Redefining the transcriptional regulatory dynamics of classically and alternatively activated macrophages by deepCAGE transcriptomics

Nucleic Acids Research

Volumn 43, Issue 14, 2015, Pages 6969-6982

  Roy, Sugata ^a   Schmeier, Sebastian ^b   Arner, Erik ^a   Alam, Tanvir ^c   Parihar, Suraj P ^d,e   Ozturk, Mumin ^d,e   Tamgue, Ousman ^d,e   Kawaji, Hideya ^a   De Hoon, Michiel J L ^a   Itoh, Masayoshi ^a   Lassmann, Timo ^a   Carninci, Piero ^a   Hayashizaki, Yoshihide ^a   Forrest, Alistair R R ^a   Bajic, Vladimir B ^c   Guler, Reto ^d,e   Brombacher, Frank ^d,e   Suzuki, Harukazu ^a  

^a RIKEN   (Japan)

^b MASSEY UNIVERSITY   (New Zealand)

^c KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^d INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^e UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CHEMOKINE RECEPTOR CCR1; COLLAGENASE 3; CXCL2 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 13; INTERLEUKIN 27; INTERLEUKIN 4; LONG UNTRANSLATED RNA; MACROPHAGE ELASTASE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; NFIL3 PROTEIN; NUCLEAR FACTOR KAPPA B1; PROTEIN HIVEP1; SOMATOMEDIN C; SUPPRESSOR OF CYTOKINE SIGNALING 2; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAFF; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; UNINDEXED DRUG; DNA; TRANSCRIPTOME;

ANIMAL CELL; ARG1 GENE; ARTICLE; BIOINFORMATICS; BONE MARROW DERIVED MACROPHAGE; CAPPED ANALYSIS OF GENE EXPRESSION; CCL17 GENE; CCL22 GENE; CCL4 GENE; CCL7 GENE; CCLL2 GENE; CCR1 GENE; CONTROLLED STUDY; CXCL1 GENE; CXCL10 GENE; CXCL2 GENE; CXCL3 GENE; DOWN REGULATION; GBP5 GENE; GBP7 GENE; GENE EXPRESSION; HNRPLL GENE; IFI205 GENE; IGF1 GENE; IL 4IL GENE; IL15RA GENE; IL27 GENE; INFANT; IRG1 GENE; MACROPHAGE ACTIVATION; MALE; MARKER GENE; MGL2 GENE; MMP12 GENE; MMP13 GENE; MOTIF ACTIVITY RESPONSE ANALYSIS; MOUSE; NONHUMAN; NOS2 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MOTIF; SOCS2 GENE; ST7 GENE; STX11 GENE; TNF GENE; TNFSF10 GENE; TNFSF9 GENE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; DNA SEQUENCE; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; MACROPHAGE; METABOLISM; NUCLEOTIDE MOTIF;

ANIMALS; CELLS, CULTURED; DNA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INTERFERON-GAMMA; INTERLEUKIN-13; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MICE, INBRED BALB C; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84944471180     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv646     Document Type: Article

References (59)

