Insufficient generation of mycobactericidal mediators and inadequate level of phagosomal maturation are related with susceptibility to virulent Mycobacterium tuberculosis infection in mouse macrophages

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  Lee, Hyo Ji ^a   Ko, Hyun Jeong ^a   Jung, Yu Jin ^a  

^a Kangwon National University   (South Korea)

Author keywords

Macrophage; Mycobacterium tuberculosis; Nitric oxide (NO); Phagosomal maturation; Reactive oxygen species (ROS); Susceptibility

Indexed keywords

CATHEPSIN D; EARLY ENDOSOME ANTIGEN 1; GAMMA INTERFERON; INTERLEUKIN 10; LACTATE DEHYDROGENASE; LIPOCORTIN 5; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NITRIC OXIDE; PROPIDIUM IODIDE; RAB PROTEIN; RAB7 PROTEIN; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; CELL VIABILITY ASSAY; COLONY FORMING UNIT; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; INFECTION SENSITIVITY; INFECTIOUS DOSE; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NATURAL KILLER CELL; NONHUMAN; PHAGOSOME; TH1 CELL; TUBERCULOSIS; WESTERN BLOTTING;

EID: 84966372683     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00541     Document Type: Article

References (55)

1. Abebe, M., Kim, L., Rook, G., Aseffa, A., Wassie, L., Zewdie, M., et al. (2011). Modulation of cell death by M. tuberculosis as a strategy for pathogen survival. Clin. Dev. Immunol. 2011, 678570. doi: 10.1155/2011/678570
2. Albina, J. E., Cui, S., Mateo, R. B., and Reichner, J. S. (1993). Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J. Immunol. 150, 5080-5085
3. Beamer, G. L., and Turner, J. (2005). Murine models of susceptibility to tuberculosis. Arch. Immunol. Ther. Exp. (Warsz.) 53, 469-483
4. Beisiegel, M., Mollenkopf, H. J., Hahnke, K., Koch, M., Dietrich, I., Reece, S. T., et al. (2009). Combination of host susceptibility and Mycobacterium tuberculosis virulence define gene expression profile in the host. Eur. J. Immunol. 39, 3369-3384. doi: 10.1002/eji.200939615
5. Benes, P., Vetvicka, V., and Fusek, M. (2008). Cathepsin D-many functions of one aspartic protease. Crit. Rev. Oncol. Hematol. 68, 12-28. doi: 10.1016/j.critrevonc.2008.02.008
6. Bosca, L., Zeini, M., Traves, P. G., and Hortelano, S. (2005). Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicology 208, 249-258. doi: 10.1016/j.tox.2004.11.035
7. Butler, R. E., Brodin, P., Jang, J., Jang, M. S., Robertson, B. D., Gicquel, B., et al. (2012). The balance of apoptotic and necrotic cell death in Mycobacterium tuberculosis infected macrophages is not dependent on bacterial virulence. PLoS ONE 7:e47573. doi: 10.1371/journal.pone.0047573
8. Chackerian, A. A., and Behar, S. M. (2003). Susceptibility to Mycobacterium tuberculosis: lessons from inbred strains of mice. Tuberculosis (Edinb.) 83, 279-285. doi: 10.1016/S1472-9792(03)00017-9
9. Chan, E. D., Chan, J., and Schluger, N. W. (2001). What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am. J. Respir. Cell Mol. Biol. 25, 606-612. doi: 10.1165/ajrcmb.25.5.4487
10. Chan, J., Xing, Y., Magliozzo, R. S., and Bloom, B. R. (1992). Killing of virulent Mycobacterium tuberculosis by reactive nitrogen intermediates produced by activated murine macrophages. J. Exp. Med. 175, 1111-1122. doi: 10.1084/jem.175.4.1111
11. Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G., and Orme, I. M. (1993). Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178, 2243-2247. doi: 10.1084/jem.178.6.2243
12. Corr, S. C., and O'Neill, L. A. (2009). Listeria monocytogenes infection in the face of innate immunity. Cell. Microbiol. 11, 703-709. doi: 10.1111/j.1462-5822.2009.01294.x
13. Danelishvili, L., Mcgarvey, J., Li, Y. J., and Bermudez, L. E. (2003). Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell. Microbiol. 5, 649-660. doi: 10.1046/j.1462-5822.2003.00312.x
14. Dupont, N., Lacas-Gervais, S., Bertout, J., Paz, I., Freche, B., Van Nhieu, G. T., et al. (2009). Shigella phagocytic vacuolar membrane remnants participate in the cellular response to pathogen invasion and are regulated by autophagy. Cell Host Microbe 6, 137-149. doi: 10.1016/j.chom.2009.07.005
15. Eurosurveillance editorial team (2013). WHO publishes Global tuberculosis report 2013. Eurosurveillance 18:20615
