The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis (original) (raw)
Ueno, M. & Yamashita, T. Bidirectional tuning of microglia in the developing brain: from neurogenesis to neural circuit formation. Curr. Opin. Neurobiol.27, 8–15 (2014). CASPubMed Google Scholar
Fulde, M. & Hornef, M.W. Maturation of the enteric mucosal innate immune system during the postnatal period. Immunol. Rev.260, 21–34 (2014). CASPubMed Google Scholar
Wynn, T.A., Chawla, A. & Pollard, J.W. Macrophage biology in development, homeostasis and disease. Nature496, 445–455 (2013). CASPubMedPubMed Central Google Scholar
Gordon, S., Plüddemann, A. & Martinez Estrada, F. Macrophage heterogeneity in tissues: phenotypic diversity and functions. Immunol. Rev.262, 36–55 (2014). CASPubMedPubMed Central Google Scholar
Sieweke, M.H. & Allen, J.E. Beyond stem cells: self-renewal of differentiated macrophages. Science342, 1242974–1242974 (2013). PubMed Google Scholar
Mucenski, M.L. et al. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell65, 677–689 (1991). CASPubMed Google Scholar
Perdiguero, E.G. et al. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature518, 547–551 (2015). CAS Google Scholar
Schulz, C. et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science336, 86–90 (2012). CASPubMed Google Scholar
Hoeffel, G. et al. C-Myb+ erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity42, 665–678 (2015). CASPubMedPubMed Central Google Scholar
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). CASPubMedPubMed Central Google Scholar
Molawi, K. et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med.211, 2151–2158 (2014). CASPubMedPubMed Central Google Scholar
Varol, C. et al. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med.204, 171–180 (2007). CASPubMedPubMed Central Google Scholar
Hashimoto, D., Miller, J. & Merad, M. Dendritic cell and macrophage heterogeneity in vivo. Immunity35, 323–335 (2011). CASPubMedPubMed Central Google Scholar
Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity38, 79–91 (2013). CASPubMed Google Scholar
Ginhoux, F. et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science330, 841–845 (2010). CASPubMedPubMed Central Google Scholar
Kierdorf, K. et al. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci.16, 273–280 (2013). CASPubMed Google Scholar
Bruttger, J. et al. Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity43, 92–106 (2015). CASPubMed Google Scholar
Hashimoto, D. et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity38, 792–804 (2013). CASPubMed Google Scholar
Malissen, B., Tamoutounour, S. & Henri, S. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol.14, 417–428 (2014). CASPubMed Google Scholar
Zigmond, E. & Jung, S. Intestinal macrophages: well educated exceptions from the rule. Trends Immunol.34, 162–168 (2013). CASPubMed Google Scholar
Gosselin, D. et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell159, 1327–1340 (2014). CASPubMedPubMed Central Google Scholar
Lavin, Y. et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell159, 1312–1326 (2014). CASPubMedPubMed Central Google Scholar
Gordon, S. The macrophage: past, present and future. Eur. J. Immunol.37, S9–S17 (2007). CASPubMed Google Scholar
Chow, A. et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J. Exp. Med.208, 261–271 (2011). CASPubMedPubMed Central Google Scholar
Muller, P.A. et al. Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell158, 300–313 (2014). CASPubMedPubMed Central Google Scholar
Niess, J.H. et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science307, 254–258 (2005). CASPubMed Google Scholar
Parkhurst, C.N. et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell155, 1596–1609 (2013). CASPubMedPubMed Central Google Scholar
Berg vom, J. et al. Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease–like pathology and cognitive decline. Nat. Med.18, 1812–1819 (2012). Google Scholar
Yamasaki, R. et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J. Exp. Med.211, 1533–1549 (2014). CASPubMedPubMed Central Google Scholar