1. Martinez, F.O., Gordon, S., Locati, M. and Mantovani, A. (2006) Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol., 177, 7303-7311.
2. Gordon, S. (2003) Alternative activation of macrophages. Nat. Rev. Immunol., 3, 23-35.
3. Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T. et al. (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity, 41, 14-20.
4. Nathan, C.F., Murray, H.W., Wiebe, M.E. and Rubin, B.Y. (1983) Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med., 158, 670-689.
5. Odegaard, J.I., Ricardo-Gonzalez, R.R., Goforth, M.H., Morel, C.R., Subramanian, V., Mukundan, L., Red Eagle, A., Vats, D., Brombacher, F., Ferrante, A.W. et al. (2007) Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature, 447, 1116-1120.
6. Nguyen, K.D., Qiu, Y., Cui, X., Goh, Y.P., Mwangi, J., David, T., Mukundan, L., Brombacher, F., Locksley, R.M. and Chawla, A. (2011) Alternatively activated macrophages produce catecholamines to sustain adaptive thermogenesis. Nature, 480, 104-108.
7. Jenkins, S.J., Ruckerl, D., Thomas, G.D., Hewitson, J.P., Duncan, S., Brombacher, F., Maizels, R.M., Hume, D.A. and Allen, J.E. (2013) IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med., 210, 2477-2491.
8. Mantovani, A., Sica, A., Sozzani, S., Allavena, P., Vecchi, A. and Locati, M. (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol., 25, 677-686.
9. Martinez, F.O., Sica, A., Mantovani, A. and Locati, M. (2008) Macrophage activation and polarization. Front. Biosci., 13, 453-461.
10. Herbert, D.R., Holscher, C., Mohrs, M., Arendse, B., Schwegmann, A., Radwanska, M., Leeto, M., Kirsch, R., Hall, P., Mossmann, H. et al. (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity, 20, 623-635.
11. Guler, R., Parihar, S.P., Savvi, S., Logan, E., Schwegmann, A., Roy, S., Nieuwenhuizen, N.E., Ozturk, M., Schmeier, S., Suzuki, H. et al. (2015) IL-4Ralpha-dependent alternative activation of macrophages is not decisive for Mycobacterium tuberculosis pathology and bacterial burden in mice. PLoS ONE, 10, e0121070.
12. Xue, J., Schmidt, S.V., Sander, J., Draffehn, A., Krebs, W., Quester, I., De Nardo, D., Gohel, T.D., Emde, M., Schmidleithner, L. et al. (2014) Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity, 40, 274-288.
13. Kahnert, A., Seiler, P., Stein, M., Bandermann, S., Hahnke, K., Mollenkopf, H. and Kaufmann, S.H. (2006) Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur. J. Immunol., 36, 631-647.
14. Heng, T.S. and Painter, M.W. (2008) The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol., 9, 1091-1094.
15. Poland, G.A., Quill, H. and Togias, A. (2013) Understanding the human immune system in the 21st century: the Human Immunology Project Consortium. Vaccine, 31, 2911-2912.
16. Gautier, E.L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K.G., Gordonov, S. et al. (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages.Nat. Immunol., 13, 1118-1128.
17. Miller, J.C., Brown, B.D., Shay, T., Gautier, E.L., Jojic, V., Cohain, A., Pandey, G., Leboeuf, M., Elpek, K.G., Helft, J. et al. (2012) Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol., 13, 888-899.
18. McDermott, J.E., Archuleta, M., Thrall, B.D., Adkins, J.N. and Waters, K.M. (2011) Controlling the response: predictive modeling of a highly central, pathogen-targeted core response module in macrophage activation. PLoS One, 6, e14673.
19. Nau, G.J., Richmond, J.F., Schlesinger, A., Jennings, E.G., Lander, E.S. and Young, R.A. (2002) Human macrophage activation programs induced by bacterial pathogens. Proc. Natl. Acad. Sci. U.S.A., 99, 1503-1508.
20. Ramsey, S.A., Klemm, S.L., Zak, D.E., Kennedy, K.A., Thorsson, V., Li, B., Gilchrist, M., Gold, E.S., Johnson, C.D., Litvak, V. et al. (2008) Uncovering a macrophage transcriptional program by integrating evidence from motif scanning and expression dynamics. PLoS Comput. Biol., 4, e1000021.
21. Hu, X. and Ivashkiv, L.B. (2009) Cross-regulation of signaling pathways by interferon-gamma: implications for immune responses and autoimmune diseases. Immunity, 31, 539-550.
