Tissue-Resident Macrophage Ontogeny and Homeostasis

Immunity

Volumn 44, Issue 3, 2016, Pages 439-449

  Ginhoux, Florent ^a,b   Guilliams, Martin ^c,d  

^a AGENCY FOR SCIENCE   (Singapore)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; PROTEIN C MYB; TAMOXIFEN; TRANSCRIPTION FACTOR RUNX1;

ADIPOSE TISSUE; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; CELL POPULATION; CYTOLOGY; EMBRYO DEVELOPMENT; ERYTHRO MYELOID PRECURSOR CELL; ERYTHROID CELL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; KUPFFER CELL; MACROPHAGE; MONOCYTE; MONOCYTE MACROPHAGE PRECURSOR CELL; MYELOID PROGENITOR CELL; NONHUMAN; ONCOGENE C MYB; ONTOGENY; PATTERN RECOGNITION; PRIORITY JOURNAL; PROGENY; REVIEW; TISSUE METABOLISM; TISSUE SPECIFICITY; ADULT; ANIMAL; HOMEOSTASIS; IMMUNOLOGY; INFLAMMATION;

ADULT; ANIMALS; BONE MARROW; CELL DIFFERENTIATION; EMBRYONIC DEVELOPMENT; HEMATOPOIESIS; HOMEOSTASIS; HUMANS; INFLAMMATION; MACROPHAGES;

EID: 84960354901     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.02.024     Document Type: Review

References (89)

