The Mononuclear Phagocyte System: The Relationship between Monocytes and Macrophages

van Furth, 1972, The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells, Bull. World Health Organ., 46, 845 van Furth, 1968, The origin and kinetics of mononuclear phagocytes, J. Exp. Med., 128, 415, 10.1084/jem.128.3.415 Rojo, 2017, Transcriptional mechanisms that control expression of the macrophage colony-stimulating factor receptor locus, Clin. Sci. (Lond.), 131, 2161, 10.1042/CS20170238 Baratin, 2017, T cell zone resident macrophages silently dispose of apoptotic cells in the lymph node, Immunity, 47, 10.1016/j.immuni.2017.07.019 Guilliams, 2014, Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny, Nat. Rev. Immunol., 14, 571, 10.1038/nri3712 Jenkins, 2014, Homeostasis in the mononuclear phagocyte system, Trends Immunol., 35, 358, 10.1016/j.it.2014.06.006 Hoeffel, 2018, Fetal monocytes and the origins of tissue-resident macrophages, Cell. Immunol., 330, 5, 10.1016/j.cellimm.2018.01.001 Stremmel, 2018, Yolk sac macrophage progenitors traffic to the embryo during defined stages of development, Nat. Commun., 9 Balic, 2014, Visualisation of chicken macrophages using transgenic reporter genes: insights into the development of the avian macrophage lineage, Development, 141, 3255, 10.1242/dev.105593 Gomez Perdiguero, 2015, Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors, Nature, 518, 547, 10.1038/nature13989 Garceau, 2015, The development and maintenance of the mononuclear phagocyte system of the chick is controlled by signals from the macrophage colony-stimulating factor receptor, BMC Biol., 13, 12, 10.1186/s12915-015-0121-9 Schulz, 2012, A lineage of myeloid cells independent of Myb and hematopoietic stem cells, Science, 336, 86, 10.1126/science.1219179 Hoeffel, 2015, C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages, Immunity, 42, 665, 10.1016/j.immuni.2015.03.011 Epelman, 2014, Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation, Immunity, 40, 91, 10.1016/j.immuni.2013.11.019 Hettinger, 2013, Origin of monocytes and macrophages in a committed progenitor, Nat. Immunol., 14, 821, 10.1038/ni.2638 Mildner, 2016, Murine monocytes: origins, subsets, fates, and functions, Microbiol. Spectr., 4, 10.1128/microbiolspec.MCHD-0033-2016 Yona, 2013, Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis, Immunity, 38, 79, 10.1016/j.immuni.2012.12.001 Patel, 2017, The fate and lifespan of human monocyte subsets in steady state and systemic inflammation, J. Exp. Med., 214, 1913, 10.1084/jem.20170355 Mildner, 2017, Genomic characterization of murine monocytes reveals C/EBPbeta transcription factor dependence of Ly6C(–) cells, Immunity, 46, 10.1016/j.immuni.2017.04.018 Schmidl, 2014, Transcription and enhancer profiling in human monocyte subsets, Blood, 123, e90, 10.1182/blood-2013-02-484188 Thomas, 2016, Deleting an Nr4a1 super-enhancer subdomain ablates Ly6C(low) monocytes while preserving macrophage gene function, Immunity, 45, 975, 10.1016/j.immuni.2016.10.011 Briseno, 2016, Distinct transcriptional programs control cross-priming in classical and monocyte-derived dendritic cells, Cell Rep., 15, 2462, 10.1016/j.celrep.2016.05.025 Summers, 2017, Identification of the macrophage-specific promoter signature in FANTOM5 mouse embryo developmental time course data, J. Leukoc. Biol., 102, 1081, 10.1189/jlb.1A0417-150RR Menezes, 2016, The heterogeneity of Ly6C(hi) monocytes controls their differentiation into iNOS(+) macrophages or monocyte-derived dendritic cells, Immunity, 45, 1205, 10.1016/j.immuni.2016.12.001 Yanez, 2017, Granulocyte-monocyte progenitors and monocyte-dendritic cell