22. Tamura, T., Yanai, H., Savitsky, D. and Taniguchi, T. (2008) The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol., 26, 535-584.
23. Waddell, S.J., Popper, S.J., Rubins, K.H., Griffiths, M.J., Brown, P.O., Levin, M. and Relman, D.A. (2010) Dissecting interferon-induced transcriptional programs in human peripheral blood cells. PLoS One, 5, e9753.
24. Satoh, T., Takeuchi, O., Vandenbon, A., Yasuda, K., Tanaka, Y., Kumagai, Y., Miyake, T., Matsushita, K., Okazaki, T., Saitoh, T. et al. (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol., 11, 936-944.
25. Lawrence, T. (2009) The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb. Perspect. Biol., 1, a001651.
26. Wang, N., Liang, H. and Zen, K. (2014) Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front. Immunol., 5, 614.
27. Benson, S.A. and Ernst, J.D. (2009) TLR2-dependent inhibition of macrophage responses to IFN-gamma is mediated by distinct, gene-specific mechanisms. PLoS One, 4, e6329.
28. Martinez, F.O. and Gordon, S. (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000prime Rep., 6, 13.
29. Sanson, M., Distel, E. and Fisher, E.A. (2013) HDL induces the expression of the M2 macrophage markers arginase 1 and Fizz-1 in a STAT6-dependent process. PLoS One, 8, e74676.
30. Pello, O.M., De Pizzol, M., Mirolo, M., Soucek, L., Zammataro, L., Amabile, A., Doni, A., Nebuloni, M., Swigart, L.B., Evan, G.I. et al. (2012) Role of c-MYC in alternative activation of human macrophages and tumor-associated macrophage biology. Blood, 119, 411-421.
31. Rehli, M., Sulzbacher, S., Pape, S., Ravasi, T., Wells, C.A., Heinz, S., Sollner, L., El Chartouni, C., Krause, S.W., Steingrimsson, E. et al. (2005) Transcription factor Tfec contributes to the IL-4-inducible expression of a small group of genes in mouse macrophages including the granulocyte colony-stimulating factor receptor. J. Immunol., 174, 7111-7122.
32. Fontana, M.F., Baccarella, A., Pancholi, N., Pufall, M.A., Herbert, D.R. and Kim, C.C. (2015) JUNB is a key transcriptional modulator of macrophage activation. J. Immunol., 194, 177-186.
33. Shay, J.E. and Celeste Simon, M. (2012) Hypoxia-inducible factors: crosstalk between inflammation and metabolism. Semin. Cell Dev. Biol., 23, 389-394.
34. Forrest, A.R., Kawaji, H., Rehli, M., Baillie, J.K., de Hoon, M.J., Haberle, V., Lassman, T., Kulakovskiy, I.V., Lizio, M., Itoh, M. et al. (2014) A promoter-level mammalian expression atlas. Nature, 507, 462-470.
35. Andersson, R., Gebhard, C., Miguel-Escalada, I., Hoof, I., Bornholdt, J., Boyd, M., Chen, Y., Zhao, X., Schmidl, C., Suzuki, T. et al. (2014) An atlas of active enhancers across human cell types and tissues. Nature, 507, 455-461.
36. Schmidl, C., Renner, K., Peter, K., Eder, R., Lassmann, T., Balwierz, P.J., Itoh, M., Nagao-Sato, S., Kawaji, H., Carninci, P. et al. (2014) Transcription and enhancer profiling in human monocyte subsets. Blood, 123, e90-e99.
37. Arner, E., Daub, C.O., Vitting-Seerup, K., Andersson, R., Lilje, B., Drablos, F., Lennartsson, A., Ronnerblad, M., Hrydziuszko, O., Vitezic, M. et al. (2015) Gene regulation. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science, 347, 1010-1014.
38. Schwegmann, A., Guler, R., Cutler, A.J., Arendse, B., Horsnell, W.G., Flemming, A., Kottmann, A.H., Ryan, G., Hide, W., Leitges, M. et al. (2007) Protein kinase C delta is essential for optimal macrophage-mediated phagosomal containment of Listeria monocytogenes. Proc. Natl. Acad. Sci. U.S.A., 104, 16251-16256.
39. Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
40. Suzuki, H., Forrest, A.R., van Nimwegen, E., Daub, C.O., Balwierz, P.J., Irvine, K.M., Lassmann, T., Ravasi, T., Hasegawa, Y., de Hoon, M.J. et al. (2009) The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat. Genet., 41, 553-562.
41. Balwierz, P.J., Carninci, P., Daub, C.O., Kawai, J., Hayashizaki, Y., Van Belle, W., Beisel, C. and van Nimwegen, E. (2009) Methods for analyzing deep sequencing expression data: constructing the human and mouse promoterome with deepCAGE data. Genome Biol., 10, R79.
