Impaired dendritic cell differentiation of CD16-positive monocytes in tuberculosis: Role of p38 MAPK

European Journal of Immunology

Volumn 43, Issue 2, 2013, Pages 335-347

  Balboa, Luciana ^a   Romero, María M ^a   Laborde, Evangelina ^a   Sabio y García, Carmen A ^a   Basile, Juan I ^a   Schierloh, Pablo ^a   Yokobori, Noemí ^a   Musella, Rosa M ^b   Castagnino, Jorge ^b   de la Barrera, Silvia ^a   Sasiain, María C ^a   Alemán, Mercedes ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b HOSPITAL F J MUÑIZ   (Argentina)

Author keywords

Dendritic cells; Monocyte differentiation; Tuberculosis

Indexed keywords

CD16 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE P38;

ARTICLE; BYSTANDER EFFECT; CELL DIFFERENTIATION; CELL POPULATION; DENDRITIC CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUBERCULOSIS;

ADULT; ANTIGENS, CD1; CELL DIFFERENTIATION; DENDRITIC CELLS; FEMALE; GPI-LINKED PROTEINS; HUMANS; MALE; MIDDLE AGED; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, IGG; SIGNAL TRANSDUCTION; TUBERCULOSIS; YOUNG ADULT;

EID: 84873750532     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242557     Document Type: Article

References (59)