progenitors independently produce functionally distinct monocytes, Immunity, 47, 10.1016/j.immuni.2017.10.021 Biermann, 1999, Murine leukocytes with ring-shaped nuclei include granulocytes, monocytes, and their precursors, J. Leukoc. Biol., 65, 217, 10.1002/jlb.65.2.217 Mass, 2016, Specification of tissue-resident macrophages during organogenesis, Science, 353, 10.1126/science.aaf4238 Scott, 2018, The transcription factor ZEB2 is required to maintain the tissue-specific identities of macrophages, Immunity, 49, 10.1016/j.immuni.2018.07.004 Gordon, 2017, Tissue macrophages: heterogeneity and functions, BMC Biol., 15, 53, 10.1186/s12915-017-0392-4 Bain, 2014, Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice, Nat. Immunol., 15, 929, 10.1038/ni.2967 Bain, 2016, Long-lived self-renewing bone marrow-derived macrophages displace embryo-derived cells to inhabit adult serous cavities, Nat. Commun., 7, 10.1038/ncomms11852 Matcovitch-Natan, 2016, Microglia development follows a stepwise program to regulate brain homeostasis, Science, 353, 10.1126/science.aad8670 Guilliams, 2017, Does niche competition determine the origin of tissue-resident macrophages?, Nat. Rev. Immunol., 17, 451, 10.1038/nri.2017.42 Mowat, 2017, Barrier-tissue macrophages: functional adaptation to environmental challenges, Nat. Med., 23, 1258, 10.1038/nm.4430 Schridde, 2017, Tissue-specific differentiation of colonic macrophages requires TGFbeta receptor-mediated signaling, Mucosal Immunol., 10, 1387, 10.1038/mi.2016.142 Asano, 2015, Intestinal CD169(+) macrophages initiate mucosal inflammation by secreting CCL8 that recruits inflammatory monocytes, Nat. Commun., 6, 7802, 10.1038/ncomms8802 Sehgal, 2018, The role of CSF1R-dependent macrophages in control of the intestinal stem-cell niche, Nat. Commun., 9, 10.1038/s41467-018-03638-6 Shaw, 2018, Tissue-resident macrophages in the intestine are long lived and defined by Tim-4 and CD4 expression, J. Exp. Med., 215, 1507, 10.1084/jem.20180019 Bonnardel, 2015, Innate and adaptive immune functions of peyer’s patch monocyte-derived cells, Cell Rep., 11, 770, 10.1016/j.celrep.2015.03.067 De Schepper, 2018, Self-maintaining gut macrophages are essential for intestinal homeostasis, Cell, 175, 400, 10.1016/j.cell.2018.07.048 Sierro, 2017, A liver capsular network of monocyte-derived macrophages restricts hepatic dissemination of intraperitoneal bacteria by neutrophil recruitment, Immunity, 47, 10.1016/j.immuni.2017.07.018 Beattie, 2016, Bone marrow-derived and resident liver macrophages display unique transcriptomic signatures but similar biological functions, J. Hepatol., 65, 758, 10.1016/j.jhep.2016.05.037 David, 2016, Combination of mass cytometry and imaging analysis reveals origin, location, and functional repopulation of liver myeloid cells in mice, Gastroenterology, 151, 1176, 10.1053/j.gastro.2016.08.024 Scott, 2016, Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells, Nat. Commun., 7, 10.1038/ncomms10321 Cohen, 2018, Lung single-cell signaling interaction map reveals basophil role in macrophage imprinting, Cell, 175, 10.1016/j.cell.2018.09.009 Garbi, 2017, Location, function, and ontogeny of pulmonary macrophages during the steady state, Pflugers Arch., 469, 561, 10.1007/s00424-017-1965-3 Gibbings, 2017, Three unique interstitial macrophages in the murine lung at steady state, Am. J. Respir. Cell Mol. Biol., 57, 66, 10.1165/rcmb.2016-0361OC Tan, 2016, Developmental origin of lung macrophage diversity, Development, 143, 1318, 10.1242/dev.129122 van de Laar, 2016, Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages, Immunity, 44, 755, 10.1016/j.immuni.2016.02.017 