1. Ajami B., Bennett J.L., Krieger C., Tetzlaff W., Rossi F.M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 2007, 10:1538-1543.
2. Ajami B., Bennett J.L., Krieger C., McNagny K.M., Rossi F.M. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 2011, 14:1142-1149.
3. Alliot F., Lecain E., Grima B., Pessac B. Microglial progenitors with a high proliferative potential in the embryonic and adult mouse brain. Proc. Natl. Acad. Sci. USA 1991, 88:1541-1545.
4. Alliot F., Godin I., Pessac B. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res. Dev. Brain Res. 1999, 117:145-152.
5. Amano S.U., Cohen J.L., Vangala P., Tencerova M., Nicoloro S.M., Yawe J.C., Shen Y., Czech M.P., Aouadi M. Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab. 2014, 19:162-171.
6. Amit I., Winter D.R., Jung S. The role of the local environment and epigenetics in shaping macrophage identity and their effect on tissue homeostasis. Nat. Immunol. 2015, 17:18-25.
7. Bain C.C., Bravo-Blas A., Scott C.L., Gomez Perdiguero E., Geissmann F., Henri S., Malissen B., Osborne L.C., Artis D., Mowat A.M. Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 2014, 15:929-937.
8. Bertrand J.Y., Jalil A., Klaine M., Jung S., Cumano A., Godin I. Three pathways to mature macrophages in the early mouse yolk sac. Blood 2005, 106:3004-3011.
9. Bruttger J., Karram K., Wörtge S., Regen T., Marini F., Hoppmann N., Klein M., Blank T., Yona S., Wolf Y., et al. Genetic cell ablation reveals clusters of local self-renewing microglia in the mammalian central nervous system. Immunity 2015, 43:92-106.
10. Calderon B., Carrero J.A., Ferris S.T., Sojka D.K., Moore L., Epelman S., Murphy K.M., Yokoyama W.M., Randolph G.J., Unanue E.R. The pancreas anatomy conditions the origin and properties of resident macrophages. J. Exp. Med. 2015, 212:1497-1512.
11. Chen M.J., Yokomizo T., Zeigler B.M., Dzierzak E., Speck N.A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 2009, 457:887-891.
12. Clarke D., Vegiopoulos A., Crawford A., Mucenski M., Bonifer C., Frampton J. In vitro differentiation of c-myb(-/-) ES cells reveals that the colony forming capacity of unilineage macrophage precursors and myeloid progenitor commitment are c-Myb independent. Oncogene 2000, 19:3343-3351.
13. Cumano A., Godin I. Ontogeny of the hematopoietic system. Annu. Rev. Immunol. 2007, 25:745-785.
14. Ensan S., Li A., Besla R., Degousee N., Cosme J., Roufaiel M., Shikatani E.A., El-Maklizi M., Williams J.W., Robins L., et al. Self-renewing resident arterial macrophages arise from embryonic CX3CR1(+) precursors and circulating monocytes immediately after birth. Nat. Immunol. 2016, 17:159-168.
15. Epelman S., Lavine K.J., Beaudin A.E., Sojka D.K., Carrero J.A., Calderon B., Brija T., Gautier E.L., Ivanov S., Satpathy A.T., et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014, 40:91-104.
16. Fogg D.K., Sibon C., Miled C., Jung S., Aucouturier P., Littman D.R., Cumano A., Geissmann F. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
17. Frame J.M., McGrath K.E., Palis J. Erythro-myeloid progenitors: "definitive" hematopoiesis in the conceptus prior to the emergence of hematopoietic stem cells. Blood Cells Mol. Dis. 2013, 51:220-225.
18. Gautier E.L., Shay T., Miller J., Greter M., Jakubzick C., Ivanov S., Helft J., Chow A., Elpek K.G., Gordonov S., et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 2012, 13:1118-1128. Immunological Genome Consortium.
19. Gibbings S.L., Goyal R., Desch A.N., Leach S.M., Prabagar M., Atif S.M., Bratton D.L., Janssen W., Jakubzick C.V. Transcriptome analysis highlights the conserved difference between embryonic and postnatal-derived alveolar macrophages. Blood 2015, 126:1357-1366.
20. Ginhoux F., Jung S. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat. Rev. Immunol. 2014, 14:392-404.
21. Ginhoux F., Merad M. Ontogeny and homeostasis of Langerhans cells. Immunol. Cell Biol. 2010, 88:387-392.
22. Ginhoux F., Liu K., Helft J., Bogunovic M., Greter M., Hashimoto D., Price J., Yin N., Bromberg J., Lira S.A., et al. The origin and development of nonlymphoid tissue CD103+ DCs. J. Exp. Med. 2009, 206:3115-3130.
