Blood monocytes and their subsets: Established features and open questions

Frontiers in Immunology

Volumn 6, Issue AUG, 2015, Pages

  Ziegler Heitbrock, Loems ^a  

^a ASKLEPIOS FACHKLINIKEN MÜNCHEN GAUTING   (Germany)

Author keywords

Classical monocytes; Intermediate monocytes; Monocyte subsets; Nomenclature; Non classical monocytes

Indexed keywords

ALPHA2 INTEGRIN; CD14 ANTIGEN; CD16 ANTIGEN; CD1C ANTIGEN; CD45 ANTIGEN; CD68 ANTIGEN; CELL SURFACE MARKER; GLUCOCORTICOID; GLYCOPROTEIN P 15095; MONOCLONAL ANTIBODY; THY 1 ANTIGEN; TRANSCRIPTOME;

CELL SUBPOPULATION; CLINICAL EFFECTIVENESS; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MEGAKARYOCYTE ERYTHROID PROGENITOR; MONOCYTE; MORPHOLOGY; NONHUMAN; ONTOGENY; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84941286399     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00423     Document Type: Review

References (71)

1. van Furth R, Cohn ZA. The origin and kinetics of mononuclear phagocytes. J Exp Med (1968) 128:415-35. doi: 10.1084/jem.128.3.415.
2. Tucker SB, Pierre RV, Jordon RE. Rapid identification of monocytes in a mixed mononuclear cell preparation. J Immunol Methods (1977) 14:267-9. doi:10.1016/0022-1759(77)90137-5.
3. UphoffCC, Drexler HG. Biology of monocyte-specific esterase. Leuk Lymphoma (2000) 39:257-70. doi:10.3109/10428190009065825.
4. Goud TJ, Schotte C, van Furth R. Identification and characterization of the monoblast in mononuclear phagocyte colonies grown in vitro. J Exp Med (1975) 142:1180-99. doi:10.1084/jem.142.5.1180.
5. Hettinger J, Richards DM, Hansson J, Barra MM, Joschko AC, Krijgsveld J, et al. Origin of monocytes and macrophages in a committed progenitor. Nat Immunol (2013) 14:821-30. doi:10.1038/ni.2638.
6. Klonz A, Wonigeit K, Pabst R, Westermann J. The marginal blood pool of the rat contains not only granulocytes, but also lymphocytes, NK-cells and monocytes: a second intravascular compartment, its cellular composition, adhesion molecule expression and interaction with the peripheral blood pool. Scand J Immunol (1996) 44:461-9. doi:10.1046/j.1365-3083.1996.d01-334.x.
7. Steppich B, Dayyani F, Gruber R, Lorenz R, Mack M, Ziegler-Heitbrock HWL. Selective mobilization of CD14(+)CD16(+) monocytes by exercise. Am J Physiol Cell Physiol (2000) 279:C578-86.
8. 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.
9. Shi C, Jia T, Mendez-Ferrer S, Hohl TM, Serbina NV, Lipuma L, et al. Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating toll-like receptor ligands. Immunity (2011) 34:590-601. doi:10.1016/j.immuni.2011.02.016.
10. Varol C, Landsman L, Fogg DK, Greenshtein L, Gildor B, Margalit R, et al. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med (2007) 204:171-80. doi:10.1084/jem.20061011.
11. Alexis N, Soukup J, Ghio A, Becker S. Sputum phagocytes from healthy individuals are functional and activated: a flow cytometric comparison with cells in bronchoalveolar lavage and peripheral blood. Clin Immunol (2000) 97:21-32. doi:10.1006/clim.2000.4911.
12. Frankenberger M, Eder C, Hofer TP, Heimbeck I, Skokann K, Kassner G, et al. Chemokine expression by small sputum macrophages in COPD. Mol Med (2011) 17:762-70. doi:10.2119/molmed.2010.00202.
13. Tamoutounour S, Guilliams M, Montanana Sanchis F, Liu H, Terhorst D, Malosse C, et al. Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity (2013) 39:925-38. doi:10.1016/j.immuni.2013.10.004.
14. Jakubzick C, Gautier EL, Gibbings SL, Sojka DK, Schlitzer A, Johnson TE, et al. Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity (2013) 39:599-610. doi:10.1016/j.immuni.2013.08.007.
15. Ziegler-Heitbrock HWL, Ulevitch RJ. CD14: cell surface receptor and differentiation marker. Immunol Today (1993) 14:121-5. doi:10.1016/0167-5699(93)90212-4.
16. Sunderkotter 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.
