Development and homeostasis of "resident" myeloid cells: The case of the microglia

GLIA

Volumn 61, Issue 1, 2013, Pages 112-120

  Gomez Perdiguero, Elisa ^a,b   Schulz, Christian ^a,b   Geissmann, Frederic ^a,b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Fetal liver; Hematopoiesis; Macrophages; Myb; Yolk sac

Indexed keywords

CD135 ANTIGEN; PROTEIN MYB; TRANSCRIPTION FACTOR PU 1;

ARTICLE; BONE MARROW CELL; CELL FATE; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CENTRAL NERVOUS SYSTEM; CHRONIC INFLAMMATION; EMBRYO DEVELOPMENT; EPIDERMIS; FETUS LIVER; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; KIDNEY CELL; KUPFFER CELL; LANGERHANS CELL; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MICROGLIA; NONHUMAN; PANCREAS CELL; PRIORITY JOURNAL; SPLEEN CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; HEMATOPOIETIC STEM CELLS; HOMEOSTASIS; HUMANS; MICROGLIA; MYELOID CELLS; NEUROGENESIS;

EID: 84869156976     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22393     Document Type: Article

References (106)

1. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM. 2011. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14: 1142-1149.
2. 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.
3. Alliot F, Godin I, Pessac B. 1999. Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res Dev Brain Res 117: 145-152.
4. Ashwell K. 1991. The distribution of microglia and cell death in the fetal rat forebrain. Brain Res Dev Brain Res 58: 1-12.
5. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. 2007. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670.
6. Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C, Saederup N, Leemput J, Bigot K, Campisi L, Abitbol M, Molina T, Charo I, Hume DA, Cumano A, Lauvau G, Geissmann F. 2009. CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 206: 595-606.
7. Badalian-Very G, Vergilio JA, Degar BA, MacConaill LE, Brandner B, Calicchio ML, Kuo FC, Ligon AH, Stevenson KE, Kehoe SM, Garraway LA, Hahn WC, Meyerson M, Fleming MD, Rollins BJ. 2010. Recurrent BRAF mutations in Langerhans cell histiocytosis. Blood 116: 1919-1923.
8. Barcellos-Hoff MH, Park C, Wright EG. 2005. Radiation and the microenvironment-Tumorigenesis and therapy. Nat Rev Cancer 5: 867-875.
9. Bartunek P, Kralova J, Blendinger G, Dvorak M, Zenke M. 2003. GATA-1 and c-myb crosstalk during red blood cell differentiation through GATA-1 binding sites in the c-myb promoter. Oncogene 22: 1927-1935.
10. Benz C, Martins VC, Radtke F, Bleul CC. 2008. The stream of precursors that colonizes the thymus proceeds selectively through the early T lineage precursor stage of T cell development. J Exp Med 205: 1187-1199.
11. Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D. 2010. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464: 108-111.
12. 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.
13. Bigley V, Haniffa M, Doulatov S, Wang XN, Dickinson R, McGovern N, Jardine L, Pagan S, Dimmick I, Chua I, Wallis J, Lordan J, Morgan C, Kumararatne DS, Doffinger R, van der Burg M, van Dongen J, Cant A, Dick JE, Hambleton S, Collin M. 2011. The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency. JExp Med 208: 227-234.
14. Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C. 2010. In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464: 116-120.
15. Bouwens L, Baekeland M, De Zanger R, Wisse E. 1986. Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 6: 718-722.
16. Buza-Vidas N, Woll P, Hultquist A, Duarte S, Lutteropp M, Bouriez-Jones T, Ferry H, Luc S, Jacobsen SE. 2011. FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells. Blood 118: 1544-1548.
17. Choi JH, Cheong C, Dandamudi DB, Park CG, Rodriguez A, Mehandru S, Velinzon K, Jung IH, Yoo JY, Oh GT, Steinman RM. 2011. Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35: 819-831.
