Monocyte and macrophage heterogeneity

Nature Reviews Immunology

Volumn 5, Issue 12, 2005, Pages 953-964

  Gordon, Siamon ^a   Taylor, Philip R ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1;

ALBERS SCHOENBERG DISEASE; CELL FUNCTION; CELL HETEROGENEITY; CELL LINEAGE; CELL MATURATION; CELL SUBPOPULATION; CENTRAL NERVOUS SYSTEM; CIRCULATION; DENDRITIC CELL; DEVELOPMENTAL STAGE; FUNCTIONAL ASSESSMENT; GENE MUTATION; GENETIC CONSERVATION; HUMAN; INFLAMMATION; INFLAMMATORY CELL; KUPFFER CELL; LANGERHANS CELL; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MAMMAL; MICROENVIRONMENT; MOLECULAR RECOGNITION; MONOCYTE; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; REVIEW; SPLEEN CELL; TARGET CELL;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; DENDRITIC CELLS; HUMANS; IMMUNE SYSTEM; MACROPHAGES; MICE; MONOCYTES; RATS; SPECIES SPECIFICITY;

EID: 28544446111     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1733     Document Type: Review

References (95)

1. Volkman, A. & Gowans, J. L. The origin of macrophages from human bone marrow in the rat. Br. J. Exp. Pathol. 46, 62-70 (1965).
2. van Furth, R. & Cohn, Z. A. The origin and kinetics of mononuclear phagocytes. J. Exp. Med. 128, 415-435 (1968).
3. Ebert, R. H. & Florey, H. W. The extravascular development of the monocyte observed in vivo. Brit. J. Exp. Pathol. 20, 342-356 (1939).
4. van Furth, R., Diesselhoff-den Dulk, M. M. & Mattie, H. Quantitative study on the production and kinetics of mononuclear phagocytes during an acute inflammatory reaction. J. Exp. Med. 138, 1314-1330 (1973).
5. Imhof, B. A. & Aurrand-Lions, M. Adhesion mechanisms regulating the migration of monocytes. Nature Rev. Immunol. 4, 432-444 (2004).
6. Passlick, B., Flieger, D. & Ziegler-Heitbrock, H. W. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74, 2527-2534 (1989). Characterization of antigenically distinct monocyte subsets in human peripheral blood.
7. + blood monocytes exhibits features of tissue macrophages. Eur. J. Immunol. 23, 2053-2058 (1993).
8. Weber, C. et al. Differential chemokine receptor expression and function in human monocyte subpopulations. J. Leukoc. Biol. 67, 699-704 (2000).
9. 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 α. J. Exp. Med. 179, 1109-1118 (1994).
10. + T cells. Int. Immunol. 13, 1571-1581 (2001).
11. Randolph, G. J., Beaulieu, S., Lebecque, S., Steinman, R. M. & Muller, W. A. Differentiation of monocytes into dendritic cells in a model of transendothdial trafficking. Science 282, 480-483 (1998).
12. + human peripheral-blood monocyte subset preferentially differentiates into DCs after endothelial reverse transmigration.
13. + monocytes. J. Exp. Med. 197, 1701-1707 (2003).
14. + blood monocytes. Eur. J. Immunol. 31, 48-56 (2001).
15. Grage-Griebenow, E., Flad, H. D. & Ernst, M. Heterogeneity of human peripheral blood monocyte subsets. J. Leukoc. Biol. 69, 11-20 (2001).
16. Palframan, R. T. 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. 194, 1361-1373 (2001).
17. Kuziel, W. A. et al. Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc. Natl Acad. Sci. USA 94, 12053-12058 (1997).
18. Kurihara, T., Warr, G., Loy, J. & Bravo, R. Defects in macrophage recruitment and host defense in mice lacking the CCR2 chemokine receptor. J. Exp. Med. 186, 1757-1762 (1997).
19. Lu, B. et al. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med. 187, 601-608 (1998).
20. Gu, L. et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol. Cell 2, 275-281 (1998).
21. Serbina, N. V., Salazar-Mather, T. P., Biron, C. A., Kuziel, W. A. & Pamer, E. G. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70 (2003).
