2014 Jeffrey M. Hoeg award lecture: Transcriptional control of monocyte development

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 9, 2016, Pages 1722-1733

  Zhu, Yanfang Peipei ^a   Thomas, Graham D ^a   Hedrick, Catherine C ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Atherosclerosis; Bone marrow; MicroRNAs; Monocytes; Transcription factors

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; KRUPPEL LIKE FACTOR 4; MICRORNA; NUCLEAR RECEPTOR NUR77; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FLI 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR SFPI1; UNCLASSIFIED DRUG;

ATHEROSCLEROSIS; BONE MARROW; DISEASE COURSE; EXTRAMEDULLARY HEMATOPOIESIS; GENETIC ASSOCIATION STUDY; HUMAN; IMMUNOCOMPETENT CELL; MACROPHAGE; MONOCYTE; MYELOPOIESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION REGULATION; ANIMAL; BONE MARROW CELL; CELL DIFFERENTIATION; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; IMMUNOLOGY; METABOLISM; PHENOTYPE; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLULAR MICROENVIRONMENT; GENE EXPRESSION REGULATION; GENOTYPE; HEMATOPOIESIS, EXTRAMEDULLARY; HUMANS; MICRORNAS; MONOCYTES; MYELOPOIESIS; PHENOTYPE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84978087221     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.304054     Document Type: Review

References (128)

1. Randolph GJ, Inaba K, Robbiani DF, Steinman RM, Muller WA, Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 1999 11 753 761
2. Carlin LM, Stamatiades EG, Auffray C, Hanna RN, Glover L, Vizcay-Barrena G, Hedrick CC, Cook HT, Diebold S, Geissmann F, Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell 2013 153 362 375. doi: 10.1016/j.cell.2013.03.010
3. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F, Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007 317 666 670. doi: 10.1126/science.1142883
4. 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, Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010 33 375 386. doi: 10.1016/j.immuni.2010.08.012
5. Hanna RN, Cekic C, Sag D, Patrolling monocytes control tumor metastasis to the lung. Science 2015 350 985 990. doi: 10.1126/science.aac9407
6. Geissmann F, Jung S, Littman DR, Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003 19 71 82
7. Ziegler-Heitbrock L, Ancuta P, Crowe S, Nomenclature of monocytes and dendritic cells in blood. Blood 2010 116 e74 e80. doi: 10.1182/blood-2010-02-258558
8. Passlick B, Flieger D, Ziegler-Heitbrock HW, Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 1989 74 2527 2534
9. Tacke F, Randolph GJ, Migratory fate and differentiation of blood monocyte subsets. Immunobiology 2006 211 609 618. doi: 10.1016/j.imbio.2006.05.025
10. Moore KJ, Sheedy FJ, Fisher EA, Macrophages in atherosclerosis: A dynamic balance. Nat Rev Immunol 2013 13 709 721. doi: 10.1038/nri3520
11. Moore KJ, Tabas I, Macrophages in the pathogenesis of atherosclerosis. Cell 2011 145 341 355. doi: 10.1016/j.cell.2011.04.005
12. Qian BZ, Pollard JW, Macrophage diversity enhances tumor progression and metastasis. Cell 2010 141 39 51. doi: 10.1016/j.cell.2010.03.014
13. Qian B, Deng Y, Im JH, Muschel RJ, Zou Y, Li J, Lang RA, Pollard JW, A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 2009 4 e6562. doi: 10.1371/journal.pone.0006562
14. Goodman JW, The use of isoimmune sera for identification of hemopoietic cells from blood-injected radiation chimeras. Ann N Y Acad Sci 1962 97 95 103
15. Goodman JW, Hodgson GS, Evidence for stem cells in the peripheral blood of mice. Blood 1962 19 702 714
