Mycobacteria-infected bystander macrophages trigger maturation of dendritic cells and enhance their ability to mediate HIV transinfection

European Journal of Immunology

Volumn 42, Issue 5, 2012, Pages 1192-1202

  Mazurek, Jolanta ^a,b   Ignatowicz, Lech ^a,b   Källenius, Gunilla ^a   Jansson, Marianne ^a,c   Pawlowski, Andrzej ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Coinfection; Dendritic cell; HIV 1; Macrophage; Mycobacterium tuberculosis

Indexed keywords

CD209 ANTIGEN; CD86 ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 12P40; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TUMOR NECROSIS FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BYSTANDER EFFECT; CELL FUNCTION; CELL MATURATION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VIRUS TRANSMISSION;

CELL DIFFERENTIATION; CELLS, CULTURED; COINFECTION; CYTOKINES; DENDRITIC CELLS; HIV INFECTIONS; HIV-1; HUMANS; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS; UP-REGULATION;

EID: 84860318604     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142049     Document Type: Article

References (59)

1. Getahun, H., Gunneberg, C., Granich, R. and Nunn, P., HIV infection-associated tuberculosis: the epidemiology and the response. Clin. Infect. Dis. 2010. 50(S3): S201-207.
2. Sharma, S. K., Mohan, A. and Kadhiravan, T., HIV-TB co-infection: epidemiology, diagnosis & management. Indian J. Med. Res. 2005. 121: 550-567.
3. Sharma, S. K. and Mohan, A., Extrapulmonary tuberculosis. Indian J. Med. Res. 2004. 120: 316-353.
4. Aaron, L., Saadoun, D., Calatroni, I., Launay, O., Memain, N., Vincent, V., Marchal, G. et al., Tuberculosis in HIV-infected patients: a comprehensive review. Clin. Microbiol. Infect. 2004. 10: 388-398.
5. Arias, M. A., Pantoja, A. E., Jaramillo, G., Lopez, Y. P., Mejia, N., Mejia, C., Paris, S. C. et al., Chemokine/cytokine production by mononuclear cells from human lymphoid tissues and their modulation by Mycobacterium tuberculosis antigens. FEMS Immunol. Med. Microbiol. 2007. 49: 272-279.
6. Toossi, Z., Hirsch, C. S., Wu, M., Mayanja-Kizza, H., Baseke, J. and Thiel, B., Distinct cytokine and regulatory T cell profile at pleural sites of dual HIV/tuberculosis infection compared to that in the systemic circulation. Clin. Exp. Immunol. 2011. 163: 333-338.
7. Berry, M. P., Graham, C. M., McNab, F. W., Xu, Z., Bloch, S. A., Oni, T., Wilkinson, K. A. et al., An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010. 466: 973-977.
8. Pathak, S., Wentzel-Larsen, T. and Asjo, B., Effects of IV-1 infection on mycobacterial growth in peripheral blood monocyte-derived macrophages. Infect. Immun. 2010. 78: 4022-4032.
9. Lawn, S. D., Butera, S. T. and Folks, T. M., Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin. Microbiol. Rev. 2001. 14: 753-777, table of contents.
10. Toossi, Z., Virological and immunological impact of tuberculosis on human immunodeficiency virus type 1 disease. J. Infect. Dis. 2003. 188: 1146-1155.
11. Vicenzi, E., Alfano, M., Ghezzi, S., Gatti, A., Veglia, F., Lazzarin, A., Sozzani, S. et al., Divergent regulation of HIV-1 replication in PBMC of infected individuals by CC chemokines: suppression by RANTES, MIP-1alpha, and MCP-3, and enhancement by MCP-1. J. Leukoc. Biol. 2000. 68: 405-412.
12. Caux, C., Ait-Yahia, S., Chemin, K., de Bouteiller, O., Dieu-Nosjean, M. C., Homey, B., Massacrier, C. et al., Dendritic cell biology and regulation of dendritic cell trafficking by chemokines. Springer Semin. Immunopathol. 2000. 22: 345-369.
13. Stockwin, L. H., McGonagle, D., Martin, I. G. and Blair, G. E., Dendritic cells: immunological sentinels with a central role in health and disease. Immunol. Cell Biol. 2000. 78: 91-102.
14. Cameron, P. U., Freudenthal, P. S., Barker, J. M., Gezelter, S., Inaba, K. and Steinman, R. M., Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 1992. 257: 383-387.
15. Steinman, R. M., Granelli-Piperno, A., Pope, M., Trumpfheller, C., Ignatius, R., Arrode, G., Racz, P. and Tenner-Racz, K., The interaction of immunodeficiency viruses with dendritic cells. Curr. Top Microbiol. Immunol. 2003. 276: 1-30.
16. Tsunetsugu-Yokota, Y., Yasuda, S., Sugimoto, A., Yagi, T., Azuma, M., Yagita, H., Akagawa, K. et al., Efficient virus transmission from dendritic cells to CD4+ T cells in response to antigen depends on close contact through adhesion molecules. Virology 1997. 239: 259-268.