22. Geissmann, F., Jung, S. & Littman, D. R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19, 71-82 (2003). The first modern functional characterization and cell-fate studies of mouse peripheral-blood monocyte subsets during steady-state conditions and inflammation.
23. Tedder, T. F., Steeber, D. A. & Pizcueta, P. L-selectin-deficient mice have impaired leukocyte recruitment into inflammatory sites. J. Exp. Med. 181, 2259-2264 (1995).
24. Rosen, S. D. Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22, 129-156 (2004).
25. Sunderkotter, C. et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 172, 4410-4417 (2004).
26. de Bruijn, M. F. et al. Distinct mouse bone marrow macrophage precursors identified by differential expression of ER-MP12 and ER-MP20 antigens. Eur. J. Immunol. 24, 2279-2284 (1994).
27. Randolph, G. J., Inaba, K., Robbiani, D. F., Steinman, R. M. & Muller, W. A. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11, 753-761 (1999).
28. Qu, C. et al. Role of CCR8 and other chemokine pathways in the migration of monocyte-derived dendritic cells to lymph nodes. J. Exp. Med. 200, 1231-1241 (2004). Suggestion that a third, intermediate monocyte phenotype in mouse peripheral blood might be an inflammatory monocyte that is prone to differentiate into DCs.
29. Ahuja, V., Miller, S. E. & Howell, D. N. Identification of two subpopulations of rat monocytes expressing disparate molecular forms and quantities of CD43. Cell. Immunol. 163, 59-69 (1995).
30. Chamorro, S. et al. Phenotypic characterization of monocyte subpopulations in the pig. Immunobiology 202, 82-93 (2000).
31. Chamorro, S. et al. Phenotypic and functional heterogeneity of porcine blood monocytes and its relation with maturation. Immunology 114, 63-71 (2005).
32. + monocytes into functional dendritic cells. Immunobiology 209, 57-65 (2004).
33. Gordon, S. Biology of the macrophage. J. Cell Sci. Suppl. 4, 267-286 (1986).
34. Gordon, S. The role of the macrophage in immune regulation. Res. Immunol. 149, 685-688 (1998).
35. Austyn, J. M. & Gordon, S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur. J. Immunol. 11, 805-815 (1981).
36. Dijkstra, C. D., Van Vliet, E., Dopp, E. A., van der Lelij, A. A. & Kraal, G. Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55, 23-30 (1985).
37. Kraal, G. & Janse, M. Marginal metallophilic cells of the mouse spleen identified by a monoclonal antibody. Immunology 58, 665-669 (1986).
38. Quinn, J. M. & Gillespie, M. T. Modulation of osteoclast formation. Biochem. Biophys. Res. Commun. 328, 739-745 (2005).
39. McCusker, K. & Hoidal, J. Characterization of scavenger receptor activity in resident human lung macrophages. Exp. Lung Res. 15, 651-661 (1989).
40. Palecanda, A. et al. Role of the scavenger receptor MARCO in alveolar macrophage binding of unopsonized environmental particles. J. Exp. Med. 189, 1497-1506 (1999).
41. Taylor, P. R. et al. The β-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169, 3876-3882 (2002).
42. Surh, C. D. & Sprent, J. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372, 100-103 (1994).
43. Tabe, H., Kawabata, I., Koba, R. & Homma, T. Cell dynamics in the germinal center of the human tonsil. Acta Otolaryngol. Suppl. 523, 64-67 (1996).
44. Smythies, L. E. et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115, 66-75 (2005).
45. van Furth, R., Diesselhoff-den Dulk, M. M., Sluiter, W. & Van Dissel, J. T. in Mononuclear Phagocytes: Characteristics, Physiology and Function (ed. van Furth, R.) 201-210 (Martinus Nijhoff, Dordrecht, 1985).
46. Merad, M. et al. Langerhans cells renew in the skin throughout life under steady-state conditions. Nature Immunol. 3, 1135-1141 (2002). Interesting demonstration of the differences in requirement for circulating precursors or local proliferation in the renewal of Langerhans cells during steady-state conditions and inflammation.