16. Weissman IL, Anderson DJ, Gage F, Stem and progenitor cells: Origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol 2001 17 387 403. doi: 10.1146/annurev.cellbio.17.1.387
17. Wright DE, Wagers AJ, Gulati AP, Johnson FL, Weissman IL, Physiological migration of hematopoietic stem and progenitor cells. Science 2001 294 1933 1936. doi: 10.1126/science.1064081
18. Weissman IL, Stem cells, clonal progenitors, and commitment to the three lymphocyte lineages: T, B, and NK cells. Immunity 1994 1 529 531
19. Osawa M, Hanada K, Hamada H, Nakauchi H, Long-Term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996 273 242 245
20. Randall TD, Lund FE, Howard MC, Weissman IL, Expression of murine CD38 defines a population of long-Term reconstituting hematopoietic stem cells. Blood 1996 87 4057 4067
21. Kondo M, Weissman IL, Akashi K, Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997 91 661 672
22. Akashi K, Traver D, Miyamoto T, Weissman IL, A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000 404 193 197. doi: 10.1038/35004599
23. Iwasaki H, Akashi K, Myeloid lineage commitment from the hematopoietic stem cell. Immunity 2007 26 726 740. doi: 10.1016/j.immuni.2007.06.004
24. Manz MG, Miyamoto T, Akashi K, Weissman IL, Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A 2002 99 11872 11877. doi: 10.1073/pnas.172384399
25. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, Cumano A, Geissmann F, A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006 311 83 87. doi: 10.1126/science.1117729
26. Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, Chu FF, Randolph GJ, Rudensky AY, Nussenzweig M, In vivo analysis of dendritic cell development and homeostasis. Science 2009 324 392 397. doi: 10.1126/science.1170540
27. Ginhoux F, Liu K, Helft J, Bogunovic M, Greter M, Hashimoto D, Price J, Yin N, Bromberg J, Lira SA, Stanley ER, Nussenzweig M, Merad M, The origin and development of nonlymphoid tissue CD103+ DCs. J Exp Med 2009 206 3115 3130. doi: 10.1084/jem.20091756
28. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, Kalchenko V, Geissmann F, Jung S, Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 2007 204 171 180. doi: 10.1084/jem.20061011
29. Varol C, Vallon-Eberhard A, Elinav E, Aychek T, Shapira Y, Luche H, Fehling HJ, Hardt WD, Shakhar G, Jung S, Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009 31 502 512. doi: 10.1016/j.immuni.2009.06.025
30. Schlitzer A, Sivakamasundari V, Chen J, 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. doi: 10.1038/ni.3200
31. 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, Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 2007 8 1217 1226. doi: 10.1038/ni1522
32. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG, Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 2007 8 1207 1216. doi: 10.1038/ni1518
33. Auffray C, Fogg DK, Narni-Mancinelli E, CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 2009 206 595 606. doi: 10.1084/jem.20081385
34. Cecchini MG, Dominguez MG, Mocci S, Wetterwald A, Felix R, Fleisch H, Chisholm O, Hofstetter W, Pollard JW, Stanley ER, Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 1994 120 1357 1372
35. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, Sylvestre V, Stanley ER, Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects. Blood 2002 99 111 120
36. Wiktor-Jedrzejczak W, Gordon S, Cytokine regulation of the macrophage (M phi) system studied using the colony stimulating factor-1-deficient op/op mouse. Physiol Rev 1996 76 927 947
37. Wiktor-Jedrzejczak WW, Ahmed A, Szczylik C, Skelly RR, Hematological characterization of congenital osteopetrosis in op/op mouse. Possible mechanism for abnormal macrophage differentiation. J Exp Med 1982 156 1516 1527
