IRF5 and IRF5 Disease-Risk Variants Increase Glycolysis and Human M1 Macrophage Polarization by Regulating Proximal Signaling and Akt2 Activation

Cell Reports

Volumn 16, Issue 9, 2016, Pages 2442-2455

  Hedl, Matija ^a   Yan, Jie ^a   Abraham, Clara ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; CASPASE RECRUITMENT DOMAIN PROTEIN 15; INTERFERON REGULATORY FACTOR 5; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; PROTEIN KINASE B BETA; PROTEIN RIP2; TRANSCRIPTION FACTOR PU 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; AKT2 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOLOGICAL ADJUVANT; INTERFERON REGULATORY FACTOR; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; IRAK1 PROTEIN, HUMAN; IRF5 PROTEIN, HUMAN; IRF5 PROTEIN, MOUSE; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; NOD2 PROTEIN, HUMAN; PROTEIN BINDING; PROTEIN KINASE B; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE 2; RIPK2 PROTEIN, HUMAN; TIFAB PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC VARIABILITY; GLYCOLYSIS; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; IRF5 GENE; MACROPHAGE; MONOCYTE DERIVED MACROPHAGE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTATION; PRIMARY CELL CULTURE;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADJUVANTS, IMMUNOLOGIC; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERFERON REGULATORY FACTORS; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NOD2 SIGNALING ADAPTOR PROTEIN; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASE 2; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 84989818658     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.07.060     Document Type: Article

References (52)