23. Ginhoux F., Greter M., Leboeuf M., Nandi S., See P., Gokhan S., Mehler M.F., Conway S.J., Ng L.G., Stanley E.R., et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010, 330:841-845.
24. Ginhoux F., Lim S., Hoeffel G., Low D., Huber T. Origin and differentiation of microglia. Front. Cell. Neurosci. 2013, 7:45.
25. Ginhoux F., Schultze J.L., Murray P.J., Ochando J., Biswas S.K. New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nat. Immunol. 2015, 17:34-40.
26. Godin I., Cumano A. The hare and the tortoise: an embryonic haematopoietic race. Nat. Rev. Immunol. 2002, 2:593-604.
27. Gomez Perdiguero E., Klapproth K., Schulz C., Busch K., Azzoni E., Crozet L., Garner H., Trouillet C., de Bruijn M.F., Geissmann F., Rodewald H.R. Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 2015, 518:547-551.
28. Gosselin D., Link V.M., Romanoski C.E., Fonseca G.J., Eichenfield D.Z., Spann N.J., Stender J.D., Chun H.B., Garner H., Geissmann F., Glass C.K. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 2014, 159:1327-1340.
29. Guilliams M., De Kleer I., Henri S., Post S., Vanhoutte L., De Prijck S., Deswarte K., Malissen B., Hammad H., Lambrecht B.N. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 2013, 210:1977-1992.
30. Guilliams M., Ginhoux F., Jakubzick C., Naik S.H., Onai N., Schraml B.U., Segura E., Tussiwand R., Yona S. Dendritic cells, monocytes and macrophages: a 0unified nomenclature based on ontogeny. Nat. Rev. Immunol. 2014, 14:571-578.
31. Haase J., Weyer U., Immig K., Klöting N., Blüher M., Eilers J., Bechmann I., Gericke M. Local proliferation of macrophages in adipose tissue during obesity-induced inflammation. Diabetologia 2014, 57:562-571.
32. Hashimoto D., Chow A., Noizat C., Teo P., Beasley M.B., Leboeuf M., Becker C.D., See P., Price J., Lucas D., et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013, 38:792-804.
33. Hettinger J., Richards D.M., Hansson J., Barra M.M., Joschko A.-C., Krijgsveld J., Feuerer M. Origin of monocytes and macrophages in a committed progenitor. Nat. Immunol. 2013, 14:821-830.
34. Hoeffel G., Ginhoux F. Ontogeny of tissue-resident macrophages. Front. Immunol. 2015, 6:486.
35. Hoeffel G., Wang Y., Greter M., See P., Teo P., Malleret B., Leboeuf M., Low D., Oller G., Almeida F., et al. Adult Langerhans cells derive predominantly from embryonic fetal liver monocytes with a minor contribution of yolk sac-derived macrophages. J. Exp. Med. 2012, 209:1167-1181.
36. Hoeffel G., Chen J., Lavin Y., Low D., Almeida F.F., See P., Beaudin A.E., Lum J., Low I., Forsberg E.C., et al. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 2015, 42:665-678.
37. Jaitin D.A., Kenigsberg E., Keren-Shaul H., Elefant N., Paul F., Zaretsky I., Mildner A., Cohen N., Jung S., Tanay A., Amit I. Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types. Science 2014, 343:776-779.
38. Jakubzick C., Gautier E.L., Gibbings S.L., Sojka D.K., Schlitzer A., Johnson T.E., Ivanov S., Duan Q., Bala S., Condon T., et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 2013, 39:599-610.
39. Kanda H., Tateya S., Tamori Y., Kotani K., Hiasa K., Kitazawa R., Kitazawa S., Miyachi H., Maeda S., Egashira K., Kasuga M. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 2006, 116:1494-1505.
40. Kierdorf K., Erny D., Goldmann T., Sander V., Schulz C., Perdiguero E.G., Wieghofer P., Heinrich A., Riemke P., Hölscher C., et al. Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nat. Neurosci. 2013, 16:273-280.
41. Lavin Y., Winter D., Blecher-Gonen R., David E., Keren-Shaul H., Merad M., Jung S., Amit I. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 2014, 159:1312-1326.
42. Lavin Y., Mortha A., Rahman A., Merad M. Regulation of macrophage development and function in peripheral tissues. Nat. Rev. Immunol. 2015, 15:731-744.
43. Liu K., Victora G.D., Schwickert T.A., Guermonprez P., Meredith M.M., Yao K., Chu F.-F., Randolph G.J., Rudensky A.Y., Nussenzweig M. In vivo analysis of dendritic cell development and homeostasis. Science 2009, 324:392-397.
44. + cells are a transient population of monocyte-derived macrophages. Immunity 2014, 41:465-477.
