The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages

Infection and Immunity

Volumn 67, Issue 2, 1999, Pages 469-477

  Astarie Dequeker, Catherine ^a   N'Diaye, Elsa Noah ^a   Le Cabec, Veronique ^a   Rittig, Michael G ^b   Prandi, Jacques ^a   Maridonneau Parini, Isabelle ^a  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; LIGAND; MANNOSE RECEPTOR; PROTEIN TYROSINE KINASE; ZYMOSAN;

ARTICLE; BACTERICIDAL ACTIVITY; ELECTRON MICROSCOPY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MYCOBACTERIUM; NONHUMAN; PATHOGENICITY; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; PROTEIN FAMILY; RECEPTOR INTRINSIC ACTIVITY; RECEPTOR OCCUPANCY; REGULATORY MECHANISM;

EID: 0032935608     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.2.469-477.1999     Document Type: Article

References (58)

1. Armstrong, J. A., and P. D. Hart. 1975. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. J. Exp. Med. 142:1-16.
2. Barker, K., H. Fan, C. Carroll, G. Kaplan, J. Barker, W. Hellmann, and Z. A. Cohn. 1996. Nonadherent cultures of human monocytes kill Mycobacterium smegmatis, but adherent cultures do not. Infect. Immun. 64:428-433.
3. Bermudez, L. E., L. S. Young, and H. Holly. 1991. Interaction of Mycobacterium avium complex with human macrophages: roles of membrane receptors and serum proteins. Infect. Immun. 59:1697-1702.
4. Berton, G., and S. Gordon. 1983. Modulation of macrophage mannosyl-specific receptors by cultivation on immobilized zymosan. Effects on superoxide-anion release and phagocytosis. Immunology 49:705-715.
5. Bodmer, J. L., and R. T. Dean. 1983. Does the induction of macrophage lysosomal enzyme secretion by zymosan involve the mannose receptor. Biochem. Biophys. Res. Commun. 113:192-198.
6. Chatterjee, D., S. N. Cho, and P. J. Brennan. 1986. Chemical synthesis and seroreactivity of O-(3,6-di-O-methyl-β-D-glucopyranosyl)-(1-4)-O-(2,3-di-O-methyl-α-L- rhamnopyranosyl)-(1-9)-oxinonanoyl-bovine serum albumin, the leprosy-specific natural disaccharide-octyl-neoglycoprotein. Carbohydr. Res. 156:39-56.
7. Daffé, M., and P. Draper. 1998. The envelope layers of mycobacteria with reference to their pathogenicity. Adv. Microb. Physiol. 39:131-203.
8. Da Silva, R. P., B. F. Hall, K. A. Joiner, and D. L. Sacks. 1989. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 143:617-622.
9. De Chastelier, C., and L. Thilo. 1997. Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle. Eur. J. Cell Biol. 74:49-62.
10. Di Carlo, F. J., and J. V. Fiore. 1957. On the composition of zymosan. Science 127:756-757.
11. Diment, S., M. S. Leech, and P. D. Stahl. 1987. Generation of macrophage variants with 5-azacytidine: selection for mannose receptor expression J. Leukoc. Biol. 42:485-490.
12. Ehlers, M. R. W., and M. Daffé. 1998. Interactions between Mycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol. 7:328-335.
13. Ezekowitz, R. A. B., D. J. Williams, H. Koziel, M. Y. K. Armstrong, A. Warner, F. F. Richards, and R. M. Rose. 1991. Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351:155-158.
14. Ezekowitz, R. A. B., K. Sastry, P. Bailly, and A. Warner. 1990. Molecular characterization of the human macrophage mannose receptor: demonstration of a multiple carbohydrate recognition-like domains and phagocytosis of yeasts in COS cells. J. Exp. Med. 172:1785-1794.
15. Falkow, S., R. R. Isberg, and D. A. Portnoy. 1992. The interaction of bacteria with mammalian cells. Annu. Rev. Cell Biol. 8:333-363.
16. Gelderman, M. P., L. Doris, S. S. Lefkowitz, A. Bollen, and N. Moguilevsky. 1998. Exposure of macrophages to an enzymatically inactive macrophage mannose receptor ligand augments killing of Candida albicans. Proc. Soc. Exp. Biol. Med. 217:81-88.
17. Goldmann, R. 1988. Characterization of the β-glucan receptor of murine macrophages. Exp. Cell Res. 174:481-490.