Askew, 2017, Coupled proliferation and apoptosis maintain the rapid turnover of microglia in the adult brain, Cell Rep., 18, 391, 10.1016/j.celrep.2016.12.041 Perry, 1985, Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain, Neuroscience, 15, 313, 10.1016/0306-4522(85)90215-5 Goldmann, 2016, Origin, fate and dynamics of macrophages at central nervous system interfaces, Nat. Immunol., 17, 797, 10.1038/ni.3423 Mildner, 2007, Microglia in the adult brain arise from Ly-6ChiCCR2+ monocytes only under defined host conditions, Nat. Neurosci., 10, 1544, 10.1038/nn2015 Beers, 2006, Wild-type microglia extend survival in PU.1 knockout mice with familial amyotrophic lateral sclerosis, Proc. Natl. Acad. Sci. U. S. A., 103, 16021, 10.1073/pnas.0607423103 Bennett, 2018, A combination of ontogeny and CNS environment establishes microglial identity, Neuron, 98, 10.1016/j.neuron.2018.05.014 Cronk, 2018, Peripherally derived macrophages can engraft the brain independent of irradiation and maintain an identity distinct from microglia, J. Exp. Med., 215, 1627, 10.1084/jem.20180247 Molawi, 2014, Progressive replacement of embryo-derived cardiac macrophages with age, J. Exp. Med., 211, 2151, 10.1084/jem.20140639 Chitu, 2017, Regulation of embryonic and postnatal development by the CSF-1 receptor, Curr. Top. Dev. Biol., 123, 229, 10.1016/bs.ctdb.2016.10.004 Lichanska, 1999, Differentiation of the mononuclear phagocyte system during mouse embryogenesis: the role of transcription factor PU.1, Blood, 94, 127, 10.1182/blood.V94.1.127.413k07_127_138 MacDonald, 2010, An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue- and tumor-associated macrophages but does not inhibit inflammation, Blood, 116, 3955, 10.1182/blood-2010-02-266296 Gow, 2014, Characterisation of a novel Fc conjugate of macrophage colony-stimulating factor, Mol. Ther., 22, 1580, 10.1038/mt.2014.112 Hawley, 2018, Csf1r-mApple transgene expression and ligand binding in vivo reveal dynamics of CSF1R expression within the mononuclear phagocyte system, J. Immunol., 200, 2209, 10.4049/jimmunol.1701488 Jenkins, 2013, IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1, J. Exp. Med., 210, 2477, 10.1084/jem.20121999 Stutchfield, 2015, CSF1 restores innate immunity after liver injury in mice and serum levels indicate outcomes of patients with acute liver failure, Gastroenterology, 149, 10.1053/j.gastro.2015.08.053 Perie, 2015, Toward defining a ‘lineage’–the case for dendritic cells, Semin. Cell Dev. Biol., 41, 3, 10.1016/j.semcdb.2015.02.004 Durai, 2018, Altered compensatory cytokine signaling underlies the discrepancy between Flt3(–/–) and Flt3l(–/–) mice, J. Exp. Med., 215, 1417, 10.1084/jem.20171784 Nandi, 2006, Developmental and functional significance of the CSF-1 proteoglycan chondroitin sulfate chain, Blood, 107, 786, 10.1182/blood-2005-05-1822 Langlais, 2016, The macrophage IRF8/IRF1 regulome is required for protection against infections and is associated with chronic inflammation, J. Exp. Med., 213, 585, 10.1084/jem.20151764 Lavine, 2014, Distinct macrophage lineages contribute to disparate patterns of cardiac recovery and remodeling in the neonatal and adult heart, Proc. Natl. Acad. Sci. U. S. A., 111, 16029, 10.1073/pnas.1406508111 Sasmono, 2003, A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse, Blood, 101, 1155, 10.1182/blood-2002-02-0569 Sauter, 2014, The MacBlue binary transgene (csf1r-gal4VP16/UAS-ECFP) provides a novel marker for visualisation of subsets of monocytes, macrophages and dendritic cells and responsiveness to CSF1 administration, PLoS One, 9, 10.1371/journal.pone.0105429 Rojo, R. et al. Germ-line