38. Hettinger J, Richards DM, Hansson J, Barra MM, Joschko AC, Krijgsveld J, Feuerer M, Origin of monocytes and macrophages in a committed progenitor. Nat Immunol 2013 14 821 830. doi: 10.1038/ni.2638
39. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ, Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009 325 612 616. doi: 10.1126/science.1175202
40. Robbins CS, Chudnovskiy A, Rauch PJ, Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 2012 125 364 374. doi: 10.1161/CIRCULATIONAHA.111.061986
41. Ensan S, Li A, Besla R, Self-renewing resident arterial macrophages arise from embryonic CX3CR1(+) precursors and circulating monocytes immediately after birth. Nat Immunol 2016 17 159 168. doi: 10.1038/ni.3343
42. Sunderkötter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, Leenen PJ, Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004 172 4410 4417
43. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, Strauss-Ayali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S, Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 2013 38 79 91. doi: 10.1016/j.immuni.2012.12.001
44. DeKoter RP, Singh H, Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 2000 288 1439 1441
45. Rieger MA, Hoppe PS, Smejkal BM, Eitelhuber AC, Schroeder T, Hematopoietic cytokines can instruct lineage choice. Science 2009 325 217 218. doi: 10.1126/science.1171461
46. Mossadegh-Keller N, Sarrazin S, Kandalla PK, Espinosa L, Stanley ER, Nutt SL, Moore J, Sieweke MH, M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 2013 497 239 243. doi: 10.1038/nature12026
47. Naik SH, Perié L, Swart E, Gerlach C, van Rooij N, de Boer RJ, Schumacher TN, Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature 2013 496 229 232. doi: 10.1038/nature12013
48. Heidt T, Sager HB, Courties G, Chronic variable stress activates hematopoietic stem cells. Nat Med 2014 20 754 758. doi: 10.1038/nm.3589
49. Murphy AJ, Akhtari M, Tolani S, Pagler T, Bijl N, Kuo CL, Wang M, Sanson M, Abramowicz S, Welch C, Bochem AE, Kuivenhoven JA, Yvan-Charvet L, Tall AR, ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J Clin Invest 2011 121 4138 4149. doi: 10.1172/JCI57559
50. Yvan-Charvet L, Pagler T, Gautier EL, Avagyan S, Siry RL, Han S, Welch CL, Wang N, Randolph GJ, Snoeck HW, Tall AR, ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 2010 328 1689 1693. doi: 10.1126/science.1189731
51. Wang M, Subramanian M, Abramowicz S, Murphy AJ, Gonen A, Witztum J, Welch C, Tabas I, Westerterp M, Tall AR, Interleukin-3/granulocyte macrophage colony-stimulating factor receptor promotes stem cell expansion, monocytosis, and atheroma macrophage burden in mice with hematopoietic ApoE deficiency. Arterioscler Thromb Vasc Biol 2014 34 976 984. doi: 10.1161/ATVBAHA.113.303097
52. Nagareddy PR, Murphy AJ, Stirzaker RA, Hu Y, Yu S, Miller RG, Ramkhelawon B, Distel E, Westerterp M, Huang LS, Schmidt AM, Orchard TJ, Fisher EA, Tall AR, Goldberg IJ, Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab 2013 17 695 708. doi: 10.1016/j.cmet.2013.04.001
53. Sarrazy V, Viaud M, Westerterp M, Ivanov S, Giorgetti-Peraldi S, Guinamard R, Gautier EL, Thorp EB, De Vivo DC, Yvan-Charvet L, Disruption of Glut1 in hematopoietic stem cells prevents myelopoiesis and enhanced glucose flux in atheromatous plaques of ApoE-/-Mice. Circ Res 2016 118 1062 1077. doi: 10.1161/CIRCRESAHA.115.307599
54. Serbina NV, Hohl TM, Cherny M, Pamer EG, Selective expansion of the monocytic lineage directed by bacterial infection. J Immunol 2009 183 1900 1910. doi: 10.4049/jimmunol.0900612