1. Abraham, C., Cho, J.H., Inflammatory bowel disease. N. Engl. J. Med. 361 (2009), 2066–2078.
2. Arranz, A., Doxaki, C., Vergadi, E., Martinez de la Torre, Y., Vaporidi, K., Lagoudaki, E.D., Ieronymaki, E., Androulidaki, A., Venihaki, M., Margioris, A.N., et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. USA 109 (2012), 9517–9522.
3. Ayi, K., Min-Oo, G., Serghides, L., Crockett, M., Kirby-Allen, M., Quirt, I., Gros, P., Kain, K.C., Pyruvate kinase deficiency and malaria. N. Engl. J. Med. 358 (2008), 1805–1810.
4. Balkhi, M.Y., Fitzgerald, K.A., Pitha, P.M., Functional regulation of MyD88-activated interferon regulatory factor 5 by K63-linked polyubiquitination. Mol. Cell. Biol. 28 (2008), 7296–7308.
5. Barnes, B.J., Kellum, M.J., Field, A.E., Pitha, P.M., Multiple regulatory domains of IRF-5 control activation, cellular localization, and induction of chemokines that mediate recruitment of T lymphocytes. Mol. Cell. Biol. 22 (2002), 5721–5740.
6. Bergstrøm, B., Aune, M.H., Awuh, J.A., Kojen, J.F., Blix, K.J., Ryan, L., Flo, T.H., Mollnes, T.E., Espevik, T., Stenvik, J., TLR8 senses Staphylococcus aureus RNA in human primary monocytes and macrophages and induces IFN-β production via a TAK1-IKKβ-IRF5 signaling pathway. J. Immunol. 195 (2015), 1100–1111.
7. Brognard, J., Sierecki, E., Gao, T., Newton, A.C., PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol. Cell 25 (2007), 917–931.
8. Chang Foreman, H.C., Van Scoy, S., Cheng, T.F., Reich, N.C., Activation of interferon regulatory factor 5 by site specific phosphorylation. PLoS ONE, 7, 2012, e33098.
9. Cramer, T., Yamanishi, Y., Clausen, B.E., Förster, I., Pawlinski, R., Mackman, N., Haase, V.H., Jaenisch, R., Corr, M., Nizet, V., et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112 (2003), 645–657.
10. Dalmas, E., Toubal, A., Alzaid, F., Blazek, K., Eames, H.L., Lebozec, K., Pini, M., Hainault, I., Montastier, E., Denis, R.G., et al. Irf5 deficiency in macrophages promotes beneficial adipose tissue expansion and insulin sensitivity during obesity. Nat. Med. 21 (2015), 610–618.
11. Everts, B., Amiel, E., van der Windt, G.J., Freitas, T.C., Chott, R., Yarasheski, K.E., Pearce, E.L., Pearce, E.J., Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood 120 (2012), 1422–1431.
12. Galván-Peña, S., O'Neill, L.A., Metabolic reprograming in macrophage polarization. Front. Immunol., 5, 2014, 420.
13. Ganeshan, K., Chawla, A., Metabolic regulation of immune responses. Annu. Rev. Immunol. 32 (2014), 609–634.
14. Graham, R.R., Kozyrev, S.V., Baechler, E.C., Reddy, M.V., Plenge, R.M., Bauer, J.W., Ortmann, W.A., Koeuth, T., González Escribano, M.F., Pons-Estel, B., et al., Argentine and Spanish Collaborative Groups. A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat. Genet. 38 (2006), 550–555.
15. Hedl, M., Abraham, C., IRF5 risk polymorphisms contribute to interindividual variance in pattern recognition receptor-mediated cytokine secretion in human monocyte-derived cells. J. Immunol. 188 (2012), 5348–5356.
16. Hedl, M., Li, J., Cho, J.H., Abraham, C., Chronic stimulation of Nod2 mediates tolerance to bacterial products. Proc. Natl. Acad. Sci. USA 104 (2007), 19440–19445.
17. Hers, I., Vincent, E.E., Tavaré, J.M., Akt signalling in health and disease. Cell. Signal. 23 (2011), 1515–1527.
18. Inoue, M., Arikawa, T., Chen, Y.H., Moriwaki, Y., Price, M., Brown, M., Perfect, J.R., Shinohara, M.L., T cells down-regulate macrophage TNF production by IRAK1-mediated IL-10 expression and control innate hyperinflammation. Proc. Natl. Acad. Sci. USA 111 (2014), 5295–5300.
19. Jeffery, E., Church, C.D., Holtrup, B., Colman, L., Rodeheffer, M.S., Rapid depot-specific activation of adipocyte precursor cells at the onset of obesity. Nat. Cell Biol. 17 (2015), 376–385.
20. Kawai, T., Akira, S., Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34 (2011), 637–650.
21. Krausgruber, T., Blazek, K., Smallie, T., Alzabin, S., Lockstone, H., Sahgal, N., Hussell, T., Feldmann, M., Udalova, I.A., IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 12 (2011), 231–238.
22. Krawczyk, C.M., Holowka, T., Sun, J., Blagih, J., Amiel, E., DeBerardinis, R.J., Cross, J.R., Jung, E., Thompson, C.B., Jones, R.G., Pearce, E.J., Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115 (2010), 4742–4749.
23. Lacey, D.C., Achuthan, A., Fleetwood, A.J., Dinh, H., Roiniotis, J., Scholz, G.M., Chang, M.W., Beckman, S.K., Cook, A.D., Hamilton, J.A., Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J. Immunol. 188 (2012), 5752–5765.
24. Lazzari, E., Jefferies, C.A., IRF5-mediated signaling and implications for SLE. Clin. Immunol. 153 (2014), 343–352.
25. Lopez-Pelaez, M., Lamont, D.J., Peggie, M., Shpiro, N., Gray, N.S., Cohen, P., Protein kinase IKKβ-catalyzed phosphorylation of IRF5 at Ser462 induces its dimerization and nuclear translocation in myeloid cells. Proc. Natl. Acad. Sci. USA 111 (2014), 17432–17437.
26. Mansour, S.J., Matten, W.T., Hermann, A.S., Candia, J.M., Rong, S., Fukasawa, K., Vande Woude, G.F., Ahn, N.G., Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265 (1994), 966–970.
27. Marsin, A.S., Bouzin, C., Bertrand, L., Hue, L., The stimulation of glycolysis by hypoxia in activated monocytes is mediated by AMP-activated protein kinase and inducible 6-phosphofructo-2-kinase. J. Biol. Chem. 277 (2002), 30778–30783.
