Macrophages of the splenic marginal zone are essential for trapping of blood-borne particulate antigen but dispensable for induction of specific T cell responses

Journal of Immunology

Volumn 171, Issue 3, 2003, Pages 1148-1155

  Aichele, Peter ^a,b   Zinke, Jana ^a   Grode, Leander ^a   Schwendener, Reto A ^b,c   Kaufmann, Stefan H E ^a   Seiler, Peter ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c PAUL SCHERRER INSTITUTE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; MICROSPHERE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ANTIGEN PRESENTATION; ARTICLE; CELL POPULATION; CELL TYPE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEPLETION; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOSTIMULATION; INFECTION CONTROL; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; SPLEEN MARGINAL ZONE; T LYMPHOCYTE ACTIVATION;

EID: 0042847262     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.3.1148     Document Type: Article

References (74)

1. Kraal, G. 1992. Cells in the marginal zone of the spleen. Int. Rev. Cytol. 132:31.
2. Moghimi, S. M. 1995. Mechanisms of splenic clearance of blood cells and particles: towards development of new splenotropic agents. Adv. Drug Deliv. Rev. 17:103.
3. Weiss, L. 1990. Mechanisms of splenic clearance of the blood; a structural overview of the mammalian spleen. In Spleen, Structure, Function and Clinical Significance. A. J. Bowdler, ed. Chapman and Hall Medical, London, pp. 23-43.
4. Dijkstra, C. D., E. Van Vliet, E. A. Dopp, A. A. Van der Lelij, and G. Kraal. 1985. Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55:23.
5. Humphrey, J. H., and D. G. Grennan. 1981. Different macrophage populations distinguished by means of fluorescent polysaccharides. Eur. J. Immunol. 11:211.
6. Snook, T. 1964. Studies on the perifollicular region of the rat's spleen. Anat. Rec. 148:149.
7. Kraal, G., and M. Janse. 1986. Marginal metallophilic cells of the mouse spleen identified by a monoclonal antibody. Immunology 58:665.
8. Groeneveld, P. H. P., and N. van Rooijen. 1985. Localization of intravenously injected lipopolysaccharide (LPS) in the spleen of the mouse. Virchows Arch. 48:237.
9. Harms, G., M. J. Hardonk, and W. Timens. 1996. In vitro complement-dependent binding and in vivo kinetics of pneumococcal polysaccharide TI-2 antigens in the rat spleen marginal zone and follicle. Infect. Immun. 64:4220.
10. Uchiyama, J., H. Kuniki, Y. Fujikura, T. Fukumoto, and A. Koshiro. 1991. Analysis of K. pneumoniae by monoclonal antibody: immunohistochemical detection of K. pneumoniae surface antigen injected into mice and rats. Immunobiology 184:63.
11. Kraal, G., H. H. Ter, C. Meelhuizen, G. Venneker, and E. Claassen. 1989. Marginal zone macrophages and their role in the immune response against T-independent type 2 antigens: modulation of the cells with specific antibody. Eur. J. Immunol. 19:675.
12. Van den Eertwegh, A. J. M., J. D. Laman, W. J. A. Boersma, and E. Claassen. 1992. Complement-mediated follicular localization of T-independent type-2 antigens: the role of marginal zone macrophages revisited. Eur. J. Immunol. 22:719.
13. Demoy, M. J. P. Andreux, C. Weingarten, B. Gouritin, V. Guilloux, and P. Couvreur. 1999. Spleen capture of nanoparticles: influence of animal species and surface characteristics. Pharm. Res. 16:37.
14. Demoy, M., S. Gibaud, J. P. Andreux, C. Weingarten, B. Gouritin, and P. Couvreur. 1997. Splenic trapping of nanoparticles: complementary approaches for in situ studies. Pharm. Res. 14:463.
15. Matsuno, K., H. Fujii, and M. Kotani. 1986. Splenic marginal zone macrophages and marginal metallophils in rats and mice. Cell Tissue Res. 246:263.