Chiu, I.M. et al. A neurodegeneration-specific gene-expression signature of acutely isolated microglia from an amyotrophic lateral sclerosis mouse model. Cell Rep.4, 385–401 (2013). CASPubMedPubMed Central Google Scholar
Jung, S. et al. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol.20, 4106–4114 (2000). CASPubMedPubMed Central Google Scholar
Davalos, D. et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci.8, 752–758 (2005). CASPubMed Google Scholar
Nimmerjahn, A., Kirchhoff, F. & Helmchen, F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science308, 1314–1318 (2005). CASPubMed Google Scholar
Tremblay, M.-È., Lowery, R.L. & Majewska, A.K. Microglial interactions with synapses are modulated by visual experience. PLoS Biol.8, e1000527 (2010). PubMedPubMed Central Google Scholar
Schafer, D.P. et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron74, 691–705 (2012). CASPubMedPubMed Central Google Scholar
Paolicelli, R.C. et al. Synaptic pruning by microglia is necessary for normal brain development. Science333, 1456–1458 (2011). CASPubMed Google Scholar
Squarzoni, P. et al. Microglia modulate wiring of the embryonic forebrain. Cell Rep.8, 1271–1279 (2014). CASPubMed Google Scholar
Prinz, M. & Priller, J. Microglia and brain macrophagesin the molecular age: from origin toneuropsychiatric disease. Nat. Rev. Neurosci.5, 300–312 (2014). Google Scholar
Rademakers, R. et al. Mutations in the colony stimulating factor 1 receptor (CSF1R) gene cause hereditary diffuse leukoencephalopathy with spheroids. Nat. Genet.44, 200–205 (2012). CAS Google Scholar
Poliani, P.L. et al. TREM2 sustains microglial expansion during aging and response to demyelination. J. Clin. Invest.125, 2161–2170 (2015). PubMedPubMed Central Google Scholar
Guerreiro, R. & Hardy, J. TREM2 and neurodegenerative disease. N. Engl. J. Med.369, 1569–1570 (2013). CASPubMed Google Scholar
Goldmann, T. et al. A new type of microglia gene targeting shows TAK1 to be pivotal in CNS autoimmune inflammation. Nat. Neurosci.16, 1618–1626 (2013). CASPubMed Google Scholar
Varol, C. et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity31, 502–512 (2009). CASPubMed Google Scholar
Ginhoux, F. & Jung, S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol.14, 392–404 (2014). CASPubMed Google Scholar
Rivollier, A., He, J., Kole, A., Valatas, V. & Kelsall, B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med.209, 139–155 (2012). CASPubMedPubMed Central Google Scholar
Weber, B., Saurer, L., Schenk, M., Dickgreber, N. & Mueller, C. CX3CR1 defines functionally distinct intestinal mononuclear phagocyte subsets which maintain their respective functions during homeostatic and inflammatory conditions. Eur. J. Immunol.41, 773–779 (2011). CASPubMed Google Scholar
Zigmond, E. et al. Ly6Chi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity37, 1076–1090 (2012). CASPubMed Google Scholar
Rubtsov, Y.P. et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity28, 546–558 (2008). CASPubMed Google Scholar
Shouval, D.S. et al. Interleukin-10 receptor signaling in innate immune cells regulates mucosal immune tolerance and anti-inflammatory macrophage function. Immunity40, 706–719 (2014). CASPubMedPubMed Central Google Scholar
Zigmond, E. et al. Macrophage-restricted interleukin-10 receptor deficiency, but not il-10 deficiency, causes severe spontaneous colitis. Immunity40, 720–733 (2014). CASPubMed Google Scholar
Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. & Medzhitov, R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell118, 229–241 (2004). CASPubMed Google Scholar
Mortha, A. et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science343, 1249288–1249288 (2014). PubMedPubMed Central Google Scholar
Seno, H. et al. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc. Natl. Acad. Sci. USA106, 256–261 (2009). CASPubMed Google Scholar
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). CASPubMedPubMed Central Google Scholar