28. Martinez, F.O., Gordon, S., Locati, M., Mantovani, A., Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177 (2006), 7303–7311.
29. Mercurio, F., Zhu, H., Murray, B.W., Shevchenko, A., Bennett, B.L., Li, J., Young, D.B., Barbosa, M., Mann, M., Manning, A., Rao, A., IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278 (1997), 860–866.
30. Muñoz-Pinedo, C., El Mjiyad, N., Ricci, J.E., Cancer metabolism: current perspectives and future directions. Cell Death Dis., 3, 2012, e248.
31. Ni, M., MacFarlane, A.W. 4th, Toft, M., Lowell, C.A., Campbell, K.S., Hamerman, J.A., B-cell adaptor for PI3K (BCAP) negatively regulates Toll-like receptor signaling through activation of PI3K. Proc. Natl. Acad. Sci. USA 109 (2012), 267–272.
32. O'Neill, L.A., Hardie, D.G., Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 493 (2013), 346–355.
33. Opitz, B., Püschel, A., Schmeck, B., Hocke, A.C., Rosseau, S., Hammerschmidt, S., Schumann, R.R., Suttorp, N., Hippenstiel, S., Nucleotide-binding oligomerization domain proteins are innate immune receptors for internalized Streptococcus pneumoniae. J. Biol. Chem. 279 (2004), 36426–36432.
34. Panasyuk, G., Espeillac, C., Chauvin, C., Pradelli, L.A., Horie, Y., Suzuki, A., Annicotte, J.S., Fajas, L., Foretz, M., Verdeguer, F., et al. PPARγ contributes to PKM2 and HK2 expression in fatty liver. Nat. Commun., 3, 2012, 672.
35. Pandey, A.K., Yang, Y., Jiang, Z., Fortune, S.M., Coulombe, F., Behr, M.A., Fitzgerald, K.A., Sassetti, C.M., Kelliher, M.A., NOD2, RIP2 and IRF5 play a critical role in the type I interferon response to Mycobacterium tuberculosis. PLoS Pathog., 5, 2009, e1000500.
36. Pelicano, H., Xu, R.H., Du, M., Feng, L., Sasaki, R., Carew, J.S., Hu, Y., Ramdas, L., Hu, L., Keating, M.J., et al. Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J. Cell Biol. 175 (2006), 913–923.
37. Pore, N., Liu, S., Shu, H.K., Li, B., Haas-Kogan, D., Stokoe, D., Milanini-Mongiat, J., Pages, G., O'Rourke, D.M., Bernhard, E., Maity, A., Sp1 is involved in Akt-mediated induction of VEGF expression through an HIF-1-independent mechanism. Mol. Biol. Cell 15 (2004), 4841–4853.
38. Raingeaud, J., Whitmarsh, A.J., Barrett, T., Dérijard, B., Davis, R.J., MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol. 16 (1996), 1247–1255.
39. Ren, J., Chen, X., Chen, Z.J., IKKβ is an IRF5 kinase that instigates inflammation. Proc. Natl. Acad. Sci. USA 111 (2014), 17438–17443.
40. Rieske, P., Pongubala, J.M., AKT induces transcriptional activity of PU.1 through phosphorylation-mediated modifications within its transactivation domain. J. Biol. Chem. 276 (2001), 8460–8468.
41. Rodríguez-Prados, J.C., Través, P.G., Cuenca, J., Rico, D., Aragonés, J., Martín-Sanz, P., Cascante, M., Boscá, L., Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J. Immunol. 185 (2010), 605–614.
42. Sabbah, A., Chang, T.H., Harnack, R., Frohlich, V., Tominaga, K., Dube, P.H., Xiang, Y., Bose, S., Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 10 (2009), 1073–1080.
43. Saliba, D.G., Heger, A., Eames, H.L., Oikonomopoulos, S., Teixeira, A., Blazek, K., Androulidaki, A., Wong, D., Goh, F.G., Weiss, M., et al. IRF5:RelA interaction targets inflammatory genes in macrophages. Cell Rep. 8 (2014), 1308–1317.
44. Sekine, N., Cirulli, V., Regazzi, R., Brown, L.J., Gine, E., Tamarit-Rodriguez, J., Girotti, M., Marie, S., MacDonald, M.J., Wollheim, C.B., et al. Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic beta-cells. Potential role in nutrient sensing. J. Biol. Chem. 269 (1994), 4895–4902.
45. Seok, J., Warren, H.S., Cuenca, A.G., Mindrinos, M.N., Baker, H.V., Xu, W., Richards, D.R., McDonald-Smith, G.P., Gao, H., Hennessy, L., et al., Inflammation and Host Response to Injury, Large Scale Collaborative Research Program. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110 (2013), 3507–3512.
46. Sica, A., Mantovani, A., Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122 (2012), 787–795.
47. Takaoka, A., Yanai, H., Kondo, S., Duncan, G., Negishi, H., Mizutani, T., Kano, S., Honda, K., Ohba, Y., Mak, T.W., Taniguchi, T., Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434 (2005), 243–249.
48. Tan, Z., Xie, N., Banerjee, S., Cui, H., Fu, M., Thannickal, V.J., Liu, G., The monocarboxylate transporter 4 is required for glycolytic reprogramming and inflammatory response in macrophages. J. Biol. Chem. 290 (2015), 46–55.
49. Troutman, T.D., Hu, W., Fulenchek, S., Yamazaki, T., Kurosaki, T., Bazan, J.F., Pasare, C., Role for B-cell adapter for PI3K (BCAP) as a signaling adapter linking Toll-like receptors (TLRs) to serine/threonine kinases PI3K/Akt. Proc. Natl. Acad. Sci. USA 109 (2012), 273–278.
50. Wang, C., Sandling, J.K., Hagberg, N., Berggren, O., Sigurdsson, S., Karlberg, O., Rönnblom, L., Eloranta, M.L., Syvänen, A.C., Genome-wide profiling of target genes for the systemic lupus erythematosus-associated transcription factors IRF5 and STAT4. Ann. Rheum. Dis. 72 (2013), 96–103.
51. Yamamoto, N., Sato, T., Kawasaki, K., Murosaki, S., Yamamoto, Y., A nonradioisotope, enzymatic assay for 2-deoxyglucose uptake in L6 skeletal muscle cells cultured in a 96-well microplate. Anal. Biochem. 351 (2006), 139–145.
52. Zheng, C., Xiang, J., Hunter, T., Lin, A., The JNKK2-JNK1 fusion protein acts as a constitutively active c-Jun kinase that stimulates c-Jun transcription activity. J. Biol. Chem. 274 (1999), 28966–28971.