16. Flynn, J. L., Goldstein, M. M., Chan, J., Triebold, K. J., Pfeffer, K., Lowenstein, C. J., et al. (1995). Tumor necrosis factor-alpha is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 2, 561-572. doi: 10.1016/1074-7613(95)90001-2
17. Fratti, R. A., Chua, J., Vergne, I., and Deretic, V. (2003). Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. U.S.A. 100, 5437-5442. doi: 10.1073/pnas.0737613100
18. Gupta, U. D., and Katoch, V. M. (2009). Animal models of tuberculosis for vaccine development. Indian J. Med. Res. 129, 11-18
19. Herbst, S., Schaible, U. E., and Schneider, B. E. (2011). Interferon gamma activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS ONE 6:e19105. doi: 10.1371/journal.pone.0019105
20. Jung, Y. J., Lacourse, R., Ryan, L., and North, R. J. (2002). Virulent but not avirulent Mycobacterium tuberculosis can evade the growth inhibitory action of a T helper 1-dependent, nitric oxide Synthase 2-independent defense in mice. J. Exp. Med. 196, 991-998. doi: 10.1084/jem.20021186
21. Jung, Y. J., Ryan, L., Lacourse, R., and North, R. J. (2009). Differences in the ability to generate type 1 T helper cells need not determine differences in the ability to resist Mycobacterium tuberculosis infection among mouse strains. J. Infect. Dis. 199, 1790-1796. doi: 10.1086/599092
22. Kahnert, A., Seiler, P., Stein, M., Bandermann, S., Hahnke, K., Mollenkopf, H., et al. (2006). Alternative activation deprives macrophages of a coordinated defense program to Mycobacterium tuberculosis. Eur. J. Immunol. 36, 631-647. doi: 10.1002/eji.200535496
23. Lee, H. J., Kim, K. C., Han, J. A., Choi, S. S., and Jung, Y. J. (2015). The early induction of suppressor of cytokine signaling 1 and the downregulation of toll-like receptors 7 and 9 induce tolerance in costimulated macrophages. Mol. Cells 38, 26-32. doi: 10.14348/molcells.2015.2136
24. Lin, P. L., and Flynn, J. L. (2010). Understanding latent tuberculosis: a moving target. J. Immunol. 185, 15-22. doi: 10.4049/jimmunol.0903856
25. Luzio, J. P., Pryor, P. R., and Bright, N. A. (2007). Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8, 622-632. doi: 10.1038/nrm2217
26. MacMicking, J. D., North, R. J., Lacourse, R., Mudgett, J. S., Shah, S. K., and Nathan, C. F. (1997). Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 94, 5243-5248. doi: 10.1073/pnas.94.10.5243
27. Marino, S., Myers, A., Flynn, J. L., and Kirschner, D. E. (2010). TNF and IL-10 are major factors in modulation of the phagocytic cell environment in lung and lymph node in tuberculosis: a next-generation two-compartmental model. J. Theor. Biol. 265, 586-598. doi: 10.1016/j.jtbi.2010.05.012
28. Marquis, J. F., Lacourse, R., Ryan, L., North, R. J., and Gros, P. (2009). Genetic and functional characterization of the mouse Trl3 locus in defense against tuberculosis. J. Immunol. 182, 3757-3767. doi: 10.4049/jimmunol.0802094
29. Medina, E., and North, R. J. (1998). Resistance ranking of some common inbred mouse strains to Mycobacterium tuberculosis and relationship to major histocompatibility complex haplotype and Nramp1 genotype. Immunology 93, 270-274. doi: 10.1046/j.1365-2567.1998.00419.x
30. Medina, E., and North, R. J. (1999). Genetically susceptible mice remain proportionally more susceptible to tuberculosis after vaccination. Immunology 96, 16-21. doi: 10.1046/j.1365-2567.1999.00663.x
31. Mitsos, L. M., Cardon, L. R., Fortin, A., Ryan, L., Lacourse, R., North, R. J., et al. (2000). Genetic control of susceptibility to infection with Mycobacterium tuberculosis in mice. Genes Immun. 1, 467-477. doi: 10.1038/sj.gene.6363712
32. Mogues, T., Goodrich, M. E., Ryan, L., Lacourse, R., and North, R. J. (2001). The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J. Exp. Med. 193, 271-280. doi: 10.1084/jem.193.3.271
33. Mohan, V. P., Scanga, C. A., Yu, K., Scott, H. M., Tanaka, K. E., Tsang, E., et al. (2001). Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect. Immun. 69, 1847-1855. doi: 10.1128/IAI.69.3.1847-1855.2001
34. North, R. J., and Jung, Y. J. (2004). Immunity to tuberculosis. Annu. Rev. Immunol. 22, 599-623. doi: 10.1146/annurev.immunol.22.012703.104635
35. O'Garra, A., Redford, P. S., Mcnab, F. W., Bloom, C. I., Wilkinson, R. J., and Berry, M. P. (2013). The immune response in tuberculosis. Annu. Rev. Immunol. 31, 475-527. doi: 10.1146/annurev-immunol-032712-095939