45. McGrath K.E., Frame J.M., Fegan K.H., Bowen J.R., Conway S.J., Catherman S.C., Kingsley P.D., Koniski A.D., Palis J. Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo. Cell Rep. 2015, 11:1892-1904.
46. Merad M., Manz M.G., Karsunky H., Wagers A., Peters W., Charo I., Weissman I.L., Cyster J.G., Engleman E.G. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 2002, 3:1135-1141.
47. Mizoguchi S., Takahashi K., Takeya M., Naito M., Morioka T. Development, differentiation, and proliferation of epidermal Langerhans cells in rat ontogeny studied by a novel monoclonal antibody against epidermal Langerhans cells, RED-1. J. Leukoc. Biol. 1992, 52:52-61.
48. Molawi K., Wolf Y., Kandalla P.K., Favret J., Hagemeyer N., Frenzel K., Pinto A.R., Klapproth K., Henri S., Malissen B., et al. Progressive replacement of embryo-derived cardiac macrophages with age. J. Exp. Med. 2014, 211:2151-2158.
49. Mucenski M.L., McLain K., Kier A.B., Swerdlow S.H., Schreiner C.M., Miller T.A., Pietryga D.W., Scott W.J., Potter S.S. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 1991, 65:677-689.
50. Naik S.H., Sathe P., Park H.-Y., Metcalf D., Proietto A.I., Dakic A., Carotta S., O'Keeffe M., Bahlo M., Papenfuss A., et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 2007, 8:1217-1226.
51. Naito M., Takahashi K., Nishikawa S. Development, differentiation, and maturation of macrophages in the fetal mouse liver. J. Leukoc. Biol. 1990, 48:27-37.
52. Naito M., Umeda S., Yamamoto T., Moriyama H., Umezu H., Hasegawa G., Usuda H., Shultz L.D., Takahashi K. Development, differentiation, and phenotypic heterogeneity of murine tissue macrophages. J. Leukoc. Biol. 1996, 59:133-138.
53. Okabe Y., Medzhitov R. Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014, 157:832-844.
54. Okabe Y., Medzhitov R. Tissue biology perspective on macrophages. Nat. Immunol. 2015, 17:9-17.
55. Onai N., Obata-Onai A., Schmid M.A., Ohteki T., Jarrossay D., Manz M.G. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat. Immunol. 2007, 8:1207-1216.
56. Orkin S.H., Zon L.I. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008, 132:631-644.
57. Palis J., Yoder M.C. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp. Hematol. 2001, 29:927-936.
58. Palis J., Robertson S., Kennedy M., Wall C., Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999, 126:5073-5084.
59. Paul F., Arkin Y., Giladi A., Jaitin D.A., Kenigsberg E., Keren-Shaul H., Winter D., Lara-Astiaso D., Gury M., Weiner A., et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 2015, 163:1663-1677.
60. Perdiguero E.G., Geissmann F. The development and maintenance of resident macrophages. Nat. Immunol. 2015, 17:2-8.
61. Platt A.M., Bain C.C., Bordon Y., Sester D.P., Mowat A.M. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J. Immunol. 2010, 184:6843-6854.
62. Price J.G., Idoyaga J., Salmon H., Hogstad B., Bigarella C.L., Ghaffari S., Leboeuf M., Merad M. CDKN1A regulates Langerhans cell survival and promotes Treg cell generation upon exposure to ionizing irradiation. Nat. Immunol. 2015, 16:1060-1068.
63. Ramsay R.G., Gonda T.J. MYB function in normal and cancer cells. Nat. Rev. Cancer 2008, 8:523-534.
64. Samokhvalov I.M., Samokhvalova N.I., Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007, 446:1056-1061.
65. Sathe P., Metcalf D., Vremec D., Naik S.H., Langdon W.Y., Huntington N.D., Wu L., Shortman K. Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage-dendritic cell-restricted progenitor. Immunity 2014, 41:104-115.
66. Schlitzer A., Sivakamasundari V., Chen J., Sumatoh H.R.B., Schreuder J., Lum J., Malleret B., Zhang S., Larbi A., Zolezzi F., et al. Identification of cDC1- and cDC2-committed DC progenitors reveals early lineage priming at the common DC progenitor stage in the bone marrow. Nat. Immunol. 2015, 16:718-728.
67. Schneider C., Nobs S.P., Kurrer M., Rehrauer H., Thiele C., Kopf M. Induction of the nuclear receptor PPAR-γ by the cytokine GM-CSF is critical for the differentiation of fetal monocytes into alveolar macrophages. Nat. Immunol. 2014, 15:1026-1037.