16. Claassen, E. 1992. Post-formation fluorescent labelling of liposomal membranes. J. Immunol. Methods 147:231.
17. Hughes, D. A., I. P. Fraser, and S. Gordon. 1995. Murine macrophage scavenger receptor: in vivo expression and function as receptor for macrophage adhesion in lymphoid and non-lymphoid organs. Eur. J. Immunol. 25:466.
18. Buiting, A. M. J., Z. DeRover, E. Claassen, and N. van Rooijen. 1993. In vivo distribution of particulate antigens and liposomes in murine spleen: a possible role in the humoral immune response. Immunobiology 188:13.
19. Kanabe, T., M. A. Jutila, and J. E. Cutler. 1992. Evidence that Candida albicans binds via a unique adhesion system on phagocytic cells in the marginal zone of the mouse spleen. Infect. Immun. 60:1972.
20. Bachmann, M. F., T. M. Kündig, B. Odermatt, H. Hengartner, and R. M. Zinkernagel. 1994. Free recirculation of memory B cells versus antigen-dependent differentiation to antibody forming cells. J. Immunol. 153:3386.
21. van Rooijen, N., and R. van Nieuwmegen. 1984. Elimination of phagocytic cells in the spleen after intravenous injection of liposome-encapsulated dichloromethylene diphosphonate. Cell Tissue Res. 238:355.
22. Seiler, P., P. Aichele, B. Odermatt, R. M. Zinkernagel, H. Hengartner, and R. Schwendener. 1997. Crucial role of marginal zone macrophages and marginal zone metallophils during clearance of lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 27:2626.
23. Van Rooijen, N., and A. Sanders. 1994. Liposome mediated depletion of macrophages, mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 174:83.
24. Mackaness, G. B. 1962. Cellular resistance to infection. J. Exp. Med. 116:381.
25. Kaufmann, S. H. E. 1993. Immunity to intracellular bacteria. Annu. Rev. Immunol. 11:129.
26. Conlan, J. W., and R. J. North. 1994. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J. Exp. Med. 179:259.
27. Rogers, H. W., and E. R. Unanue. 1993. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes. Infect. Immun. 61:5090.
28. Czuprynski, C. J., J. F. Brown, R. D. Wagner, and H. Steinberg. 1994. Administration of antigranulocyte monoclonal antibody RB6-8C5 prevents expression of acquired resistance to Listeria monocytogenes infection in previously immunized mice. Infect. Immun. 62:5161.
29. Bancroft, G. J., R. D. Schreiber, and E. R. Unanue. 1991. Natural immunity: a T cell independent pathway of macrophage activation defined in scid mice. Immunol. Rev. 124:5.
30. Unanue, E. R. 1997. Inter-relationship among macrophages, natural killer cells and neutrophils in early stages of Listeria infection. Curr. Opin. Immunol. 9:35.
31. + T cells activated during infection. Microb. Pathog. 1:249.
32. Mackaness, G. B. 1964. The immunological basis of acquired cellular resistance. J. Exp. Med. 120:105.
33. Conlan, J. W. 1996. Early pathogenisis of Listeria monocytogenes infection in the mouse spleen. J. Med. Microbiol. 44:295.
34. Kraal, G., K. Schornagel, P. R. Streeter, B. Holzmann, and E. C. Butcher. 1995. Expression of the mucosal vascular addressin, MAdCAM-1, on sinus-lining cells in the spleen. Am. J. Pathol. 147:763.
35. Tanaka, H., Y. Hataba, S. Saito, O. Fukushima, and M. Miyasaka. 1996. Phenotypic characteristics and significance of reticular meshwork surrounding splenic white pulp. J. Electron Microsc. 45:407.
36. Pinto, A. J., D. Stewart, v. R. N., and P. S. Morahan. 1991. Selective depletion of liver and splenic macrophages using liposomes encapsulating the drug dichloromethylene diphosphonate: effects on antimicrobial resistance. J. Leukocyte Biol. 49:579.