55. Serbina NV, Pamer EG, Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 2006 7 311 317. doi: 10.1038/ni1309
56. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H, Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 2006 126 755 766. doi: 10.1016/j.cell.2006.06.052
57. DeKoter RP, Walsh JC, Singh H, PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J 1998 17 4456 4468. doi: 10.1093/emboj/17.15.4456
58. Champhekar A, Damle SS, Freedman G, Carotta S, Nutt SL, Rothenberg EV, Regulation of early T-lineage gene expression and developmental progression by the progenitor cell transcription factor PU.1. Genes Dev 2015 29 832 848. doi: 10.1101/gad.259879.115
59. Anderson MK, Weiss AH, Hernandez-Hoyos G, Dionne CJ, Rothenberg EV, Constitutive expression of PU.1 in fetal hematopoietic progenitors blocks T cell development at the pro-T cell stage. Immunity 2002 16 285 296
60. Nutt SL, Metcalf D, D'Amico A, Polli M, Wu L, Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J Exp Med 2005 201 221 231. doi: 10.1084/jem.20041535
61. Scott EW, Simon MC, Anastasi J, Singh H, Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 1994 265 1573 1577
62. Friedman AD, Transcriptional regulation of myelopoiesis. Int J Hematol 2002 75 466 472
63. Ramji DP, Foka P, CCAAT/enhancer-binding proteins: Structure, function and regulation. Biochem J 2002 365 t 3 561 575. doi: 10.1042/BJ20020508
64. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG, Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Proc Natl Acad Sci U S A 1997 94 569 574
65. Radomska HS, Huettner CS, Zhang P, Cheng T, Scadden DT, Tenen DG, CCAAT/enhancer binding protein alpha is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Mol Cell Biol 1998 18 4301 4314
66. Wang X, Scott E, Sawyers CL, Friedman AD, C/EBPalpha bypasses granulocyte colony-stimulating factor signals to rapidly induce PU.1 gene expression, stimulate granulocytic differentiation, and limit proliferation in 32D cl3 myeloblasts. Blood 1999 94 560 571
67. Tamura A, Hirai H, Yokota A, Sato A, Shoji T, Kashiwagi T, Iwasa M, Fujishiro A, Miura Y, Maekawa T, Accelerated apoptosis of peripheral blood monocytes in Cebpb-deficient mice. Biochem Biophys Res Commun 2015 464 654 658. doi: 10.1016/j.bbrc.2015.07.045
68. Friedman AD, Transcriptional regulation of granulocyte and monocyte development. Oncogene 2002 21 3377 3390. doi: 10.1038/sj.onc.1205324
69. Jones LC, Lin ML, Chen SS, Krug U, Hofmann WK, Lee S, Lee YH, Koeffler HP, Expression of C/EBPbeta from the C/ebpalpha gene locus is sufficient for normal hematopoiesis in vivo. Blood 2002 99 2032 2036
70. Wang D, D'Costa J, Civin CI, Friedman AD, C/EBPalpha directs monocytic commitment of primary myeloid progenitors. Blood 2006 108 1223 1229. doi: 10.1182/blood-2005-12-008763
71. Laiosa CV, Stadtfeld M, Xie H, de Andres-Aguayo L, Graf T, Reprogramming of committed T cell progenitors to macrophages and dendritic cells by C/EBP alpha and PU.1 transcription factors. Immunity 2006 25 731 744. doi: 10.1016/j.immuni.2006.09.011
72. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010 38 576 589. doi: 10.1016/j.molcel.2010.05.004
73. Heinz S, Romanoski CE, Benner C, Allison KA, Kaikkonen MU, Orozco LD, Glass CK, Effect of natural genetic variation on enhancer selection and function. Nature 2013 503 487 492. doi: 10.1038/nature12615
74. Mak KS, Funnell AP, Pearson RC, Crossley M, PU.1 and haematopoietic cell fate: Dosage matters. Int J Cell Biol 2011 2011 808524. doi: 10.1155/2011/808524
75. Wang H, Lee CH, Qi C, Tailor P, Feng J, Abbasi S, Atsumi T, Morse HC 3rd, IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood 2008 112 4028 4038. doi: 10.1182/blood-2008-01-129049