18. Green, S. P., J. A. Hamilton, and W. A. Phillips. 1992. Zymosan-triggered tyrosine phosphorylation in mouse bone-marrow macrophages is enhanced by respiratory-burst priming agents. Biochem. J. 288:427-432.
19. Grégoire, C., H. Welch, C. Astarie-Dequeker, and I. Maridonneau-Parini. 1998. Expression of azurophil and specific granule proteins during differentiation of NB4 cells in neutrophils. J. Cell. Physiol. 175:203-210.
20. Hines, M. E., J. M. Kreeger, and A. J. Herron. 1995. Mycobacterial infections of animals: pathology and pathogenesis. Lab. Anim. Sci. 45:334-351.
21. Ishibashi, Y., and T. Arai. 1990. Role of the complement receptor type 1 (CR1) and type 3 (CR3) on phagocytosis and subsequent phagosome-lysosome fusion in Salmonella-infected murine macrophages. FEMS Microbiol. Immunol. 69:89-96.
22. Kery, V., J. J. F. Krepinsky, C. D. Warren, P. Capek, and P. D. Stahl. 1992. Ligand recognition by purified human mannose receptor. Arch. Biochem. Biophys. 298:49-55.
23. Klegeris, A., T. C. Budd, and S. A. Greenfield. 1996. Acetylcholinesterase-induced respiratory burst in macrophages: evidence for the involvement of the macrophage mannose-fucose receptor. Biochim. Biophys. Acta 1289: 159-168.
24. Kornfeld, S., and I. Mellman. 1989. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 85:483-525.
25. Kruskal, B. A., K. Sastry, A. B. Warner, C. E. Mathieu, and R. A. Ezekowitz. 1992. Phagocytic chimeric receptors require both transmembrane and cytoplasmic domains from the mannose receptor. J. Exp. Med. 176:1673-1680.
26. Le Cabec, V., and I. Maridonneau-Parini. 1995. Complete and reversible inhibition of NADPH-oxidase in human neutrophils by phenylarsine oxide at a step distal to membrane translocation of the enzyme subunits. J. Biol. Chem. 270:2067-2073.
27. Le Cabec, V., and I. Maridonneau-Parini. 1998. Unpublished data.
28. Le Cabec, V., and I. Maridonneau-Parini. 1994. Annexin-3 is associated with cytoplasmic granules in neutrophils and monocytes and translocates to the plasma membrane in activated cells. Biochem. J. 303:481-488.
29. Maridonneau-Parini, I., and J. de Gunzburg. 1992. Association of rap1 and rap2 proteins with the specific granules of human neutrophils. J. Biol. Chem. 267:6396-6402.
30. - generation by dexamethasome is mimicked by lipocortin I in alveolar macrophages. J. Clin. Investig. 83:1936-1940.
31. Metzelaar, M. J., P. L. Wijngaard, P. J. Peters, J. J. Sixma, H. K. Nieuwenhuis, and H. C. Clevers. 1991. CD63 antigen. A novel lysosomal membrane glycoprotein, cloned by a screening procedure for intracellular antigens in eukaryotic cells. J. Biol. Chem. 266:3239-3245.
32. hck is located on the secretory granules in human neutrophils and translocates toward the phagosomes during cell activation. Biochem. J. 309:657-665.
33. Murai, M., Y. Aramaki, and S. Tsuchiya. 1996. Alpha 2-macroglobulin stimulation of protein tyrosine phosphorylation in macrophages via the mannose receptor for Fc gamma-receptor-mediated phagocytosis activation. Immunology 89:436-441.
34. N'Diaye, E. N., X. Darzacq, C. Astarie-Dequeker, M. Daffé, J. Calafat, and I. Maridonneau-Parini. 1998 Fusion of azurophil granules with phagosomes and activation of the tyrosine-kinase Hck are specifically inhibited during phagocytosis of mycobacteria by human neutrophils. J. Immunol. 161:4983-4991.
35. Oshumi, Y., and Y. C. Lee. 1987. Mannose-receptor ligands stimulate the secretion of lysosomal enzymes from rabbit alveolar macrophages. J. Biol. Chem. 262:7955-7962.
36. Paul, S., P. Laochumroonvorapong, and G. Kaplan. 1996. Comparable growth of virulent and avirulent Mycobacterium tuberculosis in human macrophages in vitro. J. Infect. Dis. 174:105-112.
37. Peters, T. 1991. Synthesis and conformational analysis of methyl 2-O-(α-D-mannopyranosyl)-α-D-mannopyranoside. Liebigs Ann. Chem. 1991:135-141.
38. Pontow, S. E., V. Kery, and P. D. Stahl. 1992. Mannose receptor. Int. Rev. Cytol. 137B:221-244.