17. Drevets DA, Schawang JE, Mandava VK, Dillon MJ, Leenen PJ. Severe Listeria monocytogenes infection induces development of monocytes with distinct phenotypic and functional features. J Immunol (2010) 185:2432-41. doi:10.4049/jimmunol.1000486.
18. Schwarz H, Schmittner M, Duschl A, Horejs-Hoeck J. Residual endotoxin contaminations in recombinant proteins are sufficient to activate human CD1c+ dendritic cells. PLoS One (2014) 9:e113840. doi:10.1371/journal.pone.0113840.
19. Ziegler-Heitbrock HWL, Pechumer H, Petersmann I, Durieux JJ, Vita N, Labeta MO, et al. CD14 is expressed and functional in human B cells. Eur J Immunol (1994) 24:1937-40. doi:10.1002/eji.1830240835.
20. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol (2012) 13:1118-28. doi:10.1038/ni.2419.
21. Steinman RM, Cohn ZA. Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med (1973) 137:1142-62. doi:10.1084/jem.137.5.1142.
22. Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, et al. A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science (2006) 311:83-7. doi:10.1126/science.1117729.
23. Sathe P, Metcalf D, Vremec D, Naik SH, Langdon WY, Huntington ND, et al. Lymphoid tissue and plasmacytoid dendritic cells and macrophages do not share a common macrophage-dendritic cell-restricted progenitor. Immunity (2014) 41:104-15. doi:10.1016/j.immuni.2014.05.020.
24. Onai N, Ohteki T. Bipotent or oligopotent? A macrophage and DC progenitor revisited. Immunity (2014) 41:5-7. doi:10.1016/j.immuni.2014.07.004.
25. Sallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med (1994) 179:1109-18. doi:10.1084/jem.179.4.1109.
26. Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G, et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol (2008) 9:R17. doi:10.1186/gb-2008-9-1-r17.
27. Randolph GJ, Inaba K, Robbiani DF, Steinman RM, Muller WA. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity (1999) 11:753-61. doi:10.1016/S1074-7613(00)80149-1.
28. Landsman L, Varol C, Jung S. Distinct differentiation potential of blood monocyte subsets in the lung. J Immunol (2007) 178:2000-7. doi:10.4049/jimmunol.178.4.2000.
29. Strobl H, Scheinecker C, Riedl E, Csmarits B, Bello-Fernandez C, Pickl WF, et al. Identification of CD68+lin-peripheral blood cells with dendritic precursor characteristics. J Immunol (1998) 161:740-8.
30. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, et al. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol (2000) 165:6037-46. doi:10.4049/jimmunol.165.11.6037.
31. Frankenberger M, Hofer TP, Marei A, Dayyani F, Schewe S, Strasser C, et al. Transcript profiling of CD16-positive monocytes reveals a unique molecular fingerprint. Eur J Immunol (2012) 42:957-74. doi:10.1002/eji.201141907.
32. Debili N, Coulombel L, Croisille L, Katz A, Guichard J, Breton-Gorius J, et al. Characterization of a bipotent erythro-megakaryocytic progenitor in human bone marrow. Blood (1996) 88:1284-96.
33. Klimchenko O, Mori M, Distefano A, Langlois T, Larbret F, Lecluse Y, et al. A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis. Blood (2009) 114:1506-17. doi:10.1182/blood-2008-09-178863.
34. Macaulay IC, Tijssen MR, Thijssen-Timmer DC, Gusnanto A, Steward M, Burns P, et al. Comparative gene expression profiling of in vitro differentiated megakaryocytes and erythroblasts identifies novel activatory and inhibitory platelet membrane proteins. Blood (2007) 109:3260-9. doi:10.1182/blood-2006-07-036269.
35. Norris DA, Morris RM, Sanderson RJ, Kohler PF. Isolation of functional subsets of human peripheral blood monocytes. J Immunol (1979) 123:166-72.
36. Zembala M, Uracz W, Ruggiero I, Mytar B, Pryjma J. Isolation and functional characteristics of FcR+ and FcR-human monocyte subsets. J Immunol (1984) 133:1293-9.
37. Passlick B, Flieger D, Ziegler-Heitbrock HWL. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood (1989) 74:2527-34.
38. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, et al. Nomenclature of monocytes and dendritic cells in blood. Blood (2010) 116:e74-80. doi:10.1182/blood-2010-02-258558.
39. Ziegler-Heitbrock L, Hofer TP. Toward a refined definition of monocyte subsets. Front Immunol (2013) 4:23. doi:10.3389/fimmu.2013.00023.
40. Rogacev KS, Cremers B, Zawada AM, Seiler S, Binder N, Ege P, et al. CD14++CD16+ monocytes independently predict cardiovascular events: a cohort study of 951 patients referred for elective coronary angiography. J Am Coll Cardiol (2012) 60:1512-20. doi:10.1016/j.jacc.2012.07.019.
41. Wong KL, Yeap WH, Tai JJ, Ong SM, Dang TM, Wong SC. The three human monocyte subsets: implications for health and disease. Immunol Res (2012) 53:41-57. doi:10.1007/s12026-012-8297-3.
42. Ziegler-Heitbrock L. Monocyte subsets in man and other species. Cell Immunol (2014) 289:135-9. doi:10.1016/j.cellimm.2014.03.019.
43. Kim WK, Sun Y, Do H, Autissier P, Halpern EF, Piatak M Jr, et al. Monocyte heterogeneity underlying phenotypic changes in monocytes according to SIV disease stage. J Leukoc Biol (2010) 87:557-67. doi:10.1189/jlb.0209082.
44. Kwissa M, Nakaya HI, Oluoch H, Pulendran B. Distinct TLR adjuvants differentially stimulate systemic and local innate immune responses in nonhuman primates. Blood (2012) 119:2044-55. doi:10.1182/blood-2011-10-388579.
45. Ingersoll MA, Spanbroek R, Lottaz C, Gautier EL, Frankenberger M, Hoffmann R, et al. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood (2010) 115:e10-9. doi:10.1182/blood-2009-07-235028.
46. de Baey A, Mende I, Riethmueller G, Baeuerle PA. Phenotype and function of human dendritic cells derived from M-DC8(+) monocytes. Eur J Immunol (2001) 31:1646-55. doi:10.1002/1521-4141(200106)31:6<1646::AID-IMMU1646>3.0.CO;2-X.
47. Schakel K, Kannagi R, Kniep B, Goto Y, Mitsuoka C, Zwirner J, et al. 6-Sulfo LacNAc, a novel carbohydrate modification of PSGL-1, defines an inflammatory type of human dendritic cells. Immunity (2002) 17:289-301. doi:10.1016/S1074-7613(02)00393-X.
48. Thomas K, Dietze K, Wehner R, Metz I, Tumani H, Schultheiss T, et al. Accumulation and therapeutic modulation of 6-sulfo LacNAc(+) dendritic cells in multiple sclerosis. Neurol Neuroimmunol Neuroinflamm (2014) 1:e33. doi:10.1212/NXI.0000000000000033.
49. Belge KU, Dayyani F, Horelt A, Siedlar M, Frankenberger M, Frankenberger B, et al. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J Immunol (2002) 168:3536-42. doi:10.4049/jimmunol.168.7.3536.
50. Fingerle-Rowson G, Angstwurm M, Andreesen R, Ziegler-Heitbrock HWL. Selective depletion of CD14+ CD16+ monocytes by glucocorticoid therapy. Clin Exp Immunol (1998) 112:501-6. doi:10.1046/j.1365-2249.1998.00617.x.
51. Dutertre CA, Amraoui S, DeRosa A, Jourdain JP, Vimeux L, Goguet M, et al. Pivotal role of M-DC8(+) monocytes from viremic HIV-infected patients in TNFalpha overproduction in response to microbial products. Blood (2012) 120:2259-68. doi:10.1182/blood-2012-03-418681.
52. Siedlar M, Frankenberger M, Ziegler-Heitbrock LH, Belge KU. The M-DC8-positive leukocytes are a subpopulation of the CD14+ CD16+ monocytes. Immunobiology (2000) 202:11-7. doi:10.1016/S0171-2985(00)80047-9.
53. Cros J, Cagnard N, Woollard K, Patey N, Zhang SY, Senechal B, et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity (2010) 33:375-86. doi:10.1016/j.immuni.2010.08.012.
54. Wong KL, Tai JJ, Wong WC, Han H, Sem X, Yeap WH, et al. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood (2011) 118:e16-31. doi:10.1182/blood-2010-12-326355.
55. Maurer D, Fiebiger E, Reininger B, Wolff-Winiski B, Jouvin MH, Kilgus O, et al. Expression of functional high affinity immunoglobulin E receptors (Fc epsilon RI) on monocytes of atopic individuals. J Exp Med (1994) 179:745-50. doi:10.1084/jem.179.2.745.