47. Kanitakis, J., Petruzzo, P. & Dubernard, J. M. Turnover of epidermal Langerhans' cells. N. Engl. J. Med. 351, 2661-2662 (2004).
48. Kurihara, N., Chenu, C., Miller, M., Civin, C. & Roodman, G. D. Identification of committed mononuclear precursors for osteoclast-like cells formed in long term human marrow cultures. Endocrinology 126, 2733-2741 (1990).
49. Udagawa, N. et al. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells. Proc. Natl Acad. Sci. USA 87, 7260-7264 (1990).
50. Matsuzaki, K. et al. Osteoclast differentiation factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochem. Biophys. Res. Commun. 246, 199-204 (1998).
51. Marks, S. C. Jr & Lane, P. W. Osteopetrosis, a new recessive skeletal mutation on chromosome 12 of the mouse. J. Hered. 67, 11-18 (1976).
52. Yoshida, H. et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345, 442-444 (1990).
53. Kong, Y. Y. et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397, 315-323 (1999).
54. Arai, F. et al. Commitment and differentiation of osteoclast precursor cells by the sequential expression of c-Fms and receptor activator of nuclear factor κB (RANK) receptors. J. Exp. Med. 190, 1741-1754 (1999).
55. Sawyer, R. T., Strausbauch, P. H. & Volkman, A. Resident macrophage proliferation in mice depleted of blood monocytes by strontium-89. Lab. Invest. 46, 165-170 (1982).
56. Tarling, J. D., Lin, H. S. & Hsu, S. Self-renewal of pulmonary alveolar macrophages: evidence from radiation chimera studies. J. Leukoc. Biol. 42, 443-446 (1987).
57. Matute-Bello, G. et al. Optimal timing to repopulation of resident alveolar macrophages with donor cells following total body irradiation and bone marrow transplantation in mice. J. Immunol. Methods 292, 25-34 (2004).
58. Thomas, E. D., Ramberg, R. E., Sale, G. E., Sparkes, R. S. & Golde, D. W. Direct evidence for a bone marrow origin of the alveolar macrophage in man. Science 192, 1016-1018 (1976).
59. Nakata, K. et al. Augmented proliferation of human alveolar macrophages after allogeneic bone marrow transplantation. Blood 93, 667-673 (1999).
60. Stanley E. 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. USA 91, 5592-5596 (1994).
61. Hamilton, J. A. GM-CSF in inflammation and autoimmunity. Trends Immunol. 23, 403-408 (2002).
62. Hickey, W. F. Leukocyte traffic in the central nervous system: the participants and their roles. Semin. Immunol. 11, 125-137 (1999).
63. Lawson, L. J., Perry, V. H. & Gordon, S. Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48, 405-415 (1992).
64. de Groot, C. J., Huppes, W., Sminia, T., Kraal, G. & Dijkstra, C. D. 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 (1992).
65. Kraal, G. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132, 31-74 (1992).
66. Taylor, P. R. et al. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23, 901-944 (2005).
67. van der Laan, L. J. et al. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J. Immunol. 162, 939-947 (1999).
68. Kang, Y. S. et al. SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int. Immunol. 15, 177-186 (2003).
69. Geijtenbeek, T. B. et al. Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo. Blood 100, 2908-2916 (2002).
70. Taylor, P. R. et al. Development of a specific system for targeting protein to metallophilic macrophages. Proc. Natl Acad. Sci. USA 101, 1963-1968 (2004).
71. Eloranta, M. L. & Alm, G. V. Splenic marginal metallophilic macrophages and marginal zone macrophages are the major interferon-α/ β producers in mice upon intravenous challenge with herpes simplex virus. Scand. J. Immunol. 49, 391-394 (1999).
72. van Furth, R. & Diesselhoff-den Dulk, M. M. Dual origin of mouse spleen macrophages. J. Exp. Med. 160, 1273-1283 (1984).