76. Tsujimura H, Nagamura-Inoue T, Tamura T, Ozato K, IFN consensus sequence binding protein/IFN regulatory factor-8 guides bone marrow progenitor cells toward the macrophage lineage. J Immunol 2002 169 1261 1269
77. Scheller M, Foerster J, Heyworth CM, Waring JF, Löhler J, Gilmore GL, Shadduck RK, Dexter TM, Horak I, Altered development and cytokine responses of myeloid progenitors in the absence of transcription factor, interferon consensus sequence binding protein. Blood 1999 94 3764 3771
78. Tamura T, Thotakura P, Tanaka TS, Ko MS, Ozato K, Identification of target genes and a unique cis element regulated by IRF-8 in developing macrophages. Blood 2005 106 1938 1947. doi: 10.1182/blood-2005-01-0080
79. Kurotaki D, Osato N, Nishiyama A, Yamamoto M, Ban T, Sato H, Nakabayashi J, Umehara M, Miyake N, Matsumoto N, Nakazawa M, Ozato K, Tamura T, Essential role of the IRF8-KLF4 transcription factor cascade in murine monocyte differentiation. Blood 2013 121 1839 1849. doi: 10.1182/blood-2012-06-437863
80. Feinberg MW, Wara AK, Cao Z, Lebedeva MA, Rosenbauer F, Iwasaki H, Hirai H, Katz JP, Haspel RL, Gray S, Akashi K, Segre J, Kaestner KH, Tenen DG, Jain MK, The Kruppel-like factor KLF4 is a critical regulator of monocyte differentiation. EMBO J 2007 26 4138 4148. doi: 10.1038/sj.emboj.7601824
81. Alder JK, Georgantas RW 3rd, Hildreth RL, Kaplan IM, Morisot S, Yu X, McDevitt M, Civin CI, Kruppel-like factor 4 is essential for inflammatory monocyte differentiation in vivo. J Immunol 2008 180 5645 5652
82. Hanna RN, Carlin LM, Hubbeling HG, Nackiewicz D, Green AM, Punt JA, Geissmann F, Hedrick CC, The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C-monocytes. Nat Immunol 2011 12 778 785. doi: 10.1038/ni.2063
83. Hamers AA, Hanna RN, Nowyhed H, Hedrick CC, de Vries CJ, NR4A nuclear receptors in immunity and atherosclerosis. Curr Opin Lipidol 2013 24 381 385. doi: 10.1097/MOL.0b013e3283643eac
84. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK, A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell 2009 137 47 59. doi: 10.1016/j.cell.2009.01.038
85. Glass CK, Saijo K, Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nat Rev Immunol 2010 10 365 376. doi: 10.1038/nri2748
86. Mullican SE, Zhang S, Konopleva M, Ruvolo V, Andreeff M, Milbrandt J, Conneely OM, Abrogation of nuclear receptors Nr4a3 and Nr4a1 leads to development of acute myeloid leukemia. Nat Med 2007 13 730 735. doi: 10.1038/nm1579
87. Steidl U, Rosenbauer F, Verhaak RG, Essential role of Jun family transcription factors in PU.1 knockdown-induced leukemic stem cells. Nat Genet 2006 38 1269 1277. doi: 10.1038/ng1898
88. Hanna RN, Shaked I, Hubbeling HG, Punt JA, Wu R, Herrley E, Zaugg C, Pei H, Geissmann F, Ley K, Hedrick CC, NR4A1 (Nur77) deletion polarizes macrophages toward an inflammatory phenotype and increases atherosclerosis. Circ Res 2012 110 416 427. doi: 10.1161/CIRCRESAHA.111.253377
89. Woollard KJ, Geissmann F, Monocytes in atherosclerosis: Subsets and functions. Nat Rev Cardiol 2010 7 77 86. doi: 10.1038/nrcardio.2009.228
90. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ, Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007 117 185 194. doi: 10.1172/JCI28549
91. Epelman S, Lavine KJ, Randolph GJ, Origin and functions of tissue macrophages. Immunity 2014 41 21 35. doi: 10.1016/j.immuni.2014.06.013
92. Tacke R, Hilgendorf I, Garner H, Waterborg C, Park K, Nowyhed H, Hanna RN, Wu R, Swirski FK, Geissmann F, Hedrick CC, The transcription factor NR4A1 is essential for the development of a novel macrophage subset in the thymus. Sci Rep 2015 5 10055. doi: 10.1038/srep10055
