Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response

European Journal of Immunology

Volumn 37, Issue 6, 2007, Pages 1524-1537

  Alemán, Mercedes ^a   de la Barrera, Silvia ^a   Schierloh, Pablo ^a   Yokobori, Noemí ^a   Baldini, Matías ^b   Musella, Rosa ^b   Abbate, Eduardo ^b   Sasiain, María ^a  

^a INST DE INVEST HEMATOLOGICAS   (Argentina)

^b HOSPITAL F J MUÑIZ   (Argentina)

Author keywords

Cross presentation priming; Dentritic cells; Granulocytes; Tuberculosis

Indexed keywords

BACTERIAL ANTIGEN; CD36 ANTIGEN; GAMMA INTERFERON; HLA ANTIGEN CLASS 2; INTERLEUKIN 12;

ADULT; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CELL MATURATION; CELL SURFACE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; SUPERNATANT; TUBERCULOSIS;

ADULT; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD36; ANTIGENS, CD86; APOPTOSIS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; CYTOCHALASIN D; DENDRITIC CELLS; ENZYME INHIBITORS; HLA-DR ANTIGENS; HUMANS; IMIDAZOLES; IMMUNOGLOBULINS; INTEGRINS; INTERFERON TYPE II; INTERLEUKIN-12; KINETICS; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHILS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RECEPTORS, CELL SURFACE; RECEPTORS, VITRONECTIN;

EID: 34250684588     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200636771     Document Type: Article

References (47)

1. Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature 1998. 392: 245-252.
2. Stumbles, P. A., Thomas, J. A., Pimm, C. L., Lee, P. T., Venaille, T. J., Proksch, S. and Holt, P. G., Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J. Exp. Med. 1998. 188: 2019-2031.
3. Mellmam, I. and Steinman, R. M., Dendritic cells: specialized and regulated antigen processing machines. Cell 2001. 106: 255-258.
4. Thery, C. and Amigorena, S., The cell biology of antigen presentation in dendritic cells. Curr. Opin. Immunol. 2001. 13: 45-51.
5. Holt, P. G., Pulmonary dendritic cells in local immunity to inert and pathogenic antigens in the respiratory tract. Proc. Am. Thorac. Soc. 2005. 2: 116-120.
6. Flynn, J. L. and Chan, J., Immunology of tuberculosis. Annu. Rev. Immunol. 2001. 19: 93-129.
7. Henderson, R. A., Watkins, S. C. and Flynn, J. A., Activation of human dendritic cells following infection with Mycobacterium tuberculosis. J. Immunol. 1997, 159: 635-643.
8. Jiao, X., Lo-Man, R., Germonprez, L, Fiette, L, Dériaud, E., Burgaud, S, Gicquel, B. et al., Dendritic cells are host cells for Mycobacteria in vivo that trigger innate and acquired immunity. J. Immunol. 2002. 168: 1294-1301.
9. Giacomini, E., Iona, E., Ferroni, L., Miettinen, M., Fattorini, L., Orefici, G., Julkunen, I. and Coccia, E. M., Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 2001. 166: 7033-7041.
10. Tailleux, L., Pham-Thi, N., Bergeron-Lafaurie, A., Herrmann, J. L., Charles, P., Schwartz, O., Scheinmann, P. et al., DC-SIGN induction in alveolar macrophages defines privileged target host cells for Mycobacteria in patients with tuberculosis. PLoS. Med. 2005. 2: e381.
11. Condos, R., Rom, W. N., Liu, Y.M. and Schluger, N. W., Local immune responses correlate with presentation and outcome in tuberculosis. Am. J. Respir. Crit. Care Med. 1998. 157: 729-735.
12. Alemán, M., Beigier-Bompadre, M., Borghetti, C., de la Barrera, S., Abbate, E., Isturiz, M. and Sasiain, M. C., Activation of peripheral blood neutrophils from patients with active advanced tuberculosis. Clin. Immunol. 2001. 100: 87-95.
13. Kasahara, K., Sato, I., Ogura, K., Takeuchi, H., Kobayashi, K. and Adachi, M., Expression of chemokines and induction of rapid cell death in human blood neutrophils by Mycobacterium tuberculosis. J. Infect. Dis. 1998. 178: 127-137.
14. Alemán, M., García, A., Saab, M. A., de la Barrera, S., Finiasz, M., Abbate, E. and Sasiain, M. C., Mycobacterium tuberculosis-induced activation accelerates apoptosis in peripheral blood neutrophils from patients with active tuberculosis. Am. J. Respir. Cell. Mol. Biol. 2002. 27: 583-592.
15. Alemán, M., Schierloh, P., de la Barrera, S., Musella, R. M., Saab, M. A., Baldini, M., Abbate, E. and Sasiain, M. C., Mycobacterium tuberculosis triggers apoptosis in peripheral neutrophils involving TLR2 and p38-mitogen protein kinase in tuberculosis patients. Infect. Immun. 2004. 72: 5150-5158.
16. Alemán, M., de la Barrera, S., Schierloh, P., Alves, L., Yokobori, N., Baldini, M., Abbate, E. and Sasiain, M. C., In tuberculous pleural effusions activated neutrophils undergo apoptosis and acquire dendritic cell-like phenotype. J. Infec. Dis. 2005., 192: 399-409.
17. Tan, B. H., Meinken, C., Bastian, M., Bruns, H., Legaspi, A., Ochoa, M. T., Krutzik, S. R. et al., Macrophages acquire neutrophil granules for antimicrobial activity against intracellular pathogens. J. Immunol. 2006. 177: 1864-1871.
18. Bennouna, S., Bliss, S. K., Curiel, T. J. and Denkers, E. Y., Crosstalk in the innate immune system: neutrophils instruct recruitment and activation of dendritic cells during microbial infection. J. Immunol. 2003. 171: 6052-6058.
19. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y. J., Pulendran, B., and Palucka, K., Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000. 18: 767-811.
20. + T cell response to Mycobacterium tuberculosis and exacerbates the outcome of infection. J. Immunol. 2005. 175: 3268-3272.
21. Megiovanni, A. M., Sanchez, F., Robledo-Sarmiento, M., Morel, C., Gluckman, J. C. and Boudaly, S., Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J. Leukoc. Biol. 2006. 79: 977-988.
22. Clayton, A. R., Prue, R. L., Harper, L., Drayson, M. T. and Savage, C.O., Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheum. 2003. 48: 2362-2374.
23. van Gisbergen, K. P., Sanchez-Hernandez, M., Geijtenbeek, T. B. and van Kooyk, Y., Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 2005. 201: 1281-1292.
