New insights into the multidimensional concept of macrophage ontogeny, activation and function

Nature Immunology

Volumn 17, Issue 1, 2016, Pages 34-40

  Ginhoux, Florent ^a   Schultze, Joachim L ^b,c   Murray, Peter J ^d   Ochando, Jordi ^e,f   Biswas, Subhra K ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b UNIVERSITY OF BONN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ISOLATION; FETUS LIVER; HOMEOSTASIS; HUMAN; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MONOCYTE; ONTOGENY; PHENOTYPE; PRIORITY JOURNAL; REVIEW; YOLK SAC; ANIMAL; IMMUNOLOGY; MACROPHAGE;

ANIMALS; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGES;

EID: 84951335282     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3324     Document Type: Review

References (96)

1. Wynn, T.A., Chawla, A., & Pollard, J.W. Macrophage biology in development, homeostasis and disease. Nature 496, 445-455 (2013
2. Gordon, S., & Taylor, P.R. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953-964 (2005
3. Mantovani, A., Sozzani, S., Locati, M., Allavena, P., & Sica, A. Macrophage polarization: tumor-Associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 23, 549-555 (2002
4. Xue J., et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40, 274-288 (2014
5. Ginhoux, F., & Jung, S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 14, 392-404 (2014
6. Lavin Y., et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159, 1312-1326 (2014
7. Biswas, S.K., & Mantovani, A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11, 889-896 (2010
8. Adams, D.O., & Hamilton, T.A. The cell biology of macrophage activation. Annu. Rev. Immunol. 2, 283-318 (1984
9. Stein, M., Keshav, S., Harris, N., & Gordon, S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176, 287-292 (1992
10. Mills C.D., Kincaid, K., Alt, J.M., Heilman, M.J., & Hill, A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164, 6166-6173 2000
11. Mantovani A., et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677-686 (2004
12. Mosser, D.M., & Edwards, J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8, 958-969 (2008
13. 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, 7303-7311 (2006
14. Ghassabeh G.H., et al. Identification of a common gene signature for type II cytokine-Associated myeloid cells elicited in vivo in different pathologic conditions. Blood 108, 575-583 (2006
15. Odegaard J.I., et al. Macrophage-specific PPAR? controls alternative activation and improves insulin resistance. Nature 447, 1116-1120 (2007
16. Helm O., et al. Tumor-Associated macrophages exhibit pro-And anti-inflammatory properties by which they impact on pancreatic tumorigenesis. Int. J. Cancer 135, 843-861 (2014
17. Kratochvill F., et al. TNF Counterbalances the Emergence of M2 Tumor Macrophages. Cell Reports 12, 1902-1914 (2015
18. Stables M.J., et al. Transcriptomic analyses of murine resolution-phase macrophages. Blood 118, e192-e208 (2011
19. Egawa M., et al. Inflammatory monocytes recruited to allergic skin acquire an anti-inflammatory M2 phenotype via basophil-derived interleukin-4. Immunity 38, 570-580 (2013
20. Arnold L., et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204, 1057-1069 (2007
21. Nahrendorf, M., & Swirski, F.K. Monocyte and macrophage heterogeneity in the heart. Circ. Res. 112, 1624-1633 (2013
22. Schroder K., et al. Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages. Proc. Natl. Acad. Sci. USA 109, E944-E953 (2012
23. Martinez F.O., et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 121, e57-e69 (2013
24. Shay T., et al. Conservation and divergence in the transcriptional programs of the human and mouse immune systems. Proc. Natl. Acad. Sci. USA 110, 2946-2951 (2013
25. Murray P.J., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41, 14-20 (2014
26. Bain C.C., et al. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15, 929-937 (2014
27. Tamoutounour S., et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39, 925-938 (2013
28. Epelman S., et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40, 91-104 (2014
29. Gomez Perdiguero E., et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547-551 (2015
30. Hoeffel, G., et al C-Myb+ erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42 665-678 2015
31. Sheng, J., Ruedl, C., & Karjalainen, K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 43, 382-393 (2015