37. Samsom, J. N., A. Annema, P. H. Groeneveld, N. Van Rooijen, J. A. Langermans, and R. Van Furth. 1997. Elimination of resident macrophages from the livers and spleens of immune mice impairs acquired resistance against a secondary Listeria monocytogenes infection. Infect. Immun. 65:986.
38. Eloranta, M. L., and G. V. Alm. 1999. 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.
39. Eloranta, M. L., K. Sandberg, and G. V. Alm. 1996. The interferon α/β responses in mice to herpes simplex virus studied at the blood and tissue level in vitro and in vivo. Scand. J. Immunol. 43:355.
40. Barchet, W., M. Cella, B. Odermatt, C. Asselin-Paturel, M. Colonna, and U. Kalinke. 2002. Virus-induced interferon α production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195:507.
41. van den Broek, M. F., U. Muller, S. Huang, R. M. Zinkernagel, and M. Aguet. 1995. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol. Rev. 148:5.
42. Chao, D., and G. G. MacPherson. 1990. Analysis of thymus-independent type 2 antigen uptake by marginal zone macrophages in thin slices of viable lymphoid tissue. Eur. J. Immunol. 20:1451.
43. Demoy, M., J. P. Andreux, C. Weingarten, B. Gouritin, V. Guilloux, and P. Couvreur. 1999. In vitro evaluation of nanoparticles spleen capture. Life Sci. 64:1329.
44. Han, Y., S. Kelm, M. H. Riesselman, P. R. Crocker, and J. E. Cutler. 1994. Mouse sialoadhesin is not responsible for Candida albicans yeast cell binding to splenic marginal zone macrophages. Infect. Immun. 62:2115.
45. Janeway, C. A. J. 1992. The immune system evolved to discriminate infectious non-self from non-infectious self. Immunol. Today 13:11.
46. Medzhitov, R., and C. A. J. Janeway. 1997. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9:4.
47. Pearson, A. M. 1996. Scavenger receptors in innate immunity. Curr. Opin. Immunol. 8:20.
48. Ochsenbein, A. F., T. Fehr, C. Lutz, M. Suter, F. Brombacher, H. Hengartner, and R. M. Zinkernagel. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156.
49. Carrol, M. C. 1998. The role of complement and complement receptors in induction and regulation of immunity. Annu. Rev. Immunol. 16:545.
50. Lachmann, P. J., and A. Davies. 1997. Complement and immunity to viruses. Immunol. Rev. 159:69.
51. Wessels, M. R., M. Butko, M. Ma, H. B. Warren, A. L. Lage, and M. C. Carroll. 1995. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. USA 92:11490.
52. Brown, E. J. 1991. Complement receptors and phagocytosis. Curr. Opin. Immunol. 3:76.
53. Fraser, I. P., H. Koziel, and R. A. Ezekowitz. 1998. The serum mannose-binding protein and the macrophage mannose receptor are pattern recognition molecules that link innate and adaptive immunity. Semin. Immunol. 10:363.
54. Elomaa, O., M. Kangas, C. Sahlberg, J. Tuukkanen, R. Sormunen, A. Liakka, I. Thesleff, G. Kraal, and K. Tryggvason. 1995. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80:603.
55. Ito, S., M. Naito, Y. Kobayashi, H. Takatsuka, S. Jiang, H. Usuda, H. Umezu, G. Hasegawa, M. Arakawa, L. D. Shultz, O. Elomaa, and K. Tryggvason. 1999. Roles of macrophage receptor with collagenous structure (MACRO) in host defense and heterogeneity of splenic marginal zone macrophages. Arch. Histol. Cytol. 62:83.
56. Ishiguro, T., M. Naito, T. Yamamoto, G. Hasegawa, F. Gejyo, M. Mitsuyama, H. Suzuki, and T. Kodama. 2001. Role of scavenger receptors in response to Listeria monocytogenes infection in mice. Am. J. Pathol. 158:179.