18. Chorro L, Sarde A, Li M, Woollard KJ, Chambon P, Malissen B, Kissenpfennig A, Barbaroux JB, Groves R, Geissmann F. 2009. Langerhans cell (LC) proliferation mediates neonatal development, homeostasis, and inflammation-associated expansion of the epidermal LC network. J Exp Med 206: 3089-3100.
19. Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, Senechal B, Puel A, Biswas SK, Moshous D, Picard C, Jais JP, D'Cruz D, Casanova JL, Trouillet C, Geissmann F. 2010. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33: 375-386.
20. Cuadros MA, Martin C, Coltey P, Almendros A, Navascues J. 1993. First appearance, distribution, and origin of macrophages in the early development of the avian central nervous system. J Comp Neurol 330: 113-129.
21. Cumano A, Godin I. 2007. Ontogeny of the hematopoietic system. Annu Rev Immunol 25: 745-785.
22. Dai P, Akimaru H, Tanaka Y, Hou DX, Yasukawa T, Kanei-Ishii C, Takahashi T, Ishii S. 1996. CBP as a transcriptional coactivator of c-Myb. Genes Dev 10: 528-540.
23. Dakic A, Metcalf D, Di Rago L, Mifsud S, Wu L, Nutt SL. 2005. PU.1 regulates the commitment of adult hematopoietic progenitors and restricts granulopoiesis. J Exp Med 201: 1487-1502.
24. Davies LC, Rosas M, Smith PJ, Fraser DJ, Jones SA, Taylor PR. 2011. A quantifiable proliferative burst of tissue macrophages restores homeostatic macrophage populations after acute inflammation. Eur J Immunol 41: 2155-2164.
25. de Groot CJ, Huppes W, Sminia T, Kraal G, Dijkstra CD. 1992. Determination of the origin and nature of brain macrophages and microglial cells in mouse central nervous system, using non-radioactive in situ hybridization and immunoperoxidase techniques. Glia 6: 301-309.
26. DeKoter RP, Walsh JC, Singh H. 1998. PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J 17: 4456-4468.
27. Erblich B, Zhu L, Etgen AM, Dobrenis K, Pollard JW. 2011. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS One 6: e26317.
28. Fantin A, Schwarz Q, Davidson K, Normando EM, Denti L, Ruhrberg C. 2011. The cytoplasmic domain of neuropilin 1 is dispensable for angiogenesis, but promotes the spatial separation of retinal arteries and veins. Development 138: 4185-4191.
29. Feil R, Brocard J, Mascrez B, LeMeur M, Metzger D, Chambon P. 1996. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 93: 10887-10890.
30. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, Cumano A, Geissmann F. 2006. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 311: 83-87.
31. Geissmann F, Jung S, Littman DR. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19: 71-82.
32. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. 2010. Development of monocytes, macrophages, and dendritic cells. Science 327: 656-661.
33. 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.
34. Ginhoux F, Tacke F, Angeli V, Bogunovic M, Loubeau M, Dai XM, Stanley ER, Randolph GJ, Merad M. 2006. Langerhans cells arise from monocytes in vivo. Nat Immunol 7: 265-273.
35. Gschnait F, Brenner W. 1979. Kinetics of epidermal Langerhans cells. J Invest Dermatol 73: 566-569.
36. 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, Hubeau M, Feinberg J, Al-Muhsen S, Cant A, Abel L, Chaussabel D, Doffinger R, Talesnik E, Grumach A, Duarte A, Abarca K, Moraes-Vasconcelos D, Burk D, Berghuis A, Geissmann F, Collin M, Casanova JL, Gros P. 2011. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 365: 127-138.
37. Hanna RN, Carlin LM, Hubbeling HG, Nackiewicz D, Green AM, Punt JA, Geissmann F, Hedrick CC. 2011. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C- monocytes. Nat Immunol. 12: 778-785.
38. Herbomel P, Thisse B, Thisse C. 2001. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Dev Biol 238: 274-288.
39. Hickey WF, Kimura H. 1988. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 239: 290-292.