Schneider, C. et al. Alveolar macrophages are essential for protection from respiratory failure and associated morbidity following influenza virus infection. PLoS Pathog.10, e1004053 (2014). PubMedPubMed Central Google Scholar
Suzuki, T. et al. Familial pulmonary alveolar proteinosis caused by mutations in CSF2RA. J. Exp. Med.205, 2703–2710 (2008). PubMedPubMed Central Google Scholar
Nakamura, A. et al. Transcription repressor Bach2 is required for pulmonary surfactant homeostasis and alveolar macrophage function. J. Exp. Med.210, 2191–2204 (2013). CASPubMedPubMed Central Google Scholar
Happle, C. et al. Pulmonary transplantation of macrophage progenitors as effective and long-lasting therapy for hereditary pulmonary alveolar proteinosis. Sci. Transl. Med.6, 250ra113 (2014). PubMed Google Scholar
Mebius, R.E. & Kraal, G. Structure and function of the spleen. Nat. Rev. Immunol.5, 606–616 (2005). CASPubMed Google Scholar
Miyake, Y. et al. Critical role of macrophages in the marginal zone in the suppression of immune responses to apoptotic cell–associated antigens. J. Clin. Invest.117, 2268–2278 (2007). CASPubMedPubMed Central Google Scholar
A-Gonzalez, N. et al. The nuclear receptor LXRα controls the functional specialization of splenic macrophages. Nat. Immunol.14, 831–839 (2013). CASPubMedPubMed Central Google Scholar
Kohyama, M. et al. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature457, 318–321 (2009). CASPubMed Google Scholar
Glocker, E.-O. et al. Inflammatory bowel disease and mutations affecting the interleukin-10 receptor. N. Engl. J. Med.361, 2033–2045 (2009). CASPubMedPubMed Central Google Scholar
Farh, K.K.-H. et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature518, 337–343 (2015). CASPubMed Google Scholar
Gautier, E.L. et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol.13, 1118–1128 (2012). CASPubMedPubMed Central Google Scholar
Jaitin, D.A. et al. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science343, 776–779 (2014). CASPubMedPubMed Central Google Scholar
Jojic, V. et al. Identification of transcriptional regulators in the mouse immune system. Nat. Immunol.14, 633–643 (2013). CASPubMedPubMed Central Google Scholar
Miller, J.C. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat. Immunol.13, 888–899 (2012). CASPubMedPubMed Central Google Scholar
Cipolletta, D., Kolodin, D., Benoist, C. & Mathis, D. Tissular Tregs: a unique population of adipose-tissue-resident Foxp3+CD4+ T cells that impacts organismal metabolism. Semin. Immunol.23, 431–437 (2011). CASPubMed Google Scholar
Haldar, M. et al. Heme-mediated Spi-c induction promotes monocyte differentiation into iron-recycling macrophages. Cell156, 1223–1234 (2014). CASPubMedPubMed Central Google Scholar
Butovsky, O. et al. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat. Neurosci.17, 131–143 (2014). CASPubMed Google Scholar
Cohen, M. et al. Chronic exposure to TGFβ1 regulates myeloid cell inflammatory response in an IRF7-dependent manner. EMBO J.33, 2906–2921 (2014). PubMedPubMed Central Google Scholar
Davalos, D. et al. Fibrinogen-induced perivascular microglial clustering is required for the development of axonal damage in neuroinflammation. Nat. Commun.3, 1227 (2012). PubMed Google Scholar
Erny, D. et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci.18, 965–977 (2015). CASPubMedPubMed Central Google Scholar
Thorburn, A.N., Macia, L. & Mackay, C.R. Diet, metabolites, and “Western-lifestyle” inflammatory diseases. Immunity40, 833–842 (2014). CASPubMed Google Scholar
Ghosn, E.E.B. et al. Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. USA107, 2568–2573 (2010). CASPubMedPubMed Central Google Scholar
Gautier, E.L. et al. Gata6 regulates aspartoacylase expression in resident peritoneal macrophages and controls their survival. J. Exp. Med.211, 1525–1531 (2014). CASPubMedPubMed Central Google Scholar
Rosas, M. et al. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science344, 645–648 (2014). CASPubMedPubMed Central Google Scholar
Okabe, Y. & Medzhitov, R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell157, 832–844 (2014). CASPubMedPubMed Central Google Scholar
