Environment drives selection and function of enhancers controlling tissue-specific macrophage identities

Cell

Volumn 159, Issue 6, 2014, Pages 1327-1340

  Gosselin, David ^a   Link, Verena M ^a,b   Romanoski, Casey E ^a   Fonseca, Gregory J ^a   Eichenfield, Dawn Z ^a   Spann, Nathanael J ^a   Stender, Joshua D ^a   Chun, Hyun B ^a   Garner, Hannah ^c,d   Geissmann, Frederic ^c,d   Glass, Christopher K ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR PU 1; TRANSCRIPTOME; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL LINEAGE; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; MACROPHAGE; MALE; MICROENVIRONMENT; MICROGLIA; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; TISSUE STRUCTURE; ANIMAL; C57BL MOUSE; CYTOLOGY; HISTONE CODE; IMMUNOLOGY; INBRED MOUSE STRAIN; METABOLISM; NONOBESE DIABETIC MOUSE;

ANIMALS; ENHANCER ELEMENTS, GENETIC; GENETIC VARIATION; HISTONE CODE; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, INBRED STRAINS; TRANSCRIPTION FACTORS;

EID: 84920724792     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.11.023     Document Type: Article

References (52)

1. R. Andersson, C. Gebhard, I. Miguel-Escalada, I. Hoof, J. Bornholdt, M. Boyd, Y. Chen, X. Zhao, C. Schmidl, T. Suzuki FANTOM Consortium An atlas of active enhancers across human cell types and tissues Nature 507 2014 455 461
2. N.C. Andrews The NF-E2 transcription factor Int. J. Biochem. Cell Biol. 30 1998 429 432
3. I. Barozzi, M. Simonatto, S. Bonifacio, L. Yang, R. Rohs, S. Ghisletti, and G. Natoli Coregulation of transcription factor binding and nucleosome occupancy through DNA features of mammalian enhancers Mol. Cell 54 2014 844 857
4. M. Boudjelal, R. Taneja, S. Matsubara, P. Bouillet, P. Dolle, and P. Chambon Overexpression of Stra13, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells Genes Dev. 11 1997 2052 2065
5. J.D. Brown, C.Y. Lin, Q. Duan, G. Griffin, A.J. Federation, R.M. Paranal, S. Bair, G. Newton, A.H. Lichtman, and A.L. Kung NF-κB Directs Dynamic Super Enhancer Formation in Inflammation and Atherogenesis Mol. Cell 56 2014 219 231
6. O. Butovsky, M.P. Jedrychowski, C.S. Moore, R. Cialic, A.J. Lanser, G. Gabriely, T. Koeglsperger, B. Dake, P.M. Wu, and C.E. Doykan Identification of a unique TGF-β-dependent molecular and functional signature in microglia Nat. Neurosci. 17 2014 131 143
7. A.E. Cardona, E.P. Pioro, M.E. Sasse, V. Kostenko, S.M. Cardona, I.M. Dijkstra, D. Huang, G. Kidd, S. Dombrowski, and R. Dutta Control of microglial neurotoxicity by the fractalkine receptor Nat. Neurosci. 9 2006 917 924
8. M. Civelek, and A.J. Lusis Systems genetics approaches to understand complex traits Nat. Rev. Genet. 15 2014 34 48
9. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, and P.A. Sharp Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
10. A. Dobin, C.A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, and T.R. Gingeras STAR: ultrafast universal RNA-seq aligner Bioinformatics 29 2013 15 21
11. M. Garber, N. Yosef, A. Goren, R. Raychowdhury, A. Thielke, M. Guttman, J. Robinson, B. Minie, N. Chevrier, and Z. Itzhaki A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals Mol. Cell 47 2012 810 822
12. E.L. Gautier, T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K.G. Elpek, S. Gordonov Immunological Genome Consortium Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages Nat. Immunol. 13 2012 1118 1128
13. E.L. Gautier, S. Ivanov, J.W. Williams, S.C. Huang, G. Marcelin, K. Fairfax, P.L. Wang, J.S. Francis, P. Leone, and D.B. Wilson Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival J. Exp. Med. 211 2014 1525 1531