42. Anders, S., McCarthy, D.J., Chen, Y., Okoniewski, M., Smyth, G.K., Huber, W. and Robinson, M.D. (2013) Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature protocols, 8, 1765-1786.
43. Alam, T., Medvedeva, Y.A., Jia, H., Brown, J.B., Lipovich, L. and Bajic, V.B. (2014) Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes. PLoS One, 9, e109443.
44. Balwierz, P.J., Pachkov, M., Arnold, P., Gruber, A.J., Zavolan, M. and van Nimwegen, E. (2014) ISMARA: automated modeling of genomic signals as a democracy of regulatory motifs. Genome Res., 24, 869-884.
45. Martinez, F.O., Helming, L., Milde, R., Varin, A., Melgert, B.N., Draijer, C., Thomas, B., Fabbri, M., Crawshaw, A., Ho, L.P. et al. (2013) Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood, 121, e57-69.
46. Bhatt, D.M., Pandya-Jones, A., Tong, A.J., Barozzi, I., Lissner, M.M., Natoli, G., Black, D.L. and Smale, S.T. (2012) Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions. Cell, 150, 279-290.
47. Butler, J.E. and Kadonaga, J.T. (2002) The RNA polymerase II core promoter: a key component in the regulation of gene expression. Genes Dev., 16, 2583-2592.
48. Tussiwand, R., Lee, W.L., Murphy, T.L., Mashayekhi, M., Wumesh, K.C., Albring, J.C., Satpathy, A.T., Rotondo, J.A., Edelson, B.T., Kretzer, N.M. et al. (2012) Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature, 490, 502-507.
49. Roy, S., Guler, R., Parihar, S.P., Schmeier, S., Kaczkowski, B., Nishimura, H., Shin, J.W., Negishi, Y., Ozturk, M., Hurdayal, R. et al. (2015) Batf2/Irf1 induces inflammatory responses in classically activated macrophages, lipopolysaccharides, and mycobacterial infection. J. Immunol., 194, 6035-6044.
50. El Chartouni, C., Schwarzfischer, L. and Rehli, M. (2010) Interleukin-4 induced interferon regulatory factor (Irf) 4 participates in the regulation of alternative macrophage priming. Immunobiology, 215, 821-825.
51. Bowdridge, S. and Gause, W.C. (2010) Regulation of alternative macrophage activation by chromatin remodeling. Nat. Immunol., 11, 879-881.
52. Smith, A.M., Qualls, J.E., O'Brien, K., Balouzian, L., Johnson, P.F., Schultz-Cherry, S., Smale, S.T. and Murray, P.J. (2011) A distal enhancer in Il12b is the target of transcriptional repression by the STAT3 pathway and requires the basic leucine zipper (B-ZIP) protein NFIL3. J. Biol. Chem., 286, 23582-23590.
53. Kobayashi, T., Matsuoka, K., Sheikh, S.Z., Elloumi, H.Z., Kamada, N., Hisamatsu, T., Hansen, J.J., Doty, K.R., Pope, S.D., Smale, S.T. et al. (2011) NFIL3 is a regulator of IL-12 p40 in macrophages and mucosal immunity. J. Immunol., 186, 4649-4655.
54. Zhao, X., Ross, E.J., Wang, Y. and Horwitz, B.H. (2012) Nfkb1 inhibits LPS-induced IFN-beta and IL-12 p40 production in macrophages by distinct mechanisms. PLoS One, 7, e32811.
55. Matsushita, K., Takeuchi, O., Standley, D.M., Kumagai, Y., Kawagoe, T., Miyake, T., Satoh, T., Kato, H., Tsujimura, T., Nakamura, H. et al. (2009) Zc3h12a is an RNase essential for controlling immune responses by regulating mRNA decay. Nature, 458, 1185-1190.
56. Masuda, K., Ripley, B., Nishimura, R., Mino, T., Takeuchi, O., Shioi, G., Kiyonari, H. and Kishimoto, T. (2013) Arid5a controls IL-6 mRNA stability, which contributes to elevation of IL-6 level in vivo. Proc. Natl. Acad. Sci. U.S.A., 110, 9409-9414.
57. Grigoriadis, G., Zhan, Y., Grumont, R.J., Metcalf, D., Handman, E., Cheers, C. and Gerondakis, S. (1996) The Rel subunit of NF-kappaB-like transcription factors is a positive and negative regulator of macrophage gene expression: distinct roles for Rel in different macrophage populations. EMBO J., 15, 7099-7107.
58. Tugal, D., Liao, X. and Jain, M.K. (2013) Transcriptional control of macrophage polarization. Arterioscler. Thromb. Vasc. Biol., 33, 1135-1144.
59. Mancino, A., Termanini, A., Barozzi, I., Ghisletti, S., Ostuni, R., Prosperini, E., Ozato, K. and Natoli, G. (2015) A dual cis-regulatory code links IRF8 to constitutive and inducible gene expression in macrophages. Genes Dev., 29, 394-408.