32. Hoeffel, G., & Ginhoux, F. Ontogeny of tissue-resident macrophages. Front. Immunol. 6, 486 (2015
33. Ginhoux F., et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330, 841-845 (2010
34. Squarzoni P., et al. Microglia modulate wiring of the embryonic forebrain. Cell Reports 8, 1271-1279 (2014
35. Schneider C., et al. Induction of the nuclear receptor PPAR-? by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 15, 1026-1037 (2014
36. Guilliams M., et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210, 1977-1992 (2013
37. Hoeffel G., Squarzoni, P., Garel, S., & Ginhoux, F. Microglial ontogeny and functions in shaping brain circuits. in Macrophages: Biology and Role in the Pathology of Diseases (eds. Biswas, S.K., & Mantovani, A.) 183-215 2014
38. Guilliams, M., et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat. Rev. Immunol. 14, 571-578 (2014
39. Blériot C., et al. Liver-resident macrophage necroptosis orchestrates type 1 microbicidal inflammation and type-2-mediated tissue repair during bacterial infection. Immunity 42, 145-158 (2015
40. Yamasaki R., et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J. Exp. Med. 211, 1533-1549 (2014
41. Suzuki T., et al. Pulmonary macrophage transplantation therapy. Nature 514, 450-454 (2014
42. Gibbings S.L., et al. Transcriptome analysis highlights the conserved difference between embryonic and postnatal-derived alveolar macrophages. Blood 126, 1357-1366 (2015
43. Jaitin D.A., et al. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 343, 776-779 (2014
44. Shalek A.K., et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 510, 363-369 (2014
45. Schiwon M., et al. Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156, 456-468 (2014
46. Dal-Secco D., et al. A dynamic spectrum of monocytes arising from the in situ reprogramming of CCR2+ monocytes at a site of sterile injury. J. Exp. Med. 212, 447-456 (2015
47. Gosselin D., et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159, 1327-1340 (2014
48. Ostuni R., et al. Latent enhancers activated by stimulation in differentiated cells. Cell 152, 157-171 (2013
49. Ghisletti S., et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity 32, 317-328 (2010
50. Okabe, Y., & Medzhitov, R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157, 832-844 (2014
51. A-Gonzalez N., et al. The nuclear receptor LXRα controls the functional specialization of splenic macrophages. Nat. Immunol. 14, 831-839 (2013
52. Joseph S.B., et al. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119, 299-309 (2004
53. Haldar M., et al. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156, 1223-1234 (2014
54. Kohyama M., et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457, 318-321 (2009
55. Speliotes E.K., et al. Myocyte-specific enhancer binding factor 2C expression in gerbil brain following global cerebral ischemia. Neuroscience 70, 67-77 (1996
56. Lawrence, T., & Natoli, G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 11, 750-761 (2011
57. Gosselin, D., & Glass, C.K. Epigenomics of macrophages. Immunol. Rev. 262, 96-112 (2014
58. Smale, S.T., Tarakhovsky, A., & Natoli, G. Chromatin contributions to the regulation of innate immunity. Annu. Rev. Immunol. 32, 489-511 (2014
59. Li Z., et al. The long noncoding RNA THRIL regulates TNFα expression through its interaction with hnRNPL. Proc. Natl. Acad. Sci. USA 111, 1002-1007 (2014
60. Li T., et al. MicroRNAs modulate the noncanonical transcription factor NF-?B pathway by regulating expression of the kinase IKKα during macrophage differentiation. Nat. Immunol. 11, 799-805 (2010
61. OConnell, R.M., Taganov, K.D., Boldin, M.P., Cheng, G., & Baltimore, D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104, 1604-1609 (2007
62. Rabani M., et al. High-resolution sequencing and modeling identifies distinct dynamic RNA regulatory strategies. Cell 159, 1698-1710 (2014
63. Kratochvill F., et al. Tristetraprolin limits inflammatory cytokine production in tumor-Associated macrophages in an mRNA decay-independent manner. Cancer Res. 75, 3054-3064 (2015
64. Bekkering, S., Joosten, L.A., van der Meer, J.W., Netea, M.G., & Riksen, N.P. Trained innate immunity and atherosclerosis. Curr. Opin. Lipidol. 24, 487-492 (2013
65. Morris, M.C., Gilliam, E.A., & Li, L. Innate immune programing by endotoxin and its pathological consequences. Front. Immunol. 5, 680 (2014