14. F. Geissmann, M.G. Manz, S. Jung, M.H. Sieweke, M. Merad, and K. Ley Development of monocytes, macrophages, and dendritic cells Science 327 2010 656 661
15. S. Ghisletti, I. Barozzi, F. Mietton, S. Polletti, F. De Santa, E. Venturini, L. Gregory, L. Lonie, A. Chew, and C.L. Wei Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages Immunity 32 2010 317 328
16. E.E. Ghosn, A.A. Cassado, G.R. Govoni, T. Fukuhara, Y. Yang, D.M. Monack, K.R. Bortoluci, S.R. Almeida, L.A. Herzenberg, and L.A. Herzenberg Two physically, functionally, and developmentally distinct peritoneal macrophage subsets Proc. Natl. Acad. Sci. USA 107 2010 2568 2573
17. S. Gordon, A. Pluddemann, and F. Martinez Estrada Macrophage heterogeneity in tissues: phenotypic diversity and functions Immunol. Rev. 262 2014 36 55
18. M. Greter, I. Lelios, P. Pelczar, G. Hoeffel, J. Price, M. Leboeuf, T.M. Kündig, K. Frei, F. Ginhoux, M. Merad, and B. Becher Stroma-derived interleukin-34 controls the development and maintenance of langerhans cells and the maintenance of microglia Immunity 37 2012 1050 1060
19. H.H. He, C.A. Meyer, H. Shin, S.T. Bailey, G. Wei, Q. Wang, Y. Zhang, K. Xu, M. Ni, and M. Lupien Nucleosome dynamics define transcriptional enhancers Nat. Genet. 42 2010 343 347
20. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
21. S. Heinz, C.E. Romanoski, C. Benner, K.A. Allison, M.U. Kaikkonen, L.D. Orozco, and C.K. Glass Effect of natural genetic variation on enhancer selection and function Nature 503 2013 487 492
22. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
23. A.V. Ivanova, S.V. Ivanov, X. Zhang, V.N. Ivanov, O.A. Timofeeva, and M.I. Lerman STRA13 interacts with STAT3 and modulates transcription of STAT3-dependent targets J. Mol. Biol. 340 2004 641 653
24. S. Jung, J. Aliberti, P. Graemmel, M.J. Sunshine, G.W. Kreutzberg, A. Sher, and D.R. Littman Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion Mol. Cell. Biol. 20 2000 4106 4114
25. M.U. Kaikkonen, N.J. Spann, S. Heinz, C.E. Romanoski, K.A. Allison, J.D. Stender, H.B. Chun, D.F. Tough, R.K. Prinjha, C. Benner, and C.K. Glass Remodeling of the enhancer landscape during macrophage activation is coupled to enhancer transcription Mol. Cell 51 2013 310 325
26. T.M. Keane, L. Goodstadt, P. Danecek, M.A. White, K. Wong, B. Yalcin, A. Heger, A. Agam, G. Slater, and M. Goodson Mouse genomic variation and its effect on phenotypes and gene regulation Nature 477 2011 289 294
27. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359
28. M. Levine Transcriptional enhancers in animal development and evolution Curr. Bio. 20 2010 R754 R763
29. J. Lovén, H.A. Hoke, C.Y. Lin, A. Lau, D.A. Orlando, C.R. Vakoc, J.E. Bradner, T.I. Lee, and R.A. Young Selective inhibition of tumor oncogenes by disruption of super-enhancers Cell 153 2013 320 334
30. M. Makwana, L.L. Jones, D. Cuthill, H. Heuer, M. Bohatschek, M. Hristova, S. Friedrichsen, I. Ormsby, D. Bueringer, and A. Koppius Endogenous transforming growth factor beta 1 suppresses inflammation and promotes survival in adult CNS J. Neurosci. 27 2007 11201 11213
31. A.C. Mullen, D.A. Orlando, J.J. Newman, J. Lovén, R.M. Kumar, S. Bilodeau, J. Reddy, M.G. Guenther, R.P. DeKoter, and R.A. Young Master transcription factors determine cell-type-specific responses to TGF-β signaling Cell 147 2011 565 576
32. Y. Okabe, and R. Medzhitov Tissue-specific signals control reversible program of localization and functional polarization of macrophages Cell 157 2014 832 844
33. R. Ostuni, V. Piccolo, I. Barozzi, S. Polletti, A. Termanini, S. Bonifacio, A. Curina, E. Prosperini, S. Ghisletti, and G. Natoli Latent enhancers activated by stimulation in differentiated cells Cell 152 2013 157 171