40. Hickey WF, Vass K, Lassmann H. 1992. Bone marrow-derived elements in the central nervous system: An immunohistochemical and ultrastructural survey of rat chimeras. J Neuropathol Exp Neurol 51: 246-256.
41. Hsu AP, Sampaio EP, Khan J, Calvo KR, Lemieux JE, Patel SY, Frucht DM, Vinh DC, Auth RD, Freeman AF, Olivier KN, Uzel G, Zerbe CS, Spalding C, Pittaluga S, Raffeld M, Kuhns DB, Ding L, Paulson ML, Marciano BE, Gea-Banacloche JC, Orange JS, Cuellar-Rodriguez J, Hickstein DD, Holland SM. 2011. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood 118: 2653-2655.
42. Imayoshi I, Ohtsuka T, Metzger D, Chambon P, Kageyama R. 2006. Temporal regulation of Cre recombinase activity in neural stem cells. Genesis 44; 233-238.
43. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. 2002. A stem cell molecular signature. Science 298: 601-604.
44. Jenkins SJ, Ruckerl D, Cook PC, Jones LH, Finkelman FD, van Rooijen N, MacDonald AS, Allen JE. 2011. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332: 1284-1288.
45. Kanitakis J, Petruzzo P, Dubernard JM. 2004. Turnover of epidermal Langerhans' cells. N Engl J Med 351: 2661-2662.
46. Kasper LH, Boussouar F, Ney PA, Jackson CW, Rehg J, van Deursen JM, Brindle PK. 2002. A transcription-factor-binding surface of coactivator p300 is required for haematopoiesis. Nature 419: 738-743.
47. Katz SI, Tamaki K, Sachs DH. 1979. Epidermal Langerhans cells are derived from cells originating in bone marrow. Nature 282: 324-326.
48. King IL, Dickendesher TL, Segal BM. 2009. Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 113: 3190-3197.
49. Kissa K, Herbomel P. 2010. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464: 112-115.
50. Klein I, Cornejo JC, Polakos NK, John B, Wuensch SA, Topham DJ, Pierce RH, Crispe IN. 2007. Kupffer cell heterogeneity: Functional properties of bone marrow derived and sessile hepatic macrophages. Blood 110: 4077-4085.
51. Krall WJ, Challita PM, Perlmutter LS, Skelton DC, Kohn DB. 1994. Cells expressing human glucocerebrosidase from a retroviral vector repopulate macrophages and central nervous system microglia after murine bone marrow transplantation. Blood 83: 2737-2748.
52. Kranc KR, Schepers H, Rodrigues NP, Bamforth S, Villadsen E, Ferry H, Bouriez-Jones T, Sigvardsson M, Bhattacharya S, Jacobsen SE, Enver T. 2009. Cited2 is an essential regulator of adult hematopoietic stem cells. Cell Stem Cell 5: 659-665.
53. Labastie MC, Cortes F, Romeo PH, Dulac C, Peault B. 1998. Molecular identity of hematopoietic precursor cells emerging in the human embryo. Blood 92: 3624-3635.
54. Lassmann H, Schmied M, Vass K, Hickey WF. 1993. Bone marrow derived elements and resident microglia in brain inflammation. Glia 7: 19-24.
55. Lawson LJ, Perry VH, Dri P, Gordon S. 1990. Heterogeneity in the distribution and morphology of microglia in the normal adult mouse brain. Neuroscience 39: 151-170.
56. Lawson LJ, Perry VH, Gordon S. 1992. Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48: 405-415.
57. Lichanska AM, Browne CM, Henkel GW, Murphy KM, Ostrowski MC, McKercher SR, Maki RA, Hume DA. 1999. Differentiation of the mononuclear phagocyte system during mouse embryogenesis: The role of transcription factor PU.1. Blood 94: 127-138.
58. Lieu YK, Reddy EP. 2009. Conditional c-myb knockout in adult hematopoietic stem cells leads to loss of self-renewal due to impaired proliferation and accelerated differentiation. Proc Natl Acad Sci USA 106: 21689-21694.
59. Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, Chu FF, Randolph GJ, Rudensky AY, Nussenzweig M. 2009. In vivo analysis of dendritic cell development and homeostasis. Science 324: 392-397.
60. Liu K, Waskow C, Liu X, Yao K, Hoh J, Nussenzweig M. 2007. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 8: 578-583.
61. Massengale M, Wagers AJ, Vogel H, Weissman IL. 2005. Hematopoietic cells maintain hematopoietic fates upon entering the brain. J Exp Med 201: 1579-1589.
