Transcriptome-based profiling of yolk sac-derived macrophages reveals a role for Irf8 in macrophage maturation

EMBO Journal

Volumn 35, Issue 16, 2016, Pages 1730-1744

  Hagemeyer, Nora ^a   Kierdorf, Katrin ^a   Frenzel, Kathrin ^a   Xue, Jia ^b   Ringelhan, Marc ^c,d   Abdullah, Zeinab ^b   Godin, Isabelle ^e   Wieghofer, Peter ^a   Costa Jordão, Marta Joana ^a   Ulas, Thomas ^b   Yorgancioglu, Gülden ^a   Rosenbauer, Frank ^f   Knolle, Percy A ^c   Heikenwalder, Mathias ^c,g   Schultze, Joachim L ^b   Prinz, Marco ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e INSTITUT GUSTAVE ROUSSY   (France)

^f UNIVERSITY OF MÜNSTER   (Germany)

^g GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

CX3CR1; fate mapping; gene profiling; Kupffer cells; macrophages; microglia

Indexed keywords

BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD45 ANTIGEN; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR RUNX1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; TRANSCRIPTOMICS; YOLK SAC;

EID: 84982102656     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201693801     Document Type: Article

References (46)

1. Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM (2007) Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 10: 1538–1543
2. Bain CC, Bravo-Blas A, Scott CL, Gomez PE, Geissmann F, Henri S, Malissen B, Osborne LC, Artis D, Mowat AM (2014) Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat Immunol 15: 929–937
3. Battke F, Symons S, Nieselt K (2010) Mayday - integrative analytics for expression data. BMC Bioinformatics 11: 121
4. Bertrand JY, Jalil A, Klaine M, Jung S, Cumano A, Godin I (2005) Three pathways to mature macrophages in the early mouse yolk sac. Blood 106: 3004–3011
5. Bleriot C, Dupuis T, Jouvion G, Eberl G, Disson O, Lecuit M (2015) Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type-2-mediated tissue repair during bacterial infection. Immunity 42: 145–158
6. Boring L, Gosling J, Chensue SW, Kunkel SL, Farese RV Jr, Broxmeyer HE, Charo IF (1997) Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest 100: 2552–2561
7. Cumano A, Godin I (2007) Ontogeny of the hematopoietic system. Annu Rev Immunol 25: 745–785
8. Epelman S, Lavine KJ, Randolph GJ (2014) Origin and functions of tissue macrophages. Immunity 41: 21–35
9. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, Schwierzeck V, Utermohlen O, Chun E, Garrett WS, McCoy KD, Diefenbach A, Staeheli P, Stecher B, Amit I, Prinz M (2015) Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci 18: 965–977
10. van Furth R, Cohn ZA (1968) The origin and kinetics of mononuclear phagocytes. J Exp Med, 128: 415–435.
11. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, Gordonov S, Mazloom AR, Ma'ayan A, Chua WJ, Hansen TH, Turley SJ, Merad M, Randolph GJ (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol, 13: 1118–1128.
12. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841–845
13. Ginhoux F, Jung S (2014) Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 14: 392–404
14. Goldmann T, Wieghofer P, Muller PF, Wolf Y, Varol D, Yona S, Brendecke SM, Kierdorf K, Staszewski O, Datta M, Luedde T, Heikenwalder M, Jung S, Prinz M (2013) A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat Neurosci 16: 1618–1626
15. Gomez PE, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, Garner H, Trouillet C, de Bruijn MF, Geissmann F, Rodewald HR (2015) Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518: 547–551
16. Gosselin D, Link VM, Romanoski CE, Fonseca GJ, Eichenfield DZ, Spann NJ, Stender JD, Chun HB, Garner H, Geissmann F, Glass CK (2014) Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159: 1327–1340
17. Hambleton S, Salem S, Bustamante J, Bigley V, Boisson-Dupuis S, Azevedo J, Fortin A, Haniffa M, Ceron-Gutierrez L, Bacon CM, Menon G, Trouillet C, McDonald D, Carey P, Ginhoux F, Alsina L, Zumwalt TJ, Kong XF, Kumararatne D, Butler K et al (2011) IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 365: 127–138
18. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, Garcia-Sastre A, Stanley ER, Ginhoux F, Frenette PS et al (2013) Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38: 792–804
19. Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811–818
20. Hoeffel G, Wang Y, Greter M, See P, Teo P, Malleret B, Leboeuf M, Low D, Oller G, Almeida F, Choy SH, Grisotto M, Renia L, Conway SJ, Stanley ER, Chan JK, Ng LG, Samokhvalov IM, Merad M, Ginhoux F (2012) Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J Exp Med 209: 1167–1181
