Redefining myeloid cell subsets in murine spleen

Frontiers in Immunology

Volumn 6, Issue JAN, 2016, Pages

  Hey, Ying Ying ^a   Tan, Jonathan K H ^b   O'Neill, Helen C ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b BOND UNIVERSITY   (Australia)

Author keywords

Dendritic cells; Monocytes; Myeloid cells; Spleen

Indexed keywords

CD11B ANTIGEN; CD135 ANTIGEN; CD19 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; COLONY STIMULATING FACTOR; FLUORESCEIN ISOTHIOCYANATE; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GREEN FLUORESCENT PROTEIN; LEUKOSIALIN; LYMPHOCYTE ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SIGLEC F ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL FRACTIONATION; CELL MATURATION; CELL SELECTION; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; EOSINOPHIL; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; INFLAMMATORY CELL; MOUSE; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; SPLEEN; SPLEEN CELL;

EID: 84958178339     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00652     Document Type: Article

References (80)

1. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature (2000) 404:193-7. doi:10.1038/35004599
2. Hickey MJ, Kubes P. Intravascular immunity: the host-pathogen encounter in blood vessels. Nat Rev Immunol (2009) 9:364-75. doi:10.1038/nri2532
3. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science (2007) 317:666-70. doi:10.1126/science.1142883
4. Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG. Identification of clonogenic common Fllt3+M-CSFR+ plasmactyoid and conventional dendritic cell progneitors in mouse bone marrow. Nat Immunol (2007) 8:1207-16. doi:10.1038/ni1518
5. Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Daic A, et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol (2007) 8:1217-26. doi:10.1038/ni1522
6. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol (2005) 5:953-64. doi:10.1038/nri1733
7. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity (2003) 19:71-82. doi:10.1016/S1074-7613(03)00174-2
8. Carlin LM, Stamatiades EG, Auffray C, Hanna RN, Glover L, Vizcay-Barrena G, et al. Nr4a1-dependent Ly6C(low) monocytes monitor endothelial cells and orchestrate their disposal. Cell (2013) 153:362-75. doi:10.1016/j.cell.2013.03.010
9. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med (2007) 204:3037-47. doi:10.1084/jem.20070885
10. Sunderkötter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol (2004) 172:4410-7. doi:10.4049/jimmunol.172.7.4410
11. Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest (2007) 117:185-94. doi:10.1172/JCI28549
12. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science (2010) 330:841-5. doi:10.1126/science.1194637
13. Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, et al. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med (2013) 210:1977-92. doi:10.1084/jem.20131199
14. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity (2013) 38:792-804. doi:10.1016/j.immuni.2013.04.004
15. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science (2012) 336:86-90. doi:10.1126/science.1219179
16. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science (2009) 325:612-6. doi:10.1126/science.1175202
17. Rose S, Misharin A, Perlman H. A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A (2012) 81 A:343-50. doi:10.1002/cyto.a.22012
18. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol (2011) 12:1035-44. doi:10.1038/ni.2109
19. Voehringer D, Van Rooijen N, Locksley RM. Eosinophils develop in distinct stages and are recruited to peripheral sites by alternatively activated macrophages. J Leukoc Biol (2007) 81:1434-44. doi:10.1189/jlb.1106686
20. Heath WR, Belz GT, Behrens GMN, Smith CM, Forehan SP, Parish IA, et al. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev (2004) 199:9-26. doi:10.1111/j.0105-2896.2004.00142.x
