Mannose receptor and macrophage galactose-type lectin are involved in Bordetella pertussis mast cell interaction

Journal of Leukocyte Biology

Volumn 94, Issue 3, 2013, Pages 439-448

  Vukman, Krisztina V ^a   Ravidà, Alessandra ^a   Aldridge, Allison M ^a   O'Neill, Sandra M ^a  

^a DUBLIN CITY UNIVERSITY   (Ireland)

Author keywords

C type lectin; Cytokine; ERK; ICAM1; NF kB

Indexed keywords

ANTIBODY; C TYPE LECTIN RECEPTOR; CARBOHYDRATE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; LECTIN; LECTIN RECEPTOR; LIPOOLIGOSACCHARIDE; MACROPHAGE GALACTOSE TYPE LECTIN; MANNOSE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PERTUSSIS VACCINE; PROTEIN KINASE SYK; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BORDETELLA PERTUSSIS; CELL INTERACTION; CELL ISOLATION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; FLOW CYTOMETRY; GROWTH INHIBITION; HEAT; HOST PATHOGEN INTERACTION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; MAST CELL; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE;

C-TYPE LECTIN; CYTOKINE; ERK; ICAM1; NF-ΚB;

ANIMALS; ASIALOGLYCOPROTEINS; BORDETELLA PERTUSSIS; EGTAZIC ACID; INTERCELLULAR ADHESION MOLECULE-1; INTERFERON-GAMMA; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MANNOSE-BINDING LECTINS; MAST CELLS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NF-KAPPA B; PROTEIN-TYROSINE KINASES; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84883242753     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0313130     Document Type: Article

References (69)