Capucha, T. et al. Distinct murine mucosal langerhans cell subsets develop from pre-dendritic cells and monocytes. Immunity43, 369–381 (2015). CASPubMed Google Scholar
Garber, M. et al. A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell47, 810–822 (2012). CASPubMed Google Scholar
Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell38, 576–589 (2010). CASPubMedPubMed Central Google Scholar
Ostuni, R. & Natoli, G. Lineages, cell types and functional states: a genomic view. Curr. Opin. Cell Biol.25, 759–764 (2013). CASPubMed Google Scholar
Winter, D.R. & Amit, I. The role of chromatin dynamics in immune cell development. Immunol. Rev.261, 9–22 (2014). CASPubMed Google Scholar
Felsenfeld, G. & Groudine, M. Controlling the double helix. Nature421, 448–453 (2003). PubMed Google Scholar
Kouzarides, T. Chromatin modifications and their function. Cell128, 693–705 (2007). CASPubMed Google Scholar
Heintzman, N.D. et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature459, 108–112 (2009). CASPubMedPubMed Central Google Scholar
Zhou, V.W., Goren, A. & Bernstein, B.E. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet.12, 7–18 (2011). PubMed Google Scholar
Lawrence, T. & Natoli, G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol.11, 750–761 (2011). CASPubMed Google Scholar
Xue, J. et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity40, 274–288 (2014). CASPubMedPubMed Central Google Scholar
Ostuni, R. et al. Latent enhancers activated by stimulation in differentiated cells. Cell152, 157–171 (2013). CASPubMed Google Scholar
Lara-Astiaso, D. et al. Immunogenetics. Chromatin state dynamics during blood formation. Science345, 943–949 (2014). CASPubMedPubMed Central Google Scholar
Schultze, J.L., Freeman, T., Hume, D.A. & Latz, E. A transcriptional perspective on human macrophage biology. Semin. Immunol.27, 44–50 (2015). CASPubMed Google Scholar
Bernstein, B.E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell125, 315–326 (2006). CASPubMed Google Scholar
Lee, T.I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell125, 301–313 (2006). CASPubMedPubMed Central Google Scholar
Nord, A.S. et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell155, 1521–1531 (2013). CASPubMedPubMed Central Google Scholar
Zhang, J.A., Mortazavi, A., Williams, B.A., Wold, B.J. & Rothenberg, E.V. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell149, 467–482 (2012). CASPubMedPubMed Central Google Scholar
Bauer, D.E. et al. An erythroid enhancer of BCL11A subject to genetic variation determines fetal hemoglobin level. Science342, 253–257 (2013). CASPubMedPubMed Central Google Scholar
Heinz, S. & Glass, C.K. Roles of lineage-determining transcription factors in establishing open chromatin: lessons from high-throughput studies. Curr. Top. Microbiol. Immunol.356, 1–15 (2012). CASPubMed Google Scholar
Bossard, P. & Zaret, K.S. GATA transcription factors as potentiators of gut endoderm differentiation. Development125, 4909–4917 (1998). CASPubMed Google Scholar
Cirillo, L.A. & Zaret, K.S. An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol. Cell4, 961–969 (1999). CASPubMed Google Scholar
Lupien, M. et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell132, 958–970 (2008). CASPubMedPubMed Central Google Scholar
Cirillo, L.A. et al. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell9, 279–289 (2002). CASPubMed Google Scholar
Bornstein, C. et al. A negative feedback loop of transcription factors specifies alternative dendritic cell chromatin states. Mol. Cell56, 749–762 (2014). CASPubMedPubMed Central Google Scholar
Graf, T. & Enver, T. Forcing cells to change lineages. Nature462, 587–594 (2009). CASPubMed Google Scholar
Feng, R. et al. PU.1 and C/EBPα/β convert fibroblasts into macrophage-like cells. Proc. Natl. Acad. Sci. USA105, 6057–6062 (2008). CASPubMedPubMed Central Google Scholar
Ghisletti, S. et al. Identification and characterization of enhancers controlling the inflammatory gene expression program in macrophages. Immunity32, 317–328 (2010). CASPubMed Google Scholar