1. Auffray, C., Sieweke, M. H. and Geissmann, F., Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol. 2009. 27: 669-692.
2. Gordon, S. and Taylor, P. R., Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 2005. 5: 953-964.
3. Weber, C., Belge, K. U., von Hundelshausen, P., Draude, G., Steppich, B., Mack, M., Frankenberger, M. et al., Differential chemokine receptor expression and function in human monocyte subpopulations. J. Leukoc. Biol. 2000. 67: 699-704.
4. Swirski, F. K., Weissleder, R. and Pittet, M. J., Heterogeneous in vivo behavior of monocyte subsets in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2009. 29: 1424-1432.
5. Mizuno, K., Toma, T., Tsukiji, H., Okamoto, H., Yamazaki, H., Ohta, K., Kasahara, Y. et al., Selective expansion of CD16highCCR2- subpopulation of circulating monocytes with preferential production of haem oxygenase (HO)-1 in response to acute inflammation. Clin. Exp. Immunol. 2005. 142: 461-470.
6. Thieblemont, N., Weiss, L., Sadeghi, H. M., Estcourt, C. and Haeffner-Cavaillon, N., CD14lowCD16high: a cytokine-producing monocyte subset which expands during human immunodeficiency virus infection. Eur. J. Immunol. 1995. 25: 3418-3424.
7. Fingerle, G., Pforte, A., Passlick, B., Blumenstein, M., Strobel, M. and Ziegler-Heitbrock, H. W., The novel subset of CD14+/CD16+ blood monocytes is expanded in sepsis patients. Blood 1993. 82: 3170-3176.
8. Skrzeczynska, J., Kobylarz, K., Hartwich, Z., Zembala, M. and Pryjma, J., CD14+CD16+ monocytes in the course of sepsis in neonates and small children: monitoring and functional studies. Scand. J. Immunol. 2002. 55: 629-638.
9. Horelt, A., Belge, K. U., Steppich, B., Prinz, J. and Ziegler-Heitbrock, L., The CD14+CD16+ monocytes in erysipelas are expanded and show reduced cytokine production. Eur. J. Immunol. 2002. 32: 1319-1327.
10. Nockher, W. A., Bergmann, L. and Scherberich, J. E., Increased soluble CD14 serum levels and altered CD14 expression of peripheral blood monocytes in HIV-infected patients. Clin. Exp. Immunol. 1994. 98: 369-374.
11. Vanham, G., Edmonds, K., Qing, L., Hom, D., Toossi, Z., Jones, B., Daley, C. L. et al., Generalized immune activation in pulmonary tuberculosis: co-activation with HIV infection. Clin. Exp. Immunol. 1996. 103: 30-34.
12. Balboa, L., Romero, M. M., Basile, J. I., Sabio y Garcia, C. A., Schierloh, P., Yokobori, N., Geffner, L. et al., Paradoxical role of CD16+CCR2+CCR5+ monocytes in tuberculosis: efficient APC in pleural effusion but also mark disease severity in blood. J. Leukoc. Biol. 2011. 90: 69-75.
13. Baumann, S., Nasser Eddine, A. and Kaufmann, S. H., Progress in tuberculosis vaccine development. Curr. Opin. Immunol. 2006. 18: 438-448.
14. Flynn, J. L. and Chan, J., Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr. Opin. Immunol. 2003. 15: 450-455.
15. Mariotti, S., Teloni, R., Iona, E., Fattorini, L., Romagnoli, G., Gagliardi, M. C., Orefici, G. et al., Mycobacterium tuberculosis diverts alpha interferon-induced monocyte differentiation from dendritic cells into immunoprivileged macrophage-like host cells. Infect. Immun. 2004. 72: 4385-4392.
16. Schreiber, H. A. and Sandor, M., Monocyte-derived inflammatory dendritic cells in the granuloma during mycobacterial infection. Adv. Exp. Med. Biol. 2012. 946: 277-293.
17. Humphreys, I. R., Stewart, G. R., Turner, D. J., Patel, J., Karamanou, D., Snelgrove, R. J. and Young, D. B., A role for dendritic cells in the dissemination of mycobacterial infection. Microbes Infect. 2006. 8: 1339-1346.
18. Reljic, R., Di Sano, C., Crawford, C., Dieli, F., Challacombe, S. and Ivanyi, J., Time course of mycobacterial infection of dendritic cells in the lungs of intranasally infected mice. Tuberculosis (Edinburgh) 2005. 85: 81-88.
19. Dominguez, P. M. and Ardavin, C., Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 2010. 234: 90-104.
20. Martino, A., Mycobacteria and innate cells: critical encounter for immunogenicity. J. Biosci. 2008. 33: 137-144.