68. Schulz C., Gomez Perdiguero E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., Prinz M., Wu B., Jacobsen S.E., Pollard J.W., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012, 336:86-90.
69. Scott C.L., Henri S., Guilliams M. Mononuclear phagocytes of the intestine, the skin, and the lung. Immunol. Rev. 2014, 262:9-24.
70. Scott C.L., Zheng F., De Baetselier P., Martens L., Saeys Y., De Prijck S., Lippens S., Abels C., Schoonooghe S., Raes G., et al. Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells. Nat. Commun. 2016, 7:10321.
71. Sheng J., Ruedl C., Karjalainen K. Most tissue-resident macrophages except microglia are derived from fetal hematopoietic stem cells. Immunity 2015, 43:382-393.
72. Sorokin S.P., Hoyt R.F.J., Blunt D.G., McNelly N.A. Macrophage development: II. Early ontogeny of macrophage populations in brain, liver, and lungs of rat embryos as revealed by a lectin marker. Anat. Rec. 1992, 232:527-550.
73. Squarzoni P., Oller G., Hoeffel G., Pont-Lezica L., Rostaing P., Low D., Bessis A., Ginhoux F., Garel S. Microglia modulate wiring of the embryonic forebrain. Cell Rep. 2014, 8:1271-1279.
74. Sumner R., Crawford A., Mucenski M., Frampton J. Initiation of adult myelopoiesis can occur in the absence of c-Myb whereas subsequent development is strictly dependent on the transcription factor. Oncogene 2000, 19:3335-3342.
75. Tamoutounour S., Guilliams M., Montanana Sanchis F., Liu H., Terhorst D., Malosse C., Pollet E., Ardouin L., Luche H., Sanchez C., et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 2013, 39:925-938.
76. Tober J., Koniski A., McGrath K.E., Vemishetti R., Emerson R., de Mesy-Bentley K.K.L., Waugh R., Palis J. The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood 2007, 109:1433-1441.
77. Tober J., Yzaguirre A.D., Piwarzyk E., Speck N.A. Distinct temporal requirements for Runx1 in hematopoietic progenitors and stem cells. Development 2013, 140:3765-3776.
78. van de Laar L., Saelens W., De Prijck S., Martens L., Scott C.L., Van Isterdael G., Hoffmann E., Beyaert R., Saeys Y., Lambrecht B.N., Guilliams M. Yolk sac macrophages, fetal liver, and adult monocytes can colonize an empty niche and develop into functional tissue-resident macrophages. Immunity 2016, 44. Published online March 15, 2016.
79. van Furth R., Cohn Z.A. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 1968, 128:415-435.
80. van Furth R., Diesselhoff-Den Dulk M.M. The kinetics of promonocytes and monocytes in the bone marrow. J. Exp. Med. 1970, 132:813-828.
81. van Furth R., Cohn Z.A., Hirsch J.G., Humphrey J.H., Spector W.G., Langevoort H.L. The mononuclear phagocyte system: a new classification of macrophages, monocytes, and their precursor cells. Bull. World Health Organ. 1972, 46:845-852.
82. Weisberg S.P., McCann D., Desai M., Rosenbaum M., Leibel R.L., Ferrante A.W. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 2003, 112:1796-1808.
83. Weisberg S.P., Hunter D., Huber R., Lemieux J., Slaymaker S., Vaddi K., Charo I., Leibel R.L., Ferrante A.W. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J. Clin. Invest. 2006, 116:115-124.
84. Xue J., Schmidt S.V., Sander J., Draffehn A., Krebs W., Quester I., De Nardo D., Gohel T.D., Emde M., Schmidleithner L., et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 2014, 40:274-288.
85. Yoder M.C., Hiatt K. Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood 1997, 89:2176-2183.
86. Yona S., Gordon S. From the reticuloendothelial to mononuclear phagocyte system - the unaccounted years. Front. Immunol. 2015, 6:328.
87. Yona S., Kim K.-W., Wolf Y., Mildner A., Varol D., Breker M., Strauss-Ayali D., Viukov S., Guilliams M., Misharin A., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013, 38:79-91.
88. Zigmond E., Varol C., Farache J., Elmaliah E., Satpathy A.T., Friedlander G., Mack M., Shpigel N., Boneca I.G., Murphy K.M., et al. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 2012, 37:1076-1090.
89. Zigmond E., Bernshtein B., Friedlander G., Walker C.R., Yona S., Kim K.-W., Brenner O., Krauthgamer R., Varol C., Müller W., Jung S. Macrophage-restricted interleukin-10 receptor deficiency, but not IL-10 deficiency, causes severe spontaneous colitis. Immunity 2014, 40:720-733.