93. Dickinson RE, Griffin H, Bigley V, Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood 2011 118 2656 2658. doi: 10.1182/blood-2011-06-360313
94. Nandakumar SK, Johnson K, Throm SL, Pestina TI, Neale G, Persons DA, Low-level GATA2 overexpression promotes myeloid progenitor self-renewal and blocks lymphoid differentiation in mice. Exp Hematol 2015 43 565 77.e1. doi: 10.1016/j.exphem.2015.04.002
95. Collin M, Dickinson R, Bigley V, Haematopoietic and immune defects associated with GATA2 mutation. Br J Haematol 2015 169 173 187. doi: 10.1111/bjh.13317
96. Chou ST, Khandros E, Bailey LC, Nichols KE, Vakoc CR, Yao Y, Huang Z, Crispino JD, Hardison RC, Blobel GA, Weiss MJ, Graded repression of PU.1/Sfpi1 gene transcription by GATA factors regulates hematopoietic cell fate. Blood 2009 114 983 994. doi: 10.1182/blood-2009-03-207944
97. Masuya M, Moussa O, Abe T, Deguchi T, Higuchi T, Ebihara Y, Spyropoulos DD, Watson DK, Ogawa M, Dysregulation of granulocyte, erythrocyte, and NK cell lineages in Fli-1 gene-Targeted mice. Blood 2005 105 95 102. doi: 10.1182/blood-2003-12-4345
98. Suzuki E, Williams S, Sato S, Gilkeson G, Watson DK, Zhang XK, The transcription factor Fli-1 regulates monocyte, macrophage and dendritic cell development in mice. Immunology 2013 139 318 327. doi: 10.1111/imm.12070
99. Ichikawa M, Asai T, Chiba S, Kurokawa M, Ogawa S, Runx1/AML-1 ranks as a master regulator of adult hematopoiesis. Cell Cycle 2004 3 722 724
100. Ichikawa M, Asai T, Saito T, Seo S, Yamazaki I, Yamagata T, Mitani K, Chiba S, Ogawa S, Kurokawa M, Hirai H, AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med 2004 10 299 304. doi: 10.1038/nm997
101. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR, AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 1996 84 321 330
102. Huang G, Zhang P, Hirai H, Elf S, Yan X, Chen Z, Koschmieder S, Okuno Y, Dayaram T, Growney JD, Shivdasani RA, Gilliland DG, Speck NA, Nimer SD, Tenen DG, PU.1 is a major downstream target of AML1 (RUNX1) in adult mouse hematopoiesis. Nat Genet 2008 40 51 60. doi: 10.1038/ng.2007.7
103. Song WJ, Sullivan MG, Legare RD, Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet 1999 23 166 175. doi: 10.1038/13793
104. Islam R, Yoon WJ, Woo KM, Baek JH, Ryoo HM, Pin1-mediated prolyl isomerization of Runx1 affects PU.1 expression in pre-monocytes. J Cell Physiol 2014 229 443 452. doi: 10.1002/jcp.24462
105. Nalls MA, Couper DJ, Tanaka T, Multiple loci are associated with white blood cell phenotypes. PLoS Genet 2011 7 e1002113. doi: 10.1371/journal.pgen.1002113
106. Okada Y, Hirota T, Kamatani Y, Identification of nine novel loci associated with white blood cell subtypes in a Japanese population. PLoS Genet 2011 7 e1002067. doi: 10.1371/journal.pgen.1002067
107. Crosslin DR, McDavid A, Weston N, CHARGE Hematology Working Group; electronic Medical Records and Genomics (eMERGE) Network Genetic variation associated with circulating monocyte count in the eMERGE Network. Hum Mol Genet 2013 22 2119 2127. doi: 10.1093/hmg/ddt010
108. Rotival M, Zeller T, Wild PS, Cardiogenics Consortium Integrating genome-wide genetic variations and monocyte expression data reveals trans-regulated gene modules in humans. PLoS Genet 2011 7 e1002367. doi: 10.1371/journal.pgen.1002367
109. Zeller T, Wild P, Szymczak S, Genetics and beyond-The transcriptome of human monocytes and disease susceptibility. PLoS One 2010 5 e10693. doi: 10.1371/journal.pone.0010693
110. Etzrodt M, Cortez-Retamozo V, Newton A, Regulation of monocyte functional heterogeneity by miR-146a and Relb. Cell Rep 2012 1 317 324. doi: 10.1016/j.celrep.2012.02.009