1. Gregory, D. S. (2006) Pertussis: a disease affecting all ages. Am. Fam. Physician 74, 420-426.
2. Crowcroft, N. S., Pebody, R. G. (2006) Recent developments in pertussis. Lancet 367, 1926-1936.
3. Von Konig, C. H., Halperin, S., Riffelmann, M., Guiso, N. (2002) Pertussis of adults and infants. Lancet Infect. Dis. 2, 744-750.
4. Wierzbicki, M., Brzezinska-Blaszczyk, E. (2009) Diverse effects of bacterial cell wall components on mast cell degranulation, cysteinyl leukotriene generation and migration. Microbiol. Immunol. 53, 694-703.
5. Maurer, M., Lopez Kostka, S., Siebenhaar, F., Moelle, K., Metz, M., Knop, J., von Stebut, E. (2006) Skin mast cells control T cell-dependent host defense in Leishmania major infections. FASEB J. 20, 2460-2467.
6. Siebenhaar, F., Syska, W., Weller, K., Magerl, M., Zuberbier, T., Metz, M., Maurer, M. (2007) Control of Pseudomonas aeruginosa skin infections in mice is mast cell-dependent. Am. J. Pathol. 170, 1910-1916.
7. Abraham, S. N., St John, A. L. (2010) Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10, 440-452.
8. McLachlan, J. B., Shelburne, C. P., Hart, J. P., Pizzo, S. V., Goyal, R., Brooking-Dixon, R., Staats, H. F., Abraham, S. N. (2008) Mast cell activators: a new class of highly effective vaccine adjuvants. Nat. Med. 14, 536-541.
9. Velin, D., Bachmann, D., Bouzourene, H., Michetti, P. (2005) Mast cells are critical mediators of vaccine-induced Helicobacter clearance in the mouse model. Gastroenterology 129, 142-155.
10. Mielcarek, N., Hornquist, E. H., Johansson, B. R., Locht, C., Abraham, S. N., Holmgren, J. (2001) Interaction of Bordetella pertussis with mast cells, modulation of cytokine secretion by pertussis toxin. Cell. Microbiol. 3, 181-188.
11. Moiseeva, E. P., Bradding, P. (2011) Mast cells in lung inflammation. Adv. Exp. Med. Biol. 716, 235-269.
12. Abraham, S. N., Thankavel, K., Malaviya, R. (1997) Mast cells as modulators of host defense in the lung. Front. Biosci. 2, d78-d87.
13. Schaeffer, L. M., McCormack, F. X., Wu, H., Weiss, A. A. (2004) Bordetella pertussis lipopolysaccharide resists the bactericidal effects of pulmonary surfactant protein A. J. Immunol. 173, 1959-1965.
14. Marr, N., Novikov, A., Hajjar, A. M., Caroff, M., Fernandez, R. C. (2010) Variability in the lipooligosaccharide structure and endotoxicity among Bordetella pertussis strains. J. Infect. Dis. 202, 1897-1906.
15. Kusumoto, S., Fukase, K., Shiba, T. (2010) Key structures of bacterial peptidoglycan and lipopolysaccharide triggering the innate immune system of higher animals: chemical synthesis and functional studies. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 86, 322-337.
16. Kawai, T., Akira, S. (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650.
17. Geijtenbeek, T. B., Gringhuis, S. I. (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9, 465-479.
18. Ip, W. K., Takahashi, K., Ezekowitz, R. A., Stuart, L. M. (2009) Mannosebinding lectin and innate immunity. Immunol. Rev. 230, 9-21.
19. Lloyd, D. H., Viac, J., Werling, D., Reme, C. A., Gatto, H. (2007) Role of sugars in surface microbe-host interactions and immune reaction modulation. Vet. Dermatol. 18, 197-204.
20. Weis, W. I., Taylor, M. E., Drickamer, K. (1998) The C-type lectin superfamily in the immune system. Immunol. Rev. 163, 19-34.
21. Van Sorge, N. M., Bleumink, N. M., van Vliet, S. J., Saeland, E., van der Pol, W. L., van Kooyk, Y., van Putten, J. P. (2009) N-Glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL. Cell. Microbiol. 11, 1768-1781.
22. Van Vliet, S. J., den Dunnen, J., Gringhuis, S. I., Geijtenbeek, T. B., van Kooyk, Y. (2007) Innate signaling and regulation of dendritic cell immunity. Curr. Opin. Immunol. 19, 435-440.
23. Guthmann, M. D., Tal, M., Pecht, I. (1995) A secretion inhibitory signal transduction molecule on mast cells is another C-type lectin. Proc. Natl. Acad. Sci. USA 92, 9397-9401.
24. Katz, H. R. (2002) Inhibitory receptors and allergy. Curr. Opin. Immunol. 14, 698-704.
25. Abramson, J., Xu, R., Pecht, I. (2002) An unusual inhibitory receptor-the mast cell function-associated antigen (MAFA). Mol. Immunol. 38, 1307-1313.
26. Ribbing, C., Engblom, C., Lappalainen, J., Lindstedt, K., Kovanen, P. T., Karlsson, M. A., Lundeberg, L., Johansson, C., Nilsson, G., Lunderius-Andersson, C., Scheynius, A. (2011) Mast cells generated from patients with atopic eczema have enhanced levels of granule mediators and an impaired Dectin-1 expression. Allergy 66, 110-119.
