schiesser A.L., Kai H., Miyake K., and Calandra T. Critical role for Ets, AP-1 and GATA-like transcription factors in regulating mouse Toll-like receptor 4 (Tlr4) gene expression. Biochem. J. 387 (2005) 355-365
33. Ruggiero T., Trabucchi M., De Santa F., Zupo S., Harfe B.D., McManus M.T., Rosenfeld M.G., Briata P., and Gherzi R. LPS induces KH-type splicing regulatory protein-dependent processing of microRNA-155 precursors in macrophages. FASEB J. (2009) 10.1096/fj.09-131342 in press. Published online May 7, 2009
34. Shiratsuchi H., and Basson M.D. Akt2, but not Akt1 or Akt3 mediates pressure-stimulated serum-opsonized latex bead phagocytosis through activating mTOR and p70 S6 kinase. J. Cell. Biochem. 102 (2007) 353-367
35. Thum T., Galuppo P., Wolf C., Fiedler J., Kneitz S., van Laake L.W., Doevendans P.A., Mummery C.L., Borlak J., Haverich A., et al. MicroRNAs in the human heart: A clue to fetal gene reprogramming in heart failure. Circulation 116 (2007) 258-267
36. Tili E., Michaille J.J., Cimino A., Costinean S., Dumitru C.D., Adair B., Fabbri M., Alder H., Liu C.G., Calin G.A., and Croce C.M. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J. Immunol. 179 (2007) 5082-5089
37. Tsatsanis C., Androulidaki A., Alissafi T., Charalampopoulos I., Dermitzaki E., Roger T., Gravanis A., and Margioris A.N. Corticotropin-releasing factor and the urocortins induce the expression of TLR4 in macrophages via activation of the transcription factors PU.1 and AP-1. J. Immunol. 176 (2006) 1869-1877
38. Vigorito E., Perks K.L., Abreu-Goodger C., Bunting S., Xiang Z., Kohlhaas S., Das P.P., Miska E.A., Rodriguez A., Bradley A., et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27 (2007) 847-859
39. Williams D.L., Ozment-Skelton T., and Li C. Modulation of the phosphoinositide 3-kinase signaling pathway alters host response to sepsis, inflammation, and ischemia/reperfusion injury. Shock 25 (2006) 432-439
40. Worm J., Stenvang J., Petri A., Frederiksen K.S., Obad S., Elmen J., Hedtjarn M., Straarup E.M., Hansen J.B., and Kauppinen S. Silencing of microRNA-155 in mice during acute inflammatory response leads to derepression of c/ebp Beta and down-regulation of G-CSF. Nucleic Acids Res. (2009) 10.1093/nar/gkp577 in press. Published online July 13, 2009
41. Xiao C., and Rajewsky K. MicroRNA control in the immune system: Basic principles. Cell 136 (2009) 26-36
42. Yang Z.Z., Tschopp O., Di-Poi N., Bruder E., Baudry A., Dummler B., Wahli W., and Hemmings B.A. Dosage-dependent effects of Akt1/protein kinase Balpha (PKBalpha) and Akt3/PKBgamma on thymus, skin, and cardiovascular and nervous system development in mice. Mol. Cell. Biol. 25 (2005) 10407-10418
43. Yu J., Wang F., Yang G.H., Wang F.L., Ma Y.N., Du Z.W., and Zhang J.W. Human microRNA clusters: Genomic organization and expression profile in leukemia cell lines. Biochem. Biophys. Res. Commun. 349 (2006) 59-68
44. Zhang W.J., Wei H., Hagen T., and Frei B. Alpha-lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc. Natl. Acad. Sci. USA 104 (2007) 4077-4082
45. Zhou X., Jeker L.T., Fife B.T., Zhu S., Anderson M.S., McManus M.T., and Bluestone J.A. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205 (2008) 1983-1991