24. Shrestha, N., Ida, J. A., Lubinsky, A. S., Pallin, M., Kaplan, G. and Haslett, P. A. J., Regulation of acquired immunity by T-cell/ dendritic-cell interactions. Ann. NY Acad. Sci. 2005. 1062: 79-94.
25. Tailleux, L., Schwartz, O., Herrmann, J. L., Pivert, E., Jackson, M., Amara, A., Legres, L. et al., DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 2003. 197: 121-127.
26. Fadok, V. A., Warner, M. L., Bratton, D. L. and Henson, P. M., CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phophatidylserine receptor or the vitronectin receptor (αvβ3). J. Immunol. 1998. 161: 6250-6257.
27. Albert, M. L., Pearce, S. F. A., Francisco, L. M., Sauter, B., Roy, P., Silverstein, R. L. and Bhardwaj, N., Immature dendritic cells phagocytose apoptotic cells via alpha(v)beta(5) and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 1998. 188: 1359-1368.
28. Schorey, J. S. and Cooper, A. M., Macrophage signaling upon mycobacterial infection: the MAP kinases lead the way. Cell Microbiol. 2003. 5: 133-142.
29. Schaible, U. E., Collins, H. L., and Kaufmann, S. H., Confrontation between intracellular bacteria and the immune system. Adv. Immunol. 1999. 71: 267-377.
30. de la Barrera, S. S., Finiasz, M., Frias, A., Aleman, M., Barrionuevo, P., Fink, S., Franco, M. C. et al., Specific lytic activity against mycobacterial antigens is inversely correlated with the severity of tuberculosis. Clin. Exp. Immunol. 2003. 132: 450-461.
31. Schaible, U. E., Winau, F., Sieling, P. A., Fischer, K., Collins, H. L., Hagens, K., Modlin, R. L. et al., Apoptosis facilitates antigen presentation to T lymphocytes through MHC-I and CD1 in tuberculosis. Nat. Med. 2003. 9: 1039-1046.
32. Heath, W. R. and Carbone, F. R., Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol. 2001. 19: 47-64.
33. Gallucci, S., Lolkema, M. and Matzinger, P., Natural adjuvants: endogenous activators of dendritic cells. Nat. Med. 1999. 5: 1249-1255.
34. Sauter, B., Albert, M. L., Francisco, L., Larsson, M., Somersan, S. and Bhardwaj, N., Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 2000. 191: 423-433.
35. Fortsch, D., Rollinghoff, M. and Stenger, S., IL-10 converts human dendritic cells into macrophage-like cells with increased antibacterial activity against virulent Mycobacterium tuberculosis. J. Immunol. 2000. 165: 978-987.
36. Stuart, L. M., Lucas, M., Sipmson, C., Lamb, J., Savill, J. and Lacy-Hulbert, A., Inhibitory effects of apoptotic cells ingestion upon endotoxin-driven myeloid dendritic cell maturation. J. Immunol. 2002. 168: 1627-1635.
37. Hirsch, C. S., Toossi, Z., Othieno, C., Johnson, J. L., Schwander, S. K., Robertson, S., Wallis, R. S. et al., Depressed T-cell interferon-gamma responses in pulmonary tuberculosis: analysis of underlying mechanisms and modulation with therapy. J. Infect. Dis. 1999. 180: 2069-2073.
38. Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Rivera, M., Ravetch, J. V. et al., Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 2001. 194: 769-779.
39. Geijtenbeek, T. B., Van Vliet, S. J., Koppel, E. A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C. M., Appelmelk, B. and Van Kooyk, Y., Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 2003. 197: 7-17.
40. Quesniaux, V. J., Nicolle, D. M., Torres, D., Kremer, L., Guerardel, Y., Nigou, J., Puzo, G. et al., Toll-like receptor 2 (TLR2)-dependent-positive and TLR2-independent-negative regulation of proinflammatory cytokines by mycobacterial lipomannans. J. Immunol. 2004. 172: 4425-4434.
41. Tsuji, S., Matsumoto, M., Takeuchi, O., Akira, S., Azuma, I. Hayashi, A., Toyoshima, K. and Seya, T., Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guérin: Involvement of Toll-like receptors. Infect. Immun. 2000. 68: 6883-6890.
42. Re, F. and Strominger, J. L., Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem 2001. 276: 37692-37699.
43. Kaufmann, S. H., How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 2001. 1: 20-30.
44. Winau, F., Kaufmann, S. H. E. and Schaible, U. E., Apoptosis paves the detour path for CD8 T cell activation against intracellular bacteria. Cell. Microbiol. 2004. 6:599-607.
45. Bevan, M. J., Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 1976. 143: 1283-1288.
46. Boyum, A., Isolation of mononuclear cells and granulocytes from human blood. Scand. J. Clin. Invest. 1968. 97: 77-89.
47. Hanekom, W. A., Mendillo, M., Manca, C., Haslett, P. A., Siddiqui, M. R., Barry, C. 3rd and Kaplan, G., Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 2003. 188: 257-266.