17. Coleman, C. M. and Wu, L., HIV interactions with monocytes and dendritic cells: viral latency and reservoirs. Retrovirology 2009. 6: 51.
18. Geijtenbeek, T. B., Kwon, D. S., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Middel, J., Cornelissen, I. L. et al., DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000. 100: 587-597.
19. Turville, S., Wilkinson, J., Cameron, P., Dable, J. and Cunningham, A. L., The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J. Leukoc. Biol. 2003. 74: 710-718.
20. Robinson, M. J., Sancho, D., Slack, E. C., LeibundGut-Landmann, S. and Reis e Sousa, C., Myeloid C-type lectins in innate immunity. Nat. Immunol. 2006. 7: 1258-1265.
21. Gringhuis, S. I., den Dunnen, J., Litjens, M., van der Vlist, M. and Geijtenbeek, T. B., Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 2009. 10: 1081-1088.
22. van Kooyk, Y., Appelmelk, B. and Geijtenbeek, T. B., A fatal attraction: Mycobacterium tuberculosis and HIV-1 target DC-SIGN to escape immune surveillance. Trends Mol. Med. 2003. 9: 153-159.
23. Torrelles, J. B., Azad, A. K., Henning, L. N., Carlson, T. K. and Schlesinger, L. S., Role of C-type lectins in mycobacterial infections. Curr. Drug Targets 2008. 9: 102-112.
24. Tailleux, L., Neyrolles, O., Honore-Bouakline, S., Perret, E., Sanchez, F., Abastado, J. P., Lagrange, P. H. et al., Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J. Immunol. 2003. 170: 1939-1948.
25. Mortellaro, A., Robinson, L. and Ricciardi-Castagnoli, P., Spotlight on Mycobacteria and dendritic cells: will novel targets to fight tuberculosis emerge? EMBO Mol. Med. 2009. 1: 19-29.
26. Bellora, F., Castriconi, R., Dondero, A., Reggiardo, G., Moretta, L., Mantovani, A., Moretta, A. and Bottino, C., The interaction of human natural killer cells with either unpolarized or polarized macrophages results in different functional outcomes. Proc. Natl. Acad. Sci. USA 2010. 107: 21659-21664.
27. Ji, X., Chen, Y., Faro, J., Gewurz, H., Bremer, J. and Spear, G. T., Interaction of human immunodeficiency virus (HIV) glycans with lectins of the human immune system. Curr. Protein. Pept. Sci. 2006. 7: 317-324.
28. Toossi, Z., Wu, M., Islam, N., Teixeira-Johnson, L., Hejal, R. and Aung, H., Transactivation of human immunodeficiency virus-1 in T-cells by Mycobacterium tuberculosis-infected mononuclear phagocytes. J. Lab. Clin. Med. 2004. 144: 108-115.
29. Hammad, H. and Lambrecht, B. N., Lung dendritic cell migration. Adv. Immunol. 2007. 93: 265-278.
30. Cook, D. N. and Bottomly, K., Innate immune control of pulmonary dendritic cell trafficking. Proc. Am. Thorac. Soc. 2007. 4: 234-239.
31. 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.
32. Sada, E., Aguilar, D., Torres, M. and Herrera, T., Detection of lipoarabinomannan as a diagnostic test for tuberculosis. J. Clin. Microbiol. 1992. 30: 2415-2418.
33. Hamasur, B., Bruchfeld, J., Haile, M., Pawlowski, A., Bjorvatn, B., Kallenius, G. and Svenson, S. B., Rapid diagnosis of tuberculosis by detection of mycobacterial lipoarabinomannan in urine. J. Microbiol. Methods 2001. 45: 41-52.
34. Shende, N., Gupta, S., Upadhye, V., Kumar, S. and Harinath, B. C., Isolation and analysis of circulating tuberculous antigens in Mycobacterium tuberculosis. Indian J. Tuberc. 2007. 54: 125-129.
35. Rajashree, P. and Das, S. D., Infection with prevalent clinical strains of Mycobacterium tuberculosis leads to differential maturation of monocyte derived dendritic cells. Immunol. Lett. 2008. 117: 174-180.
36. Ranjbar, S., Boshoff, H. I., Mulder, A., Siddiqi, N., Rubin, E. J. and Goldfeld, A. E., HIV-1 replication is differentially regulated by distinct clinical strains of Mycobacterium tuberculosis. PLoS One 2009. 4: e6116.
37. Wallis, R. S., Reactivation of latent tuberculosis by TNF blockade: the role of interferon gamma. J. Investig Dermatol. Symp. Proc. 2007. 12: 16-21.
38. Swingler, S., Morris, A. and Easton, A., Tumour necrosis factor alpha and interleukin-1 beta induce specific subunits of NFKB to bind the HIV-1 enhancer: characterisation of transcription factors controlling human immunodeficiency virus type 1 gene expression in neural cells. Biochem. Biophys. Res. Commun. 1994. 203: 623-630.
39. 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.