73. van Rooijen, N., Kors, N. & Kraal, G. Macrophage subset repopulation in the spleen: differential kinetics after liposome-mediated elimination. J. Leukoc. Biol. 45, 97-104 (1989).
74. Van Rooijen, N., Kors, N., van de Ende, M. & Dijkstra, C. D. Depletion and repopulation of macrophages in spleen and liver of rat after intravenous treatment with liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res. 260, 215-222 (1990).
75. Wijffels, J. F., de Rover, Z., Beelen, R. H., Kraal, G. & van Rooijen, N. Macrophage subpopulations in the mouse spleen renewed by local proliferation. Immunobiology 191, 52-64 (1994).
76. Witmer-Pack, M. D. et al. Identification of macrophages and dendritic cells in the osteopetrotic (op/op) mouse. J. Cell Sci. 104, 1021-1029 (1993).
77. Takahashi, K., Umeda, S., Shultz, L. D., Hayashi, S. & Nishikawa, S. Effects of macrophage colony-stimulating factor (M-CSF) on the development, differentiation, and maturation of marginal metallophilic macrophages and marginal zone macrophages in the spleen of osteopetrosis (op) mutant mice lacking functional M-CSF activity. J. Leukoc. Biol. 55, 581-588 (1994).
78. Cecchini, M. G. et al. Role of colony stimulating factor-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120, 1357-1372 (1994).
79. Crofton, R. W., Diesselhoff-den Dulk, M. M. & van Furth, R. The origin, kinetics, and characteristics of the Kupffer cells in the normal steady state. J. Exp. Med. 148, 1-17 (1978).
80. Naito, M., Hasegawa, G. & Takahashi, K. Development, differentiation, and maturation of Kupffer cells. Microsc. Res. Tech. 39, 350-364 (1997).
81. Bouwens, L., Baekeland, M., De Zanger, R. & Wisse, E. Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 6, 718-722 (1986).
82. Gordon, S. Alternative activation of macrophages. Nature Rev. Immunol. 3, 23-35 (2003).
83. Mosser, D. M. The many faces of macrophage activation. J. Leukoc. Biol. 73, 209-212 (2003).
84. Goerdt, S. & Orfanos, C. E. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10, 137-142 (1999).
85. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
86. Davies, J. R., Rudd, J. F., Fryer, T. D. & Weissberg, P. L. Targeting the vulnerable plaque: the evolving role of nuclear imaging. J. Nucl. Cardiol. 12, 234-246 (2005).
87. Aschoff, L. Das Reticulo-endotheliale System. Ergeb. Inn. Med. Kinderheilkd. 26, 1-118 (1924) (in German).
88. Lichanska, A. M. & Hume, D. A. Origins and functions of phagocytes in the embryo. Exp. Hematol. 28, 601-611 (2000).
89. Shepard, J. L. & Zon, L. I. Developmental derivation of embryonic and adult macrophages. Curr. Opin. Hematol. 7, 3-8 (2000).
90. Takahashi, K., Donovan, M. J., Rogers, R. A. & Ezekowitz, R. A. Distribution of murine mannose receptor expression from early embryogenesis through to adulthood. Cell Tissue Res. 292, 311-323 (1998).
91. Hughes, D. A. & Gordon, S. Expression and function of the type 3 complement receptor in tissues of the developing mouse. J. Immunol. 160, 4543-4552 (1998).
92. Hume, D. A., Monkley, S. J. & Wainwright, B. J. Detection of c-fms protooncogene in early mouse embryos by whole mount in situ hybridization indicates roles for macrophages in tissue remodelling. Br. J. Haematol. 90, 939-942 (1995).
93. Herbomel, P., Thisse, B. & Thisse, C. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735-3745 (1999).
94. Henderson, R. B., Hobbs, J. A., Mathies, M. & Hogg, N. Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 102, 328-335 (2003).
95. Taylor, P. R., Brown, G. D., Geldhof, A. B., Martinez-Pomares, L. & Gordon, S. Pattern recognition receptors and differentiation antigens define murine myeloid cell heterogeneity ex vivo. Eur. J. Immunol. 33, 2090-2097 (2003).