56. Dehlink E, Baker AH, Yen E, Nurko S, Fiebiger E. Relationships between levels of serum IgE, cell-bound IgE, and IgE-receptors on peripheral blood cells in a pediatric population. PLoS One (2010) 5:e12204. doi:10.1371/journal.pone.0012204.
57. Greer AM, Wu N, Putnam AL, WoodruffPG, Wolters P, Kinet JP, et al. Serum IgE clearance is facilitated by human FcepsilonRI internalization. J Clin Invest (2014) 124:1187-98. doi:10.1172/JCI68964.
58. Clanchy FI, Holloway AC, Lari R, Cameron PU, Hamilton JA. Detection and properties of the human proliferative monocyte subpopulation. J Leukoc Biol (2006) 79:757-66. doi:10.1189/jlb.0905522.
59. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A. Circulating fibrocytes define a new leukocyte subpopulation that mediates tissue repair. Mol Med (1994) 1:71-81.
60. Komano Y, Nanki T, Hayashida K, Taniguchi K, Miyasaka N. Identification of a human peripheral blood monocyte subset that differentiates into osteoclasts. Arthritis Res Ther (2006) 8:R152. doi:10.1186/ar2046.
61. Fingerle G, Pforte A, Passlick B, Blumenstein M, Strobel M, Ziegler-Heitbrock HWL. The novel subset of CD14+/CD16+ blood monocytes is expanded in sepsis patients. Blood (1993) 82:3170-6.
62. Horelt A, Belge KU, Steppich B, Prinz J, Ziegler-Heitbrock L. The CD14+CD16+ monocytes in erysipelas are expanded and show reduced cytokine production. Eur J Immunol (2002) 32:1319-27. doi:10.1002/1521-4141(200205)32:5<1319::AID-IMMU1319>3.0.CO;2-2.
63. Shalova IN, Kajiji T, Lim JY, Gomez-Pina V, Fernandez-Ruiz I, Arnalich F, et al. CD16 regulates TRIF-dependent TLR4 response in human monocytes and their subsets. J Immunol (2012) 188:3584-93. doi:10.4049/jimmunol.1100244.
64. Fingerle-Rowson G, Auers J, Kreuzer E, Fraunberger P, Blumenstein M, Ziegler-Heitbrock LH. Expansion of CD14+CD16+ monocytes in critically ill cardiac surgery patients. Inflammation (1998) 22:367-79. doi:10.1023/A:1022316815196.
65. Dayyani F, Belge KU, Frankenberger M, Mack M, Berki T, Ziegler-Heitbrock L. Mechanism of glucocorticoid-induced depletion of human CD14+CD16+ monocytes. J Leukoc Biol (2003) 74:33-9. doi:10.1189/jlb.1202612.
66. Korkosz M, Bukowska-Strakova K, Sadis S, Grodzicki T, Siedlar M. Monoclonal antibodies against macrophage colony-stimulating factor diminish the number of circulating intermediate and nonclassical (CD14(++)CD16(+)/CD14(+)CD16(++)) monocytes in rheumatoid arthritis patient. Blood (2012) 119:5329-30. doi:10.1182/blood-2012-02-412551.
67. MacDonald KP, Palmer JS, Cronau S, Seppanen E, Olver S, Raffelt NC, et al. An antibody against the colony-stimulating factor 1 receptor depletes the resident subset of monocytes and tissue-and tumor-associated macrophages but does not inhibit inflammation. Blood (2010) 116:3955-63. doi:10.1182/blood-2010-02-266296.
68. Lenzo JC, Turner AL, Cook AD, Vlahos R, Anderson GP, Reynolds EC, et al. Control of macrophage lineage populations by CSF-1 receptor and GM-CSF in homeostasis and inflammation. Immunol Cell Biol (2012) 90:429-40. doi:10.1038/icb.2011.58.
69. Frankenberger M, Ekici AB, Angstwurm MW, Hoffmann H, Hofer TP, Heimbeck I, et al. A defect of CD16-positive monocytes can occur without disease. Immunobiology (2013) 218:169-74. doi:10.1016/j.imbio.2012.02.013.
70. Heine GH, Ortiz A, Massy ZA, Lindholm B, Wiecek A, Martinez-Castelao A, et al. Transplant, monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat Rev Nephrol (2012) 8:362-9. doi:10.1038/nrneph.2012.41.
71. Rogacev KS, Zawada AM, Emrich I, Seiler S, Bohm M, Fliser D, et al. Lower Apo A-I and lower HDL-C levels are associated with higher intermediate CD14++CD16+ monocyte counts that predict cardiovascular events in chronic kidney disease. Arterioscler Thromb Vasc Biol (2014) 34:2120-7. doi:10.1161/ATVBAHA.114.304172.