27. Yang, Z., Marshall, J. S. (2009) Zymosan treatment of mouse mast cells enhances Dectin-1 expression and induces Dectin-1-dependent reactive oxygen species (ROS) generation. Immunobiology 214, 321-330.
28. Wells, C. A., Salvage-Jones, J. A., Li, X., Hitchens, K., Butcher, S., Murray, R. Z., Beckhouse, A. G., Lo, Y. L., Manzanero, S., Cobbold, C., Sch-roder, K., Ma, B., Orr, S., Stewart, L., Lebus, D., Sobieszczuk, P., Hume, D. A., Stow, J., Blanchard, H., Ashman, R. B. (2008) The macrophageinducible C-type lectin, Mincle, is an essential component of the innate immune response to Candida albicans. J. Immunol. 180, 7404-7413.
29. Kerrigan, A. M., Brown, G. D. (2010) Syk-coupled C-type lectin receptors that mediate cellular activation via single tyrosine based activation motifs. Immunol. Rev. 234, 335-352.
30. Vukman, K.V., Adams, P.N., Metz, M., Maurer, M., O'Neill, S.M. (2013) Fasciola hepatica tegumental coat impairs mast cells ability to drive Th1 immune responses. J. Immunol. 190, 2873-2879.
31. Mahon, B. P., Ryan, M. S., Griffin, F., Mills, K. H. (1996) Interleukin-12 is produced by macrophages in response to live or killed Bordetella pertussis and enhances the efficacy of an acellular pertussis vaccine by promoting induction of Th1 cells. Infect. Immun. 64, 5295-5301.
32. Mrabet-Dahbi, S., Metz, M., Dudeck, A., Zuberbier, T., Maurer, M. (2009) Murine mast cells secrete a unique profile of cytokines and prostaglandins in response to distinct TLR2 ligands. Exp. Dermatol. 18, 437-444.
33. Vukman, K. V., Visnovitz, T., Adams, P. N., Metz, M., Maurer, M., O'Neill, S. M. (2012) Mast cells cultured from IL-3-treated mice show impaired responses to bacterial antigen stimulation. Inflamm. Res. 61, 79-85.
34. Kimura, I., Moritani, Y., Tanizaki, Y. (1973) Basophils in bronchial asthma with reference to reagin-type allergy. Clin. Allergy 3, 195-202.
35. Kittelberger, R., Hilbink, F. (1993) Sensitive silver-staining detection of bacterial lipopolysaccharides in polyacrylamide gels. J. Biochem. Biophys. Methods 26, 81-86.
36. Inzana, T. J., Glindemann, G., Cox, A. D., Wakarchuk, W., Howard, M. D. (2002) Incorporation of N-acetylneuraminic acid into Haemophilus somnus lipooligosaccharide (LOS): enhancement of resistance to serum and reduction of LOS antibody binding. Infect. Immun. 70, 4870-4879.
37. Guthmann, M. D., Tal, M., Pecht, I. (1995) A new member of the Ctype lectin family is a modulator of the mast cell secretory response. Int. Arch. Allergy Immunol. 107, 82-86.
38. Huels, C., Germann, T., Goedert, S., Hoehn, P., Koelsch, S., Hultner, L., Palm, N., Rude, E., Schmitt, E. (1995) Co-activation of naive CD4+ T cells and bone marrow-derived mast cells results in the development of Th2 cells. Int. Immunol. 7, 525-532.
39. Nakae, S., Suto, H., Iikura, M., Kakurai, M., Sedgwick, J. D., Tsai, M., Galli, S. J. (2006) Mast cells enhance T cell activation: importance of mast cell costimulatory molecules and secreted TNF. J. Immunol. 176, 2238-2248.
40. Nakae, S., Suto, H., Kakurai, M., Sedgwick, J. D., Tsai, M., Galli, S. J. (2005) Mast cells enhance T cell activation: importance of mast cellderived TNF. Proc. Natl. Acad. Sci. USA 102, 6467-6472.
41. Nie, X., Cai, G., Zhang, W., Wang, H., Wu, B., Li, Q., Shen, Q. (2011) Lipopolysaccharide mediated mast cells induce IL-10 producing regulatory T cells through the ICOSL/ICOS axis. Clin. Immunol. 142, 269-279.
42. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C., Mills, K. H. (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177, 7980-7989.
43. Metcalfe, D. D., Baram, D., Mekori, Y. A. (1997) Mast cells. Physiol. Rev. 77, 1033-1079.
44. Dawicki, W., Marshall, J. S. (2007) New and emerging roles for mast cells in host defence. Curr. Opin. Immunol. 19, 31-38.
45. Galli, S. J., Tsai, M. (2010) Mast cells in allergy and infection: versatile effector and regulatory cells in innate and adaptive immunity. Eur. J. Immunol. 40, 1843-1851.
46. Weller, C. L., Collington, S. J., Williams, T., Lamb, J. R. (2011) Mast cells in health and disease. Clin. Sci. (Lond.) 120, 473-484.
47. Van Vliet, S. J., Garcia-Vallejo, J. J., van Kooyk, Y. (2008) Dendritic cells and C-type lectin receptors: coupling innate to adaptive immune responses. Immunol. Cell Biol. 86, 580-587.
48. Rajaram, M. V., Brooks, M. N., Morris, J. D., Torrelles, J. B., Azad, A. K., Schlesinger, L. S. (2010) Mycobacterium tuberculosis activates human macrophage peroxisome proliferator-activated receptor γ linking mannose receptor recognition to regulation of immune responses. J. Immunol. 185, 929-942.