21. Naik SH. Demystifying the development of dendritic cell subtypes, a little. Immunol Cell Biol (2008) 86:439-52. doi:10.1038/icb.2008.28
22. Vremec D, Pooley J, Hochrein H, Wu L, Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol (2000) 164:2978-86. doi:10.4049/jimmunol.164.6.2978
23. Hochrein H, Shortman K, Vremec D, Scott B, Hertzog P, O'Keeffe M. Differential production of IL-12, IFN-a, and IFN-β by mouse dendritic cell subsets. J Immunol (2001) 166:5448-55. doi:10.4049/jimmunol.166.9.5448
24. Pelayo R, Hirose J, Huang J, Garrett KP, Delogu A, Busslinger M, et al. Derivation of 2 categories of plasmacytoid dendritic cells in murine bone marrow. Blood (2005) 105:4407-15. doi:10.1182/blood-2004-07-2529
25. Geissmann F, Auffray C, Palframan R, Wirrig C, Ciocca A, Campisi L, et al. Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol (2008) 86:398-408. doi:10.1038/icb.2008.19
26. León B, López-Bravo M, Ardavín C. Monocyte-derived dendritic cells. Semin Immunol (2005) 17:313-8. doi:10.1016/j.smim.2005.05.013
27. León B, López-Bravo M, Ardavín C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity (2007) 26:519-31. doi:10.1016/j.immuni.2007.01.017
28. Quah B, Ni K, O'Neill HC. In vitro hematopoiesis produces a distinct class of immature dendritic cells from spleen progenitors with limited T cell stimulation capacity. Int Immunol (2004) 16:567-77. doi:10.1093/intimm/dxh060
29. Wilson HL, Ni K, O'Neill HC. Identification of progenitor cells in long-term spleen stromal cultures that produce immature dendritic cells. Proc Natl Acad Sci U S A (2000) 97:4784-9. doi:10.1073/pnas.080278897
30. Wilson NS, El-Sukkari D, Villadangos JA. Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood (2004) 103:2187-95. doi:10.1182/blood-2003-08-2729
31. Periasamy P, Tan JKH, Griffiths KL, O'Neill HC. Splenic stromal niches support hematopoiesis of dendritic-like cells from precursors in bone marrow and spleen. Exp Hematol (2009) 37:1060-71. doi:10.1016/j.exphem.2009.06.001
32. Petvises S, O'Neill HC. Characterisation of dendritic cells arising from progenitors endogenous to murine spleen. PLoS One (2014) 9(2):e88311. doi:10.1371/journal.pone.0088311
33. Periasamy P, O'Neill HC. Stroma-dependent development of two dendritic-like cell types with distinct antigen presenting capability. Exp Hematol (2013) 41:281-92. doi:10.1016/j.exphem.2012.11.003
34. Xu Y, Zhan Y, Lew AM, Naik SH, Kershaw MH. Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J Immunol (2007) 179:7577-84. doi:10.4049/jimmunol.179.11.7577
35. Petvises S, Talaulikar D, O'Neill HC. Delineation of a novel dendritic-like subset in human spleen. Cell Mol Immunol (2015). doi:10.1038/cmi.2015.16
36. Tan JKH, Quah BJC, Griffiths KL, Periasamy P, Hey YY, O'Neill HC. Identification of a novel antigen cross-presenting cell type in spleen. J Cell Mol Med (2011) 15:1189-99. doi:10.1111/j.1582-4934.2010.01089.x
37. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, Dezutter-Dambuyant C, et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol (2001) 2:1144-50. doi:10.1038/ni736
38. Björck P. Isolation and characterization of plasmacytoid dendritic cells from Flt3 ligand and granulocyte-macrophage colony-stimulating factor-treated mice. Blood (2001) 98:3520-6. doi:10.1182/blood. V98.13.3520
39. Nakano H, Yanagita M, Gunn MD. CD11c+B220+Gr-1+ cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med (2001) 194:1171-8. doi:10.1084/jem.194.8.1171
40. Jaiswal H, Kaushik M, Sougrat R, Gupta M, Dey A, Verma R, et al. Batf3 and Id2 have a synergistic effect on Irf8-directed classical CD8a+ dendritic cell development. J Immunol (2013) 191:5993-6001. doi:10.4049/jimmunol.1203541
41. Tussiwand R, Lee WL, Murphy TL, Mashayekhi M, Kc W, Albring JC, et al. Compensatory dendritic cell development mediated by BATF-IRF interactions. Nature (2012) 490:502-7. doi:10.1038/nature11531