34. R.C. Paolicelli, G. Bolasco, F. Pagani, L. Maggi, M. Scianni, P. Panzanelli, M. Giustetto, T.A. Ferreira, E. Guiducci, and L. Dumas Synaptic pruning by microglia is necessary for normal brain development Science 333 2011 1456 1458
35. E.G. Perdiguero, K. Klapproth, C. Schulz, K. Busch, E. Azzoni, L. Crozet, H. Garner, C. Trouillet, M.F. de Bruijn, and F. Geissmann Tissue-resident macrophages originate from yok sac-derived erythro-myeloid progenitors Nature 2014 10.1038/nature13989 Published online December 3, 2014
36. X. Piao, R.S. Hill, A. Bodell, B.S. Chang, L. Basel-Vanagaite, R. Straussberg, W.B. Dobyns, B. Qasrawi, R.M. Winter, and A.M. Innes G protein-coupled receptor-dependent development of human frontal cortex Science 303 2004 2033 2036
37. D.M. Pilla, J.A. Hagar, A.K. Haldar, A.K. Mason, D. Degrandi, K. Pfeffer, R.K. Ernst, M. Yamamoto, E.A. Miao, and J. Coers Guanylate binding proteins promote caspase-11-dependent pyroptosis in response to cytoplasmic LPS Proc. Natl. Acad. Sci. USA 111 2014 6046 6051
38. M. Rosas, L.C. Davies, P.J. Giles, C.T. Liao, B. Kharfan, T.C. Stone, V.B. O'Donnell, D.J. Fraser, S.A. Jones, and P.R. Taylor The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal Science 344 2014 645 648
39. R.M. Samstein, A. Arvey, S.Z. Josefowicz, X. Peng, A. Reynolds, R. Sandstrom, S. Neph, P. Sabo, J.M. Kim, and W. Liao Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification Cell 151 2012 153 166
40. S. Sarrazin, N. Mossadegh-Keller, T. Fukao, A. Aziz, F. Mourcin, L. Vanhille, L. Kelly Modis, P. Kastner, S. Chan, and E. Duprez MafB restricts M-CSF-dependent myeloid commitment divisions of hematopoietic stem cells Cell 138 2009 300 313
41. C. Schulz, E. Gomez Perdiguero, L. Chorro, H. Szabo-Rogers, N. Cagnard, K. Kierdorf, M. Prinz, B. Wu, S.E. Jacobsen, and J.W. Pollard A lineage of myeloid cells independent of Myb and hematopoietic stem cells Science 336 2012 86 90
42. D. Shlyueva, G. Stampfel, and A. Stark Transcriptional enhancers: from properties to genome-wide predictions Nat. Rev. Genet. 15 2014 272 286
43. V. Steimle, L.A. Otten, M. Zufferey, and B. Mach Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome) Cell 75 1993 135 146
44. D.W. Threadgill, and G.A. Churchill Ten years of the collaborative cross G3 (Bethesda) 2 2012 153 156
45. S. Uderhardt, M. Herrmann, O.V. Oskolkova, S. Aschermann, W. Bicker, N. Ipseiz, K. Sarter, B. Frey, T. Rothe, and R. Voll 12/15-lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance Immunity 36 2012 834 846
46. Y. Wang, K.J. Szretter, W. Vermi, S. Gilfillan, C. Rossini, M. Cella, A.D. Barrow, M.S. Diamond, and M. Colonna IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia Nat. Immunol. 13 2012 753 760
47. W.A. Whyte, D.A. Orlando, D. Hnisz, B.J. Abraham, C.Y. Lin, M.H. Kagey, P.B. Rahl, T.I. Lee, and R.A. Young Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell 153 2013 307 319
48. M.D. Witmer-Pack, D.A. Hughes, G. Schuler, L. Lawson, A. McWilliam, K. Inaba, R.M. Steinman, and S. Gordon Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse J. Cell Sci. 104 1993 1021 1029
49. T.A. Wynn, A. Chawla, and J.W. Pollard Macrophage biology in development, homeostasis and disease Nature 496 2013 445 455
50. M. Yamamoto, M. Okuyama, J.S. Ma, T. Kimura, N. Kamiyama, H. Saiga, J. Ohshima, M. Sasai, H. Kayama, and T. Okamoto A cluster of interferon-γ-inducible p65 GTPases plays a critical role in host defense against Toxoplasma gondii Immunity 37 2012 302 313
51. W. Huang da, B.T. Sherman, and R.A. Lempicki Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 37 2009 1 13
52. W. Huang da, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57