21. Balboa, L., Romero, M. M., Yokobori, N., Schierloh, P., Geffner, L., Basile, J. I., Musella, R. M. et al., Mycobacterium tuberculosis impairs dendritic cell response by altering CD1b, DC-SIGN and MR profile. Immunol. Cell Biol. 2010. 88: 716-726.
22. Skold, M. and Behar, S. M., Tuberculosis triggers a tissue-dependent program of differentiation and acquisition of effector functions by circulating monocytes. J. Immunol. 2008. 181: 6349-6360.
23. Lichtner, M., Rossi, R., Mengoni, F., Vignoli, S., Colacchia, B., Massetti, A. P., Kamga, I. et al., Circulating dendritic cells and interferon-alpha production in patients with tuberculosis: correlation with clinical outcome and treatment response. Clin. Exp. Immunol. 2006. 143: 329-337.
24. Stenger, S., Niazi, K. R. and Modlin, R. L., Down-regulation of CD1 on antigen-presenting cells by infection with Mycobacterium tuberculosis. J. Immunol. 1998. 161: 3582-3588.
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. Aleman, M., de la Barrera, S., Schierloh, P., Yokobori, N., Baldini, M., Musella, R., Abbate, E. et al., Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur. J. Immunol. 2007. 37: 1524-1537.
27. Sanchez-Torres, C., Garcia-Romo, G. S., Cornejo-Cortes, M. A., Rivas-Carvalho, A. and Sanchez-Schmitz, G., CD16 +and CD16- human blood monocyte subsets differentiate in vitro to dendritic cells with different abilities to stimulate CD4+ T cells. Int. Immunol. 2001. 13: 1571-1581.
28. Rivas-Carvalho, A., Meraz-Rios, M. A., Santos-Argumedo, L., Bajana, S., Soldevila, G., Moreno-Garcia, M. E. and Sanchez-Torres, C., CD16+ human monocyte-derived dendritic cells matured with different and unrelated stimuli promote similar allogeneic Th2 responses: regulation by pro- and anti-inflammatory cytokines. Int. Immunol. 2004. 16: 1251-1263.
29. Tuyaerts, S., Aerts, J. L., Corthals, J., Neyns, B., Heirman, C., Breckpot, K., Thielemans, K. et al., Current approaches in dendritic cell generation and future implications for cancer immunotherapy. Cancer Immunol. Immunother. 2007. 56: 1513-1537.
30. Laborde, E. A., Vanzulli, S., Beigier-Bompadre, M., Isturiz, M. A., Ruggiero, R. A., Fourcade, M. G., Catalan Pellet, A. C. et al., Immune complexes inhibit differentiation, maturation, and function of human monocyte-derived dendritic cells. J. Immunol. 2007. 179: 673-681.
31. Xie, J., Qian, J., Yang, J., Wang, S., Freeman, M. E., 3rd and Yi, Q., Critical roles of Raf/MEK/ERK and PI3K/AKT signaling and inactivation of p38 MAP kinase in the differentiation and survival of monocyte-derived immature dendritic cells. Exp. Hematol. 2005. 33: 564-572.
32. Geiger, P. C., Wright, D. C., Han, D. H. and Holloszy, J. O., Activation of p38 MAP kinase enhances sensitivity of muscle glucose transport to insulin. Am. J. Physiol. Endocrinol. Metab. 2005. 288: E782-788.
33. Lee, J. C., Laydon, J. T., McDonnell, P. C., Gallagher, T. F., Kumar, S., Green, D., McNulty, D. et al., A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 1994. 372: 739-746.
34. Essner, R., Rhoades, K., McBride, W. H., Morton, D. L. and Economou, J. S., IL-4 down-regulates IL-1 and TNF gene expression in human monocytes. J. Immunol. 1989. 142: 3857-3861.
35. Ma, W., Lim, W., Gee, K., Aucoin, S., Nandan, D., Kozlowski, M., Diaz-Mitoma, F. et al., The p38 mitogen-activated kinase pathway regulates the human interleukin-10 promoter via the activation of Sp1 transcription factor in lipopolysaccharide-stimulated human macrophages. J. Biol. Chem. 2001. 276: 13664-13674.
36. Wesa, A. K. and Galy, A., IL-1 beta induces dendritic cells to produce IL-12. Int. Immunol. 2001. 13: 1053-1061.
37. 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.
38. Ancuta, P., Weiss, L. and Haeffner-Cavaillon, N., CD14+CD16++ cells derived in vitro from peripheral blood monocytes exhibit phenotypic and functional dendritic cell-like characteristics. Eur. J. Immunol. 2000. 30: 1872-1883.
39. Randolph, G. J., Sanchez-Schmitz, G., Liebman, R. M. and Schakel, K., The CD16(+) (FcgammaRIII(+)) subset of human monocytes preferentially becomes migratory dendritic cells in a model tissue setting. J. Exp. Med. 2002. 196: 517-527.