deletion of a conserved macrophage-specific enhancer within the mouse Csf1r locus has a selective impact on tissue macrophage populations including microglia. Nat. Immunol. (in press) Thion, 2018, Microbiome influences prenatal and adult microglia in a sex-specific manner, Cell, 172, 10.1016/j.cell.2017.11.042 Stamatiades, 2016, Immune monitoring of trans-endothelial transport by kidney-resident macrophages, Cell, 166, 991, 10.1016/j.cell.2016.06.058 Avetisyan, 2018, Muscularis macrophage development in the absence of an enteric nervous system, Proc. Natl. Acad. Sci. U. S. A., 115, 4696, 10.1073/pnas.1802490115 Nimmerjahn, 2005, Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo, Science, 308, 1314, 10.1126/science.1110647 Poche, 2015, Macrophages engulf endothelial cell membrane particles preceding pupillary membrane capillary regression, Dev. Biol., 403, 30, 10.1016/j.ydbio.2015.03.017 Wood, 2017, Macrophage functions in tissue patterning and disease: new insights from the fly, Dev. Cell, 40, 221, 10.1016/j.devcel.2017.01.001 Pridans, 2018, Targetted disruption of the rat Csf1r locus generates viable adult animals with selective macrophage and microglial deficiencies, J. Immunol., 201, 2683, 10.4049/jimmunol.1701783 Hodgkin, 2018, Modifying clonal selection theory with a probabilistic cell, Immunol. Rev., 285, 249, 10.1111/imr.12695 Hagai, 2018, Gene expression variability across cells and species shapes innate immunity, Nature, 563, 197, 10.1038/s41586-018-0657-2 Schroder, 2012, Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages, Proc. Natl. Acad. Sci. U. S. A., 109, E944, 10.1073/pnas.1110156109 Jubb, 2016, Enhancer turnover is associated with a divergent transcriptional response to glucocorticoid in mouse and human macrophages, J. Immunol., 196, 813, 10.4049/jimmunol.1502009 Pridans, 2018, Macrophage colony-stimulating factor increases hepatic macrophage content, liver growth, and lipid accumulation in neonatal rats, Am. J. Physiol. Gastrointest. Liver Physiol., 314, G388, 10.1152/ajpgi.00343.2017 Kapetanovic, 2013, The impact of breed and tissue compartment on the response of pig macrophages to lipopolysaccharide, BMC Genomics, 14, 581, 10.1186/1471-2164-14-581 Sauter, 2016, Macrophage colony-stimulating factor (CSF1) controls monocyte production and maturation and the steady-state size of the liver in pigs, Am. J. Physiol. Gastrointest. Liver Physiol., 311, G533, 10.1152/ajpgi.00116.2016 Pridans, 2016, A Csf1r-EGFP transgene provides a novel marker for monocyte subsets in sheep, J. Immunol., 197, 2297, 10.4049/jimmunol.1502336 Lavin, 2014, Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment, Cell, 159, 1312, 10.1016/j.cell.2014.11.018 Baranska, 2018, Unveiling skin macrophage dynamics explains both tattoo persistence and strenuous removal, J. Exp. Med., 215, 1115, 10.1084/jem.20171608 Pirzgalska, 2017, Sympathetic neuron-associated macrophages contribute to obesity by importing and metabolizing norepinephrine, Nat. Med., 23, 1309, 10.1038/nm.4422 Ensan, 2016, Self-renewing resident arterial macrophages arise from embryonic CX3CR1(+) precursors and circulating monocytes immediately after birth, Nat. Immunol., 17, 159, 10.1038/ni.3343 Lim, 2018, Hyaluronan receptor LYVE-1-expressing macrophages maintain arterial tone through hyaluronan-mediated regulation of smooth muscle cell collagen, Immunity, 49, 10.1016/j.immuni.2018.12.009 Calderon, 2015, The pancreas anatomy conditions the origin and properties of resident macrophages, J. Exp. Med., 212, 1497, 10.1084/jem.20150496 Mussar, 2017, A CCR2+ myeloid cell niche required for pancreatic beta cell growth, JCI