36. O'Leary, S., O'Sullivan, M. P., and Keane, J. (2011). IL-10 blocks phagosome maturation in Mycobacterium tuberculosis-infected human macrophages. Am. J. Respir. Cell Mol. Biol. 45, 172-180. doi: 10.1165/rcmb.2010-0319OC
37. Parandhaman, D. K., and Narayanan, S. (2014). Cell death paradigms in the pathogenesis of Mycobacterium tuberculosis infection. Front. Cell. Infect. Microbiol. 4:31. doi: 10.3389/fcimb.2014.00031
38. Park, J. S., Tamayo, M. H., Gonzalez-Juarrero, M., Orme, I. M., and Ordway, D. J. (2006). Virulent clinical isolates of Mycobacterium tuberculosis grow rapidly and induce cellular necrosis but minimal apoptosis in murine macrophages. J. Leukoc. Biol. 79, 80-86. doi: 10.1189/jlb.0505250
39. Pearl, J. E., Saunders, B., Ehlers, S., Orme, I. M., and Cooper, A. M. (2001). Inflammation and lymphocyte activation during mycobacterial infection in the interferon-gamma-deficient mouse. Cell. Immunol. 211, 43-50. doi: 10.1006/cimm.2001.1819
40. Poirier, V., and Av-Gay, Y. (2012). Mycobacterium tuberculosis modulators of the macrophage's cellular events. Microbes Infect. 14, 1211-1219. doi: 10.1016/j.micinf.2012.07.001
41. Porcelli, S. A., and Jacobs, W. R. Jr. (2008). Tuberculosis: unsealing the apoptotic envelope. Nat. Immunol. 9, 1101-1102. doi: 10.1038/ni1008-1101
42. Puri, R. V., Reddy, P. V., and Tyagi, A. K. (2013). Secreted acid phosphatase (SapM) of Mycobacterium tuberculosis is indispensable for arresting phagosomal maturation and growth of the pathogen in guinea pig tissues. PLoS ONE 8:e70514. doi: 10.1371/journal.pone.0070514
43. Raja, A. (2004). Immunology of tuberculosis. Indian J. Med. Res. 120, 213-232
44. Redford, P. S., Boonstra, A., Read, S., Pitt, J., Graham, C., Stavropoulos, E., et al. (2010). Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 40, 2200-2210. doi: 10.1002/eji.201040433
45. Redford, P. S., Murray, P. J., and O'garra, A. (2011). The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol. 4, 261-270. doi: 10.1038/mi.2011.7
46. Robinson, J. M. (2009). Phagocytic leukocytes and reactive oxygen species. Histochem. Cell Biol. 131, 465-469. doi: 10.1007/s00418-009-0565-5
47. Scherr, N., Jayachandran, R., Mueller, P., and Pieters, J. (2009). Interference of Mycobacterium tuberculosis with macrophage responses. Indian J. Exp. Biol. 47, 401-406
48. Sun, J., Singh, V., Lau, A., Stokes, R. W., Obregon-Henao, A., Orme, I. M., et al. (2013). Mycobacterium tuberculosis nucleoside diphosphate kinase inactivates small GTPases leading to evasion of innate immunity. PLoS Pathog. 9:e1003499. doi: 10.1371/journal.ppat.1003499
49. Turk, V., Stoka, V., Vasiljeva, O., Renko, M., Sun, T., Turk, B., et al. (2012). Cysteine cathepsins: from structure, function and regulation to new frontiers. Biochim. Biophys. Acta 1824, 68-88. doi: 10.1016/j.bbapap.2011.10.002
50. Vashishta, A., Ohri, S. S., and Vetvicka, V. (2009). Pleiotropic effects of cathepsin D. Endocr. Metab. Immune Disord. Drug Targets 9, 385-391. doi: 10.2174/187153009789839174
51. Voskuil, M. I., Bartek, I. L., Visconti, K., and Schoolnik, G. K. (2011). The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front. Microbiol. 2:105. doi: 10.3389/fmicb.2011.00105
52. Xu, J., Laine, O., Masciocchi, M., Manoranjan, J., Smith, J., Du, S. J., et al. (2007). A unique Mycobacterium ESX-1 protein co-secretes with CFP-10/ESAT-6 and is necessary for inhibiting phagosome maturation. Mol. Microbiol. 66, 787-800. doi: 10.1111/j.1365-2958.2007.05959.x
53. Yang, C. S., Shin, D. M., Kim, K. H., Lee, Z. W., Lee, C. H., Park, S. G., et al. (2009). NADPH oxidase 2 interaction with TLR2 is required for efficient innate immune responses to mycobacteria via cathelicidin expression. J. Immunol. 182, 3696-3705. doi: 10.4049/jimmunol.0802217
54. Young, D. B., Perkins, M. D., Duncan, K., and Barry, C. E. I. I. I. (2008). Confronting the scientific obstacles to global control of tuberculosis. J. Clin. Invest. 118, 1255-1265. doi: 10.1172/JCI34614
55. Zhou, Z., and Yu, X. (2008). Phagosome maturation during the removal of apoptotic cells: receptors lead the way. Trends Cell Biol. 18, 474-485. doi: 10.1016/j.tcb.2008.08.002