39. Quintrell, N., R. Lebo, H. Varmus, J. M. Bishop, M. J. Pettenati, M. M. LeBeau, M. O. Diaz, and J. D. Rowley. 1987. Identification of the human gene (HCK) that encodes for a protein tyrosine kinase and is expressed in hematopoietic cells. Mol. Cell. Biol. 7:2267-2275.
40. Rabinowitz, S., H. Horstmann, S. Gordon, and G. Griffiths. 1992. Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macrophages. J. Cell Biol. 116:95-112.
41. Rittig, M., K. Schröppel, K. H. Seack, U. Sander, E. N. N'Diaye, I. Maridonneau-Parini, W. Solbach, and C. Bodgard. 1998. Coiling phagocytosis of trypanosomatids and fungal cells. Infect. Immun. 66:4331-4339.
42. Rittig, R. G., E. N. N'Diaye, and I. Maridonneau-Parini. 1998. Zymosan phagocytosis revisited: new results from an old model. Eur. J. Haematol. 60: 324-325.
43. Rocklein, J. A., R. P. Schwartz, and H. Yeager. 1992. Nonopsonic uptake of Mycobacterium avium complex by human monocytes and alveolar macrophages. J. Lab. Clin. Med. 119:772-781.
44. Russell, D. G., J. Dante, and S. Sturgill-Koszycki. 1996. Mycobacterium avium and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from host cell plasmalemma. J. Immunol. 156:4764-4773.
45. Schlesinger, L. S. 1993. Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by the mannose receptors in addition to complement receptors. J. Immunol. 150:2920-2930.
46. Schlesinger, L. S. 1996. Entry of Mycobacterium tuberculosis into mononuclear phagocytes. Curr. Top. Microbiol. Immunol. 215:71-96.
47. Shepherd, V. L., M. G. Konish, and P. Stahl. 1985. Dexamethasone increases the expression of mannose receptors and decreases extracellular lysosomal enzyme accumulation in macrophages. J. Biol. Chem. 260:160-164.
48. Shibata, Y., W. J. Metzger, and Q. N. Myrvik. 1997. Chitin particle-induced cell-mediated immunity is inhibited by soluble mannan. Mannose receptor-mediated phagocytosis initiates IL-12 production. J. Immunol. 159:2462-2467.
49. Speert, P. D., and S. C. Silverstein. 1985. Phagocytosis of unopsonized zymosan by human monocyte-derived macrophages: maturation and inhibition by mannan. J. Leukoc. Biol. 38:655-658.
50. Stokes, R. W., I. D. Haidl, W. A. Jefferies, and D. P. Speert. 1993. Mycobacteria-macrophage interactions. Macrophage phenotype determines the nonopsonic binding of mycobacterium tuberculosis to murine macrophages. J. Immunol. 151:7067-7076.
51. Welch, H., and I. Maridonneau-Parini. 1997. Hck is activated by opsonized zymosan and A23187 in distinct subcellular fractions of human neutrophils. J. Biol. Chem. 272:102-109.
52. Welch, H., C. Mauran, and I. Maridonneau-Parini. 1996. Nonreceptor protein-tyrosine kinases in neutrophil activation. Methods Companion Methods Enzymol. 9:607-618.
53. Wilson, M. E., and R. D. Pearson. 1988. Role of the CR3 and mannose receptors in the attachment and ingestion of Leishmania donovani by human mononuclear phagocytes. Infect. Immun. 56:363-369.
54. Wright, S. D., and S. C. Silverstein. 1983. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J. Exp. Med. 158:2016-2023.
55. Yamamoto, K., and R. B. Johnston, Jr. 1984. Dissociation of phagocytosis from stimulation of the oxidative metabolic burst in macrophages. J. Exp. Med. 159:405-416.
56. Yamamoto, Y., T. W. Klein, and H. Friedman. 1997. Involvement of the mannose receptor in cytokine interleukin-1β (IL-1β), IL-6, and granulocytemacrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1β (MIP-1β), MIP-2. and KC responses, caused by attachment of Candida albicans to macrophages. Infect. Immun. 65:1077-1082.
57. Ziegler, S. F., J. D. Marth, D. B. Lewis, and R. M. Perlmutter. 1987. Novel protein tyrosine kinase (Hck) expressed in cells of hematopoietic cells. Mol. Cell. Biol. 7:2275-2285.
58. Zimmerli, S., M. Majeed, M. Gustavsson, O. Stendahl, D. A. Sanan, and J. D. Ernst. 1996. Phagosome-lysosome fusion is a calcium-independent event in macrophages. J. Cell Biol. 132:49-61.