66. Netea, M.G., & van Crevel, R. BCG-induced protection: effects on innate immune memory. Semin. Immunol. 26, 512-517 (2014
67. Cheng S.C., et al. mTOR-And HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345, 1250684 (2014
68. Saeed S., et al. Epigenetic programming of monocyte-To-macrophage differentiation and trained innate immunity. Science 345, 1251086 (2014
69. Holt, P.G. Alveolar macrophages. III. Studies on the mechanisms of inhibition of T-cell proliferation. Immunology 37, 437-445 (1979
70. Bai B., et al. Microglia and microglia-like cell differentiated from DC inhibit CD4 T cell proliferation. PLoS One 4, e7869 (2009
71. Hadis U., et al. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 34, 237-246 (2011
72. Bilyk, N., & Holt, P.G. Cytokine modulation of the immunosuppressive phenotype of pulmonary alveolar macrophage populations. Immunology 86, 231-237 (1995
73. Bilyk, N., & Holt, P.G. Inhibition of the immunosuppressive activity of resident pulmonary alveolar macrophages by granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 177, 1773-1777 (1993
74. Lambert C., et al. Dendritic cell differentiation signals induce anti-inflammatory properties in human adult microglia. J. Immunol. 181, 8288-8297 (2008
75. Kayama H., et al. Intestinal CX3C chemokine receptor 1(high) (CX3CR1(high)) myeloid cells prevent T-cell-dependent colitis. Proc. Natl. Acad. Sci. USA 109, 5010-5015 (2012
76. Ueda Y., et al. Commensal microbiota induce LPS hyporesponsiveness in colonic macrophages via the production of IL-10. Int. Immunol. 22, 953-962 (2010
77. Thornley T.B., et al. Fragile TIM-4-expressing tissue resident macrophages are migratory and immunoregulatory. J. Clin. Invest. 124, 3443-3454 (2014
78. Li L., et al. The chemokine receptors CCR2 and CX3CR1 mediate monocyte/macrophage trafficking in kidney ischemia-reperfusion injury. Kidney Int. 74, 1526-1537 (2008
79. Soudja, S.M., Ruiz, A.L., Marie, J.C., & Lauvau, G. Inflammatory monocytes activate memory CD8+ T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 37, 549-562 (2012
80. Netea, M.G., Quintin, J., & van der Meer, J.W. Trained immunity: a memory for innate host defense. Cell Host Microbe 9, 355-361 (2011
81. Conde P., et al. DC-SIGN+ macrophages control the induction of transplantation tolerance. Immunity 42, 1143-1158 (2015
82. Qian B.Z., et al. CCL2 recruits inflammatory monocytes to facilitate breast-Tumour metastasis. Nature 475, 222-225 (2011
83. Pyonteck S.M., et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med. 19, 1264-1272 (2013
84. Leuschner F., et al. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29, 1005-1010 (2011
85. Butovsky O., et al. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J. Clin. Invest. 122, 3063-3087 (2012
86. Parsa R., et al. Adoptive transfer of immunomodulatory M2 macrophages prevents type 1 diabetes in NOD mice. Diabetes 61, 2881-2892 (2012
87. Riquelme P., et al. IFN-?-induced iNOS expression in mouse regulatory macrophages prolongs allograft survival in fully immunocompetent recipients. Mol. Ther. 21, 409-422 (2013
88. Mia, S., Warnecke, A., Zhang, X.M., Malmström, V., & Harris, R.A. An optimized protocol for human M2 macrophages using M-CSF and IL-4/IL-10/TGF-β yields a dominant immunosuppressive phenotype. Scand. J. Immunol. 79, 305-314 (2014
89. Schebesch C., et al. Alternatively activated macrophages actively inhibit proliferation of peripheral blood lymphocytes and CD4+ T cells in vitro. Immunology 92, 478-486 (1997
90. Hutchinson J.A., et al. Cutting edge: immunological consequences and trafficking of human regulatory macrophages administered to renal transplant recipients. J. Immunol. 187, 2072-2078 (2011
91. Yona S., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79-91 (2013
92. Klein A.M., et al. Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells. Cell 161, 1187-1201 (2015
93. Lara-Astiaso D., et al. Immunogenetics. Chromatin state dynamics during blood formation. Science 345, 943-949 (2014
94. Buenrostro J.D., et al. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523, 486-490 (2015
95. Becher B., et al. High-dimensional analysis of the murine myeloid cell system. Nat. Immunol. 15, 1181-1189 (2014
96. Bendall S.C., et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332, 687-696 (2011