21. Hoeffel G, Chen J, Lavin Y, Low D, Almeida FF, See P, Beaudin AE, Lum J, Low I, Forsberg EC, Poidinger M, Zolezzi F, Larbi A, Ng LG, Chan JK, Greter M, Becher B, Samokhvalov IM, Merad M, Ginhoux F (2015) C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42: 665–678
22. Holtschke T, Lohler J, Kanno Y, Fehr T, Giese N, Rosenbauer F, Lou J, Knobeloch KP, Gabriele L, Waring JF, Bachmann MF, Zinkernagel RM, Morse HC III, Ozato K, Horak I (1996) Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 87: 307–317
23. Huang LR, Wohlleber D, Reisinger F, Jenne CN, Cheng RL, Abdullah Z, Schildberg FA, Odenthal M, Dienes HP, Van RN, Schmitt E, Garbi N, Croft M, Kurts C, Kubes P, Protzer U, Heikenwalder M, Knolle PA (2013) Intrahepatic myeloid-cell aggregates enable local proliferation of CD8(+) T cells and successful immunotherapy against chronic viral liver infection. Nat Immunol 14: 574–583
24. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, Littman DR (2000) Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 20: 4106–4114
25. Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C, Muller DN, Luckow B, Brocker T, Debowski K, Fritz G, Opdenakker G, Diefenbach A, Biber K, Heikenwalder M, Geissmann F et al (2013) Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat Neurosci 16: 273–280
26. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I (2014) Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159: 1312–1326
27. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448–3449
28. McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, Baribault H, Klemsz M, Feeney AJ, Wu GE, Paige CJ, Maki RA (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15: 5647–5658
29. Merico D, Isserlin R, Stueker O, Emili A, Bader GD (2010) Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One 5: e13984
30. Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M (2007) Microglia in the adult brain arise from Ly-6C(hi)CCR2(+) monocytes only under defined host conditions. Nat Neurosci 10: 1544–1553
31. Molawi K, Wolf Y, Kandalla PK, Favret J, Hagemeyer N, Frenzel K, Pinto AR, Klapproth K, Henri S, Malissen B, Rodewald HR, Rosenthal NA, Bajenoff M, Prinz M, Jung S, Sieweke MH (2014) Progressive replacement of embryo-derived cardiac macrophages with age. J Exp Med 211: 2151–2158
32. Newman AM, Liu CL, Green MR, Gentles AJ, Feng W, Xu Y, Hoang CD, Diehn M, Alizadeh AA (2015) Robust enumeration of cell subsets from tissue expression profiles. Nat Methods 12: 453–457
33. Oesper L, Merico D, Isserlin R, Bader GD (2011) WordCloud: a Cytoscape plugin to create a visual semantic summary of networks. Source Code Biol Med 6: 7
34. Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15: 300–312
35. Rosenbauer F, Tenen DG (2007) Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol 7: 105–117
36. Schonheit J, Kuhl C, Gebhardt ML, Klett FF, Riemke P, Scheller M, Huang G, Naumann R, Leutz A, Stocking C, Priller J, Andrade-Navarro MA, Rosenbauer F (2013) PU.1 level-directed chromatin structure remodeling at the irf8 gene drives dendritic cell commitment. Cell Rep 3: 1617–1628
37. Schulz C, Gomez PE, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86–90
38. Scott CL, Zheng F, De BP, Martens L, Saeys Y, De PS, Lippens S, Abels C, Schoonooghe S, Raes G, Devoogdt N, Lambrecht BN, Beschin A, Guilliams M (2016) Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat Commun 7: 10321
39. Sheng J, Ruedl C, Karjalainen K (2015) Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43: 382–393
40. Shiau CE, Kaufman Z, Meireles AM, Talbot WS (2015) Differential requirement for irf8 in formation of embryonic and adult macrophages in zebrafish. PLoS One 10: e0117513
41. Sieweke MH, Allen JE (2013) Beyond stem cells: self-renewal of differentiated macrophages. Science 342: 1242974
42. Tamura T, Ozato K (2002) ICSBP/IRF-8: its regulatory roles in the development of myeloid cells. J Interferon Cytokine Res 22: 145–152
43. Tamura T, Yanai H, Savitsky D, Taniguchi T (2008) The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 26: 535–584
44. Theocharidis A, van Dongen S, Enright AJ, Freeman TC (2009) Network visualization and analysis of gene expression data using BioLayout Express(3D). Nat Protoc, 4: 1535–1550.
45. Wilson K, Grenfell BT (1997) Generalized linear modelling for parasitologists. Parasitol Today 13: 33–38
46. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, Strauss-Ayali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38: 79–91