40. Ziegler-Heitbrock, H. W., Heterogeneity of human blood monocytes: the CD14+ CD16+ subpopulation. Immunol. Today 1996. 17: 424-428.
41. Landsman, L., Varol, C. and Jung, S., Distinct differentiation potential of blood monocyte subsets in the lung. J. Immunol. 2007. 178: 2000-2007.
42. Aguilar-Ruiz, S. R., Torres-Aguilar, H., Gonzalez-Dominguez, E., Narvaez, J., Gonzalez-Perez, G., Vargas-Ayala, G., Meraz-Rios, M. A. et al., Human CD16+ and CD16- monocyte subsets display unique effector properties in inflammatory conditions in vivo. J. Leukoc. Biol. 2011. 90: 1119-1131.
43. Steppich, B., Dayyani, F., Gruber, R., Lorenz, R., Mack, M. and Ziegler-Heitbrock, H. W., Selective mobilization of CD14(+)CD16(+) monocytes by exercise. Am. J. Physiol. Cell Physiol. 2000. 279: C578-586.
44. Strauss-Ayali, D., Conrad, S. M. and Mosser, D. M., Monocyte subpopulations and their differentiation patterns during infection. J. Leukoc. Biol. 2007. 82: 244-252.
45. Castano, D., Garcia, L. F. and Rojas, M., Increased frequency and cell death of CD16+ monocytes with Mycobacterium tuberculosis infection. Tuberculosis (Edinburgh) 2011. 91: 348-360.
46. Ulrichs, T., Moody, D. B., Grant, E., Kaufmann, S. H. and Porcelli, S. A., T-cell responses to CD1-presented lipid antigens in humans with Mycobacterium tuberculosis infection. Infect. Immun. 2003. 71: 3076-3087.
47. Bajana, S., Herrera-Gonzalez, N., Narvaez, J., Torres-Aguilar, H., Rivas-Carvalho, A., Aguilar, S. R. and Sanchez-Torres, C., Differential CD4(+) T-cell memory responses induced by two subsets of human monocyte-derived dendritic cells. Immunology 2007. 122: 381-393.
48. Ancuta, P., Liu, K. Y., Misra, V., Wacleche, V. S., Gosselin, A., Zhou, X. and Gabuzda, D., Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD16- monocyte subsets. BMC Genomics 2009. 10: 403.
49. Ziegler-Heitbrock, H. W., Fingerle, G., Strobel, M., Schraut, W., Stelter, F., Schutt, C., Passlick, B. et al., The novel subset of CD14+/CD16+ blood monocytes exhibits features of tissue macrophages. Eur. J. Immunol. 1993. 23: 2053-2058.
50. Geissmann, F., Jung, S. and Littman, D. R., Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003. 19: 71-82.
51. Cros, J., Cagnard, N., Woollard, K., Patey, N., Zhang, S. Y., Senechal, B., Puel, A. et al., Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010. 33: 375-386.
52. Randolph, G. J., Inaba, K., Robbiani, D. F., Steinman, R. M. and Muller, W. A., Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 1999. 11: 753-761.
53. Leon, B., Lopez-Bravo, M. and Ardavin, C., Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007. 26: 519-531.
54. Wolf, A. J., Linas, B., Trevejo-Nunez, G. J., Kincaid, E., Tamura, T., Takatsu, K. and Ernst, J. D., Mycobacterium tuberculosis infects dendritic cells with high frequency and impairs their function in vivo. J. Immunol. 2007. 179: 2509-2519.
55. Mendelson, M., Hanekom, W. A., Ntutela, S., Vogt, M., Steyn, L., Maartens, G. and Kaplan, G., Quantitative and functional differences between peripheral blood myeloid dendritic cells from patients with pleural and parenchymal lung tuberculosis. Clin. Vacc. Immunol. 2006. 13: 1299-1306.
56. Rajashree, P., Krishnan, G. and Das, S. D., Impaired phenotype and function of monocyte derived dendritic cells in pulmonary tuberculosis. Tuberculosis (Edinburgh) 2009. 89: 77-83.
57. Ziegler-Heitbrock, L., The CD14 +CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol. 2007. 81: 584-592.
58. Abdallah, A. M., Gey van Pittius, N. C., Champion, P. A., Cox, J., Luirink, J., Vandenbroucke-Grauls, C. M., Appelmelk, B. J. et al., Type VII secretion-mycobacteria show the way. Nat. Rev. Microbiol. 2007. 5: 883-891.
59. Schellekens, P. T., Vriesendorp, B., Eijsvoogel, V. P., Van Leeuwen, A., Van Rood, J. J., Miggiano, V. et al., Lymphocyte transformation in vitro. II. Mixed lymphocyte culture in relation to leucocyte antigens. Clin. Exp. Immunol. 1970. 6: 241-254.