42. Auffray C, Sieweke MH, Geissmann F. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol (2009) 27:669-92. doi:10.1146/annurev.immunol.021908.132557
43. Dai XM, Ryan GR, Hapel AJ, Dominguez MG, Russell RG, Kapp S, et al. 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) 99:111-20. doi:10.1182/blood. V99.1.111
44. Sasmono RT, Oceandy D, Pollard JW, Tong W, Pavli P, Wainwright BJ, et al. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse. Blood (2003) 101:1155-63. doi:10.1182/blood-2002-02-0569
45. Dunay IR, Fuchs A, David Sibley L. Inflammatory monocytes but not neutrophils are necessary to control infection with Toxoplasma gondii in mice. Infect Immun (2010) 78:1564-70. doi:10.1128/IAI.00472-09
46. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, et al. A clonogenic bone harrow progenitor specific for macrophages and dendritic cells. Science (2006) 311:83-7. doi:10.1126/science.1117729
47. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, et al. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol (2000) 20:4106-14. doi:10.1128/MCB.20.11.4106-4114.2000
48. Palframan RT, Jung S, Cheng G, Weninger W, Luo Y, Dorf M, et al. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J Exp Med (2001) 194:1361-73. doi:10.1084/jem.194.9.1361
49. Auffray C, Fogg DK, Narni-Mancinelli E, Senechal B, Trouillet C, Saederup N, et al. CX 3CR1 + CD115 + CD135 + common macrophage/DC precursors and the role of CX 3CR1 in their response to inflammation. J Exp Med (2009) 206:595-606. doi:10.1084/jem.20081385
50. Bar-On L, Birnberg T, Lewis KL, Edelson BT, Bruder D, Hildner K, et al. CX3CR1+ CD8a+ dendritic cells are a steady-state population related to plasmacytoid dendritic cells. Proc Natl Acad Sci U S A (2010) 107:14745-50. doi:10.1073/pnas.1001562107
51. Hildner K, Edelson BT, Purtha WE, Diamond M, Matsushita H, Kohyama M, et al. Batf3 deficiency reveals a critical role for CD8a+ dendritic cells in cytotoxic T cell immunity. Science (2008) 322:1097-100. doi:10.1126/science.1164206
52. Murphy TL, Tussiwand R, Murphy KM. Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks. Nat Rev Immunol (2013) 13:499-509. doi:10.1038/nri3470
53. Satpathy AT, Wu X, Albring JC, Murphy KM. Re(de)fining the dendritic cell lineage. Nat Immunol (2012) 13:1145-54. doi:10.1038/ni.2467
54. McKenna HJ, Stocking KL, Miller RE, Brasel K, De Smedt T, Maraskovsky E, et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood (2000) 95:3489-97.
55. Maraskovsky E, Brasel K, Teepe M, Roux ER, Lyman SD, Shortman K, et al. Dramatic increase in the number of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med (1996) 184:1953-62. doi:10.1084/jem.184.5.1953
56. Pulendran B, Lingappa J, Kennedy MK, Smith J, Teepe M, Rudensky A, et al. Developmental pathways of dendritic cells in vivo: distinct function, phenotype, and localization of dendritic cell subsets in FLT3 ligand-treated mice. J Immunol (1997) 159:2222-31.
57. Shurin MR, Pandharipande PP, Zorina TD, Haluszczak C, Subbotin VM, Hunter O, et al. FLT3 ligand induces the generation of functionally active dendritic cells in mice. Cell Immunol (1997) 179:174-84. doi:10.1006/cimm.1997.1152
58. Beaudin AE, Boyer SW, Forsberg EC. Flk2/Flt3 promotes both myeloid and lymphoid development by expanding non-self-renewing multipotent hematopoietic progenitor cells. Exp Hematol (2014) 42:218-29. doi:10.1016/j.exphem.2013.11.013
59. Karsunky H, Merad M, Cozzio A, Weissman IL, Manz MG. Flt3 ligand regulates dendritic cell development from Flt3+ lymphoid and myeloid-committed progenitors to Flt3+ dendritic cells in vivo. J Exp Med (2003) 198:305-13. doi:10.1084/jem.20030323
60. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol (2008) 26:421-52. doi:10.1146/annurev.immunol.26.021607.090326