40. Warwick-Davies, J., Watson, A. J., Griffin, G. E., Krishna, S. and Shattock, R. J., Enhancement of Mycobacterium tuberculosis-induced tumor necrosis factor alpha production from primary human monocytes by an activated T-cell membrane-mediated mechanism. Infect. Immun. 2001. 69: 6580-6587.
41. Sporri, R. and Reis e Sousa, C., Inflammatory mediators are insufficient for full dendritic cell activation and promote expansion of CD4+ T cell populations lacking helper function. Nat. Immunol. 2005. 6: 163-170.
42. Izquierdo-Useros, N., Blanco, J., Erkizia, I., Fernandez-Figueras, M. T., Borras, F. E., Naranjo-Gomez, M., Bofill, M. et al., Maturation of blood-derived dendritic cells enhances human immunodeficiency virus type 1 capture and transmission. J. Virol. 2007. 81: 7559-7570.
43. Garcia, E., Pion, M., Pelchen-Matthews, A., Collinson, L., Arrighi, J. F., Blot, G., Leuba, F. et al., HIV-1 trafficking to the dendritic cell-T-cell infectious synapse uses a pathway of tetraspanin sorting to the immunological synapse. Traffic 2005. 6: 488-501.
44. Lin, C. L., Sewell, A. K., Gao, G. F., Whelan, K. T., Phillips, R. E. and Austyn, J. M., Macrophage-tropic HIV induces and exploits dendritic cell chemotaxis. J. Exp. Med. 2000. 192: 587-594.
45. Wang, J. H., Janas, A. M., Olson, W. J. and Wu, L., Functionally distinct transmission of human immunodeficiency virus type 1 mediated by immature and mature dendritic cells. J. Virol. 2007. 81: 8933-8943.
46. Macatonia, S. E., Lau, R., Patterson, S., Pinching, A. J. and Knight, S. C., Dendritic cell infection, depletion and dysfunction in HIV-infected individuals. Immunology 1990. 71: 38-45.
47. Andrieu, M., Chassin, D., Desoutter, J. F., Bouchaert, I., Baillet, M., Hanau, D., Guillet, J. G. and Hosmalin, A., Downregulation of major histocompatibility class I on human dendritic cells by HIV Nef impairs antigen presentation to HIV-specific CD8+ T lymphocytes. AIDS Res. Hum. Retroviruses 2001. 17: 1365-1370.
48. Crowe, S., Zhu, T. and Muller, W. A., The contribution of monocyte infection and trafficking to viral persistence, and maintenance of the viral reservoir in HIV infection. J. Leukoc. Biol. 2003. 74: 635-641.
49. Borggren, M., Repits, J., Kuylenstierna, C., Sterjovski, J., Churchill, M. J., Purcell, D. F. J., Karlsson, A. et al., Evolution of DC-SIGN use revealed by fitness studies of R5 HIV-I variants emerging during AIDS progression. Retrovirology 2008. 5: 28.
50. Gringhuis, S. I., van der Vlist, M., van den Berg, L. M., den Dunnen, J., Litjens, M. and Geijtenbeek, T. B., HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 2010. 11: 419-426.
51. Reuter, M. A., Pecora, N. D., Harding, C. V., Canaday, D. H. and McDonald, D., Mycobacterium tuberculosis promotes HIV trans-infection and suppresses major histocompatibility complex class II antigen processing by dendritic cells. J. Virol. 2010. 84: 8549-8560.
52. Shortman, K. and Naik, S. H., Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 2007. 7: 19-30.
53. Randolph, G. J., Ochando, J. and Partida-Sanchez, S., Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 2008. 26: 293-316.
54. Gordeuk, V. R., Moyo, V. M., Nouraie, M., Gangaidzo, I. T., Murphree, N. L., Gomo, Z. A., Boelaert, J. R. et al., Circulating cytokines in pulmonary tuberculosis according to HIV status and dietary iron content. Int. J. Tuberc. Lung Dis. 2009. 13: 1267-1273.
55. Kiers, A., Drost, A. P., van Soolingen, D. and Veen, J., Use of DNA fingerprinting in international source case finding during a large outbreak of tuberculosis in The Netherlands. Int. J. Tuberc Lung Dis. 1997. 1: 239-245.
56. Ghebremichael, S., Petersson, R., Koivula, T., Pennhag, A., Romanus, V., Berggren, I., Petrini, B. et al., Molecular epidemiology of drug-resistant tuberculosis in Sweden. Microbes Infect. 2008. 10: 699-705.
57. Sandegren, L., Groenheit, R., Koivula, T., Ghebremichael, S., Advani, A., Castro, E., Pennhag, A. et al., Genomic stability over 9 years of an isoniazid resistant Mycobacterium tuberculosis outbreak strain in Sweden. PLoS One 2011. 6: e16647.
58. Jansson, M., Popovic, M., Karlsson, A., Cocchi, F., Rossi, P., Albert, J. and Wigzell, H., Sensitivity to inhibition by beta-chemokines correlates with biological phenotypes of primary HIV-1 isolates. Proc. Natl. Acad. Sci. U S A 1996. 93: 15382-15387.
59. Bjorndal, A., Deng, H., Jansson, M., Fiore, J. R., Colognesi, C., Karlsson, A., Albert, J. et al., Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 1997. 71: 7478-7487.