62. Matsumoto Y, Fujiwara M. 1987. Absence of donor-type major histocompatibility complex class I antigen-bearing microglia in the rat central nervous system of radiation bone marrow chimeras. J Neuroimmunol 17: 71-82.
63. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CC, Beck PL, Muruve DA, Kubes P. 2010. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
64. 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.
65. Medvinsky A, Dzierzak E. 1996. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86: 897-906.
66. Merad M, Manz MG, Karsunky H, Wagers A, Peters W, Charo I, Weissman IL, Cyster JG, Engleman EG. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat Immunol 3: 1135-1141.
67. Metzger D, Clifford J, Chiba H, Chambon P. 1995. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc Natl Acad Sci USA 92: 6991-6995.
68. 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-6ChiCCR2+ monocytes only under defined host conditions. Nat Neurosci 10: 1544-1553.
69. Mildner A, Mack M, Schmidt H, Brück W, Djukic M, Zabel MD, Hille A, Priller J, Prinz M. 2009. CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 132: 2487-2500.
70. Miyauchi S, Hashimoto K. 1987. Epidermal Langerhans cells undergo mitosis during the early recovery phase after ultraviolet-B irradiation. J Invest Dermatol 88: 703-708.
71. Mucenski ML, McLain K, Kier AB, Swerdlow SH, Schreiner CM, Miller TA, Pietryga DW, Scott WJ, Jr., Potter SS. 1991. A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65: 677-689.
72. Mukouyama Y, Chiba N, Mucenski ML, Satake M, Miyajima A, Hara T, Watanabe T. 1999. Hematopoietic cells in cultures of the murine embryonic aorta-gonad-mesonephros region are induced by c-Myb. Curr Biol 9: 833-836.
73. Muller AM, Medvinsky A, Strouboulis J, Grosveld F, Dzierzak E. 1994. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1: 291-301.
74. Murayama E, Kissa K, Zapata A, Mordelet E, Briolat V, Lin HF, Handin RI, Herbomel P. 2006. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 25: 963-975.
75. Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Dakic A, Carotta S, O'Keeffe M, Bahlo M, Papenfuss A, Kwak JY, Wu L, Shortman K. 2007. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8: 1217-1226.
76. Nerlov C, Graf T. 1998. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev 12: 2403-2412.
77. Nimmerjahn A, Kirchhoff F, Helmchen F. 2005. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
78. Oelgeschlager M, Nuchprayoon I, Luscher B, Friedman AD. 1996. C/EBP, c-Myb, and PU.1 cooperate to regulate the neutrophil elastase promoter. Mol Cell Biol 16: 4717-4725.
79. Olson MC, Scott EW, Hack AA, Su GH, Tenen DG, Singh H, Simon MC. 1995. PU. 1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity 3: 703-714.
80. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG. 2007. Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8: 1207-1216.
81. Orkin SH, Zon LI. 2008. Hematopoiesis: An evolving paradigm for stem cell biology. Cell 132: 631-644.
82. Palis J, Robertson S, Kennedy M, Wall C, Keller G. 1999. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126: 5073-5084.
83. Palis J, Chan RJ, Koniski A, Patel R, Starr M, Yoder MC. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. 2001. Proc Natl Acad Sci USA 10; 98: 4528-4533.
84. Perreault C, Pelletier M, Landry D, Gyger M. 1984. Study of Langerhans cells after allogeneic bone marrow transplantation. Blood 63: 807-811.
85. Perry VH, Hume DA, Gordon S. 1985. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15: 313-326.
86. Priller J, Flugel A, Wehner T, Boentert M, Haas CA, Prinz M, Fernandez-Klett F, Prass K, Bechmann I, de Boer BA, Frotscher M, Kreutzberg GW, Persons PA, Dirnagl U. 2001. Targeting gene-modified hematopoietic cells to the central nervous system: Use of green fluorescent protein uncovers microglial engraftment. Nat Med 7: 1356-1361.
87. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA, Pollard JW. 2011. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475: 222-225.
88. Rae F, Woods K, Sasmono T, Campanale N, Taylor D, Ovchinnikov DA, Grimmond SM, Hume DA, Ricardo SD, Little MH. 2007. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter. Dev Biol 308: 232-246.
89. Reddy MA, Yang BS, Yue X, Barnett CJ, Ross IL, Sweet MJ, Hume DA, Ostrowski MC. 1994. Opposing actions of c-ets/PU.1 and c-myb protooncogene products in regulating the macrophage-specific promoters of the human and mouse colony-stimulating factor-1 receptor (c-fms) genes. J Exp Med 180: 2309-2319.
90. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK. 2009. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 137: 47-59.
91. Samokhvalov IM, Samokhvalova NI, Nishikawa S. 2007. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446: 1056-1061.
92. Sandberg ML, Sutton SE, Pletcher MT, Wiltshire T, Tarantino LM, Hogenesch JB, Cooke MP. 2005. c-Myb and p300 regulate hematopoietic stem cell proliferation and differentiation. Dev Cell 8: 153-166.
93. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, Ostrowski MC, Himes SR, Hume DA. 2003. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood 101: 1155-1163.
94. Satoh T, Smith A, Sarde A, Lu HC, Mian S, Trouillet C, Mufti G, Emile JF, Fraternali F, Donadieu J, Geissmann F. 2012. B-RAF mutant alleles associated with langerhans cell histiocytosis, a Granulomatous pediatric disease. PLoS One 7: e33891.
95. Schulz C, Gomez Perdiguero E, 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.
96. Shankaran M, Marino ME, Busch R, Keim C, King C, Lee J, Killion S, Awada M, Hellerstein MK. 2007. Measurement of brain microglial proliferation rates in vivo in response to neuroinflammatory stimuli: Application to drug discovery. J Neurosci Res 85: 2374-2384.
97. Shapiro LH. 1995. Myb and Ets proteins cooperate to transactivate an early myeloid gene. J Biol Chem 270: 8763-8771.
98. Sorokin SP, Hoyt RFJr, Blunt DG, McNelly NA. 1992. Macrophage development: II. Early ontogeny of macrophage populations in brain, liver, and lungs of rat embryos as revealed by a lectin marker. Anat Rec 232: 527-550.
99. Soza-Ried C, Hess I, Netuschil N, Schorpp M, Boehm T. 2010. Essential role of c-myb in definitive hematopoiesis is evolutionarily conserved. Proc Natl Acad Sci USA 107: 17304-17308.
100. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1: 4.
101. Sumner R, Crawford A, Mucenski M, Frampton J. 2000. Initiation of adult myelopoiesis can occur in the absence of c-Myb whereas subsequent development is strictly dependent on the transcription factor. Oncogene 19: 3335-3342.
102. Thored P, Heldmann U, Gomes-Leal W, Gisler R, Darsalia V, Taneera J, Nygren JM, Jacobsen SE, Ekdahl CT, Kokaia Z, Lindvall O. 2009. Long-term accumulation of microglia with proneurogenic phenotype concomitant with persistent neurogenesis in adult subventricular zone after stroke. Glia 57: 835-849.
103. Vandenbunder B, Pardanaud L, Jaffredo T, Mirabel MA, Stehelin D. 1989. Complementary patterns of expression of c-ets 1, c-myb and c-myc in the blood-forming system of the chick embryo. Development 107: 265-274.
104. Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, Fehling HJ, Hardt WD, Shakhar G, Jung S. 2009. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31: 502-512.
105. Wake H, Moorhouse AJ, Jinno S, Kohsaka S, Nabekura J. 2009. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J Neurosci 29: 3974-3980.
106. Zhao L, Glazov EA, Pattabiraman DR, Al-Owaidi F, Zhang P, Brown MA, Leo PJ, Gonda TJ. 2011. Integrated genome-wide chromatin occupancy and expression analyses identify key myeloid pro-differentiation transcription factors repressed by Myb. Nucleic Acids Res 39: 4664-4679.