61. Berthier R, Martinon-Ego C, Laharie AM, Marche PN. A two-step culture method starting with early growth factors permits enhanced production of functional dendritic cells from murine splenocytes. J Immunol Methods (2000) 239:95-107. doi:10.1016/S0022-1759(00)00186-1
62. Inaba K, Inaba M, Deguchi M, Hagi K, Yasumizu R, Ikehara S, et al. Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class II-negative progenitor in mouse bone marrow. Proc Natl Acad Sci U S A (1993) 90:3038-42. doi:10.1073/pnas.90.7.3038
63. Kingston D, Schmid MA, Onai N, Obata-Onai A, Baumjohann D, Manz MG. The concerted action of GM-CSF and Flt3-ligand on in vivo dendritic cell homeostasis. Blood (2009) 114:835-43. doi:10.1182/blood-2009-02-206318
64. Vremec D, Lieschke GJ, Dunn AR, Robb L, Metcalf D, Shortman K. The influence of granulocyte/macrophage colony-stimulating factor on dendritic cell levels in mouse lymphoid organs. Eur J Immunol (1997) 27:40-4. doi:10.1002/eji.1830270107
65. Guilliams M, Ginhoux F, Jakubzick C, Naik SH, Onai N, Schraml BU, et al. Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol (2014) 14:571-8. doi:10.1038/nri3712
66. Bochner BS. Siglec-8 on human eosinophils and mast cells, and Siglec-F on murine eosinophils, are functionally related inhibitory receptors. Clin Exp Allergy (2009) 39:317-24. doi:10.1111/j.1365-2222.2008.03173.x
67. Guo JP, Nutku E, Yokoi H, Schnaar RL, Zimmermann N, Bochner BS. Siglec-8 and siglec-F: inhibitory receptors on eosinophils, basophils, and mast cells. Allergy Clin Immunol Int (2007) 19:54-9. doi:10.1027/0838-1925.19.2.54
68. Domínguez PM, Ardavín C. Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol Rev (2010) 234:90-104. doi:10.1111/j.0105-2896.2009.00876.x
69. Mori Y, Iwasaki H, Kohno K, Yoshimoto G, Kikushige Y, Okeda A, et al. Identification of the human eosinophil lineage-committed progenitor: revision of phenotypic definition of the human common myeloid progenitor. J Exp Med (2009) 206:183-93. doi:10.1084/jem.20081756
70. Langerhans P. Uber die nerven der menschlichen haut. Arch Pathol Anat (1868) 44:325-37. doi:10.1007/BF01959006
71. Silberberg I. Apposition of mononuclear cells to langerhans cells in contact allergic reactions. An ultrastructural study. Acta Derm Venereol (1973) 53:1-12.
72. Hinton R, O'Neill H. Extramedullary hematopoiesis leading to the production of a novel antigen presenting cell type in murine spleen. Int J Med Biol Front (2012) 18:569-81.
73. Petvises S, O'Neill HC. Distinct progenitor origin distinguishes a lineage of dendritic-like cells in spleen. Front Immunol (2014) 4:501. doi:10.3389/fimmu.2013.00501
74. Liu K, Victora GD, Schwickert TA, Guermonprez P, Meredith MM, Yao K, et al. In vivo analysis of dendritic cell development and homeostasis. Science (2009) 324:392-7. doi:10.1126/science.1170540
75. Kurachi M, Barnitz RA, Yosef N, Odorizzi PM, DiIorio MA, Lemieux ME, et al. The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+ T cells. Nat Immunol (2014) 15(4):373-83. doi:10.1038/ni.2834
76. Schraml BU, Hildner K, Ise W, Lee WL, Smith WAE, Solomon B, et al. The AP-1 transcription factor Batf controls T H 17 differentiation. Nature (2009) 460:405-9. doi:10.1038/nature08114
77. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature (2006) 441:235-8. doi:10.1038/nature04753
78. Brüstle A, Heink S, Huber M, Rosenplänter C, Stadelmann C, Yu P, et al. The development of inflammatory TH-17 cells requires interferon-regulatory factor 4. Nat Immunol (2007) 8:958-66. doi:10.1038/ni1500
79. Waskow C, Liu K, Darrasse-Jèze G, Guermonprez P, Ginhoux F, Merad M, et al. The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat Immunol (2008) 9:676-83. doi:10.1038/ni.1615
80. Stanley E, Lieschke GJ, Grail D, Metcalf D, Hodgson G, Gall JAM, et al. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc Natl Acad Sci U S A (1994) 91:5592-6. doi:10.1073/pnas.91.12.5592