111. Sugatani T, Vacher J, Hruska KA, A microRNA expression signature of osteoclastogenesis. Blood 2011 117 3648 3657. doi: 10.1182/blood-2010-10-311415
112. Fontana L, Pelosi E, Greco P, Racanicchi S, Testa U, Liuzzi F, Croce CM, Brunetti E, Grignani F, Peschle C, MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 2007 9 775 787. doi: 10.1038/ncb1613
113. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K, Batte K, Shah P, Wisler J, Eubank TD, Tridandapani S, Paulaitis ME, Piper MG, Marsh CB, Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013 121 984 995. doi: 10.1182/blood-2011-08-374793
114. Chang RC, Ying W, Bazer FW, Zhou B, MicroRNAs Control Macrophage formation and activation: The inflammatory link between obesity and cardiovascular diseases. Cells 2014 3 702 712. doi: 10.3390/cells3030702
115. Zhuang G, Meng C, Guo X, Cheruku PS, Shi L, Xu H, Li H, Wang G, Evans AR, Safe S, Wu C, Zhou B, A novel regulator of macrophage activation: MiR-223 in obesity-Associated adipose tissue inflammation. Circulation 2012 125 2892 2903. doi: 10.1161/CIRCULATIONAHA.111.087817
116. Chaudhuri AA, So AY, Sinha N, Gibson WS, Taganov KD, O'Connell RM, Baltimore D, MicroRNA-125b potentiates macrophage activation. J Immunol 2011 187 5062 5068. doi: 10.4049/jimmunol.1102001
117. Fordham JB, Naqvi AR, Nares S, miR-24 Regulates Macrophage Polarization and Plasticity. J Clin Cell Immunol 2015 6. doi: 10.4172/2155-9899.1000362
118. Fordham JB, Naqvi AR, Nares S, Regulation of miR-24, miR-30b, and miR-142-3p during macrophage and dendritic cell differentiation potentiates innate immunity. J Leukoc Biol 2015 98 195 207. doi: 10.1189/jlb.1A1014-519RR
119. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT, MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011 13 423 433. doi: 10.1038/ncb2210
120. Vickers KC, Rye KA, Tabet F, MicroRNAs in the onset and development of cardiovascular disease. Clin Sci (Lond) 2014 126 183 194. doi: 10.1042/CS20130203
121. Boon RA, Vickers KC, Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol 2013 33 186 192. doi: 10.1161/ATVBAHA.112.300139
122. Njock MS, Cheng HS, Dang LT, Nazari-Jahantigh M, Lau AC, Boudreau E, Roufaiel M, Cybulsky MI, Schober A, Fish JE, Endothelial cells suppress monocyte activation through secretion of extracellular vesicles containing antiinflammatory microRNAs. Blood 2015 125 3202 3212. doi: 10.1182/blood-2014-11-611046
123. Cheng HS, Fish JE, Neovascularization driven by MicroRNA delivery to the endothelium. Arterioscler Thromb Vasc Biol 2015 35 2263 2265. doi: 10.1161/ATVBAHA.115.306558
124. Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, Parathath S, van Gils JM, Rayner AJ, Chang AN, Suarez Y, Fernandez-Hernando C, Fisher EA, Moore KJ, Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 2011 121 2921 2931. doi: 10.1172/JCI57275
125. 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. doi: 10.1016/j.cell.2014.11.018
126. Gosselin D, Link VM, Romanoski CE, Fonseca GJ, Eichenfield DZ, Spann NJ, Stender JD, Chun HB, Garner H, Geissmann F, Glass CK, Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 2014 159 1327 1340. doi: 10.1016/j.cell.2014.11.023
127. Zigmond E, Varol C, Farache J, Elmaliah E, Satpathy AT, Friedlander G, Mack M, Shpigel N, Boneca IG, Murphy KM, Shakhar G, Halpern Z, Jung S, Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 2012 37 1076 1090. doi: 10.1016/j.immuni.2012.08.026
128. Grainger JR, Wohlfert EA, Fuss IJ, Bouladoux N, Askenase MH, Legrand F, Koo LY, Brenchley JM, Fraser ID, Belkaid Y, Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med 2013 19 713 721. doi: 10.1038/nm.3189