Insight, 2, 93834, 10.1172/jci.insight.93834 Mossadegh-Keller, 2017, Developmental origin and maintenance of distinct testicular macrophage populations, J. Exp. Med., 214, 2829, 10.1084/jem.20170829 Kaur, 2018, Self-repopulating recipient bone marrow resident macrophages promote long-term hematopoietic stem cell engraftment, Blood, 132, 735, 10.1182/blood-2018-01-829663 Batoon, 2017, CD169(+) macrophages are critical for osteoblast maintenance and promote intramembranous and endochondral ossification during bone repair, Biomaterials, 10.1016/j.biomaterials.2017.10.033 Gabanyi, 2016, Neuro-immune interactions drive tissue programming in intestinal macrophages, Cell, 164, 378, 10.1016/j.cell.2015.12.023 Berry, 2017, Renal sodium gradient orchestrates a dynamic antibacterial defense zone, Cell, 170, 10.1016/j.cell.2017.07.022 Wolf, 2017, Brown-adipose-tissue macrophages control tissue innervation and homeostatic energy expenditure, Nat. Immunol., 18, 665, 10.1038/ni.3746 Kim, 2016, MHC II+ resident peritoneal and pleural macrophages rely on IRF4 for development from circulating monocytes, J. Exp. Med., 213, 1951, 10.1084/jem.20160486 Lever, 2018, Parabiosis reveals leukocyte dynamics in the kidney, Lab. Invest., 98, 391, 10.1038/labinvest.2017.130 Munro, 2017, The origins and functions of tissue-resident macrophages in kidney development, Front. Physiol., 8, 837, 10.3389/fphys.2017.00837 Tacke, 2015, The transcription factor NR4A1 is essential for the development of a novel macrophage subset in the thymus, Sci. Rep., 5, 10.1038/srep10055 Donaldson, 2015, Reciprocal regulation of lymphoid tissue development in the large intestine by IL-25 and IL-23, Mucosal Immunol., 8, 582, 10.1038/mi.2014.90 Epelman, 2014, Origin and functions of tissue macrophages, Immunity, 41, 21, 10.1016/j.immuni.2014.06.013 Jung, 2018, Macrophages and monocytes in 2017: macrophages and monocytes: of tortoises and hares, Nat. Rev. Immunol., 18, 85, 10.1038/nri.2017.158 Perdiguero, 2016, The development and maintenance of resident macrophages, Nat. Immunol., 17, 2, 10.1038/ni.3341 Varol, 2015, Macrophages: development and tissue specialization, Annu. Rev. Immunol., 33, 643, 10.1146/annurev-immunol-032414-112220 Rojo, 2018, Maternal tamoxifen treatment expands the macrophage population of early mouse embryos, bioRxiv Pepe, 2017, Self-renewal and phenotypic conversion are the main physiological responses of macrophages to the endogenous estrogen surge, Sci. Rep., 7, 44270, 10.1038/srep44270 Gaskill, 2017, Stressed out: providing laboratory animals with behavioral control to reduce the physiological effects of stress, Lab. Anim. (N. Y.), 46, 142, 10.1038/laban.1218 Williams, 2017, Thermoneutrality but not UCP1 deficiency suppresses monocyte mobilization into blood, Circ. Res., 121, 662, 10.1161/CIRCRESAHA.117.311519 Crofton, 1978, The origin, kinetics, and characteristics of the Kupffer cells in the normal steady state, J. Exp. Med., 148, 1, 10.1084/jem.148.1.1 Petkova, 2008, Genetic influence on immune phenotype revealed strain-specific variations in peripheral blood lineages, Physiol. Genomics, 34, 304, 10.1152/physiolgenomics.00185.2007 Sauter, 2014, Pleiotropic effects of extended blockade of CSF1R signaling in adult mice, J. Leukoc. Biol., 96, 265, 10.1189/jlb.2A0114-006R Raza, 2014, Analysis of the transcriptional networks underpinning the activation of murine macrophages by inflammatory mediators, J. Leukoc. Biol., 96, 167, 10.1189/jlb.6HI0313-169R Campbell, 2018, Myeloid cell recruitment versus local proliferation differentiates susceptibility from resistance to filarial infection, eLife, 7, 10.7554/eLife.30947