49. Terrazas, C. A., Sanchez-Munoz, F., Mejia-Dominguez, A. M., Amezcua-Guerra, L. M., Terrazas, L. I., Bojalil, R., Gomez-Garcia, L. (2011) Cestode antigens induce a tolerogenic-like phenotype and inhibit LPS inflammatory responses in human dendritic cells. Int. J. Biol. Sci. 7, 1391-1400.
50. Napoletano, C., Zizzari, I. G., Rughetti, A., Rahimi, H., Irimura, T., Clausen, H., Wandall, H. H., Belleudi, F., Bellati, F., Pierelli, L., Frati, L., Nuti, M. (2012) Targeting of macrophage galactose-type C-type lectin (MGL) induces DC signaling and activation. Eur. J. Immunol. 42, 936-945.
51. Kang, B. K., Schlesinger, L. S. (1998) Characterization of mannose receptor-dependent phagocytosis mediated by Mycobacterium tuberculosis lipoarabinomannan. Infect. Immun. 66, 2769-2777.
52. Denda-Nagai, K., Aida, S., Saba, K., Suzuki, K., Moriyama, S., Oo-Puthinan, S., Tsuiji, M., Morikawa, A., Kumamoto, Y., Sugiura, D., Kudo, A., Akimoto, Y., Kawakami, H., Bovin, N. V., Irimura, T. (2010) Distribution and function of macrophage galactose-type C-type lectin 2 (MGL2/ CD301b): efficient uptake and presentation of glycosylated antigens by dendritic cells. J. Biol. Chem. 285, 19193-19204.
53. Marshall, J. S., King, C. A., McCurdy, J. D. (2003) Mast cell cytokine and chemokine responses to bacterial and viral infection. Curr. Pharm. Des. 9, 11-24.
54. Galli, S. J., Grimbaldeston, M., Tsai, M. (2008) Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nat. Rev. Immunol. 8, 478-486.
55. Desai, P., Thurmond, R. L. (2011) Histamine H receptor activation enhances LPS-induced IL-6 production in mast cells via ERK and PI3K activation. Eur. J. Immunol. 41, 1764-1773.
56. Li, G., Domenico, J., Jia, Y., Lucas, J. J., Gelfand, E. W. (2009) NF-κBdependent induction of cathelicidin-related antimicrobial peptide in murine mast cells by lipopolysaccharide. Int. Arch. Allergy Immunol. 150, 122-132.
57. Lin, Y. C., Huang, D. Y., Chu, C. L., Lin, W. W. (2010) Anti-inflammatory actions of Syk inhibitors in macrophages involve non-specific inhibition of Toll-like receptors-mediated JNK signaling pathway. Mol. Immunol. 47, 1569-1578.
58. Tsang, C. M., Wong, C. K., Ip, W. K., Lam, C. W. (2005) Synergistic effect of SCF and TNF-κ on the up-regulation of cell-surface expression of ICAM-1 on human leukemic mast cell line (HMC)-1 cells. J. Leukoc. Biol. 78, 239-247.
59. Eberle, M. E., Dalpke, A. H. (2012) Dectin-1 stimulation induces suppressor of cytokine signaling 1, thereby modulating TLR signaling and T cell responses. J. Immunol. 188, 5644-5654.
60. Miller, Y. I., Choi, S. H., Wiesner, P., Bae, Y. S. (2012) The SYK side of TLR4: signalling mechanisms in response to LPS and minimally oxidized LDL. Br. J. Pharmacol. 167, 990-999.
61. Olynych, T. J., Jakeman, D. L., Marshall, J. S. (2006) Fungal zymosan induces leukotriene production by human mast cells through a Dectin-1-dependent mechanism. J. Allergy Clin. Immunol. 118, 837-843.
62. Lang, R., Schoenen, H., Desel, C. (2011) Targeting Syk-Card9-activating C-type lectin receptors by vaccine adjuvants: findings, implications and open questions. Immunobiology 216, 1184-1191.
63. Chaudhary, A., Fresquez, T. M., Naranjo, M. J. (2007) Tyrosine kinase Syk associates with Toll-like receptor 4 and regulates signaling in human monocytic cells. Immunol. Cell Biol. 85, 249-256.
64. Ulanova, M., Asfaha, S., Stenton, G., Lint, A., Gilbertson, D., Schreiber, A., Befus, D. (2007) Involvement of Syk protein tyrosine kinase in LPSinduced responses in macrophages. J. Endotoxin Res. 13, 117-125.
65. Locht, C., Antoine, R., Jacob-Dubuisson, F. (2001) Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr. Opin. Microbiol. 4, 82-89.
66. Van Vliet, S. J., van Liempt, E., Saeland, E., Aarnoudse, C. A., Appelmelk, B., Irimura, T., Geijtenbeek, T. B., Blixt, O., Alvarez, R., van Die, I., van Kooyk, Y. (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int. Immunol. 17, 661-669.
67. Tsuiji, M., Fujimori, M., Ohashi, Y., Higashi, N., Onami, T. M., Hedrick, S. M., Irimura, T. (2002) Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J. Biol. Chem. 277, 28892-28901.
68. Gazi, U., Martinez-Pomares, L. (2009) Influence of the mannose receptor in host immune responses. Immunobiology 214, 554-561.
69. De Gouw, D., Diavatopoulos, D. A., Bootsma, H. J., Hermans, P. W., Mooi, F. R. (2011) Pertussis: a matter of immune modulation. FEMS Microbiol. Rev. 35, 441-474.