57. Thomas, C. A., Y. Li, T. Kodama, H. Suzuki, S. C. Silverstein, and J. El Khoury. 2000. Protection from lethal Gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J. Exp. Med. 191:147.
58. Eugster, H. P., M. Muller, U. Karrer, B. D. Car, B. Schnyder, V. M. Eng, G. Woerly, M. Le Hir, F. di Padova, M. Aguet, et al. 1996. Multiple immune abnormalities in tumor necrosis factor and lymphotoxin-α double-deficient mice. Int. Immunol. 8:23.
59. -/-) mutant mice. J. Exp. Med. 185:2157.
60. Koike, R., T. Nishimura, R. Yasumizu, H. Tanaka, Y. Hataba, Y. Hataba, T. Watanabe, S. Miyawaki, and M. Miyasaka. 1996. The splenic marginal zone is absent in aly mutant mice. Eur. J. Immunol. 26:669.
61. Guinamard, R., M. Okigaki, J. Schlessinger, and J. V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1:3136.
62. Cariappa, A., H. C. Liou, B. H. Horwitz, and S. Pillai. 2000. Nuclear factor κB is required for the development of marginal zone B lymphocytes. J. Exp. Med. 192:1175.
63. Weih, D. S., Z. Buket Yilmaz, and F. Weih. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167:1909.
64. Fransoso, G., L. Carlson, T. Scharton-Kersten, E. W. Shores, S. Epstein, A. Grinberg, T. Tran, E. Shacter, A. Leonardi, M. Anver, et al. 1997. Critical role for the Bcl-3 oncoprotein in T cell-mediated immunity, splenic microarchitecture, and germinal center reactions. Immunity 6:479.
65. Alimzhanov, M. B., D. V. Kuprash, M. H. Kosco-Vilbois, A. Luz, R. L. Turetskaya, A. Tarakhovsky, K. Rajewsky, S. A. Nedospasov, and K. Pfeffer. 1997. Abnormal development of secondary lymphoid tissues in lymphotoxin β-deficient mice. Proc. Natl. Acad. Sci. 94:9302.
66. Umeda, S., K. Takahashi, L. D. Shultz, M. Naito, and K. Takagi. 1996. Effects of macrophage colony-stimulating factor on macrophages and their related cell populations in the osteopetrosis mouse defective in production of functional macrophage colony-stimulating factor protein. Am. J. Pathol. 149:559.
67. Oehen, S., B. Odermatt, U. Karrer, H. Hengartner, R. Zinkernagel, and C. Lopez-Macias. 2002. Marginal zone macrophages and immune responses against viruses. J. Immunol. 169:1453.
68. Claasen, I. T. J. M., D. M. E. Osterhaus, and E. Claasen. 1995. Antigen detection in vivo after immunization with different presentation forms of rabies virus antigen: involvement of marginal metallophilic macrophages in the uptake of immune-stimulating complexes. Eur. J. Immunol. 25:1446.
69. MacLennan, I. C., and Y. J. Liu. 1991. Marginal zone B cells respond both to polysaccharide antigens and protein antigens. Res. Immunol. 142:346.
70. Martin, F., A. M. Oliver, and J. F. Kearney, 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14:617.
71. Cyster, J. G. 2000. B cells on the front line. Nat. Immunol. 1:9.
72. high lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells. J. Immunol. 162:7198.
73. Claasen, I. J. T., A. D. M. Osterhaus, M. Poelen, N. Van Rooijen, and E. Claassen. 1998. Antigen detection in vivo after immunization with different presentation forms of rabies virus antigen. II. Cellular, but not humoral, systemic immune response against rabies virus immune stimulating complexes are macrophage dependent. Immunology 94:455.
74. Nair, S., A. M. J. Buiting, R. J. D. Rouse, N. Van Rooijen, L. Huang, and B. T. Rouse. 1995. Role of macrophages and dendritic cells in primary cytotoxic T lymphocyte responses. Int. Immunol. 7:679.